Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam: an epidemiological and genomic analysis

Vinh Trung Nguyen, Dorota Jamrozy, Sébastien Matamoros, Juan J. Carrique-Mas, Huynh Mai Ho, Quoc Hieu Thai, Thi Nhu Mai Nguyen, Jaap A. Wagenaar, Guy Thwaites, Julian Parkhill, Constance Schultsz, Thi Hoa Ngo

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Abstract

OBJECTIVES: To investigate the risk of colonization with ESBL-producing Escherichia coli (ESBL-Ec) in humans in Vietnam associated with non-intensive chicken farming. METHODS: Faecal samples from 204 randomly selected farmers and their chickens, and from 306 age- and sex-matched community-based individuals who did not raise poultry were collected. Antimicrobial usage in chickens and humans was assessed by medicine cabinet surveys. WGS was employed to obtain a high-resolution genomic comparison between ESBL-Ec isolated from humans and chickens. RESULTS: The adjusted prevalence of ESBL-Ec colonization was 20.0% (95% CI 10.8%-29.1%) and 35.2% (95% CI 30.4%-40.1%) in chicken farms and humans in Vietnam, respectively. Colonization with ESBL-Ec in humans was associated with antimicrobial usage (OR = 2.52, 95% CI = 1.08-5.87) but not with involvement in chicken farming. blaCTX-M-55 was the most common ESBL-encoding gene in strains isolated from chickens (74.4%) compared with blaCTX-M-27 in human strains (47.0%). In 3 of 204 (1.5%) of the farms, identical ESBL genes were detected in ESBL-Ec isolated from farmers and their chickens. Genomic similarity indicating recent sharing of ESBL-Ec between chickens and farmers was found in only one of these farms. CONCLUSIONS: The integration of epidemiological and genomic data in this study has demonstrated a limited contribution of non-intensive chicken farming to ESBL-Ec colonization in humans in Vietnam and further emphasizes the importance of reducing antimicrobial usage in both human and animal host reservoirs.

LanguageEnglish
Pages561-570
JournalThe Journal of antimicrobial chemotherapy
Volume74
Issue number3
DOIs
Publication statusPublished - 1 Mar 2019

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Vietnam
Agriculture
Chickens
Escherichia coli
Poultry
Genes
Medicine

Cite this

Nguyen, Vinh Trung ; Jamrozy, Dorota ; Matamoros, Sébastien ; Carrique-Mas, Juan J. ; Ho, Huynh Mai ; Thai, Quoc Hieu ; Nguyen, Thi Nhu Mai ; Wagenaar, Jaap A. ; Thwaites, Guy ; Parkhill, Julian ; Schultsz, Constance ; Ngo, Thi Hoa. / Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam : an epidemiological and genomic analysis. In: The Journal of antimicrobial chemotherapy. 2019 ; Vol. 74, No. 3. pp. 561-570.
@article{1628286b837348b192939132d0623aea,
title = "Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam: an epidemiological and genomic analysis",
abstract = "OBJECTIVES: To investigate the risk of colonization with ESBL-producing Escherichia coli (ESBL-Ec) in humans in Vietnam associated with non-intensive chicken farming. METHODS: Faecal samples from 204 randomly selected farmers and their chickens, and from 306 age- and sex-matched community-based individuals who did not raise poultry were collected. Antimicrobial usage in chickens and humans was assessed by medicine cabinet surveys. WGS was employed to obtain a high-resolution genomic comparison between ESBL-Ec isolated from humans and chickens. RESULTS: The adjusted prevalence of ESBL-Ec colonization was 20.0{\%} (95{\%} CI 10.8{\%}-29.1{\%}) and 35.2{\%} (95{\%} CI 30.4{\%}-40.1{\%}) in chicken farms and humans in Vietnam, respectively. Colonization with ESBL-Ec in humans was associated with antimicrobial usage (OR = 2.52, 95{\%} CI = 1.08-5.87) but not with involvement in chicken farming. blaCTX-M-55 was the most common ESBL-encoding gene in strains isolated from chickens (74.4{\%}) compared with blaCTX-M-27 in human strains (47.0{\%}). In 3 of 204 (1.5{\%}) of the farms, identical ESBL genes were detected in ESBL-Ec isolated from farmers and their chickens. Genomic similarity indicating recent sharing of ESBL-Ec between chickens and farmers was found in only one of these farms. CONCLUSIONS: The integration of epidemiological and genomic data in this study has demonstrated a limited contribution of non-intensive chicken farming to ESBL-Ec colonization in humans in Vietnam and further emphasizes the importance of reducing antimicrobial usage in both human and animal host reservoirs.",
author = "Nguyen, {Vinh Trung} and Dorota Jamrozy and S{\'e}bastien Matamoros and Carrique-Mas, {Juan J.} and Ho, {Huynh Mai} and Thai, {Quoc Hieu} and Nguyen, {Thi Nhu Mai} and Wagenaar, {Jaap A.} and Guy Thwaites and Julian Parkhill and Constance Schultsz and Ngo, {Thi Hoa}",
year = "2019",
month = "3",
day = "1",
doi = "10.1093/jac/dky506",
language = "English",
volume = "74",
pages = "561--570",
journal = "Journal of Antimicrobial Chemotherapy",
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Nguyen, VT, Jamrozy, D, Matamoros, S, Carrique-Mas, JJ, Ho, HM, Thai, QH, Nguyen, TNM, Wagenaar, JA, Thwaites, G, Parkhill, J, Schultsz, C & Ngo, TH 2019, 'Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam: an epidemiological and genomic analysis', The Journal of antimicrobial chemotherapy, vol. 74, no. 3, pp. 561-570. https://doi.org/10.1093/jac/dky506

Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam : an epidemiological and genomic analysis. / Nguyen, Vinh Trung; Jamrozy, Dorota; Matamoros, Sébastien; Carrique-Mas, Juan J.; Ho, Huynh Mai; Thai, Quoc Hieu; Nguyen, Thi Nhu Mai; Wagenaar, Jaap A.; Thwaites, Guy; Parkhill, Julian; Schultsz, Constance; Ngo, Thi Hoa.

In: The Journal of antimicrobial chemotherapy, Vol. 74, No. 3, 01.03.2019, p. 561-570.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam

T2 - Journal of Antimicrobial Chemotherapy

AU - Nguyen, Vinh Trung

AU - Jamrozy, Dorota

AU - Matamoros, Sébastien

AU - Carrique-Mas, Juan J.

AU - Ho, Huynh Mai

AU - Thai, Quoc Hieu

AU - Nguyen, Thi Nhu Mai

AU - Wagenaar, Jaap A.

AU - Thwaites, Guy

AU - Parkhill, Julian

AU - Schultsz, Constance

AU - Ngo, Thi Hoa

PY - 2019/3/1

Y1 - 2019/3/1

N2 - OBJECTIVES: To investigate the risk of colonization with ESBL-producing Escherichia coli (ESBL-Ec) in humans in Vietnam associated with non-intensive chicken farming. METHODS: Faecal samples from 204 randomly selected farmers and their chickens, and from 306 age- and sex-matched community-based individuals who did not raise poultry were collected. Antimicrobial usage in chickens and humans was assessed by medicine cabinet surveys. WGS was employed to obtain a high-resolution genomic comparison between ESBL-Ec isolated from humans and chickens. RESULTS: The adjusted prevalence of ESBL-Ec colonization was 20.0% (95% CI 10.8%-29.1%) and 35.2% (95% CI 30.4%-40.1%) in chicken farms and humans in Vietnam, respectively. Colonization with ESBL-Ec in humans was associated with antimicrobial usage (OR = 2.52, 95% CI = 1.08-5.87) but not with involvement in chicken farming. blaCTX-M-55 was the most common ESBL-encoding gene in strains isolated from chickens (74.4%) compared with blaCTX-M-27 in human strains (47.0%). In 3 of 204 (1.5%) of the farms, identical ESBL genes were detected in ESBL-Ec isolated from farmers and their chickens. Genomic similarity indicating recent sharing of ESBL-Ec between chickens and farmers was found in only one of these farms. CONCLUSIONS: The integration of epidemiological and genomic data in this study has demonstrated a limited contribution of non-intensive chicken farming to ESBL-Ec colonization in humans in Vietnam and further emphasizes the importance of reducing antimicrobial usage in both human and animal host reservoirs.

AB - OBJECTIVES: To investigate the risk of colonization with ESBL-producing Escherichia coli (ESBL-Ec) in humans in Vietnam associated with non-intensive chicken farming. METHODS: Faecal samples from 204 randomly selected farmers and their chickens, and from 306 age- and sex-matched community-based individuals who did not raise poultry were collected. Antimicrobial usage in chickens and humans was assessed by medicine cabinet surveys. WGS was employed to obtain a high-resolution genomic comparison between ESBL-Ec isolated from humans and chickens. RESULTS: The adjusted prevalence of ESBL-Ec colonization was 20.0% (95% CI 10.8%-29.1%) and 35.2% (95% CI 30.4%-40.1%) in chicken farms and humans in Vietnam, respectively. Colonization with ESBL-Ec in humans was associated with antimicrobial usage (OR = 2.52, 95% CI = 1.08-5.87) but not with involvement in chicken farming. blaCTX-M-55 was the most common ESBL-encoding gene in strains isolated from chickens (74.4%) compared with blaCTX-M-27 in human strains (47.0%). In 3 of 204 (1.5%) of the farms, identical ESBL genes were detected in ESBL-Ec isolated from farmers and their chickens. Genomic similarity indicating recent sharing of ESBL-Ec between chickens and farmers was found in only one of these farms. CONCLUSIONS: The integration of epidemiological and genomic data in this study has demonstrated a limited contribution of non-intensive chicken farming to ESBL-Ec colonization in humans in Vietnam and further emphasizes the importance of reducing antimicrobial usage in both human and animal host reservoirs.

U2 - 10.1093/jac/dky506

DO - 10.1093/jac/dky506

M3 - Article

VL - 74

SP - 561

EP - 570

JO - Journal of Antimicrobial Chemotherapy

JF - Journal of Antimicrobial Chemotherapy

SN - 0305-7453

IS - 3

ER -