Revisiting summer infertility in the boar: impact of heat stress on the quality and DNA integrity of spermatozoa, and its mitigation by antioxidant therapy
Peña Jr., Santiago T. (2018) Revisiting summer infertility in the boar: impact of heat stress on the quality and DNA integrity of spermatozoa, and its mitigation by antioxidant therapy. PhD thesis, James Cook University.
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Abstract
Summer infertility in the pig continues to affect both productivity and profitability among pig producers in tropical and subtropical regions, with losses due to heat stress amounting to at least $300 million per year in the US swine industry alone. Given the wide scale production of pork globally, with at least five tropical countries among the top producers in the world, there is a need to revisit the problem of summer infertility in the pig and identify putative boar factors likely to contribute to poor reproductive performance during periods of heat stress. An important endpoint with this approach is to improve boar management practices and develop strategies to mitigate summer infertility in the pig.
While the scrotum, pampiniform plexus, and cremaster and dartos muscles in mammals are specific adaptations to ensure sperm production in a regulated environment 4-6 °C below body temperature, the boar's inefficient capacity to sweat, non-pendulous scrotum, and low antioxidant activity in the semen, can make the it particularly vulnerable to the effects of heat stress. In Chapter 2, we demonstrated for the first time the link between summer heat stress and sperm DNA damage in Large White boars. Boars raised in the dry tropics of Townsville, Queensland, Australia during summer (peak wet) showed 16-fold more sperm DNA damage than early dry (cool and dry), and nearly 9-fold more than the late dry (warm and humid) season, respectively. Sperm concentration also decreased significantly in the peak wet. Sperm DNA damage has been previously demonstrated to contribute to early embryonic death in the mouse, and this magnitude of fragmentation is known to cause a reduction in litter size in sows. These findings provide impetus for the evaluation of sperm DNA integrity in commercial boar herds housed in the tropics as a putative contributing factor to seasonal infertility in the sow.
While cryopreservation of boar spermatozoa is not widely practiced in commercial pig production, mostly due to reduced viability and fertilising capacity of post-thawed spermatozoa, it has a greater potential in advancing studies related to seasonal effects of heat stress on boar sperm fertility using in vitro fertilisation. Since the freeze-thaw process can led to increased sperm DNA damage and subsequently contribute to early embryo loss, in Chapter 3 we tried to address the limited information about the protective effects of the more common cryoprotectant glycerol on sperm DNA integrity during boar sperm cryopreservation. We aimed to determine the optimal concentration of glycerol to protect sperm DNA integrity, without the deleterious effect of high concentrations negatively affecting sperm motility. We deemed this work particularly important to permit us to freeze boar sperm collected during summer, for downstream use to fertilise eggs in vitro during winter when oocyte quality is high. Our study revealed that 3%, 6% or 8% glycerol could be safely used to cryopreserve boar spermatozoa without inducing additional DNA damage compared to fresh spermatozoa. We deemed a concentration of 6% glycerol provided the best DNA protection, while maintaining sufficient levels of sperm motility.
In chapter 4, we aimed to develop reliable heat stress models that could be used at any time of the year, to advance the study of seasonal infertility in the pig by overcoming the variation and limitations associated with seasonal studies. We have successfully induced biologically meaningful levels of DNA damage in boar spermatozoa using either a whole animal in vivo model (hot room) or by direct exposure of semen to heat in vitro (heat shock model). However, we were only able to induce levels of damage observed during natural tropical summer (Chapter 2) using extreme in vitro temperatures that rendered boar spermatozoa completely immotile or dead. Here, our results suggest that boar sperm is vulnerable to heat-induced DNA damage, but individual factors may also contribute to a boar's overall susceptibility to heat stress.
Given the limited endogenous levels of antioxidants in boar semen and the insufficient DNA repair mechanisms these cells have, Chapter 5 aimed to formulate and evaluate antioxidant therapy as a strategy to mitigate the effect of heat stress on boar sperm DNA integrity. We proposed that an exogenous multi-compound antioxidant supplementation could effectively combat heat stress induced oxidative damage and prevent the build-up of DNA fragmentation in boar spermatozoa. Supplementing boar diets with 100 g/day custom-mixed antioxidant during summer effectively reduced sperm DNA damage by as much as 55% after 42 and 84 days treatment, respectively. This implies that antioxidant supplementation during tropical summer could provide a measurable solution to the problem of boar-mediated summer infertility in the pig.
Overall, boar sperm DNA integrity can be compromised during tropical summer and this can be induced experimentally using our in vivo or in vitro heat stress models; with response particularly affected by individual boar variability. Exogenous antioxidant supplementation in feed could provide an effective means to mitigate the problem of summer infertility. Apparently, neither seasonal heat stress or heat stress models negatively affected sperm motility, suggesting that traditional evaluation of sperm motility in boars may not detect inherently compromised DNA damage spermatozoa. Antioxidant supplementation only appears to mitigate DNA damage since it did not improve sperm motility or concentration after 42 or 84 days treatment. Future studies are needed to measure the beneficial impact of antioxidant supplementation under tropical farm conditions, in terms of improved sperm DNA integrity and increased litter size following artificial insemination.
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