Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients

Thomas Bjarnsholt; Peter Østrup Jensen; Mark J Fiandaca; Jette Pedersen; Christine Rønne Hansen; Claus Bøgelund Andersen; Tacjana Pressler; Michael Givskov; Niels Høiby

doi:10.1002/ppul.21011

Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients

Thomas Bjarnsholt, Peter Østrup Jensen, Mark J Fiandaca, Jette Pedersen, Christine Rønne Hansen, Claus Bøgelund Andersen, Tacjana Pressler, Michael Givskov, Niels Høiby

Department of Immunology and Microbiology

477 Citations (Scopus)

Abstract

The present study was undertaken to investigate the appearance and location of Pseudomonas aeruginosa in the cystic fibrosis (CF) lung and in sputum. Samples include preserved tissues of CF patients who died due to chronic P. aeruginosa lung infection prior to the advent of intensive antibiotic therapy, explanted lungs from 3 intensively treated chronically P. aeruginosa infected CF patients and routine sputum from 77 chronically P. aeruginosa infected CF patients. All samples were investigated microscopically using hematoxylin-eosin (HE), Gram and alcian-blue stain, PNA FISH and immunofluorescence for alginate.Investigation of the preserved tissues revealed that prior to aggressive antibiotic therapy, P. aeruginosa infection and destruction of the CF lung correlated with the occurrence of mucoid (alginate) bacteria present in aggregating structures surrounded by pronounced polymorphonuclear-leukocyte (PMN) inflammation in the respiratory zone (9/9). Non-mucoid bacteria were not observed here, and rarely in the conductive zone (1/9). However, in the explanted lungs, the P. aeruginosa aggregates were also mucoid but in contrast to the autopsies, they were very rare in the respiratory zone but abundant in the sputum of the conductive zone (3/3), which also contained abundances of PMNs (3/3). Non-mucoid and planktonic P. aeruginosa were also observed here (3/3).In conclusion, the present intensive antibiotic therapy of chronic P. aeruginosa infections, at the Copenhagen CF Centre, seems to restrain but not eradicate the bacteria from the conductive zone, whereas the remaining healthy respiratory zone appears to be protected, for a long period, from massive biofilm infection. This strongly suggests that the conductive zone serves as a bacterial reservoir where the bacteria are organized in mucoid biofilms within the mucus, protected against antibiotics and host defenses.

Original language	English
Journal	Pediatric Pulmonology
Volume	44
Issue number	6
Pages (from-to)	547-58
Number of pages	12
ISSN	8755-6863
DOIs	https://doi.org/10.1002/ppul.21011 https://doi.org/10.1002/ppul.21011
Publication status	Published - 1 Jun 2009

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@article{c71c6f50b27911debc73000ea68e967b,

title = "Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients",

abstract = "The present study was undertaken to investigate the appearance and location of Pseudomonas aeruginosa in the cystic fibrosis (CF) lung and in sputum. Samples include preserved tissues of CF patients who died due to chronic P. aeruginosa lung infection prior to the advent of intensive antibiotic therapy, explanted lungs from 3 intensively treated chronically P. aeruginosa infected CF patients and routine sputum from 77 chronically P. aeruginosa infected CF patients. All samples were investigated microscopically using hematoxylin-eosin (HE), Gram and alcian-blue stain, PNA FISH and immunofluorescence for alginate.Investigation of the preserved tissues revealed that prior to aggressive antibiotic therapy, P. aeruginosa infection and destruction of the CF lung correlated with the occurrence of mucoid (alginate) bacteria present in aggregating structures surrounded by pronounced polymorphonuclear-leukocyte (PMN) inflammation in the respiratory zone (9/9). Non-mucoid bacteria were not observed here, and rarely in the conductive zone (1/9). However, in the explanted lungs, the P. aeruginosa aggregates were also mucoid but in contrast to the autopsies, they were very rare in the respiratory zone but abundant in the sputum of the conductive zone (3/3), which also contained abundances of PMNs (3/3). Non-mucoid and planktonic P. aeruginosa were also observed here (3/3).In conclusion, the present intensive antibiotic therapy of chronic P. aeruginosa infections, at the Copenhagen CF Centre, seems to restrain but not eradicate the bacteria from the conductive zone, whereas the remaining healthy respiratory zone appears to be protected, for a long period, from massive biofilm infection. This strongly suggests that the conductive zone serves as a bacterial reservoir where the bacteria are organized in mucoid biofilms within the mucus, protected against antibiotics and host defenses.",

author = "Thomas Bjarnsholt and Jensen, {Peter {\O}strup} and Fiandaca, {Mark J} and Jette Pedersen and Hansen, {Christine R{\o}nne} and Andersen, {Claus B{\o}gelund} and Tacjana Pressler and Michael Givskov and Niels H{\o}iby",

note = "Keywords: Adolescent; Adult; Biofilms; Case-Control Studies; Child; Child, Preschool; Female; Humans; Infant; Male; Middle Aged; Neutrophils; Pneumonia, Bacterial; Pseudomonas Infections; Pseudomonas aeruginosa; Sputum; Young Adult",

year = "2009",

month = jun,

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doi = "10.1002/ppul.21011",

language = "English",

volume = "44",

pages = "547--58",

journal = "Pediatric pulmonology. Supplement",

issn = "1054-187X",

publisher = "JohnWiley & Sons, Inc.",

number = "6",

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T1 - Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients

