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Changes in vaginal microbiome of beef cows enrolled in estrous synchronization protocols and its relation to fertility

Estrus synchronization (ES) is a valuable technology that can help beef cow-calf producers to overcome infertility caused by prolonged anestrus. Protocols for ES that use progesterone (P4) supplementation are of particular value to cows with prolonged postpartum anestrus as P4 triggers them to begin cycling and allows them to have fertility similar to that of cycling cows. Supplementation of P4 intravaginally with the use of a controlled internal drug release device (CIDR) improves cycle induction when compared to oral administration of P4. Vaginitis has been reported as a side effect to CIDR use in cattle, which raises concerns about its downstream effects on fertility. More specifically, the effects of CIDR use on the vaginal environment requires exploration, as no studies have explored the changes in vaginal microbiome in response to CIDR based ES protocols. In cattle, the vaginal microbiome has not been widely explored. On the contrary, the human vaginal microbiome is a well-defined environment, rich in bacteria from the genus Lactobacillus, which are responsible for promoting an environment of acidic pH. The dominance of Lactobacillus in the human vagina, however, fluctuates according to steroid hormone concentrations, and disruptions in the vaginal environment will cause depletion of Lactobacillus species, increase in vaginal pH and decreased fertility. Based on this data in humans, our objectives were to describe incidence of vaginitis caused by the CIDR in beef cows, as well as the vaginal microbiome changes in response to CIDR based protocols, and explore their relation to fertility. We found high incidences of vaginitis caused by CIDR use, yet CIDR-induced vaginitis did not negatively affect pregnancy outcomes. However, at CIDR withdrawal, there was decreased bacterial diversity, increased vaginal pH, increased bacterial abundance, and increased vaginal inflammation when compared to what was observed prior to CIDR insertion. Furthermore, abundance of bacteria, vaginal inflammation, and bacterial diversity, but not vaginal pH, were restored to normal values by the day of timed artificial insemination. This important finding suggests that although the vaginal microbiome was disrupted by the use of CIDR, the vaginal microbiome is resilient and capable of restoring its natural conditions without intervention. Finally, cows that ultimately became pregnant were found to have had increased bacterial diversity and decreased vaginal pH prior to protocol initiation, suggesting that the vaginal microbiome may play a role in individual cow fertility. In conclusion, our results indicate that for beef cows a more diverse vaginal microbiome with decreased vaginal pH presents greater resilience of the microbiome towards disruptions caused by an ES protocol, which is translated in greater pregnancy success. / Doctor of Philosophy / According to the Food and Agriculture Organization, the world population is expected to grow by 51% by the year of 2100. The efficiency of food production must therefore be optimized, given the finite availability of farmable land. In beef production, cow fertility is of great importance, since it will ultimately determine the number of animals available for slaughter. The main reproductive issue that cow-calf producers face is that after calving, cows will undergo a period known as postpartum anestrus, in which cows fail to ovulate. Artificial insemination (AI) can help to optimize beef production efficiency, since it allows for the dispersal of semen from valuable bulls to facilitate the genetic enhancement of herds. The use of estrus synchronization (ES) protocols allows for induction and synchronization of ovulation, which allows AI to be performed at the same time for large groups of cows. Progesterone is often used in ES protocols and is the hormone responsible for inducing cyclicity in postpartum cows. Progesterone can be administered either orally or intravaginally via the use of a controlled internal drug release (CIDR). While the CIDR seems to be more effective at inducing cyclicity of cattle compared to oral progesterone administration, vaginal inflammation as response to the CIDR has been reported in cattle. Little is known about the downstream effects of this inflammation on the normal vaginal microbiota and fertility in cattle. In humans, the vaginal microbiome is predominated by a single genus of bacteria (Lactobacillus), that has an essential role in producing lactic acid, which results in the human vagina being remarkably acidic. In humans, depletion of this bacteria, a condition called bacterial vaginosis (BV), allows for other types of bacteria to grow, which results in an increased vaginal pH and decreased fertility. The bovine vaginal microbiome composition and pH in response to the hormones administered during ES protocols and its relation to fertility have not been widely explored. Our objectives were to document the incidence of vaginitis caused by the CIDR in beef cows and evaluate its effects on the vaginal microbiome changes and fertility. We found high incidences of vaginitis caused by the CIDR, yet no effects of CIDR-induced vaginitis were seen on pregnancy success to the protocol. However, decreased bacterial diversity, followed by increases in vaginal pH, abundance of bacteria and vaginal inflammation are all detected at CIDR withdrawal when compared to before CIDR insertion. Furthermore, abundance of bacteria, vaginal inflammation, and bacterial diversity, but not vaginal pH, were restored to normal values by the day of timed AI, indicating that although the vaginal microbiome was disrupted using CIDR, the vaginal microbiome can restore to natural conditions, and indicate resilience of the vaginal microbiome. Finally, cows that became pregnant to the protocol presented increased bacterial diversity and decreased vaginal pH prior to the protocol. In conclusion, our results indicate that for beef cows a more diverse vaginal microbiome with decreased vaginal pH presents greater resilience of the microbiome towards disruptions caused by an ES protocol, which is translated in greater pregnancy success.

Identiferoai:union.ndltd.org:VTETD/oai:vtechworks.lib.vt.edu:10919/113248
Date18 January 2023
CreatorsWege Dias, Nicholas
ContributorsAnimal and Poultry Sciences, Mercadante, Vitor Rodriques Gomes, Biase, Fernando H., Ealy, Alan Dale, Stewart, Jamie L., Currin, John Franklin
PublisherVirginia Tech
Source SetsVirginia Tech Theses and Dissertation
LanguageEnglish
Detected LanguageEnglish
TypeDissertation
FormatETD, application/pdf
RightsCreative Commons Attribution-NonCommercial 4.0 International, http://creativecommons.org/licenses/by-nc/4.0/

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