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Hormones

, Volume 14, Issue 4, pp 563–568 | Cite as

The impact of obesity on male fertility

  • Thomas J. G. Chambers
  • Richard A. Anderson
Review

Abstract

Obesity in men of reproductive age is globally on the increase. There is clear evidence from epidemiological studies that obesity impacts negatively on male fertility; it is associated with hypogonadism, although it is less consistently linked to impaired spermatogenesis and tests of sperm function, including DNA fragmentation. Sperm from obese men used for in vitro fertilisation/intra cytoplasmic sperm injection is associated with a greater number of pregnancy losses and is less likely to result in live births. There are also increasing data from animal studies that paternal obesity may impact negatively on the reproductive and metabolic health of offspring and grand-offspring. It has been suggested that high-fat dietary exposures could affect the epigenetic content of sperm or the endocrine content of seminal fluid and thus impact early fetal development. Experimental and epidemiological data show that male fertility, and offspring health, can be improved by weight loss in obese and overweight males.

Key words

Fertility Hypogonadism Infertility Metabolic syndrome Overweight Paternal Sperm 

References

  1. 1.
    Ng M, Fleming T, Robinson M, et al, 2014 Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384: 766–781.CrossRefGoogle Scholar
  2. 2.
    Wang YC, McPherson K, Marsh T, Gortmaker SL, Brown M, 2011 Health and economic burden of the projected obesity trends in the USA and the UK. Lancet 378: 815–825.CrossRefGoogle Scholar
  3. 3.
    WHO. WHO Obesity and overweight [Internet]. WHO2014 [cited 2014 May 21]; Available from: http://www.who.int/mediacentre/factsheets/fs311/en/
  4. 4.
    Eisenberg ML, Kim S, Chen Z, Sundaram R, Schisterman EF, Buck Louis GM, 2014 The relationship between male BMI and waist circumference on semen quality: data from the LIFE study. Hum Reprod Oxf Engl 29: 193–200.CrossRefGoogle Scholar
  5. 5.
    Kaya E, Sikka SC, Gur S, 2015 A Comprehensive Review of Metabolic Syndrome Affecting Erectile Dysfunction. J Sex Med 12: 856–875.CrossRefGoogle Scholar
  6. 6.
    Wu FCW, Tajar A, Pye SR, Silman AJ, et al, 2008 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: 2737–2745.CrossRefGoogle Scholar
  7. 7.
    MacDonald AA, Herbison GP, Showeil M, Farquhar CM, 2010 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.CrossRefGoogle Scholar
  8. 8.
    Vermeulen A, Kaufman JM, Deslypere JP, Thomas G, 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.PubMedGoogle Scholar
  9. 9.
    Roa J, Tena-Sempere M, 2014 Connecting metabolism and reproduction: roles of central energy sensors and key molecular mediators. Mol Cell Endocrinol 397: 4–14.CrossRefGoogle Scholar
  10. 10.
    Camacho EM, Huhtaniemi IT, O’Neill TW, et al, 2013 Age-associated changes in hypothalamic-pituitary-testicular function in middle-aged and older men are modified by weight change and lifestyle factors: longitudinal results from the European Male Ageing Study. Eur J Endocrinol Eur Fed Endocr Soc 168: 445–455.CrossRefGoogle Scholar
  11. 11.
    Rastrelli G, Carter EL, Ahern T, et al, 2015 Development of and Recovery from Secondary Hypogonadism in Ageing Men: Prospective Results from the EMAS. J Clin Endocrinol Metab 100: 3172–3182.CrossRefGoogle Scholar
  12. 12.
    Corona G, Rastrelli G, Monami M, et al, 2013 Body weight loss reverts obesity-associated hypogonadotropic hypogonadism: a systematic review and meta-analysis. Eur J Endocrinol Eur Fed Endocr Soc 168: 829–843.CrossRefGoogle Scholar
  13. 13.
    Martin JA, Hamilton BE, Osterman MJ, Curtin SC, Matthews TJ, 2015 Births: final data for 2013. Natl Vital Stat Rep Cent Dis Control Prev Natl Cent Health Stat Natl Vital Stat Syst 64: 1–65.Google Scholar
  14. 14.
    Priskorn L, Holmboe SA, Jacobsen R, Jensen TK, Lassen TH, Skakkebaek NE, 2012 Increasing trends in childlessness in recent birth cohorts — a registry-based study of the total Danish male population born from 1945 to 1980. Int J Androl 35: 449–455.CrossRefGoogle Scholar
