Hospital-wide genomic surveillance reveals heterogeneous transmission dynamics of sink-associated carbapenemase-producing Enterobacterales

After a 2019 multispecies carbapenemase-producing Enterobacterales (CPE) outbreak, transmission persisted in a 660-bed hospital in South Korea despite enhanced screening and infection prevention and control measures. We evaluated the extent of environmental contamination, contribution of environmental reservoirs to ongoing transmission, and impact of targeted interventions. From January 2021 to April 2022, we conducted three rounds of hospital-wide environmental surveillance. Whole-genome sequencing of 61 environmental and clinical isolates was performed to assess clonal relatedness and plasmid-mediated spread. Interventions included daily sink decontamination, reinforcement of appropriate sink use, and waste-pipe replacement. In the first surveillance round, CPE was detected at 26 of 349 sampled sites (7.5%) across 13 of 16 hospital units (81.3%), with most positive sites identified in sinks (92.3%, 24/26). Among 42 environmental isolates, New Delhi metallo-β-lactamase (NDM)-1 was the predominant carbapenemase (59.5%, 25/42), and NDM-1-producing Enterobacter asburiae (NDM-1-EAS) was recovered from 15 sinks across 7 wards. Following intervention, contamination was eliminated from 21 of 26 positive sites (80.8%); however, NDM-1-EAS recurred in 4 sinks after waste-pipe replacement. Among 57 hospital-linked CPE cases, NDM-1 was identified in 9 species ( n = 24), whereas Klebsiella pneumoniae carbapenemase (KPC)-2 was detected predominantly in Klebsiella pneumoniae ( n = 23). After intervention, NDM-1 incidence declined, whereas KPC-2-producing K. pneumoniae (KPC-2-KPN) persisted. Genomic analysis demonstrated that a persistent NDM-1-EAS ST484 sink clone was associated with subsequent patient acquisition and that bla NDM−1 dissemination was mediated by highly conserved IncX3 plasmids shared between environmental and clinical isolates. In contrast, KPC-2-KPN ST307 spread through person-to-person contact, with sinks acting as transient reservoirs. Hospital sink reservoirs sustained NDM-1-CPE transmission through both clonal spread and horizontal plasmid dissemination, whereas KPC-2_KPN transmission was largely independent of sink colonisation. Effective CPE control requires both reservoir- and patient-directed strategies.