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Infection Control & Hospital Epidemiology


environment, environmental cultures were conducted eight times during the outbreak period from May to December 2014. In total, 195 samples were collected on eight different sampling days (see supplementary materials). A retrospective study was conducted to explore the risk factors of MBL-producing Enterobacteriaceae acquisition. We obtained demographic and clinical data of patients with an active surveillance culture (see Supplementary Materials online).


Statistical analysis


Univariate analysis was performed using the χ2 test and the Fisher exact test. The Mann-Whitney U test was used for continuous vari- ables. Candidate variables with P<.10 in univariate analysis were included in the multivariate analysis. Sensitivity analysis controlling for other covariates was conducted. All statistical analyses were con- ducted with SPSS version 22 software (IBM, Armonk, NY).


Results


In total, 249 patients were admitted to the ward during the study period. Active surveillance was performed once weekly except at the time of admission; however, 104 patients did not undergo a rectal swab for the surveillance culture due to their shorter period of hospitalization. The 145 patients who had undergone a rectal swab were included for analysis. The characteristics of these patients are shown in Table 1. Overall, 36 patients (24.8 %) yielded a total of 39 strains ofMBL-


producing Enterobacteriaceae including 30 cases of K. pneumoniae, 5cases of Escherichia coli,2casesof Citrobacter freundii,1 case of Klebsiella oxytoca, and 1 case of Enterobacter aerogenes. MBL-producing K. pneumoniae was isolated from 7 environ-


mental samples (3.6 %). At the first sampling, a sink in the nurses’ station tested positive. At the third sampling, another sink in the nurse’s station and the milk bottle cabinet were positive. Finally, at the eighth sampling, 4 positive samples were obtained from the tea dispenser. We sequenced the whole genome of 37 K. pneumoniae strains


isolated from the clinical and environmental samples. All isolates harbored the blaIMP-1 gene. A core-genome single nucleotide polymorphism (SNP)–based phylogenetic analysis revealed that 33 of the blaIMP-1-positive K. pneumoniae strains had a common ancestor (see the Supplementary Materials online).


Risk factor analysis


The results of our univariate analysis exploring the risk factors of MBL-producing Enterobacteriaceae acquisition are shown in Table 1. Our multivariate analysis revealed that use of the tea dispenser (adjusted OR [aOR], 43.69; 95% CI, 7.33–260.49) and longer length of hospital stay (aOR, 1.03; 95% CI, 1.01–1.04) were associated with the acquisition of these pathogens. Sensitivity analysis controlling for other covariates did not affect the results of the multivariate analysis.


Infection control measures


We applied strict cohorting of patients with MBL-producing Enter- obacteriaceae. Use of public areas such as the playroom and dining hall in the ward was banned due to the potential sources of trans- mission. Staff education in appropriate standard and contact pre- cautions was reinforced. Routine environmental cleaning, including


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cleaning of the sinks and frequently touched areas using 0.1% hypochlorite was increased from 1 to 3 times daily. Admission to the ward was restricted twice during the outbreak to prevent spreading the pathogens. NoMBL-producing Enterobacteriaceae were isolated from patients admitted to the ward or occupying the ward environment after banning the use of the tea dispenser.


Discussion


We have described the largest documented pediatric outbreak of blaIMP-1-positive K. pneumoniae in Japan. Environmental sam- pling and epidemiological investigation identified a tea dispenser in the ward as the contaminant source. The tea dispenser, placed in a public area in the ward for the


use of patients and visitors, automatically mixes barley tea powder with hot water in a shaker before diluting with cold water and dispensing the liquid as iced tea. The maintenance and cleaning of the tea dispenser were done by the cleaning staff using detergents once daily according to the manufacturer’s instructions. The cleaning staff were also responsible for the disposal of the children’s diapers in the ward. MBL-producing Enterobacteriaceae were detected in the shaker, which was handled only by the cleaning staff, suggesting that it had become contaminated by their hand- ling. An interview of the cleaning staff later revealed that their knowledge and practice of hand hygiene were inadequate. Self- service tea and water dispensers, commonly available to patients in medical facilities throughout Japan, may readily act as a medium for infection among a patient population if contaminated. However, reports of CPE outbreaks among the pediatric population are rare, and the mode of transmission has never been clarified.7,8 Moreover, existing reports have focused on the molecular characteristics of CPE or were unable to determine the route of transmission due to inadequate outbreak investigation. In contrast, in our study, rigorous outbreak investigation and com- prehensive molecular typing demonstrated that a tea dispenser was thelikely sourceof transmission. The surveillance cultures of the environmental samples in the present study revealed that 2 cultures from the sinks in the nurses’ station were positive for MBL-producing K. pneumoniae. It is likely that these positive results are due to environmental contamination because the outbreak continued despite rigorous cleaning of these areas. Another hypothesis proposes that water supplied in the hospital was contaminated by MBL- producing K. pneumoniae, but this is unlikely because none of the clinical samples from other wards yielded the pathogens, and cultures of the water samples from the tea dispenser were also negative. The phylogenetic analysis based on core-genome SNPs


revealed that the blaIMP-1-positive ST34 K. pneumoniae isolated in the outbreak had a common ancestor (see Supplementary Mate- rials online). Therefore, the analysis suggested that the tea dis- penser was the source. Also, a longer stay in the ward was significantly related to CPE colonization. Usually, a long hospital stay is a risk factor for acquiring CPE,9 but its relationship to CPE acquisition is weaker than in the present case of the use of the tea dispenser. We assume that the longer hospital stay created more opportunities for using the contaminated tea dispenser. In summary, we experienced an outbreak of IMP-1 MBL-


producing Enterobacteriaceae among pediatric patients in a tertiary-care children’s hospital. After rigorous investigation, a cold tea dispenser was identified as the source of contamination. Despite the rarity of this mode of transmission, infection control


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