Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of <i>Salmonella</i> Isolated from Chickens in Sichuan, China

The aim of this study was to explore the association between antimicrobial resistance, ESBL genes, and virulence genes of <i>Salmonella</i> isolates. From 2019 to 2021, a total of 117 <i>Salmonella</i> isolates were obtained from symptomatic chickens in Sichuan Province, Chin...

Full description

Bibliographic Details
Main Authors: Gang Shu, Jianyu Qiu, Yilei Zheng, Lijen Chang, Haohuan Li, Funeng Xu, Wei Zhang, Lizi Yin, Hualin Fu, Qigui Yan, Ting Gan, Juchun Lin
Format: Article
Language:English
Published: MDPI AG 2023-08-01
Series:Animals
Subjects:
Online Access:https://www.mdpi.com/2076-2615/13/17/2770
_version_ 1797582853213519872
author Gang Shu
Jianyu Qiu
Yilei Zheng
Lijen Chang
Haohuan Li
Funeng Xu
Wei Zhang
Lizi Yin
Hualin Fu
Qigui Yan
Ting Gan
Juchun Lin
author_facet Gang Shu
Jianyu Qiu
Yilei Zheng
Lijen Chang
Haohuan Li
Funeng Xu
Wei Zhang
Lizi Yin
Hualin Fu
Qigui Yan
Ting Gan
Juchun Lin
author_sort Gang Shu
collection DOAJ
description The aim of this study was to explore the association between antimicrobial resistance, ESBL genes, and virulence genes of <i>Salmonella</i> isolates. From 2019 to 2021, a total of 117 <i>Salmonella</i> isolates were obtained from symptomatic chickens in Sichuan Province, China. The strains were tested for antimicrobial resistance and the presence of ESBL according to the Clinical and Laboratory Standards Institute (CLSI) instructions. The presence of ESBL genes and genes for virulence was determined using Polymerase Chain Reaction (PCR). In addition, Multilocus Sequence Typing (MLST) was applied to confirm the molecular genotyping. Moreover, the mechanism of ESBL and virulence gene transfer and the relationships between the resistance phenotype, ESBL genes, and virulence genes were explored. The isolates exhibited different frequencies of resistance to antibiotics (resistance rates ranged from 21.37% to 97.44%), whereas 68.38% and 41.03% of isolates were multi-drug resistance (MDR) and ESBL-producers, respectively. In the PCR analysis, <i>bla</i><sub>CTX-M</sub> was the most prevalent ESBL genotype (73.42%, 58/79), and <i>bla</i><sub>CTX-M-55</sub> showed the most significant effect on the resistance to cephalosporins as tested by logistic regression analysis. Isolates showed a high carriage rate of <i>invA</i>, <i>avrA</i>, <i>sopB</i>, <i>sopE</i>, <i>ssaQ</i>, <i>spvR</i>, <i>spvB</i>, <i>spvC</i>, <i>stn</i>, and <i>bcfC</i> (ranged from 51.28% to 100%). MLST analysis revealed that the 117 isolates were divided into 11 types, mainly ST92, ST11, and ST3717. Of 48 ESBL-producers, 21 transconjugants were successfully obtained by conjugation. Furthermore, ESBL and <i>spv</i> virulence genes were obtained simultaneously in 15 transconjugants. These results highlighted that <i>Salmonella</i> isolates were common carriers of ESBLs and multiple virulence genes. Horizontal transfer played a key role in disseminating antimicrobial resistance and pathogenesis. Therefore, it is necessary to continuously monitor the use of antimicrobials and the prevalence of AMR and virulence in <i>Salmonella</i> from food animals and to improve the antibiotic stewardship for salmonellosis.
first_indexed 2024-03-10T23:28:28Z
format Article
id doaj.art-3101fe6f62c94845a2473de22b6b7143
institution Directory Open Access Journal
issn 2076-2615
language English
last_indexed 2024-03-10T23:28:28Z
publishDate 2023-08-01
publisher MDPI AG
record_format Article
series Animals
spelling doaj.art-3101fe6f62c94845a2473de22b6b71432023-11-19T07:47:09ZengMDPI AGAnimals2076-26152023-08-011317277010.3390/ani13172770Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of <i>Salmonella</i> Isolated from Chickens in Sichuan, ChinaGang Shu0Jianyu Qiu1Yilei Zheng2Lijen Chang3Haohuan Li4Funeng Xu5Wei Zhang6Lizi Yin7Hualin Fu8Qigui Yan9Ting Gan10Juchun Lin11Department of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaCenter for Veterinary Sciences, Zhejiang University, Hangzhou 310058, ChinaDepartment of Small Animal Clinical Sciences, Virginia-Maryland College of Veterinary Medicine, Blacksburg, VA 24061, USADepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaThe aim of this study was to explore the association between antimicrobial resistance, ESBL genes, and virulence genes of <i>Salmonella</i> isolates. From 