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Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates

Campylobacter is a major cause of gastroenteritis worldwide, with broiler meat accounting for most illnesses. Antimicrobial intervention is recommended in severe cases of campylobacteriosis. The emergence of antimicrobial resistance (AMR) in Campylobacter is a concerning food safety challenge, and m...

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Autores principales: Habib, Ihab, Ibrahim Mohamed, Mohamed-Yousif, Ghazawi, Akela, Lakshmi, Glindya Bhagya, Khan, Mushtaq, Li, Dan, Sahibzada, Shafi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9850066/
https://www.ncbi.nlm.nih.gov/pubmed/36687171
http://dx.doi.org/10.1016/j.crfs.2023.100434
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author Habib, Ihab
Ibrahim Mohamed, Mohamed-Yousif
Ghazawi, Akela
Lakshmi, Glindya Bhagya
Khan, Mushtaq
Li, Dan
Sahibzada, Shafi
author_facet Habib, Ihab
Ibrahim Mohamed, Mohamed-Yousif
Ghazawi, Akela
Lakshmi, Glindya Bhagya
Khan, Mushtaq
Li, Dan
Sahibzada, Shafi
author_sort Habib, Ihab
collection PubMed
description Campylobacter is a major cause of gastroenteritis worldwide, with broiler meat accounting for most illnesses. Antimicrobial intervention is recommended in severe cases of campylobacteriosis. The emergence of antimicrobial resistance (AMR) in Campylobacter is a concerning food safety challenge, and monitoring the trends of AMR is vital for a better risk assessment. This study aimed to characterize the phenotypic profiles and molecular markers of AMR and virulence in the prevalent Campylobacter species contaminating chilled chicken carcasses sampled from supermarkets in the United Arab Emirates (UAE). Campylobacter was detected in 90 (28.6%) out of 315 tested samples, and up to five isolates from each were confirmed using multiplex PCR. The species C. coli was detected in 83% (75/90) of the positive samples. Whole-genome sequencing was used to characterize the determinants of AMR and potential virulence genes in 45 non-redundant C. coli isolates. We identified nine resistance genes, including four associated with resistance to aminoglycoside (aph(3′)-III, ant(6)-Ia, aph(2″)-Ib, and aac(6′)-Im), and three associated with Beta-lactam resistance (blaOXA-61, blaOXA-193, and blaOXA-489), and two linked to tetracycline resistance (tet(O/32/O), and tet(O)), as well as point mutations in gyrA (fluoroquinolones resistance), 23S rRNA (macrolides resistance), and rpsL (streptomycin resistance) genes. A mutation in gyrA 2 p.T86I, conferring resistance to fluoroquinolones, was detected in 93% (42/45) of the isolates and showed a perfect match with the phenotype results. The simultaneous presence of blaOXA-61 and blaOXA-193 genes was identified in 86.6% (39/45) of the isolates. In silico analysis identified 7 to 11 virulence factors per each C. coli isolate. Some of these factors were prevalent in all examined strains and were associated with adherence (cadF, and jlpA), colonization and immune evasion (capsule biosynthesis and transport, lipooligosaccharide), and invasion (ciaB). This study provides the first published evidence from the UAE characterizing Campylobacter virulence, antimicrobial resistance genotype, and phenotype analysis from retail chicken. The prevalent C. coli in the UAE retail chicken carries multiple virulence genes and antimicrobial resistance markers and exhibits frequent phenotype resistance to macrolides, quinolones, and tetracyclines. The present investigation adds to the current knowledge on molecular epidemiology and AMR development in non-jejuni Campylobacter species in the Middle East and globally.
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spelling pubmed-98500662023-01-20 Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates Habib, Ihab Ibrahim Mohamed, Mohamed-Yousif Ghazawi, Akela Lakshmi, Glindya Bhagya Khan, Mushtaq Li, Dan Sahibzada, Shafi Curr Res Food Sci Research Article Campylobacter is a major cause of gastroenteritis worldwide, with broiler meat accounting for most illnesses. Antimicrobial intervention is recommended in severe cases of campylobacteriosis. The emergence of antimicrobial resistance (AMR) in Campylobacter is a concerning food safety challenge, and monitoring the trends of AMR is vital for a better risk assessment. This study aimed to characterize the phenotypic profiles and molecular markers of AMR and virulence in the prevalent Campylobacter species contaminating chilled chicken carcasses sampled from supermarkets in the United Arab Emirates (UAE). Campylobacter was detected in 90 (28.6%) out of 315 tested samples, and up to five isolates from each were confirmed using multiplex PCR. The species C. coli was detected in 83% (75/90) of the positive samples. Whole-genome sequencing was used to characterize the determinants of AMR and potential virulence genes in 45 non-redundant C. coli isolates. We identified nine resistance genes, including four associated with resistance to aminoglycoside (aph(3′)-III, ant(6)-Ia, aph(2″)-Ib, and aac(6′)-Im), and three associated with Beta-lactam resistance (blaOXA-61, blaOXA-193, and blaOXA-489), and two linked to tetracycline resistance (tet(O/32/O), and tet(O)), as well as point mutations in gyrA (fluoroquinolones resistance), 23S rRNA (macrolides resistance), and rpsL (streptomycin resistance) genes. A mutation in gyrA 2 p.T86I, conferring resistance to fluoroquinolones, was detected in 93% (42/45) of the isolates and showed a perfect match with the phenotype results. The simultaneous presence of blaOXA-61 and blaOXA-193 genes was identified in 86.6% (39/45) of the isolates. In silico analysis identified 7 to 11 virulence factors per each C. coli isolate. Some of these factors were prevalent in all examined strains and were associated with adherence (cadF, and jlpA), colonization and immune evasion (capsule biosynthesis and transport, lipooligosaccharide), and invasion (ciaB). This study provides the first published evidence from the UAE characterizing Campylobacter virulence, antimicrobial resistance genotype, and phenotype analysis from retail chicken. The prevalent C. coli in the UAE retail chicken carries multiple virulence genes and antimicrobial resistance markers and exhibits frequent phenotype resistance to macrolides, quinolones, and tetracyclines. The present investigation adds to the current knowledge on molecular epidemiology and AMR development in non-jejuni Campylobacter species in the Middle East and globally. Elsevier 2023-01-03 /pmc/articles/PMC9850066/ /pubmed/36687171 http://dx.doi.org/10.1016/j.crfs.2023.100434 Text en © 2023 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Research Article
Habib, Ihab
Ibrahim Mohamed, Mohamed-Yousif
Ghazawi, Akela
Lakshmi, Glindya Bhagya
Khan, Mushtaq
Li, Dan
Sahibzada, Shafi
Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates
title Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates
title_full Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates
title_fullStr Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates
title_full_unstemmed Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates
title_short Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates
title_sort genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent campylobacter coli isolated from retail chicken meat in the united arab emirates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9850066/
https://www.ncbi.nlm.nih.gov/pubmed/36687171
http://dx.doi.org/10.1016/j.crfs.2023.100434
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