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Early life administration of milk fat globule membrane promoted SCFA-producing bacteria colonization, intestinal barriers and growth performance of neonatal piglets.

ABSTRACT: Milk fat globule membrane (MFGM) possesses various nutritional and biological benefits for mammals, whereas its effects on neonatal gut microbiota and barrier integrity remained unclear. This study investigated the effects of MFGM administration on microbial compositions and intestinal barrier functions of neonatal piglets. Sixteen newborn piglets were randomly allocated into a CON group or MFGM group, orally administered with saline or MFGM solution (1 g/kg body weight) respectively during the first postnatal week, and all piglets were breastfed during the whole neonatal period. The present study found that the MFGM oral administration during the first postnatal week increased the plasma immunoglobulin (Ig) G level, body weight and average daily gain of piglets (P < 0.05) on 21 d. Additionally, MFGM administration enriched fecal SCFA-producing bacteria (Ruminococ aceae_UCG-002, Ruminococ aceae_UCG-010, Ruminococ aceae_UCG-004, Ruminococ aceae_UCG-014 and [Ruminococcus]_gauvrearuii_group), SCFA concentrations (acetate, propionate and butyrate; P < 0.05) and their receptor (G-protein coupled receptor 41, GPR41). Furthermore, MFGM administration promoted intestinal villus morphology (P < 0.05) and barrier functions by upregulating genes of tight junctions (E-cadherin, claudin-1, occludin and zonula occludin 1 [ZO-1]), mucins (mucin-13 and mucin-20) and interleukin (IL)-22 (P < 0.05). Positive correlation was found between the beneficial microbes and SCFA levels pairwise with the intestinal barrier genes (P < 0.05). In conclusion, orally administrating MFGM during the first postnatal week stimulated SCFA-producing bacteria colonization and SCFA generation, enhanced intestinal barrier functions and consequently improved growth performance of neonatal piglets on 21 d. Our findings will provide new insights about MFGM intervention for microbial colonization and intestinal development of neonates during their early life.

SUBMITTER: Wu Y

PROVIDER: S-EPMC8245794 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Milk fat globule membrane (MFGM), mainly comprising protein and fat, has been reported to have multiple biological functions for relieving intestinal inflammation and enhancing growth performance. We hypothesized that MFGM supplementation into sows' diet during late gestation can have a positive impact on the intestinal microecology of sows and their piglets, as well as on the growth of neonates. Therefore, the present study was conducted to investigate such effects and their potential mechanisms. Twenty-two pregnant sows were selected and randomly divided into the CON group (basal diet) and MFGM group (basal diet supplemented with 9.9 g per day MFGM). The feeding period began from d 85 of gestation and until farrowing. The concentrations of albumin (ALB), low-density lipoprotein cholesterol (LDL-C), and non-esterified fatty acids (NEFA) in plasma and short-chain fatty acids (SCFAs) in feces of sows from the MFGM group were determined. The concentrations of growth hormone (GH), immunoglobulin A (IgA), glucose (GLU), and NEFA in the umbilical cord blood in the MFGM group were significantly higher than those in the CON group. Piglets from the MFGM group showed improved growth performance, increased villus height in the jejunum, decreased crypt depth in the duodenum and jejunum, upregulated mRNA expressions of tight junctions (namely, Occludin; Claudin-1, Claudin-2, and Claudin-4; zonulin-1 (ZO-1)); mucins such as Mucin 2, Mucin 4, Mucin 13, and Mucin 20; and immune-related genes, such as tumor necrosis factor-α (TNF-α), interferon-γ (INF-γ), interleukin-22 (IL-22), toll-like receptor 2 (TLR2), and toll-like receptor 4 (TLR4). In addition, the abundance of Prevotella in the feces of sows at farrowing and the abundance of Christensenellaceae_R-7_group in the feces of 21 day-old piglets from the MFGM group were significantly higher. Further correlation analysis revealed that the Christensenellaceae_R-7_group was positively correlated with the relative mRNA expressions of Occludin, Claudin-1, Claudin-2, Claudin-4, Mucin 13, TLR2, and TLR4. In conclusion, MFGM supplementation during late gestation improved the physiological status of sows by improving their plasma parameters and intestinal microecology. The improved provision of nutrients through the umbilical cord blood and optimized microbiota colonization in neonatal piglets were beneficial to the intestinal morphological structure and barrier functions, consequently improving the growth performance of neonates during lactation. These findings provide insights into the future applications of MFGM with regard to maternal-fetal nutrition and a new option for nutritional intervention of neonates through maternal dietary manipulation.

Project description:Background:The benefits of breastfeeding infants are well characterized, including those on the immune system. However, determining the mechanism by which human breast milk (HBM) elicits effects on immune response requires investigation in an appropriate animal model. Objective:The primary aim of this study was to develop a novel porcine model and to determine the differential effects of feeding HBM and a commercial milk formula (MF) on immune response and gastrointestinal microbial colonization in a controlled environment. Methods:Male piglets were fed HBM (n = 26) or MF (n = 26) from day 2 through day 21. Piglets were vaccinated (n = 9/diet group) with cholera toxin and cholera toxin subunit B (CTB) and tetanus toxoid at 21 d or were fed placebo (n = 6/diet group) and then weaned to a standard solid diet at the age of 21 d. Humoral and cell-mediated immune responses were assessed from blood on days 35 and 48. Immune response was further examined from tissues, including mesenteric lymph nodes (MLNs), Peyer's patches (PPs), and spleen. The colonization of gut microbiota was characterized from feces on days 16 and 49. Results:Serum antibody titers in piglets fed HBM were 4-fold higher (P < 0.05) to CTB and 3-fold higher (P < 0.05) to tetanus toxoid compared with piglets fed MF on day 48. Compared with MF, the numbers of immunoglobulin A antibody-producing cells to CTB were 13-fold higher (P < 0.05) in MLNs and 11-fold higher (P < 0.05) in PPs in the HBM diet group on day 51. In addition, significantly increased T cell proliferation was observed in the HBM group relative to the MF group. Furthermore, microbial diversity in the HBM group was lower (P < 0.05) than in the MF group. Conclusions:This porcine model appears to be valid for studying the effects of early postnatal diet on immune responses and the gastrointestinal microbiome. Our results lay the groundwork for future studies defining the role of infant diet on microbiota and immune function.

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Early life administration of milk fat globule membrane promoted SCFA-producing bacteria colonization, intestinal barriers and growth performance of neonatal piglets.

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