2019 to 2021, a total of 117 <i>Salmonella</i> isolates were obtained from symptomatic chickens in Sichuan Province, China. The strains were tested for antimicrobial resistance and the presence of ESBL according to the Clinical and Laboratory Standards Institute (CLSI) instructions. The presence of ESBL genes and genes for virulence was determined using Polymerase Chain Reaction (PCR). In addition, Multilocus Sequence Typing (MLST) was applied to confirm the molecular genotyping. Moreover, the mechanism of ESBL and virulence gene transfer and the relationships between the resistance phenotype, ESBL genes, and virulence genes were explored. The isolates exhibited different frequencies of resistance to antibiotics (resistance rates ranged from 21.37% to 97.44%), whereas 68.38% and 41.03% of isolates were multi-drug resistance (MDR) and ESBL-producers, respectively. In the PCR analysis, <i>bla</i><sub>CTX-M</sub> was the most prevalent ESBL genotype (73.42%, 58/79), and <i>bla</i><sub>CTX-M-55</sub> showed the most significant effect on the resistance to cephalosporins as tested by logistic regression analysis. Isolates showed a high carriage rate of <i>invA</i>, <i>avrA</i>, <i>sopB</i>, <i>sopE</i>, <i>ssaQ</i>, <i>spvR</i>, <i>spvB</i>, <i>spvC</i>, <i>stn</i>, and <i>bcfC</i> (ranged from 51.28% to 100%). MLST analysis revealed that the 117 isolates were divided into 11 types, mainly ST92, ST11, and ST3717. Of 48 ESBL-producers, 21 transconjugants were successfully obtained by conjugation. Furthermore, ESBL and <i>spv</i> virulence genes were obtained simultaneously in 15 transconjugants. These results highlighted that <i>Salmonella</i> isolates were common carriers of ESBLs and multiple virulence genes. Horizontal transfer played a key role in disseminating antimicrobial resistance and pathogenesis. Therefore, it is necessary to continuously monitor the use of antimicrobials and the prevalence of AMR and virulence in <i>Salmonella</i> from food animals and to improve the antibiotic stewardship for salmonellosis.https://www.mdpi.com/2076-2615/13/17/2770<i>Salmonella</i>antimicrobial resistanceESBL genesvirulence genesMLSTchicken
spellingShingle Gang Shu
Jianyu Qiu
Yilei Zheng
Lijen Chang
Haohuan Li
Funeng Xu
Wei Zhang
Lizi Yin
Hualin Fu
Qigui Yan
Ting Gan
Juchun Lin
Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of <i>Salmonella</i> Isolated from Chickens in Sichuan, China
Animals
<i>Salmonella</i>
antimicrobial resistance
ESBL genes
virulence genes
MLST
chicken
title Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of <i>Salmonella</i> Isolated from Chickens in Sichuan, China
title_full Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of <i>Salmonella</i> Isolated from Chickens in Sichuan, China
title_fullStr Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of <i>Salmonella</i> Isolated from Chickens in Sichuan, China
title_full_unstemmed Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of <i>Salmonella</i> Isolated from Chickens in Sichuan, China
title_short Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of <i>Salmonella</i> Isolated from Chickens in Sichuan, China
title_sort association between phenotypes of antimicrobial resistance esbl resistance genes and virulence genes of i salmonella i isolated from chickens in sichuan china
topic <i>Salmonella</i>
antimicrobial resistance
ESBL genes
virulence genes
MLST
chicken
url https://www.mdpi.com/2076-2615/13/17/2770
work_keys_str_mv AT gangshu associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT jianyuqiu associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT yileizheng associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT lijenchang associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT haohuanli associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT funengxu associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT weizhang associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT liziyin associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT hualinfu associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT qiguiyan associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT tinggan associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina
AT juchunlin associationbetweenphenotypesofantimicrobialresistanceesblresistancegenesandvirulencegenesofisalmonellaiisolatedfromchickensinsichuanchina