113
Views
8
CrossRef citations to date
0
Altmetric
Review

The impact of obesity on male reproduction: its biological significance

, , , &
Pages 139-148 | Published online: 10 Jan 2014

References

  • Carlsen E, Giwercman A, Keiding N, Skakkebaek NE. Evidence for decreasing quality of semen during past 50 years. BMJ 305(6854), 609–613 (1992).
  • Jouannet P, Wang C, Eustache F, Kold-Jensen T, Auger J. Semen quality and male reproductive health: the controversy about human sperm concentration decline. APMIS 109(5), 333–344 (2001).
  • Swan SH, Elkin EP, Fenster L. The question of declining sperm density revisited: an analysis of 101 studies published 1934–1996. Environ. Health. Perspect. 108, 961–966 (2000).
  • Cabler S, Agarwal A, Flint M, du Plessis SS. Obesity: modern man’s fertility nemesis. Asian J. Androl. 12(4), 480–489 (2010).
  • Teerds KJ, de Rooij DG, Keijer J. Functional relationship between obesity and male reproduction: from humans to animal models. Hum. Reprod. Update 17(5), 667–683 (2011).
  • Jensen TK, Andersson AM, Jørgensen N et al. Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertil. Steril. 82(4), 863–870 (2004).
  • Du Plessis SS, Cabler S, McAlister DA, Sabanegh E, Agarwal A. The effect of obesity on sperm disorders and male infertility. Nat. Rev. Urol. 7(3), 153–161 (2010).
  • Hammoud AO, Gibson M, Peterson CM, Meikle AW, Carrell DT. Impact of male obesity on infertility: a critical review of the current literature. Fertil. Steril. 90(4), 897–904 (2008).
  • Mah PM, Wittert GA. Obesity and testicular function. Mol. Cell. Endocrinol. 316(2), 180–186 (2010).
  • BragaDP, HalpernG, FigueiraRde C, SettiAS, IaconelliA Jr, BorgesE Jr. Food intake and social habits in male patients and its relationship to intracytoplasmic sperm injection outcomes. Fertil. Steril. 97(1), 53–59 (2012).
  • Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of obesity in the United States, 2009–2010. NCHS Data Brief 82, 1–8 (2012).
  • Kaufman JM, Vermeulen A. The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocr. Rev. 26(6), 833–876 (2005).
  • Pasquali R, Patton L, Gambineri A. Obesity and infertility. Curr. Opin. Endocrinol. Diabetes. Obes. 14(6), 482–487 (2007).
  • Hammoud AO, Gibson M, Peterson CM, Hamilton BD, Carrell DT. Obesity and male reproductive potential. J. Androl. 27(5), 619–626 (2006).
  • Pardridge WM. Serum bioavailability of sex steroid hormones. Clin. Endocrinol. Metab. 15(2), 259–278 (1986).
  • 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. 85(9), 3276–3282 (2000).
  • Roth MY, Amory JK, Page ST. Treatment of male infertility secondary to morbid obesity. Nat. Clin. Pract. Endocrinol. Metab. 4(7), 415–419 (2008).
  • Berndtson WE, Thompson TL. Changing relationships between testis size, Sertoli cell number and spermatogenesis in Sprague–Dawley rats. J. Androl. 11(5), 429–435 (1990).
  • Kumanov P, Nandipati K, Tomova A, Agarwal A. Inhibin B is a better marker of spermatogenesis than other hormones in the evaluation of male factor infertility. Fertil. Steril. 86(2), 332–338 (2006).
  • Pauli EM, Legro RS, Demers LM, Kunselman AR, Dodson WC, Lee PA. Diminished paternity and gonadal function with increasing obesity in men. Fertil. Steril. 90(2), 346–351 (2008).
  • Haffner SM. Sex hormones, obesity, fat distribution, Type 2 diabetes and insulin resistance: epidemiological and clinical correlation. Int. J. Obes. Relat. Metab. Disord. 24(Suppl. 2), S56–S58 (2000).
  • Pasquali R, Casimirri F, Cantobelli S et al. Effect of obesity and body fat distribution on sex hormones and insulin in men. Metab. Clin. Exp. 40(1), 101–104 (1991).
  • Isidori AM, Caprio M, Strollo F et al. Leptin and androgens in male obesity: evidence for leptin contribution to reduced androgen levels. J. Clin. Endocrinol. Metab. 84(10), 3673–3680 (1999).
  • Lima N, Cavaliere H, Knobel M, Halpern A, Medeiros-Neto G. Decreased androgen levels in massively obese men may be associated with impaired function of the gonadostat. Int. J. Obes. Relat. Metab. Disord. 24(11), 1433–1437 (2000).