  15. 15.
    Le Cornet C, Lortet-Tieulent J, Forman D, et al, 2014 Testicular cancer incidence to rise by 25% by 2025 in Europe? Model-based predictions in 40 countries using population-based registry data. Eur J Cancer 50: 831–839.CrossRefGoogle Scholar
  16. 16.
    Rolland M, Moal JL, Wagner V, Royère D, Mouzon JD, 2012 Decline in semen concentration and morphology in a sample of 26 609 men close to general population between 1989 and 2005 in France. Hum Reprod 28: 462–470.CrossRefGoogle Scholar
  17. 17.
    Romero-Otero J, Medina-Polo J, García-Gómez B, et al, 2015 Semen Quality Assessment in Fertile Men in Madrid During the Last 3 Decades. Urology 85: 1333–1338.CrossRefGoogle Scholar
  18. 18.
    Jørgensen N, Joensen UN, Jensen TK, et al, 2012 Human semen quality in the new millennium: a prospective cross-sectional population-based study of 4867 men. BMJ Open 2:e000990.CrossRefGoogle Scholar
  19. 19.
    Ramlau-Hansen CH, Thulstrup AM, Nohr EA, Bonde JP, Sørensen TIA, Olsen J, 2007 Subfecundity in overweight and obese couples. Hum Reprod 22: 1634–1637.CrossRefGoogle Scholar
  20. 20.
    Nguyen RHN, Wilcox AJ, Skjaerven R, Baird DD, 2007 Men’s body mass index and infertility. Hum Reprod Oxf Engl 22: 2488–2493.CrossRefGoogle Scholar
  21. 21.
    Sallmén M, Sandler DP, Hoppin JA, Blair A, Baird DD, 2006 Reduced fertility among overweight and obese men. Epidemiol Camb Mass 17: 520–523.CrossRefGoogle Scholar
  22. 22.
    Jensen TK, Andersson A-M, Jørgensen N, et al, 2004 Body mass index in relation to semen quality and reproductive hormonesamong 1,558 Danish men. Fertil Steril 82: 863–870.CrossRefGoogle Scholar
  23. 23.
    Sermondade N, Massin N, Boitrelle F, et al, 2012 Sperm parameters and male fertility after bariatric surgery: three case series. Reprod Biomed Online 24: 206–210.CrossRefGoogle Scholar
  24. 24.
    Colaci DS, Afeiche M, Gaskins AJ, et al, 2012 Men’s body mass index in relation to embryo quality and clinical outcomes in couples undergoing in vitro fertilization. Fertil Steril 98: 1193–9.e1.CrossRefGoogle Scholar
  25. 25.
    Moragianni VA, Jones S-ML, Ryley DA, 2012 The effect of body mass index on the outcomes of first assisted reproductive technology cycles. Fertil Steril 98: 102–108.CrossRefGoogle Scholar
  26. 26.
    Bakos HW, Henshaw RC, Mitchell M, Lane M, 2011 Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil Steril 95: 1700–1704.CrossRefGoogle Scholar
  27. 27.
    Fariello RM, Pariz JR, Spaine DM, Cedenho AP, Bertolla RP, Fraietta R, 2012 Association between obesity and alteration of sperm DNA integrity and mitochondrial activity. BJU Int 110: 863–867.CrossRefGoogle Scholar
  28. 28.
    Kort HI, Massey JB, Eisner CW, et al, 2006 Impact of Body Mass Index Values on Sperm Quantity and Quality. J Androl 27: 450–452.CrossRefGoogle Scholar
  29. 29.
    Barratt CLR, Aitken RJ, Björndahl L, et al, 2010 Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications—a position report. Hum Reprod Oxf Engl 25: 824–838.CrossRefGoogle Scholar
  30. 30.
    Zini A, Boman JM, Belzile E, Ciampi A, 2008 Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod Oxf Engl 23: 2663–2668.CrossRefGoogle Scholar
  31. 31.
    Zini A, Jamal W, Cowan L, Al-Hathal N, 2011 Is sperm DNA damage associated with IVF embryo quality? A systematic review. J Assist Reprod Genet 28: 391–397.CrossRefGoogle Scholar
  32. 32.
    Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN, 2014 Oxidative stress and male reproductive health. Asian J Androl 16: 31–38.CrossRefGoogle Scholar
  33. 33.
    Tunc O, Bakos HW, Tremellen K, 2011 Impact of body mass index on seminal oxidative stress. Andrologia 43: 121–128.CrossRefGoogle Scholar
  34. 34.
    Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M, 2012 Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod 27: 1391–1400.CrossRefGoogle Scholar
  35. 35.
    Fullston T, McPherson NO, Owens JA, Kang WX, Sandeman LY, Lane M, 2015 Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an “obesogenic” diet. Physiol Rep 3:e12336.CrossRefGoogle Scholar
