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Bacterial biofilms predominate in both acute and chronic human lung infections

BACKGROUND: A basic paradigm of human infection is that acute bacterial disease is caused by fast growing planktonic bacteria while chronic infections are caused by slow-growing, aggregated bacteria, a phenomenon known as a biofilm. For lung infections, this paradigm has been thought to be supported...

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Autores principales: Kolpen, Mette, Kragh, Kasper Nørskov, Enciso, Juan Barraza, Faurholt-Jepsen, Daniel, Lindegaard, Birgitte, Egelund, Gertrud Baunbæk, Jensen, Andreas Vestergaard, Ravn, Pernille, Mathiesen, Inger Hee Mabuza, Gheorge, Alexandra Gabriella, Hertz, Frederik Boëtius, Qvist, Tavs, Whiteley, Marvin, Jensen, Peter Østrup, Bjarnsholt, Thomas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BMJ Publishing Group 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9510407/
https://www.ncbi.nlm.nih.gov/pubmed/35017313
http://dx.doi.org/10.1136/thoraxjnl-2021-217576
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author Kolpen, Mette
Kragh, Kasper Nørskov
Enciso, Juan Barraza
Faurholt-Jepsen, Daniel
Lindegaard, Birgitte
Egelund, Gertrud Baunbæk
Jensen, Andreas Vestergaard
Ravn, Pernille
Mathiesen, Inger Hee Mabuza
Gheorge, Alexandra Gabriella
Hertz, Frederik Boëtius
Qvist, Tavs
Whiteley, Marvin
Jensen, Peter Østrup
Bjarnsholt, Thomas
author_facet Kolpen, Mette
Kragh, Kasper Nørskov
Enciso, Juan Barraza
Faurholt-Jepsen, Daniel
Lindegaard, Birgitte
Egelund, Gertrud Baunbæk
Jensen, Andreas Vestergaard
Ravn, Pernille
Mathiesen, Inger Hee Mabuza
Gheorge, Alexandra Gabriella
Hertz, Frederik Boëtius
Qvist, Tavs
Whiteley, Marvin
Jensen, Peter Østrup
Bjarnsholt, Thomas
author_sort Kolpen, Mette
collection PubMed
description BACKGROUND: A basic paradigm of human infection is that acute bacterial disease is caused by fast growing planktonic bacteria while chronic infections are caused by slow-growing, aggregated bacteria, a phenomenon known as a biofilm. For lung infections, this paradigm has been thought to be supported by observations of how bacteria proliferate in well-established growth media in the laboratory—the gold standard of microbiology. OBJECTIVE: To investigate the bacterial architecture in sputum from patients with acute and chronic lung infections. METHODS: Advanced imaging technology was used for quantification and direct comparison of infection types on fresh sputum samples, thereby directly testing the acute versus chronic paradigm. RESULTS: In this study, we compared the bacterial lifestyle (planktonic or biofilm), growth rate and inflammatory response of bacteria in freshly collected sputum (n=43) from patient groups presenting with acute or chronic lung infections. We found that both acute and chronic lung infections are dominated by biofilms (aggregates of bacteria within an extracellular matrix), although planktonic cells were observed in both sample types. Bacteria grew faster in sputum from acute infections, but these fast-growing bacteria were enriched in biofilms similar to the architecture thought to be reserved for chronic infections. Cellular inflammation in the lungs was also similar across patient groups, but systemic inflammatory markers were only elevated in acute infections. CONCLUSIONS: Our findings indicate that the current paradigm of equating planktonic with acute and biofilm with chronic infection needs to be revisited as the difference lies primarily in metabolic rates, not bacterial architecture.
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spelling pubmed-95104072022-09-27 Bacterial biofilms predominate in both acute and chronic human lung infections Kolpen, Mette Kragh, Kasper Nørskov Enciso, Juan Barraza Faurholt-Jepsen, Daniel Lindegaard, Birgitte Egelund, Gertrud Baunbæk Jensen, Andreas Vestergaard Ravn, Pernille Mathiesen, Inger Hee Mabuza Gheorge, Alexandra Gabriella Hertz, Frederik Boëtius Qvist, Tavs Whiteley, Marvin Jensen, Peter Østrup Bjarnsholt, Thomas Thorax Respiratory Infection BACKGROUND: A basic paradigm of human infection is that acute bacterial disease is caused by fast growing planktonic bacteria while chronic infections are caused by slow-growing, aggregated bacteria, a phenomenon known as a biofilm. For lung infections, this paradigm has been thought to be supported by observations of how bacteria proliferate in well-established growth media in the laboratory—the gold standard of microbiology. OBJECTIVE: To investigate the bacterial architecture in sputum from patients with acute and chronic lung infections. METHODS: Advanced imaging technology was used for quantification and direct comparison of infection types on fresh sputum samples, thereby directly testing the acute versus chronic paradigm. RESULTS: In this study, we compared the bacterial lifestyle (planktonic or biofilm), growth rate and inflammatory response of bacteria in freshly collected sputum (n=43) from patient groups presenting with acute or chronic lung infections. We found that both acute and chronic lung infections are dominated by biofilms (aggregates of bacteria within an extracellular matrix), although planktonic cells were observed in both sample types. Bacteria grew faster in sputum from acute infections, but these fast-growing bacteria were enriched in biofilms similar to the architecture thought to be reserved for chronic infections. Cellular inflammation in the lungs was also similar across patient groups, but systemic inflammatory markers were only elevated in acute infections. CONCLUSIONS: Our findings indicate that the current paradigm of equating planktonic with acute and biofilm with chronic infection needs to be revisited as the difference lies primarily in metabolic rates, not bacterial architecture. BMJ Publishing Group 2022-10 2022-01-11 /pmc/articles/PMC9510407/ /pubmed/35017313 http://dx.doi.org/10.1136/thoraxjnl-2021-217576 Text en © Author(s) (or their employer(s)) 2022. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) .
spellingShingle Respiratory Infection
Kolpen, Mette
Kragh, Kasper Nørskov
Enciso, Juan Barraza
Faurholt-Jepsen, Daniel
Lindegaard, Birgitte
Egelund, Gertrud Baunbæk
Jensen, Andreas Vestergaard
Ravn, Pernille
Mathiesen, Inger Hee Mabuza
Gheorge, Alexandra Gabriella
Hertz, Frederik Boëtius
Qvist, Tavs
Whiteley, Marvin
Jensen, Peter Østrup
Bjarnsholt, Thomas
Bacterial biofilms predominate in both acute and chronic human lung infections
title Bacterial biofilms predominate in both acute and chronic human lung infections
title_full Bacterial biofilms predominate in both acute and chronic human lung infections
title_fullStr Bacterial biofilms predominate in both acute and chronic human lung infections
title_full_unstemmed Bacterial biofilms predominate in both acute and chronic human lung infections
title_short Bacterial biofilms predominate in both acute and chronic human lung infections
title_sort bacterial biofilms predominate in both acute and chronic human lung infections
topic Respiratory Infection
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9510407/
https://www.ncbi.nlm.nih.gov/pubmed/35017313
http://dx.doi.org/10.1136/thoraxjnl-2021-217576
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