  • Wu FC, Tajar A, Pye SR et al.; European Male Aging Study Group. 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. 93(7), 2737–2745 (2008).
  • Vermeulen A, Kaufman JM, Deslypere JP, Thomas G. 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(5), 1140–1146 (1993).
  • Giagulli VA, Kaufman JM, Vermeulen A. Pathogenesis of the decreased androgen levels in obese men. J. Clin. Endocrinol. Metab. 79(4), 997–1000 (1994).
  • Trayhurn P, Beattie JH. Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ. Proc. Nutr. Soc. 60(3), 329–339 (2001).
  • El-Hefnawy T, Ioffe S, Dym M. Expression of the leptin receptor during germ cell development in the mouse testis. Endocrinology 141(7), 2624–2630 (2000).
  • Ishikawa T, Fujioka H, Ishimura T, Takenaka A, Fujisawa M. Expression of leptin and leptin receptor in the testis of fertile and infertile patients. Andrologia 39(1), 22–27 (2007).
  • Luboshitzky R, Lavie L, Shen-Orr Z, Herer P. Altered luteinizing hormone and testosterone secretion in middle-aged obese men with obstructive sleep apnea. Obes. Res. 13(4), 780–786 (2005).
  • Meston N, Davies RJ, Mullins R, Jenkinson C, Wass JA, Stradling JR. Endocrine effects of nasal continuous positive airway pressure in male patients with obstructive sleep apnoea. J. Intern. Med. 254(5), 447–454 (2003).
  • HayesFJ, SeminaraSB, DecruzS, BoepplePA, CrowleyWF Jr. Aromatase inhibition in the human male reveals a hypothalamic site of estrogen feedback. J. Clin. Endocrinol. Metab. 85(9), 3027–3035 (2000).
  • Akingbemi BT. Estrogen regulation of testicular function. Reprod. Biol. Endocrinol. 3, 51 (2005).
  • de Boer H, Verschoor L, Ruinemans-Koerts J, Jansen M. Letrozole normalizes serum testosterone in severely obese men with hypogonadotropic hypogonadism. Diabetes. Obes. Metab. 7(3), 211–215 (2005).
  • Hammoud AO, Wilde N, Gibson M, Parks A, Carrell DT, Meikle AW. Male obesity and alteration in sperm parameters. Fertil. Steril. 90(6), 2222–2225 (2008).
  • Pavlovich CP, King P, Goldstein M, Schlegel PN. Evidence of a treatable endocrinopathy in infertile men. J. Urol. 165(3), 837–841 (2001).
  • Goyal HO, Robateau A, Braden TD, Williams CS, Srivastava KK, Ali K. Neonatal estrogen exposure of male rats alters reproductive functions at adulthood. Biol. Reprod. 68(6), 2081–2091 (2003).
  • Hammoud A, Carrell DT, Meikle AW et al. An aromatase polymorphism modulates the relationship between weight and estradiol levels in obese men. Fertil. Steril. 94(5), 1734–1738 (2010).
  • Caprio M, Isidori AM, Carta AR, Moretti C, Dufau ML, Fabbri A. Expression of functional leptin receptors in rodent Leydig cells. Endocrinology 140(11), 4939–4947 (1999).
  • Jope T, Lammert A, Kratzsch J, Paasch U, Glander HJ. Leptin and leptin receptor in human seminal plasma and in human spermatozoa. Int. J. Androl. 26(6), 335–341 (2003).
  • Bener A, Al-Ansari AA, Zirie M, Al-Hamaq AO. Is male fertility associated with type 2 diabetes mellitus? Int. Urol. Nephrol. 41(4), 777–784 (2009).
  • Kasturi SS, Tannir J, Brannigan RE. The metabolic syndrome and male infertility. J. Androl. 29(3), 251–259 (2008).
  • Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P. Frequent occurrence of hypogonadotropic hypogonadism in Type 2 diabetes. J. Clin. Endocrinol. Metab. 89(11), 5462–5468 (2004).
  • Kapoor D, Channer KS, Jones TH. Rosiglitazone increases bioactive testosterone and reduces waist circumference in hypogonadal men with Type 2 diabetes. Diab. Vasc. Dis. Res. 5(2), 135–137 (2008).
  • Globerman H, Shen-Orr Z, Karnieli E, Aloni Y, Charuzi I. Inhibin B in men with severe obesity and after weight reduction following gastroplasty. Endocr. Res. 31(1), 17–26 (2005).
