Androgen activity and markers of inflammation among men in NHANES III

American Journal of Human Biology

Volumn 25, Issue 5, 2013, Pages 622-628

  Schooling, C Mary ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROSTANE 3,17 DIOL GLUCURONIDE; ANDROSTANE-3,17-DIOL GLUCURONIDE; ANDROSTANEDIOL; BIOLOGICAL MARKER; C REACTIVE PROTEIN; DRUG DERIVATIVE; FIBRINOGEN; TESTOSTERONE;

ADULT; ARTICLE; BLOOD; CONFIDENCE INTERVAL; ENZYME IMMUNOASSAY; HUMAN; INFLAMMATION; LEUKOCYTE COUNT; LUMINESCENCE; MALE; METABOLISM; MIDDLE AGED; NUTRITION; UNITED STATES;

ADULT; ANDROSTANE-3,17-DIOL; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; CONFIDENCE INTERVALS; FIBRINOGEN; HUMANS; IMMUNOENZYME TECHNIQUES; INFLAMMATION; LEUKOCYTE COUNT; LUMINESCENT MEASUREMENTS; MALE; MIDDLE AGED; NUTRITION SURVEYS; TESTOSTERONE; UNITED STATES;

EID: 84883055803     PISSN: 10420533     EISSN: 15206300     Source Type: Journal    
DOI: 10.1002/ajhb.22421     Document Type: Article

References (69)