AU - Bjarnsholt, Thomas

AU - Jensen, Peter Østrup

AU - Fiandaca, Mark J

AU - Pedersen, Jette

AU - Hansen, Christine Rønne

AU - Andersen, Claus Bøgelund

AU - Pressler, Tacjana

AU - Givskov, Michael

AU - Høiby, Niels

N1 - Keywords: Adolescent; Adult; Biofilms; Case-Control Studies; Child; Child, Preschool; Female; Humans; Infant; Male; Middle Aged; Neutrophils; Pneumonia, Bacterial; Pseudomonas Infections; Pseudomonas aeruginosa; Sputum; Young Adult

PY - 2009/6/1

Y1 - 2009/6/1

N2 - The present study was undertaken to investigate the appearance and location of Pseudomonas aeruginosa in the cystic fibrosis (CF) lung and in sputum. Samples include preserved tissues of CF patients who died due to chronic P. aeruginosa lung infection prior to the advent of intensive antibiotic therapy, explanted lungs from 3 intensively treated chronically P. aeruginosa infected CF patients and routine sputum from 77 chronically P. aeruginosa infected CF patients. All samples were investigated microscopically using hematoxylin-eosin (HE), Gram and alcian-blue stain, PNA FISH and immunofluorescence for alginate.Investigation of the preserved tissues revealed that prior to aggressive antibiotic therapy, P. aeruginosa infection and destruction of the CF lung correlated with the occurrence of mucoid (alginate) bacteria present in aggregating structures surrounded by pronounced polymorphonuclear-leukocyte (PMN) inflammation in the respiratory zone (9/9). Non-mucoid bacteria were not observed here, and rarely in the conductive zone (1/9). However, in the explanted lungs, the P. aeruginosa aggregates were also mucoid but in contrast to the autopsies, they were very rare in the respiratory zone but abundant in the sputum of the conductive zone (3/3), which also contained abundances of PMNs (3/3). Non-mucoid and planktonic P. aeruginosa were also observed here (3/3).In conclusion, the present intensive antibiotic therapy of chronic P. aeruginosa infections, at the Copenhagen CF Centre, seems to restrain but not eradicate the bacteria from the conductive zone, whereas the remaining healthy respiratory zone appears to be protected, for a long period, from massive biofilm infection. This strongly suggests that the conductive zone serves as a bacterial reservoir where the bacteria are organized in mucoid biofilms within the mucus, protected against antibiotics and host defenses.

AB - The present study was undertaken to investigate the appearance and location of Pseudomonas aeruginosa in the cystic fibrosis (CF) lung and in sputum. Samples include preserved tissues of CF patients who died due to chronic P. aeruginosa lung infection prior to the advent of intensive antibiotic therapy, explanted lungs from 3 intensively treated chronically P. aeruginosa infected CF patients and routine sputum from 77 chronically P. aeruginosa infected CF patients. All samples were investigated microscopically using hematoxylin-eosin (HE), Gram and alcian-blue stain, PNA FISH and immunofluorescence for alginate.Investigation of the preserved tissues revealed that prior to aggressive antibiotic therapy, P. aeruginosa infection and destruction of the CF lung correlated with the occurrence of mucoid (alginate) bacteria present in aggregating structures surrounded by pronounced polymorphonuclear-leukocyte (PMN) inflammation in the respiratory zone (9/9). Non-mucoid bacteria were not observed here, and rarely in the conductive zone (1/9). However, in the explanted lungs, the P. aeruginosa aggregates were also mucoid but in contrast to the autopsies, they were very rare in the respiratory zone but abundant in the sputum of the conductive zone (3/3), which also contained abundances of PMNs (3/3). Non-mucoid and planktonic P. aeruginosa were also observed here (3/3).In conclusion, the present intensive antibiotic therapy of chronic P. aeruginosa infections, at the Copenhagen CF Centre, seems to restrain but not eradicate the bacteria from the conductive zone, whereas the remaining healthy respiratory zone appears to be protected, for a long period, from massive biofilm infection. This strongly suggests that the conductive zone serves as a bacterial reservoir where the bacteria are organized in mucoid biofilms within the mucus, protected against antibiotics and host defenses.

U2 - 10.1002/ppul.21011

DO - 10.1002/ppul.21011

M3 - Journal article

C2 - 19418571

SN - 1054-187X

VL - 44

SP - 547

EP - 558

JO - Pediatric pulmonology. Supplement

JF - Pediatric pulmonology. Supplement

IS - 6

ER -

Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients

Abstract

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