Long-term dissemination of NDM-producing Enterobacterales in two French hospitals (2020–2024): outbreak complexity and the role of drains as environmental reservoirs

Background Carbapenemase-producing Enterobacterales (CPE) represent a major public health threat, particularly in healthcare settings where long-term outbreaks may be sustained by environmental reservoirs. In France, although OXA-48-like enzymes remain predominant, NDM-producing Enterobacterales are increasingly reported, notably among Enterobacter cloacae complex (ECC) and Citrobacter freundii complex (CFC). The contribution of hospital drainage systems to the persistence of such outbreaks remains insufficiently characterised. Methods We conducted a five-year genomic and epidemiological investigation (2020–2024) of NDM-producing ECC and CFC in two hospitals in western France. Clinical and environmental isolates were analysed using whole-genome sequencing to assess clonality, resistance profiles and plasmid structures. Fourier-transform infrared spectroscopy was used to compare additional environmental and clinical isolates. Targeted environmental control bundles, including replacement with valve drains, daily bleaching and steam-based sanitization, were implemented and evaluated. Results Fifty-one patients were identified as carriers or infected with NDM-producing ECC or CFC. Two clonal outbreaks were documented: Enterobacter xiangfangensis ST111, persisting in both hospitals over four years ( n = 34), and Citrobacter portucalensis ST408, responsible for a shorter outbreak in one hospital ( n = 7). Whole-genome sequencing confirmed clonal transmission without evidence of plasmid-mediated spread between species. Environmental sampling repeatedly identified E. xiangfangensis ST111 in drains, including sink and shared shower drains, over time, demonstrating sustained environmental persistence despite reinforced infection prevention and control measures. Conclusions Our findings demonstrate that hospital drainage systems can act as long-term reservoirs sustaining the transmission of NDM-producing Enterobacterales. Standard infection control measures alone may be insufficient to control such outbreaks. Targeted environmental interventions should be systematically integrated into infection prevention strategies to limit the spread of highly resistant organisms.