  • Winters SJ, Wang C, Abdelrahaman E, Hadeed V, Dyky MA, Brufsky A. Inhibin-B levels in healthy young adult men and prepubertal boys: is obesity the cause for the contemporary decline in sperm count because of fewer Sertoli cells? J. Androl. 27(4), 560–564 (2006).
  • Zorn B, Osredkar J, Meden-Vrtovec H, Majdic G. Leptin levels in infertile male patients are correlated with inhibin B, testosterone and SHBG but not with sperm characteristics. Int. J. Androl. 30, 439–444 (2007).
  • Olsen J, Melbye M, Olsen SF et al. The Danish National Birth Cohort – its background, structure and aim. Scand. J. Public Health 29(4), 300–307 (2001).
  • Nguyen RH, Wilcox AJ, Skjaerven R, Baird DD. Men’s body mass index and infertility. Hum. Reprod. 22(9), 2488–2493 (2007).
  • Magnusdottir EV, Thorsteinsson T, Thorsteinsdottir S, Heimisdottir M, Olafsdottir K. Persistent organochlorines, sedentary occupation, obesity and human male subfertility. Hum. Reprod. 20(1), 208–215 (2005).
  • WHO. WHO Laboratory Manual for the Examination of Human Semen and Sperm-cervical Mucus Interaction. Cambridge University Press, MA, USA (1999).
  • Stewart TM, Liu DY, Garrett C, Jørgensen N, Brown EH, Baker HW. Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output. Hum. Reprod. 24(7), 1561–1568 (2009).
  • Sermondade N, Faure C, Fezeu L, Lévy R, Czernichow S; Obesity-Fertility Collaborative Group. Obesity and increased risk for oligozoospermia and azoospermia. Arch. Intern. Med. 172(5), 440–442 (2012).
  • Martini AC, Tissera A, Estofán D et al. Overweight and seminal quality: a study of 794 patients. Fertil. Steril. 94(5), 1739–1743 (2010).
  • MacDonald AA, Herbinson GP, Showell M, Farquhar CM. The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis. Hum. Reprod. Update 16, 293–311 (2010).
  • Qin DD, Yuan W, Zhou WJ, Cui YQ, Wu JQ, Gao ES. Do reproductive hormones explain the association between body mass index and semen quality? Asian J. Androl. 9(6), 827–834 (2007).
  • Chauvin TR, Griswold MD. Androgen-regulated genes in the murine epididymis. Biol. Reprod. 71(2), 560–569 (2004).
  • Cooper TG, Yeung CH, Nashan D, Nieschlag E. Epididymal markers in human infertility. J. Androl. 9(2), 91–101 (1988).
  • Mahmoud AM, Geslevich J, Kint J et al. Seminal plasma α-glucosidase activity and male infertility. Hum. Reprod. 13(3), 591–595 (1998).
  • Castellón EA, Huidobro CC. Androgen regulation of glycosidase secretion in epithelial cell cultures from human epididymis. Hum. Reprod. 14(6), 1522–1527 (1999).
  • Martini AC, Molina RI, Vincenti LM et al. Neutral α-glucosidase activity in mouse: a marker of epididymal function? Reprod. Fertil. Dev. 19(4), 563–568 (2007).
  • Kort HI, Massey JB, Elsner CW et al. Impact of body mass index values on sperm quantity and quality. J. Androl. 27(3), 450–452 (2006).
  • Lanfranco F, Kamischke A, Zitzmann M, Nieschlag E. Klinefelter’s syndrome. Lancet 364(9430), 273–283 (2004).
  • Suzuki Y, Sasagawa I, Tateno T, Yazawa H, Ashida J, Nakada T. Absence of microdeletions in the Y chromosome in patients with Prader–Willi syndrome with cryptorchidism. Int. J. Androl. 25(1), 1–5 (2002).
  • Bacon CG, Mittleman MA, Kawachi I, Giovannucci E, Glasser DB, Rimm EB. Sexual function in men older than 50 years of age: results from the health professionals follow-up study. Ann. Intern. Med. 139(3), 161–168 (2003).
  • Feldman HA, Johannes CB, Derby CA et al. Erectile dysfunction and coronary risk factors: prospective results from the Massachusetts male aging study. Prev. Med. 30(4), 328–338 (2000).
  • Guay AT, Traish A. Testosterone deficiency and risk factors in the metabolic syndrome: implications for erectile dysfunction. Urol. Clin. North Am. 38(2), 175–183 (2011).
  • Yassin AA, Akhras F, El-Sakka AI, Saad F. Cardiovascular diseases and erectile dysfunction: the two faces of the coin of androgen deficiency. Andrologia 43(1), 1–8 (2011).
