Exploration of associations among dietary tryptophan, microbiome composition and function, and symptom severity in irritable bowel syndrome.
diet
gastrointestinal microbiome
irritable bowel syndrome
tryptophan
Journal
Neurogastroenterology and motility
ISSN: 1365-2982
Titre abrégé: Neurogastroenterol Motil
Pays: England
ID NLM: 9432572
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
revised:
30
12
2022
received:
15
07
2022
accepted:
24
01
2023
medline:
26
4
2023
pubmed:
14
2
2023
entrez:
13
2
2023
Statut:
ppublish
Résumé
Imbalance of the tryptophan (TRP) pathway may influence symptoms among patients with irritable bowel syndrome (IBS). This study explored relationships among different components that contribute to TRP metabolism (dietary intake, stool metabolite levels, predicted microbiome metabolic capability) in females with IBS and healthy controls (HCs). Within the IBS group, we also investigated relationships between TRP metabolic determinants, Bifidobacterium abundance, and symptoms of IBS. Participants with IBS (Rome III) and HCs completed a 28-day diary of gastrointestinal symptoms and a 3-day food record for TRP intake. They provided a stool sample for shotgun metagenomics, 16 S rRNA analyses, and quantitative measurement of TRP by mass spectrometry. Our cohort included 115 females, 69 with IBS and 46 HCs, with a mean age of 28.5 years (SD 7.4). TRP intake (p = 0.71) and stool TRP level (p = 0.27) did not differ between IBS and HC. Bifidobacterium abundance was lower in the IBS group than in HCs (p = 0.004). Predicted TRP metabolism gene content was higher in IBS than HCs (FDR-corrected q = 0.006), whereas predicted biosynthesis gene content was lower (q = 0.045). Within the IBS group, there was no association between symptom severity and TRP intake or stool TRP, but there was a significant interaction between Bifidobacterium abundance and TRP intake (q = 0.029) in predicting stool character. Dietary TRP intake, microbiome composition, and differences in TRP metabolism constitute a complex interplay of factors that could modulate IBS symptom severity.
Sections du résumé
BACKGROUND
Imbalance of the tryptophan (TRP) pathway may influence symptoms among patients with irritable bowel syndrome (IBS). This study explored relationships among different components that contribute to TRP metabolism (dietary intake, stool metabolite levels, predicted microbiome metabolic capability) in females with IBS and healthy controls (HCs). Within the IBS group, we also investigated relationships between TRP metabolic determinants, Bifidobacterium abundance, and symptoms of IBS.
METHODS
Participants with IBS (Rome III) and HCs completed a 28-day diary of gastrointestinal symptoms and a 3-day food record for TRP intake. They provided a stool sample for shotgun metagenomics, 16 S rRNA analyses, and quantitative measurement of TRP by mass spectrometry.
RESULTS
Our cohort included 115 females, 69 with IBS and 46 HCs, with a mean age of 28.5 years (SD 7.4). TRP intake (p = 0.71) and stool TRP level (p = 0.27) did not differ between IBS and HC. Bifidobacterium abundance was lower in the IBS group than in HCs (p = 0.004). Predicted TRP metabolism gene content was higher in IBS than HCs (FDR-corrected q = 0.006), whereas predicted biosynthesis gene content was lower (q = 0.045). Within the IBS group, there was no association between symptom severity and TRP intake or stool TRP, but there was a significant interaction between Bifidobacterium abundance and TRP intake (q = 0.029) in predicting stool character.
CONCLUSIONS
Dietary TRP intake, microbiome composition, and differences in TRP metabolism constitute a complex interplay of factors that could modulate IBS symptom severity.
