Fertility and Sterility
Volume 90, Issue 4 , Pages 897-904 , October 2008

Impact of male obesity on infertility: a critical review of the current literature

  • Ahmad O. Hammoud, M.D.

      Affiliations

    • Division of Reproductive Endocrinology and Infertility, Department of Obstetrics and Gynecology, University of Utah School of Medicine, Salt Lake City, Utah
  • ,
  • Mark Gibson, M.D.

      Affiliations

    • Division of Reproductive Endocrinology and Infertility, Department of Obstetrics and Gynecology, University of Utah School of Medicine, Salt Lake City, Utah
  • ,
  • C. Matthew Peterson, M.D.

      Affiliations

    • Division of Reproductive Endocrinology and Infertility, Department of Obstetrics and Gynecology, University of Utah School of Medicine, Salt Lake City, Utah
  • ,
  • A. Wayne Meikle, M.D.

      Affiliations

    • Endocrinology/Diabetes Research, Department of Medicine, University of Utah School of Medicine, Salt Lake City, Utah
  • ,
  • Douglas T. Carrell, Ph.D.

      Affiliations

    • Division of Reproductive Endocrinology and Infertility, Department of Obstetrics and Gynecology, University of Utah School of Medicine, Salt Lake City, Utah
    • Andrology and IVF Laboratories, Department of Surgery (Urology) and Physiology, University of Utah School of Medicine, Salt Lake City, Utah
    • Corresponding Author InformationReprint requests: Dr. Douglas T. Carrell, Division of Urology-Andrology/IVF Laboratories, Department of Andrology, University of Utah School of Medicine, 675 Arapeen Dr., Suite 205, Salt Lake City, Utah 84108 (FAX: 801-581-3740).

Received 5 October 2007 ,Revised 8 January 2008 ,Accepted 7 August 2008.

