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Whole Rye Consumption Improves Blood and Liver n-3 Fatty Acid Profile and Gut Microbiota Composition in Rats

BACKGROUND: Whole rye (WR) consumption seems to be associated with beneficial health effects. Although rye fiber and polyphenols are thought to be bioactive, the mechanisms behind the health effects of WR have yet to be fully identified. This study in rats was designed to investigate whether WR can...

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Autores principales: Ounnas, Fayçal, Privé, Florence, Salen, Patricia, Gaci, Nadia, Tottey, William, Calani, Luca, Bresciani, Letizia, López-Gutiérrez, Noelia, Hazane-Puch, Florence, Laporte, François, Brugère, Jean-François, Del Rio, Daniele, Demeilliers, Christine, de Lorgeril, Michel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4749345/
https://www.ncbi.nlm.nih.gov/pubmed/26862900
http://dx.doi.org/10.1371/journal.pone.0148118
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author Ounnas, Fayçal
Privé, Florence
Salen, Patricia
Gaci, Nadia
Tottey, William
Calani, Luca
Bresciani, Letizia
López-Gutiérrez, Noelia
Hazane-Puch, Florence
Laporte, François
Brugère, Jean-François
Del Rio, Daniele
Demeilliers, Christine
de Lorgeril, Michel
author_facet Ounnas, Fayçal
Privé, Florence
Salen, Patricia
Gaci, Nadia
Tottey, William
Calani, Luca
Bresciani, Letizia
López-Gutiérrez, Noelia
Hazane-Puch, Florence
Laporte, François
Brugère, Jean-François
Del Rio, Daniele
Demeilliers, Christine
de Lorgeril, Michel
author_sort Ounnas, Fayçal
collection PubMed
description BACKGROUND: Whole rye (WR) consumption seems to be associated with beneficial health effects. Although rye fiber and polyphenols are thought to be bioactive, the mechanisms behind the health effects of WR have yet to be fully identified. This study in rats was designed to investigate whether WR can influence the metabolism of n-3 and n-6 long-chain fatty acids (LCFA) and gut microbiota composition. METHODS: For 12 weeks, rats were fed a diet containing either 50% WR or 50% refined rye (RR). The WR diet provided more fiber (+21%) and polyphenols (+29%) than the RR diet. Fat intake was the same in both diets and particularly involved similar amounts of essential (18-carbon) n-3 and n-6 LCFAs. RESULTS: The WR diet significantly increased the 24-hour urinary excretion of polyphenol metabolites–including enterolactone–compared with the RR diet. The WR rats had significantly more n-3 LCFA–in particular, eicosapentanoic (EPA) and docosahexanoic (DHA) acids–in their plasma and liver. Compared with the RR diet, the WR diet brought significant changes in gut microbiota composition, with increased diversity in the feces (Shannon and Simpson indices), decreased Firmicutes/Bacteroidetes ratio and decreased proportions of uncultured Clostridiales cluster IA and Clostridium cluster IV in the feces. In contrast, no difference was found between groups with regards to cecum microbiota. The WR rats had lower concentrations of total short-chain fatty acids (SCFA) in cecum and feces (p<0.05). Finally, acetate was lower (p<0.001) in the cecum of WR rats while butyrate was lower (p<0.05) in the feces of WR rats. INTERPRETATION: This study shows for the first time that WR consumption results in major biological modifications–increased plasma and liver n-3 EPA and DHA levels and improved gut microbiota profile, notably with increased diversity–known to provide health benefits. Unexpectedly, WR decreased SCFA levels in both cecum and feces. More studies are needed to understand the interactions between whole rye (fiber and polyphenols) and gut microbiota and also the mechanisms of action responsible for stimulating n-3 fatty acid metabolism.
