Age-related evolution of serum biochemistry and intestinal fatty acid signaling, innate immune response, and barrier function in suckling and newly weaned piglets

J Anim Sci. 2025 Jan 4:103:skaf313. doi: 10.1093/jas/skaf313.

Abstract

It is helpful for diagnostic purposes to improve our current knowledge of gut development and serum biochemistry in young piglets. This study investigated serum biochemistry, gut site-specific patterns of short-chain fatty acids (SCFA), and expression of genes related to barrier function, innate immune response, antioxidative status, and sensing of fatty and bile acids in suckling and newly weaned piglets. The experiment consisted of two replicate batches with 10 litters each. Piglets could suckle freely and had access to creep feed from day of life (DoL) 3. Weaning occurred on DoL28. Blood, gastric, cecal, and colonic digesta, as well as jejunal and cecal tissue were collected on DoL3, 7, 14, 21, 28, 31, and 35 (n = 10/sex/DoL). Serum liver enzyme activities were high on DoL3 but decreased thereafter, reflecting the immature state of hepatocytes after birth (P < 0.05). Age-related fluctuations in serum glucose and lipids indicated changes in energy metabolism within the suckling period and lower feed intake after weaning. Short-chain fatty acids increased in cecal digesta from DoL3 to 28 (P < 0.05). After weaning, lower gastric and cecal SCFA on DoL31 and DoL35, respectively, versus DoL28 mirrored lower feed intake, whereas colonic SCFA increased after weaning (P < 0.05). Jejunal and cecal expression of free fatty acid receptors and monocarboxylate transporters changed with increasing age (P < 0.05). For some genes including FFAR2 and FFAR3 in the cecum, expression levels declined from DoL3 onwards (P < 0.05), indicating an inverse relationship with luminal SCFA availability. However, there was no unique jejunal and cecal expression pattern for fatty acid receptors and transporters, and pattern recognition receptors (PRR), probably corresponding to the age-related changes in their ligands. Increasing expression of anti-inflammatory IL10 in jejunum and cecum from DoL3 to 28 may be indicative of a build-up of immune tolerance (P < 0.05). Postweaning expression of PRR was not increased, but reduced jejunal expression of antioxidative enzymes and increased cecal expression of proinflammatory TNFA combined with lower expression of MUC2, OCLN, and ZO1 compared to the suckling phase indicated compromised gut homeostasis (P < 0.05). Overall, the present results show study-specific age-related patterns of genes associated with mucosal metabolite sensing or defense mechanisms in the jejunum and cecum from birth to after weaning.

Keywords: gene expression; piglet; postweaning phase; serum parameters; short-chain fatty acid; suckling phase.

Plain language summary

Improving the current understanding of age-related changes in serum biochemistry and gut mucosal response to luminal stimuli in the early neonatal phase is valuable to categorize whether the development is within the normal range. In the present study, we investigated gut site-specific patterns of microbial metabolites, expression of genes related to barrier function, innate immune response, antioxidative status and sensing of fatty and bile acids and serum biochemistry in suckling and newly weaned piglets from day 3 to 35 of life. Weaning occurred on day 28 of life. Results for serum liver enzyme activities indicated maturational processes during the suckling phase. Moreover, results demonstrate differential expression patterns of genes related to microbial metabolite and bile acid sensing, host recognition of microbial antigens, and barrier function in the jejunum and cecum from birth to weaning and thereafter. The age-related gene expression patterns were partially specific to this study, which emphasizes that the comparison of age-related gene expression profiles between studies may be helpful to decipher the degree of variation in the influence of microbial presence on gene transcription during the first weeks of life.

MeSH terms

  • Aging* / physiology
  • Animals
  • Animals, Suckling
  • Fatty Acids* / metabolism
  • Fatty Acids, Volatile* / metabolism
  • Female
  • Immunity, Innate* / physiology
  • Male
  • Signal Transduction
  • Swine / blood
  • Swine / immunology
  • Swine / physiology
  • Weaning

Substances

  • Fatty Acids, Volatile
  • Fatty Acids