Paternal Diet and Obesity: Effects on Reproduction

Abstract

Although most research has focused on maternal obesity, there is growing data to indicate that obesity in the father can affect reproduction. Supporting data come from both mouse and human studies. Murine studies found that obese male mice exhibited decreased motility and reduced hyperactivated progression versus lean mice. Obese mice also exhibited sperm with increased levels of intracellular and mitochondrial levels of reactive oxygen species, increased sperm damage, and lower levels of capacitation, which has been shown to be associated with poor fertilization rates following in vitro fertilization, defective preimplantation embryonic development, and high rates of miscarriage and morbidity in the offspring. Furthermore, diet-induced paternal obesity was found to initiate intergenerational transmission of obesity and insulin resistance in two generations of murine offspring. Meta-analysis from human studies found obese males were more likely to demonstrate sperm DNA fragmentation, infertility, decreased live birth per cycle of assisted reproduction technology, and increased absolute risk of pregnancy nonviability, with no consistent effect on conventional semen parameters. There is a need for future studies to expound on the mechanisms of sperm DNA damage and the impact of weight loss in reversing this damage.

Keywords

obesity - infertility - reproduction - DNA fragmentation - sperm damage - systematic review - meta-analysis - andrology

• References

• 1 World Health Organization. Diet, nutrition and the prevention of chronic diseases. Available at: http://www.who.int/dietphysicalactivity/publications/trs916/en/ . Accessed February 2017
• 2 Bakos HW, Mitchell M, Setchell BP, Lane M. The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int J Androl 2011; 34 (5, Pt 1): 402-410
• 3 Ghanayem BI, Bai R, Kissling GE, Travlos G, Hoffler U. Diet-induced obesity in male mice is associated with reduced fertility and Potentiation of Acrylamide-Induced reproductive toxicity1. 2009 ;82(1). Available at https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2802115/ . Accessed February 2017
• 4 Chavarro JE, Toth TL, Wright DL, Meeker JD, Hauser R. Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil Steril 2010; 93 (07) 2222-2231
• 5 Fariello RM, Pariz JR, Spaine DM, Cedenho AP, Bertolla RP, Fraietta R. Association between obesity and alteration of sperm DNA integrity and mitochondrial activity. BJU Int 2012; 110 (06) 863-867
• 6 Hammiche F, Laven JS, Twigt JM, Boellaard WP, Steegers EA, Steegers-Theunissen RP. Body mass index and central adiposity are associated with sperm quality in men of subfertile couples. Hum Reprod 2012; 27 (08) 2365-2372
• 7 Hammoud A, Wilde N, Gibson M, Parks A, Carrell D, Meikle A. Male obesity and alteration in sperm parameters. Fertil Steril 2008; 90 (06) 2222-2225
• 8 Koloszár S, Fejes I, Závaczki Z, Daru J, Szöllosi J, Pál A. Effect of body weight on sperm concentration in normozoospermic males. Arch Androl 2005; 51 (04) 299-304
• 9 Evenson DP, Jost LK, Marshall D. , et al. Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod 1999; 14 (04) 1039-1049
• 10 Guzick DS, Overstreet JW, Factor-Litvak P. , et al; National Cooperative Reproductive Medicine Network. Sperm morphology, motility, and concentration in fertile and infertile men. N Engl J Med 2001; 345 (19) 1388-1393
• 11 Kodama H, Yamaguchi R, Fukuda J, Kasai H, Tanaka T. Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients. Fertil Steril 1997; 68 (03) 519-524
• 12 Spanò M, Bonde JP, Hjøllund HI, Kolstad HA, Cordelli E, Leter G. Sperm chromatin damage impairs human fertility. The Danish First pregnancy planner study team. Fertil Steril 2000; 73 (01) 43-50
• 13 Zini A, Bielecki R, Phang D, Zenzes MT. Correlations between two markers of sperm DNA integrity, DNA denaturation and DNA fragmentation, in fertile and infertile men. Fertil Steril 2001; 75 (04) 674-677
• 14 Zini A, Kamal K, Phang D, Willis J, Jarvi K. Biologic variability of sperm DNA denaturation in infertile men. Urology 2001; 58 (02) 258-261
• 15 Barroso G, Morshedi M, Oehninger S. Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa. Hum Reprod 2000; 15 (06) 1338-1344
• 16 Twigg J, Irvine DS, Houston P, Fulton N, Michael L, Aitken RJ. Iatrogenic DNA damage induced in human spermatozoa during sperm preparation: protective significance of seminal plasma. Mol Hum Reprod 1998; 4 (05) 439-445
• 17 Lamirande E, Gagnon C. The dark and bright sides of reactive oxygen species on sperm function. In: Gagnon C. , ed. The Male Gamete: From Basic Science to Clinical Applications. Vienna, IL: Cache River Press; 1999: 455-467
• 18 Aitken RJ, Krausz C. Oxidative stress, DNA damage and the Y chromosome. Reproduction 2001; 122 (04) 497-506
• 19 Bennetts LE, Aitken RJ. A comparative study of oxidative DNA damage in mammalian spermatozoa. Mol Reprod Dev 2005; 71 (01) 77-87
• 20 Binder NK, Mitchell M, Gardner DK. Parental diet-induced obesity leads to retarded early mouse embryo development and altered carbohydrate utilisation by the blastocyst. Reprod Fertil Dev 2012; 24 (06) 804-812
• 21 Binder NK, Hannan NJ, Gardner DK. Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One 2012; 7 (12) e52304
• 22 Mitchell M, Bakos HW, Lane M. Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil Steril 2011; 95 (04) 1349-1353
• 23 Ansell JD, Snow MH. The development of trophoblast in vitro from blastocysts containing varying amounts of inner cell mass. J Embryol Exp Morphol 1975; 33 (01) 177-185
• 24 Fullston T, Ohlsson Teague EM, Palmer NO. , et al. 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 2013; 27 (10) 4226-4243
• 25 El Hajj N, Zechner U, Schneider E. , et al. Methylation status of imprinted genes and repetitive elements in sperm DNA from infertile males. Sex Dev 2011; 5 (02) 60-69
• 26 Tunc O, Tremellen K. Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet 2009; 26 (9–10): 537-544
• 27 MacDonald AA, Herbison 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 2010; 16 (03) 293-311
• 28 Campbell JM, Lane M, Owens JA, Bakos HW. Paternal obesity negatively affects male fertility and assisted reproduction outcomes: a systematic review and meta-analysis. Reprod Biomed Online 2015; 31 (05) 593-604
• 29 Faure C, Dupont C, Baraibar MA. , et al. In Subfertile couple, abdominal fat loss in men is associated with improvement of sperm quality and pregnancy: a case-series. PLoS One 2014; 9 (02) e86300