Discussion

Given the increasing awareness that hospital water environment, especially sinks, can be a source of multidrug-resistant bacteria, including CPE, several studies have evaluated methods of sink-trap decontamination, including bleach, alcohol, acetic acid, hot water, hydrogen peroxide vapor, ultraviolet light, and sink-trap replacement. ^{Reference Kizny Gordon, Mathers and Cheong6,Reference Carling10} Regev-Yochay et al. attempted to decontaminate sink-traps during an outbreak of OXA-48-producing Serratia marcescens by replacing the “disinfecting” sink traps, heating and hyperchlorination of the main water tank, weekly acetic acid treatment, and daily treatment with 1,000 ppm hypochlorite. However, none of aforementioned strategies could disinfect the contaminated sink traps. ^{Reference Regev-Yochay, Smollan and Tal11} In 2019, many sinks in the wards of our hospital were contaminated with CPEs, which prompted us to initiate daily cleaning of the sinks with 1,000 ppm hypochlorite. Although complete elimination was not achieved, the number of CPE-positive sinks was significantly decreased.

Although the replacement of sinks and drainage systems seems to be the most effective method to eliminate CPE, ^{Reference Kizny Gordon, Mathers and Cheong6} we could not replace all CPE-positive sinks. In 2021, we replaced sink basins in the PICU, high-care unit, and cardiology wards with deeper ones to facilitate appropriate handwashing procedures and eliminate horizontal transmission of the resistant organisms. Shallow basins can cause cross-contamination of hands during handwashing and promote splashing, with subsequent contamination of the faucet, sink collar, and adjacent surfaces. ^{Reference Parkes and Hota12–Reference Gestrich, Jencson, Cadnum, Livingston, Wilson and Donskey14} In 2023, CPEs were not detected from the replaced sinks, and we plan to introduce the deeper basins in the wards other than those mentioned above.

We selected the daily use of 1,000 ppm foam-type sodium hypochlorite to prevent CPE transmission from contaminated sinks because of cost-effectiveness and convenience. According to one review article by Gordon et al. some studies reported successful cessation of CPE outbreaks using disinfection with bleach. ^{Reference Kizny Gordon, Mathers and Cheong6} On the other hand, more recently, Buchan et al. reported that a hydrogen peroxide-based foam disinfectant was more effective than liquid bleach in decreasing sink drain bacterial counts. ^{Reference Buchan, Arvan and Graham15} Furthermore, according to the study of Jones et al. the use of foam-type application of hydrogen peroxide and peracetic acid disinfectant significantly reduced recovery of gram-negative bacilli comparing with pouring liquid. ^{Reference Jones, Mana and Cadnum16} Although hypochlorite might be less effective than hydrogen peroxide and peracetic acid, daily application of foamy disinfectant was likely effective enough to reduce the number of contaminated sinks.

Although we started cleaning sinks with hypochlorite in 2019, the CPE outbreak in 2020–2021 could not be prevented. Contaminated sinks probably did not play a main role in the outbreak, considering that E. cloacae complex was only detected from the sinks in two rooms of the cardiology ward, and eight of the 19 patients became CPE-positive without prior admission to the cardiology ward. At the time of the outbreak, hand hygiene compliance was <70%, and we attributed the outbreak to the low awareness of hand hygiene. To eliminate this outbreak, we enforced infection control methods, including isolation of CPE-positive patients, appropriate use of personal protective equipment, and appropriate handwashing. Since late 2021, hand hygiene at our hospital has remained around 80%.

In our study, the number of CPE-positive sinks was significantly decreased after daily cleaning with bleach was started. However, when data were examined separately for the risk of contact with nutrition-rich substances, only Risk L (lower risk) sinks showed a reduced risk. It is possible that the drain pipes of Risk H (higher risk) sinks contain more biofilms than those of Risk L, leading to the continuous release of resistant bacteria. Parkes et al. reviewed several studies related to strategies for biofilm disruption. ^{Reference Parkes and Hota12} Pressurized steam with a chlorine-containing solution showed temporary clearance followed by re-emergence of carbapenemase-producing K. pneumoniae. Self-disinfecting traps, using vibration, heat, and ultraviolet light to prevent biofilm formation, seems promising, although they incur substantial cost and may require further evaluation in healthcare settings.

