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Distribution and association of antimicrobial resistance and virulence characteristics in Enterococcus spp. isolates from captive Asian elephants in China

Enterococcus spp., as an opportunistic pathogen, are widely distributed in the environment and the gastrointestinal tracts of both humans and animals. Captive Asian elephants, popular animals at tourist attractions, have frequent contact with humans. However, there is limited information on whether...

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Autores principales: Yang, Jinpeng, Chen, Yanshan, Dong, Zhiyou, Zhang, Wenqing, Liu, Lijuan, Meng, Wanyu, Li, Qianlan, Fu, Keyi, Zhou, Ziyao, Liu, Haifeng, Zhong, Zhijun, Xiao, Xiao, Zhu, Jieyao, Peng, Guangneng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10635408/
https://www.ncbi.nlm.nih.gov/pubmed/37954234
http://dx.doi.org/10.3389/fmicb.2023.1277221
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author Yang, Jinpeng
Chen, Yanshan
Dong, Zhiyou
Zhang, Wenqing
Liu, Lijuan
Meng, Wanyu
Li, Qianlan
Fu, Keyi
Zhou, Ziyao
Liu, Haifeng
Zhong, Zhijun
Xiao, Xiao
Zhu, Jieyao
Peng, Guangneng
author_facet Yang, Jinpeng
Chen, Yanshan
Dong, Zhiyou
Zhang, Wenqing
Liu, Lijuan
Meng, Wanyu
Li, Qianlan
Fu, Keyi
Zhou, Ziyao
Liu, Haifeng
Zhong, Zhijun
Xiao, Xiao
Zhu, Jieyao
Peng, Guangneng
author_sort Yang, Jinpeng
collection PubMed
description Enterococcus spp., as an opportunistic pathogen, are widely distributed in the environment and the gastrointestinal tracts of both humans and animals. Captive Asian elephants, popular animals at tourist attractions, have frequent contact with humans. However, there is limited information on whether captive Asian elephants can serve as a reservoir of antimicrobial resistance (AMR). The aim of this study was to characterize AMR, antibiotic resistance genes (ARGs), virulence-associated genes (VAGs), gelatinase activity, hemolysis activity, and biofilm formation of Enterococcus spp. isolated from captive Asian elephants, and to analyze the potential correlations among these factors. A total of 62 Enterococcus spp. strains were isolated from fecal samples of captive Asian elephants, comprising 17 Enterococcus hirae (27.4%), 12 Enterococcus faecalis (19.4%), 8 Enterococcus faecium (12.9%), 7 Enterococcus avium (11.3%), 7 Enterococcus mundtii (11.3%), and 11 other Enterococcus spp. (17.7%). Isolates exhibited high resistance to rifampin (51.6%) and streptomycin (37.1%). 50% of Enterococcus spp. isolates exhibited multidrug resistance (MDR), with all E. faecium strains demonstrating MDR. Additionally, nine ARGs were identified, with tet(M) (51.6%), erm(B) (24.2%), and cfr (21.0%) showing relatively higher detection rates. Biofilm formation, gelatinase activity, and α-hemolysin activity were observed in 79.0, 24.2, and 14.5% of the isolates, respectively. A total of 18 VAGs were detected, with gelE being the most prevalent (69.4%). Correlation analysis revealed 229 significant positive correlations and 12 significant negative correlations. The strongest intra-group correlations were observed among VAGs. Notably, we found that vancomycin resistance showed a significant positive correlation with ciprofloxacin resistance, cfr, and gelatinase activity, respectively. In conclusion, captive Asian elephants could serve as significant reservoirs for the dissemination of AMR to humans.
