Dataset Information

The Effect of Butyrate-Supplemented Parenteral Nutrition on Intestinal Defence Mechanisms and the Parenteral Nutrition-Induced Shift in the Gut Microbiota in the Rat Model.

ABSTRACT: Butyrate produced by the intestinal microbiota is essential for proper functioning of the intestinal immune system. Total dependence on parenteral nutrition (PN) is associated with numerous adverse effects, including severe microbial dysbiosis and loss of important butyrate producers. We hypothesised that a lack of butyrate produced by the gut microbiota may be compensated by its supplementation in PN mixtures. We tested whether i.v. butyrate administration would (a) positively modulate intestinal defence mechanisms and (b) counteract PN-induced dysbiosis. Male Wistar rats were randomised to chow, PN, and PN supplemented with 9 mM butyrate (PN+But) for 12 days. Antimicrobial peptides, mucins, tight junction proteins, and cytokine expression were assessed by RT-qPCR. T-cell subpopulations in mesenteric lymph nodes (MLN) were analysed by flow cytometry. Microbiota composition was assessed in caecum content. Butyrate supplementation resulted in increased expression of tight junction proteins (ZO-1, claudin-7, E-cadherin), antimicrobial peptides (Defa 8, Rd5, RegIII?), and lysozyme in the ileal mucosa. Butyrate partially alleviated PN-induced intestinal barrier impairment and normalised IL-4, IL-10, and IgA mRNA expression. PN administration was associated with an increase in Tregs in MLN, which was normalised by butyrate. Butyrate increased the total number of CD4+ and decreased a relative amount of CD8+ memory T cells in MLN. Lack of enteral nutrition and PN administration led to a shift in caecal microbiota composition. Butyrate did not reverse the altered expression of most taxa but did influence the abundance of some potentially beneficial/pathogenic genera, which might contribute to its overall beneficial effect.

SUBMITTER: Jirsova Z

PROVIDER: S-EPMC6421034 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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The Effect of Butyrate-Supplemented Parenteral Nutrition on Intestinal Defence Mechanisms and the Parenteral Nutrition-Induced Shift in the Gut Microbiota in the Rat Model.

Jirsova Zuzana Z Heczkova Marie M Dankova Helena H Malinska Hana H Videnska Petra P Vespalcova Hana H Micenkova Lenka L Bartonova Lenka L Sticova Eva E Lodererova Alena A Prefertusová Lucia L Sekerkova Alena A Hradecky Jaromir J Cahova Monika M

BioMed research international 20190228

Butyrate produced by the intestinal microbiota is essential for proper functioning of the intestinal immune system. Total dependence on parenteral nutrition (PN) is associated with numerous adverse effects, including severe microbial dysbiosis and loss of important butyrate producers. We hypothesised that a lack of butyrate produced by the gut microbiota may be compensated by its supplementation in PN mixtures. We tested whether <i>i.v.</i> butyrate administration would (a) positively modulate i ...[more]

PMID: 30941370

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Project description:BACKGROUND:Total parenteral nutrition (TPN) provides all nutritional needs intravenously. Although lifesaving, enthusiasm is significantly tempered due to side effects of liver and gut injury, as well as lack of mechanistic understanding into drivers of TPN injury. We hypothesized that the state of luminal nutritional deprivation with TPN drives alterations in gut-systemic signaling, contributing to injury, and tested this hypothesis using our ambulatory TPN model. METHODS:A total of 16 one-week-old piglets were allocated randomly to TPN (n = 8) or enteral nutrition (EN, n = 8) for 3 weeks. Liver, gut, and serum were analyzed. All tests were two-sided, with a significance level of 0.05. RESULTS:TPN resulted in significant hyperbilirubinemia and cholestatic liver injury, p = 0.034. Hepatic inflammation (cluster of differentiation 3 (CD3) immunohistochemistry) was higher with TPN (p = 0.021). No significant differences in alanine aminotransferase (ALT) or bile ductular proliferation were noted. TPN resulted in reduction of muscularis mucosa thickness and marked gut atrophy. Median and interquartile range for gut mass was 0.46 (0.30-0.58) g/cm in EN, and 0.19 (0.11-0.29) g/cm in TPN (p = 0.024). Key gut-systemic signaling regulators, liver farnesoid X receptor (FXR; p = 0.021), liver constitutive androstane receptor (CAR; p = 0.014), gut FXR (p = 0.028), G-coupled bile acid receptor (TGR5) (p = 0.003), epidermal growth factor (EGF; p = 0.016), organic anion transporter (OAT; p = 0.028), Mitogen-activated protein kinases-1 (MAPK1) (p = 0.037), and sodium uptake transporter sodium glucose-linked transporter (SGLT-1; p = 0.010) were significantly downregulated in TPN animals, whereas liver cholesterol 7 alpha-hydroxylase (CyP7A1) was substantially higher with TPN (p = 0.011). CONCLUSION:We report significant alterations in key hepatobiliary receptors driving gut-systemic signaling in a TPN piglet model. This presents a major advancement to our understanding of TPN-associated injury and suggests opportunities for strategic targeting of the gut-systemic axis, specifically, FXR, TGR5, and EGF in developing ameliorative strategies.

Project description:Weaning is a critical period for piglets, in which unbalanced gut microbiota and/or pathogen colonisation can contribute to diseases that interfere with animal performance. Tannins are natural compounds that could be used as functional ingredients to improve gut health in pig farming thanks to their antibacterial, antioxidant, and antidiarrhoeal properties. In this study, a mixture of quebracho and chestnut tannins (1.25%) was evaluated for its efficacy in reducing the negative weaning effects on piglet growth. Microbiota composition was assessed by Illumina MiSeq 16S rRNA gene sequencing of DNA extracted from stools at the end of the trial. Sequence analysis revealed an increase in the genera Shuttleworthia, Pseudobutyrivibrio, Peptococcus, Anaerostipes, and Solobacterium in the tannin-supplemented group. Conversely, this dietary intervention reduced the abundance of the genera Syntrophococcus, Atopobium, Mitsuokella, Sharpea, and Prevotella. The populations of butyrate-producing bacteria were modulated by tannin, and higher butyrate concentrations in stools were detected in the tannin-fed pigs. Co-occurrence analysis revealed that the operational taxonomic units (OTUs) belonging to the families Veillonellaceae, Lachnospiraceae, and Coriobacteriaceae occupied the central part of the network in both the control and the tannin-fed animals. Instead, in the tannin group, the OTUs belonging to the families Acidaminococcaceae, Alcaligenaceae, and Spirochaetaceae characterised its network, whereas Family XIII Incertae Sedis occupied a more central position than in the control group. Conversely, the presence of Desulfovibrionaceae characterised the network of the control group, and this family was not present in the network of the tannin group. Moreover, the prediction of metabolic pathways revealed that the gut microbiome of the tannin group possessed an enhanced potential for carbohydrate transport and metabolism, as well as a lower abundance of pathways related to cell wall/membrane/envelope biogenesis and inorganic ion transport. In conclusion, the tested tannins seem to modulate the gut microbiota, favouring groups of butyrate-producing bacteria.

Dataset Information

The Effect of Butyrate-Supplemented Parenteral Nutrition on Intestinal Defence Mechanisms and the Parenteral Nutrition-Induced Shift in the Gut Microbiota in the Rat Model.

Publications

The Effect of Butyrate-Supplemented Parenteral Nutrition on Intestinal Defence Mechanisms and the Parenteral Nutrition-Induced Shift in the Gut Microbiota in the Rat Model.

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