References 

  1. Barnett R. Obesity. Lancet. 2005;365:1843
  2. Abdel-Halim RE. Obesity: 1000 years ago. Lancet. 2005;366:204
  3. Avicenna. The disadvantages of excessive weight. In: Avicenna. The canon of medicine, book IV: diseases involving more than one member; the Cosmetic art. Rome: Medical Press, 1593:173–174.
  4. Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999–2002. JAMA. 2004;291:2847–2850
  5. Mokdad AH, Serdula MK, Dietz WH, Bowman BA, Marks JS, Koplan JP. The spread of the obesity epidemic in the United States, 1991–1998. JAMA. 1999;282:1519–1522
  6. Pasquali R, Pelusi C, Genghini S, Cacciari M, Gambineri A. Obesity and reproductive disorders in women. Hum Reprod Update. 2003;9:359–372
  7. Sallmen M, Sandler DP, Hoppin JA, Blair A, Baird DD. Reduced fertility among overweight and obese men. Epidemiology. 2006;17:520–523
  8. Alavanja MC, Sandler DP, McMaster SB, Zahm SH, McDonnell CJ, Lynch CF, et al. The Agricultural Health Study. Environ Health Perspect. 1996;104:362–369
  9. Reddy UM, Wapner RJ, Rebar RW, Tasca RJ. Infertility, assisted reproductive technology, and adverse pregnancy outcomes: executive summary of a National Institute of Child Health and Human Development workshop. Obstet Gynecol. 2007;109:967–977
  10. Jimenez Torres M, Campoy Folgoso C, Canabate Reche F, Rivas Velasco A, Cerrillo Garcia I, Mariscal Arcas M, et al. Organochlorine pesticides in serum and adipose tissue of pregnant women in southern Spain giving birth by cesarean section. Sci Total Environ. 2006;372:32–38
  11. Munoz-de-Toro M, Beldomenico HR, Garcia SR, Stoker C, De Jesus JJ, Beldomenico PM, et al. Organochlorine levels in adipose tissue of women from a littoral region of Argentina. Environ Res. 2006;102:107–112
  12. Kahn H, Cheng Y. Longitudinal changes in BMI and in an index estimating excess lipids among white and black adults in the United States. Int J Obes. 2008;32:136–143
  13. Ramlau-Hansen CH, Thulstrup AM, Nohr EA, Bonde JP, Sorensen TI, Olsen J. Subfecundity in overweight and obese couples. Hum Reprod. 2007;22:1634–1637
  14. Olsen J, Melbye M, Olsen SF, Sorensen TI, Aaby P, Andersen AM, et al. The Danish National Birth Cohort—its background, structure and aim. Scand J Public Health. 2001;29:300–307
  15. Nguyen R, Wilcox A, Skjaerven R, Baird DD. Men's body mass index and infertility. Hum Reprod. 2007;17:2488–2493
  16. Magnusdottir EV, Thorsteinsson T, Thorsteinsdottir S, Heimisdottir M, Olafsdottir K. Persistent organochlorines, sedentary occupation, obesity and human male subfertility. Hum Reprod. 2005;20:208–215
  17. Hanafy S, Halawa FA, Mostafa T, Mikhael NW, Khalil KT. Serum leptin correlates in infertile oligozoospermic males. Andrologia. 2007;39:177–180
  18. 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. 2006;
  19. Bonde JP, Ernst E, Jensen TK, Hjollund NH, Kolstad H, Henriksen TB, et al. Relation between semen quality and fertility: a population-based study of 430 first-pregnancy planners. Lancet. 1998;352:1172–1177
  20. Slama R, Eustache F, Ducot B, Jensen TK, Jorgensen N, Horte A, et al. Time to pregnancy and semen parameters: a cross-sectional study among fertile couples from four European cities. Hum Reprod. 2002;17:503–515
  21. Guzick DS, Overstreet JW, Factor-Litvak P, Brazil CK, Nakajima ST, Coutifaris C, et al. Sperm morphology, motility, and concentration in fertile and infertile men. N Engl J Med. 2001;345:1388–1393
  22. Jensen TK, Andersson AM, Jorgensen N, Andersen AG, Carlsen E, Petersen JH, et al. Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertil Steril. 2004;82:863–870
  23. Castilla JA, Alvarez C, Aguilar J, Gonzalez-Varea C, Gonzalvo MC, Martinez L. Influence of analytical and biological variation on the clinical interpretation of seminal parameters. Hum Reprod. 2006;21:847–851
  24. Hammoud AO, Gibson M, Peterson CM, Carrell DT. Effect of sperm preparation techniques by density gradient on intra-individual variation of sperm motility. Arch Androl. 2007;53:349–351
