Dongyan Shao, Xiaoyang Ju, Yuchen Wu, Yanyan Zhang, Zelin Yan, Yifei Li, Lu Wang, Julian Parkhill, Timothy R. Walsh, Congming Wu, Jianzhong Shen, Yang Wang, Rong Zhang, Yingbo Shen
{"title":"Quaternary Ammonium Compounds: A New Driver and Hidden Threat for mcr-1 Prevalence in Hospital Wastewater and Human Feces","authors":"Dongyan Shao, Xiaoyang Ju, Yuchen Wu, Yanyan Zhang, Zelin Yan, Yifei Li, Lu Wang, Julian Parkhill, Timothy R. Walsh, Congming Wu, Jianzhong Shen, Yang Wang, Rong Zhang, Yingbo Shen","doi":"10.1021/acs.est.4c11368","DOIUrl":null,"url":null,"abstract":"The emergence of mobile colistin resistance gene <i>mcr-1</i> has attracted global attention. The prevalence of <i>mcr-1</i>-positive <i>Escherichia coli</i> (MCRPEC) in humans largely decreased following the ban of colistin as an animal growth promoter in China. However, the prevalence of MCRPEC in the hospital environment and the relationship between disinfectants and <i>mcr-1</i> remain unclear. We found that MCRPEC prevalence was low in the feces of healthy humans attending physical examinations in six hospitals (4.6%, 71/1532) but high in hospital wastewater (50.0%, 27/54). <i>mcr-1</i> was mainly located on IncI2 (63.0% in wastewater and 62.0% in feces) and IncHI2 plasmids (18.5% in wastewater and 21.1% in feces). High similarity of the <i>mcr-1</i> context and its carrying plasmids was observed in human and wastewater MCRPEC, with several isolates clustering together. The coexistence of the ESBL gene <i>bla</i><sub>CTX-M</sub> with <i>mcr-1</i> occurred in 19.7% of IncI2 plasmids. Notably, 60.0% of IncHI2 plasmids exhibited co-occurrence of <i>mcr-1</i> with the disinfectant resistance gene (DRG) <i>qacE<i>Δ</i><i>1</i></i>, conferring resistance to quaternary ammonium compounds (QACs). We revealed that QACs, rather than the other two types of disinfectants─<i>ortho</i>-phthalaldehyde (OPA) and povidone–iodine (PVP–I)─select for plasmids carrying both <i>qacE<i>Δ</i><i>1</i></i> and <i>mcr-1</i> and elevate their conjugative transfer frequency. Monitoring of DRGs in MCRPEC and managing disinfectant use are urgently needed in healthcare settings to mitigate the spread of colistin resistance from hospital environments to inpatients.","PeriodicalId":36,"journal":{"name":"环境科学与技术","volume":"5 1","pages":""},"PeriodicalIF":10.8000,"publicationDate":"2025-01-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"环境科学与技术","FirstCategoryId":"1","ListUrlMain":"https://doi.org/10.1021/acs.est.4c11368","RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ENGINEERING, ENVIRONMENTAL","Score":null,"Total":0}
引用次数: 0
Abstract
The emergence of mobile colistin resistance gene mcr-1 has attracted global attention. The prevalence of mcr-1-positive Escherichia coli (MCRPEC) in humans largely decreased following the ban of colistin as an animal growth promoter in China. However, the prevalence of MCRPEC in the hospital environment and the relationship between disinfectants and mcr-1 remain unclear. We found that MCRPEC prevalence was low in the feces of healthy humans attending physical examinations in six hospitals (4.6%, 71/1532) but high in hospital wastewater (50.0%, 27/54). mcr-1 was mainly located on IncI2 (63.0% in wastewater and 62.0% in feces) and IncHI2 plasmids (18.5% in wastewater and 21.1% in feces). High similarity of the mcr-1 context and its carrying plasmids was observed in human and wastewater MCRPEC, with several isolates clustering together. The coexistence of the ESBL gene blaCTX-M with mcr-1 occurred in 19.7% of IncI2 plasmids. Notably, 60.0% of IncHI2 plasmids exhibited co-occurrence of mcr-1 with the disinfectant resistance gene (DRG) qacEΔ1, conferring resistance to quaternary ammonium compounds (QACs). We revealed that QACs, rather than the other two types of disinfectants─ortho-phthalaldehyde (OPA) and povidone–iodine (PVP–I)─select for plasmids carrying both qacEΔ1 and mcr-1 and elevate their conjugative transfer frequency. Monitoring of DRGs in MCRPEC and managing disinfectant use are urgently needed in healthcare settings to mitigate the spread of colistin resistance from hospital environments to inpatients.
期刊介绍:
Environmental Science & Technology (ES&T) is a co-sponsored academic and technical magazine by the Hubei Provincial Environmental Protection Bureau and the Hubei Provincial Academy of Environmental Sciences.
Environmental Science & Technology (ES&T) holds the status of Chinese core journals, scientific papers source journals of China, Chinese Science Citation Database source journals, and Chinese Academic Journal Comprehensive Evaluation Database source journals. This publication focuses on the academic field of environmental protection, featuring articles related to environmental protection and technical advancements.