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Consumption of Dietary Fiber from Different Sources during Pregnancy Alters Sow Gut Microbiota and Improves Performance and Reduces Inflammation in Sows and Piglets

In pregnant and lactating sows, metabolism and immunity undergo drastic changes, which can lead to constipation, abortion, and intrauterine growth restriction (IUGR) and reduce production performance. Dietary fiber can regulate animal gut microbiota, alleviate inflammatory responses, and improve per...

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Autores principales: Liu, Boshuai, Zhu, Xiaoyan, Cui, Yalei, Wang, Wenjing, Liu, Hua, Li, Zidan, Guo, Zhiguo, Ma, Sen, Li, Defeng, Wang, Chengzhang, Shi, Yinghua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7842364/
https://www.ncbi.nlm.nih.gov/pubmed/33500330
http://dx.doi.org/10.1128/mSystems.00591-20
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author Liu, Boshuai
Zhu, Xiaoyan
Cui, Yalei
Wang, Wenjing
Liu, Hua
Li, Zidan
Guo, Zhiguo
Ma, Sen
Li, Defeng
Wang, Chengzhang
Shi, Yinghua
author_facet Liu, Boshuai
Zhu, Xiaoyan
Cui, Yalei
Wang, Wenjing
Liu, Hua
Li, Zidan
Guo, Zhiguo
Ma, Sen
Li, Defeng
Wang, Chengzhang
Shi, Yinghua
author_sort Liu, Boshuai
collection PubMed
description In pregnant and lactating sows, metabolism and immunity undergo drastic changes, which can lead to constipation, abortion, and intrauterine growth restriction (IUGR) and reduce production performance. Dietary fiber can regulate animal gut microbiota, alleviate inflammatory responses, and improve performance. Here, 48 sows (Large × Landrace) were randomly allocated to groups including, control, and with alfalfa meal (AM), beet pulp, and soybean skin dietary supplementation for 60 days of gestation. The AM diet decreased IUGR, increased food intake during lactation, and promoted the reproductive performance and physical condition of sows. Further, the AM diet significantly reduced markers of intestinal permeability (reactive oxygen species and endotoxin) in sow serum, and of systemic inflammation (interleukin-6 [IL-6] and tumor necrosis factor alpha) in sow feces and serum, as well as piglet serum, while it increased the anti-inflammatory marker, IL-10, in sow serum and feces. The AM diet also significantly affected gut microbiota by increasing the relative abundance of proinflammatory bacteria, while decreasing anti-inflammatory bacteria. Moreover, the total short-chain fatty acid (SCFA) content was higher in feces from sows fed an AM diet, with butyric acid content significantly higher during lactation, than in controls. Sow performance was correlated with intestinal permeability, inflammation, and gut microbiota, which were also vertically transmitted to piglets. Our results are significant for guiding feed management in the pig breeding industry. Further, the “sows to piglets” model provides a reference for the effect of dietary fiber on the gastrointestinal function of human mothers and infants. IMPORTANCE Although the direct effects of dietary fiber on gut microbiota composition have been studied extensively, systematic evaluation of different fiber sources on gut health and inflammatory responses of sows and their offspring has rarely been conducted. Excessive reactive oxygen species produced by overactive metabolic processes during late pregnancy and lactation of sows leads to increased endotoxin levels, disordered gut microbiota, decreased SCFA production, and secretion of proinflammatory factors, which in turn causes local inflammation of the gut, potential damage of the gut microbial barrier, increased gut permeability, increased blood endotoxin levels (resulting in systemic inflammation), and ultimately decreased sow and piglet performance. Our results showed that supplementation of the diet with alfalfa meal in mid and late pregnancy can reverse this process. Our findings lay a foundation for improving the gut health of sows and piglets and provide insights into the study of the gastrointestinal tract function in human mothers and infants.
