Cargando…

Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019

The Center for Disease Control and Prevention identifies antimicrobial resistant (AMR) Campylobacter as a serious threat to U.S. public health due to high community burden, increased transmissibility, and limited treatability. The National Antimicrobial Resistance Monitoring System (NARMS) plays an...

Descripción completa

Detalles Bibliográficos
Autores principales: Hull, Dawn M., Harrell, Erin, van Vliet, Arnoud H. M., Correa, Maria, Thakur, Siddhartha
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7877606/
https://www.ncbi.nlm.nih.gov/pubmed/33571292
http://dx.doi.org/10.1371/journal.pone.0246571
_version_ 1783650202711752704
author Hull, Dawn M.
Harrell, Erin
van Vliet, Arnoud H. M.
Correa, Maria
Thakur, Siddhartha
author_facet Hull, Dawn M.
Harrell, Erin
van Vliet, Arnoud H. M.
Correa, Maria
Thakur, Siddhartha
author_sort Hull, Dawn M.
collection PubMed
description The Center for Disease Control and Prevention identifies antimicrobial resistant (AMR) Campylobacter as a serious threat to U.S. public health due to high community burden, increased transmissibility, and limited treatability. The National Antimicrobial Resistance Monitoring System (NARMS) plays an important role in surveillance of AMR bacterial pathogens in humans, food animals and retail meats. This study investigated C. coli and C. jejuni from live food animals, poultry carcasses at production, and retail meat in North Carolina between January 2018-December 2019. Whole genome sequencing and bioinformatics were used for phenotypic and genotypic characterization to compare AMR profiles, virulence factors associated with Guillain-Barré Syndrome (GBS) (neuABC and cst-II or cst-III), and phylogenic linkage between 541 Campylobacter isolates (C. coli n = 343, C. jejuni n = 198). Overall, 90.4% (489/541) Campylobacter isolates tested positive for AMR genes, while 43% (233/541) carried resistance genes for three or more antibiotic classes and were classified molecularly multidrug resistant. AMR gene frequencies were highest against tetracyclines (64.3%), beta-lactams (63.6%), aminoglycosides (38.6%), macrolides (34.8%), quinolones (24.4%), lincosamides (13.5%), and streptothricins (5%). A total of 57.6% (114/198) C. jejuni carried GBS virulence factors, while three C. coli carried the C. jejuni-like lipooligosaccharide locus, neuABC and cst-II. Further evidence of C. coli and C. jejuni interspecies genomic exchange was observed in identical multilocus sequence typing, shared sequence type (ST) 7818 clonal complex 828, and identical species-indicator genes mapA, ceuE, and hipO. There was a significant increase in novel STs from 2018 to 2019 (2 in 2018 and 21 in 2019, p<0.002), illustrating variable Campylobacter genomes within food animal production. Introgression between C. coli and C. jejuni may aid pathogen adaption, lead to higher AMR and increase Campylobacter persistence in food processing. Future studies should further characterize interspecies gene transfer and evolutionary trends in food animal production to track evolving risks to public health.
format Online
Article
Text
id pubmed-7877606
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-78776062021-02-19 Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019 Hull, Dawn M. Harrell, Erin van Vliet, Arnoud H. M. Correa, Maria Thakur, Siddhartha PLoS One Research Article The Center for Disease Control and Prevention identifies antimicrobial resistant (AMR) Campylobacter as a serious threat to U.S. public health due to high community burden, increased transmissibility, and limited treatability. The National Antimicrobial Resistance Monitoring System (NARMS) plays an important role in surveillance of AMR bacterial pathogens in humans, food animals and retail meats. This study investigated C. coli and C. jejuni from live food animals, poultry carcasses at production, and retail meat in North Carolina between January 2018-December 2019. Whole genome sequencing and bioinformatics were used for phenotypic and genotypic characterization to compare AMR profiles, virulence factors associated with Guillain-Barré Syndrome (GBS) (neuABC and cst-II or cst-III), and phylogenic linkage between 541 Campylobacter isolates (C. coli n = 343, C. jejuni n = 198). Overall, 90.4% (489/541) Campylobacter isolates tested positive for AMR genes, while 43% (233/541) carried resistance genes for three or more antibiotic classes and were classified molecularly multidrug resistant. AMR gene frequencies were highest against tetracyclines (64.3%), beta-lactams (63.6%), aminoglycosides (38.6%), macrolides (34.8%), quinolones (24.4%), lincosamides (13.5%), and streptothricins (5%). A total of 57.6% (114/198) C. jejuni carried GBS virulence factors, while three C. coli carried the C. jejuni-like lipooligosaccharide locus, neuABC and cst-II. Further evidence of C. coli and C. jejuni interspecies genomic exchange was observed in identical multilocus sequence typing, shared sequence type (ST) 7818 clonal complex 828, and identical species-indicator genes mapA, ceuE, and hipO. There was a significant increase in novel STs from 2018 to 2019 (2 in 2018 and 21 in 2019, p<0.002), illustrating variable Campylobacter genomes within food animal production. Introgression between C. coli and C. jejuni may aid pathogen adaption, lead to higher AMR and increase Campylobacter persistence in food processing. Future studies should further characterize interspecies gene transfer and evolutionary trends in food animal production to track evolving risks to public health. Public Library of Science 2021-02-11 /pmc/articles/PMC7877606/ /pubmed/33571292 http://dx.doi.org/10.1371/journal.pone.0246571 Text en © 2021 Hull et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hull, Dawn M.
Harrell, Erin
van Vliet, Arnoud H. M.
Correa, Maria
Thakur, Siddhartha
Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019
title Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019
title_full Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019
title_fullStr Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019
title_full_unstemmed Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019
title_short Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019
title_sort antimicrobial resistance and interspecies gene transfer in campylobacter coli and campylobacter jejuni isolated from food animals, poultry processing, and retail meat in north carolina, 2018–2019
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7877606/
https://www.ncbi.nlm.nih.gov/pubmed/33571292
http://dx.doi.org/10.1371/journal.pone.0246571
work_keys_str_mv AT hulldawnm antimicrobialresistanceandinterspeciesgenetransferincampylobactercoliandcampylobacterjejuniisolatedfromfoodanimalspoultryprocessingandretailmeatinnorthcarolina20182019
AT harrellerin antimicrobialresistanceandinterspeciesgenetransferincampylobactercoliandcampylobacterjejuniisolatedfromfoodanimalspoultryprocessingandretailmeatinnorthcarolina20182019
AT vanvlietarnoudhm antimicrobialresistanceandinterspeciesgenetransferincampylobactercoliandcampylobacterjejuniisolatedfromfoodanimalspoultryprocessingandretailmeatinnorthcarolina20182019
AT correamaria antimicrobialresistanceandinterspeciesgenetransferincampylobactercoliandcampylobacterjejuniisolatedfromfoodanimalspoultryprocessingandretailmeatinnorthcarolina20182019
AT thakursiddhartha antimicrobialresistanceandinterspeciesgenetransferincampylobactercoliandcampylobacterjejuniisolatedfromfoodanimalspoultryprocessingandretailmeatinnorthcarolina20182019