Clonal and plasmid-mediated dissemination of environmental carbapenem-resistant Enterobacteriaceae in large animal breeding areas in northern China

Congcong Gu; Xuewen Li; Huiyun Zou; Ling Zhao; Chen Meng; Chengxia Yang; Hui Zhang; Björn Berglund

doi:10.1016/j.envpol.2022.118800

Clonal and plasmid-mediated dissemination of environmental carbapenem-resistant Enterobacteriaceae in large animal breeding areas in northern China

Environ Pollut. 2022 Mar 15:297:118800. doi: 10.1016/j.envpol.2022.118800. Epub 2022 Jan 7.

Authors

Congcong Gu¹, Xuewen Li², Huiyun Zou¹, Ling Zhao¹, Chen Meng¹, Chengxia Yang¹, Hui Zhang¹, Björn Berglund³

Affiliations

¹ Department of Environment and Health, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, China.
² Department of Environment and Health, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, China. Electronic address: lxw@sdu.edu.cn.
³ Department of Biomedical and Clinical Sciences, Linköping University, 58185, Linköping, Sweden.

PMID: 35007671
DOI: 10.1016/j.envpol.2022.118800

Abstract

The emergence and dissemination of carbapenem-resistant Enterobacteriaceae (CRE) constitute a major global health problem. The environment plays an important role in the dissemination of CRE, but large-scale studies on CRE in groundwater environments in animal breeding areas are scarce. The aim of this study was to investigate CRE occurrence and environmental transmission of carbapenem resistance genes in large animal breeding areas in northern China. In total, 280 well water and 102 animal feces samples in large animal breeding areas in six counties from the two provinces Inner Mongolia and Shandong in China, were screened for CRE. A total of 39 CRE were isolated and characterized with next-generation sequencing. 5.3% of well water samples were contaminated with CRE. The well water in chicken farms had the highest number of detections of CRE (15.9%). More than half of the isolates carried closely related, conjugative IncX3 plasmids with bla_NDM-genes from multiple geographic areas, indicating that this kind of plasmid plays an important role in dissemination of carbapenem resistance determinants. The clonal expansion of various CRE isolates in well water and animal feces were demonstrated; clonally related CRE were isolated from different wells within the same county, from different counties in the same province, and even from different provinces. In addition to harboring various ARGs, two closely related K. pneumoniae belonging to ST11 isolated from well water carried genetic hypervirulence determinants on a virulence plasmid, highlighting the potential health risk posed by further dissemination of this strain. These findings suggest that groundwater may be an underappreciated reservoir and source of dissemination of CRE, from which resistance genes may disseminate among different bacterial strains and over large geographic distances. Further research and multi-sectorial monitoring, with a "One health" perspective, is urgently needed to investigate the need for interventions aimed at preventing CRE dissemination.

Keywords: CRE; IncX3 plasmid; Well water; Whole-genome sequencing; bla(NDM).

MeSH terms

Animals
Anti-Bacterial Agents
Breeding
Carbapenem-Resistant Enterobacteriaceae* / genetics
China
Enterobacteriaceae Infections* / epidemiology
Enterobacteriaceae Infections* / veterinary
Microbial Sensitivity Tests
Plasmids / genetics
beta-Lactamases / genetics

Substances

Anti-Bacterial Agents
beta-Lactamases