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

Jinpeng Yang; Yanshan Chen; Zhiyou Dong; Wenqing Zhang; Lijuan Liu; Wanyu Meng; Qianlan Li; Keyi Fu; Ziyao Zhou; Haifeng Liu; Zhijun Zhong; Xiao Xiao; Jieyao Zhu; Guangneng Peng

doi:10.3389/fmicb.2023.1277221

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

Front Microbiol. 2023 Oct 23:14:1277221. doi: 10.3389/fmicb.2023.1277221. eCollection 2023.

Authors

Jinpeng Yang^#¹, Yanshan Chen^#¹, Zhiyou Dong^#¹, Wenqing Zhang^#¹, Lijuan Liu¹, Wanyu Meng¹, Qianlan Li¹, Keyi Fu¹, Ziyao Zhou¹, Haifeng Liu¹, Zhijun Zhong¹, Xiao Xiao², Jieyao Zhu³, Guangneng Peng¹

Affiliations

¹ Key Laboratory of Animal Disease and Human Health of Sichuan Province, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China.
² College of Veterinary Medicine, Yunnan Agricultural University, Kunming, Yunnan, China.
³ Xishuangbanna Vocational and Technical College, Yunnan, China.

^# Contributed equally.

Abstract

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.

Keywords: Asian elephants; Enterococcus faecalis; Enterococcus faecium; Enterococcus spp.; antimicrobial resistance; virulence-associated genes.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was financially supported by the National Science and Technology Department’s “13th Five-Year” Special Subproject of China (no. 2016YFD0501009).