Candida auris is an emerging multidrug-resistant fungus that can cause invasive disease in critically ill patients with a mortality rate as high as 30%–60%. Reference Weber, Rutala and Sickbert-Bennett1 Increasing numbers of infections have been identified since it was first identified in Japan in 2009. In the United States, C. auris was made nationally notifiable in 2018. Between 2016 and the present, there has been a steady increase in the number of cases in the United States (53 cases in 2016 and 1,471 cases in 2021) as well as the number of states and countries reporting clinical cases of C. auris. Currently, C. auris has been divided into 5 geographical clades. Reference Weber, Rutala and Sickbert-Bennett1
C. auris presents a serious global health threat for several reasons to include the following: causes serious infections with high mortality; antifungal treatment options are limited; increasing prevalence; biofilm formation; has caused multiple outbreaks in healthcare facilities; persists on environment surfaces for days to weeks; a person can be colonized (or infected) with C. auris and shed it into the environment; C. auris can be spread from person-to-person directly via touch or secondarily through contact with contaminated surfaces and medical equipment; and C. auris is not rapidly inactivated by some commonly used disinfectants (eg, quaternary ammonium compounds diluted in water). Reference Weber, Rutala and Sickbert-Bennett1–Reference Cadnum, Shaikh and Piedrahita3 Patients with comorbidities, patients with immunosuppressive conditions, and patients on ventilators are more likely to develop C. auris infection. Reference Weber, Rutala and Sickbert-Bennett1
Floors are contaminated with Candida spp, Reference Kumar, Eilertson and Cadnum4 and there is indirect evidence supporting the potential for transfer of pathogens from floors to patients. Reference Donskey5 Deshpande et al Reference Deshpande, Cadnum and Fertelli6 showed that surfaces such as blood-pressure cuffs and call buttons were often in contact with the floor and in contact with those objects frequently resulted in transfer of pathogens to hands. One potential intervention to address floor contamination is the use of ultraviolet-C light (UV-C) and disinfectants with or without microfiber because microfiber may be more effective in removing microorganisms from environmental surfaces. Reference Rutala, Gergen and Weber7 This study was undertaken using current floor cleaning and disinfection methods to assess whether these strategies minimize the environmental spread of C. auris.
Methods
Disinfectants and C. auris clade used in this study
We investigated the efficacy of different cleaning and disinfection methods against C. auris. We evaluated 1 detergent cleaner (Prominence Heavy Duty Floor Cleaner, Diversey, Charlotte, NC) and 2 disinfectants. We evaluated 1 disinfectant with nonsporicidal claims [Virex II 256 One Step Disinfectant Cleaner (a quaternary ammonium compound), Diversey] and 1 disinfectant with a sporicidal claim [Spore Defense, Clorox, CA (0.25% sodium hypochlorite)]. The Virex II 256 did not have a Clostridioides difficile spore claim or a C. auris claim, whereas the Spore Defense had a 5-minute C. difficile spore claim and a 3-minute C. auris claim. C. auris (CDC AR no. 0385, clade 4) was obtained from the CDC Antibiotic Resistance Isolate Bank.
Test-surface inoculation and disinfection
We inoculated three 30×30-cm (12×12-inch) floor tiles with 105 to 106 colony-forming units (CFU) of C. auris in phosphate-buffered saline with 5% fetal calf serum. The 100 µL inoculum was spread to cover an entire tile using an L-shaped plastic spreader. To compare the microfiber (Hygen, Rubbermaid) and cotton mop (VanDuck 100% Cotton Mop Pads), the microfiber and cotton-mop pads were immersed in the test product (ie, water, detergent, disinfectant), and the excess fluid was wrung out. The tiles were wiped 3 times (from left to right and back) first covering the C. auris inoculated tiles and then the 2 adjacent tiles (Fig. 1). The purpose of wiping the 2 adjacent tiles was to assess the potential for transfer of C. auris to uninoculated tiles. Each of the tile surfaces were sampled using rayon swabs (BBL CultureSwabs; Becton, Dickinson, and Company, Franklin Lakes, NJ) premoistened with Dey-Engley neutralizer. The swabs were spun in a vortexer in 200 μL PBS with 0.5% polysorbate 80. Dilutions were plated on Sabouraud dextrose agar, and the plates were incubated for 72 hours at 37oC. The experiments were repeated 3 times. The recovery of C. auris from control (ie, untreated) tiles was ∼4-log.
Figure 1. Picture of 30×30-cm (12×12-inch) floor tiles used for inoculation with Candida auris and wiping with microfiber and cotton cloth mops. Three 30×30-cm (12×12-inch) tiles were inoculated (shown as 1–3) and wiped from left to right and back 3 times.
