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Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk
BACKGROUND: Commensal Escherichia coli residing in the guts of humans and animals are reservoirs of multidrug resistance (MDR) genes, including quinolone resistance genes, in humans and poultry. This study aimed to characterize quinolones resistance in E. coli recovered from poultry workers, chicken...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9976508/ https://www.ncbi.nlm.nih.gov/pubmed/36855171 http://dx.doi.org/10.1186/s42522-023-00079-0 |
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author | Aworh, Mabel Kamweli Kwaga, Jacob K. P. Hendriksen, Rene S. Okolocha, Emmanuel C. Harrell, Erin Thakur, Siddhartha |
author_facet | Aworh, Mabel Kamweli Kwaga, Jacob K. P. Hendriksen, Rene S. Okolocha, Emmanuel C. Harrell, Erin Thakur, Siddhartha |
author_sort | Aworh, Mabel Kamweli |
collection | PubMed |
description | BACKGROUND: Commensal Escherichia coli residing in the guts of humans and animals are reservoirs of multidrug resistance (MDR) genes, including quinolone resistance genes, in humans and poultry. This study aimed to characterize quinolones resistance in E. coli recovered from poultry workers, chickens, and poultry farm/market environments in Abuja, Nigeria. METHODS: This was a cross-sectional study conducted between December 2018 and April 2019 comprising poultry workers, chickens and their poultry farm/market environments. This study characterized E. coli isolates from stool, faecal and environmental samples using antimicrobial susceptibility testing and whole-genome sequencing methods. Core-genome multilocus sequences-based phylogeny was used to determine the relatedness between quinolone-resistant E. coli isolates. Data were analyzed using descriptive statistics. RESULTS: Of 110 E. coli isolates, quinolone-resistant phenotypes were observed in 68.2% (n = 75) isolates. Whole-genome sequencing detected plasmid-mediated quinolone resistance (PMQR) genes in 63.6% (n = 70) isolates. The most prevalent PMQR gene detected in 56 of these 70 E. coli isolates was qnrS1, followed by qnrB19 in 14 isolates and aac(6’)-lb-cr in two isolates. Fifteen ciprofloxacin and 19 nalidixic acid-resistant isolates respectively showed double mutations in the quinolone-resistance determining regions (QRDRs) of gyrA, with single or double mutations in parC, and a single mutation in parE. The most prevalent amino-acid substitutions observed were S83L + D87N in gyrA (46.5%, n = 20), S80I in parC (51.2%, n = 22) and S458A in parE (14%, n = 6). About 2.9% (2/70) of PMQR isolates were extended-spectrum beta-lactamase (ESBL) producers while 2.9% (2/70) had plasmid-mediated colistin resistance (PMCR) genes. CONCLUSIONS: PMQR genes were prevalent in E. coli isolates recovered from healthy humans, chickens and poultry farm/market environments. PMCR genes (mcr-1.1) occurred in PMQR-positive isolates recovered from manure and drinking water originating from poultry farm/market environments. It was found that the gene encoding ESBL coexisted with qnrS-positive isolates of human and avian origin. Horizontal transfer of PMQR genes among E. coli isolates in the human-poultry-environment interface has public health implications for the spread of antimicrobial resistance. Relevant government agencies should enforce regulations to restrict the use of critically important antimicrobials in poultry production. |
format | Online Article Text |
id | pubmed-9976508 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-99765082023-03-02 Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk Aworh, Mabel Kamweli Kwaga, Jacob K. P. Hendriksen, Rene S. Okolocha, Emmanuel C. Harrell, Erin Thakur, Siddhartha One Health Outlook Research BACKGROUND: Commensal Escherichia coli residing in the guts of humans and animals are reservoirs of multidrug resistance (MDR) genes, including quinolone resistance genes, in humans and poultry. This study aimed to characterize quinolones resistance in E. coli recovered from poultry workers, chickens, and poultry farm/market environments in Abuja, Nigeria. METHODS: This was a cross-sectional study conducted between December 2018 and April 2019 comprising poultry workers, chickens and their poultry farm/market environments. This study characterized E. coli isolates from stool, faecal and environmental samples using antimicrobial susceptibility testing and whole-genome sequencing methods. Core-genome multilocus sequences-based phylogeny was used to determine the relatedness between quinolone-resistant E. coli isolates. Data were analyzed using descriptive statistics. RESULTS: Of 110 E. coli isolates, quinolone-resistant phenotypes were observed in 68.2% (n = 75) isolates. Whole-genome sequencing detected plasmid-mediated quinolone resistance (PMQR) genes in 63.6% (n = 70) isolates. The most prevalent PMQR gene detected in 56 of these 70 E. coli isolates was qnrS1, followed by qnrB19 in 14 isolates and aac(6’)-lb-cr in two isolates. Fifteen ciprofloxacin and 19 nalidixic acid-resistant isolates respectively showed double mutations in the quinolone-resistance determining regions (QRDRs) of gyrA, with single or double mutations in parC, and a single mutation in parE. The most prevalent amino-acid substitutions observed were S83L + D87N in gyrA (46.5%, n = 20), S80I in parC (51.2%, n = 22) and S458A in parE (14%, n = 6). About 2.9% (2/70) of PMQR isolates were extended-spectrum beta-lactamase (ESBL) producers while 2.9% (2/70) had plasmid-mediated colistin resistance (PMCR) genes. CONCLUSIONS: PMQR genes were prevalent in E. coli isolates recovered from healthy humans, chickens and poultry farm/market environments. PMCR genes (mcr-1.1) occurred in PMQR-positive isolates recovered from manure and drinking water originating from poultry farm/market environments. It was found that the gene encoding ESBL coexisted with qnrS-positive isolates of human and avian origin. Horizontal transfer of PMQR genes among E. coli isolates in the human-poultry-environment interface has public health implications for the spread of antimicrobial resistance. Relevant government agencies should enforce regulations to restrict the use of critically important antimicrobials in poultry production. BioMed Central 2023-02-28 /pmc/articles/PMC9976508/ /pubmed/36855171 http://dx.doi.org/10.1186/s42522-023-00079-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Aworh, Mabel Kamweli Kwaga, Jacob K. P. Hendriksen, Rene S. Okolocha, Emmanuel C. Harrell, Erin Thakur, Siddhartha Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk |
title | Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk |
title_full | Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk |
title_fullStr | Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk |
title_full_unstemmed | Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk |
title_short | Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk |
title_sort | quinolone-resistant escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9976508/ https://www.ncbi.nlm.nih.gov/pubmed/36855171 http://dx.doi.org/10.1186/s42522-023-00079-0 |
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