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Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China

The prevalence of Campylobacter spp.in pets is a potential concern for human health. However, little is known about the pet-related Campylobacter spp. in China. A total of 325 fecal samples were collected from dogs, cats, and pet foxes. Campylobacter spp. were isolated by culture, and MALDI-TOF MS w...

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Autores principales: Ju, Changyan, Ma, Yanping, Zhang, Bi, Zhou, Guilan, Wang, Hairui, Yu, Muhua, He, Jiaoming, Duan, Yongxiang, Zhang, Maojun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10267384/
https://www.ncbi.nlm.nih.gov/pubmed/37323906
http://dx.doi.org/10.3389/fmicb.2023.1152719
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author Ju, Changyan
Ma, Yanping
Zhang, Bi
Zhou, Guilan
Wang, Hairui
Yu, Muhua
He, Jiaoming
Duan, Yongxiang
Zhang, Maojun
author_facet Ju, Changyan
Ma, Yanping
Zhang, Bi
Zhou, Guilan
Wang, Hairui
Yu, Muhua
He, Jiaoming
Duan, Yongxiang
Zhang, Maojun
author_sort Ju, Changyan
collection PubMed
description The prevalence of Campylobacter spp.in pets is a potential concern for human health. However, little is known about the pet-related Campylobacter spp. in China. A total of 325 fecal samples were collected from dogs, cats, and pet foxes. Campylobacter spp. were isolated by culture, and MALDI-TOF MS was used to identify 110 Campylobacter spp. isolates in total. C. upsaliensis (30.2%, 98/325), C. helveticus (2.5%, 8/325), and C. jejuni (1.2%, 4/325) were the three found species. In dogs and cats, the prevalence of Campylobacter spp. was 35.0% and 30.1%, respectively. A panel of 11 antimicrobials was used to evaluate the antimicrobial susceptibility by the agar dilution method. Among C. upsaliensis isolates, ciprofloxacin had the highest rate of resistance (94.9%), followed by nalidixic acid (77.6%) and streptomycin (60.2%). Multidrug resistance (MDR) was found in 55.1% (54/98) of the C. upsaliensis isolates. Moreover, 100 isolates, including 88 C. upsaliensis, 8 C. helveticus, and 4 C. jejuni, had their whole genomes sequenced. By blasting the sequence against the VFDB database, virulence factors were identified. In total, 100% of C. upsaliensis isolates carried the cadF, porA, pebA, cdtA, cdtB, and cdtC genes. The flaA gene was present in only 13.6% (12/88) of the isolates, while the flaB gene was absent. By analyzing the sequence against the CARD database, we found that 89.8% (79/88) of C. upsaliensis isolates had antibiotic target alteration in the gyrA gene conferring resistance to fluoroquinolone, 36.4% (32/88) had the aminoglycoside resistance gene, and 19.3% (17/88) had the tetracycline resistance gene. The phylogenetic analysis using the K-mer tree method obtained two major clades among the C. upsaliensis isolates. All eight isolates in subclade 1 possessed the gyrA gene mutation, the aminoglycoside and tetracycline resistance genes, and were phenotypically resistant to six classes of antimicrobials. It has been established that pets are a significant source of Campylobacter spp. strains and a reservoir for them. This study is the first to have documented the presence of Campylobacter spp. in pets in Shenzhen, China. In this study, C. upsaliensis of subclade 1 required additional attention due to its broad MDR phenotype and relatively high flaA gene prevalence.
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spelling pubmed-102673842023-06-15 Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China Ju, Changyan Ma, Yanping Zhang, Bi Zhou, Guilan Wang, Hairui Yu, Muhua He, Jiaoming Duan, Yongxiang Zhang, Maojun Front Microbiol Microbiology The prevalence of Campylobacter spp.in pets is a potential concern for human health. However, little is known about the pet-related Campylobacter spp. in China. A total of 325 fecal samples were collected from dogs, cats, and pet foxes. Campylobacter spp. were isolated by culture, and MALDI-TOF MS was used to identify 110 Campylobacter spp. isolates in total. C. upsaliensis (30.2%, 98/325), C. helveticus (2.5%, 8/325), and C. jejuni (1.2%, 4/325) were the three found species. In dogs and cats, the prevalence of Campylobacter spp. was 35.0% and 30.1%, respectively. A panel of 11 antimicrobials was used to evaluate the antimicrobial susceptibility by the agar dilution method. Among C. upsaliensis isolates, ciprofloxacin had the highest rate of resistance (94.9%), followed by nalidixic acid (77.6%) and streptomycin (60.2%). Multidrug resistance (MDR) was found in 55.1% (54/98) of the C. upsaliensis isolates. Moreover, 100 isolates, including 88 C. upsaliensis, 8 C. helveticus, and 4 C. jejuni, had their whole genomes sequenced. By blasting the sequence against the VFDB database, virulence factors were identified. In total, 100% of C. upsaliensis isolates carried the cadF, porA, pebA, cdtA, cdtB, and cdtC genes. The flaA gene was present in only 13.6% (12/88) of the isolates, while the flaB gene was absent. By analyzing the sequence against the CARD database, we found that 89.8% (79/88) of C. upsaliensis isolates had antibiotic target alteration in the gyrA gene conferring resistance to fluoroquinolone, 36.4% (32/88) had the aminoglycoside resistance gene, and 19.3% (17/88) had the tetracycline resistance gene. The phylogenetic analysis using the K-mer tree method obtained two major clades among the C. upsaliensis isolates. All eight isolates in subclade 1 possessed the gyrA gene mutation, the aminoglycoside and tetracycline resistance genes, and were phenotypically resistant to six classes of antimicrobials. It has been established that pets are a significant source of Campylobacter spp. strains and a reservoir for them. This study is the first to have documented the presence of Campylobacter spp. in pets in Shenzhen, China. In this study, C. upsaliensis of subclade 1 required additional attention due to its broad MDR phenotype and relatively high flaA gene prevalence. Frontiers Media S.A. 2023-06-01 /pmc/articles/PMC10267384/ /pubmed/37323906 http://dx.doi.org/10.3389/fmicb.2023.1152719 Text en Copyright © 2023 Ju, Ma, Zhang, Zhou, Wang, Yu, He, Duan and Zhang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ju, Changyan
Ma, Yanping
Zhang, Bi
Zhou, Guilan
Wang, Hairui
Yu, Muhua
He, Jiaoming
Duan, Yongxiang
Zhang, Maojun
Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China
title Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China
title_full Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China
title_fullStr Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China
title_full_unstemmed Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China
title_short Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China
title_sort prevalence, genomic characterization and antimicrobial resistance of campylobacter spp. isolates in pets in shenzhen, china
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10267384/
https://www.ncbi.nlm.nih.gov/pubmed/37323906
http://dx.doi.org/10.3389/fmicb.2023.1152719
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