Effects of FODMAPs and Gluten on Gut Microbiota and Their Association with the Metabolome in Irritable Bowel Syndrome: A Double-Blind, Randomized, Cross-Over Intervention Study.
FODMAPs
SCFAs
gluten
gut microbiota
irritable bowel syndrome
metabolome
multiomics
Journal
Nutrients
ISSN: 2072-6643
Titre abrégé: Nutrients
Pays: Switzerland
ID NLM: 101521595
Informations de publication
Date de publication:
05 Jul 2023
05 Jul 2023
Historique:
received:
11
05
2023
revised:
30
06
2023
accepted:
30
06
2023
medline:
17
7
2023
pubmed:
14
7
2023
entrez:
14
7
2023
Statut:
epublish
Résumé
A mechanistic understanding of the effects of dietary treatment in irritable bowel syndrome (IBS) is lacking. Our aim was therefore to investigate how fermentable oligo- di-, monosaccharides, and polyols (FODMAPs) and gluten affected gut microbiota and circulating metabolite profiles, as well as to investigate potential links between gut microbiota, metabolites, and IBS symptoms. We used data from a double-blind, randomized, crossover study with week-long provocations of FODMAPs, gluten, and placebo in participants with IBS. To study the effects of the provocations on fecal microbiota, fecal and plasma short-chain fatty acids, the untargeted plasma metabolome, and IBS symptoms, we used Random Forest, linear mixed model and Spearman correlation analysis. FODMAPs increased fecal saccharolytic bacteria, plasma phenolic-derived metabolites, 3-indolepropionate, and decreased isobutyrate and bile acids. Gluten decreased fecal isovalerate and altered carnitine derivatives, CoA, and fatty acids in plasma. For FODMAPs, modest correlations were observed between microbiota and phenolic-derived metabolites and 3-indolepropionate, previously associated with improved metabolic health, and reduced inflammation. Correlations between molecular data and IBS symptoms were weak. FODMAPs, but not gluten, altered microbiota composition and correlated with phenolic-derived metabolites and 3-indolepropionate, with only weak associations with IBS symptoms. Thus, the minor effect of FODMAPs on IBS symptoms must be weighed against the effect on microbiota and metabolites related to positive health factors.
Sections du résumé
BACKGROUND
BACKGROUND
A mechanistic understanding of the effects of dietary treatment in irritable bowel syndrome (IBS) is lacking. Our aim was therefore to investigate how fermentable oligo- di-, monosaccharides, and polyols (FODMAPs) and gluten affected gut microbiota and circulating metabolite profiles, as well as to investigate potential links between gut microbiota, metabolites, and IBS symptoms.
METHODS
METHODS
We used data from a double-blind, randomized, crossover study with week-long provocations of FODMAPs, gluten, and placebo in participants with IBS. To study the effects of the provocations on fecal microbiota, fecal and plasma short-chain fatty acids, the untargeted plasma metabolome, and IBS symptoms, we used Random Forest, linear mixed model and Spearman correlation analysis.
RESULTS
RESULTS
FODMAPs increased fecal saccharolytic bacteria, plasma phenolic-derived metabolites, 3-indolepropionate, and decreased isobutyrate and bile acids. Gluten decreased fecal isovalerate and altered carnitine derivatives, CoA, and fatty acids in plasma. For FODMAPs, modest correlations were observed between microbiota and phenolic-derived metabolites and 3-indolepropionate, previously associated with improved metabolic health, and reduced inflammation. Correlations between molecular data and IBS symptoms were weak.
CONCLUSIONS
CONCLUSIONS
FODMAPs, but not gluten, altered microbiota composition and correlated with phenolic-derived metabolites and 3-indolepropionate, with only weak associations with IBS symptoms. Thus, the minor effect of FODMAPs on IBS symptoms must be weighed against the effect on microbiota and metabolites related to positive health factors.
