Patient-environment transmission dynamics of multidrug resistant Enterobacteriaceae in a Dutch intensive care unit: a longitudinal retrospective and prospective analysis in a non-outbreak setting

Abstract Background In the intensive care unit (ICU), nosocomial acquisition of multidrug resistant Enterobacteriaceae (MDRE) may lead to adverse patient outcomes; however, investigating the link between patient MDRE colonization and environmental reservoirs is often not straightforward in a non-outbreak setting. This study aimed to characterize the patient-environment transmission dynamics of MDRE strains with a common resistance phenotype and genotype at the ICU wards of two hospitals. Methods The sink drains, faucet aerators, high-touch sites of medical devices and beds of (non-)patient rooms of two ICU were repetitively sampled (up to ten times) over the course of 18 months (2022 to 2023). Patient isolates and epidemiological data were collected retrospectively (2017 to 2022) and prospectively (during the environmental sampling). Inclusion criteria for MDRE isolates were: resistance to 3 rd -generation cephalosporins, gentamicin, ciprofloxacin and cotrimoxazole; and PCR positive for the antimicrobial resistance genes bla CTX-M-15 , qnrB1 and bla OXA-1 — aac(6’)-Ib-cr . Patient and subsetted environmental MDRE isolates were whole genome sequenced using Illumina technology. Clonal clusters were identified with SNP-analysis (≤25 SNPs), and further assessed through spatial and temporal epidemiological links. Results A total of 553 environmental MDRE isolates from 990 samples were primarily recovered from sink drains (97,1%), and 136 isolates from 91 patients. Both environmental isolates (98,7%) and patient isolates (91,2%; 80 patients) were mainly derived from a single ICU. Clonal assessment revealed a total of 19 patient-environment SNP-clusters, which incorporated 75 environmental and 36 patient isolates from eight distinct Enterobacteriaceae spp. Epidemiological investigation showed spatial links with environmental isolates for 31 patients. Furthermore, temporal links indicated possible transmission events from sink-to-patient for seven patients, and from patient-to-environment for three patients. Conclusion ICU sinks form an inherent and persistent risk-factor in the exchange of MDRE with patients. This risk appeared highly diffuse through various species and clones in the current non-outbreak setting. The MDRE patient colonization rates can likely be reduced through the reconsideration of the role and necessity of sinks in the ICU environmental, combined with prospective genomic monitoring of the patient and remaining sink drains MDRE isolates to detect patient-environment clusters and facilitate targeted interventions.