The shared NDM-positive strains in the hospital and connecting aquatic environments

Huiyun Zou; Jingyi Han; Ling Zhao; Di Wang; Yanyu Guan; Tianle Wu; Xinjiao Hou; Hui Han; Xuewen Li

doi:10.1016/j.scitotenv.2022.160404

The shared NDM-positive strains in the hospital and connecting aquatic environments

Sci Total Environ. 2023 Feb 20:860:160404. doi: 10.1016/j.scitotenv.2022.160404. Epub 2022 Nov 22.

Authors

Huiyun Zou¹, Jingyi Han², Ling Zhao¹, Di Wang¹, Yanyu Guan¹, Tianle Wu¹, Xinjiao Hou¹, Hui Han³, 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 Thoracic Surgery, Qilu Hospital of Shandong University, Jinan, Shandong, China.
³ Department of Infection Control, Qilu Hospital of Shandong University, Jinan, China. Electronic address: 18560085566@163.com.
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: 36427732
DOI: 10.1016/j.scitotenv.2022.160404

Abstract

The spread of antibiotic-resistant priority pathogens outside hospital settings is, both, a significant public health concern and an environmental problem. In recent years, New Delhi Metallo-β-lactamase (NDM)-positive strains have caused nosocomial infections with high mortality and poor prognosis worldwide. Our study investigated the links of NDM-positive strains between the hospital and the connecting river system in Jinan city, Eastern China by using NDM-producing Escherichia coli (NDM-EC) as an indicator via whole genome sequencing. Thirteen NDM-EC isolates were detected from 187 river water and sediment samples, while 9 isolates were identified from patients at the local hospital. All NDM-EC isolates were resistant to imipenem, meropenem, cefotaxime, cefoxitin, ampicillin, tetracycline, fosfomycin, piperacillin-tazobactam. The bla_NDM-5 (n = 20) and bla_NDM-9 (n = 2) genes were identified, which were predominantly on IncX3 plasmids (n = 13), followed by IncFII plasmids (n = 5) and IncFIA plasmids (n = 2). Conjugation experiments showed that 21 isolates could transfer NDM-harboring plasmids. The well-conserved bla_NDM-5 genetic environment (ISAba125-bla_NDM-5/9-ble_MBL-trpF-dsbD-IS26) of these plasmids suggested a common genetic origin. Nine sequence types (STs) were detected, including three international high-risk clones ST167 (n = 8), ST410 (n = 1), and ST617 (n = 1). Phylogenetic analysis showed ST167 E. coli from the river was genotypically related to clinical isolates recovered from patients. Furthermore, ST167 isolates showed high genetic similarities with other clinical strains from geographically distinct regions. The genetic concordance between isolates from different sampling sites in the same river (ST218 clone), and different rivers (ST448 clone) raises concerns regarding the rapid dissemination of NDM-EC in the aquatic environment. The emergence and spread of the clinically relevant NDM-positive strains, especially for E. coli ST167 clone, an international high-risk clone associated with multi-resistance and virulence capacity, within and between the hospital and aquatic environments were elucidated, highlighting the need for attention and action.

Keywords: Aquatic environment; Hospital; NDM-positive strains; Transmission; indicator strain.

MeSH terms

Anti-Bacterial Agents / pharmacology
Drug Resistance, Multiple, Bacterial* / genetics
Escherichia coli*
Hospitals
Humans
Microbial Sensitivity Tests
Phylogeny
Plasmids
beta-Lactamases / genetics

Substances

Anti-Bacterial Agents
beta-Lactamases