Candida auris is an emerging fungal pathogen that is often resistant to antifungal drugs. It is a serious global health threat and has caused severe infections with frequent mortality in many countries. Candida auris can survive on healthcare environmental surfaces for at least 7 days and cause outbreaks in healthcare facilities. Reference Vallabhaneni, Kallen and Tsay1–Reference Rutala, Kanamori, Gergen, Sickbert-Bennett and Weber5 These findings suggest that C. auris has an environmental route of transmission. Thus, infection prevention strategies, such as surface disinfection and room decontamination technologies (eg, ultraviolet-C or UV-C), are essential to controlling transmission. Reference Vallabhaneni, Kallen and Tsay1–Reference deGroot, Chowdhary, Meis and Voss8 Unfortunately, data on the activity of UV to inactivate this pathogen are limited. Reference Cadnum, Shaikh and Piedrahita7,Reference deGroot, Chowdhary, Meis and Voss8 In this study, a UV-C device was evaluated for its antimicrobial activity against C. auris and C. albicans.
Methods
This study was conducted at the University of North Carolina Hospitals, an acute-care tertiary hospital in Chapel Hill, North Carolina. A single UV-C device was investigated (Tru-D, Lumalier, Memphis, TN). We tested the antifungal activity of this device using the vegetative bacteria cycle, which delivers a reflected dose of 12,000 µWs/cm Reference Schelenz, Hagen and Rhodes2 . Testing was performed in an unoccupied room [13.38 m Reference Schelenz, Hagen and Rhodes2 (144 ft Reference Schelenz, Hagen and Rhodes2 ) room plus 4.1 m Reference Schelenz, Hagen and Rhodes2 (45 ft Reference Schelenz, Hagen and Rhodes2 ) for bathroom] using Formica sheets [7.6 cm × 7.6 cm (3 in × 3 in)] with a template of a Rodac plate drawn on each sheet. The Candida spp were grown in trypticase soy broth (Remel, Lenexa, KS) with and without fetal calf serum (FCS) as an organic material challenge. Inocula of ˜104–105 organisms per Rodac template (10 µL or 15 µL of a 106 inoculum of the test organism) of the 2 test organisms were spread separately on the Formica sheet using a sterile glass spreader. The C. auris isolate (Antibiotic Resistance Bank no. 0385) was obtained from the Centers for Disease Control and Prevention (CDC). Based on tentative minimum inhibitory concentration (MIC) break points, 9 it was resistant to fluconazole and susceptible to anidulafungin, micafungin, caspofungin, and amphotericin B. To determine whether C. auris susceptibility to UV-C was similar to other Candida spp, we also tested C. albicans (ATCC strain no. 60193). The carriers were placed horizontal on the surface or vertical (ie, perpendicular) to the vertical UV-C lamp and at a distance of ˜1.5–2.5 m (˜4–8 ft) (Table 1). The Formica sheets were then placed in 10 locations throughout the patient room (Table 1) and the UV-C device was remotely activated for ˜17–19 minutes for the vegetative bacterial cycle. Following decontamination, Rodac plates (Becton Dickinson, Sparks, MD) containing Dey-Engley Neutralizing Agar (Becton Dickinson) were used to culture each Formica template. The plates were incubated for 48 hours at 37°C and counted. Two separate experiments with 8 total replicates were performed for each organism and test condition (eg, C. auris without 5% FCS). Quantitation of the inoculating suspension was performed in triplicate. Compared to mean carrier control counts, the log10 reduction and the 95% confidence intervals for the log10 reduction of each organism and test condition were calculated.
Mean Log10 Reductions of Surfaces Contaminated With Candida auris and Candida albicans With Variations in Test Methods

Note. D, direct line-of-sight (laser point visible on site); I, indirect-line-of-sight (laser point not visible on site); H, horizontal (flat on surface); V, vertical (perpendicular to UV light); FCS, fetal calf serum.
a A sample of UV efficacy against C. auris with 5% FCS at the overbed table was not available. The bed mattress was covered with a nonpermeable plastic and the chair also had a nonpermeable surface.
Results
The UV-C room decontamination unit tested achieved an overall 2.93-log10 reduction (95% CI, 2.45–3.41) of C. auris with FCS and an overall 2.48-log10 reduction (95% CI, 1.87–3.08) of C. auris without FCS. The overall reductions of C. albicans were 4.44-log10 (95% CI, 3.00–5.88) with FCS and 4.01-log10 (95% CI, 3.20–4.82) without FCS. C. auris had a lower log10 reduction than C. albicans. Direct UV-C had a log10 reduction of 4.57 with FCS and a log10 reduction of 4.45 without FCS. Indirect UV-C had a lower log10 reduction for C. auris of log10 reductions of 2.41 with FCS and 1.96 without FCS, which was statistically significant (Fig. 1). For C. albicans, although direct UV-C had a higher log10 reduction (5.26 with FCS and 5.07 without FCS) compared to indirect exposure (3.96 with FCS and 3.56 without FCS), this difference was not statistically different. The vertical UV had statistically higher log10 reductions than horizontal UV against C. auris and C. albicans with FCS and without FCS. For example, for C. auris with FCS, the log10 reduction for vertical surfaces was 4.92 (95% CI, 3.79–6.04), and for horizontal surfaces it was 2.87 (95% CI, 2.36–3.38).