1. Allen NE, Appleby PN, Davey GK, Key TJ. 2002. Lifestyle and nutritional determinants of bioavailable androgens and related hormones in British men. Cancer Causes Control 13:353-363.
2. Aragon-Ching JB, Williams KM, Gulley JL. 2007. Impact of androgen-deprivation therapy on the immune system: implications for combination therapy of prostate cancer. Front Biosci 12:4957-4971.
3. Auchus ML, Auchus RJ. 2012. Human steroid biosynthesis for the oncologist. J Investig Med 60:495-503.
4. Aversa A, Bruzziches R, Francomano D, Rosano G, Isidori AM, Lenzi A, Spera G. 2010. Effects of testosterone undecanoate on cardiovascular risk factors and atherosclerosis in middle-aged men with late-onset hypogonadism and metabolic syndrome: results from a 24-month, randomized, double-blind, placebo-controlled study. J Sex Med 7:3495-3503.
5. Bonaterra GA, Zugel S, Kinscherf R. 2010. Novel systemic cardiovascular disease biomarkers. Curr Mol Med 10:180-205.
6. Bonithon-Kopp C, Scarabin PY, Bara L, Castanier M, Jacqueson A, Roger M. 1988. Relationship between sex hormones and haemostatic factors in healthy middle-aged men. Atherosclerosis 71:71-76.
7. Brand JS, van der Schouw YT, Dowsett M, Folkerd E, Luben RN, Wareham NJ, Khaw KT. 2012. Testosterone, SHBG and differential white blood cell count in middle-aged and older men. Maturitas 71:274-278.
8. Brufani C, Tozzi A, Fintini D, Ciampalini P, Grossi A, Fiori R, Kiepe D, Manco M, Schiaffini R, Porzio O, Cappa M, Barbetti F. 2009. Sexual dimorphism of body composition and insulin sensitivity across pubertal development in obese Caucasian subjects. Eur J Endocrinol 160:769-775.
9. Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Seriolo B, Straub RH. 2004. Sex hormones influence on the immune system: basic and clinical aspects in autoimmunity. Lupus 13:635-638.
10. Derby CA, Zilber S, Brambilla D, Morales KH, McKinlay JB. 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.
11. Dougherty T. 1952. Effect of hormones on lymphatic tissue. Physiol Rev 32:379-401.
12. English KM, Steeds RP, Jones TH, Diver MJ, Channer KS. 2000. Low-dose transdermal testosterone therapy improves angina threshold in men with chronic stable angina: a randomized, double-blind, placebo-controlled study. Circulation 102:1906-1911.
13. Fernandez-Balsells MM, Murad MH, Lane M, Lampropulos JF, Albuquerque F, Mullan RJ, Agrwal N, Elamin MB, Gallegos-Orozco JF, Wang AT, Erwin PJ, Bhasin S, Montori VM. 2010. Clinical review 1: adverse effects of testosterone therapy in adult men: a systematic review and meta-analysis. J Clin Endocrinol Metab 95:2560-2575.
14. Field AE, Colditz GA, Willett WC, Longcope C, McKinlay JB. 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.
15. Fizazi K, Scher HI, Molina A, Logothetis CJ, Chi KN, Jones RJ, Staffurth JN, North S, Vogelzang NJ, Saad F, Mainwaring P, Harland S, Goodman OB Jr, Sternberg CN, Li JH, Kheoh T, Haqq CM, de Bono JS. 2012. Abiraterone acetate for treatment of metastatic castration-resistant prostate cancer: final overall survival analysis of the COU-AA-301 randomised, double-blind, placebo-controlled phase 3 study. Lancet Oncol 13:983-992.
16. Folstad I, Karter AJ. 1992. Parasites, bright males, and the immunocompetence handicap. Am Naturalist 139:603-622.
17. Frederiksen L, Glintborg D, Hojlund K, Hougaard DM, Brixen K, Rasmussen LM, Andersen M. 2013. Osteoprotegerin levels decrease during testosterone therapy in aging men and are associated with changed distribution of regional fat. Horm Metab Res 45:308-313.
18. Gannage-Yared MH, Chedid R, Abs L. 2011. Relation between androgens and cardiovascular risk factors in a young population. Clin Endocrinol (Oxf) 74:720-725.
19. Grossman CJ. 1985. Interactions between the gonadal steroids and the immune system. Science 227:257-261.
20. Guerra-Silveira F, Abad-Franch F. 2013. Sex bias in infectious disease epidemiology: patterns and processes. PLoS ONE 8:e62390.
21. Haring R, Baumeister SE, Volzke H, Dorr M, Kocher T, Nauck M, Wallaschofski H. 2012. Prospective inverse associations of sex hormone concentrations in men with biomarkers of inflammation and oxidative stress. J Androl 33:944-950.
22. Haring R, Teumer A, Volker U, Dorr M, Nauck M, Biffar R, Volzke H, Baumeister SE, Wallaschofski H. 2013. Mendelian randomization suggests non-causal associations of testosterone with cardiometabolic risk factors and mortality. Andrology 1:17-23.
23. Hepworth MR, Hardman MJ, Grencis RK. 2010. The role of sex hormones in the development of Th2 immunity in a gender-biased model of Trichuris muris infection. Eur J Immunol 40:406-416.
