Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma

Yvonne J. Huang, Craig E. Nelson, Eoin L. Brodie, Todd Z. Desantis, Marshall S. Baek, Jane Liu, Tanja Woyke, Martin Allgaier, Jim Bristow, Jeanine P. Wiener-Kronish, E. Rand Sutherland, Tonya S. King, Nikolina Icitovic, Richard J. Martin, William Calhoun, Mario Castro, Loren C. Denlinger, Emily Dimango, Monica Kraft, Stephen P. Peters & 4 others Stephen I. Wasserman, Michael E. Wechsler, Homer A. Boushey, Susan V. Lynch

Research output: Contribution to journalArticle

373 Citations (Scopus)

Abstract

Background: Improvement in lung function after macrolide antibiotic therapy has been attributed to reduction in bronchial infection by specific bacteria. However, the airway might be populated by a more diverse microbiota, and clinical features of asthma might be associated with characteristics of the airway microbiota present. Objective: We sought to determine whether relationships exist between the composition of the airway bacterial microbiota and clinical features of asthma using culture-independent tools capable of detecting the presence and relative abundance of most known bacteria. Methods: In this pilot study bronchial epithelial brushings were collected from 65 adults with suboptimally controlled asthma participating in a multicenter study of the effects of clarithromycin on asthma control and 10 healthy control subjects. A combination of high-density 16S ribosomal RNA microarray and parallel clone library-sequencing analysis was used to profile the microbiota and examine relationships with clinical measurements. Results: Compared with control subjects, 16S ribosomal RNA amplicon concentrations (a proxy for bacterial burden) and bacterial diversity were significantly higher among asthmatic patients. In multivariate analyses airway microbiota composition and diversity were significantly correlated with bronchial hyperresponsiveness. Specifically, the relative abundance of particular phylotypes, including members of the Comamonadaceae, Sphingomonadaceae, Oxalobacteraceae, and other bacterial families were highly correlated with the degree of bronchial hyperresponsiveness. Conclusion: The composition of bronchial airway microbiota is associated with the degree of bronchial hyperresponsiveness among patients with suboptimally controlled asthma. These findings support the need for further functional studies to examine the potential contribution of members of the airway microbiota in asthma pathogenesis.

Original languageEnglish (US)
JournalJournal of Allergy and Clinical Immunology
Volume127
Issue number2
DOIs
StatePublished - Feb 2011

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Microbiota
Asthma
16S Ribosomal RNA
Oxalobacteraceae
Sphingomonadaceae
Comamonadaceae
Bacteria
Clarithromycin
Macrolides
Proxy
Multicenter Studies
Healthy Volunteers
Multivariate Analysis
Clone Cells
Anti-Bacterial Agents
Lung
Infection

Keywords

  • 16S ribosomal RNA
  • asthma
  • bacteria
  • Microbiome
  • PhyloChip

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology

Cite this

Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. / Huang, Yvonne J.; Nelson, Craig E.; Brodie, Eoin L.; Desantis, Todd Z.; Baek, Marshall S.; Liu, Jane; Woyke, Tanja; Allgaier, Martin; Bristow, Jim; Wiener-Kronish, Jeanine P.; Sutherland, E. Rand; King, Tonya S.; Icitovic, Nikolina; Martin, Richard J.; Calhoun, William; Castro, Mario; Denlinger, Loren C.; Dimango, Emily; Kraft, Monica; Peters, Stephen P.; Wasserman, Stephen I.; Wechsler, Michael E.; Boushey, Homer A.; Lynch, Susan V.

In: Journal of Allergy and Clinical Immunology, Vol. 127, No. 2, 02.2011.

Research output: Contribution to journalArticle

Huang, YJ, Nelson, CE, Brodie, EL, Desantis, TZ, Baek, MS, Liu, J, Woyke, T, Allgaier, M, Bristow, J, Wiener-Kronish, JP, Sutherland, ER, King, TS, Icitovic, N, Martin, RJ, Calhoun, W, Castro, M, Denlinger, LC, Dimango, E, Kraft, M, Peters, SP, Wasserman, SI, Wechsler, ME, Boushey, HA & Lynch, SV 2011, 'Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma', Journal of Allergy and Clinical Immunology, vol. 127, no. 2. https://doi.org/10.1016/j.jaci.2010.10.048
Huang, Yvonne J. ; Nelson, Craig E. ; Brodie, Eoin L. ; Desantis, Todd Z. ; Baek, Marshall S. ; Liu, Jane ; Woyke, Tanja ; Allgaier, Martin ; Bristow, Jim ; Wiener-Kronish, Jeanine P. ; Sutherland, E. Rand ; King, Tonya S. ; Icitovic, Nikolina ; Martin, Richard J. ; Calhoun, William ; Castro, Mario ; Denlinger, Loren C. ; Dimango, Emily ; Kraft, Monica ; Peters, Stephen P. ; Wasserman, Stephen I. ; Wechsler, Michael E. ; Boushey, Homer A. ; Lynch, Susan V. / Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. In: Journal of Allergy and Clinical Immunology. 2011 ; Vol. 127, No. 2.
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AU - Nelson, Craig E.

AU - Brodie, Eoin L.

AU - Desantis, Todd Z.

AU - Baek, Marshall S.

AU - Liu, Jane

AU - Woyke, Tanja

AU - Allgaier, Martin

AU - Bristow, Jim

AU - Wiener-Kronish, Jeanine P.

AU - Sutherland, E. Rand

AU - King, Tonya S.

AU - Icitovic, Nikolina

AU - Martin, Richard J.

AU - Calhoun, William

AU - Castro, Mario

AU - Denlinger, Loren C.

AU - Dimango, Emily

AU - Kraft, Monica

AU - Peters, Stephen P.

AU - Wasserman, Stephen I.

AU - Wechsler, Michael E.

AU - Boushey, Homer A.

AU - Lynch, Susan V.

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N2 - Background: Improvement in lung function after macrolide antibiotic therapy has been attributed to reduction in bronchial infection by specific bacteria. However, the airway might be populated by a more diverse microbiota, and clinical features of asthma might be associated with characteristics of the airway microbiota present. Objective: We sought to determine whether relationships exist between the composition of the airway bacterial microbiota and clinical features of asthma using culture-independent tools capable of detecting the presence and relative abundance of most known bacteria. Methods: In this pilot study bronchial epithelial brushings were collected from 65 adults with suboptimally controlled asthma participating in a multicenter study of the effects of clarithromycin on asthma control and 10 healthy control subjects. A combination of high-density 16S ribosomal RNA microarray and parallel clone library-sequencing analysis was used to profile the microbiota and examine relationships with clinical measurements. Results: Compared with control subjects, 16S ribosomal RNA amplicon concentrations (a proxy for bacterial burden) and bacterial diversity were significantly higher among asthmatic patients. In multivariate analyses airway microbiota composition and diversity were significantly correlated with bronchial hyperresponsiveness. Specifically, the relative abundance of particular phylotypes, including members of the Comamonadaceae, Sphingomonadaceae, Oxalobacteraceae, and other bacterial families were highly correlated with the degree of bronchial hyperresponsiveness. Conclusion: The composition of bronchial airway microbiota is associated with the degree of bronchial hyperresponsiveness among patients with suboptimally controlled asthma. These findings support the need for further functional studies to examine the potential contribution of members of the airway microbiota in asthma pathogenesis.

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