Revisiting summer infertility in the pig: could heat stress-induced sperm DNA damage negatively affect early embryo development?

Abstract

Abstract.Temperature is a crucial factor in mammalian spermatogenesis. The scrotum, pampiniform plexus, and cremaster and dartos muscles in mammals are specific adaptations to ensure sperm production in a regulated environment 4À6 C below internal body temperature. However, the limited endogenous antioxidant systems inherent in mammalian spermatozoa compounded by the loss of cytosolic repair mechanisms during spermatogenesis, make the DNA in these cells particularly vulnerable to oxidative damage. Boar sperm is likely to be more susceptible to the effects of heat stress and thus oxidative damage due to the relatively high unsaturated fatty acids in the plasma membrane, low antioxidant capacity in boar seminal plasma, and the boar's non-pendulous scrotum. Heat stress has a significant negative impact on reproductive performance in piggeries, which manifests as summer infertility and results in productivity losses that amount to millions of dollars. This problem is particularly prevalent in tropical and subtropical regions where ambient temperatures rise beyond the animal's zone of thermal comfort. Based on preliminary studies in the pig and other species, this article discusses whether heat stress could induce sufficient DNA damage in boar sperm to significantly contribute to the high rates of embryo loss and pregnancy failure observed in the sow during summer infertility. Heat stress-induced damage to sperm DNA can lead to disrupted expression of key developmental genes essential for the differentiation of early cell lineages, such as the trophectoderm, and can distort the timely formation of the blastocyst; resulting in a failure of implantation and ultimately pregnancy loss. Confirming such a link would prompt greater emphasis on boar management and strategies to mitigate summer infertility during periods of heat stress.

Tropical summer induces DNA fragmentation in boar spermatozoa: implications for evaluating seasonal infertility

“…Heat stress induced by scrotal immersion in 428C water for 20 min also causes dissociation in X-Y chromosomes of mice and rats, leading to chromosomally unbalanced gametes, even in heat-adapted animals (van Zelst et al 1995). We postulate that the above mechanisms may play a significant role in inducing DNA damage in boar spermatozoa during periods of heat stress (Peña et al 2017).…”

“…Of concern is the fact that the high rates of sperm DNA fragmentation observed during the peak wet season in our study (without noticeable effect on sperm motility) may currently go undetected by pig industries in tropical and subtropical climates. Moreover, they could significantly contribute to the high rates of embryo loss and pregnancy failure observed in sows during summer infertility (Peña et al 2017). Didion et al (2009) reported that a sperm sample with greater than 6% DNA fragmentation could result in decreased farrowing rates and average number of piglets born.…”

“…Moreover, the relatively high levels of unsaturated fatty acids in the plasma membrane (Cerolini et al 2001) and low antioxidant activity of seminal plasma (Brzezińska-Ś lebodzińska et al 1995) all contribute to the high sensitivity of boar spermatozoa to peroxidative damage. We have recently proposed that such mechanisms may make boar spermatozoa highly prone to DNA damage during periods of heat stress (Peña et al 2017). Recent studies in mice have conclusively demonstrated that heat stress induces sperm DNA damage, which causes abnormal and arrested embryo development and ultimately embryo and fetal loss (Paul et al 2008).…”

“…Recent studies in mice have conclusively demonstrated that heat stress induces sperm DNA damage, which causes abnormal and arrested embryo development and ultimately embryo and fetal loss (Paul et al 2008). This suggests that heat stress-induced DNA damage in boar spermatozoa may contribute significantly to seasonal pregnancy failure and reduced litter size in sows (Peña et al 2017). In pigs, Didion et al (2009) have proposed that spermatozoa with greater than 6% DNA fragmentation can cause both decreased farrowing rates and average number of piglets born.…”

Effect of Supplementation with Trimethylglycine (Betaine) and/or Vitamins on Semen Quality, Fertility, Antioxidant Status, DNA Repair and Welfare of Roosters Exposed to Chronic Heat Stress

“…In addition, HS can have negative effects on testosterone, causing hypertrophy and weakening of Leydig cell function [55]. The sperm’s damaged DNA can determine abnormal spermatozoa, which could cause low male fertility and subsequently fewer surviving embryos [4,56,57]. Even if the sperm can fertilize eggs normally, embryos that have received an injured paternal genome could die, causing poor performance [58].…”