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Influence of cigarette smoking on the human duodenal mucosa-associated microbiota

BACKGROUND: Cigarette smoking is a known risk factor in a number of gastrointestinal (GI) diseases in which the microbiota is implicated, including duodenal ulcer and Crohn’s disease. Smoking has the potential to alter the microbiota; however, to date, the impact of smoking on the mucosa-associated...

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Autores principales: Shanahan, Erin R., Shah, Ayesha, Koloski, Natasha, Walker, Marjorie M., Talley, Nicholas J., Morrison, Mark, Holtmann, Gerald J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6116507/
https://www.ncbi.nlm.nih.gov/pubmed/30157953
http://dx.doi.org/10.1186/s40168-018-0531-3
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author Shanahan, Erin R.
Shah, Ayesha
Koloski, Natasha
Walker, Marjorie M.
Talley, Nicholas J.
Morrison, Mark
Holtmann, Gerald J.
author_facet Shanahan, Erin R.
Shah, Ayesha
Koloski, Natasha
Walker, Marjorie M.
Talley, Nicholas J.
Morrison, Mark
Holtmann, Gerald J.
author_sort Shanahan, Erin R.
collection PubMed
description BACKGROUND: Cigarette smoking is a known risk factor in a number of gastrointestinal (GI) diseases in which the microbiota is implicated, including duodenal ulcer and Crohn’s disease. Smoking has the potential to alter the microbiota; however, to date, the impact of smoking on the mucosa-associated microbiota (MAM), and particularly that of the upper GI tract, remains very poorly characterised. Thus, we investigated the impact of smoking on the upper small intestinal MAM. A total of 102 patients undergoing upper GI endoscopy for the assessment of GI symptoms, iron deficiency, or Crohn’s disease, but without identifiable lesions in the duodenum, were recruited. Smoking status was determined during clinical assessment and patients classified as current (n = 21), previous smokers (n = 40), or having never smoked (n = 41). The duodenal (D2) MAM was profiled via 16S rRNA gene amplicon sequencing. RESULTS: Smoking, both current and previous, is associated with significantly reduced bacterial diversity in the upper small intestinal mucosa, as compared to patients who had never smoked. This was accompanied by higher relative abundance of Firmicutes, specifically Streptococcus and Veillonella spp. The relative abundance of the genus Rothia was also observed to be greater in current smokers; while in contrast, levels of Prevotella and Neisseria were lower. The MAM profiles and diversity of previous smokers were observed to be intermediate between current and never smokers. Smoking did not impact the total density of bacteria present on the mucosa. CONCLUSIONS: These data indicate the duodenal MAM of current smokers is characterised by reduced bacterial diversity, which is partially but not completely restored in previous smokers. While the precise mechanisms remain to be elucidated, these microbiota changes may in some part explain the adverse effects of smoking on mucosa-associated diseases of the GI tract. Smoking status requires consideration when interpreting MAM data. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0531-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-61165072018-10-02 Influence of cigarette smoking on the human duodenal mucosa-associated microbiota Shanahan, Erin R. Shah, Ayesha Koloski, Natasha Walker, Marjorie M. Talley, Nicholas J. Morrison, Mark Holtmann, Gerald J. Microbiome Research BACKGROUND: Cigarette smoking is a known risk factor in a number of gastrointestinal (GI) diseases in which the microbiota is implicated, including duodenal ulcer and Crohn’s disease. Smoking has the potential to alter the microbiota; however, to date, the impact of smoking on the mucosa-associated microbiota (MAM), and particularly that of the upper GI tract, remains very poorly characterised. Thus, we investigated the impact of smoking on the upper small intestinal MAM. A total of 102 patients undergoing upper GI endoscopy for the assessment of GI symptoms, iron deficiency, or Crohn’s disease, but without identifiable lesions in the duodenum, were recruited. Smoking status was determined during clinical assessment and patients classified as current (n = 21), previous smokers (n = 40), or having never smoked (n = 41). The duodenal (D2) MAM was profiled via 16S rRNA gene amplicon sequencing. RESULTS: Smoking, both current and previous, is associated with significantly reduced bacterial diversity in the upper small intestinal mucosa, as compared to patients who had never smoked. This was accompanied by higher relative abundance of Firmicutes, specifically Streptococcus and Veillonella spp. The relative abundance of the genus Rothia was also observed to be greater in current smokers; while in contrast, levels of Prevotella and Neisseria were lower. The MAM profiles and diversity of previous smokers were observed to be intermediate between current and never smokers. Smoking did not impact the total density of bacteria present on the mucosa. CONCLUSIONS: These data indicate the duodenal MAM of current smokers is characterised by reduced bacterial diversity, which is partially but not completely restored in previous smokers. While the precise mechanisms remain to be elucidated, these microbiota changes may in some part explain the adverse effects of smoking on mucosa-associated diseases of the GI tract. Smoking status requires consideration when interpreting MAM data. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0531-3) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-29 /pmc/articles/PMC6116507/ /pubmed/30157953 http://dx.doi.org/10.1186/s40168-018-0531-3 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. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Shanahan, Erin R.
Shah, Ayesha
Koloski, Natasha
Walker, Marjorie M.
Talley, Nicholas J.
Morrison, Mark
Holtmann, Gerald J.
Influence of cigarette smoking on the human duodenal mucosa-associated microbiota
title Influence of cigarette smoking on the human duodenal mucosa-associated microbiota
title_full Influence of cigarette smoking on the human duodenal mucosa-associated microbiota
title_fullStr Influence of cigarette smoking on the human duodenal mucosa-associated microbiota
title_full_unstemmed Influence of cigarette smoking on the human duodenal mucosa-associated microbiota
title_short Influence of cigarette smoking on the human duodenal mucosa-associated microbiota
title_sort influence of cigarette smoking on the human duodenal mucosa-associated microbiota
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6116507/
https://www.ncbi.nlm.nih.gov/pubmed/30157953
http://dx.doi.org/10.1186/s40168-018-0531-3
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