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The use of a UV-C disinfection robot in the routine cleaning process: a field study in an Academic hospital

The use of a UV-C disinfection robot in the routine cleaning process: a field study in an... Background: Environmental surface decontamination is a crucial tool to prevent the spread of infections in hos‑ pitals. However, manual cleaning and disinfection may be insufficient to eliminate pathogens from contaminated surfaces. Ultraviolet‑ C (UV‑ C) irradiation deploying autonomous disinfection devices, i.e. robots, are increasingly advertised to complement standard decontamination procedures with concurrent reduction of time and workload. Although the principle of UV‑ C based disinfection is proven, little is known about the operational details of UV‑ C dis‑ infection delivered by robots. To explore the impact of a UV‑ C disinfection robot in the clinical setting, we investigated its usability and the effectiveness as an add‑ on to standard environmental cleaning and disinfection. Additionally, its effect on Candida auris, a yeast pathogen resistant to antifungals and disinfectants, was studied. Methods: After setting the parameters “surface distance” and “exposure time” for each area as given by the manufac‑ turer, the robot moved autonomously and emitted UV‑ C irradiation in the waiting areas of two hospital outpatient clinics after routine cleaning and/or disinfection. To quantify the efficacy of the robotic UV ‑ C disinfection, we obtained cultures from defined sampling sites in these areas at baseline, after manual cleaning/disinfection and after the use of the robot. Four different C. auris strains at two concentrations and either in a lag or in a stationary growth phase were placed in these areas and exposed to UV‑ C disinfection as well. Results: The UV‑ C irradiation significantly reduced the microbial growth on the surfaces after manual cleaning and disinfection. C. auris growth in the lag phase was inhibited by the UV‑ C irradiation but not in the presence of the rim shadows. The effects on C. auris in the stationary phase were differential, but overall C. auris strains were not effectively killed by the standard UV‑ C disinfection cycle. Regarding usability, the robot’s interface was not intuitive, requiring advanced technical knowledge or intensive training prior to its use. Additionally, the robot required interventions by the technical operator during the disinfection process, e.g. stopping due to unforeseen minor dislocation of items during the clinical service or due to moving individuals, making it a delicate high‑tech device but not yet ready for the autonomous use in the clinical routine. Conclusions: Presently, the UV‑ C robot tested in this study is not ready to be integrated in the environmental clean‑ ing and disinfection procedures in our hospital. The single standard disinfection UV‑ C irradiation cycle is not sufficient to inactivate pathogens with augmented environmental resilience, e.g. C. auris, particularly when microbial loads are high. Keywords: Healthcare‑associated infections, Infection control, Ultraviolet ‑ C, UV‑ C robot, Candida auris *Correspondence: elisabeth.presterl@meduniwien.ac.at Department of Infection Control and Hospital Epidemiology, Medical University Vienna, Währinger Gürtel 18‑20, 1090 Vienna, Austria © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 2 of 10 presence of shadows [21]. Organic soils, furniture, dra- Introduction peries or other healthcare equipment etc. are the most Healthcare-associated infections (HAIs) are a major common cause of shadows. Shadows drastically reduce complication of medical treatment and care, necessi- the efficacy of UV-C irradiation. To remove soils, sur - tating a prolonged hospital stay and causing morbid- faces must be cleaned manually before applying UV-C ity associated with increased costs and last but not least irradiation. UV-C efficacy also declines with increasing increased mortality [1]. Up to 7% of the patients in devel- distance of the UV-C source to the surfaces. oped and 10% of the patients in developing countries are Candida auris is an emerging, multidrug-resistant at risk to acquire at least one HAI, most of which may yeast pathogen first described in 2009 as the cause of be prevented through infection prevention and control multiple nosocomial outbreaks worldwide, leading to (IPC) measures [2]. severe infections and high mortality rates [22]. C. auris Pathogens, e.g. methicillin-resistant Staphylococcus poses a particular challenge for IPC in hospitals because aureus (MRSA), vancomycin-resistant Enterococcus it can stay viable on surfaces for prolonged periods and (VRE), Clostridium difficile, Norovirus and fungi are via - is resistant to several commonly used disinfectants [25]. ble on surfaces for prolonged periods [3–6]. As a result, Consequently, the hospital environment is considered environmental contamination leads to an increased risk an important reservoir for transmission [22–25]. Fur- of HAIs [3, 7]. To prevent HAIs and the spread of patho- ther, compared to other pathogens, C. auris is resistant to gens via contaminated surfaces, hospital rooms have to UV-C light and needs extended exposure to UV-C irra- be cleaned and disinfected at regular intervals by trained diation to induce growth inhibition [26, 27]. personnel. For decontamination in hospitals, cleaning UV-C disinfection robots have been increasingly agents and disinfectants approved by technical expert employed in different settings such as hospitals, airports committees must be used. However, manual cleaning and shopping malls as a result of the COVID-19 pan- and disinfection is time and personnel consuming and— demic [28]. However, little information is available on due to lack of time and training—sometimes not suffi - their efficacy and usability in the routine cleaning and cient. Erratic cleaning and disinfection processes, wrong disinfection process in hospital settings. To shed some choice of the appropriate formulation of cleansers or further light on operational aspects, we aimed to test a disinfectants and non-adherence to the required contact new UV-C robot in real life. To evaluate the antimicrobial time of disinfectants may impair the efficacy of standard efficacy of a standard UV-C disinfection cycle, we inves - approaches. Studies have shown that more than 50% of tigated its effect on the microbial burden on clinical sur - surfaces may go untouched by manual cleaning [3, 8, 9]. faces when applied after standard terminal cleaning and Secondly, in times of crisis, the supply of disinfectants disinfection (STC&D) in the waiting areas of two outpa- may be disrupted, as has been demonstrated in the cur- tient clinics. As a surrogate for resilient microorganisms, rent COVID-19 pandemic [10]. four different  C. auris  strains in varying densities (10 Because of the shortcomings of routine environmen- and 10   CFUs/ml) and different growth characteristics tal decontamination as mentioned above, autonomous (lag vs stationary growth phase) were placed within these touchless surface disinfection technologies have evolved. areas and exposed to UV-C irradiation as well. By disrupting the structure of DNA or RNA of microor- ganisms, UV-C irradiation at a wavelength of 254  nm is Materials and methods most effective in killing bacteria, viruses, fungi, and even UV‑C light emitting disinfection device spores (in falling order of effectiveness) [11]. We studied the self-driving Ultra Violet Disinfection Previous studies indicate that disinfection technologies Robot (UVD-R) by Clean Room Solutions because it using UV-C irradiation are an enhancement to standard was the most advanced UV-C irradiation device available cleaning and disinfection, reducing the environmental for autonomous use (Fig. 1). microbial burden and potentially mitigating the risk of This robot moves autonomously in a pre-defined area acquiring a HAI [12–18]. This has been demonstrated for after being programmed for the parameters exposure different pathogens such as MRSA, Clostridium difficile time and distance of surfaces. It consists of eight lamps and VRE [13, 18] and in different clinical settings such as that are located on top of a platform. During a disinfec- ambulances [19], inpatient rooms [16, 20] and operating tion cycle, they emit UV-C irradiation at a wavelength of theaters [15]. 