Air pollution from livestock farms and the oropharyngeal microbiome of COPD patients and controls

Warner van Kersen; Alex Bossers; Wouter A.A. de Steenhuijsen Piters; Myrna M.T. de Rooij; Marc Bonten; Ad C. Fluit; Dick Heederik; Fernanda L. Paganelli; Malbert Rogers; Marco Viveen; Debby Bogaert; Helen L. Leavis; Lidwien A.M. Smit

doi:10.1016/j.envint.2022.107497

Air pollution from livestock farms and the oropharyngeal microbiome of COPD patients and controls

Warner van Kersen, Alex Bossers, Wouter A.A. de Steenhuijsen Piters, Myrna M.T. de Rooij, Marc Bonten, Ad C. Fluit, Dick Heederik, Fernanda L. Paganelli, Malbert Rogers, Marco Viveen, Debby Bogaert, Helen L. Leavis, Lidwien A.M. Smit^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

Air pollution from livestock farms is known to affect respiratory health of patients with chronic obstructive pulmonary disease (COPD). The mechanisms behind this relationship, however, remain poorly understood. We hypothesise that air pollutants could influence respiratory health through modulation of the airway microbiome. Therefore, we studied associations between air pollution exposure and the oropharyngeal microbiota (OPM) composition of COPD patients and controls in a livestock-dense area. Oropharyngeal swabs were collected from 99 community-based (mostly mild) COPD cases and 184 controls (baseline), and after 6 and 12 weeks. Participants were non-smokers or former smokers. Annual average livestock-related outdoor air pollution at the home address was predicted using dispersion modelling. OPM composition was analysed using 16S rRNA-based sequencing in all baseline samples and 6-week and 12-week repeated samples of 20 randomly selected subjects (n = 323 samples). A random selection of negative control swabs, taken every sampling day, were also included in the downstream analysis. Both farm-emitted endotoxin and PM₁₀ levels were associated with increased OPM richness in COPD patients (p < 0.05) but not in controls. COPD case-control status was not associated with community structure, while correcting for known confounders (multivariate PERMANOVA p > 0.05). However, members of the genus Streptococcus were more abundant in COPD patients (Benjamini-Hochberg adjusted p < 0.01). Moderate correlation was found between ordinations of 20 subjects analysed at 0, 6, and 12 weeks (Procrustes r = 0.52 to 0.66; p < 0.05; Principal coordinate analysis of Bray-Curtis dissimilarity), indicating that the OPM is relatively stable over a 12 week period and that a single sample sufficiently represents the OPM. Air pollution from livestock farms is associated with OPM richness of COPD patients, suggesting that the OPM of COPD patients is susceptible to alterations induced by exposure to air pollutants.

Original language	English
Article number	107497
Pages (from-to)	1-9
Journal	Environment International
Volume	169
DOIs	https://doi.org/10.1016/j.envint.2022.107497
Publication status	Published - Nov 2022

Keywords

Air Pollutants/analysis
Air Pollution/adverse effects
Animals
Endotoxins/analysis
Farms
Humans
Livestock
Microbiota
Pulmonary Disease, Chronic Obstructive
RNA, Ribosomal, 16S/analysis

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van Kersen, W., Bossers, A., de Steenhuijsen Piters, W. A. A., de Rooij, M. M. T., Bonten, M., Fluit, A. C., Heederik, D., Paganelli, F. L., Rogers, M., Viveen, M., Bogaert, D., Leavis, H. L., & Smit, L. A. M. (2022). Air pollution from livestock farms and the oropharyngeal microbiome of COPD patients and controls. Environment International, 169, 1-9. Article 107497. https://doi.org/10.1016/j.envint.2022.107497