Substances chimiques
Tryptophan
8DUH1N11BX
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
e14545Subventions
Organisme : NIDDK NIH HHS
ID : P30 DK035816
Pays : United States
Organisme : NINR NIH HHS
ID : T32 NR016913
Pays : United States
Organisme : NINR NIH HHS
ID : K23 NR020044
Pays : United States
Organisme : NINR NIH HHS
ID : R01 NR014479
Pays : United States
Organisme : NIAID NIH HHS
ID : P01 AI152999
Pays : United States
Organisme : NIAID NIH HHS
ID : U01 AI042590
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK130517
Pays : United States
Organisme : NINR NIH HHS
ID : R01 NR013497
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK056338
Pays : United States
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Chey WD, Kurlander J, Eswaran S. Irritable bowel syndrome: a clinical review. JAMA. 2015;313(9):949-958. doi:10.1001/jama.2015.0954
Canavan C, West J, Card T. Review article: the economic impact of the irritable bowel syndrome. Aliment Pharmacol Ther. 2014;40(9):1023-1034. doi:10.1111/apt.12938
Sperber AD, Bangdiwala SI, Drossman DA, et al. Worldwide prevalence and burden of functional gastrointestinal disorders, results of Rome foundation global study. Gastroenterology. 2021;160(1):99-114. doi:10.1053/j.gastro.2020.04.014
Gao K, Mu CL, Farzi A, Zhu WY. Tryptophan metabolism: a link between the gut microbiota and brain. Adv Nutr. 2020;11(3):709-723. doi:10.1093/advances/nmz127
Lee JS, Kim S-Y, Chun YS, et al. Characteristics of fecal metabolic profiles in patients with irritable bowel syndrome with predominant diarrhea investigated using 1H-NMR coupled with multivariate statistical analysis. Neurogastroenterol Motil. 2020;32(6):e13830. doi:10.1111/nmo.13830
Xiao L, Liu Q, Luo M, Xiong L. Gut microbiota-derived metabolites in irritable bowel syndrome. Front Cell Infect Microbiol. 2021;11:729346. doi:10.3389/fcimb.2021.729346
Heitkemper MM, Han CJ, Jarrett ME, et al. Serum tryptophan metabolite levels during sleep in patients with and without irritable bowel syndrome (IBS). Biol Res Nurs. 2016;18(2):193-198. doi:10.1177/1099800415594251
Osadchiy V, Mayer EA, Gao K, et al. Analysis of brain networks and fecal metabolites reveals brain-gut alterations in premenopausal females with irritable bowel syndrome. Transl Psychiatry. 2020;10(1):367. doi:10.1038/s41398-020-01071-2
Christmas DM, Badawy AA, Hince D, et al. Increased serum free tryptophan in patients with diarrhea-predominant irritable bowel syndrome. Nutr Res. 2010;30(10):678-688. doi:10.1016/j.nutres.2010.09.009
Bosi A, Banfi D, Bistoletti M, Giaroni C, Baj A. Tryptophan metabolites along the microbiota-gut-brain axis: an interkingdom communication system influencing the gut in health and disease. Int J Tryptophan Res. 2020;13:1-25. doi:10.1177/1178646920928984
Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG. The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res. 2008;43(2):164-174. doi:10.1016/j.jpsychires.2008.03.009
Carabotti M, Scirocco A, Maselli MA, Severi C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol. 2015;28(2):203-209.
Tian P, Wang G, Zhao J, Zhang H, Chen W. Bifidobacterium with the role of 5-hydroxytryptophan synthesis regulation alleviates the symptom of depression and related microbiota dysbiosis. J Nutr Biochem. 2019;66:43-51. doi:10.1016/j.jnutbio.2019.01.007
Kim J, Cho K, Kim JS, et al. Probiotic treatment induced change of inflammation related metabolites in IBS-D patients/double-blind, randomized, placebo-controlled trial. Food Sci Biotechnol. 2020;29(6):837-844. doi:10.1007/s10068-019-00717-2
Burr RL, Gu H, Cain K, et al. Tryptophan metabolites in irritable bowel syndrome: an overnight time-course study. J Neurogastroenterol Motil. 2019;25(4):551-562. doi:10.5056/jnm19042
Han L, Zhao L, Zhou Y, et al. Altered metabolome and microbiome features provide clues in understanding irritable bowel syndrome and depression comorbidity. ISME J. 2022;16(4):983-996. doi:10.1038/s41396-021-01123-5
Shi J, Zhao D, Zhao F, Wang C, Zamaratskaia G, Li C. (2021). Chicken-eaters and pork-eaters have different gut microbiota and tryptophan metabolites. Sci Rep. 2021;11(1):1-10. doi:10.1038/s41598-021-91429-3
Agazzi A, De Ponti F, De Giorgio R, et al. Review of the implications of dietary tryptophan intake in patients with irritable bowel syndrome and psychiatric disorders. Dig Liver Dis. 2003;35(8):590-595. doi:10.1016/s1590-8658(03)00277-9
Daskova N, Heczkova M, Modos I, et al. Determination of butyrate synthesis capacity in gut microbiota: quantification of but gene abundance by qPCR in fecal samples. Biomolecules. 2021;11(9):1303. doi:10.3390/biom11091303
Kamp KJ, Cain KC, Utleg A, et al. Bile acids and microbiome among individuals with irritable bowel syndrome and healthy volunteers. Biol Res Nurs. 2021;23(1):65-74. doi:10.1177/1099800420941255
Kamp KJ, Han C, Shulman RJ, et al. Cytokine levels and symptoms among women with irritable bowel syndrome: considering the role of hormonal contraceptive use. Biol Res Nurs. 2021;23(3):171-179. doi:10.1177/1099800420941252
Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC. Functional bowel disorders. Gastroenterology. 2006;130(5):1480-1491.
