Increased risk of pneumonia in residents living near poultry farms: does the upper respiratory tract microbiota play a role?

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Abstract

Background

Air pollution has been shown to increase the susceptibility to community-acquired pneumonia (CAP). Previously, we observed an increased incidence of CAP in adults living within 1 km from poultry farms, potentially related to particulate matter and endotoxin emissions. We aim to confirm the increased risk of CAP near poultry farms by refined spatial analyses, and we hypothesize that the oropharyngeal microbiota composition in CAP patients may be associated with residential proximity to poultry farms.

Methods

A spatial kernel model was used to analyze the association between proximity to poultry farms and CAP diagnosis, obtained from electronic medical records of 92,548 GP patients. The oropharyngeal microbiota composition was determined in 126 hospitalized CAP patients using 16S-rRNA-based sequencing, and analyzed in relation to residential proximity to poultry farms.

Results

Kernel analysis confirmed a significantly increased risk of CAP when living near poultry farms, suggesting an excess risk up to 1.15 km, followed by a sharp decline. Overall, the oropharyngeal microbiota composition differed borderline significantly between patients living <1 km and ≥1 km from poultry farms (PERMANOVA p = 0.075). Results suggested a higher abundance of Streptococcus pneumoniae (mean relative abundance 34.9% vs. 22.5%, p = 0.058) in patients living near poultry farms, which was verified by unsupervised clustering analysis, showing overrepresentation of a S. pneumoniae cluster near poultry farms ( p = 0.049).

Conclusion

Living near poultry farms is associated with an 11% increased risk of CAP, possibly resulting from changes in the upper respiratory tract microbiota composition in susceptible individuals. The abundance of S. pneumoniae near farms needs to be replicated in larger, independent studies.

Electronic supplementary material

The online version of this article (doi:10.1186/s41479-017-0027-0) contains supplementary material, which is available to authorized users.

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Most cited references 24

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Yoav Benjamini, Yosef Hochberg (1995)

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Respiratory risks from household air pollution in low and middle income countries.

Stephen Gordon, Nigel G. Bruce, Jonathan Grigg … (2014)

A third of the world's population uses solid fuel derived from plant material (biomass) or coal for cooking, heating, or lighting. These fuels are smoky, often used in an open fire or simple stove with incomplete combustion, and result in a large amount of household air pollution when smoke is poorly vented. Air pollution is the biggest environmental cause of death worldwide, with household air pollution accounting for about 3·5-4 million deaths every year. Women and children living in severe poverty have the greatest exposures to household air pollution. In this Commission, we review evidence for the association between household air pollution and respiratory infections, respiratory tract cancers, and chronic lung diseases. Respiratory infections (comprising both upper and lower respiratory tract infections with viruses, bacteria, and mycobacteria) have all been associated with exposure to household air pollution. Respiratory tract cancers, including both nasopharyngeal cancer and lung cancer, are strongly associated with pollution from coal burning and further data are needed about other solid fuels. Chronic lung diseases, including chronic obstructive pulmonary disease and bronchiectasis in women, are associated with solid fuel use for cooking, and the damaging effects of exposure to household air pollution in early life on lung development are yet to be fully described. We also review appropriate ways to measure exposure to household air pollution, as well as study design issues and potential effective interventions to prevent these disease burdens. Measurement of household air pollution needs individual, rather than fixed in place, monitoring because exposure varies by age, gender, location, and household role. Women and children are particularly susceptible to the toxic effects of pollution and are exposed to the highest concentrations. Interventions should target these high-risk groups and be of sufficient quality to make the air clean. To make clean energy available to all people is the long-term goal, with an intermediate solution being to make available energy that is clean enough to have a health impact.

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Towards an ecology of the lung: new conceptual models of pulmonary microbiology and pneumonia pathogenesis.

