A comparative analysis of gastrointestinal tract barrier function and immune markers in gilt vs. sow progeny at birth and weaning

J Anim Sci. 2024 Jan 3:102:skae054. doi: 10.1093/jas/skae054.

Abstract

Progeny born to primiparous sows (gilt progeny; GP) have lower birth, weaning and slaughter weights than sow progeny (SP). GP also have reduced gastrointestinal tract (GIT) development, as evidenced by lower organ weights. Therefore, the aim of this experiment was to quantify changes in GIT barrier function that occur in birth and weaning, representing two major challenges to the young piglet. The effects of parity (GP vs. SP) in GIT barrier integrity function were quantified at four timepoints: birth (~0 h), 24 h after birth (24 h), 1-d preweaning (PrW), and 1-d postweaning (PoW) in commercially reared piglets. Due to inherent differences between newborn and weanling pigs, the results were analyzed in two cohorts, birth (0 vs. 24 h, n = 31) and weaning (PrW vs. PoW, n = 40). Samples of the stomach, jejunum, ileum, and colon were excised after euthanasia and barrier integrity was quantified by measuring transepithelial resistance (TER), macromolecular permeability, the abundance of inflammatory proteins (IL-8, IL-1β, and TNF-α) and tight junction proteins (claudin-2 and -3). Papp was characterized using a dual tracer approach comprising 4 KDa fluorescein isothiocyanate (FD4) and 150 kDa tetramethyl rhodamine isothiocyanate (T150)-labeled dextrans. Characteristic effects of the initiation of feeding and weaning were observed on the GIT with the initiation of feeding, such as increasing TER and reducing Papp at 24 h, consistent with mucosal growth (P = 0.058) This was accompanied by increased cytokine abundance as evidenced by elevations in TNF-α and IL-1β. However, GP had increased IL-8 abundance (P = 0.011 and 0.063 for jejunum and ileum respectively) at birth than 24 h overall. In the weaning cohort, jejunal and ileal permeability to FD4 was higher in GP (P = 0.05 and 0.022, respectively) while only higher ileal T150 was observed in GP (P = 0.032). Ileal claudin-2 abundance tended to be higher in SP overall (P = 0.063), but GP ileal claudin-2 expression was upregulated weaning while no change was observed in SP (P = 0.043). Finally, other than a higher jejunal TNF-α abundance observed in SP (P = 0.016), no other effect of parity was observed on inflammatory markers in the weaning cohort. The results from this study indicate that the GIT of GP have poorer adaptation to early life events, with the response to weaning, being more challenging which is likely to contribute to poorer postweaning growth.

Keywords: barrier integrity; gastrointestinal tract; gilt progeny; parity; sow progeny; weaning.

Plain language summary

The progeny of primiparous sows (gilt progeny; GP) have poorer lifetime growth performance in comparison to progeny from multiparous sows (sow progeny; SP). Previous research suggests that there is an underlying biological basis for reduced growth performance which is attributed to differences in gastrointestinal tract (GIT) barrier development during early life. This study aimed to clarify the timeframes of when these differences are in effect by investigating GIT development during two major events of a piglet’s life: birth and weaning. To do this, GIT tissue was collected from GP and SP at four time points; birth, 24 h after birth, 1-d preweaning, and 1-d postweaning and assessed for functional development. The main findings from this study indicate there are early signs of variation in GIT development within the first 24 h of life between GP and SP, and that these differences increase through the preweaning period, with GP entering weaning with poorer GIT development and function. Possible explanations for the reduced GI development may be reduced maternal nutrition during the suckling period.

MeSH terms

  • Animals
  • Biomarkers
  • Claudin-2*
  • Female
  • Humans
  • Interleukin-8
  • Jejunum
  • Lactation
  • Pregnancy
  • Sus scrofa
  • Swine
  • Tumor Necrosis Factor-alpha*
  • Weaning

Substances

  • Tumor Necrosis Factor-alpha
  • Claudin-2
  • Interleukin-8
  • Biomarkers