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spelling pubmed-106354082023-11-10 Distribution and association of antimicrobial resistance and virulence characteristics in Enterococcus spp. isolates from captive Asian elephants in China Yang, Jinpeng Chen, Yanshan Dong, Zhiyou Zhang, Wenqing Liu, Lijuan Meng, Wanyu Li, Qianlan Fu, Keyi Zhou, Ziyao Liu, Haifeng Zhong, Zhijun Xiao, Xiao Zhu, Jieyao Peng, Guangneng Front Microbiol Microbiology Enterococcus spp., as an opportunistic pathogen, are widely distributed in the environment and the gastrointestinal tracts of both humans and animals. Captive Asian elephants, popular animals at tourist attractions, have frequent contact with humans. However, there is limited information on whether captive Asian elephants can serve as a reservoir of antimicrobial resistance (AMR). The aim of this study was to characterize AMR, antibiotic resistance genes (ARGs), virulence-associated genes (VAGs), gelatinase activity, hemolysis activity, and biofilm formation of Enterococcus spp. isolated from captive Asian elephants, and to analyze the potential correlations among these factors. A total of 62 Enterococcus spp. strains were isolated from fecal samples of captive Asian elephants, comprising 17 Enterococcus hirae (27.4%), 12 Enterococcus faecalis (19.4%), 8 Enterococcus faecium (12.9%), 7 Enterococcus avium (11.3%), 7 Enterococcus mundtii (11.3%), and 11 other Enterococcus spp. (17.7%). Isolates exhibited high resistance to rifampin (51.6%) and streptomycin (37.1%). 50% of Enterococcus spp. isolates exhibited multidrug resistance (MDR), with all E. faecium strains demonstrating MDR. Additionally, nine ARGs were identified, with tet(M) (51.6%), erm(B) (24.2%), and cfr (21.0%) showing relatively higher detection rates. Biofilm formation, gelatinase activity, and α-hemolysin activity were observed in 79.0, 24.2, and 14.5% of the isolates, respectively. A total of 18 VAGs were detected, with gelE being the most prevalent (69.4%). Correlation analysis revealed 229 significant positive correlations and 12 significant negative correlations. The strongest intra-group correlations were observed among VAGs. Notably, we found that vancomycin resistance showed a significant positive correlation with ciprofloxacin resistance, cfr, and gelatinase activity, respectively. In conclusion, captive Asian elephants could serve as significant reservoirs for the dissemination of AMR to humans. Frontiers Media S.A. 2023-10-23 /pmc/articles/PMC10635408/ /pubmed/37954234 http://dx.doi.org/10.3389/fmicb.2023.1277221 Text en Copyright © 2023 Yang, Chen, Dong, Zhang, Liu, Meng, Li, Fu, Zhou, Liu, Zhong, Xiao, Zhu and Peng. 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
Yang, Jinpeng
Chen, Yanshan
Dong, Zhiyou
Zhang, Wenqing
Liu, Lijuan
Meng, Wanyu
Li, Qianlan
Fu, Keyi
Zhou, Ziyao
Liu, Haifeng
Zhong, Zhijun
Xiao, Xiao
Zhu, Jieyao
Peng, Guangneng
Distribution and association of antimicrobial resistance and virulence characteristics in Enterococcus spp. isolates from captive Asian elephants in China
title Distribution and association of antimicrobial resistance and virulence characteristics in Enterococcus spp. isolates from captive Asian elephants in China
title_full Distribution and association of antimicrobial resistance and virulence characteristics in Enterococcus spp. isolates from captive Asian elephants in China
title_fullStr Distribution and association of antimicrobial resistance and virulence characteristics in Enterococcus spp. isolates from captive Asian elephants in China
title_full_unstemmed Distribution and association of antimicrobial resistance and virulence characteristics in Enterococcus spp. isolates from captive Asian elephants in China
title_short Distribution and association of antimicrobial resistance and virulence characteristics in Enterococcus spp. isolates from captive Asian elephants in China
title_sort distribution and association of antimicrobial resistance and virulence characteristics in enterococcus spp. isolates from captive asian elephants in china
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10635408/
https://www.ncbi.nlm.nih.gov/pubmed/37954234
http://dx.doi.org/10.3389/fmicb.2023.1277221
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