Intramucosal bacterial microcolonies exist in chronic rhinosinusitis without inducing a local immune response

A.J. Wood, J.D. Fraser, S. Swift, Emma A C Patterson-Emanuelson, S. Amirapu, R.G. Douglas

Research output: Contribution to journalArticle

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Abstract

Background: Although chronic rhinosinusitis (CRS) causes very significant morbidity, much about its pathogenesis remains uncertain. Recent studies have identified polymicrobial biofilms on the surface of sinus mucosa and Staphylococcus aureus within the sinus mucosa of patients with CRS, both with and without nasal polyps. The pathogenic implications of intramucosal bacteria in CRS are unknown. This study was designed to determine the prevalence and species of bacterial colonies within the sinus mucosa of adult patients with and without CRS and to describe the relationship of these bacterial colonies to the host immune response. Methods: Sinus mucosa from patients with and without CRS was examined using Gram and Giemsa staining, immunohistochemistry, bacterial culture, and fluorescence in situ hybridization techniques. Results: Bacterial microcolonies were observed within the mucosa in 14 of 18 patients with CRS. In 10 of these patients colonies were positively identified as S. aureus. Staphylococcal microcolonies were observed at a lower level (1 of 8 patients) in normal sinus mucosa. There was no correlation between detection of S. aureus on the mucosal surface and microcolonization of the mucosa. Surprisingly, there was no evidence of an immune reaction to microcolonies. Indeed, fewer T lymphocytes (p = 0.03) and eosinophils (p = 0.03) were counted immediately surrounding the microcolonies compared with uninfected areas of the same tissue. Conclusion: Bacterial microcolonies are prevalent within paranasal sinus mucosa and are commonly S. aureus. These microcolonies do not provoke immune detection and may represent a phenotype that actively evades host immunity. This may underpin the recalcitrance of CRS to antibiotic therapy. These findings challenge classic views of both infection and mucosal immunity in human chronic disease. The presence of intramucosal bacteria in samples of normal sinus mucosa also questions the sensitivity of detecting nasal carriage of pathogens by swabbing the surface of the anterior nares.
Original languageEnglish
Pages (from-to)265-270
Number of pages6
JournalAmerican Journal of Rhinology and Allergy
Volume26
Issue number4
DOIs
Publication statusPublished - 1 Jul 2012

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Mucous Membrane
Staphylococcus aureus
Bacteria
Nasal Polyps
Mucosal Immunity
Paranasal Sinuses
Biofilms
Fluorescence In Situ Hybridization
Nose
Eosinophils
Immunity
Chronic Disease
Immunohistochemistry
Staining and Labeling
Anti-Bacterial Agents
Morbidity
T-Lymphocytes
Phenotype
Infection

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Intramucosal bacterial microcolonies exist in chronic rhinosinusitis without inducing a local immune response. / Wood, A.J.; Fraser, J.D.; Swift, S.; Patterson-Emanuelson, Emma A C; Amirapu, S.; Douglas, R.G.

In: American Journal of Rhinology and Allergy, Vol. 26, No. 4, 01.07.2012, p. 265-270.

Research output: Contribution to journalArticle

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abstract = "Background: Although chronic rhinosinusitis (CRS) causes very significant morbidity, much about its pathogenesis remains uncertain. Recent studies have identified polymicrobial biofilms on the surface of sinus mucosa and Staphylococcus aureus within the sinus mucosa of patients with CRS, both with and without nasal polyps. The pathogenic implications of intramucosal bacteria in CRS are unknown. This study was designed to determine the prevalence and species of bacterial colonies within the sinus mucosa of adult patients with and without CRS and to describe the relationship of these bacterial colonies to the host immune response. Methods: Sinus mucosa from patients with and without CRS was examined using Gram and Giemsa staining, immunohistochemistry, bacterial culture, and fluorescence in situ hybridization techniques. Results: Bacterial microcolonies were observed within the mucosa in 14 of 18 patients with CRS. In 10 of these patients colonies were positively identified as S. aureus. Staphylococcal microcolonies were observed at a lower level (1 of 8 patients) in normal sinus mucosa. There was no correlation between detection of S. aureus on the mucosal surface and microcolonization of the mucosa. Surprisingly, there was no evidence of an immune reaction to microcolonies. Indeed, fewer T lymphocytes (p = 0.03) and eosinophils (p = 0.03) were counted immediately surrounding the microcolonies compared with uninfected areas of the same tissue. Conclusion: Bacterial microcolonies are prevalent within paranasal sinus mucosa and are commonly S. aureus. These microcolonies do not provoke immune detection and may represent a phenotype that actively evades host immunity. This may underpin the recalcitrance of CRS to antibiotic therapy. These findings challenge classic views of both infection and mucosal immunity in human chronic disease. The presence of intramucosal bacteria in samples of normal sinus mucosa also questions the sensitivity of detecting nasal carriage of pathogens by swabbing the surface of the anterior nares.",
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AB - Background: Although chronic rhinosinusitis (CRS) causes very significant morbidity, much about its pathogenesis remains uncertain. Recent studies have identified polymicrobial biofilms on the surface of sinus mucosa and Staphylococcus aureus within the sinus mucosa of patients with CRS, both with and without nasal polyps. The pathogenic implications of intramucosal bacteria in CRS are unknown. This study was designed to determine the prevalence and species of bacterial colonies within the sinus mucosa of adult patients with and without CRS and to describe the relationship of these bacterial colonies to the host immune response. Methods: Sinus mucosa from patients with and without CRS was examined using Gram and Giemsa staining, immunohistochemistry, bacterial culture, and fluorescence in situ hybridization techniques. Results: Bacterial microcolonies were observed within the mucosa in 14 of 18 patients with CRS. In 10 of these patients colonies were positively identified as S. aureus. Staphylococcal microcolonies were observed at a lower level (1 of 8 patients) in normal sinus mucosa. There was no correlation between detection of S. aureus on the mucosal surface and microcolonization of the mucosa. Surprisingly, there was no evidence of an immune reaction to microcolonies. Indeed, fewer T lymphocytes (p = 0.03) and eosinophils (p = 0.03) were counted immediately surrounding the microcolonies compared with uninfected areas of the same tissue. Conclusion: Bacterial microcolonies are prevalent within paranasal sinus mucosa and are commonly S. aureus. These microcolonies do not provoke immune detection and may represent a phenotype that actively evades host immunity. This may underpin the recalcitrance of CRS to antibiotic therapy. These findings challenge classic views of both infection and mucosal immunity in human chronic disease. The presence of intramucosal bacteria in samples of normal sinus mucosa also questions the sensitivity of detecting nasal carriage of pathogens by swabbing the surface of the anterior nares.

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