254 nm, enabling a 360 degree coverage. During the dis- The efficacy of UV-C irradiation to inactivate microor - infection process, the UV-C light emitting robot moves ganisms depends on a number of factors including vary- at 10 cm per second, providing a dose of 2.7 mJ/cm  per ing resistance levels of different microorganisms to UV-C second for directly exposed surfaces in 1 m distance and light, the initial inoculum and the UV-C dose received, achieving a coverage of areas at a distance of several which is a result of distance, duration of exposure and the A strid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 3 of 10 cleaned once a day while chairs and tables are disinfected once a day using either alcohol-based products or prod- ucts based on active oxygen (Descogen Liquid). Prior to the start of the study, a member of the UVD Robot installation team pre-programmed area maps with the exact position of furniture and other items to enable autonomous disinfection cycles. For the pre-pro- gramming, the team inspected the two outpatient clinics to map the robot’s route and identify critical areas that required longer UV-C light exposure. The robot was pre- programmed to stop at various predefined positions for 3  min to achieve optimal UV-C exposure of all relevant surfaces (Figs. 2, 3). The device was used after the room had been manually cleaned and disinfected according to SOP. The proce - dure was then initiated remotely once all doors had been Fig. 1 UVD Robot (Clean Room Solutions) meters (according to manufacturer’s specifications). However, it is worth bearing in mind that the UV-C light intensity over distance is governed by the inverse square law, resulting in significantly smaller doses for areas fur - ther away from the device. To enable autonomous mov- ing, the robot must be pre-programmed using a detailed map of the position of furniture and other obstacles in the area to be treated with UV-C irradiation. Once every parameter is set, furniture and all other objects must Fig. 2 Area map pre‑programmed into the UV ‑ C robot in the ENT remain in exactly the same place to enable an autono- outpatient clinic. The blue dots indicate where the robot had to stop mous functioning. Due to the high-intensity UV-C irradi- for 3 min during the disinfection cycle. The red color indicates which ation, the UV-C robot may only be used in rooms devoid area was covered by the mapping procedure and exposed to UV‑ C of people. Unintentional exposure leads to cutaneous light erythema and photokeratitis. For safety, this UV-C robot automatically shuts off when its motion sensor detects any moving individuals during the disinfection process. Setting Between July 23rd and August 2nd 2020, the study was performed in the waiting areas of two outpatient clin- ics (ear, nose and throat medicine and oncology waiting areas with a size of 137  m each) of Vienna General Hos- pital (VGH), a 1728 bed tertiary hospital in the capital of Austria. During the study period, 347 patients were treated in the ENT (23/07–26/07) and 400 patients in the oncology outpatient department (29/07–02/08). Fig. 3 Area map pre‑programmed into the UV ‑ C robot in the In one of the outpatient areas, manual cleaning/disin- oncology outpatient clinic. The blue dots indicate where the robot fection was carried out by in-house cleaning personnel had to stop for 3 min during the disinfection cycle. The red color while the other outpatient clinic was served by a clean- indicates which area was covered by the mapping procedure and exposed to UV‑ C light. The violet color indicates “light detection and ing service providing company. Cleaning and disinfec- ranging” (Lidar), which is a way for the robot to see an obstacle and tion followed the standard operating procedures (SOP) of avoid that area VGH: Floors in the outpatient waiting areas are manually Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 4 of 10 closed. Each disinfection cycle was completed within 20–25 min per outpatient setting. Sampling procedure To evaluate the robot’s effect on residual contamina - tion, samples were collected from different surface sites before and after routine cleaning and/or disinfection, and after the use of the UV-C robot. Surface sites selected for sampling included high-touch surfaces and remote sites supposedly to be out of reach for easy cleaning and those that appeared unlikely to achieve full exposure to UV-C irradiation. In the ENT waiting area, six sites were sampled (wall, armrests of two different chairs, back of a chair, wooden play element for children, window countertop) (see Addi tional file 1: Table S1). In the oncology waiting area, sampling was performed from eight different sites (patient registration area, table surface next to patient registration, armrests of two dif- ferent chairs, window countertop, push button of a vend- ing machine, leaflet dispenser) (see Additional file  1: Table S2). To monitor the amount of exposure to UV-C irradia- tion, disposable indicators were placed on all surfaces used for sampling before initiating the UV-C cycle. The indicators changed color depending on the achieved dose, corresponding to doses ranging from 25  mJ/cm in shadowed areas to 100  mJ/cm at the most highly exposed sites (Fig. 4). The achieved UV-C doses corresponding to each sam - pling site are presented in the supplemental material (see Additional file 1: Tables S1–S2). Microbiological methods Determination of the microbial burden on hospital surfaces We collected environmental contact cultures from each sampling site using Tryptic Soy Agar (TSA) plates with a diameter of 5.5  cm (VWR International, Vienna, Aus- tria). Samples were collected on 9  days by the same lab Fig. 4 Reference chart (UV‑ C dose received according to indicator’s change of color); Intellego Technologies technician following a predefined standardized sampling scheme: During the study period, sampling was performed three times per study day: Surfaces were subdivided into three categories accord- ing to their level of contamination used routinely for (a) before routine cleaning and/or disinfection, environmental samples at our institution: (b) after routine cleaning and/or disinfection, and (c) after the use of the UV-C robot. (1) surfaces with a low microbial burden, defined as 0–3 CFUs/24  cm After sampling, TSA plates were incubated at 37  °C (2) surfaces with an average microbial burden, defined for 48  h. Following incubation, the number of colony as 4–50 CFUs/24  cm forming units (CFUs) on each plate was counted. Sub- (3) surfaces with a high microbial burden, defined sequently, the colonies were identified using the MALDI- as > 50 CFUs/24  cm . TOF mass spectrometry method (Bruker, USA). A strid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 5 of 10 Preparation of Candida auris strains performed at a two-sided significance level of 0.05, using We investigated whether the type of C. auris strain, seed- SPSS (Version 26.0, IBM). ing density and incubation prior to UV-C light exposure In an exploratory data analysis, the plates of UV-C affected UV-C efficacy. exposed C. auris strains with a concentration of 10 To study potential differences in sensitivity to UV-C CFUs/ml were visually compared to unexposed controls. irradiation, four C. auris strains were evaluated: C. auris Results of C. auris with an initial concentration of 10 NCPF 8971, C. auris NCPF 8977, C. auris NCPF 8984 CFUs/ml were quantified as the number of CFUs, com - and C. auris DSM 21092. paring exposed and unexposed plates. Plates containing Sabouraud Dextrose Agar (SDA) (Becton Dickinson, Franklin Lakes, USA) were inoculated Results with 100  µl of C. auris suspension at two different con - Eec ff ts on the environmental microbial burden 3 6 centrations, 10 CFUs/ml and 10 CFUs/ml respectively. During the study period, we collected 192 samples (72 Each strain of C. auris suspension containing 10 in the ENT and 120 in the oncology outpatient areas, CFUs/ml was spread on three SDA plates and incubated respectively) from 14 sites (64 samples prior to any clean- for 24  h at 30  °C. For the field experiment, rimless TSA ing and disinfection, 64 after manual cleaning and dis- plates were pressed on these SDA plates, mimicking infection and 64 after the use of the UV-C robot). Prior surface contamination by hands and fomites as demon- to manual cleaning, the surfaces most heavily contami- strated by Adams et al. [29]. Overall, 12 TSA plates were nated were the armrests of chairs, followed by the win- used per study day. dow countertops. The least contaminated sites were Additionally, each strain of C. auris suspension con- the walls, the leaflet dispenser and the backs of patient taining 10 CFUs/ml was spread on one SDA plate with- chairs. The leaflet dispenser, however, was empty during out further incubation, yielding four plates with C. auris the study period according to an in-house IPC order to in a lag phase per study day. Then, C. auris exposed avoid potential cross-transmission via contaminated leaf- TSA plates (10 CFUs/ml, incubated overnight) as well lets during the COVID-19 pandemic. In general, contam- as inoculated SDA plates (10 CFUs/ml without further ination levels prior to any cleaning and disinfection were incubation) were placed on two tables in the waiting area higher in the oncology outpatient area than in the ENT of the oncology outpatient clinic during the standard outpatient area. disinfection cycle. Indicators were placed alongside that In Table  1, the level of contamination according to measured the UV-C dose received. This experiment was the time of sampling is summarized for each outpatient performed in triplicate. waiting area. UV-C indicators showed that some of the Following UV-C exposure, all plates were incubated at sites received a suboptimal UV-C dose. Nonetheless, the 30 °C for 7 days. Then, C. auris growth was compared to additional use of UV-C irradiation achieved a further unexposed controls. reduction of CFUs compared to standard cleaning and/ or disinfection, resulting in decontamination of 96.9% Statistical analysis (62/64) of the surfaces compared to decontamination of Standard descriptive analysis was done to summarize 50.0% (32/64) of the surfaces after manual cleaning and the microbiological findings. Differences between the disinfection alone. number of CFUs after standard terminal cleaning and With regard to the microbial burden, the additional use disinfection compared to the combined use of STC&D of the UV-C robot significantly decreased the median and UV-C irradiation were analyzed using the Wilcoxon number of CFUs in both outpatient areas compared to matched-pairs signed rank test. Statistical analysis was manual cleaning and disinfection alone (p = 0.008 and Table 1 Proportion of contact cultures with low, acceptable and high microbial burden before routine cleaning and/or disinfection, after routine cleaning and/or disinfection and after the use of the UV‑ C robot ENT outpatient area Oncology outpatient area Low Average