Considering the difficulties of eliminating CPE-containing biofilm from sink traps, educational interventions seem important. Kotay et al. demonstrated in their experimental sinks where biofilm-containing traps were transplanted that, even if CPE turned negative with soap and water cleaning, they immediately re-emerged after the introduction of carbon- and nitrogen-rich nutrients. ^{Reference Kotay, Parikh and Barry17} In pediatric wards, excess milk and enteral formula tend to be unintentionally discarded in handwashing sinks. Therefore, strict guidelines regarding sink use should be developed and followed by the staff, including avoiding discarding excess milk into handwashing sinks, specifying sinks that are used exclusively for handwashing, and prohibiting the storage of clean patient material around sinks.

Among the carbapenemases of CPEs, IMP-1 is the most commonly detected in Japan. ^{Reference Kotay, Parikh and Barry17} Other frequently detected genotypes outside Japan, such as NDM, KPC, and OXA-48, are rarely found in Japan. ^{Reference Hara, Iguchi and Tetsuka18,Reference Eda, Nakamura and Takayama19} In our study, the CPEs isolated from sinks and patients had IMP-1 or IMP-11. Although Chen et al. found that IMP-11-producing CRE were reported among the long-term care facilities in Japan, ^{Reference Chen, Jean and Lee20} the Yokohama City Institute of Public Health has never detected CPEs producing IMP-11 except those isolated from our hospital (personal communication). In 2018, three patients were identified as carriers of CPEs producing IMP-11, although none of them were identical species. Therefore, we speculate that these resistant bacteria isolated from patients were likely derived from the sinks, rather than outside the hospital.

This study has several limitations that should be acknowledged. First, we collected environmental samples from only sink bowls and drain outlets. Samples from deeper zone of the drain tubes, faucets, or surfaces outside the sink bowls were not obtained. Furthermore, we seeded samples directly onto selective agar media, without prior broth enrichment. If we obtained samples from wider areas and cultured samples in broth media before seeding onto agar media, CPE might be detected from a higher number of sinks. Second, we obtained environmental culture three times with an interval of 2 years. If we had implemented the surveillance culture more frequently, the effect of our intervention, such as cleaning sink bowls with bleach and prohibiting disposal of milk into sinks, might have been described in more detail. Third, we used PFGE to describe phylogeny of outbreak isolates. Although whole genome sequencing seems to have replaced PFGE in recent outbreak investigations due to its advantage in tracking the outbreak process, ^{Reference Decraene, Phan and George4,Reference Chen, Zhou and Fan21} our laboratory was in the process of transitioning to a new analysis method such as next-generation sequencing, and we used the conventional analysis method for this study.

In conclusion, after we noticed that three patients admitted to our hospital were CPE-positive, we initiated sequential surveillance cultures of 180 sinks in nine wards of our hospital in 2019, 2021, and 2023. In total, 30 of 180 sinks were contaminated with CPE in 2019. Therefore, we conducted daily cleaning of sinks with sodium hypochlorite. Although the number of CPE-contaminated sinks was significantly decreased, contamination of sinks with a high risk of contact with nutrition-rich substances was not reduced despite daily cleaning with bleach, even after discarding excess milk into the handwashing sinks was prohibited. Because the PFGE patterns of CPEs isolated from patients and nearby sinks were almost identical, it is likely that the contaminated sinks in our hospital wards were reservoirs of disseminating CPE to the patients, although the main cause of the outbreak in 2020–2021 was horizontal transmission due to insufficient hand hygiene. In addition to the efforts to decrease the sink-related CPE contamination, educational interventions, such as compliance monitoring of strict hand hygiene and guidelines of sink use, is important to prevent outbreaks.