Robert P. Dickson, John Erb-Downward, Gary Huffnagle (2014)

Pneumonia is a major cause of morbidity and mortality for which no new methods of treatment have entered clinical practice since the discovery of antibiotics. Innovations in the techniques of culture-independent microbial identification have shown that the lungs, previously deemed sterile in the absence of infection, contain diverse and dynamic communities of microbes. In this Personal View, we argue that these observations have shown the inadequacy of traditional conceptual models of lung microbiology and the pathogenesis of pneumonia, hampering progress in research and practice. We propose three new conceptual models to replace the traditional models of lung microbiology: an adapted island model of lung biogeography, the effect of environmental gradients on lung microbiota, and pneumonia as an emergent phenomenon propelled by unexplored positive feedback loops. We argue that the ecosystem of lung microbiota has all of the features of a complex adaptive system: diverse entities interacting with each other within a common space, showing interdependent actions and possessing the capacity to adapt to changes in conditions. Complex adaptive systems are fundamentally different in behaviour from the simple, linear systems typified by the traditional model of pneumonia pathogenesis, and need distinct analytical approaches. Copyright © 2014 Elsevier Ltd. All rights reserved.

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Author and article information

Contributors

Lidwien A. M. Smit: +31 30 2538696 , L.A.Smit@uu.nl

Journal

Journal ID (nlm-ta): Pneumonia (Nathan)

Journal ID (iso-abbrev): Pneumonia (Nathan)

Title: Pneumonia

Publisher: BioMed Central (London )

ISSN (Electronic): 2200-6133

Publication date (Electronic): 25 February 2017

Publication date PMC-release: 25 February 2017

Publication date Collection: 2017

Volume: 9

Electronic Location Identifier: 3

Affiliations

[1 ]ISNI 0000000120346234, GRID grid.5477.1, Institute for Risk Assessment Sciences (IRAS), Division Environmental Epidemiology, , Utrecht University, ; PO Box 80178, 3508 TD Utrecht, The Netherlands

[2 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Central Veterinary Institute, , Wageningen University and Research Centre, ; Lelystad, The Netherlands

[3 ]Department of Paediatric Immunology and Infectious Diseases, The Wilhelmina Children’s Hospital/University Medical Center Utrecht, Utrecht, The Netherlands

[4 ]ISNI 0000 0004 0396 792X, GRID grid.413972.a, Department of Medical Microbiology, , Albert Schweitzer Hospital, ; Dordrecht, The Netherlands

[5 ]GRID grid.416373.4, Laboratory of Medical Microbiology and Immunology, , St. Elisabeth Hospital, ; Tilburg, The Netherlands

[6 ]Department of Medical Microbiology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

[7 ]ISNI 000000040459992X, GRID grid.5645.2, Department of Virology, , Erasmus Medical Centre, ; Rotterdam, The Netherlands

[8 ]ISNI 0000 0000 9730 5476, GRID grid.413764.3, , Current address: GD Animal Health, ; Deventer, The Netherlands

[9 ]ISNI 0000 0001 2208 0118, GRID grid.31147.30, , National Institute for Public Health and the Environment, ; Bilthoven, The Netherlands

[10 ]ISNI 0000 0001 0681 4687, GRID grid.416005.6, , NIVEL, Netherlands Institute for Health Services Research, ; Utrecht, The Netherlands

Article

Publisher ID: 27

DOI: 10.1186/s41479-017-0027-0

PMC ID: 5471663

PubMed ID: 28702305

SO-VID: 93b5ecc8-d2e3-45d8-9774-c2dc3cdd6403

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 11 August 2016

Date accepted : 18 January 2017

Funding

Funded by: Wilhelmina Children's Hospital Fund

Funded by: FundRef http://dx.doi.org/10.13039/501100001826, ZonMW;

Award ID: 91209010

Funded by: FundRef http://dx.doi.org/10.13039/501100003195, Ministerie van Economische Zaken;

Award ID: BO-20-009-030

Funded by: FundRef http://dx.doi.org/10.13039/501100003195, Ministerie van Economische Zaken;

Funded by: FundRef http://dx.doi.org/10.13039/501100002999, Ministerie van Volksgezondheid, Welzijn en Sport;

Funded by: NWO

Award ID: VENI grant 91610121

Award Recipient : Debby Bogaert

Custom metadata

Keywords: air pollution,environment,microbiome,pneumonia

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Keywords: air pollution, environment, microbiome, pneumonia

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Increased risk of pneumonia in residents living near poultry farms: does the upper respiratory tract microbiota play a role?

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Abstract

Background

Methods

Results

Conclusion

Electronic supplementary material

Related collections

Pneumonia, sex, and the environment

Most cited references 24

Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

Respiratory risks from household air pollution in low and middle income countries.

Towards an ecology of the lung: new conceptual models of pulmonary microbiology and pneumonia pathogenesis.

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Cited by 20

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