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spelling pubmed-78423642021-01-29 Consumption of Dietary Fiber from Different Sources during Pregnancy Alters Sow Gut Microbiota and Improves Performance and Reduces Inflammation in Sows and Piglets Liu, Boshuai Zhu, Xiaoyan Cui, Yalei Wang, Wenjing Liu, Hua Li, Zidan Guo, Zhiguo Ma, Sen Li, Defeng Wang, Chengzhang Shi, Yinghua mSystems Research Article In pregnant and lactating sows, metabolism and immunity undergo drastic changes, which can lead to constipation, abortion, and intrauterine growth restriction (IUGR) and reduce production performance. Dietary fiber can regulate animal gut microbiota, alleviate inflammatory responses, and improve performance. Here, 48 sows (Large × Landrace) were randomly allocated to groups including, control, and with alfalfa meal (AM), beet pulp, and soybean skin dietary supplementation for 60 days of gestation. The AM diet decreased IUGR, increased food intake during lactation, and promoted the reproductive performance and physical condition of sows. Further, the AM diet significantly reduced markers of intestinal permeability (reactive oxygen species and endotoxin) in sow serum, and of systemic inflammation (interleukin-6 [IL-6] and tumor necrosis factor alpha) in sow feces and serum, as well as piglet serum, while it increased the anti-inflammatory marker, IL-10, in sow serum and feces. The AM diet also significantly affected gut microbiota by increasing the relative abundance of proinflammatory bacteria, while decreasing anti-inflammatory bacteria. Moreover, the total short-chain fatty acid (SCFA) content was higher in feces from sows fed an AM diet, with butyric acid content significantly higher during lactation, than in controls. Sow performance was correlated with intestinal permeability, inflammation, and gut microbiota, which were also vertically transmitted to piglets. Our results are significant for guiding feed management in the pig breeding industry. Further, the “sows to piglets” model provides a reference for the effect of dietary fiber on the gastrointestinal function of human mothers and infants. IMPORTANCE Although the direct effects of dietary fiber on gut microbiota composition have been studied extensively, systematic evaluation of different fiber sources on gut health and inflammatory responses of sows and their offspring has rarely been conducted. Excessive reactive oxygen species produced by overactive metabolic processes during late pregnancy and lactation of sows leads to increased endotoxin levels, disordered gut microbiota, decreased SCFA production, and secretion of proinflammatory factors, which in turn causes local inflammation of the gut, potential damage of the gut microbial barrier, increased gut permeability, increased blood endotoxin levels (resulting in systemic inflammation), and ultimately decreased sow and piglet performance. Our results showed that supplementation of the diet with alfalfa meal in mid and late pregnancy can reverse this process. Our findings lay a foundation for improving the gut health of sows and piglets and provide insights into the study of the gastrointestinal tract function in human mothers and infants. American Society for Microbiology 2021-01-26 /pmc/articles/PMC7842364/ /pubmed/33500330 http://dx.doi.org/10.1128/mSystems.00591-20 Text en Copyright © 2021 Liu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Liu, Boshuai
Zhu, Xiaoyan
Cui, Yalei
Wang, Wenjing
Liu, Hua
Li, Zidan
Guo, Zhiguo
Ma, Sen
Li, Defeng
Wang, Chengzhang
Shi, Yinghua
Consumption of Dietary Fiber from Different Sources during Pregnancy Alters Sow Gut Microbiota and Improves Performance and Reduces Inflammation in Sows and Piglets
title Consumption of Dietary Fiber from Different Sources during Pregnancy Alters Sow Gut Microbiota and Improves Performance and Reduces Inflammation in Sows and Piglets
title_full Consumption of Dietary Fiber from Different Sources during Pregnancy Alters Sow Gut Microbiota and Improves Performance and Reduces Inflammation in Sows and Piglets
title_fullStr Consumption of Dietary Fiber from Different Sources during Pregnancy Alters Sow Gut Microbiota and Improves Performance and Reduces Inflammation in Sows and Piglets
title_full_unstemmed Consumption of Dietary Fiber from Different Sources during Pregnancy Alters Sow Gut Microbiota and Improves Performance and Reduces Inflammation in Sows and Piglets
title_short Consumption of Dietary Fiber from Different Sources during Pregnancy Alters Sow Gut Microbiota and Improves Performance and Reduces Inflammation in Sows and Piglets
title_sort consumption of dietary fiber from different sources during pregnancy alters sow gut microbiota and improves performance and reduces inflammation in sows and piglets
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7842364/
https://www.ncbi.nlm.nih.gov/pubmed/33500330
http://dx.doi.org/10.1128/mSystems.00591-20
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