First reported detection of the mobile colistin resistance genes, mcr-8 and mcr-9, in the Irish environment

Niamh Cahill; Brigid Hooban; Kelly Fitzhenry; Aoife Joyce; Louise O'Connor; Georgios Miliotis; Francesca McDonagh; Liam Burke; Alexandra Chueiri; Maeve Louise Farrell; James E Bray; Niall Delappe; Wendy Brennan; Deirdre Prendergast; Montserrat Gutierrez; Catherine Burgess; Martin Cormican; Dearbháile Morris

doi:10.1016/j.scitotenv.2023.162649

First reported detection of the mobile colistin resistance genes, mcr-8 and mcr-9, in the Irish environment

Sci Total Environ. 2023 Jun 10:876:162649. doi: 10.1016/j.scitotenv.2023.162649. Epub 2023 Mar 10.

Authors

Niamh Cahill¹, Brigid Hooban², Kelly Fitzhenry², Aoife Joyce², Louise O'Connor², Georgios Miliotis², Francesca McDonagh², Liam Burke², Alexandra Chueiri², Maeve Louise Farrell², James E Bray³, Niall Delappe⁴, Wendy Brennan⁴, Deirdre Prendergast⁵, Montserrat Gutierrez⁵, Catherine Burgess⁶, Martin Cormican⁷, Dearbháile Morris²

Affiliations

¹ Antimicrobial Resistance and Microbial Ecology Group, School of Medicine, University of Galway, Galway, Ireland; Centre for One Health, Ryan Institute, University of Galway, Galway, Ireland. Electronic address: niamh.cahill@universityofgalway.ie.
² Antimicrobial Resistance and Microbial Ecology Group, School of Medicine, University of Galway, Galway, Ireland; Centre for One Health, Ryan Institute, University of Galway, Galway, Ireland.
³ Department of Biology, University of Oxford, Oxford, United Kingdom.
⁴ National Carbapenemase-Producing Enterobacterales Reference Laboratory, National Salmonella, Shigella and Listeria Reference Laboratory, University Hospital Galway, Galway, Ireland.
⁵ Department of Agriculture, Food and the Marine, Celbridge, Co. Kildare, Ireland.
⁶ Food Safety Department, Teagasc Food Research Centre, Ashtown, Dublin, Ireland.
⁷ Antimicrobial Resistance and Microbial Ecology Group, School of Medicine, University of Galway, Galway, Ireland; Centre for One Health, Ryan Institute, University of Galway, Galway, Ireland; National Carbapenemase-Producing Enterobacterales Reference Laboratory, National Salmonella, Shigella and Listeria Reference Laboratory, University Hospital Galway, Galway, Ireland.

PMID: 36906027
DOI: 10.1016/j.scitotenv.2023.162649

Abstract

The emergence and dissemination of mobile colistin resistance (mcr) genes across the globe poses a significant threat to public health, as colistin remains one of the last line treatment options for multi-drug resistant infections. Environmental samples (157 water and 157 wastewater) were collected in Ireland between 2018 and 2020. Samples collected were assessed for the presence of antimicrobial resistant bacteria using Brilliance ESBL, Brilliance CRE, mSuperCARBA and McConkey agar containing a ciprofloxacin disc. All water and integrated constructed wetland influent and effluent samples were filtered and enriched in buffered peptone water prior to culture, while wastewater samples were cultured directly. Isolates collected were identified via MALDI-TOF, were tested for susceptibility to 16 antimicrobials, including colistin, and subsequently underwent whole genome sequencing. Overall, eight mcr positive Enterobacterales (one mcr-8 and seven mcr-9) were recovered from six samples (freshwater (n = 2), healthcare facility wastewater (n = 2), wastewater treatment plant influent (n = 1) and integrated constructed wetland influent (piggery farm waste) (n = 1)). While the mcr-8 positive K. pneumoniae displayed resistance to colistin, all seven mcr-9 harbouring Enterobacterales remained susceptible. All isolates demonstrated multi-drug resistance and through whole genome sequencing analysis, were found to harbour a wide variety of antimicrobial resistance genes i.e., 30 ± 4.1 (10-61), including the carbapenemases, bla_OXA-48 (n = 2) and bla_NDM-1 (n = 1), which were harboured by three of the isolates. The mcr genes were located on IncHI2, IncFIIK and IncI1-like plasmids. The findings of this study highlight potential sources and reservoirs of mcr genes in the environment and illustrate the need for further research to gain a better understanding of the role the environment plays in the persistence and dissemination of antimicrobial resistance.

Keywords: Antimicrobial resistance; Colistin; Enterobacterales; Environment; mcr-8; mcr-9.

MeSH terms

Anti-Bacterial Agents* / pharmacology
Bacteria / genetics
Colistin* / pharmacology
Drug Resistance, Bacterial / genetics
Klebsiella pneumoniae
Microbial Sensitivity Tests
Plasmids
Wastewater

Substances

Colistin
Anti-Bacterial Agents
Wastewater