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Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients

PURPOSE: There is considerable interest in the effects of the intestinal microbiota (IM) composition, its activities in relation with the metabolism of dietary substrates and the impact these effects may have in the development and prevention of certain non-communicable diseases. It is acknowledged...

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Autores principales: Shortt, Colette, Hasselwander, Oliver, Meynier, Alexandra, Nauta, Arjen, Fernández, Estefanía Noriega, Putz, Peter, Rowland, Ian, Swann, Jonathan, Türk, Jessica, Vermeiren, Joan, Antoine, Jean-Michel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5847024/
https://www.ncbi.nlm.nih.gov/pubmed/29086061
http://dx.doi.org/10.1007/s00394-017-1546-4
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author Shortt, Colette
Hasselwander, Oliver
Meynier, Alexandra
Nauta, Arjen
Fernández, Estefanía Noriega
Putz, Peter
Rowland, Ian
Swann, Jonathan
Türk, Jessica
Vermeiren, Joan
Antoine, Jean-Michel
author_facet Shortt, Colette
Hasselwander, Oliver
Meynier, Alexandra
Nauta, Arjen
Fernández, Estefanía Noriega
Putz, Peter
Rowland, Ian
Swann, Jonathan
Türk, Jessica
Vermeiren, Joan
Antoine, Jean-Michel
author_sort Shortt, Colette
collection PubMed
description PURPOSE: There is considerable interest in the effects of the intestinal microbiota (IM) composition, its activities in relation with the metabolism of dietary substrates and the impact these effects may have in the development and prevention of certain non-communicable diseases. It is acknowledged that a complex interdependence exists between the IM and the mammalian host and that the IM possesses a far greater diversity of genes and repertoire of metabolic and enzymatic capabilities than their hosts. However, full knowledge of the metabolic activities and interactions of the IM and the functional redundancy that may exist are lacking. Thus, the current review aims to assess recent literature relating to the role played by the IM in the absorption and metabolism of key nutrients and non-nutrients. METHODS: A systematic review (PROSPERO registration: CRD42015019087) was carried out focussing on energy and the following candidate dietary substrates: protein, carbohydrate, fat, fibre, resistant starch (RS), and polyphenols to further understand the effect of the IM on the dietary substrates and the resulting by-products and host impacts. Particular attention was paid to the characterisation of the IM which are predominantly implicated in each case, changes in metabolites, and indirect markers and any potential impacts on the host. RESULTS: Studies show that the IM plays a key role in the metabolism of the substrates studied. However, with the exception of studies focusing on fibre and polyphenols, there have been relatively few recent human studies specifically evaluating microbial metabolism. In addition, comparison of the effects of the IM across studies was difficult due to lack of specific analysis/description of the bacteria involved. Considerable animal-derived data exist, but experience suggests that care must be taken when extrapolating these results to humans. Nevertheless, it appears that the IM plays a role in energy homeostasis and that protein microbial breakdown and fermentation produced ammonia, amines, phenols and branch chain fatty acids, and a greater diversity in the microbes present. Few recent studies appear to have evaluated the effect of the IM composition and metabolism per se in relation with digestible dietary carbohydrate or fat in humans. Intakes of RS and prebiotics altered levels of specific taxa that selectively metabolised specific prebiotic/carbohydrate-type substances and levels of bifidobacteria and lactobacilli were observed to increase. In controlled human studies, consistent data exist that show a correlation between the intake of fibre and an increase in bifidobacteria and short-chain fatty acids, in particular butyrate, which leads to lower intestinal pH. Dietary polyphenols rely on modification either by host digestive enzymes or those derived from the IM for absorption to occur. In the polyphenol-related studies, a large amount of inter-individual variation was observed in the microbial metabolism and absorption of certain polyphenols. CONCLUSIONS: The systematic review demonstrates that the IM plays a major role in the breakdown and transformation of the dietary substrates examined. However, recent human data are limited with the exception of data from studies examining fibres and polyphenols. Results observed in relation with dietary substrates were not always consistent or coherent across studies and methodological limitations and differences in IM analyses made comparisons difficult. Moreover, non-digestible components likely to reach the colon are often not well defined or characterised in studies making comparisons between studies difficult if not impossible. Going forward, further rigorously controlled randomised human trials with well-defined dietary substrates and utilizing omic-based technologies to characterise and measure the IM and their functional activities will advance the field. Current evidence suggests that more detailed knowledge of the metabolic activities and interactions of the IM hold considerable promise in relation with host health.