@article{5f8dc493c8ee4885a89a76719ebaf800,

title = "Air pollution from livestock farms and the oropharyngeal microbiome of COPD patients and controls",

abstract = "Air pollution from livestock farms is known to affect respiratory health of patients with chronic obstructive pulmonary disease (COPD). The mechanisms behind this relationship, however, remain poorly understood. We hypothesise that air pollutants could influence respiratory health through modulation of the airway microbiome. Therefore, we studied associations between air pollution exposure and the oropharyngeal microbiota (OPM) composition of COPD patients and controls in a livestock-dense area. Oropharyngeal swabs were collected from 99 community-based (mostly mild) COPD cases and 184 controls (baseline), and after 6 and 12 weeks. Participants were non-smokers or former smokers. Annual average livestock-related outdoor air pollution at the home address was predicted using dispersion modelling. OPM composition was analysed using 16S rRNA-based sequencing in all baseline samples and 6-week and 12-week repeated samples of 20 randomly selected subjects (n = 323 samples). A random selection of negative control swabs, taken every sampling day, were also included in the downstream analysis. Both farm-emitted endotoxin and PM10 levels were associated with increased OPM richness in COPD patients (p < 0.05) but not in controls. COPD case-control status was not associated with community structure, while correcting for known confounders (multivariate PERMANOVA p > 0.05). However, members of the genus Streptococcus were more abundant in COPD patients (Benjamini-Hochberg adjusted p < 0.01). Moderate correlation was found between ordinations of 20 subjects analysed at 0, 6, and 12 weeks (Procrustes r = 0.52 to 0.66; p < 0.05; Principal coordinate analysis of Bray-Curtis dissimilarity), indicating that the OPM is relatively stable over a 12 week period and that a single sample sufficiently represents the OPM. Air pollution from livestock farms is associated with OPM richness of COPD patients, suggesting that the OPM of COPD patients is susceptible to alterations induced by exposure to air pollutants.",

keywords = "Air Pollutants/analysis, Air Pollution/adverse effects, Animals, Endotoxins/analysis, Farms, Humans, Livestock, Microbiota, Pulmonary Disease, Chronic Obstructive, RNA, Ribosomal, 16S/analysis",

author = "{van Kersen}, Warner and Alex Bossers and {de Steenhuijsen Piters}, {Wouter A.A.} and {de Rooij}, {Myrna M.T.} and Marc Bonten and Fluit, {Ad C.} and Dick Heederik and Paganelli, {Fernanda L.} and Malbert Rogers and Marco Viveen and Debby Bogaert and Leavis, {Helen L.} and Smit, {Lidwien A.M.}",

year = "2022",

month = nov,

doi = "10.1016/j.envint.2022.107497",

language = "English",

volume = "169",

pages = "1--9",

journal = "Environment International",

issn = "0160-4120",

publisher = "Elsevier Limited",

}

van Kersen, W, Bossers, A, de Steenhuijsen Piters, WAA, de Rooij, MMT, Bonten, M, Fluit, AC, Heederik, D, Paganelli, FL, Rogers, M, Viveen, M, Bogaert, D , Leavis, HL & Smit, LAM 2022, 'Air pollution from livestock farms and the oropharyngeal microbiome of COPD patients and controls', Environment International, vol. 169, 107497, pp. 1-9. https://doi.org/10.1016/j.envint.2022.107497

TY - JOUR

T1 - Air pollution from livestock farms and the oropharyngeal microbiome of COPD patients and controls

AU - van Kersen, Warner

AU - Bossers, Alex

AU - de Steenhuijsen Piters, Wouter A.A.

AU - de Rooij, Myrna M.T.

AU - Bonten, Marc

AU - Fluit, Ad C.

AU - Heederik, Dick

AU - Paganelli, Fernanda L.

AU - Rogers, Malbert

AU - Viveen, Marco

AU - Bogaert, Debby

AU - Leavis, Helen L.

AU - Smit, Lidwien A.M.