High Low Average High Before C&D 45.8% (11/24) 37.5% (9/24) 16.7% (4/24) 22.5% (9/40) 60.0% (24/40) 17.5% (7/40) After C&D 79.2% (19/24) 20.8% (5/24) 0% (0/24) 32.5% (13/40) 62.5% (25/40) 5.0% (2/40) After C&D + UV‑ C 100% (24/24) 0% (0/24) 0% (0/24) 95.0% (38/40) 5.0% (2/40) 0% (0/40) 2 2 2 C&D cleaning and disinfection, UV-C ultraviolet C; low = 0–3 CFUs/24  cm , average = 4–50 CFUs/24  cm , high > 50 CFUs/24 cm Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 6 of 10 p < 0.001, for the ENT and for the oncology outpatient areas, respectively) (Table 2). Qualitative description of the environmental microbiome Most bacterial isolates were classified as physiological skin flora (222/297; 74.7%). Next, 13.1% of bacteria were classified as environmental microorganisms (39/297), 6.4% of bacteria were classified as oropharyngeal flora (19/297) and 5.7% of bacteria as potential pathogens (17/297). Typical pathogens were Staphylococcus saprophyticus (n = 5) and Staphylococcus lugdunensis (n = 1), Acinte- tobacter baumanii (n = 2), Aerococcus viridans (n = 1), Streptococcus pneumonia (n = 1), Staphylococcus aureus (n = 1) and Enterococcus casseliflavus (n = 1). The arm - rests of chairs were the sites most frequently contami- nated with pathogens. All identified microorganisms in both waiting areas, the median CFUs and the achieved UV-C doses, reported separately for each sampling site, Fig. 5 C. auris (10 CFUs/ml) on Sabouraud plates without (above) time of sampling and outpatient waiting area, are given and with (below) exposure to UV‑ C irradiation following incubation in the supplemental material (Additional file  1: Tables S1–S4). consistently showed growth greater than 50 CFUs on Eec ff ts on Candida auris each TSA contact plate after UV-C exposure. In terms UV-C irradiation emitted by the robot reduced the of the UV-C dose received, the indicators indicated high growth of all four C. auris strains spread at a concen- exposure (75–100 mJ/cm ) for all C. auris plates (Table 3, tration of 10 CFUs/ml on SDA plates, mimicking the Fig. 6). microbial lag phase. However, as shown in Fig. 5, growth of C. auris was observed on one fourth of the plate. Use of a UV‑C robot for the routine cleaning and/ According to the indicators placed alongside, the meas- or disinfection process ured UV-C dose was 100  mJ/cm (indicating maximum The UV-C robot required many attempts until it could exposure) except for the area right next to the rim of the carry out the UV-C disinfection process indepen- plate, demonstrating the shadow effect of the rim. dently. Interventions by the operator were necessary The effect of the UV-C robot on stationary C. auris due to initial programming imprecisions, furniture cells at an initial concentration of 10  CFUs/ml was vari- that had accidentally been moved during routine clini- able and depended on the C. auris strain tested (Table 3). cal operations, detection of movement during an The C. auris NCPF 8984 strain was the most sensitive ongoing disinfection cycle or loss of internet connec- of the tested strains. It also showed the most consistent tion. Although the area was cordoned off during the results regarding growth reduction after UV-C expo- disinfection cycles and appropriate warning signs were sure compared to control plates. C. auris NCPF 8971 posted on the access doors, we found it difficult to Table 2 Reductions in Colony‑Forming Units after routine cleaning and/or disinfection compared to baseline and after routine cleaning and/or disinfection + UV‑ C irradiation compared to routine cleaning and/or disinfection alone ENT outpatient area Oncology outpatient area No. of Median CFU (IQR) Min Max p value No. of Median CFU (IQR) Min Max p value samples samples Before C&D 24 8.5 (8.5–28.3) 0 207 0.003 40 22.0 (4.3–36.0) 0 200 After C&D 24 0 (0–2.8) 0 18 40 6.5 (2.3–20.5) 0 101 <0.001 After C&D 24 0 (0–2.8) 0 18 0.008 40 6.5 (2.3–20.5) 0 101 After C&D + UV‑ C 24 0 (0–0) 0 1 40 0 (0–0) 0 5 <0.001 No. number, CFU Colony Forming Unit, IQR interquartile range, Min minimum, Max maximum, C&D cleaning and disinfection, UV-C ultraviolet C A strid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 7 of 10 Table 3 Colony counts per TSA plate containing C. auris in a Discussion stationary phase (10 CFUs/ml) with and without UV‑ C exposure The contaminated hospital environment is a reservoir for various pathogens and may thus serve as a source of C. auris C. auris C. auris C. auris NCPF NCPF NCPF DSM HAIs [30]. Conventional manual cleaning and disinfec- 8971 8977 8984 21092 tion processes are not always   sufficient to eliminate the Control (without > 100 > 100 > 100 > 100 risk posed by contaminated surfaces [3, 8, 9]. Human UV‑ C exposure) factors are likely to be a major contributor. Further- Day1 (after UV‑ C) more, during the COVID-19 pandemic, effective stand - 1 > 50 35 1 > 50 ard disinfectants were unavailable in times of crisis [10], 2 > 50 > 50 28 35 indicating the need of new disinfectants or disinfection methods. Most recently, autonomously moving UV-C 3 > 50 > 50 1 > 50 disinfection devices—UV-C robots—have been devel- Day2 (after UV‑ C) oped to overcome these shortcomings. 1 > 50 > 100 > 50 20 The present study shows that UV-C irradiation emit - 2 > 50 > 100 11 > 50 ted by the robot significantly decreased the residual sur - 3 > 100 > 100 10 > 50 face contamination in the waiting areas of two outpatient Day3 (after UV‑ C) clinics of a tertiary hospital compared to manual clean- 1 > 50 > 50 11 > 50 ing and disinfection alone. This is in accordance with 2 > 50 > 50 0 > 50 other studies that have found a significant decrease of the 3 > 50 > 50 > 50 30 pathogen bioburden in clinical settings by using a robotic Corresponding UV-C doses received during each disinfection cycle ranged from 75 to 100 mJ/cm UV-C irradiation device [12, 13, 15, 31]. Anderson et  al. found that the application of UV-C light significantly reduced the presence of Vancomycin-resistant entero- ensure the total absence of health personnel returning cocci (VRE) and Clostridium difficile in patient rooms to their nightshift rooms nearby or other individuals previously occupied by colonized patients compared to who moved in and out the closed area. baseline (without prior manual cleaning and disinfection) In terms of its user-friendliness and simplicity of [20]. Similarly, Yang et  al. observed a significant reduc - operation, the device required—in addition to the tion of the number of bacteria colonies sampled from dif- pre-programming of the area’s maps—further preced- ferent surfaces after UV-C exposure in uncleaned rooms ing steps to start the disinfection process. The user previously occupied by VRE and MRSA carriers [32]. In had to select several items in two different apps on the the present study—despite the fact that not all surfaces device’s control panel, which was not self-explanatory. achieved full UV-C light exposure—almost all microor- ganisms still present after manual cleaning and disinfec- tion were eliminated. However the microbial burden on surfaces was low to average on almost all surfaces after Fig. 6 Growth of C. auris strains in a stationary phase on TSA contact plates after UV‑ C exposure Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 8 of 10 manual cleaning and/or disinfection alone. Especially in assistance to operate the robot. Future technological the ENT outpatient waiting area, manual cleaning and advances  are  supposed to overcome these failings. In disinfection had been carried out meticulously, resulting addition to a somewhat complicated programming of in the recovery of only few CFUs. Insufficient UV-C light the parameter settings, the robot tested was mostly not exposure might have yielded less effective results in other autonomous and not able to carry out the room disinfec- settings, e.g. with higher surface contamination levels. tion independently. Apart from technical reasons, this Using C. auris as a surrogate for microorganisms resil- dysfunction was also due to the fact that furniture and ient in the environment, the UV-C disinfection robot other objects had been  slightly moved between the ini- tested showed varying effectiveness: For C. auris that had tial programming and the robot’s use. Moreover, despite been incubated for 24  h before exposure to UV-C irra- sealing the areas off during the UV-C disinfection cycles, diation, growth inhibition was not effectively achieved people moved in and out. Yet, this is normal in the hos- compared to C. auris without prior incubation (for fully pital reality. Advances in IT, particularly using artificial exposed areas). However, this may be due to our dif- intelligence together with high-tech cameras may be the ferent sample preparations, mimicking C. auris in a lag clue for solving these problems. Additionally, further versus a stationary growth phase. Furthermore, the for- technical developments such as making the UV-C light mation of shadows from the rim of SDA plates drastically source more flexible and the robot itself smaller will be decreased the effectiveness of UV-C light. De Groot et al. necessary in addition to adjustments in the clinical envi- investigated the effect of different distances (two or four ronment to minimize the formation of shadows, thus meters) from the UV-C emitting device as well as differ - enabling the proper use of this novel technology. ent cycle times (5, 10, 20 or 30 min) on C. auris in vitro, The decision to use a UV-C disinfection robotic device demonstrating strain-dependent effectiveness. Longer in clinical settings must be made on the basis of the UV-C exposure and less distance improved the effects intended application area, the practicability of use and of UV-C