Associations between acquired antimicrobial resistance genes in the upper respiratory tract and livestock farm exposures: a case-control study in COPD and non-COPD individuals

Beatrice Cornu Hewitt; Alex Bossers; Warner van Kersen; Myrna M T de Rooij; Lidwien A M Smit

doi:10.1093/jac/dkae335

Associations between acquired antimicrobial resistance genes in the upper respiratory tract and livestock farm exposures: a case-control study in COPD and non-COPD individuals

Beatrice Cornu Hewitt^*, Alex Bossers, Warner van Kersen, Myrna M T de Rooij, Lidwien A M Smit

^*Corresponding author for this work

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

Abstract

BACKGROUND: Livestock-related emissions have been associated with aggravations of respiratory symptoms in patients with chronic obstructive pulmonary disease (COPD), potentially by altering the respiratory resistome.

OBJECTIVES: This study investigates the structure of the acquired oropharyngeal (OP) resistome of patients with COPD and controls, its interplay with the respiratory microbiome and associations with residential livestock exposure.

METHODS: In a matched case-control study in the rural Netherlands, we analysed OP swabs from 35 patients with COPD and 34 controls, none of whom had used antibiotics in the preceding 4 weeks. Resistome profiling was performed using ResCap, complemented by prior characterization of the microbiome via 16S rRNA-based sequencing. Residential livestock farm exposure was defined using distance-based variables alongside modelled concentrations of livestock-emitted microbial pollutants. We compared resistome profiles between patients with COPD and controls, examining alpha and beta diversity as well as differential abundance. Additionally, we assessed the interplay between the resistome and microbiome using co-occurrence networks and Procrustes analysis. Variations in resistome profiles were also analysed based on residential livestock exposures.

RESULTS: Patients with COPD exhibited higher resistome diversity than controls (Shannon diversity, P = 0.047), though resistome composition remained similar between groups (PERMANOVA, P = 0.19). Significant correlations were observed between the OP resistome and microbiome compositions, with distinct patterns in co-occurrence networks. Residential exposure to livestock farms was not associated with resistome alterations.

CONCLUSIONS: Our findings reveal the COPD airway as a hospitable environment for antimicrobial resistance genes, irrespective of recent antimicrobial usage. Demonstrating the interplay between the resistome and microbiome, our study underscores the importance of a deeper understanding of the resistome in respiratory health.

Original language	English
Pages (from-to)	3160–3168
Number of pages	9
Journal	Journal of Antimicrobial Chemotherapy
Volume	79
Issue number	12
Early online date	24 Sept 2024
DOIs	https://doi.org/10.1093/jac/dkae335
Publication status	Published - Dec 2024

Bibliographical note

Funding

This study was part of the Livestock Farming and Neighbouring Residents' Health (VGO) that was funded by the Ministry of Health, Welfare and Sports and the Ministry of Agriculture, Nature and Food Quality of the Netherlands. Data collection for this study was supported by a grant from the Lung Foundation Netherlands (Grant No: 3.2.11.022). The current study was funded by a Dutch Research Council (Nederlandse Organisatie voor Wetenschappelijk Onderzoek) Aspasia grant to L.A.M.S. (015.014.067).

Funders	Funder number
Ministry of Health, Welfare and Sports
Ministry of Agriculture, Nature and Food Quality of The Netherlands
Lung Foundation Netherlands	3.2.11.022
Dutch Research Council	015.014.067

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This output contributes to the following UN Sustainable Development Goals (SDGs)

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Cite this

@article{b61e8ba7b73943eebfe5bd63e6a8f614,

title = "Associations between acquired antimicrobial resistance genes in the upper respiratory tract and livestock farm exposures: a case-control study in COPD and non-COPD individuals",

abstract = "BACKGROUND: Livestock-related emissions have been associated with aggravations of respiratory symptoms in patients with chronic obstructive pulmonary disease (COPD), potentially by altering the respiratory resistome.OBJECTIVES: This study investigates the structure of the acquired oropharyngeal (OP) resistome of patients with COPD and controls, its interplay with the respiratory microbiome and associations with residential livestock exposure.METHODS: In a matched case-control study in the rural Netherlands, we analysed OP swabs from 35 patients with COPD and 34 controls, none of whom had used antibiotics in the preceding 4 weeks. Resistome profiling was performed using ResCap, complemented by prior characterization of the microbiome via 16S rRNA-based sequencing. Residential livestock farm exposure was defined using distance-based variables alongside modelled concentrations of livestock-emitted microbial pollutants. We compared resistome profiles between patients with COPD and controls, examining alpha and beta diversity as well as differential abundance. Additionally, we assessed the interplay between the resistome and microbiome using co-occurrence networks and Procrustes analysis. Variations in resistome profiles were also analysed based on residential livestock exposures.RESULTS: Patients with COPD exhibited higher resistome diversity than controls (Shannon diversity, P = 0.047), though resistome composition remained similar between groups (PERMANOVA, P = 0.19). Significant correlations were observed between the OP resistome and microbiome compositions, with distinct patterns in co-occurrence networks. Residential exposure to livestock farms was not associated with resistome alterations.CONCLUSIONS: Our findings reveal the COPD airway as a hospitable environment for antimicrobial resistance genes, irrespective of recent antimicrobial usage. Demonstrating the interplay between the resistome and microbiome, our study underscores the importance of a deeper understanding of the resistome in respiratory health.",