Identifiants
pubmed: 37447371
pii: nu15133045
doi: 10.3390/nu15133045
pmc: PMC10346910
pii:
doi:
Substances chimiques
Glutens
8002-80-0
Oligosaccharides
0
Types de publication
Randomized Controlled Trial
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Swedish Research Council
ID : 2019-01264
Organisme : Swedish Research Council
ID : 2017-05840
Organisme : Swedish Research Council for Environment Agricultural Sciences and Spatial Planning
ID : 2016-00314
Références
Int J Tryptophan Res. 2020 Jun 11;13:1178646920928984
pubmed: 32577079
World J Gastroenterol. 2015 Aug 7;21(29):8787-803
pubmed: 26269668
Mutat Res. 2005 Jan;589(1):47-65
pubmed: 15652226
Future Microbiol. 2017 Feb;12:157-170
pubmed: 28139139
Aliment Pharmacol Ther. 1997 Apr;11(2):395-402
pubmed: 9146781
Br J Nutr. 2009 Feb;101(4):541-50
pubmed: 18590586
F1000Res. 2018 Jul 9;7:
pubmed: 30026921
Aliment Pharmacol Ther. 2002 Apr;16(4):759-67
pubmed: 11929394
Nat Commun. 2022 Sep 23;13(1):5370
pubmed: 36151114
Nat Commun. 2018 Aug 17;9(1):3294
pubmed: 30120222
Gastroenterology. 2019 Jul;157(1):97-108
pubmed: 30940523
Methods. 2018 Oct 1;149:3-12
pubmed: 29715508
Nutrients. 2020 Nov 10;12(11):
pubmed: 33182700
Nat Commun. 2018 Nov 13;9(1):4630
pubmed: 30425247
Gastroenterol Hepatol (N Y). 2017 Jan;13(1):36-45
pubmed: 28420945
Nutr Diabetes. 2018 May 25;8(1):35
pubmed: 29795366
Nat Methods. 2016 Jul;13(7):581-3
pubmed: 27214047
Sci Rep. 2019 Mar 20;9(1):4736
pubmed: 30894560
PLoS One. 2013 Apr 22;8(4):e61217
pubmed: 23630581
Nat Rev Gastroenterol Hepatol. 2015 Aug;12(8):472-85
pubmed: 26194942
Arq Gastroenterol. 2014 Apr-Jun;51(2):139-43
pubmed: 25003267
Clin Nutr. 2019 Apr;38(2):697-707
pubmed: 29653862
Nature. 2017 Nov 30;551(7682):648-652
pubmed: 29168502
Nutrients. 2022 Apr 17;14(8):
pubmed: 35458231
Nature. 2008 Sep 25;455(7212):481-3
pubmed: 18818648
J Appl Bacteriol. 1992 Jan;72(1):57-64
pubmed: 1541601
Sci Rep. 2021 Nov 10;11(1):21602
pubmed: 34759297
Br J Nutr. 1999 Feb;81(2):121-32
pubmed: 10450330
Appl Environ Microbiol. 2007 Aug;73(16):5261-7
pubmed: 17586664
Gut. 2017 Nov;66(11):1968-1974
pubmed: 28213610
Neurogastroenterol Motil. 2017 Apr;29(4):
pubmed: 27747984
Mol Nutr Food Res. 2009 May;53 Suppl 1:S68-75
pubmed: 19415668
Neurogastroenterol Motil. 2008 Dec;20(12):1291-7
pubmed: 18823288
Mol Nutr Food Res. 2018 Jan;62(2):
pubmed: 29024323
J Am Heart Assoc. 2020 Sep 15;9(18):e016518
pubmed: 32893710
Am J Gastroenterol. 2018 Sep;113(9):1290-1300
pubmed: 30046155
Am J Clin Nutr. 2020 Apr 1;111(4):864-876
pubmed: 32097450
Nat Rev Endocrinol. 2014 Feb;10(2):74-6
pubmed: 24322652
Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6
pubmed: 23193283
Cell. 2018 Mar 8;172(6):1198-1215
pubmed: 29522742
Compr Rev Food Sci Food Saf. 2022 Sep;21(5):3931-3962
pubmed: 36037277
