Exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosis

Abstract Studies of microbiota reveal inter-relationships between the microbiomes of the gut and lungs. This relationship may influence the progression of lung disease, particularly in patients with cystic fibrosis (CF), who often experience extraoesophageal reflux (EOR). Despite identifying this re...

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Main Authors: Hafez Al-Momani, Audrey Perry, Andrew Nelson, Christopher J. Stewart, Rhys Jones, Amaran Krishnan, Andrew Robertson, Stephen Bourke, Simon Doe, Stephen Cummings, Alan Anderson, Tara Forrest, Ian Forrest, Michael Griffin, Matthew Wilcox, Malcolm Brodlie, Jeffrey Pearson, Christopher Ward
Format: Article
Language:English
Published: Nature Portfolio 2022-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-15375-4
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author Hafez Al-Momani
Audrey Perry
Andrew Nelson
Christopher J. Stewart
Rhys Jones
Amaran Krishnan
Andrew Robertson
Stephen Bourke
Simon Doe
Stephen Cummings
Alan Anderson
Tara Forrest
Ian Forrest
Michael Griffin
Matthew Wilcox
Malcolm Brodlie
Jeffrey Pearson
Christopher Ward
author_facet Hafez Al-Momani
Audrey Perry
Andrew Nelson
Christopher J. Stewart
Rhys Jones
Amaran Krishnan
Andrew Robertson
Stephen Bourke
Simon Doe
Stephen Cummings
Alan Anderson
Tara Forrest
Ian Forrest
Michael Griffin
Matthew Wilcox
Malcolm Brodlie
Jeffrey Pearson
Christopher Ward
author_sort Hafez Al-Momani
collection DOAJ
description Abstract Studies of microbiota reveal inter-relationships between the microbiomes of the gut and lungs. This relationship may influence the progression of lung disease, particularly in patients with cystic fibrosis (CF), who often experience extraoesophageal reflux (EOR). Despite identifying this relationship, it is not well characterised. Our hypothesis is that the gastric and lung microbiomes in CF are related, with the potential for aerodigestive pathophysiology. We evaluated gastric and sputum bacterial communities by culture and 16S rRNA gene sequencing in 13 CF patients. Impacts of varying levels of bile acids, pepsin and pH on patient isolates of Pseudomonas aeruginosa (Pa) were evaluated. Clonally related strains of Pa and NTM were identified in gastric and sputum samples from patients with symptoms of EOR. Bacterial diversity was more pronounced in sputa compared to gastric juice. Gastric and lung bile and pepsin levels were associated with Pa biofilm formation. Analysis of the aerodigestive microbiomes of CF patients with negative sputa indicates that the gut can be a reservoir of Pa and NTM. This combined with the CF patient’s symptoms of reflux and potential aspiration, highlights the possibility of communication between microorganisms of the gut and the lungs. This phenomenon merits further research.
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spelling doaj.art-468ee9505acd40c2b4349386f6c625472022-12-22T02:27:57ZengNature PortfolioScientific Reports2045-23222022-06-0112111110.1038/s41598-022-15375-4Exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosisHafez Al-Momani0Audrey Perry1Andrew Nelson2Christopher J. Stewart3Rhys Jones4Amaran Krishnan5Andrew Robertson6Stephen Bourke7Simon Doe8Stephen Cummings9Alan Anderson10Tara Forrest11Ian Forrest12Michael Griffin13Matthew Wilcox14Malcolm Brodlie15Jeffrey Pearson16Christopher Ward17Basic Medical Science Department, School of Medicine, The Hashemite UniversityDepartment of Microbiology, Freeman Hospital, Newcastle upon Tyne Hospitals NHS Foundation TrustFaculty of Health and Life Sciences, Northumbria UniversityTranslational and Clinical Research Institute, Newcastle UniversityInstitutes of Cellular Medicine and Cell & Molecular Biosciences, Newcastle University Medical School, Newcastle UniversityInstitutes of Cellular Medicine and Cell & Molecular Biosciences, Newcastle University Medical School, Newcastle UniversityNHS Fife and Newcastle University Medical School, Newcastle UniversityAdult Cystic Fibrosis Centre and Northern Oesophago-Gastric Unit, Royal Victoria InfirmaryAdult Cystic Fibrosis Centre and Northern Oesophago-Gastric Unit, Royal Victoria InfirmarySchool of Science and Engineering, Teesside UniversityAdult Cystic Fibrosis Centre and Northern Oesophago-Gastric Unit, Royal Victoria InfirmaryAdult Cystic Fibrosis Centre and Northern Oesophago-Gastric Unit, Royal Victoria InfirmaryAdult Cystic Fibrosis Centre and Northern Oesophago-Gastric Unit, Royal Victoria InfirmaryAdult Cystic Fibrosis Centre and Northern Oesophago-Gastric Unit, Royal Victoria InfirmaryInstitutes of Cellular Medicine and Cell & Molecular Biosciences, Newcastle University Medical School, Newcastle UniversityInstitutes of Cellular Medicine and Cell & Molecular Biosciences, Newcastle University Medical School, Newcastle UniversityInstitutes of Cellular Medicine and Cell & Molecular Biosciences, Newcastle University Medical School, Newcastle UniversityInstitutes of Cellular Medicine and Cell & Molecular Biosciences, Newcastle University Medical School, Newcastle UniversityAbstract Studies of microbiota reveal inter-relationships between the microbiomes of the gut and lungs. This relationship may influence the progression of lung disease, particularly in patients with cystic fibrosis (CF), who often experience extraoesophageal reflux (EOR). Despite identifying this relationship, it is not well characterised. Our hypothesis is that the gastric and lung microbiomes in CF are related, with the potential for aerodigestive pathophysiology. We evaluated gastric and sputum bacterial communities by culture and 16S rRNA gene sequencing in 13 CF patients. Impacts of varying levels of bile acids, pepsin and pH on patient isolates of Pseudomonas aeruginosa (Pa) were evaluated. Clonally related strains of Pa and NTM were identified in gastric and sputum samples from patients with symptoms of EOR. Bacterial diversity was more pronounced in sputa compared to gastric juice. Gastric and lung bile and pepsin levels were associated with Pa biofilm formation. Analysis of the aerodigestive microbiomes of CF patients with negative sputa indicates that the gut can be a reservoir of Pa and NTM. This combined with the CF patient’s symptoms of reflux and potential aspiration, highlights the possibility of communication between microorganisms of the gut and the lungs. This phenomenon merits further research.https://doi.org/10.1038/s41598-022-15375-4
spellingShingle Hafez Al-Momani
Audrey Perry
Andrew Nelson
Christopher J. Stewart
Rhys Jones
Amaran Krishnan
Andrew Robertson
Stephen Bourke
Simon Doe
Stephen Cummings
Alan Anderson
Tara Forrest
Ian Forrest
Michael Griffin
Matthew Wilcox
Malcolm Brodlie
Jeffrey Pearson
Christopher Ward
Exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosis
Scientific Reports
title Exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosis
title_full Exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosis
title_fullStr Exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosis
title_full_unstemmed Exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosis
title_short Exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosis
title_sort exposure to bile and gastric juice can impact the aerodigestive microbiome in people with cystic fibrosis
url https://doi.org/10.1038/s41598-022-15375-4
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