Biomarkers predictive of long-term fertility found in vaginal lipidome of gilts at weaning

Abstract

A marker indicative of fertility potential of replacement gilts early in development would decrease culling rates in the sow herd, improve sow herd reproductive efficiency, and reduce production costs. The objective of this study was to determine if vaginal lipid profiles at 21 d postnatal (PN) could predict sow reproductive performance. Vaginal swabs of the anterior vagina were taken at 21 ± 4 d PN from gilts born on a commercial sow production facility for lipidomic analysis. Animals were followed prospectively for two years and assigned to reproductive performance categories based on observation of estrus or piglets weaned per sow per year (PSY) across two farrowings. Lipids were extracted from cellular material collected with swabs taken from high fertility (HF; n=28; ≥26 PSY) and infertile (IF; n=34; no estrus, no pregnancy) animals and multiple reaction monitoring (MRM)-profiling was used for lipidome analysis. Relative abundance of arachidonic acid (ARA, C20:4) and docosahexaenoic acid (DHA, C22:6) were lower (P<0.05) in IF gilts than HF gilts, whereas abundance of the free fatty acids cerotic (C26:0), ximenic (C26:1), and nonadecanoic (C19:0) acids were greater (P<0.05) in IF gilts. Additionally, eicosapentaenoic acid (C20:5) a precursor of prostaglandins was higher (P<0.05) in IF gilts. The perspective of having a panel of lipids captured with vaginal swabs at weaning that can predict reproductive efficiency of gilts shows promise and warrants future research in this area.

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

“…Thus, the morphology and developmental changes of the vagina in the first weeks postnatal reflect and preserve the history of exposures and metabolic reactions in a manner analogous to hair growth and temporal study of the bioaccumulation of substances in hair. This is significant, as it connects our previous findings of a longitudinal observational study of commercial replacement gilts that found vaginal lipidome at weaning differentiated between the most fertile animals, which went on to produce at least 26 piglets per year, from infertile gilts ( Mills et al, 2021 ).…”

“…The rapid screening of lipids by mass spectrometry was performed using the multiple reaction monitoring (MRM) profiling method on lipids previously identified as differentiating for colostrum versus formula feeding (method 1-M1 and 2-M2; Harlow et al, 2019a ) and fertility outcome ( Mills et al, 2021 ), including free fatty acids (FFA). Another distinct analysis of phosphatidylcholine and sphingomyelin classes (PCSM) of lipids was also run.…”

“…Lipids found in greater abundance in animals with high IM or high 24 h gain were the free fatty acids arachidonic acid (C20:4) and dihomo-γ-linolenic acid (C20:3). C20:4 was identified as a potential marker of colostrum intake in our previous work ( Casey et al, 2018a ), and more abundant in vaginal lipids of gilts that became highly fertile production sows versus infertile animals ( Mills et al, 2021 ). Although ROC analysis found that C20:4 alone was only a fair biomarker to distinguish between animals with high and low IM, when it was combined with C22:0, which was more abundant in low IM, the sensitivity and specificity increased so combined the pair scored as excellent biomarkers.…”

“…De novo discovery and screening analysis of phosphate and sphingomyelin lipids (PCSM profiles) also identified PC40:7 as a differentiating lipid between IM high and low groups and AUC score from ROC analysis indicated it as a fair biomarker (AUC=0.74). PC40:7 was previously identified as a lipid that in vaginal swabs of gilts taken at weaning was more abundant in animals found to be infertile versus highly fertile production sows ( Mills et al, 2021 ). Similarly, the PC lipid with long-very long chain fatty acids and a high number of unsaturated binds PC40:8 was found to differentiate between high and low 24 h gain in the PCSM profiling method, being relatively more abundant in the low group.…”

“…We then investigated if there was a relationship between the vaginal lipidome on PN d21 and long-term fertility in a longitudinal study. A similar set of lipids distinguished between gilts that were formula fed versus colostrum fed on PN d2 and those sampled on PN d21 and distinguished between animals found to be infertile versus highly fertile production sows ( Mills et al, 2021 ). The overall aim of the study described here was to determine if the level of colostrum intake of gilts raised within their litters was reflected in their vaginal lipidome at weaning.…”