Maternal consumption of a fermented diet protects offspring against intestinal inflammation by regulating the gut microbiota

Abstract

The neonatal intestinal tract is immature and can be easily infected by pathogens causing inflammation. Maternal diet manipulation is a promising nutritional strategy to enhance the gut health of offspring. A fermented diet is a gut microbiota targeting diet containing live probiotics and their metabolites, which benefit the gut and overall health host. However, it remains unclear how a maternal fermented diet (MFD) affects neonatal intestinal inflammation. Here, in vivo and in vitro models together with multi-omics analysis were applied to investigate the impacts and the underlying mechanism through which an MFD prevents from gut inflammation in neonates. An MFD remarkably improved the performance of both sows and piglets and significantly altered the gut microbiome and milk metabolome of sows. In addition, the MFD significantly accelerated the maturation of the gut microbiota of neonates and increased the abundance of gut Lactobacillus and the microbial functions of amino acid-related enzymes and glucose metabolism on the weaning day. Notably, the MFD reduced susceptibility to colonic inflammation in offspring. The fecal microbiota of sows was then transplanted into mouse dams and it was found that the mouse dams and pups in the MFD group alleviated the LPS-induced decrease in gut Lactobacillus abundance and barrier injury. Milk L-glutamine (GLN) and gut Lactobacillus reuteri (LR) were found as two of the main MFD-induced sow effectors that contributed to the gut health of piglets. The properties of LR and GLN in modulating gut microbiota and alleviating colonic inflammation by inhibiting the phosphorylation of p38 and JNK and activation of Caspase 3 were further verified. These findings provide the first data revealing that an MFD drives neonate gut microbiota development and ameliorates the colonic inflammation by regulating the gut microbiota. This fundamental evidence might provide references for modulating maternal nutrition to enhance early-life gut health and prevent gut inflammation.

Development of Intestinal Injury and Restoration of Weaned Piglets under Chronic Immune Stress

“…Approximately 3–4 μm thick microtome sections of intestinal tissues were obtained from each sample and stained with hematoxylin and eosin (H&E) as previously described [ 28 ]. The hematoxylin-eosin stained images of intestine were captured and measured with computer-assisted microscopy (Micrometrics TM; Nikon ECLIPSE E200, Tokyo, Japan).…”

“…The cassettes with constructs were quickly transferred to beakers with melted paraffin wax and left to rest in the oven for 1–2 days (60 °C), and the pre-treated tissue blocks were embedded with melted paraffin wax in specific embedding molds to form tissue wax blocks. Intestinal tissue paraffin sections were dewaxed in absolute ethanol, then placed them in a repair box filled with EDTA antigen recovery solution (pH 8.0) which was prepared in a microwave oven [ 28 ]. Subsequently, the sections were added, with BSA incubating for 30 min and then the primary antibody was added overnight at 4°C.…”

Gut Health and Influencing Factors in Pigs

“…Adding probiotics to the maternal diets affects the maternal colonic microbiota and influences the offspring’s gut microbiota profile and metabolites [ 163 , 188 ]. Furthermore, maternal consumption of a fermented diet protected neonates from colonic inflammation by facilitating the maturation of the gut microbiota and proliferation of gut lactobacillus [ 189 ]. The strong correlations between the microbiota compositions of sows and their offspring are proof of maternal imprinting, which has benefits that persist after weaning [ 190 ].…”

Quercetin Reduces Inflammation and Protects Gut Microbiota in Broilers

“…Meanwhile, intestinal microflora dysbiosis also led to gastrointestinal and inflammatory disorders [ 13 , 14 ]. Maternal fermented diet could ameliorate neonatal colonic inflammation by inducing an abundance of gut Lactobacillus reuteri [ 15 ]. Licochalcone A alleviated ulcerative colitis by maintaining tight junction protein expression (maintaining integrity of the intestinal barrier), inhibiting inflammation levels and regulating intestinal barrier-associated bacteria [ 16 ].…”