  36. 36.
    Lane M, McPherson NO, Fullston T, et al, 2014 Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring. PloS One 9:e100832.CrossRefGoogle Scholar
  37. 37.
    Jääskeläinen A, Pussinen J, Nuutinen O, et al, 2011 Intergenerational transmission of overweight among Finnish adolescents and their parents: a 16-year follow-up study. Int J Obes 35: 1289–1294.CrossRefGoogle Scholar
  38. 38.
    Patro B, Liber A, Zalewski B, Poston L, Szajewska H, Koletzko B, 2013 Maternal and Paternal Body Mass Index and Offspring Obesity: A Systematic Review. Ann Nutr Metab 63: 32–41.CrossRefGoogle Scholar
  39. 39.
    Kaati G, Bygren LO, Pembrey M, Sjöström M, 2007 Transgenerational response to nutrition, early life circumstances and longevity. Eur J Hum Genet 15: 784–790.CrossRefGoogle Scholar
  40. 40.
    Anderson LM, Riffle L, Wilson R, Travlos GS, Lubomirski MS, Alvord WG, 2006 Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 22: 327–331.CrossRefGoogle Scholar
  41. 41.
    Carone BR, Fauquier L, Habib N, et al, 2010 Paternally Induced Transgenerational Environmental Reprogramming of Metabolic Gene Expression in Mammals. Cell 143: 1084–1096.CrossRefGoogle Scholar
  42. 42.
    Fullston T, Teague EMCO, Palmer NO, et al, 2013 Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J 27: 4226–4243.CrossRefGoogle Scholar
  43. 43.
    Ng S-F, Lin RCY, Laybutt DR, Barres R, Owens JA, Morris MJ, 2010 Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 467: 963–966.CrossRefGoogle Scholar
  44. 44.
    Ost A, Lempradl A, Casas E, et al, 2014 Paternal Diet Defines Offspring Chromatin State and Intergenerational Obesity. Cell 159: 1352–1364.CrossRefGoogle Scholar
  45. 45.
    Binder NK, Sheedy JR, Hannan NJ, Gardner DK, 2015 Male obesity is associated with changed spermatozoa Cox4i1 mRNA level and altered seminal vesicle fluid composition in a mouse model. Mol Hum Reprod 21: 424–434.CrossRefGoogle Scholar
  46. 46.
    Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA, 2014 Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci 111: 2200–2205.CrossRefGoogle Scholar
  47. 47.
    Crean AJ, Kopps AM, Bonduriansky R, 2014 Revisiting telegony: offspring inherit an acquired characteristic of their mother’s previous mate. Ecol Lett 17: 1545–1552.CrossRefGoogle Scholar
  48. 48.
    Curley JP, Mashoodh R, Champagne FA, 2011 Epigenetics and the origins of paternal effects. Horm Behav 59: 306–314.CrossRefGoogle Scholar
  49. 49.
    Belan M, Duval K, Jean-Denis F, et al, 2015 Impacts of Lifestyle and Anthropometric Changes in Male Partners of Obese Infertile Women on Couples’ Fertility — Preliminary Results from a Cohort Study. San Diego: 2015.Google Scholar
  50. 50.
    McPherson NO, Bakos HW, Owens JA, Setchell BP, Lane M, 2013 Improving Metabolic Health in Obese Male Mice via Diet and Exercise Restores Embryo Development and Fetal Growth. PLoS ONE 8:e71459.CrossRefGoogle Scholar
  51. 51.
    McPherson NO, Owens JA, Fullston T, Lane M, 2015 Preconception diet or exercise intervention in obese fathers normalizes sperm microRNA profile and metabolic syndrome in female offspring. Am J Physiol — Endocrinol Metab 308: E805–821.CrossRefGoogle Scholar
  52. 52.
    Reis LO, Zani EL, Saad RD, Chaim EA, de Oliveira LC, Fregonesi A, 2012 Bariatric Surgery Does not Interfere With Sperm Quality—A Preliminary Long-Term Study. Reprod Sci Thousand Oaks Calif 19: 1057–1062.CrossRefGoogle Scholar
  53. 53.
    Lazaros L, Hatzi E, Markoula S, et al, Dramatic reduction in sperm parameters following bariatric surgery: report of two cases. Andrologia 44: 428–432.Google Scholar
  54. 54.
    Håkonsen LB, Thulstrup AM, Aggerholm AS, et al, 2011 Does weight loss improve semen quality and reproductive hormones? Results from a cohort of severely obese men. Reprod Health 8: 24.CrossRefGoogle Scholar

Copyright information

© Hellenic Endocrine Society 2015

Authors and Affiliations

  1. 1.MRC Centre for Reproductive Health, Queen’s Medical Research InstituteUniversity of EdinburghEdinburghUK

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