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spelling pubmed-58470242018-03-20 Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients Shortt, Colette Hasselwander, Oliver Meynier, Alexandra Nauta, Arjen Fernández, Estefanía Noriega Putz, Peter Rowland, Ian Swann, Jonathan Türk, Jessica Vermeiren, Joan Antoine, Jean-Michel Eur J Nutr Review PURPOSE: There is considerable interest in the effects of the intestinal microbiota (IM) composition, its activities in relation with the metabolism of dietary substrates and the impact these effects may have in the development and prevention of certain non-communicable diseases. It is acknowledged that a complex interdependence exists between the IM and the mammalian host and that the IM possesses a far greater diversity of genes and repertoire of metabolic and enzymatic capabilities than their hosts. However, full knowledge of the metabolic activities and interactions of the IM and the functional redundancy that may exist are lacking. Thus, the current review aims to assess recent literature relating to the role played by the IM in the absorption and metabolism of key nutrients and non-nutrients. METHODS: A systematic review (PROSPERO registration: CRD42015019087) was carried out focussing on energy and the following candidate dietary substrates: protein, carbohydrate, fat, fibre, resistant starch (RS), and polyphenols to further understand the effect of the IM on the dietary substrates and the resulting by-products and host impacts. Particular attention was paid to the characterisation of the IM which are predominantly implicated in each case, changes in metabolites, and indirect markers and any potential impacts on the host. RESULTS: Studies show that the IM plays a key role in the metabolism of the substrates studied. However, with the exception of studies focusing on fibre and polyphenols, there have been relatively few recent human studies specifically evaluating microbial metabolism. In addition, comparison of the effects of the IM across studies was difficult due to lack of specific analysis/description of the bacteria involved. Considerable animal-derived data exist, but experience suggests that care must be taken when extrapolating these results to humans. Nevertheless, it appears that the IM plays a role in energy homeostasis and that protein microbial breakdown and fermentation produced ammonia, amines, phenols and branch chain fatty acids, and a greater diversity in the microbes present. Few recent studies appear to have evaluated the effect of the IM composition and metabolism per se in relation with digestible dietary carbohydrate or fat in humans. Intakes of RS and prebiotics altered levels of specific taxa that selectively metabolised specific prebiotic/carbohydrate-type substances and levels of bifidobacteria and lactobacilli were observed to increase. In controlled human studies, consistent data exist that show a correlation between the intake of fibre and an increase in bifidobacteria and short-chain fatty acids, in particular butyrate, which leads to lower intestinal pH. Dietary polyphenols rely on modification either by host digestive enzymes or those derived from the IM for absorption to occur. In the polyphenol-related studies, a large amount of inter-individual variation was observed in the microbial metabolism and absorption of certain polyphenols. CONCLUSIONS: The systematic review demonstrates that the IM plays a major role in the breakdown and transformation of the dietary substrates examined. However, recent human data are limited with the exception of data from studies examining fibres and polyphenols. Results observed in relation with dietary substrates were not always consistent or coherent across studies and methodological limitations and differences in IM analyses made comparisons difficult. Moreover, non-digestible components likely to reach the colon are often not well defined or characterised in studies making comparisons between studies difficult if not impossible. Going forward, further rigorously controlled randomised human trials with well-defined dietary substrates and utilizing omic-based technologies to characterise and measure the IM and their functional activities will advance the field. Current evidence suggests that more detailed knowledge of the metabolic activities and interactions of the IM hold considerable promise in relation with host health. Springer Berlin Heidelberg 2017-10-30 2018 /pmc/articles/PMC5847024/ /pubmed/29086061 http://dx.doi.org/10.1007/s00394-017-1546-4 Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
spellingShingle Review
Shortt, Colette
Hasselwander, Oliver
Meynier, Alexandra
Nauta, Arjen
Fernández, Estefanía Noriega
Putz, Peter
Rowland, Ian
Swann, Jonathan
Türk, Jessica
Vermeiren, Joan
Antoine, Jean-Michel
Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients
title Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients
title_full Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients
title_fullStr Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients
title_full_unstemmed Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients
title_short Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients
title_sort systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients
topic Review
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5847024/
https://www.ncbi.nlm.nih.gov/pubmed/29086061
http://dx.doi.org/10.1007/s00394-017-1546-4
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