Postnatal development of gut microbial activity and their importance for jejunal motility in piglets

Abstract

Despite their anti-inflammatory properties, role in barrier function, absorption and microbial balance in the gut, knowledge on maturational and dietary effects on intestinal short-chain fatty acids (SCFA) in neonatal piglets is scarce. Moreover, little information exists whether SCFA and lactic acid (LA) modulates gut motility at this age. The present study aimed 1) to investigate the maturational changes in the SCFA profile with and without creep feeding of piglets in the first 3 weeks of life; and 2) to examine the effects of SCFA and LA on muscle contractibility in jejunal tissue from neonatal piglets ex vivo. SCFA concentrations were measured in fecal samples of 52 piglets from 10 litters collected on days 2, 6, 13, and 20 of life using gas chromatography. Half of the litters were fed a commercial creep feed from day 10 of life. The organ bath system was used to test the effect of SCFA (acetate, propionate, butyrate, isobutyrate, valerate, isovalerate and caproate) as well as of LA and the combination of LA and SCFA on muscle contractibility in piglet’s jejunum. Average daily gain of piglets was similar between groups before and after introduction of creep feed. SCFA were detectable in feces in relevant concentrations from day 2 of life and increased on day 6 in males by 3.0-fold and on day 13 in females by 1.6-fold but decreased again on day 20 in both sexes compared to day 2 (P < 0.05). Creep feeding reduced fecal SCFA by 0.6-fold on day 13 without largely modifying molar proportions, whereas it increased fecal SCFA by 0.8-fold on day 20 of life compared to the sow-reared only piglets (P < 0.05). Applying SCFA ex vivo increased the muscle contraction of the jejunum by 30% (P < 0.05). Likewise, addition of LA and the combination of LA and SCFA increased the jejunal muscle contractibility by 34.9 and 32.2%, respectively, compared to the muscle tension pre-addition (P < 0.05). In conclusion, the present results for fecal SCFA in first days of life suggest high bacterial activity on milk components and emphasize the importance of SCFA for intestinal development and function. After a lag phase, creep feeding promotes fermentation in the distal colon, which may be beneficial for the gut homeostasis. Results further demonstrate the stimulating effect of SCFA and LA for jejunal motility, suggesting a role for mixing of digesta (segmentation) and digestion and absorption of nutrients as well as passage in the jejunum of neonatal piglets.

The Role of Dietary and Microbial Fatty Acids in the Control of Inflammation in Neonatal Piglets

“…The SCFA profiles and amounts fluctuate postnatally, mirroring maturational changes in microbial species abundances [65,84,85]. To illustrate this, SCFAs increased from day 2 to 13 of life, while their concentration decreased again until day 20 [66].…”

“…For instance, coconut oil is rich in saturated lauric acid (C12:0, 49%) and contains in total about 82% saturated FAs, whereas palm oil comprises about 50% saturated FAs, 40% monounsaturated FAs and 10% PUFAs [65]. The introduction of creep feed has an effect on microbial activity, first suppressing fermentation in the hindgut but later stimulating the SCFA production when the microbes have adapted to the plant-based starchy components [66]. This can be assumed to be beneficial for the gut homeostasis.…”

“…While there has been substantial research interest on these microbial lipid derivatives in ruminants, in pigs the focus has been on the benefits of SCFAs on gut and systemic inflammation and health. Most evidence for intestinal SCFA production in piglets exists from the fourth week of life onwards [82,83], while only recent research has started to have a closer look into the neonatal phase [66,84]. Accumulating research data show that physiologically relevant concentrations of SCFA exist in the ileum, cecum and colon from the first days of life and rise until weaning [66,85].…”

“…Most evidence for intestinal SCFA production in piglets exists from the fourth week of life onwards [82,83], while only recent research has started to have a closer look into the neonatal phase [66,84]. Accumulating research data show that physiologically relevant concentrations of SCFA exist in the ileum, cecum and colon from the first days of life and rise until weaning [66,85]. Already the meconium comprises small amounts of SCFAs, which may play an important role for host mucosal nutrition and priming in neonatal piglets [86,87].…”

Short-Chain Fatty Acids Modulate Permeability, Motility and Gene Expression in the Porcine Fetal Jejunum Ex Vivo

“…Postnatally, SCFA, such as acetate, propionate, butyrate, isobutyrate, valerate, isovalerate and caproate, are recognized as important energetic and signaling agents. They are involved in host nutrition, imprinting of the immune system, cell metabolism, barrier function and intestinal motility [9][10][11]. However, their mechanistic action on the host can differ depending on the type of SCFA and molar proportions in which the SCFA occur.…”