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A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs

Polyphenols are a class of bioactive plant secondary metabolites that are thought to have beneficial effects on gut health, such as modulation of mucosal immune and inflammatory responses and regulation of parasite burdens. Here, we examined the interactions between a polyphenol-rich diet supplement...

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Autores principales: Williams, Andrew R., Krych, Lukasz, Fauzan Ahmad, Hajar, Nejsum, Peter, Skovgaard, Kerstin, Nielsen, Dennis S., Thamsborg, Stig M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5640243/
https://www.ncbi.nlm.nih.gov/pubmed/29028844
http://dx.doi.org/10.1371/journal.pone.0186546
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author Williams, Andrew R.
Krych, Lukasz
Fauzan Ahmad, Hajar
Nejsum, Peter
Skovgaard, Kerstin
Nielsen, Dennis S.
Thamsborg, Stig M.
author_facet Williams, Andrew R.
Krych, Lukasz
Fauzan Ahmad, Hajar
Nejsum, Peter
Skovgaard, Kerstin
Nielsen, Dennis S.
Thamsborg, Stig M.
author_sort Williams, Andrew R.
collection PubMed
description Polyphenols are a class of bioactive plant secondary metabolites that are thought to have beneficial effects on gut health, such as modulation of mucosal immune and inflammatory responses and regulation of parasite burdens. Here, we examined the interactions between a polyphenol-rich diet supplement and infection with the enteric nematode Ascaris suum in pigs. Pigs were fed either a basal diet or the same diet supplemented with grape pomace (GP), an industrial by-product rich in polyphenols such as oligomeric proanthocyanidins. Half of the animals in each group were then inoculated with A. suum for 14 days to assess parasite establishment, acquisition of local and systemic immune responses and effects on the gut microbiome. Despite in vitro anthelmintic activity of GP-extracts, numbers of parasite larvae in the intestine were not altered by GP-supplementation. However, the bioactive diet significantly increased numbers of eosinophils induced by A. suum infection in the duodenum, jejunum and ileum, and modulated gene expression in the jejunal mucosa of infected pigs. Both GP-supplementation and A. suum infection induced significant and apparently similar changes in the composition of the prokaryotic gut microbiota, and both also decreased concentrations of isobutyric and isovaleric acid (branched-chain short chain fatty acids) in the colon. Our results demonstrate that while a polyphenol-enriched diet in pigs may not directly influence A. suum establishment, it significantly modulates the subsequent host response to helminth infection. Our results suggest an influence of diet on immune function which may potentially be exploited to enhance immunity to helminths.
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spelling pubmed-56402432017-10-30 A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs Williams, Andrew R. Krych, Lukasz Fauzan Ahmad, Hajar Nejsum, Peter Skovgaard, Kerstin Nielsen, Dennis S. Thamsborg, Stig M. PLoS One Research Article Polyphenols are a class of bioactive plant secondary metabolites that are thought to have beneficial effects on gut health, such as modulation of mucosal immune and inflammatory responses and regulation of parasite burdens. Here, we examined the interactions between a polyphenol-rich diet supplement and infection with the enteric nematode Ascaris suum in pigs. Pigs were fed either a basal diet or the same diet supplemented with grape pomace (GP), an industrial by-product rich in polyphenols such as oligomeric proanthocyanidins. Half of the animals in each group were then inoculated with A. suum for 14 days to assess parasite establishment, acquisition of local and systemic immune responses and effects on the gut microbiome. Despite in vitro anthelmintic activity of GP-extracts, numbers of parasite larvae in the intestine were not altered by GP-supplementation. However, the bioactive diet significantly increased numbers of eosinophils induced by A. suum infection in the duodenum, jejunum and ileum, and modulated gene expression in the jejunal mucosa of infected pigs. Both GP-supplementation and A. suum infection induced significant and apparently similar changes in the composition of the prokaryotic gut microbiota, and both also decreased concentrations of isobutyric and isovaleric acid (branched-chain short chain fatty acids) in the colon. Our results demonstrate that while a polyphenol-enriched diet in pigs may not directly influence A. suum establishment, it significantly modulates the subsequent host response to helminth infection. Our results suggest an influence of diet on immune function which may potentially be exploited to enhance immunity to helminths. Public Library of Science 2017-10-13 /pmc/articles/PMC5640243/ /pubmed/29028844 http://dx.doi.org/10.1371/journal.pone.0186546 Text en © 2017 Williams et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Williams, Andrew R.
Krych, Lukasz
Fauzan Ahmad, Hajar
Nejsum, Peter
Skovgaard, Kerstin
Nielsen, Dennis S.
Thamsborg, Stig M.
A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs
title A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs
title_full A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs
title_fullStr A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs
title_full_unstemmed A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs
title_short A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs
title_sort polyphenol-enriched diet and ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5640243/
https://www.ncbi.nlm.nih.gov/pubmed/29028844
http://dx.doi.org/10.1371/journal.pone.0186546
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