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Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites

In humans, the metabolic and immune changes occurring during perinatal period also describe metabolic syndrome. Gut microbiota can cause symptoms of metabolic syndrome in pregnant women. Increased gut permeability is also involved in metabolic disorders in non-pregnant hosts. However, longitudinal s...

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Autores principales: Cheng, Chuanshang, Wei, Hongkui, Yu, Huichao, Xu, Chuanhui, Jiang, Siwen, Peng, Jian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6117386/
https://www.ncbi.nlm.nih.gov/pubmed/30197635
http://dx.doi.org/10.3389/fmicb.2018.01989
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author Cheng, Chuanshang
Wei, Hongkui
Yu, Huichao
Xu, Chuanhui
Jiang, Siwen
Peng, Jian
author_facet Cheng, Chuanshang
Wei, Hongkui
Yu, Huichao
Xu, Chuanhui
Jiang, Siwen
Peng, Jian
author_sort Cheng, Chuanshang
collection PubMed
description In humans, the metabolic and immune changes occurring during perinatal period also describe metabolic syndrome. Gut microbiota can cause symptoms of metabolic syndrome in pregnant women. Increased gut permeability is also involved in metabolic disorders in non-pregnant hosts. However, longitudinal studies investigating the changes in metabolic characteristics, gut microbiota, and gut permeability of sows throughout pregnancy and lactation are lacking. The correlation between gut microbiota and metabolic status of sows is also poorly known. The present study was conducted to investigate the temporal variations in sow metabolic characteristics, gut microbiota, gut permeability, and gut inflammation at days 30 (G30) and 109 (G109) of gestation and days 3 (L3) and 14 (L14) of lactation. Results showed that insulin sensitivity was decreased in L3. Circulating concentrations of pro-inflammatory cytokine IL-6 increased in G109 and L3. 16S rRNA gene sequencing of the V3-V4 region showed that gut microbiota changed dramatically across different reproductive stages. The bacterial abundance and alpha diversity in L3 were the lowest. The phyla Proteobacteria and Fusobacteria exhibited the highest relative abundance in L3. Among the genera, Bacteroides, Escherichia_Shigella, and Fusobacterium were highest, but Oscillospira the lowest, in relative abundance in L3. The fecal levels of acetate and total short-chain fatty acids were increased in G109, but fecal butyrate concentrations were markedly decreased in L3. The plasma zonulin concentrations, a biomarker for gut permeability, were increased in G109 and L3. The plasma endotoxin concentrations were increased in L3. Furthermore, levels of fecal lipocalin-2 and pro-inflammatory cytokines IL-6 and TNF-α were increased in G109 and L3. In contrast, fecal levels of anti-inflammatory cytokine IL-10 were significantly decreased in G109 and L3. Additionally, the increased relative abundances of Fusobacterium in L3 were positively correlated with plasma zonulin and fecal endotoxin but negatively correlated with fecal IL-10. These findings indicate that the mother sow exhibits a metabolic syndrome and dramatical changes in gut microbiota during perinatal period, especially in early lactation. Besides, increased gut permeability and plasma endotoxin concentrations caused by negative microbial changes would possibly be the potential mechanisms under which sow’s metabolic disorders and inflammatory status were exacerbated during early lactation.
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spelling pubmed-61173862018-09-07 Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites Cheng, Chuanshang Wei, Hongkui Yu, Huichao Xu, Chuanhui Jiang, Siwen Peng, Jian Front Microbiol Microbiology In humans, the metabolic and immune changes occurring during perinatal period also describe metabolic syndrome. Gut microbiota can cause symptoms of metabolic syndrome in pregnant women. Increased gut permeability is also involved in metabolic disorders in non-pregnant hosts. However, longitudinal studies investigating the changes in metabolic characteristics, gut microbiota, and gut permeability of sows throughout pregnancy and lactation are lacking. The correlation between gut microbiota and metabolic status of sows is also poorly known. The present study was conducted to investigate the temporal variations in sow metabolic characteristics, gut microbiota, gut permeability, and gut inflammation at days 30 (G30) and 109 (G109) of gestation and days 3 (L3) and 14 (L14) of lactation. Results showed that insulin sensitivity was decreased in L3. Circulating concentrations of pro-inflammatory cytokine IL-6 increased in G109 and L3. 16S rRNA gene sequencing of the V3-V4 region showed that gut microbiota changed dramatically across different reproductive stages. The bacterial abundance and alpha diversity in L3 were the lowest. The phyla Proteobacteria and Fusobacteria exhibited the highest relative abundance in L3. Among the genera, Bacteroides, Escherichia_Shigella, and Fusobacterium were highest, but Oscillospira the lowest, in relative abundance in L3. The fecal levels of acetate and total short-chain fatty acids were increased in G109, but fecal butyrate concentrations were markedly decreased in L3. The plasma zonulin concentrations, a biomarker for gut permeability, were increased in G109 and L3. The plasma endotoxin concentrations were increased in L3. Furthermore, levels of fecal lipocalin-2 and pro-inflammatory cytokines IL-6 and TNF-α were increased in G109 and L3. In contrast, fecal levels of anti-inflammatory cytokine IL-10 were significantly decreased in G109 and L3. Additionally, the increased relative abundances of Fusobacterium in L3 were positively correlated with plasma zonulin and fecal endotoxin but negatively correlated with fecal IL-10. These findings indicate that the mother sow exhibits a metabolic syndrome and dramatical changes in gut microbiota during perinatal period, especially in early lactation. Besides, increased gut permeability and plasma endotoxin concentrations caused by negative microbial changes would possibly be the potential mechanisms under which sow’s metabolic disorders and inflammatory status were exacerbated during early lactation. Frontiers Media S.A. 2018-08-24 /pmc/articles/PMC6117386/ /pubmed/30197635 http://dx.doi.org/10.3389/fmicb.2018.01989 Text en Copyright © 2018 Cheng, Wei, Yu, Xu, Jiang and Peng. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Cheng, Chuanshang
Wei, Hongkui
Yu, Huichao
Xu, Chuanhui
Jiang, Siwen
Peng, Jian
Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites
title Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites
title_full Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites
title_fullStr Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites
title_full_unstemmed Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites
title_short Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites
title_sort metabolic syndrome during perinatal period in sows and the link with gut microbiota and metabolites
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6117386/
https://www.ncbi.nlm.nih.gov/pubmed/30197635
http://dx.doi.org/10.3389/fmicb.2018.01989
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