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Changes in Microbiome Dominance Are Associated With Declining Lung Function and Fluctuating Inflammation in People With Cystic Fibrosis

Airway inflammation and microbiome dysbiosis are hallmarks of cystic fibrosis (CF) lung disease. However, longitudinal studies are needed to decipher which factors contribute to the long-term evolution of these key features of CF. We therefore evaluated the relationship between fluctuation in microb...

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Autores principales: Frey, Dario L., Bridson, Calum, Dittrich, Susanne, Graeber, Simon Y., Stahl, Mirjam, Wege, Sabine, Herth, Felix, Sommerburg, Olaf, Schultz, Carsten, Dalpke, Alexander, Mall, Marcus A., Boutin, Sébastien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9136159/
https://www.ncbi.nlm.nih.gov/pubmed/35633718
http://dx.doi.org/10.3389/fmicb.2022.885822
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author Frey, Dario L.
Bridson, Calum
Dittrich, Susanne
Graeber, Simon Y.
Stahl, Mirjam
Wege, Sabine
Herth, Felix
Sommerburg, Olaf
Schultz, Carsten
Dalpke, Alexander
Mall, Marcus A.
Boutin, Sébastien
author_facet Frey, Dario L.
Bridson, Calum
Dittrich, Susanne
Graeber, Simon Y.
Stahl, Mirjam
Wege, Sabine
Herth, Felix
Sommerburg, Olaf
Schultz, Carsten
Dalpke, Alexander
Mall, Marcus A.
Boutin, Sébastien
author_sort Frey, Dario L.
collection PubMed
description Airway inflammation and microbiome dysbiosis are hallmarks of cystic fibrosis (CF) lung disease. However, longitudinal studies are needed to decipher which factors contribute to the long-term evolution of these key features of CF. We therefore evaluated the relationship between fluctuation in microbiome and inflammatory parameters in a longitudinal study including a short- (1-year) and a long-term (3+ years) period. We collected 118 sputum samples from 26 CF adult patients and analyzed them by 16S rRNA gene sequencing. We measured the levels of inflammatory cytokines, neutrophil elastase, and anti-proteinases; lung function (FEV1% predicted); and BMI. The longitudinal evolution was analyzed based on (i) the rates of changes; (ii) the intra-patient stability of the variables; and (iii) the dependency of the rates of changes on the baseline values. We observed that the diversity of the microbiome was highly variable over a 1-year period, while the inflammatory markers showed a slower evolution, with significant changes only observed in the 3+ year cohort. Further, the degree of fluctuation of the biomass and the dominance of the microbiome were associated with changes in inflammatory markers, especially IL-1β and IL-8. This longitudinal study demonstrates for the first time that the long-term establishment and periodical variation of the abundance of a dominant pathogen is associated with a more severe increase in inflammation. This result indicates that a single time point or 1-year study might fail to reveal the correlation between microbial evolution and clinical degradation in cystic fibrosis.
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spelling pubmed-91361592022-05-28 Changes in Microbiome Dominance Are Associated With Declining Lung Function and Fluctuating Inflammation in People With Cystic Fibrosis Frey, Dario L. Bridson, Calum Dittrich, Susanne Graeber, Simon Y. Stahl, Mirjam Wege, Sabine Herth, Felix Sommerburg, Olaf Schultz, Carsten Dalpke, Alexander Mall, Marcus A. Boutin, Sébastien Front Microbiol Microbiology Airway inflammation and microbiome dysbiosis are hallmarks of cystic fibrosis (CF) lung disease. However, longitudinal studies are needed to decipher which factors contribute to the long-term evolution of these key features of CF. We therefore evaluated the relationship between fluctuation in microbiome and inflammatory parameters in a longitudinal study including a short- (1-year) and a long-term (3+ years) period. We collected 118 sputum samples from 26 CF adult patients and analyzed them by 16S rRNA gene sequencing. We measured the levels of inflammatory cytokines, neutrophil elastase, and anti-proteinases; lung function (FEV1% predicted); and BMI. The longitudinal evolution was analyzed based on (i) the rates of changes; (ii) the intra-patient stability of the variables; and (iii) the dependency of the rates of changes on the baseline values. We observed that the diversity of the microbiome was highly variable over a 1-year period, while the inflammatory markers showed a slower evolution, with significant changes only observed in the 3+ year cohort. Further, the degree of fluctuation of the biomass and the dominance of the microbiome were associated with changes in inflammatory markers, especially IL-1β and IL-8. This longitudinal study demonstrates for the first time that the long-term establishment and periodical variation of the abundance of a dominant pathogen is associated with a more severe increase in inflammation. This result indicates that a single time point or 1-year study might fail to reveal the correlation between microbial evolution and clinical degradation in cystic fibrosis. Frontiers Media S.A. 2022-05-13 /pmc/articles/PMC9136159/ /pubmed/35633718 http://dx.doi.org/10.3389/fmicb.2022.885822 Text en Copyright © 2022 Frey, Bridson, Dittrich, Graeber, Stahl, Wege, Herth, Sommerburg, Schultz, Dalpke, Mall and Boutin. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Frey, Dario L.
Bridson, Calum
Dittrich, Susanne
Graeber, Simon Y.
Stahl, Mirjam
Wege, Sabine
Herth, Felix
Sommerburg, Olaf
Schultz, Carsten
Dalpke, Alexander
Mall, Marcus A.
Boutin, Sébastien
Changes in Microbiome Dominance Are Associated With Declining Lung Function and Fluctuating Inflammation in People With Cystic Fibrosis
title Changes in Microbiome Dominance Are Associated With Declining Lung Function and Fluctuating Inflammation in People With Cystic Fibrosis
title_full Changes in Microbiome Dominance Are Associated With Declining Lung Function and Fluctuating Inflammation in People With Cystic Fibrosis
title_fullStr Changes in Microbiome Dominance Are Associated With Declining Lung Function and Fluctuating Inflammation in People With Cystic Fibrosis
title_full_unstemmed Changes in Microbiome Dominance Are Associated With Declining Lung Function and Fluctuating Inflammation in People With Cystic Fibrosis
title_short Changes in Microbiome Dominance Are Associated With Declining Lung Function and Fluctuating Inflammation in People With Cystic Fibrosis
title_sort changes in microbiome dominance are associated with declining lung function and fluctuating inflammation in people with cystic fibrosis
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9136159/
https://www.ncbi.nlm.nih.gov/pubmed/35633718
http://dx.doi.org/10.3389/fmicb.2022.885822
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