Early intervention with faecal microbiota transplantation: an effective means to improve growth performance and the intestinal development of suckling piglets

Abstract

Recent studies indicate that early postnatal period is a critical window for gut microbiota manipulation to optimise the immunity and body growth. This study investigated the effects of maternal faecal microbiota orally administered to neonatal piglets after birth on growth performance, selected microbial populations, intestinal permeability and the development of intestinal mucosal immune system. In total, 12 litters of crossbred newborn piglets were selected in this study. Litter size was standardised to 10 piglets. On day 1, 10 piglets in each litter were randomly allotted to the faecal microbiota transplantation (FMT) and control groups. Piglets in the FMT group were orally administrated with 2ml faecal suspension of their nursing sow per day from the age of 1 to 3 days; piglets in the control group were treated with the same dose of a placebo (0.1M potassium phosphate buffer containing 10% glycerol (vol/vol)) inoculant. The experiment lasted 21 days. On days 7, 14 and 21, plasma and faecal samples were collected for the analysis of growth-related hormones and cytokines in plasma and lipocalin-2, secretory immunoglobulin A (sIgA), selected microbiota and short-chain fatty acids (SCFAs) in faeces. Faecal microbiota transplantation increased the average daily gain of piglets during week 3 and the whole experiment period. Compared with the control group, the FMT group had increased concentrations of plasma growth hormone and IGF-1 on days 14 and 21. Faecal microbiota transplantation also reduced the incidence of diarrhoea during weeks 1 and 3 and plasma concentrations of zonulin, endotoxin and diamine oxidase activities in piglets on days 7 and 14. The populations of Lactobacillus spp. and Faecalibacterium prausnitzii and the concentrations of faecal and plasma acetate, butyrate and total SCFAs in FMT group were higher than those in the control group on day 21. Moreover, the FMT piglets have higher concentrations of plasma transforming growth factor-β and immunoglobulin G, and faecal sIgA than the control piglets on day 21. These findings indicate that early intervention with maternal faecal microbiota improves growth performance, decreases intestinal permeability, stimulates sIgA secretion, and modulates gut microbiota composition and metabolism in suckling piglets.

Early-Life Intervention Using Fecal Microbiota Combined with Probiotics Promotes Gut Microbiota Maturation, Regulates Immune System Development, and Alleviates Weaning Stress in Piglets

“…It has been shown that fecal sIgA can be quantified as a biomarker of intestinal permeability and immune functions [48]. Besides, early intervention with FMT-CS increased plasma IgG and IgM, and similar results were reported in previous studies of suckling piglets [20,35]. Our results indicate that early intervention with FMT-CS can improve the adaptive immune function of piglets.…”

“…Early infancy is considered as an ideal window for gut microbial colonization [18,38]. Our previous study has validated the benefits of transplanting sow fecal microbiota to newborn piglets [20]. Here, by combining the oral administration of fecal microbiota of gestation sows with C. butyricum and S. boulardii in newborn piglets, this study for the first time focuses on the promotion of immune development through improving the gut microbiota of piglets.…”

“…Recently, a number of studies have demonstrated an association between the immune system and gut microbiota [20,[32][33][34][35][36][37]. Early infancy is considered as an ideal window for gut microbial colonization [18,38].…”

“…Fecal Lactobacillus is associated with the regulation of the gut immune function and maintenance of the balance of gut microbiota to reduce the inflammatory responses [56,[60][61][62][63]. Recent studies have confirmed that FMT could enrich the abundance of gut Lactobacillus, which may contribute to the improvement of the intestinal barrier and reduction of diarrhea incidence in piglets [20,35,53]. Moreover, Lactobacillus was reported to enhance the gut barrier to confer diarrhea resistance after the weaning of piglets [64].…”

“…Newborn piglets are usually used as an ideal animal model for studying human nutrition and physiology [19]. In our previous study, early intervention with mature maternal fecal microbiota transplantation (FMT) was found to have positive effects on the improvement of growth performance and immunity and decrease diarrhea in the newborn piglet model [20]. However, the developmental changes in the intestinal microbiota after early intervention remain elusive.…”