Hrboticky N, Leiter LA, Anderson GH. Menstrual cycle effects on the metabolism of tryptophan loads. Am J Clin Nutr. 1989;50(1):46-52. doi:10.1093/ajcn/50.1.46
Han CJ, Pike K, Jarrett ME, Heitkemper MM. Symptom-based latent classes of persons with irritable bowel syndrome. Res Nurs Health. 2019;42(5):382-391. doi:10.1002/nur.21974
MacLean B, Tomazela DM, Shulman N, et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics. 2010;26(7):966-968. doi:10.1093/bioinformatics/btq054
Aagaard K, Petrosino J, Keitel W, et al. The human microbiome project strategy for comprehensive sampling of the human microbiome and why it matters. FASEB J. 2013;27(3):1012-1022. doi:10.1096/fj.12-220806
Hildebrand F, Tadeo R, Voigt AY, Bork P, Raes J. LotuS: an efficient and user-friendly OTU processing pipeline. Microbiome. 2014;2(1):30. doi:10.1186/2049-2618-2-30
Hollister EB, Cain KC, Shulman RJ, et al. Relationships of microbiome markers with extraintestinal, psychological distress and gastrointestinal symptoms, and quality of life in women with irritable bowel syndrome. J Clin Gastroenterol. 2020;54(2):175-183. doi:10.1097/mcg.0000000000001107
Truong DT, Franzosa EA, Tickle TL, et al. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods. 2015;12(10):902-903. doi:10.1038/nmeth.3589
Franzosa EA, McIver LJ, Rahnavard G, et al. Species-level functional profiling of metagenomes and metatranscriptomes. Nat Methods. 2018;15(11):962-968. doi:10.1038/s41592-018-0176-y
Wemheuer F, Taylor JA, Daniel R, et al. Tax4Fun2: prediction of habitat-specific functional profiles and functional redundancy based on 16 S rRNA gene sequences. Environ Microbiome. 2020;15(1):11. doi:10.1186/s40793-020-00358-7
Djemiel C, Maron PA, Terrat S, Dequiedt S, Cottin A, Ranjard L. Inferring microbiota functions from taxonomic genes: a review. Gigascience. 2022;11(1):giab090. doi:10.1093/gigascience/giab090
Zhuang X, Xiong L, Li L, Li M, Chen M. Alterations of gut microbiota in patients with irritable bowel syndrome: a systematic review and meta-analysis. J Gastroenterol Hepatol. 2017;32(1):28-38. doi:10.1111/jgh.13471
Wang L, Alammar N, Singh R, et al. Gut microbial dysbiosis in the irritable bowel syndrome: a systematic review and meta-analysis of case-control studies. J Acad Nutr Diet. 2020;120(4):565-586. doi:10.1016/j.jand.2019.05.015
Kerckhoffs APM, Samsom M, van der Rest ME, et al. Lower Bifidobacteria counts in both duodenal mucosa-associated and fecal microbiota in irritable bowel syndrome patients. World J Gastroenterol. 2009;15(23):2887-2892. doi:10.3748/wjg.15.2887
Mazzawi T, Lied GA, Sangnes DA, et al. The kinetics of gut microbial community composition in patients with irritable bowel syndrome following fecal microbiota transplantation. PLoS One. 2018;13(11):e0194904. doi:10.1371/journal.pone.0194904
Fan YJ, Chen SJ, Yu YC, Si JM, Liu B. A probiotic treatment containing lactobacillus, Bifidobacterium and Enterococcus improves IBS symptoms in an open label trial. J Zhejiang Univ Sci B. 2006;7(12):987-991. doi:10.1631/jzus.2006.B0987
Whorwell PJ, Altringer L, Morel J, et al. Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome. Am J Gastroenterol. 2006;101(7):1581-1590. doi:10.1111/j.1572-0241.2006.00734.x
Guyonnet D, Chassany O, Ducrotte P, et al. Effect of a fermented milk containing Bifidobacterium animalis DN-173 010 on the health-related quality of life and symptoms in irritable bowel syndrome in adults in primary care: a multicentre, randomized, double-blind, controlled trial. Aliment Pharmacol Ther. 2007;26(3):475-486. doi:10.1111/j.1365-2036.2007.03362.x
Guglielmetti S, Mora D, Gschwender M, Popp K. Randomised clinical trial: Bifidobacterium bifidum MIMBb75 significantly alleviates irritable bowel syndrome and improves quality of life -- a double-blind, placebo-controlled study. Aliment Pharmacol Ther. 2011;33(10):1123-1132. doi:10.1111/j.1365-2036.2011.04633.x
Chojnacki C, Popławski T, Chojnacki J, Fila M, Konrad P, Blasiak J. Tryptophan intake and metabolism in older adults with mood disorders. Nutrients. 2020;12(10):3183. doi:10.3390/nu12103183
Iguacel I, Schmidt JA, Perez-Cornago A, et al. Associations between dietary amino acid intakes and blood concentration levels. Clin Nutr. 2021;40(6):3772-3779. doi:10.1016/j.clnu.2021.04.036
Zhang Y, Bhosle A, Bae S, et al. Discovery of bioactive microbial gene products in inflammatory bowel disease. Nature. 2022;606(7915):754-760. doi:10.1038/s41586-022-04648-7