irradiation [21]. The present study evaluated the additional expected benefit. At the present stage of the effects of UV-C irradiation on C. auris delivered by UV-C robot technology, these robots will be preferably a robot in a clinical setting. These results confirm that used in areas with stationary furniture that can easily longer UV-C exposure is necessary to eradicate C. auris, be sealed off to avoid  people walking in and out during especially when inoculums are high and pathogens have an ongoing disinfection cycle. Practicability means that already had time to mature. Thus, it is pivotal to vali - the UV-C robot will be operated by trained cleaning staff date the effectiveness of UV-C robotic devices separately rather than by an engineer or a technician. An additional for each clinical setting. To achieve this, the robot’s set- expected benefit, however, might be achieved in areas tings (distance and duration of exposure) must be care- with vulnerable patients or in over-busy areas with highly fully calibrated and adapted further until microbiological contaminated surfaces including the risk of multidrug- outcomes are satisfactory. This requires the expertise of resistant microorganisms, e.g. emergency departments. a clinical microbiologist and IPC specialist. UV-C sensi- There are some limitations to this study. First, show - tive, color-changing indicators measuring the amount of ing a reduction in the microbial burden on surfaces is a UV-C irradiation received must be used as quality con- surrogate outcome. The study design did not allow for an trols. Particularly for surfaces or objects that create shad- evaluation of the effect of UV-C irradiation in addition to ows and cannot be reached by UV-C irradiation, manual manual cleaning and disinfection on HAI rates compared cleaning and disinfection are still needed. In the future, to manual cleaning and disinfection alone. Next, the clas- design of hospital areas will have to avoid structures cre- sification of the sampling sites into surfaces with a low, ating shadows if UV-C disinfection is applied. Neverthe- average and high microbial burden was made accord- less, for surfaces beyond the reach of the cleaners, UV-C ing to our in-house standard, which is used to audit the robots may be useful. Then, to achieve effective UV-C cleaning efficacy. It refers to the colony count but is not disinfection the UV-C source must be able to move into directly associated with patients’ outcomes. Further, the three dimensions (tilt, move up and down). cleaning personnel was not blinded to the intervention, The usability of the UV-C robot in the clinical set - which might have affected their behavior, resulting in ting was not as satisfactory as expected from a robotic more thorough cleaning and not reflecting the quality of device. This study aimed to evaluate the UV-C robot in cleaning in daily practice. Therefore, our results might action, particularly its usability when integrated into underestimate the benefit provided by adding a UV-C the standard cleaning and disinfection process. UV-C component. Next, to determine the effects of the UV-C robots are usually advertised as being simple to use robotic device on C. auris, artificially inoculated plates with no additional decontamination needed. However, were used as a surrogate for surface-bound contamina- in our own experience, we repeatedly needed technical tion. This might not accurately reflect growth patterns A strid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 9 of 10 the manuscript. DM, PE, EJ and NM revised the manuscript. All authors read of C. auris on real-world surfaces. Moreover, densities and approved the final manuscript. occurring on contaminated hospital surfaces may not be as high, resulting in an underestimation of the ability of Funding This research did not receive any specific grant from funding agencies in the UV-C light to kill C. auris. public, commercial, or not‑for ‑profit sectors. Availability of data and materials The datasets used and/or analyzed during the current study are available from Conclusion the corresponding author on reasonable request. The UV-C disinfection model robot tested in our study was not yet ready for everyday use in hospitals due to Declarations several technical shortcomings and difficulty of use as well as likely significant additional expense. We also Ethics approval and consent to participate Not applicable. observed persistence of C. auris in a stationary phase, indicating that a standard disinfection cycle might not Consent for publication suffice to inactivate more UV-C resistant pathogens, Not applicable. especially when inoculums are high. While UV-C tech- Competing interests nologies improve surface decontamination results, they The authors certify that they have no affiliations with or involvement in any do not simplify current processes and can presently only organization or entity with any financial interest or non‑financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in serve as add-on components to manual cleaning and the subject matter or materials discussed in this manuscript. disinfection carried out by trained and audited cleaning staff. However, there is huge potential in this technology Received: 2 December 2020 Accepted: 26 February 2021 once it is further developed. Abbreviations References C. auris: Candida auris; C&D: Cleaning and disinfection; CFU: Colony‑Forming 1. Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, Unit; ENT: Ear, nose and throat; IPC: Infection prevention and control; HAI: et al. Multistate point‑prevalence survey of health care ‑associated infec‑ Healthcare‑associated infection; MRSA: Methicillin‑resistant Staphylococcus tions. N Engl J Med. 2014;370(13):1198–208. aureus; SDA: Sabouraud Dextrose Agar; SOP: Standard operating procedure; 2. WHO. Report on the endemic burden of healthcare‑associated infection STC&D: Standard terminal room cleaning and disinfection; TSA: Tryptic Soy worldwide. 2011. https:// www. who. int/ infec tion‑ preve ntion/ publi catio Agar; UV‑ C: Ultraviolet‑ C; VRE: Vancomycin‑resistant Enterococcus. ns/ burden_ hcai/ en/. 05 Nov 2020. 3. Dancer SJ. Importance of the environment in meticillin‑resistant Staphy - lococcus aureus acquisition: the case for hospital cleaning. Lancet Infect Supplementary Information Dis. 2008;8(2):101–13. The online version contains supplementary material available at https:// doi. 4. Guerrero DM, Nerandzic MM, Jury LA, Jinno S, Chang S, Donskey CJ. org/ 10. 1186/ s13756‑ 021‑ 00945‑4. Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms. Am J Infect Control. 2012;40(6):556–8. Additional file 1. The use of a UV ‑ C disinfection robot in the routine 5. Hayden MK, Blom DW, Lyle EA, Moore CG, Weinstein RA. Risk of hand clearning process: a field study in an Academic Hospital. Table S1. or glove contamination after contact with patients colonized with Reductions in Colony‑Forming Units in the ENT outpatient area after vancomycin‑resistant enterococcus or the colonized patients’ environ‑ routine cleaning and/or disinfection, and after the use of the UV‑ C robot. ment. Infect Control Hosp Epidemiol. 2008;29(2):149–54. Table S2. Reductions in Colony‑Forming Units in the oncology outpatient 6. Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens area after routine cleaning and/or disinfection, and after the use of the persist on inanimate surfaces? A systematic review. BMC Infect Dis. UV‑ C robot. Table S3. ENT outpatient area: Environmental microbiome 2006;6:130. identified during the study period. Table S4. Oncology outpatient area: 7. Weber DJ, Anderson D, Rutala WA. The role of the surface environment in Environmental microbiome identified during the study period. healthcare‑associated infections. Curr Opin Infect Dis. 2013;26(4):338–44. 8. Carling PC. Evaluating the thoroughness of environmental cleaning in hospitals. J Hosp Infect. 2008;68(3):273–4. Acknowledgements 9. Carling PC, Parry MM, Rupp ME, Po JL, Dick B, Von Beheren S. Improv‑ We would like to thank Clean Room Solutions for providing their Ultra Violet ing cleaning of the environment surrounding patients in 36 acute care Disinfection Robot (UVD‑R) as well as technical support during the study hospitals. Infect Control Hosp Epidemiol. 2008;29(11):1035–41. period. Clean Room Solutions did not provide any funding for the study and 10. Kampf G, Scheithauer S, Lemmen S, Saliou P, Suchomel M. COVID‑ did not contribute to the study design or writing of the manuscript. We would 19‑associated shortage of alcohol‑based hand rubs, face masks, medical also like to thank Thi Lan Vi Tran for assisting with the statistical analysis as gloves and gowns—proposal for a risk‑adapted approach to ensure well as the ESCMID Study Group for Nosocomial Infections (ESGNI) for their patient and healthcare worker safety. J Hosp Infect. 2020;105(3):424–7. valuable input. 11. Misovic M, Milenkovic D, Martinovic T, Ciric D, Bumbasirevic V, Kravic‑Ste ‑ vovic T. Short‑term exposure to UV ‑A, UV ‑B, and UV ‑ C irradiation induces Authors’ contributions alteration in cytoskeleton and autophagy in human keratinocytes. DM and PE designed the study. ZB prepared the Candida auris samples and Ultrastruct Pathol. 2013;37(4):241–8. summarized the results regarding Candida auris growth inhibition as a result of 12. Liscynesky C, Hines LP, Smyer J, Hanrahan M, Orellana RC, Mangino JE. UV‑ C exposure. NM and EJ assisted in the execution of the study. FA executed The effect of ultraviolet light on Clostridium difficile spore recovery the study, analyzed and interpreted data regarding the effect of UV ‑ C irradia‑ versus bleach alone. Infect Control Hosp Epidemiol. 