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...
Main Authors: | , , , , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Nature Portfolio
2022-06-01
|
Series: | Scientific Reports |
Online Access: | https://doi.org/10.1038/s41598-022-15375-4 |
_version_ | 1817976615782580224 |
---|---|
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. |
first_indexed | 2024-04-13T22:06:01Z |
format | Article |
id | doaj.art-468ee9505acd40c2b4349386f6c62547 |
institution | Directory Open Access Journal |
issn | 2045-2322 |
language | English |
last_indexed | 2024-04-13T22:06:01Z |
publishDate | 2022-06-01 |
publisher | Nature Portfolio |
record_format | Article |
series | Scientific Reports |
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 |
work_keys_str_mv | AT hafezalmomani exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT audreyperry exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT andrewnelson exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT christopherjstewart exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT rhysjones exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT amarankrishnan exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT andrewrobertson exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT stephenbourke exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT simondoe exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT stephencummings exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT alananderson exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT taraforrest exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT ianforrest exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT michaelgriffin exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT matthewwilcox exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT malcolmbrodlie exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT jeffreypearson exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis AT christopherward exposuretobileandgastricjuicecanimpacttheaerodigestivemicrobiomeinpeoplewithcysticfibrosis |