  25. Keel BA. Within- and between-subject variation in semen parameters in infertile men and normal semen donors. Fertil Steril. 2006;85:128–134
  26. Fejes I, Koloszar S, Szollosi J, Zavaczki Z, Pal A. Is semen quality affected by male body fat distribution?. Andrologia. 2005;37:155–159
  27. Kort HI, Massey JB, Elsner CW, Mitchell-Leef D, Shapiro DB, Witt MA, et al. Impact of body mass index values on sperm quantity and quality. J Androl. 2006;27:450–452
  28. Giagulli VA, Kaufman JM, Vermeulen A. Pathogenesis of the decreased androgen levels in obese men. J Clin Endocrinol Metab. 1994;79:997–1000
  29. Tchernof A, Despres JP, Belanger A, Dupont A, Prud'homme D, Moorjani S, et al. Reduced testosterone and adrenal C19 steroid levels in obese men. Metabolism. 1995;44:513–519
  30. Schneider G, Kirschner MA, Berkowitz R, Ertel NH. Increased estrogen production in obese men. J Clin Endocrinol Metab. 1979;48:633–638
  31. Akingbemi BT. Estrogen regulation of testicular function. Reprod Biol Endocrinol. 2005;3:51
  32. de Boer H, Verschoor L, Ruinemans-Koerts J, Jansen M. Letrozole normalizes serum testosterone in severely obese men with hypogonadotropic hypogonadism. Diabetes Obes Metab. 2005;7:211–215
  33. Pavlovich CP, King P, Goldstein M, Schlegel PN. Evidence of a treatable endocrinopathy in infertile men. J Urol. 2001;165:837–841
  34. 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. 2003;68:2081–2091
  35. 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
  36. 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. 2005;31:17–26
  37. Tsai EC, Matsumoto AM, Fujimoto WY, Boyko EJ. Association of bioavailable, free, and total testosterone with insulin resistance: influence of sex hormone-binding globulin and body fat. Diabetes Care. 2004;27:861–868
  38. 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. 2005;13:780–786
  39. Luboshitzky R, Zabari Z, Shen-Orr Z, Herer P, Lavie P. Disruption of the nocturnal testosterone rhythm by sleep fragmentation in normal men. J Clin Endocrinol Metab. 2001;86:1134–1139
  40. 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. 1993;76:1140–1146
  41. Blank DM, Clark RV, Heymsfield SB, Rudman DR, Blank MS. Endogenous opioids and hypogonadism in human obesity. Brain Res Bull. 1994;34:571–574
  42. Ballester J, Munoz MC, Dominguez J, Rigau T, Guinovart JJ, Rodriguez-Gil JE. Insulin-dependent diabetes affects testicular function by FSH- and LH-linked mechanisms. J Androl. 2004;25:706–719
  43. Baccetti B, La Marca A, Piomboni P, Capitani S, Bruni E, Petraglia F, et al. Insulin-dependent diabetes in men is associated with hypothalamo-pituitary derangement and with impairment in semen quality. Hum Reprod. 2002;17:2673–2677
  44. Agbaje IM, Rogers DA, McVicar CM, McClure N, Atkinson AB, Mallidis C, et al. Insulin dependant diabetes mellitus: implications for male reproductive function. Hum Reprod. 2007;22:1871–1877
  45. 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. 2006;86:332–338
  46. 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. 2006;27:560–564
  47. Cortet-Rudelli C, Pigny P, Decanter C, Leroy M, Maunoury-Lefebvre C, Thomas-Desrousseaux P, et al. Obesity and serum luteinizing hormone level have an independent and opposite effect on the serum inhibin B level in patients with polycystic ovary syndrome. Fertil Steril. 2002;77:281–287
  48. De Pergola G, Maldera S, Tartagni M, Pannacciulli N, Loverro G, Giorgino R. Inhibitory effect of obesity on gonadotropin, estradiol, and inhibin B levels in fertile women. Obesity (Silver Spring). 2006;14:1954–1960
  49. Oliva A, Spira A, Multigner L. Contribution of environmental factors to the risk of male infertility. Hum Reprod. 2001;16:1768–1776
  50. Sharpe RM. Lifestyle and environmental contribution to male infertility. Br Med Bull. 2000;56:630–642
  51. Mieusset R, Bujan LE, Massat G, Mansat A, Pontonnier F. Inconstant ascending testis as a potential risk factor for spermatogenesis in infertile men with no history of cryptorchism. Hum Reprod. 1997;12:974–979