2017;38(9):1116–7. tion on environmental contamination and Candida auris growth and wrote Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 10 of 10 13. Wong T, Woznow T, Petrie M, Murzello E, Muniak A, Kadora A, et al. 23. Kordalewska M, Perlin DS. Identification of drug resistant Candida auris. Postdischarge decontamination of MRSA, VRE, and Clostridium difficile Front Microbiol. 2019;10:1918. isolation rooms using 2 commercially available automated ultraviolet‑ C‑ 24. Calvo B, Melo AS, Perozo‑Mena A, Hernandez M, Francisco EC, Hagen F, emitting devices. Am J Infect Control. 2016;44(4):416–20. et al. First report of Candida auris in America: clinical and microbiological 14. Hosein I, Madeloso R, Nagaratnam W, Villamaria F, Stock E, Jinadatha aspects of 18 episodes of candidemia. J Infect. 2016;73(4):369–74. C. Evaluation of a pulsed xenon ultraviolet light device for isolation 25. Schelenz S, Hagen F, Rhodes JL, Abdolrasouli A, Chowdhary A, Hall A, room disinfection in a United Kingdom hospital. Am J Infect Control. et al. First hospital outbreak of the globally emerging Candida auris in a 2016;44(9):e157–61. European hospital. Antimicrob Resist Infect Control. 2016;5:35. 15. El Haddad L, Ghantoji SS, Stibich M, Fleming JB, Segal C, Ware KM, 26. Cadnum JL, Shaikh AA, Piedrahita CT, Jencson AL, Larkin EL, Ghannoum et al. Evaluation of a pulsed xenon ultraviolet disinfection system to MA, et al. Relative resistance of the emerging fungal pathogen Candida decrease bacterial contamination in operating rooms. BMC Infect Dis. auris and other Candida species to killing by ultraviolet light. Infect Con‑ 2017;17(1):672. trol Hosp Epidemiol. 2018;39(1):94–6. 16. Anderson DJ, Chen LF, Weber DJ, Moehring RW, Lewis SS, Triplett PF, 27. Ponnachan P, Vinod V, Pullanhi U, Varma P, Singh S, Biswas R, et al. Antifun‑ et al. Enhanced terminal room disinfection and acquisition and infection gal activity of octenidine dihydrochloride and ultraviolet‑ C light against caused by multidrug‑resistant organisms and Clostridium difficile (the multidrug‑resistant Candida auris. J Hosp Infect. 2019;102(1):120–4. Benefits of Enhanced Terminal Room Disinfection study): a cluster ‑ 28. O’Meara S. Mechanical medics to the rescue. Nature. 2020;582:49. randomised, multicentre, crossover study. Lancet (London, England). 29. Adams E, Quinn M, Tsay S, Poirot E, Chaturvedi S, Southwick K, et al. Can- 2017;389(10071):805–14. dida auris in healthcare facilities, New York, USA, 2013–2017. Emerg Infect 17. Health Quality Ontario. Portable ultraviolet light surface‑ disinfecting Dis J. 2018;24(10):1816. devices for prevention of hospital‑acquired infections: a health technol‑ 30. Suleyman G, Alangaden G, Bardossy AC. The role of environmental con‑ ogy assessment. Ont Health Technol Assess Ser. 2018;18(1):1–73. tamination in the transmission of nosocomial pathogens and healthcare‑ 18. Nerandzic MM, Cadnum JL, Pultz MJ, Donskey CJ. Evaluation of an auto‑ associated infections. Curr Infect Dis Rep. 2018;20(6):12. mated ultraviolet radiation device for decontamination of Clostridium 31. Doll M, Morgan DJ, Anderson D, Bearman G. Touchless technologies for difficile and other healthcare ‑associated pathogens in hospital rooms. decontamination in the hospital: a review of hydrogen peroxide and UV BMC Infect Dis. 2010;10:197. devices. Curr Infect Dis Rep. 2015;17(9):498. 19. Lindsley WG, McClelland TL, Neu DT, Martin SB Jr, Mead KR, Thewlis RE, 32. Yang J‑H, Wu U‑I, Tai H‑M, Sheng W ‑H. Eec ff tiveness of an ultraviolet ‑ C et al. Ambulance disinfection using Ultraviolet Germicidal Irradiation disinfection system for reduction of healthcare‑associated pathogens. J (UVGI): effects of fixture location and surface reflectivity. J Occup Environ Microbiol Immunol Infect. 2019;52(3):487–93. Hyg. 2018;15(1):1–12. 20. Anderson DJ, Gergen MF, Smathers E, Sexton DJ, Chen LF, Weber DJ, et al. Publisher’s Note Decontamination of targeted pathogens from patient rooms using an Springer Nature remains neutral with regard to jurisdictional claims in pub‑ automated ultraviolet‑ C‑ emitting device. Infect Control Hosp Epidemiol. lished maps and institutional affiliations. 2013;34(5):466–71. 21. de Groot T, Chowdhary A, Meis JF, Voss A. Killing of Candida auris by UV‑ C: importance of exposure time and distance. Mycoses. 2019;62(5):408–12. 22. Alfouzan W, Dhar R, Albarrag A, Al‑Abdely H. The emerging pathogen Candida auris: a focus on the Middle‑Eastern countries. J Infect Public Health. 2019;12(4):451–9. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance & Infection Control Springer Journals

The use of a UV-C disinfection robot in the routine cleaning process: a field study in an Academic hospital

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2047-2994
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10.1186/s13756-021-00945-4
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Abstract

Background: Environmental surface decontamination is a crucial tool to prevent the spread of infections in hos‑ pitals. However, manual cleaning and disinfection may be insufficient to eliminate pathogens from contaminated surfaces. Ultraviolet‑ C (UV‑ C) irradiation deploying autonomous disinfection devices, i.e. robots, are increasingly advertised to complement standard decontamination procedures with concurrent reduction of time and workload. Although the principle of UV‑ C based disinfection is proven, little is known about the operational details of UV‑ C dis‑ infection delivered by robots. To explore the impact of a UV‑ C disinfection robot in the clinical setting, we investigated its usability and the effectiveness as an add‑ on to standard environmental cleaning and disinfection. Additionally, its effect on Candida auris, a yeast pathogen resistant to antifungals and disinfectants, was studied. Methods: After setting the parameters “surface distance” and “exposure time” for each area as given by the manufac‑ turer, the robot moved autonomously and emitted UV‑ C irradiation in the waiting areas of two hospital outpatient clinics after routine cleaning and/or disinfection. To quantify the efficacy of the robotic UV ‑ C disinfection, we obtained cultures from defined sampling sites in these areas at baseline, after manual cleaning/disinfection and after the use of the robot. Four different C. auris strains at two concentrations and either in a lag or in a stationary growth phase were placed in these areas and exposed to UV‑ C disinfection as well. Results: The UV‑ C irradiation significantly reduced the microbial growth on the surfaces after manual cleaning and disinfection. C. auris growth in the lag phase was inhibited by the UV‑ C irradiation but not in the presence of the rim shadows. The effects on C. auris in the stationary phase were differential, but overall C. auris strains were not effectively killed by the standard UV‑ C disinfection cycle. Regarding usability, the robot’s interface was not intuitive, requiring advanced technical knowledge or intensive training prior to its use. Additionally, the robot required interventions by the technical operator during the disinfection process, e.g. stopping due to unforeseen minor dislocation of items during the clinical service or due to moving individuals, making it a delicate high‑tech device but not yet ready for the autonomous use in the clinical routine. Conclusions: Presently, the UV‑ C robot tested in this study is not ready to be integrated in the environmental clean‑ ing and disinfection procedures in our hospital. The single standard disinfection UV‑ C irradiation cycle is not sufficient to inactivate pathogens with augmented environmental resilience, e.g. C. auris, particularly when microbial loads are high. Keywords: Healthcare‑associated infections, Infection control, Ultraviolet ‑ C, UV‑ C robot, Candida auris *Correspondence: elisabeth.presterl@meduniwien.ac.at Department of Infection Control and Hospital Epidemiology, Medical University Vienna, Währinger Gürtel 18‑20, 1090 Vienna, Austria © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 2 of 10 presence of shadows [21]. Organic soils, furniture, dra- Introduction peries or other healthcare equipment etc. are the most Healthcare-associated infections (HAIs) are a major common cause of shadows. Shadows drastically reduce complication of medical treatment and care, necessi- the efficacy of UV-C irradiation. To remove soils, sur - tating a prolonged hospital stay and causing morbid- faces must be cleaned manually before applying UV-C ity associated with increased costs and last but not least irradiation. UV-C efficacy also declines with increasing increased mortality [1]. Up to 7% of the patients in devel- distance of the UV-C source to the surfaces. oped and 10% of the patients in developing countries are Candida auris is an emerging, multidrug-resistant at risk to acquire at least one HAI, most of which may yeast pathogen first described in 2009 as the cause of be prevented through infection prevention and control multiple nosocomial outbreaks worldwide, leading to (IPC) measures [2]. severe infections and high mortality rates [22]. C. auris Pathogens, e.g. methicillin-resistant Staphylococcus poses a particular challenge for IPC in hospitals because aureus (MRSA), vancomycin-resistant Enterococcus it can stay viable on surfaces for prolonged periods and (VRE), Clostridium difficile, Norovirus and fungi are via - is resistant to several commonly used disinfectants [25]. ble on surfaces for prolonged periods [3–6]. As a result, Consequently, the hospital environment is considered environmental contamination leads to an increased risk an important reservoir for transmission [22–25]. Fur- of HAIs [3, 7]. To prevent HAIs and the spread of patho- ther, compared to other