Dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota, metabolic activity, and epithelial function

Abstract Background Intrauterine growth retardation (IUGR) is one of the major constraints in animal production. Our previous study showed that piglets with IUGR are associated with abnormal bile acid (BA) metabolism. This study explored whether dietary BA supplementation could improve growth perfor...

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Main Authors: Yang Liu, Md. Abul Kalam Azad, Sujuan Ding, Qian Zhu, Francois Blachier, Zugong Yu, Haijun Gao, Xiangfeng Kong
Format: Article
Language:English
Published: BMC 2023-07-01
Series:Journal of Animal Science and Biotechnology
Subjects:
Online Access:https://doi.org/10.1186/s40104-023-00897-2
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author Yang Liu
Md. Abul Kalam Azad
Sujuan Ding
Qian Zhu
Francois Blachier
Zugong Yu
Haijun Gao
Xiangfeng Kong
author_facet Yang Liu
Md. Abul Kalam Azad
Sujuan Ding
Qian Zhu
Francois Blachier
Zugong Yu
Haijun Gao
Xiangfeng Kong
author_sort Yang Liu
collection DOAJ
description Abstract Background Intrauterine growth retardation (IUGR) is one of the major constraints in animal production. Our previous study showed that piglets with IUGR are associated with abnormal bile acid (BA) metabolism. This study explored whether dietary BA supplementation could improve growth performance and colonic development, function, microbiota, and metabolites in the normal birth weight (NBW) and IUGR piglets. A total of 48 weaned piglets (24 IUGR and 24 NBW) were allocated to four groups (12 piglets per group): (i) NBW group, (ii) NBW + BA group, (iii) IUGR group, and (iv) IUGR + BA group. Samples were collected after 28 days of feeding. Results The results showed that dietary BA supplementation increased the length and weight of the colon and colon weight to body weight ratio, while decreased the plasma diamine oxidase (DAO) concentration in the NBW piglets (P < 0.05). Dietary BA supplementation to IUGR piglets decreased (P < 0.05) the plasma concentrations of D-lactate and endotoxin and colonic DAO and endotoxin, suggesting a beneficial effect on epithelial integrity. Moreover, dietary BA supplementation to NBW and IUGR piglets increased Firmicutes abundance and decreased Bacteroidetes abundance (P < 0.05), whereas Lactobacillus was the dominant genus in the colon. Metabolome analysis revealed 65 and 51 differential metabolites in the colon of piglets fed a diet with/without BA, respectively, which was associated with the colonic function of IUGR piglets. Furthermore, dietary BA supplementation to IUGR piglets upregulated the expressions of CAT, GPX, SOD, Nrf1, IL-2, and IFN-γ in colonic mucosa (P < 0.05). Conclusions Collectively, dietary BA supplementation could improve the colonic function of IUGR piglets, which was associated with increasing proportions of potentially beneficial bacteria and metabolites. Furthermore, BA shows a promising application prospect in improving the intestinal ecosystem and health of animals.
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spelling doaj.art-e49058f829a34e198228c7af6203fbf12023-07-16T11:24:03ZengBMCJournal of Animal Science and Biotechnology2049-18912023-07-0114111810.1186/s40104-023-00897-2Dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota, metabolic activity, and epithelial functionYang Liu0Md. Abul Kalam Azad1Sujuan Ding2Qian Zhu3Francois Blachier4Zugong Yu5Haijun Gao6Xiangfeng Kong7Key Laboratory of Agro-Ecological Process in Subtropical Region, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory of Agro-Ecological Process in Subtropical Region, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory of Agro-Ecological Process in Subtropical Region, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory of Agro-Ecological Process in Subtropical Region, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of SciencesUniversité Paris-SaclayAgroParisTech, INRAE, UMR PNCA, 75005College of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Medicine, Howard UniversityKey Laboratory of Agro-Ecological Process in Subtropical Region, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of SciencesAbstract Background Intrauterine growth retardation (IUGR) is one of the major constraints in animal production. Our previous study showed that piglets with IUGR are associated with abnormal bile acid (BA) metabolism. This study explored whether dietary BA supplementation could improve growth performance and colonic development, function, microbiota, and metabolites in the normal birth weight (NBW) and IUGR piglets. A total of 48 weaned piglets (24 IUGR and 24 NBW) were allocated to four groups (12 piglets per group): (i) NBW group, (ii) NBW + BA group, (iii) IUGR group, and (iv) IUGR + BA group. Samples were collected after 28 days of feeding. Results The results showed that dietary BA supplementation increased the length and weight of the colon and colon weight to body weight ratio, while decreased the plasma diamine oxidase (DAO) concentration in the NBW piglets (P < 0.05). Dietary BA supplementation to IUGR piglets decreased (P < 0.05) the plasma concentrations of D-lactate and endotoxin and colonic DAO and endotoxin, suggesting a beneficial effect on epithelial integrity. Moreover, dietary BA supplementation to NBW and IUGR piglets increased Firmicutes abundance and decreased Bacteroidetes abundance (P < 0.05), whereas Lactobacillus was the dominant genus in the colon. Metabolome analysis revealed 65 and 51 differential metabolites in the colon of piglets fed a diet with/without BA, respectively, which was associated with the colonic function of IUGR piglets. Furthermore, dietary BA supplementation to IUGR piglets upregulated the expressions of CAT, GPX, SOD, Nrf1, IL-2, and IFN-γ in colonic mucosa (P < 0.05). Conclusions Collectively, dietary BA supplementation could improve the colonic function of IUGR piglets, which was associated with increasing proportions of potentially beneficial bacteria and metabolites. Furthermore, BA shows a promising application prospect in improving the intestinal ecosystem and health of animals.https://doi.org/10.1186/s40104-023-00897-2Bile acidIntrauterine growth retardationMetaboliteMicrobiotaPiglet
spellingShingle Yang Liu
Md. Abul Kalam Azad
Sujuan Ding
Qian Zhu
Francois Blachier
Zugong Yu
Haijun Gao
Xiangfeng Kong
Dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota, metabolic activity, and epithelial function
Journal of Animal Science and Biotechnology
Bile acid
Intrauterine growth retardation
Metabolite
Microbiota
Piglet
title Dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota, metabolic activity, and epithelial function
title_full Dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota, metabolic activity, and epithelial function
title_fullStr Dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota, metabolic activity, and epithelial function
title_full_unstemmed Dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota, metabolic activity, and epithelial function
title_short Dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota, metabolic activity, and epithelial function
title_sort dietary bile acid supplementation in weaned piglets with intrauterine growth retardation improves colonic microbiota metabolic activity and epithelial function
topic Bile acid
Intrauterine growth retardation
Metabolite
Microbiota
Piglet
url https://doi.org/10.1186/s40104-023-00897-2
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