PY - 2022/11

Y1 - 2022/11

N2 - Air pollution from livestock farms is known to affect respiratory health of patients with chronic obstructive pulmonary disease (COPD). The mechanisms behind this relationship, however, remain poorly understood. We hypothesise that air pollutants could influence respiratory health through modulation of the airway microbiome. Therefore, we studied associations between air pollution exposure and the oropharyngeal microbiota (OPM) composition of COPD patients and controls in a livestock-dense area. Oropharyngeal swabs were collected from 99 community-based (mostly mild) COPD cases and 184 controls (baseline), and after 6 and 12 weeks. Participants were non-smokers or former smokers. Annual average livestock-related outdoor air pollution at the home address was predicted using dispersion modelling. OPM composition was analysed using 16S rRNA-based sequencing in all baseline samples and 6-week and 12-week repeated samples of 20 randomly selected subjects (n = 323 samples). A random selection of negative control swabs, taken every sampling day, were also included in the downstream analysis. Both farm-emitted endotoxin and PM10 levels were associated with increased OPM richness in COPD patients (p < 0.05) but not in controls. COPD case-control status was not associated with community structure, while correcting for known confounders (multivariate PERMANOVA p > 0.05). However, members of the genus Streptococcus were more abundant in COPD patients (Benjamini-Hochberg adjusted p < 0.01). Moderate correlation was found between ordinations of 20 subjects analysed at 0, 6, and 12 weeks (Procrustes r = 0.52 to 0.66; p < 0.05; Principal coordinate analysis of Bray-Curtis dissimilarity), indicating that the OPM is relatively stable over a 12 week period and that a single sample sufficiently represents the OPM. Air pollution from livestock farms is associated with OPM richness of COPD patients, suggesting that the OPM of COPD patients is susceptible to alterations induced by exposure to air pollutants.

AB - Air pollution from livestock farms is known to affect respiratory health of patients with chronic obstructive pulmonary disease (COPD). The mechanisms behind this relationship, however, remain poorly understood. We hypothesise that air pollutants could influence respiratory health through modulation of the airway microbiome. Therefore, we studied associations between air pollution exposure and the oropharyngeal microbiota (OPM) composition of COPD patients and controls in a livestock-dense area. Oropharyngeal swabs were collected from 99 community-based (mostly mild) COPD cases and 184 controls (baseline), and after 6 and 12 weeks. Participants were non-smokers or former smokers. Annual average livestock-related outdoor air pollution at the home address was predicted using dispersion modelling. OPM composition was analysed using 16S rRNA-based sequencing in all baseline samples and 6-week and 12-week repeated samples of 20 randomly selected subjects (n = 323 samples). A random selection of negative control swabs, taken every sampling day, were also included in the downstream analysis. Both farm-emitted endotoxin and PM10 levels were associated with increased OPM richness in COPD patients (p < 0.05) but not in controls. COPD case-control status was not associated with community structure, while correcting for known confounders (multivariate PERMANOVA p > 0.05). However, members of the genus Streptococcus were more abundant in COPD patients (Benjamini-Hochberg adjusted p < 0.01). Moderate correlation was found between ordinations of 20 subjects analysed at 0, 6, and 12 weeks (Procrustes r = 0.52 to 0.66; p < 0.05; Principal coordinate analysis of Bray-Curtis dissimilarity), indicating that the OPM is relatively stable over a 12 week period and that a single sample sufficiently represents the OPM. Air pollution from livestock farms is associated with OPM richness of COPD patients, suggesting that the OPM of COPD patients is susceptible to alterations induced by exposure to air pollutants.

KW - Air Pollutants/analysis

KW - Air Pollution/adverse effects

KW - Animals

KW - Endotoxins/analysis

KW - Farms

KW - Humans

KW - Livestock

KW - Microbiota

KW - Pulmonary Disease, Chronic Obstructive

KW - RNA, Ribosomal, 16S/analysis

UR - http://www.scopus.com/inward/record.url?scp=85137584427&partnerID=8YFLogxK

U2 - 10.1016/j.envint.2022.107497

DO - 10.1016/j.envint.2022.107497

M3 - Article

C2 - 36088872

AN - SCOPUS:85137584427

SN - 0160-4120

VL - 169

SP - 1

EP - 9

JO - Environment International

JF - Environment International

M1 - 107497

ER -

Air pollution from livestock farms and the oropharyngeal microbiome of COPD patients and controls

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