Dissemination of blaNDM-5 via IncX3 plasmids in carbapenem-resistant Enterobacteriaceae among humans and in the environment in an intensive vegetable cultivation area in eastern China

Qian Zhao; Björn Berglund; Huiyun Zou; Ziyu Zhou; Huiyu Xia; Ling Zhao; Lennart E Nilsson; Xuewen Li

doi:10.1016/j.envpol.2020.116370

Dissemination of bla_NDM-5 via IncX3 plasmids in carbapenem-resistant Enterobacteriaceae among humans and in the environment in an intensive vegetable cultivation area in eastern China

Environ Pollut. 2021 Jan 2:273:116370. doi: 10.1016/j.envpol.2020.116370. Online ahead of print.

Authors

Qian Zhao¹, Björn Berglund², Huiyun Zou¹, Ziyu Zhou¹, Huiyu Xia¹, Ling Zhao¹, Lennart E Nilsson³, Xuewen Li⁴

Affiliations

¹ Department of Environment and Health, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, China.
² Department of Biomedical and Clinical Sciences, Linköping University, 581 85, Linköping, Sweden; State Key Laboratory for Diagnosis and Treatment of Infectious Disease, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China.
³ Department of Biomedical and Clinical Sciences, Linköping University, 581 85, Linköping, Sweden.
⁴ 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.

PMID: 33460870
DOI: 10.1016/j.envpol.2020.116370

Abstract

The environment of a large-scale vegetable production area can be exposed to antibiotic residues and antibiotic-resistant bacteria (ARB) via animal manure and irrigation with contaminated water, which can facilitate the dissemination of ARB. However, the occurrence of ARB in plantation areas and their dissemination in this environment remain largely unexplored. In total, 382 samples including those from vegetable (n = 106), soil (n = 87), well water (n = 24), river water (n = 20), river sediments (n = 20), farmer feces (n = 58) and farmer hands (n = 67) were collected in 2019 from a large-scale cultivation area in Shandong, China. Selective agar plates were used to screen for carbapenem-resistant Enterobacteriaceae (CRE) and whole-genome sequencing and Southern blotting were used to characterise isolates and mobile genetic elements carrying carbapenem resistance determinants. A total of nine NDM-5-producing isolates of Escherichia coli, Klebsiella pneumoniae, and Citrobacter spp. were identified from environmental sources and human feces, all of which were multidrug-resistant. Single nucleotide polymorphism analysis suggested clonal transmission of carbapenem-resistant Citrobacter sedlakii within greenhouse soils in the area. Eight of the isolates carried closely related or identical IncX3 plasmids carrying bla_NDM-5, which were shown to be conjugative via filter mating experiments, indicating the highly transmissible nature of this genetic element. Isolates of E. coli and Citrobacter freundii were detected in the feces of local farm workers and contained similar IncX3 plasmids with bla_NDM-5 environmental isolates, suggesting a potential risk of CRE transfer from the work environment to the farm workers. Thus, further research is required to investigate the potential health risks associated with environmental exposure to CRE in vegetable cultivation areas.

Keywords: CRE; IncX3 plasmids; Intensive vegetable cultivation area; NDM-5; Whole-genome sequencing.