24. Hero M, Wickman S, Hanhijarvi R, Siimes MA, Dunkel L. 2005. Pubertal upregulation of erythropoiesis in boys is determined primarily by androgen. J Pediatr 146:245-252.
25. Isidori AM, Giannetta E, Greco EA, Gianfrilli D, Bonifacio V, Isidori A, Lenzi A, Fabbri A. 2005. Effects of testosterone on body composition, bone metabolism and serum lipid profile in middle-aged men: a meta-analysis. Clin Endocrinol (Oxf) 63:280-293.
26. Kalinchenko SY, Tishova YA, Mskhalaya GJ, Gooren LJ, Giltay EJ, Saad F. 2010. Effects of testosterone supplementation on markers of the metabolic syndrome and inflammation in hypogonadal men with the metabolic syndrome: the double-blinded placebo-controlled Moscow study. Clin Endocrinol (Oxf) 73:602-612.
27. Kapoor D, Clarke S, Stanworth R, Channer KS, Jones TH. 2007. The effect of testosterone replacement therapy on adipocytokines and C-reactive protein in hypogonadal men with type 2 diabetes. Eur J Endocrinol 156:595-602.
28. Kley HK, Deselaers T, Peerenboom H, Kruskemper HL. 1980. Enhanced conversion of androstenedione to estrogens in obese males. J Clin Endocrinol Metab 51:1128-1132.
29. Kolaczkowska E, Kubes P. 2013. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13:159-175.
30. Korenchevsky V, Dennison M, Schalit R. 1932. The response of castrated male rats to the injection of testicular hormone. Biochem J 26:1306-1314.
31. Kotiaho JS. 2001. Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol Rev Camb Philos Soc 76:365-376.
32. Kupelian V, Chiu GR, Araujo AB, Williams RE, Clark RV, McKinlay JB. 2010. Association of sex hormones and C-reactive protein levels in men. Clin Endocrinol (Oxf) 72:527-533.
33. Laaksonen DE, Niskanen L, Punnonen K, Nyyssonen K, Tuomainen TP, Salonen R, Rauramaa R, Salonen JT. 2003. Sex hormones, inflammation and the metabolic syndrome: a population-based study. Eur J Endocrinol 149:601-608.
34. Labrie F. 1991. Intracrinology. Mol Cell Endocrinol 78:C113-C118.
35. Labrie F, Cusan L, Gomez JL, Martel C, Berube R, Belanger P, Belanger A, Vandenput L, Mellstrom D, Ohlsson C. 2009. Comparable amounts of sex steroids are made outside the gonads in men and women: strong lesson for hormone therapy of prostate and breast cancer. J Steroid Biochem Mol Biol 113:52-56.
36. Lowe GD. 2005. Circulating inflammatory markers and risks of cardiovascular and non-cardiovascular disease. J Thromb Haemost 3:1618-1627.
37. Madjid M, Willerson JT. 2011. Inflammatory markers in coronary heart disease. Br Med Bull 100:23-38.
38. Madsen EL, Rissanen A, Bruun JM, Skogstrand K, Tonstad S, Hougaard DM, Richelsen B. 2008. Weight loss larger than 10% is needed for general improvement of levels of circulating adiponectin and markers of inflammation in obese subjects: a 3-year weight loss study. Eur J Endocrinol 158:179-187.
39. Marriott I, Huet-Hudson YM. 2006. Sexual dimorphism in innate immune responses to infectious organisms. Immunol Res 34:177-192.
40. Mauvais-Jarvis P, Bercovici JP, Crepy O, Gauthier F. 1970. Studies on testosterone metabolism in subjects with testicular feminization syndrome. J Clin Invest 49:31-40.
41. Moghissi E, Ablan F, Horton R. 1984. Origin of plasma androstanediol glucuronide in men. J Clin Endocrinol Metab 59:417-421.
42. Morse MD, McNeel DG. 2010. Prostate cancer patients on androgen deprivation therapy develop persistent changes in adaptive immune responses. Hum Immunol 71:496-504.
43. Munoz-Cruz S, Togno-Pierce C, Morales-Montor J. 2011. Non-reproductive effects of sex steroids: their immunoregulatory role. Curr Top Med Chem 11:1714-1727.
44. Nakhai-Pour HR, Grobbee DE, Emmelot-Vonk MH, Bots ML, Verhaar HJ, van der Schouw YT. 2007. Oral testosterone supplementation and chronic low-grade inflammation in elderly men: a 26-week randomized, placebo-controlled trial. Am Heart J 154:1228.e1-7.
45. Nakhai Pour HR, Grobbee DE, Muller M, van der Schouw YT. 2007. Association of endogenous sex hormone with C-reactive protein levels in middle-aged and elderly men. Clin Endocrinol (Oxf) 66:394-398.
46. Ng MK, Liu PY, Williams AJ, Nakhla S, Ly LP, Handelsman DJ, Celermajer DS. 2002. Prospective study of effect of androgens on serum inflammatory markers in men. Arterioscler Thromb Vasc Biol. 22:1136-1141.
47. Pinto AC, Caetano LC, Levy AM, Fernandes RD, Santos CD, do Prado JCJ. 2010. Experimental Chagas' disease in orchiectomized Calomys callosus infected with the CM strain of Trypanosoma cruzi. Exp Parasitol 124:147-152.