pathogens, C. auris is resistant to gens via contaminated surfaces, hospital rooms have to UV-C light and needs extended exposure to UV-C irra- be cleaned and disinfected at regular intervals by trained diation to induce growth inhibition [26, 27]. personnel. For decontamination in hospitals, cleaning UV-C disinfection robots have been increasingly agents and disinfectants approved by technical expert employed in different settings such as hospitals, airports committees must be used. However, manual cleaning and shopping malls as a result of the COVID-19 pan- and disinfection is time and personnel consuming and— demic [28]. However, little information is available on due to lack of time and training—sometimes not suffi - their efficacy and usability in the routine cleaning and cient. Erratic cleaning and disinfection processes, wrong disinfection process in hospital settings. To shed some choice of the appropriate formulation of cleansers or further light on operational aspects, we aimed to test a disinfectants and non-adherence to the required contact new UV-C robot in real life. To evaluate the antimicrobial time of disinfectants may impair the efficacy of standard efficacy of a standard UV-C disinfection cycle, we inves - approaches. Studies have shown that more than 50% of tigated its effect on the microbial burden on clinical sur - surfaces may go untouched by manual cleaning [3, 8, 9]. faces when applied after standard terminal cleaning and Secondly, in times of crisis, the supply of disinfectants disinfection (STC&D) in the waiting areas of two outpa- may be disrupted, as has been demonstrated in the cur- tient clinics. As a surrogate for resilient microorganisms, rent COVID-19 pandemic [10]. four different  C. auris  strains in varying densities (10 Because of the shortcomings of routine environmen- and 10   CFUs/ml) and different growth characteristics tal decontamination as mentioned above, autonomous (lag vs stationary growth phase) were placed within these touchless surface disinfection technologies have evolved. areas and exposed to UV-C irradiation as well. By disrupting the structure of DNA or RNA of microor- ganisms, UV-C irradiation at a wavelength of 254  nm is Materials and methods most effective in killing bacteria, viruses, fungi, and even UV‑C light emitting disinfection device spores (in falling order of effectiveness) [11]. We studied the self-driving Ultra Violet Disinfection Previous studies indicate that disinfection technologies Robot (UVD-R) by Clean Room Solutions because it using UV-C irradiation are an enhancement to standard was the most advanced UV-C irradiation device available cleaning and disinfection, reducing the environmental for autonomous use (Fig. 1). microbial burden and potentially mitigating the risk of This robot moves autonomously in a pre-defined area acquiring a HAI [12–18]. This has been demonstrated for after being programmed for the parameters exposure different pathogens such as MRSA, Clostridium difficile time and distance of surfaces. It consists of eight lamps and VRE [13, 18] and in different clinical settings such as that are located on top of a platform. During a disinfec- ambulances [19], inpatient rooms [16, 20] and operating tion cycle, they emit UV-C irradiation at a wavelength of theaters [15]. 254 nm, enabling a 360 degree coverage. During the dis- The efficacy of UV-C irradiation to inactivate microor - infection process, the UV-C light emitting robot moves ganisms depends on a number of factors including vary- at 10 cm per second, providing a dose of 2.7 mJ/cm  per ing resistance levels of different microorganisms to UV-C second for directly exposed surfaces in 1 m distance and light, the initial inoculum and the UV-C dose received, achieving a coverage of areas at a distance of several which is a result of distance, duration of exposure and the A strid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 3 of 10 cleaned once a day while chairs and tables are disinfected once a day using either alcohol-based products or prod- ucts based on active oxygen (Descogen Liquid). Prior to the start of the study, a member of the UVD Robot installation team pre-programmed area maps with the exact position of furniture and other items to enable autonomous disinfection cycles. For the pre-pro- gramming, the team inspected the two outpatient clinics to map the robot’s route and identify critical areas that required longer UV-C light exposure. The robot was pre- programmed to stop at various predefined positions for 3  min to achieve optimal UV-C exposure of all relevant surfaces (Figs. 2, 3). The device was used after the room had been manually cleaned and disinfected according to SOP. The proce - dure was then initiated remotely once all doors had been Fig. 1 UVD Robot (Clean Room Solutions) meters (according to manufacturer’s specifications). However, it is worth bearing in mind that the UV-C light intensity over distance is governed by the inverse square law, resulting in significantly smaller doses for areas fur - ther away from the device. To enable autonomous mov- ing, the robot must be pre-programmed using a detailed map of the position of furniture and other obstacles in the area to be treated with UV-C irradiation. Once every parameter is set, furniture and all other objects must Fig. 2 Area map pre‑programmed into the UV ‑ C robot in the ENT remain in exactly the same place to enable an autono- outpatient clinic. The blue dots indicate where the robot had to stop mous functioning. Due to the high-intensity UV-C irradi- for 3 min during the disinfection cycle. The red color indicates which ation, the UV-C robot may only be used in rooms devoid area was covered by the mapping procedure and exposed to UV‑ C of people. Unintentional exposure leads to cutaneous light erythema and photokeratitis. For safety, this UV-C robot automatically shuts off when its motion sensor detects any moving individuals during the disinfection process. Setting Between July 23rd and August 2nd 2020, the study was performed in the waiting areas of two outpatient clin- ics (ear, nose and throat medicine and oncology waiting areas with a size of 137  m each) of Vienna General Hos- pital (VGH), a 1728 bed tertiary hospital in the capital of Austria. During the study period, 347 patients were treated in the ENT (23/07–26/07) and 400 patients in the oncology outpatient department (29/07–02/08). Fig. 3 Area map pre‑programmed into the UV ‑ C robot in the In one of the outpatient areas, manual cleaning/disin- oncology outpatient clinic. The blue dots indicate where the robot fection was carried out by in-house cleaning personnel had to stop for 3 min during the disinfection cycle. The red color while the other outpatient clinic was served by a clean- indicates which area was covered by the mapping procedure and exposed to UV‑ C light. The violet color indicates “light detection and ing service providing company. Cleaning and disinfec- ranging” (Lidar), which is a way for the robot to see an obstacle and tion followed the standard operating procedures (SOP) of avoid that area VGH: Floors in the outpatient waiting areas are manually Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 4 of 10 closed. Each disinfection cycle was completed within 20–25 min per outpatient setting. Sampling procedure To evaluate the robot’s effect on residual contamina - tion, samples were collected from different surface sites before and after routine cleaning and/or disinfection, and after the use of the UV-C robot. Surface sites selected for sampling included high-touch surfaces and remote sites supposedly to be out of reach for easy cleaning and those that appeared unlikely to achieve full exposure to UV-C irradiation. In the ENT waiting area, six sites were sampled (wall, armrests of two different chairs, back of a chair, wooden play element for children, window countertop) (see Addi tional file 1: Table S1). In the oncology waiting area, sampling was performed from eight different sites (patient registration area, table surface next to patient registration, armrests of two dif- ferent chairs, window countertop, push button of a vend- ing machine, leaflet dispenser) (see Additional file  1: Table S2). To monitor the amount of exposure to UV-C irradia- tion, disposable indicators were placed on all surfaces used for sampling before initiating the UV-C cycle. The indicators changed color depending on the achieved dose, corresponding to doses ranging from 25  mJ/cm in shadowed areas to 100  mJ/cm at the most highly exposed sites (Fig. 4). The achieved UV-C doses corresponding to each sam - pling site are presented in the supplemental material (see Additional file 1: Tables S1–S2). Microbiological methods Determination of the microbial burden on hospital surfaces We collected environmental contact cultures from each sampling site using Tryptic Soy Agar (TSA) plates with a diameter of 5.5  cm (VWR International, Vienna, Aus- tria). Samples were collected on 9  days by the same lab Fig. 4 Reference chart (UV‑ C dose received according to indicator’s change of color); Intellego Technologies technician following a predefined standardized sampling scheme: During the study period, sampling was performed three times per study day: Surfaces were subdivided into three categories accord- ing to their level of contamination used routinely for (a) before routine cleaning and/or disinfection, environmental samples at our institution: (b) after routine cleaning and/or disinfection, and (c) after the use of the UV-C robot. (1) surfaces with a low microbial burden, defined as 0–3 CFUs/24  cm After sampling, TSA plates were incubated at 37  °C (2) surfaces with an average microbial burden, defined