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spelling pubmed-47493452016-02-26 Whole Rye Consumption Improves Blood and Liver n-3 Fatty Acid Profile and Gut Microbiota Composition in Rats Ounnas, Fayçal Privé, Florence Salen, Patricia Gaci, Nadia Tottey, William Calani, Luca Bresciani, Letizia López-Gutiérrez, Noelia Hazane-Puch, Florence Laporte, François Brugère, Jean-François Del Rio, Daniele Demeilliers, Christine de Lorgeril, Michel PLoS One Research Article BACKGROUND: Whole rye (WR) consumption seems to be associated with beneficial health effects. Although rye fiber and polyphenols are thought to be bioactive, the mechanisms behind the health effects of WR have yet to be fully identified. This study in rats was designed to investigate whether WR can influence the metabolism of n-3 and n-6 long-chain fatty acids (LCFA) and gut microbiota composition. METHODS: For 12 weeks, rats were fed a diet containing either 50% WR or 50% refined rye (RR). The WR diet provided more fiber (+21%) and polyphenols (+29%) than the RR diet. Fat intake was the same in both diets and particularly involved similar amounts of essential (18-carbon) n-3 and n-6 LCFAs. RESULTS: The WR diet significantly increased the 24-hour urinary excretion of polyphenol metabolites–including enterolactone–compared with the RR diet. The WR rats had significantly more n-3 LCFA–in particular, eicosapentanoic (EPA) and docosahexanoic (DHA) acids–in their plasma and liver. Compared with the RR diet, the WR diet brought significant changes in gut microbiota composition, with increased diversity in the feces (Shannon and Simpson indices), decreased Firmicutes/Bacteroidetes ratio and decreased proportions of uncultured Clostridiales cluster IA and Clostridium cluster IV in the feces. In contrast, no difference was found between groups with regards to cecum microbiota. The WR rats had lower concentrations of total short-chain fatty acids (SCFA) in cecum and feces (p<0.05). Finally, acetate was lower (p<0.001) in the cecum of WR rats while butyrate was lower (p<0.05) in the feces of WR rats. INTERPRETATION: This study shows for the first time that WR consumption results in major biological modifications–increased plasma and liver n-3 EPA and DHA levels and improved gut microbiota profile, notably with increased diversity–known to provide health benefits. Unexpectedly, WR decreased SCFA levels in both cecum and feces. More studies are needed to understand the interactions between whole rye (fiber and polyphenols) and gut microbiota and also the mechanisms of action responsible for stimulating n-3 fatty acid metabolism. Public Library of Science 2016-02-10 /pmc/articles/PMC4749345/ /pubmed/26862900 http://dx.doi.org/10.1371/journal.pone.0148118 Text en © 2016 Ounnas 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
Ounnas, Fayçal
Privé, Florence
Salen, Patricia
Gaci, Nadia
Tottey, William
Calani, Luca
Bresciani, Letizia
López-Gutiérrez, Noelia
Hazane-Puch, Florence
Laporte, François
Brugère, Jean-François
Del Rio, Daniele
Demeilliers, Christine
de Lorgeril, Michel
Whole Rye Consumption Improves Blood and Liver n-3 Fatty Acid Profile and Gut Microbiota Composition in Rats
title Whole Rye Consumption Improves Blood and Liver n-3 Fatty Acid Profile and Gut Microbiota Composition in Rats
title_full Whole Rye Consumption Improves Blood and Liver n-3 Fatty Acid Profile and Gut Microbiota Composition in Rats
title_fullStr Whole Rye Consumption Improves Blood and Liver n-3 Fatty Acid Profile and Gut Microbiota Composition in Rats
title_full_unstemmed Whole Rye Consumption Improves Blood and Liver n-3 Fatty Acid Profile and Gut Microbiota Composition in Rats
title_short Whole Rye Consumption Improves Blood and Liver n-3 Fatty Acid Profile and Gut Microbiota Composition in Rats
title_sort whole rye consumption improves blood and liver n-3 fatty acid profile and gut microbiota composition in rats
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4749345/
https://www.ncbi.nlm.nih.gov/pubmed/26862900
http://dx.doi.org/10.1371/journal.pone.0148118
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