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

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

Animals, Bacteria/metabolism, Dietary Carbohydrates/metabolism, Dietary Fats/metabolism, Dietary Fiber/metabolism, Dietary Proteins/metabolism, Digestion, Energy Metabolism, Food, Gastrointestinal Microbiome/physiology, Homeostasis, Humans, Isoflavones/metabolism, Polyphenols/metabolism, Starch/metabolism
1436-6207
25-49
Shortt, Colette
23ead2bb-7d1b-40cc-8afe-31b8bf2bdddb
Hasselwander, Oliver
c16f8955-e09d-41cb-811c-5469acd85cd4
Meynier, Alexandra
c8aed99e-f79c-4290-bfac-a6e3e4f9a1f3
Nauta, Arjen
8963e77f-0e63-4acb-ac34-44d85b8669d9
Fernández, Estefanía Noriega
f8f4f583-4fdc-48de-9b8c-cd0c7141ef94
Putz, Peter
a05e5c41-09d3-45d0-b78d-ce325d103355
Rowland, Ian
0cfbfdaf-648e-4e44-a59a-ddf708c2ebd0
Swann, Jonathan
7c11a66b-f4b8-4dbf-aa17-ad8b0561b85c
Türk, Jessica
186a5c02-77cb-4181-bc41-9d1dc456c9b3
Vermeiren, Joan
3944b1ed-bc74-419c-956a-c2604a3ab869
Antoine, Jean-Michel
bffa178d-7ddb-4c23-878c-89271ca8f5a4
Shortt, Colette
23ead2bb-7d1b-40cc-8afe-31b8bf2bdddb
Hasselwander, Oliver
c16f8955-e09d-41cb-811c-5469acd85cd4
Meynier, Alexandra
c8aed99e-f79c-4290-bfac-a6e3e4f9a1f3
Nauta, Arjen
8963e77f-0e63-4acb-ac34-44d85b8669d9
Fernández, Estefanía Noriega
f8f4f583-4fdc-48de-9b8c-cd0c7141ef94
Putz, Peter
a05e5c41-09d3-45d0-b78d-ce325d103355
Rowland, Ian
0cfbfdaf-648e-4e44-a59a-ddf708c2ebd0
Swann, Jonathan
7c11a66b-f4b8-4dbf-aa17-ad8b0561b85c
Türk, Jessica
186a5c02-77cb-4181-bc41-9d1dc456c9b3
Vermeiren, Joan
3944b1ed-bc74-419c-956a-c2604a3ab869
Antoine, Jean-Michel
bffa178d-7ddb-4c23-878c-89271ca8f5a4

Shortt, Colette, Hasselwander, Oliver, Meynier, Alexandra, Nauta, Arjen, Fernández, Estefanía Noriega, Putz, Peter, Rowland, Ian, Swann, Jonathan, Türk, Jessica, Vermeiren, Joan and Antoine, Jean-Michel (2018) Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients. European Journal of Nutrition, 57 (1), 25-49. (doi:10.1007/s00394-017-1546-4).

Record type: Review

Abstract

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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Shortt 2018 Article Systematic Review - Version of Record
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Accepted/In Press date: 20 September 2017
e-pub ahead of print date: 30 October 2017
Published date: February 2018
Keywords: Animals, Bacteria/metabolism, Dietary Carbohydrates/metabolism, Dietary Fats/metabolism, Dietary Fiber/metabolism, Dietary Proteins/metabolism, Digestion, Energy Metabolism, Food, Gastrointestinal Microbiome/physiology, Homeostasis, Humans, Isoflavones/metabolism, Polyphenols/metabolism, Starch/metabolism

Identifiers

Local EPrints ID: 440821
URI: http://eprints.soton.ac.uk/id/eprint/440821
ISSN: 1436-6207
PURE UUID: 3f717feb-a154-487d-9e9c-2ff5f3b9a9a3
ORCID for Jonathan Swann: ORCID iD orcid.org/0000-0002-6485-4529

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Date deposited: 19 May 2020 17:32
Last modified: 17 Mar 2024 04:00

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Contributors

Author: Colette Shortt
Author: Oliver Hasselwander
Author: Alexandra Meynier
Author: Arjen Nauta
Author: Estefanía Noriega Fernández
Author: Peter Putz
Author: Ian Rowland
Author: Jonathan Swann ORCID iD
Author: Jessica Türk
Author: Joan Vermeiren
Author: Jean-Michel Antoine

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