Drivers of the emergence and dissemination of high-risk resistance genes in cattle farm

IF 12.2 1区环境科学与生态学 Q1 ENGINEERING, ENVIRONMENTAL

Journal of Hazardous Materials Pub Date : 2025-01-29 DOI:10.1016/j.jhazmat.2025.137415

Yanxiang Jiao, Xingxing Zhang, Feifan Yang, Luchao Lv, Yingbo Gao, Zhongpeng Cai, Wenxian Pu, Guolong Gao, Dandan He, Fagang Zhong, Jian-Hua Liu

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引用次数: 0

Abstract

Extended spectrum β-lactamase (ESBL)- and carbapenemase-producing Enterobacterales (CPE) are recognized by WHO as critical concerns. The high cephalosporin resistance rate in a cattle farm in 2018 prompted us to conduct long-term (2019-2023) and extensive monitoring to explore risk factors for the import and transmission of ESBLs and CPE in this farm. Among 1288 samples from cattle, the environment, milk, and biological vectors, 48.8% carried bla_CTX-M-positive Enterobacterales with bla_CTX-M-55 being dominant (76.4%), and bla_NDM-5-positive strains emerged in 2022 with a 1.9% detection rate. bla_CTX-M-55 and bla_NDM-5 were likely introduced through various routes, especially wild birds, and have persisted due to overuse of cephalosporins in the farm. The spread of these genes was driven by the horizontal transmission of IncHI2 and IncX3 plasmids and clonal dissemination of certain clones. Cross-regional and cross-border transmission of bla_CTX-M-55- and/or bla_NDM-5-bearing bacteria and plasmids possibly occurred via wild birds, animal trade, and other means. Our findings suggest that the import, persistence, and dissemination of these genes within and beyond this farm, were fueled by suboptimal biosecurity practices and inadequate antibiotic stewardship, highlighting the urgency for integrated public and ecosystem health policies to prevent the spread of resistance genes as part of a holistic One Health strategy.

Environmental implication

The high prevalence and long-term persistence of extended-spectrum β-lactamases and the emergence of carbapenemases in cattle and the environment signify a critical risk of transmitting high-risk resistance genes, posing a significant threat to human health. Consequently, bacteria carrying these genes in animal farms should be regarded as "hazardous materials". Import, persistence, and dissemination of these genes within and beyond this farm were exacerbated by suboptimal biosecurity practices and inadequate antibiotic stewardship, highlighting the urgency for integrated public and ecosystem health policies to mitigate the environmental risks associated with gene transmission as part of a comprehensive One Health strategy.

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来源期刊

Journal of Hazardous Materials 工程技术-工程：环境

CiteScore

25.40

自引率

5.90%

发文量

3059

审稿时长

58 days

期刊介绍： The Journal of Hazardous Materials serves as a global platform for promoting cutting-edge research in the field of Environmental Science and Engineering. Our publication features a wide range of articles, including full-length research papers, review articles, and perspectives, with the aim of enhancing our understanding of the dangers and risks associated with various materials concerning public health and the environment. It is important to note that the term "environmental contaminants" refers specifically to substances that pose hazardous effects through contamination, while excluding those that do not have such impacts on the environment or human health. Moreover, we emphasize the distinction between wastes and hazardous materials in order to provide further clarity on the scope of the journal. We have a keen interest in exploring specific compounds and microbial agents that have adverse effects on the environment.