Inactivation of Candida auris and Candida albicans by UV-C. Note. FCS, fetal calf serum; UV-C, ultraviolet light-C. “Direct” refers to direct line of sight (laser point visible on site); “Indirect” refers to indirect line of sight (laser point not visible on site).

Discussion
Because C. auris can persist on surfaces in healthcare environments, cleaning and disinfecting the patient care environment (daily and discharge or terminal cleaning) with an effective product is critical. Reference Vallabhaneni, Kallen and Tsay1–Reference Piedrahita, Cadnum, Jencson, Shaikh, Ghannoum and Donskey6 The CDC has recommended the use of EPA-registered hospital-grade disinfectants effective against Clostridiodes difficile spores (primarily chlorine-based products). 9 Studies have demonstrated that several commonly used surface disinfectants (ie, a phenolic, 1.4% improved hydrogen peroxide, and alcohol-quaternary ammonium compounds) are as effective against C. auris as chlorine-based products. Reference Rutala, Kanamori, Gergen, Sickbert-Bennett and Weber5 Other infection prevention strategies to minimize the contribution of the environment to C. auris transmission are no-touch room decontamination technologies and monitoring thoroughness of cleaning and disinfecting environmental surfaces using thoroughness indicators (eg, fluorescent markers).
Our study demonstrated a 4.45-log10 reduction at direct line-of-sight (overall 2.48-log10 reduction) for C. auris without FCS and a 4.57-log10 reduction at direct line of sight (overall 2.93-log10 reduction) of C. auris with FCS when the UV-C unit was set on the vegetative bacterial cycle for 17–19 minutes. Cadnum et al Reference Cadnum, Shaikh and Piedrahita7 found ˜4.5-log10 reduction for C. auris and ˜5.5-log10 reduction for C. albicans using an alternate mobile UV-C unit (Optimum UV system) for 20 minutes. DeGroot et al Reference deGroot, Chowdhary, Meis and Voss8 evaluated exposure times and distance and found a third UV-C device (UV-360 room sanitizer) inactivated ˜2.5-log10 reduction of C. auris at 2 m for 10 minutes and ˜5.5-log10 reduction at 2 m for 30 minutes. Increasing the distance to the UV-C source from 2 m to 4 m reduced the efficacy of UV-C to kill C. auris. Reference deGroot, Chowdhary, Meis and Voss8
Our results did not demonstrate an impairment of UV-C efficacy with an organic challenge. One possible explanation is that interference with efficacy does not occur at the concentrations of organic matter used and with the microbes, which are susceptible to UV-C, and the relatively short distances (eg, ˜1.5–2.5 m or ˜4–8 feet). Other investigators have demonstrated with other pathogens (including C. difficile spores) that variation in test conditions can significantly affect the efficacy of UV-C. Reference Cadnum, Tomas and Sankar10 These factors include inoculum dispersal, orientation of carriers, type of organic material, carrier type, distance, exposure time, and direct versus indirect line of sight. Reference deGroot, Chowdhary, Meis and Voss8,Reference Cadnum, Tomas and Sankar10
These studies demonstrated that C. auris can be inactivated on nonporous environmental surfaces as long as factors that affect inactivation are optimized (eg, exposure time and distance). There is no standard level of germicidal efficacy for environmental surfaces, but a log10 reduction of at least 3-log10 (or 99.9% reduction) is likely to be clinically effective against C. auris. Our data demonstrated substantial reductions following UV-C exposure of C. aurus with and without an organic challenge and for both direct and indirect line of sight. The environmental sites (eg, bedside table and overbed table) that were not directly exposed to UV-C had significantly lower microbial reductions. In our investigation, the UV-C device was set on the bacterial cycle (12,000 µWs/cm Reference Schelenz, Hagen and Rhodes2 ) and the device operated for 17–19 minutes. Cadnum et al Reference Cadnum, Shaikh and Piedrahita7 suggested that longer cycles (ie, sporicidal) may be beneficial, as has been recommended for some UV-C devices in C. difficile contaminated rooms. These data and other published UV-C should be used in developing cycle parameters that prevent contaminated surfaces from being a source of acquisition by staff or patients of this globally emerging pathogen.
Acknowledgments
Financial support
This study was supported by UNC Medical Center.
Conflicts of interest
Drs Rutala and Weber are consultants for Professional Disposables Incorporated (PDI).