  • Kolotkin RL, Zunker C, Østbye T. Sexual functioning and obesity: a review. Obesity (Silver Spring). 20(12), 2325–2333 (2012).
  • Strain GW, Zumoff B, Kream J et al. Mild Hypogonadotropic hypogonadism in obese men. Metab. Clin. Exp. 31(9), 871–875 (1982).
  • Traish AM, Feeley RJ, Guay A. Mechanisms of obesity and related pathologies: androgen deficiency and endothelial dysfunction may be the link between obesity and erectile dysfunction. FEBS J. 276(20), 5755–5767 (2009).
  • Sullivan ME, Thompson CS, Dashwood MR et al. Nitric oxide and penile erection: is erectile dysfunction another manifestation of vascular disease? Cardiovasc. Res. 43(3), 658–665 (1999).
  • Tamler R. Diabetes, obesity, and erectile dysfunction. Gend. Med. 6(Suppl. 1), 4–16 (2009).
  • Agarwal A, Nandipati KC, Sharma RK, Zippe CD, Raina R. Role of oxidative stress in the pathophysiological mechanism of erectile dysfunction. J. Androl. 27(3), 335–347 (2006).
  • Oliva A, Spira A, Multigner L. Contribution of environmental factors to the risk of male infertility. Hum. Reprod. 16(8), 1768–1776 (2001).
  • Sikka SC, Wang R. Endocrine disruptors and estrogenic effects on male reproductive axis. Asian J. Androl. 10(1), 134–145 (2008).
  • Lampiao F, du Plessis SS. TNF-α and IL-6 affect human sperm function by elevating nitric oxide production. Reprod. Biomed. Online 17(5), 628–631 (2008).
  • Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R. Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 111(11), 1448–1454 (2005).
  • Davì G, Falco A. Oxidant stress, inflammation and atherogenesis. Lupus 14(9), 760–764 (2005).
  • Agarwal A, Sharma RK, Nallella KP, Thomas AJ Jr, Alvarez JG, Sikka SC. Reactive oxygen species as an independent marker of male factor infertility. Fertil. Steril. 86(4), 878–885 (2006).
  • Aitken RJ, Jones KT, Robertson SA. Reactive oxygen species and sperm function – in sickness and in health. J. Androl. 33(6), 1096–1106 (2012).
  • Sharpe RM. Environmental/lifestyle effects on spermatogenesis. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 365(1546), 1697–1712 (2010).
  • Ganong WF. Review of Medical Physiology, 22nd edition. Lange Medical Books/Mc Graw-Hill, OH, USA (2005).
  • Setchell BP. The Parkes Lecture. Heat and the testis. J. Reprod. Fertil. 114(2), 179–194 (1998).
  • Paul C, Teng S, Saunders PT. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol. Reprod. 80(5), 913–919 (2009).
  • Hjollund NH, Storgaard L, Ernst E, Bonde JP, Olsen J. The relation between daily activities and scrotal temperature. Reprod. Toxicol. 16(3), 209–214 (2002).
  • Shafik A, Olfat S. Lipectomy in the treatment of scrotal lipomatosis. Br. J. Urol. 53(1), 55–61 (1981).
  • Hjollund NH, Bonde JP, Jensen TK, Olsen J. Diurnal scrotal skin temperature and semen quality. The Danish First Pregnancy Planner Study Team. Int. J. Androl. 23(5), 309–318 (2000).
  • Kaukua J, Pekkarinen T, Sane T, Mustajoki P. Sex hormones and sexual function in obese men losing weight. Obes. Res. 11(6), 689–694 (2003).
  • Bastounis EA, Karayiannakis AJ, Syrigos K, Zbar A, Makri GG, Alexiou D. Sex hormone changes in morbidly obese patients after vertical banded gastroplasty. Eur. Surg. Res. 30(1), 43–47 (1998).
  • di Frega AS, Dale B, Di Matteo L, Wilding M. Secondary male factor infertility after Roux-en-Y gastric bypass for morbid obesity: case report. Hum. Reprod. 20(4), 997–998 (2005).
  • Sermondade N, Massin N, Boitrelle F et al. Sperm parameters and male fertility after bariatric surgery: three case series. Reprod. Biomed. Online 24(2), 206–210 (2012).
  • Pasquali R. Obesity and androgens: facts and perspectives. Fertil. Steril. 85(5), 1319–1340 (2006).
  • Raman JD, Schlegel PN. Aromatase inhibitors for male infertility. J. Urol. 167(2 Pt 1), 624–629 (2002).
  • Martini AC, Molina RI, Ruiz RD et al. [Obesity and male fertility]. Rev. Fac. Cs Med. 69(2), 102–110 (2012).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.