Past, Present, and Future Research on the Lung Microbiome in Inflammatory Airway Disease

doi:10.1016/j.chest.2019.05.011

Chest

Volume 156, Issue 2, August 2019, Pages 376-382

https://doi.org/10.1016/j.chest.2019.05.011 Get rights and content

COPD, asthma, and cystic fibrosis (CF) are obstructive lung diseases with distinct pathophysiologies and clinical phenotypes. In this paper, we highlight recent advances in our understanding of relationships between clinical phenotypes, host inflammatory response, and lung microbiota in these diseases. Although COPD, asthma, and CF largely have distinct lung microbiota and inflammatory profiles, certain commonalities exist. In all three of these lung diseases, and in healthy persons, anaerobic taxa that are typically associated with oral microbiota (eg, Prevotella species, Veillonella species) are present in the airways and associated with increased host inflammatory response. Similarly, across all three diseases, members of the Proteobacteria phylum are associated with more advanced disease. Finally, we highlight challenges in translating these findings into advances in clinical care, including continued knowledge gaps regarding the causal relationships between host inflammatory response, lung microbiota, medication effects, and clinical phenotypes.

Section snippets

COPD

Over the last 10 to 15 years, studies from multiple laboratories have helped highlight the key correlations between the lung microbiota and host response at all stages of COPD.6, 7, 9, 11^-19 For tissue studies, few differences in the microbiota can be identified between smokers and nonsmokers or between mild and moderate COPD.9, 18 Similarly, studies on the BAL bacterial community have identified few differences between smokers, nonsmokers, and early COPD.7, 11 Although Segal et al¹¹ did not

Asthma

The role of microbiota in asthma pathogenesis has, until recently, focused on the early life period and interactions between microbiota (gut and nasopharynx), the maturation of immune responses during infancy, and subsequent risk for asthma during childhood. Earlier epidemiologic studies conducted in Europe and the United States were seminal in highlighting links between differences in environmental microbial exposures and the prevalence of allergic diseases including asthma.24, 25, 26 Numerous

CF

Over the past decade, studies of the CF lung microbiome have expanded our understanding of the relationships between CF lung microbiota, inflammation, and lung disease. Alterations in lung microbiota and inflammatory markers in CF begin as early as infancy. Lung microbiota, as measured in BAL fluid, differs in infants with CF compared with healthy infant control subjects.⁵² Studies of BAL fluid CF animal models⁵³ and infants with CF⁵⁴ demonstrate that inflammation can occur in the absence of

Conclusions

From this review, relationships between the microbiota and host vary by the lung disease being studied; however, many taxa are common to lungs in health and disease. Across these three inflammatory airway diseases with distinct pathophysiology, certain common host-microbial interactions have been identified. For example, members of the Proteobacteria phylum have consistently been identified as enriched in individuals with COPD, asthma, and CF vs healthy control subjects, and have been

Acknowledgments

Financial/nonfinancial disclosures: None declared.

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: Drs Caverly, Huang, and Sze contributed equally to this manuscript.

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Chest

Translating Basic Research Into Clinical PracticePast, Present, and Future Research on the Lung Microbiome in Inflammatory Airway Disease

Section snippets

COPD

Asthma

CF

Conclusions

Acknowledgments

Sci Total Environ

Chest

J Allergy Clin Immunol

Respir Med

J Allergy Clin Immunol

J Allerg Clin Immunol

Lancet

Cell Host Microbe

Cell Host Microbe

J Allergy Clin Immunol

J Allergy Clin Immunol

J Allergy Clin Immunol

J Cyst Fibros

Chest

Belowground microbiota and the health of tree crops

Front Microbiol

Microbial ecology of the cryosphere: sea ice and glacial habitats

Nat Rev Microbiol

Bronchoalveolar lavage for diagnosing acute bacterial pneumonia

J Infect Dis

Disordered microbial communities in asthmatic airways

PLoS One

Analysis of the lung microbiome in the “healthy” smoker and in COPD

PLoS One

Analysis of culture-dependent versus culture-independent techniques for identification of bacteria in clinically obtained bronchoalveolar lavage fluid

J Clin Microbiol

The lung tissue microbiome in chronic obstructive pulmonary disease

Am J Respir Crit Care Med

Spatial variation in the healthy human lung microbiome and the adapted island model of lung biogeography

Ann Am Thorac Soc

Enrichment of lung microbiome with supraglottic taxa is associated with increased pulmonary inflammation

Microbiome

Enrichment of the lung microbiome with oral taxa is associated with lung inflammation of a Th17 phenotype

Nat Microbiol

The host response to the lung microbiome in chronic obstructive pulmonary disease

Am J Respir Crit Care Med

Airway microbiome dynamics in exacerbations of chronic obstructive pulmonary disease

J Clin Microbiol

A persistent and diverse airway microbiota present during chronic obstructive pulmonary disease exacerbations

OMICS

Longitudinal profiling of the lung microbiome in the AERIS study demonstrates repeatability of bacterial and eosinophilic COPD exacerbations

Thorax

Lung microbiome dynamics in COPD exacerbations

Eur Respir J

The lung tissue microbiota of mild and moderate chronic obstructive pulmonary disease

Microbiome

An airway epithelial IL-17A response signature identifies a steroid-unresponsive COPD patient subgroup

J Clin Invest

Association between functional small airway disease and FEV1 decline in chronic obstructive pulmonary disease

Am J Respir Crit Care Med

Clinical significance of symptoms in smokers with preserved pulmonary function

N Engl J Med

Translating Basic Research Into Clinical Practice
Past, Present, and Future Research on the Lung Microbiome in Inflammatory Airway Disease