Low colostrum intake results in accumulation of peroxisome lipid substrates in stratified epithelial vaginal tissue of 3 week old gilts

Authors: Mills, Kayla; SHEETS, JOCELYN - Purdue University; TEEPLE, KELSEY - Purdue University; MANN, ADRIANNA - Purdue University; SUAREZ-TRUJILLO, ARIDANY - Purdue University; STEWART, KARA - Purdue University; FERREIRA, CHRISTINA - Purdue University; CASEY, THERESA - Purdue University

Submitted to: Biology Open
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/10/2023
Publication Date: 8/11/2023
Citation: Mills, K.M., Sheets, J., Teeple, K., Mann, A., Suarez-Trujillo, A., Stewart, K., Ferreira, C., Casey, T. 2023. Low colostrum intake results in accumulation of peroxisome lipid substrates in stratified epithelial vaginal tissue of 3 week old gilts. Biology Open. https://doi.org/10.1242/bio.060044.
DOI: https://doi.org/10.1242/bio.060044

Interpretive Summary: Colostrum is the first milk available to newborns and is a concentrated source of nutrients, essential fatty acids, and other important factors essential for proper development. It has also been documented that the level of colostrum intake is related to long-term success within the swine breeding herd. Thus, identifying a way to detect young female swine (gilts) that drink adequate amounts of colostrum would help in the selection of breeding herd replacements. In our previous work, the vaginal lipidome (cellular fat composition) of gilts on day 2 of life was reflective of colostrum consumption and the vaginal lipidome in gilts at weaning (21 days of age) were related to long-term fertility. Our aim was to determine if differences in vaginal lipidome profiles of gilts at weaning were reflective of variation in colostrum intake. Here, we evaluated traditional markers of colostrum intake (immunocrit ratio and 24 hour weight gain) and their relationship to vaginal lipidome profiles of gilts at weaning. Gilts that had high versus low immunocrit ratios and 24 hour weight gain showed a difference in vaginal lipid profiles and these lipids may serve as excellent biomarkers of colostrum intake. We also observed that gilts with low colostrum intake shared a similar lipid profile to the infertile gilts identified in our previous study. Therefore, colostrum intake of gilts during the first 24 hours of life is crucial to their longevity within the sow herd, and thus warrants future research in the proper management colostrum intake during the first 24 hours of life.

Technical Abstract: Colostrum is the first milk available to neonates and is a concentrated source of nutrients, essential fatty acids, and other bioactive factors. The level of colostrum intake affects body composition and fertility of swine at maturity. Using multiple reaction monitoring (MRM) profiling we found lipids isolated from vaginal cytology swabs at the time of weaning were related to gilt’s long-term fertility. We hypothesized that differences in vaginal lipidome profiles of gilts at 21 d were due to variation in colostrum intake. The immunocrit ratio (IM) and weight gain over the first 24 h postnatal (PN) are indicators of level of colostrum intake and we investigated their relationship to relative abundance of lipids extracted from vaginal swabs taken at weaning. Gilts (n=60) were weighed at birth and 24 h PN and blood sampled to measure IM. On d21 PN vaginal swabs were taken from surviving gilts (n=53). Lipids were extracted from swabs using the Bligh-Dyer method and measured using MRM profiling. Relative abundance was calculated and MetaboAnalyst 5.0 was used for statistical analysis and receiver operator curve (ROC) analysis. Abundance of multiple lipids differed (P<0.05) between gilts categorized as high versus low IM and high versus low 24 h gain. Linear regression analysis found abundance of multiple lipids correlated with IM and 24 h gain. Phosphatidylcholine (PC) (36:3), PC(36:2),and arachidonic acid positively (P<0.05) correlated with IM. PCo(38:6) and multiple cholesterol esters negatively (P<0.05) correlated with IM. ROC analysis indicated combined arachidonic acid and docosanoic acid (C22:0) may serve as excellent biomarkers (AUC=0.95) that distinguish between high and low IM. The stratified histomorphology of the vaginal cells preserves the history of metabolic processes responsive to nutritional environment in the early postnatal period. Similar to gilts found to be infertile, lipid profiles of low colostrum intake animals had greater abundance of very long chain fatty acids, lipids with high levels of unsaturation, and cholesterol esters, which are metabolized in peroxisomes indicating their potential dysfunction.