For UV-C light treatment (UVDI, Santa Clarita, CA), a 10-minute exposure was used with the device positioned 91cm (3 feet) from and perpendicular to the inoculated tile.
Results
The sporicidal disinfectant with microfiber and UV-C reduced C. auris on the floor to undetectable levels (Table 1) and did not allow transfer to adjacent tiles. Microfiber with water, detergent and the 2 disinfectants reduced C. auris by >3-log10 or 99.9% on tile 1. Cotton mop pads with the 2 disinfectants and the detergent reduced C. auris by >3-log10 on tile 1, but cotton mop pads with water did not. Microfiber and/or cotton mops transferred C. auris to uninoculated tiles when used with water, the detergent, and the quaternary ammonium compound, but no transfer to uninoculated tiles occurred with the sporicidal disinfectant.
Table 1. Inactivation and/or Removal of C. auris From Floors by UV-C and Microfiber or Cloth Mops With Water, Detergent
Note. SEM, standard error of the mean; N/A, not applicable; ND, none detected.
Discussion
C. auris is inactivated by many disinfectants, but it is not rapidly inactivated by a commonly used floor disinfectant (ie, a quaternary ammonium compound diluted in water). Reference Rutala, Kanamori, Gergen, Sickbert-Bennett and Weber2,Reference Cadnum, Shaikh and Piedrahita3 Because floors may be a source of pathogen contamination on hands, Reference Deshpande, Cadnum and Fertelli6 and quaternary-ammonium compounds are not rapidly effective against C. auris, we investigated other strategies for inactivating or removing C. auris on floors.
Our data suggest that the most effective method to eliminate C. auris from floors is UV-C and a sporicidal disinfectant. Sporicidal disinfectants have been shown to inactivate C. auris and provide an option to eliminate C. auris from floors. Reference Rutala, Kanamori, Gergen, Sickbert-Bennett and Weber2,Reference Cadnum, Shaikh and Piedrahita3 Another possible option, which was not tested, is nonsporicidal disinfectants that are registered against C. auris (ie, List P). 8
Water, detergent, and a nonsporicidal disinfectant (with no C. auris claim) cross-contaminated uncontaminated surfaces from an inoculated tile. This procedure demonstrated that when C. auris was not inactivated by the floor “treatment” procedure, the mop (cotton or microfiber) will physically move the C. auris from a contaminated to clean surface because C. auris remained viable and the potential for hand contamination was not eliminated. Reference Rutala, Kanamori, Gergen, Sickbert-Bennett and Weber2,Reference Cadnum, Shaikh and Piedrahita3,Reference Cadnum, Hurless, Kundrapu and Donskey9
A 10-minute UV-C exposure was very effective in eliminating C auris on the floor. In an earlier publication, longer UV-C treatment cycles (eg, 20 minutes) were necessary to achieve a 3 log10 reduction in C. auris at 152.4 cm (5 feet). Reference Cadnum, Shaikh, Piedrahita, Jencson, Larkin, Ghannoum and Donskey10 In the current study, the UV-C device was in closer proximity to the inoculated tiles (91 cm) and the inoculum was less concentrated because it was spread over an entire tile versus a 10–40-mm–diameter steel disk. Reference Cadnum, Shaikh, Piedrahita, Jencson, Larkin, Ghannoum and Donskey10
Our study had several limitations. Only one detergent, quaternary ammonium disinfectant, and sporicidal disinfectant were tested, and only 3 repetitions were performed. Although the microfiber mop with Virex II transferred C. auris, no transfer was detected with the cotton mop and Virex II. Therefore, we cannot exclude the possibility that cotton mop with Virex II would be as effective as the cotton mop with Spore Defense. Evaluations of UV-C in clinical settings are needed because it is not known whether the laboratory results for UV-C are applicable to real-world settings. Finally, the detergent Prominence may contain octyl phenol ethoxylate, which could have some antimicrobial activity.
In summary, several publications have offered indirect evidence that contaminated floors may contribute to transmission of pathogens. Reference Donskey5,Reference Deshpande, Cadnum and Fertelli6 Although additional evidence may be required before substantial interventions in cleaning and disinfection are justified, Reference Donskey5 prudent practices to minimize transmission of C. auris from floors in endemic or epidemic settings include the use of disinfectants [US EPA List P (C. auris claim) and List K (sporicidal)] and technologies (eg, UV-C) known to be effective in killing C. auris.
Acknowledgments
Financial support
No financial support was provided relevant to this article.
Competing interests
Dr. Rutala is a consultant to PDI and Kinnos. Dr. Donskey has received research grants from Clorox, Pfizer, and EcoLab.