for 48  h. Following incubation, the number of colony as 4–50 CFUs/24  cm forming units (CFUs) on each plate was counted. Sub- (3) surfaces with a high microbial burden, defined sequently, the colonies were identified using the MALDI- as > 50 CFUs/24  cm . TOF mass spectrometry method (Bruker, USA). A strid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 5 of 10 Preparation of Candida auris strains performed at a two-sided significance level of 0.05, using We investigated whether the type of C. auris strain, seed- SPSS (Version 26.0, IBM). ing density and incubation prior to UV-C light exposure In an exploratory data analysis, the plates of UV-C affected UV-C efficacy. exposed C. auris strains with a concentration of 10 To study potential differences in sensitivity to UV-C CFUs/ml were visually compared to unexposed controls. irradiation, four C. auris strains were evaluated: C. auris Results of C. auris with an initial concentration of 10 NCPF 8971, C. auris NCPF 8977, C. auris NCPF 8984 CFUs/ml were quantified as the number of CFUs, com - and C. auris DSM 21092. paring exposed and unexposed plates. Plates containing Sabouraud Dextrose Agar (SDA) (Becton Dickinson, Franklin Lakes, USA) were inoculated Results with 100  µl of C. auris suspension at two different con - Eec ff ts on the environmental microbial burden 3 6 centrations, 10 CFUs/ml and 10 CFUs/ml respectively. During the study period, we collected 192 samples (72 Each strain of C. auris suspension containing 10 in the ENT and 120 in the oncology outpatient areas, CFUs/ml was spread on three SDA plates and incubated respectively) from 14 sites (64 samples prior to any clean- for 24  h at 30  °C. For the field experiment, rimless TSA ing and disinfection, 64 after manual cleaning and dis- plates were pressed on these SDA plates, mimicking infection and 64 after the use of the UV-C robot). Prior surface contamination by hands and fomites as demon- to manual cleaning, the surfaces most heavily contami- strated by Adams et al. [29]. Overall, 12 TSA plates were nated were the armrests of chairs, followed by the win- used per study day. dow countertops. The least contaminated sites were Additionally, each strain of C. auris suspension con- the walls, the leaflet dispenser and the backs of patient taining 10 CFUs/ml was spread on one SDA plate with- chairs. The leaflet dispenser, however, was empty during out further incubation, yielding four plates with C. auris the study period according to an in-house IPC order to in a lag phase per study day. Then, C. auris exposed avoid potential cross-transmission via contaminated leaf- TSA plates (10 CFUs/ml, incubated overnight) as well lets during the COVID-19 pandemic. In general, contam- as inoculated SDA plates (10 CFUs/ml without further ination levels prior to any cleaning and disinfection were incubation) were placed on two tables in the waiting area higher in the oncology outpatient area than in the ENT of the oncology outpatient clinic during the standard outpatient area. disinfection cycle. Indicators were placed alongside that In Table  1, the level of contamination according to measured the UV-C dose received. This experiment was the time of sampling is summarized for each outpatient performed in triplicate. waiting area. UV-C indicators showed that some of the Following UV-C exposure, all plates were incubated at sites received a suboptimal UV-C dose. Nonetheless, the 30 °C for 7 days. Then, C. auris growth was compared to additional use of UV-C irradiation achieved a further unexposed controls. reduction of CFUs compared to standard cleaning and/ or disinfection, resulting in decontamination of 96.9% Statistical analysis (62/64) of the surfaces compared to decontamination of Standard descriptive analysis was done to summarize 50.0% (32/64) of the surfaces after manual cleaning and the microbiological findings. Differences between the disinfection alone. number of CFUs after standard terminal cleaning and With regard to the microbial burden, the additional use disinfection compared to the combined use of STC&D of the UV-C robot significantly decreased the median and UV-C irradiation were analyzed using the Wilcoxon number of CFUs in both outpatient areas compared to matched-pairs signed rank test. Statistical analysis was manual cleaning and disinfection alone (p = 0.008 and Table 1 Proportion of contact cultures with low, acceptable and high microbial burden before routine cleaning and/or disinfection, after routine cleaning and/or disinfection and after the use of the UV‑ C robot ENT outpatient area Oncology outpatient area Low Average High Low Average High Before C&D 45.8% (11/24) 37.5% (9/24) 16.7% (4/24) 22.5% (9/40) 60.0% (24/40) 17.5% (7/40) After C&D 79.2% (19/24) 20.8% (5/24) 0% (0/24) 32.5% (13/40) 62.5% (25/40) 5.0% (2/40) After C&D + UV‑ C 100% (24/24) 0% (0/24) 0% (0/24) 95.0% (38/40) 5.0% (2/40) 0% (0/40) 2 2 2 C&D cleaning and disinfection, UV-C ultraviolet C; low = 0–3 CFUs/24  cm , average = 4–50 CFUs/24  cm , high > 50 CFUs/24 cm Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 6 of 10 p < 0.001, for the ENT and for the oncology outpatient areas, respectively) (Table 2). Qualitative description of the environmental microbiome Most bacterial isolates were classified as physiological skin flora (222/297; 74.7%). Next, 13.1% of bacteria were classified as environmental microorganisms (39/297), 6.4% of bacteria were classified as oropharyngeal flora (19/297) and 5.7% of bacteria as potential pathogens (17/297). Typical pathogens were Staphylococcus saprophyticus (n = 5) and Staphylococcus lugdunensis (n = 1), Acinte- tobacter baumanii (n = 2), Aerococcus viridans (n = 1), Streptococcus pneumonia (n = 1), Staphylococcus aureus (n = 1) and Enterococcus casseliflavus (n = 1). The arm - rests of chairs were the sites most frequently contami- nated with pathogens. All identified microorganisms in both waiting areas, the median CFUs and the achieved UV-C doses, reported separately for each sampling site, Fig. 5 C. auris (10 CFUs/ml) on Sabouraud plates without (above) time of sampling and outpatient waiting area, are given and with (below) exposure to UV‑ C irradiation following incubation in the supplemental material (Additional file  1: Tables S1–S4). consistently showed growth greater than 50 CFUs on Eec ff ts on Candida auris each TSA contact plate after UV-C exposure. In terms UV-C irradiation emitted by the robot reduced the of the UV-C dose received, the indicators indicated high growth of all four C. auris strains spread at a concen- exposure (75–100 mJ/cm ) for all C. auris plates (Table 3, tration of 10 CFUs/ml on SDA plates, mimicking the Fig. 6). microbial lag phase. However, as shown in Fig. 5, growth of C. auris was observed on one fourth of the plate. Use of a UV‑C robot for the routine cleaning and/ According to the indicators placed alongside, the meas- or disinfection process ured UV-C dose was 100  mJ/cm (indicating maximum The UV-C robot required many attempts until it could exposure) except for the area right next to the rim of the carry out the UV-C disinfection process indepen- plate, demonstrating the shadow effect of the rim. dently. Interventions by the operator were necessary The effect of the UV-C robot on stationary C. auris due to initial programming imprecisions, furniture cells at an initial concentration of 10  CFUs/ml was vari- that had accidentally been moved during routine clini- able and depended on the C. auris strain tested (Table 3). cal operations, detection of movement during an The C. auris NCPF 8984 strain was the most sensitive ongoing disinfection cycle or loss of internet connec- of the tested strains. It also showed the most consistent tion. Although the area was cordoned off during the results regarding growth reduction after UV-C expo- disinfection cycles and appropriate warning signs were sure compared to control plates. C. auris NCPF 8971 posted on the access doors, we found it difficult to Table 2 Reductions in Colony‑Forming Units after routine cleaning and/or disinfection compared to baseline and after routine cleaning and/or disinfection + UV‑ C irradiation compared to routine cleaning and/or disinfection alone ENT outpatient area Oncology outpatient area No. of Median CFU (IQR) Min Max p value No. of Median CFU (IQR) Min Max p value samples samples Before C&D 24 8.5 (8.5–28.3) 0 207 0.003 40 22.0 (4.3–36.0) 0 200 After C&D 24 0 (0–2.8) 0 18 40 6.5 (2.3–20.5) 0 101 <0.001 After C&D 24 0 (0–2.8) 0 18 0.008 40 6.5 (2.3–20.5) 0 101 After C&D + UV‑ C 24 0 (0–0) 0 1 40 0 (0–0) 0 5 <0.001 No. number, CFU Colony Forming Unit, IQR interquartile range, Min minimum, Max maximum, C&D cleaning and disinfection, UV-C ultraviolet C A strid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 7 of 10 Table 3 Colony counts per TSA plate containing C. auris in a Discussion stationary phase (10 CFUs/ml) with and without UV‑ C exposure The contaminated hospital environment is a reservoir for various pathogens and may thus serve as a source of C. auris C. auris C. auris C. auris NCPF NCPF NCPF DSM HAIs [30]. Conventional manual cleaning and disinfec- 8971 8977 8984 21092 tion processes are not always   sufficient to eliminate the Control (without > 100 > 100 > 100 > 100 risk posed by contaminated surfaces [3, 8, 9]. Human UV‑ C exposure) factors are likely to be a major contributor. Further- Day1 (after UV‑ C) more, during the COVID-19 pandemic, effective stand - 1 > 50 35 1 > 50 ard disinfectants were unavailable in times of crisis [10], 2 > 50 > 50 28 35 indicating the need of new disinfectants or disinfection methods. Most recently, autonomously moving UV-C 3 > 50 > 50 1 > 50 disinfection devices—UV-C robots—have been devel- Day2 (after UV‑ C) oped to overcome these shortcomings. 