Quaternary Ammonium Compounds: A New Driver and Hidden Threat for <i>mcr-1</i> Prevalence in Hospital Wastewater and Human Feces

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>_CTX-M 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.