  52. Ivell R. Lifestyle impact and the biology of the human scrotum. Reprod Biol Endocrinol. 2007;5:15
  53. Bujan L, Daudin M, Charlet JP, Thonneau P, Mieusset R. Increase in scrotal temperature in car drivers. Hum Reprod. 2000;15:1355–1357
  54. Figa-Talamanca I, Cini C, Varricchio GC, Dondero F, Gandini L, Lenzi A, et al. Effects of prolonged autovehicle driving on male reproduction function: a study among taxi drivers. Am J Ind Med. 1996;30:750–758
  55. Brindley GS. Deep scrotal temperature and the effect on it of clothing, air temperature, activity, posture and paraplegia. Br J Urol. 1982;54:49–55
  56. Momen MN, Fahmy I, Amer M, Arafa M, Zohdy W, Naser TA. Semen parameters in men with spinal cord injury: changes and aetiology. Asian J Androl. 2007;9:684–689
  57. Shafik A, Olfat S. Lipectomy in the treatment of scrotal lipomatosis. Br J Urol. 1981;53:55–61
  58. Jung A, Schill WB. [Male infertility. Current life style could be responsible for infertility]. MMW Fortschr Med. 2000;142:31–33German
  59. Lanfranco F, Kamischke A, Zitzmann M, Nieschlag E. Klinefelter's syndrome. Lancet. 2004;364:273–283
  60. 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. 2002;25:1–5
  61. Diemer T, Desjardins C. Developmental and genetic disorders in spermatogenesis. Hum Reprod Update. 1999;5:120–140
  62. Chehab FF, Lim ME, Lu R. Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nat Genet. 1996;12:318–320
  63. Farooqi IS, Wangensteen T, Collins S, Kimber W, Matarese G, Keogh JM, et al. Clinical and molecular genetic spectrum of congenital deficiency of the leptin receptor. N Engl J Med. 2007;356:237–247
  64. 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. 2003;139:161–168
  65. Feldman HA, Johannes CB, Derby CA, Kleinman KP, Mohr BA, Araujo AB, et al. Erectile dysfunction and coronary risk factors: prospective results from the Massachusetts Male Aging Study. Prev Med. 2000;30:328–338
  66. O'Brien JH, Lazarou S, Deane L, Jarvi K, Zini A. Erectile dysfunction and andropause symptoms in infertile men. J Urol. 2005;174:1932–1934discussion 1934
  67. Seftel A. Male hypogonadism. Part II: etiology, pathophysiology, and diagnosis. Int J Impot Res. 2006;18:223–228
  68. Sullivan ME, Thompson CS, Dashwood MR, Khan MA, Jeremy JY, Morgan RJ, et al. Nitric oxide and penile erection: is erectile dysfunction another manifestation of vascular disease?. Cardiovasc Res. 1999;43:658–665
  69. Chung WS, Sohn JH, Park YY. Is obesity an underlying factor in erectile dysfunction?. Eur Urol. 1999;36:68–70
  70. Brody S. Slimness is associated with greater intercourse and lesser masturbation frequency. J Sex Marital Ther. 2004;30:251–261
  71. Kaukua J, Pekkarinen T, Sane T, Mustajoki P. Sex hormones and sexual function in obese men losing weight. Obes Res. 2003;11:689–694
  72. Niskanen L, Laaksonen DE, Punnonen K, Mustajoki P, Kaukua J, Rissanen A. Changes in sex hormone–binding globulin and testosterone during weight loss and weight maintenance in abdominally obese men with the metabolic syndrome. Diabetes Obes Metab. 2004;6:208–215
  73. 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. 1998;30:43–47
  74. Esposito K, Giugliano F, Di Palo C, Giugliano G, Marfella R, D'Andrea F, et al. Effect of lifestyle changes on erectile dysfunction in obese men: a randomized controlled trial. JAMA. 2004;291:2978–2984
  75. Semple PA, Graham A, Malcolm Y, Beastall GH, Watson WS. Hypoxia, depression of testosterone, and impotence in pickwickian syndrome reversed by weight reduction. Br Med J (Clin Res Ed). 1984;289:801–802

 Edward E. Wallach, M.D.Associate Editor

 A.H. has nothing to disclose. M.G. has nothing to disclose. C.M.P. has nothing to disclose. A.W.M. has nothing to disclose. D.C. has nothing to disclose.

PII: S0015-0282(08)03352-9

doi: 10.1016/j.fertnstert.2008.08.026

Fertility and Sterility
Volume 90, Issue 4 , Pages 897-904 , October 2008