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Omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation

BACKGROUND: Irritable bowel syndrome (IBS) is a disorder of gut–brain interaction, including dysregulation of the hypothalamic–pituitary–adrenal axis with salivary cortisol changes. However, the role of gastrointestinal microbiota during IBS symptom exacerbation remains unclear. We tested the hypoth...

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Autores principales: Tanaka, Yukari, Yamashita, Riu, Kawashima, Junko, Mori, Hiroshi, Kurokawa, Ken, Fukuda, Shinji, Gotoh, Yasuhiro, Nakamura, Keiji, Hayashi, Tetsuya, Kasahara, Yoshiyuki, Sato, Yukuto, Fukudo, Shin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Nature Singapore 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9522833/
https://www.ncbi.nlm.nih.gov/pubmed/35908139
http://dx.doi.org/10.1007/s00535-022-01888-2
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author Tanaka, Yukari
Yamashita, Riu
Kawashima, Junko
Mori, Hiroshi
Kurokawa, Ken
Fukuda, Shinji
Gotoh, Yasuhiro
Nakamura, Keiji
Hayashi, Tetsuya
Kasahara, Yoshiyuki
Sato, Yukuto
Fukudo, Shin
author_facet Tanaka, Yukari
Yamashita, Riu
Kawashima, Junko
Mori, Hiroshi
Kurokawa, Ken
Fukuda, Shinji
Gotoh, Yasuhiro
Nakamura, Keiji
Hayashi, Tetsuya
Kasahara, Yoshiyuki
Sato, Yukuto
Fukudo, Shin
author_sort Tanaka, Yukari
collection PubMed
description BACKGROUND: Irritable bowel syndrome (IBS) is a disorder of gut–brain interaction, including dysregulation of the hypothalamic–pituitary–adrenal axis with salivary cortisol changes. However, the role of gastrointestinal microbiota during IBS symptom exacerbation remains unclear. We tested the hypothesis that the microbial species, gene transcripts, and chemical composition of fecal and oral samples are altered during the exacerbation of IBS symptoms. METHODS: Fecal, salivary, and dental plaque samples were collected at baseline from 43 men with IBS with diarrhea (IBS-D) and 40 healthy control (HC) men. Samples in the IBS-D patients were also collected during symptom exacerbation. The composition of the fecal microbiota was determined by analyzing the 16S rRNA gene, RNA-based metatranscriptome, and metabolites in samples from HC and IBS patients with and without symptom exacerbation. Oral samples were also analyzed using omics approaches. RESULTS: The fecal microbiota during IBS symptom exacerbation exhibited significant differences in the phylogenic pattern and short-chain fatty acid compared with fecal samples during defecation when symptoms were not exacerbated. Although there were no significant differences in the phylogenic pattern of fecal microbiota abundance between HCs and IBS-D patients, significant differences were detected in the expression patterns of bacterial transcriptomes related to butyrate production and neuroendocrine hormones, including tryptophan-serotonin-melatonin synthesis and glutamine/GABA. The composition of plaque microbiota was different between HC and IBS-D patients during normal defecation. CONCLUSIONS: Our findings suggest that colonic host-microbial interactions are altered in IBS-D patients during exacerbation of symptoms. There were no overlaps between feces and oral microbiomes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00535-022-01888-2.
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spelling pubmed-95228332022-10-01 Omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation Tanaka, Yukari Yamashita, Riu Kawashima, Junko Mori, Hiroshi Kurokawa, Ken Fukuda, Shinji Gotoh, Yasuhiro Nakamura, Keiji Hayashi, Tetsuya Kasahara, Yoshiyuki Sato, Yukuto Fukudo, Shin J Gastroenterol Original Article—Alimentary Tract BACKGROUND: Irritable bowel syndrome (IBS) is a disorder of gut–brain interaction, including dysregulation of the hypothalamic–pituitary–adrenal axis with salivary cortisol changes. However, the role of gastrointestinal microbiota during IBS symptom exacerbation remains unclear. We tested the hypothesis that the microbial species, gene transcripts, and chemical composition of fecal and oral samples are altered during the exacerbation of IBS symptoms. METHODS: Fecal, salivary, and dental plaque samples were collected at baseline from 43 men with IBS with diarrhea (IBS-D) and 40 healthy control (HC) men. Samples in the IBS-D patients were also collected during symptom exacerbation. The composition of the fecal microbiota was determined by analyzing the 16S rRNA gene, RNA-based metatranscriptome, and metabolites in samples from HC and IBS patients with and without symptom exacerbation. Oral samples were also analyzed using omics approaches. RESULTS: The fecal microbiota during IBS symptom exacerbation exhibited significant differences in the phylogenic pattern and short-chain fatty acid compared with fecal samples during defecation when symptoms were not exacerbated. Although there were no significant differences in the phylogenic pattern of fecal microbiota abundance between HCs and IBS-D patients, significant differences were detected in the expression patterns of bacterial transcriptomes related to butyrate production and neuroendocrine hormones, including tryptophan-serotonin-melatonin synthesis and glutamine/GABA. The composition of plaque microbiota was different between HC and IBS-D patients during normal defecation. CONCLUSIONS: Our findings suggest that colonic host-microbial interactions are altered in IBS-D patients during exacerbation of symptoms. There were no overlaps between feces and oral microbiomes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00535-022-01888-2. Springer Nature Singapore 2022-07-30 2022 /pmc/articles/PMC9522833/ /pubmed/35908139 http://dx.doi.org/10.1007/s00535-022-01888-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article—Alimentary Tract
Tanaka, Yukari
Yamashita, Riu
Kawashima, Junko
Mori, Hiroshi
Kurokawa, Ken
Fukuda, Shinji
Gotoh, Yasuhiro
Nakamura, Keiji
Hayashi, Tetsuya
Kasahara, Yoshiyuki
Sato, Yukuto
Fukudo, Shin
Omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation
title Omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation
title_full Omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation
title_fullStr Omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation
title_full_unstemmed Omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation
title_short Omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation
title_sort omics profiles of fecal and oral microbiota change in irritable bowel syndrome patients with diarrhea and symptom exacerbation
topic Original Article—Alimentary Tract
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9522833/
https://www.ncbi.nlm.nih.gov/pubmed/35908139
http://dx.doi.org/10.1007/s00535-022-01888-2
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