48. Rana JS, Boekholdt SM, Ridker PM, Jukema JW, Luben R, Bingham SA, Day NE, Wareham NJ, Kastelein JJ, Khaw KT. 2007. Differential leucocyte count and the risk of future coronary artery disease in healthy men and women: the EPIC-Norfolk Prospective Population Study. J Intern Med 262:678-689.
49. Rolff J. 2002. Bateman's principle and immunity. Proc Biol Sci 269:867-872.
50. Sakiani S, Olsen NJ, Kovacs WJ. 2013. Gonadal steroids and humoral immunity. Nat Rev Endocrinol 9:56-62.
51. Sasaki M, Fujii Y, Iwamoto M, Ikadai H. 2013. Effect of sex steroids on Babesia microti infection in mice. Am J Trop Med Hyg 88:367-375.
52. Scher HI, Fizazi K, Saad F, Taplin ME, Sternberg CN, Miller K, de WR, Mulders P, Chi KN, Shore ND, Armstrong AJ, Flaig TW, Flechon A, Mainwaring P, Fleming M, Hainsworth JD, Hirmand M, Selby B, Seely L, de Bono JS. 2012. Increased survival with enzalutamide in prostate cancer after chemotherapy. N Engl J Med 367:1187-1197.
53. Schroderus E, Jokinen I, Koivula M, Koskela E, Mappes T, Mills SC, Oksanen TA, Poikonen T. 2010. Intra- and intersexual trade-offs between testosterone and immune system: implications for sexual and sexually antagonistic selection. Am Nat 176:E90-E97.
54. Schuurs AH, Verheul HA. 1990. Effects of gender and sex steroids on the immune response. J Steroid Biochem 35:157-172.
55. Selvin E, Feinleib M, Zhang L, Rohrmann S, Rifai N, Nelson WG, Dobs A, Basaria S, Golden SH, Platz EA. 2007. Androgens and diabetes in men: results from the Third National Health and Nutrition Examination Survey (NHANES III). Diabetes Care 30:234-238.
56. Shiels MS, Rohrmann S, Menke A, Selvin E, Crespo CJ, Rifai N, Dobs A, Feinleib M, Guallar E, Platz EA. 2009. Association of cigarette smoking, alcohol consumption, and physical activity with sex steroid hormone levels in US men. Cancer Causes Control 20:877-886.
57. Smith AM, English KM, Malkin CJ, Jones RD, Jones TH, Channer KS. 2005. Testosterone does not adversely affect fibrinogen or tissue plasminogen activator (tPA) and plasminogen activator inhibitor-1 (PAI-1) levels in 46 men with chronic stable angina. Eur J Endocrinol 152:285-291.
58. Stearns SC. 2005. Issues in evolutionary medicine. Am J Hum Biol 17:131-140.
59. Suzuki R, Allen NE, Appleby PN, Key TJ, Dossus L, Tjonneland A, Fons JN, Overvad K, Sacerdote C, Palli D, Krogh V, Tumino R, Rohrmann S, Linseisen J, Boeing H, Trichopoulou A, Makrygiannis G, Misirli G, Bueno-de-Mesquita HB, May AM, Diaz MJ, Sanchez MJ, Barricarte GA, Rodriguez SL, Buckland G, Larranaga N, Bingham S, Khaw KT, Rinaldi S, Slimani N, Jenab M, Riboli E, Kaaks R. 2009. Lifestyle factors and serum androgens among 636 middle aged men from seven countries in the European Prospective Investigation into Cancer and Nutrition (EPIC). Cancer Causes Control 20:811-821.
60. Swirski FK, Nahrendorf M. 2013. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science 339:161-166.
61. Tabas I, Glass CK. 2013. Anti-inflammatory therapy in chronic disease: challenges and opportunities. Science 339:166-172.
62. Tang YJ, Lee WJ, Chen YT, Liu PH, Lee MC, Sheu WH. 2007. Serum testosterone level and related metabolic factors in men over 70 years old. J Endocrinol Invest 30:451-458.
63. Turnbull AV, Rivier C. 1997. Inhibition of gonadotropin-induced testosterone secretion by the intracerebroventricular injection of interleukin-1 beta in the male rat. Endocrinology 138:1008-1013.
64. van der Poll T, Romijn JA, Endert E, Sauerwein HP. 1993. Effects of tumor necrosis factor on the hypothalamic-pituitary-testicular axis in healthy men. Metabolism 42:303-307.
65. Welsh P, Polisecki E, Robertson M, Jahn S, Buckley BM, de Craen AJ, Ford I, Jukema JW, Macfarlane PW, Packard CJ, Stott DJ, Westendorp RG, Shepherd J, Hingorani AD, Smith GD, Schaefer E, Sattar N. 2010. Unraveling the directional link between adiposity and inflammation: a bidirectional Mendelian randomization approach. J Clin Endocrinol Metab 95:93-99.
66. Xu L, Freeman G, Cowling BJ, Schooling CM. 2013. Testosterone and cardiovascular events among men: a systematic review and meta-analysis of placebo-controlled randomized trials. BMC Med 11:108.
67. Yang XC, Jing TY, Resnick LM, Phillips GB. 1993. Relation of hemostatic risk factors to other risk factors for coronary heart disease and to sex hormones in men. Arterioscler Thromb 13:467-471.
68. Zhang Y, Gao Y, Tan A, Yang X, Zhang H, Zhang S, Wu C, Lu Z, Wang M, Liao M, Qin X, Li L, Hu Y, Mo Z. 2013. Endogenous Sex Hormones and C-reactive protein in Healthy Chinese Men. Clin Endocrinol (Oxf) 78:60-66.
69. Zuk M. 2009. The sicker sex. PLoS Pathog 5:e1000267.