Nat Genet. 2018 Jun;50(6):790-795
pubmed: 29808030
Metabolomics. 2010 Mar;6(1):119-128
pubmed: 20339442
Nat Rev Microbiol. 2021 Feb;19(2):77-94
pubmed: 32968241
Gastroenterology. 2018 Feb;154(3):529-539.e2
pubmed: 29102613
J Med Chem. 2009 May 14;52(9):2786-93
pubmed: 19338303
Sci Rep. 2021 Jul 7;11(1):13964
pubmed: 34234185
Gastroenterology. 2014 Jan;146(1):67-75.e5
pubmed: 24076059
Int J Mol Sci. 2022 Jan 22;23(3):
pubmed: 35163143
Nat Rev Microbiol. 2021 Jan;19(1):55-71
pubmed: 32887946
Front Microbiol. 2016 Feb 17;7:185
pubmed: 26925050
Eur J Nutr. 2012 Apr;51(3):293-9
pubmed: 21671042
J Agric Food Chem. 2020 Nov 4;68(44):12295-12309
pubmed: 33095019
Br J Nutr. 2020 Nov 14;124(9):931-942
pubmed: 32475373
Clin Nutr ESPEN. 2022 Feb;47:45-50
pubmed: 35063241
Am J Physiol Gastrointest Liver Physiol. 2022 Jun 1;322(6):G535-G552
pubmed: 35271353
Med Care. 1992 Jun;30(6):473-83
pubmed: 1593914
Aliment Pharmacol Ther. 2020 Jul;52(2):233-246
pubmed: 32562590
Scand J Gastroenterol. 1997 Sep;32(9):920-4
pubmed: 9299672
J Travel Med. 2015 Jul-Aug;22(4):242-50
pubmed: 26058758
Gut. 2017 Aug;66(8):1517-1527
pubmed: 28592442
Digestion. 2016;94(1):50-6
pubmed: 27487397
Bioinform Biol Insights. 2020 Jan 31;14:1177932219899051
pubmed: 32076369
Cancers (Basel). 2021 Aug 04;13(16):
pubmed: 34439088
J Nutr. 2012 Aug;142(8):1510-8
pubmed: 22739368
Gut. 1987 Oct;28(10):1221-7
pubmed: 3678950
Mol Med Rep. 2012 Dec;6(6):1223-5
pubmed: 22992886
Front Biosci (Elite Ed). 2012 Jun 01;4(8):2783-800
pubmed: 22652678
J Physiol Pharmacol. 2011 Dec;62(6):591-9
pubmed: 22314561
Am J Clin Nutr. 2022 Oct 6;116(4):943-952
pubmed: 35728042
BMC Biol. 2019 Oct 28;17(1):83
pubmed: 31660948
United European Gastroenterol J. 2015 Apr;3(2):160-5
pubmed: 25922675
Am J Gastroenterol. 2011 Mar;106(3):508-14; quiz 515
pubmed: 21224837
FEBS J. 2020 Mar;287(5):856-865
pubmed: 31709683
Bioinformatics. 2019 Mar 15;35(6):972-980
pubmed: 30165467
Genome Med. 2016 Apr 21;8(1):45
pubmed: 27102333
Gut. 2018 Feb;67(2):263-270
pubmed: 27872184
Eur J Nutr. 2020 Aug;59(5):1845-1858
pubmed: 31273523
Adv Nutr. 2020 May 1;11(3):709-723
pubmed: 31825083
Gut. 2015 Jan;64(1):93-100
pubmed: 25016597
Am J Physiol Regul Integr Comp Physiol. 2023 Jul 3;:
pubmed: 37399002
Am J Clin Nutr. 2022 Feb 9;115(2):344-352
pubmed: 34617561
BMC Gastroenterol. 2023 May 12;23(1):150
pubmed: 37173627
Gastroenterology. 2016 Feb 19;:
pubmed: 27144617
Anaerobe. 2019 Feb;55:67-77
pubmed: 30396006
Expert Rev Gastroenterol Hepatol. 2018 May;12(5):439-445
pubmed: 29493330
Proc Natl Acad Sci U S A. 2017 Jan 17;114(3):E367-E375
pubmed: 28049818
PLoS One. 2018 Jul 26;13(7):e0201410
pubmed: 30048547
J Mol Diagn. 2019 May;21(3):449-461
pubmed: 31005411
Nutrients. 2021 May 13;13(5):
pubmed: 34068353
Gut. 2017 Jul;66(7):1241-1251
pubmed: 26976734