author = "{Cornu Hewitt}, Beatrice and Alex Bossers and {van Kersen}, Warner and {de Rooij}, {Myrna M T} and Smit, {Lidwien A M}",

note = "{\textcopyright} The Author(s) 2024. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.",

year = "2024",

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Associations between acquired antimicrobial resistance genes in the upper respiratory tract and livestock farm exposures: a case-control study in COPD and non-COPD individuals. / Cornu Hewitt, Beatrice ; Bossers, Alex ; van Kersen, Warner et al.
In: Journal of Antimicrobial Chemotherapy, Vol. 79, No. 12, 12.2024, p. 3160–3168.

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

TY - JOUR

T1 - Associations between acquired antimicrobial resistance genes in the upper respiratory tract and livestock farm exposures

T2 - a case-control study in COPD and non-COPD individuals

AU - Cornu Hewitt, Beatrice

AU - Bossers, Alex

AU - van Kersen, Warner

AU - de Rooij, Myrna M T

AU - Smit, Lidwien A M

N1 - © The Author(s) 2024. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.

PY - 2024/12

Y1 - 2024/12

N2 - BACKGROUND: Livestock-related emissions have been associated with aggravations of respiratory symptoms in patients with chronic obstructive pulmonary disease (COPD), potentially by altering the respiratory resistome.OBJECTIVES: This study investigates the structure of the acquired oropharyngeal (OP) resistome of patients with COPD and controls, its interplay with the respiratory microbiome and associations with residential livestock exposure.METHODS: In a matched case-control study in the rural Netherlands, we analysed OP swabs from 35 patients with COPD and 34 controls, none of whom had used antibiotics in the preceding 4 weeks. Resistome profiling was performed using ResCap, complemented by prior characterization of the microbiome via 16S rRNA-based sequencing. Residential livestock farm exposure was defined using distance-based variables alongside modelled concentrations of livestock-emitted microbial pollutants. We compared resistome profiles between patients with COPD and controls, examining alpha and beta diversity as well as differential abundance. Additionally, we assessed the interplay between the resistome and microbiome using co-occurrence networks and Procrustes analysis. Variations in resistome profiles were also analysed based on residential livestock exposures.RESULTS: Patients with COPD exhibited higher resistome diversity than controls (Shannon diversity, P = 0.047), though resistome composition remained similar between groups (PERMANOVA, P = 0.19). Significant correlations were observed between the OP resistome and microbiome compositions, with distinct patterns in co-occurrence networks. Residential exposure to livestock farms was not associated with resistome alterations.CONCLUSIONS: Our findings reveal the COPD airway as a hospitable environment for antimicrobial resistance genes, irrespective of recent antimicrobial usage. Demonstrating the interplay between the resistome and microbiome, our study underscores the importance of a deeper understanding of the resistome in respiratory health.

AB - BACKGROUND: Livestock-related emissions have been associated with aggravations of respiratory symptoms in patients with chronic obstructive pulmonary disease (COPD), potentially by altering the respiratory resistome.OBJECTIVES: This study investigates the structure of the acquired oropharyngeal (OP) resistome of patients with COPD and controls, its interplay with the respiratory microbiome and associations with residential livestock exposure.METHODS: In a matched case-control study in the rural Netherlands, we analysed OP swabs from 35 patients with COPD and 34 controls, none of whom had used antibiotics in the preceding 4 weeks. Resistome profiling was performed using ResCap, complemented by prior characterization of the microbiome via 16S rRNA-based sequencing. Residential livestock farm exposure was defined using distance-based variables alongside modelled concentrations of livestock-emitted microbial pollutants. We compared resistome profiles between patients with COPD and controls, examining alpha and beta diversity as well as differential abundance. Additionally, we assessed the interplay between the resistome and microbiome using co-occurrence networks and Procrustes analysis. Variations in resistome profiles were also analysed based on residential livestock exposures.RESULTS: Patients with COPD exhibited higher resistome diversity than controls (Shannon diversity, P = 0.047), though resistome composition remained similar between groups (PERMANOVA, P = 0.19). Significant correlations were observed between the OP resistome and microbiome compositions, with distinct patterns in co-occurrence networks. Residential exposure to livestock farms was not associated with resistome alterations.CONCLUSIONS: Our findings reveal the COPD airway as a hospitable environment for antimicrobial resistance genes, irrespective of recent antimicrobial usage. Demonstrating the interplay between the resistome and microbiome, our study underscores the importance of a deeper understanding of the resistome in respiratory health.

U2 - 10.1093/jac/dkae335

DO - 10.1093/jac/dkae335

M3 - Article

C2 - 39315772

SN - 0305-7453

VL - 79

SP - 3160

EP - 3168

JO - Journal of Antimicrobial Chemotherapy

JF - Journal of Antimicrobial Chemotherapy

IS - 12

ER -

Associations between acquired antimicrobial resistance genes in the upper respiratory tract and livestock farm exposures: a case-control study in COPD and non-COPD individuals

Abstract

Bibliographical note

Funding

UN SDGs

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