Genomic Investigation and Successful Containment of an Intermittent Common Source Outbreak of OXA-48-Producing Enterobacter cloacae Related to Hospital Shower Drains

Abstract

ABSTRACT The hospital environment has been reported as a source of transmission events and outbreaks of carbapenemase-producing Enterobacterales. Interconnected plumbing systems and the microbial diversity in these reservoirs pose a challenge for outbreak investigation and control. A total of 133 clinical and environmental OXA-48-producing Enterobacter cloacae isolates collected between 2015 and 2021 were characterized by whole-genome sequencing (WGS) to investigate a prolonged intermittent outbreak involving 41 patients in the hematological unit. A mock-shower experiment was performed to investigate the possible acquisition route. WGS indicated the hospital water environmental reservoir as the most likely source of the outbreak. The lack of diversity of the blaOXA-48-like harbouring plasmids was a challenge for data interpretation. The detection of blaOXA-48-like-harboring E. cloacae strains in the shower area after the mock-shower experiment provided strong evidence that showering is the most likely route of acquisition. Initially, in 20 out of 38 patient rooms, wastewater traps and drains were contaminated with OXA-48-positive E. cloacae. Continuous decontamination using 25% acetic acid three times weekly was effective in reducing the trap/drain positivity in monthly environmental screening but not in reducing new acquisitions. However, the installation of removable custom-made shower tubs did prevent new acquisitions over a subsequent 12-month observation period. In the present study, continuous decontamination was effective in reducing the bacterial burden in the nosocomial reservoirs but was not sufficient to prevent environment-to-patient transmission in the long term. Construction interventions may be necessary for successful infection prevention and control. IMPORTANCE The hospital water environment can be a reservoir for a multiward outbreak, leading to acquisitions or transmissions of multidrug-resistant organisms in a hospital setting. The majority of Gram-negative bacteria are able to build biofilms and persist in the hospital plumbing system over a long period of time. The elimination of the reservoir is essential to prevent further transmission and spread, but proposed decontamination regimens, e.g., using acetic acid, can only suppress but not fully eliminate the environmental reservoir. In this study, we demonstrated that colonization with multidrug-resistant organisms can be acquired by showering in showers with contaminated water traps and drains. A construction intervention by installing removable and autoclavable shower inserts to avoid sink contact during showering was effective in containing this outbreak and may be a viable alternative infection prevention and control measure in outbreak situations involving contaminated shower drains and water traps.

Keywords

• carbapenemase
• Enterobacter cloacae
• hospital outbreak
• infection control
• whole-genome sequencing