1 > 50 > 100 > 50 20 The present study shows that UV-C irradiation emit - 2 > 50 > 100 11 > 50 ted by the robot significantly decreased the residual sur - 3 > 100 > 100 10 > 50 face contamination in the waiting areas of two outpatient Day3 (after UV‑ C) clinics of a tertiary hospital compared to manual clean- 1 > 50 > 50 11 > 50 ing and disinfection alone. This is in accordance with 2 > 50 > 50 0 > 50 other studies that have found a significant decrease of the 3 > 50 > 50 > 50 30 pathogen bioburden in clinical settings by using a robotic Corresponding UV-C doses received during each disinfection cycle ranged from 75 to 100 mJ/cm UV-C irradiation device [12, 13, 15, 31]. Anderson et  al. found that the application of UV-C light significantly reduced the presence of Vancomycin-resistant entero- ensure the total absence of health personnel returning cocci (VRE) and Clostridium difficile in patient rooms to their nightshift rooms nearby or other individuals previously occupied by colonized patients compared to who moved in and out the closed area. baseline (without prior manual cleaning and disinfection) In terms of its user-friendliness and simplicity of [20]. Similarly, Yang et  al. observed a significant reduc - operation, the device required—in addition to the tion of the number of bacteria colonies sampled from dif- pre-programming of the area’s maps—further preced- ferent surfaces after UV-C exposure in uncleaned rooms ing steps to start the disinfection process. The user previously occupied by VRE and MRSA carriers [32]. In had to select several items in two different apps on the the present study—despite the fact that not all surfaces device’s control panel, which was not self-explanatory. achieved full UV-C light exposure—almost all microor- ganisms still present after manual cleaning and disinfec- tion were eliminated. However the microbial burden on surfaces was low to average on almost all surfaces after Fig. 6 Growth of C. auris strains in a stationary phase on TSA contact plates after UV‑ C exposure Astrid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 8 of 10 manual cleaning and/or disinfection alone. Especially in assistance to operate the robot. Future technological the ENT outpatient waiting area, manual cleaning and advances  are  supposed to overcome these failings. In disinfection had been carried out meticulously, resulting addition to a somewhat complicated programming of in the recovery of only few CFUs. Insufficient UV-C light the parameter settings, the robot tested was mostly not exposure might have yielded less effective results in other autonomous and not able to carry out the room disinfec- settings, e.g. with higher surface contamination levels. tion independently. Apart from technical reasons, this Using C. auris as a surrogate for microorganisms resil- dysfunction was also due to the fact that furniture and ient in the environment, the UV-C disinfection robot other objects had been  slightly moved between the ini- tested showed varying effectiveness: For C. auris that had tial programming and the robot’s use. Moreover, despite been incubated for 24  h before exposure to UV-C irra- sealing the areas off during the UV-C disinfection cycles, diation, growth inhibition was not effectively achieved people moved in and out. Yet, this is normal in the hos- compared to C. auris without prior incubation (for fully pital reality. Advances in IT, particularly using artificial exposed areas). However, this may be due to our dif- intelligence together with high-tech cameras may be the ferent sample preparations, mimicking C. auris in a lag clue for solving these problems. Additionally, further versus a stationary growth phase. Furthermore, the for- technical developments such as making the UV-C light mation of shadows from the rim of SDA plates drastically source more flexible and the robot itself smaller will be decreased the effectiveness of UV-C light. De Groot et al. necessary in addition to adjustments in the clinical envi- investigated the effect of different distances (two or four ronment to minimize the formation of shadows, thus meters) from the UV-C emitting device as well as differ - enabling the proper use of this novel technology. ent cycle times (5, 10, 20 or 30 min) on C. auris in vitro, The decision to use a UV-C disinfection robotic device demonstrating strain-dependent effectiveness. Longer in clinical settings must be made on the basis of the UV-C exposure and less distance improved the effects intended application area, the practicability of use and of UV-C irradiation [21]. The present study evaluated the additional expected benefit. At the present stage of the effects of UV-C irradiation on C. auris delivered by UV-C robot technology, these robots will be preferably a robot in a clinical setting. These results confirm that used in areas with stationary furniture that can easily longer UV-C exposure is necessary to eradicate C. auris, be sealed off to avoid  people walking in and out during especially when inoculums are high and pathogens have an ongoing disinfection cycle. Practicability means that already had time to mature. Thus, it is pivotal to vali - the UV-C robot will be operated by trained cleaning staff date the effectiveness of UV-C robotic devices separately rather than by an engineer or a technician. An additional for each clinical setting. To achieve this, the robot’s set- expected benefit, however, might be achieved in areas tings (distance and duration of exposure) must be care- with vulnerable patients or in over-busy areas with highly fully calibrated and adapted further until microbiological contaminated surfaces including the risk of multidrug- outcomes are satisfactory. This requires the expertise of resistant microorganisms, e.g. emergency departments. a clinical microbiologist and IPC specialist. UV-C sensi- There are some limitations to this study. First, show - tive, color-changing indicators measuring the amount of ing a reduction in the microbial burden on surfaces is a UV-C irradiation received must be used as quality con- surrogate outcome. The study design did not allow for an trols. Particularly for surfaces or objects that create shad- evaluation of the effect of UV-C irradiation in addition to ows and cannot be reached by UV-C irradiation, manual manual cleaning and disinfection on HAI rates compared cleaning and disinfection are still needed. In the future, to manual cleaning and disinfection alone. Next, the clas- design of hospital areas will have to avoid structures cre- sification of the sampling sites into surfaces with a low, ating shadows if UV-C disinfection is applied. Neverthe- average and high microbial burden was made accord- less, for surfaces beyond the reach of the cleaners, UV-C ing to our in-house standard, which is used to audit the robots may be useful. Then, to achieve effective UV-C cleaning efficacy. It refers to the colony count but is not disinfection the UV-C source must be able to move into directly associated with patients’ outcomes. Further, the three dimensions (tilt, move up and down). cleaning personnel was not blinded to the intervention, The usability of the UV-C robot in the clinical set - which might have affected their behavior, resulting in ting was not as satisfactory as expected from a robotic more thorough cleaning and not reflecting the quality of device. This study aimed to evaluate the UV-C robot in cleaning in daily practice. Therefore, our results might action, particularly its usability when integrated into underestimate the benefit provided by adding a UV-C the standard cleaning and disinfection process. UV-C component. Next, to determine the effects of the UV-C robots are usually advertised as being simple to use robotic device on C. auris, artificially inoculated plates with no additional decontamination needed. However, were used as a surrogate for surface-bound contamina- in our own experience, we repeatedly needed technical tion. This might not accurately reflect growth patterns A strid et al. Antimicrob Resist Infect Control (2021) 10:84 Page 9 of 10 the manuscript. DM, PE, EJ and NM revised the manuscript. All authors read of C. auris on real-world surfaces. Moreover, densities and approved the final manuscript. occurring on contaminated hospital surfaces may not be as high, resulting in an underestimation of the ability of Funding This research did not receive any specific grant from funding agencies in the UV-C light to kill C. auris. public, commercial, or not‑for ‑profit sectors. Availability of data and materials The datasets used and/or analyzed during the current study are available from Conclusion the corresponding author on reasonable request. The UV-C disinfection model robot tested in our study was not yet ready for everyday use in hospitals due to Declarations several technical shortcomings and difficulty of use as well as likely significant additional expense. We also Ethics approval and consent to participate Not applicable. observed persistence of C. auris in a stationary phase, indicating that a standard disinfection cycle might not Consent for publication suffice to inactivate more UV-C resistant pathogens, Not applicable. especially when inoculums are high. While UV-C tech- Competing interests nologies improve surface decontamination results, they The authors certify that they have no affiliations with or involvement in any do not simplify current processes and can presently only organization or entity with any financial interest or non‑financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in serve as add-on components to manual cleaning and the subject matter or materials discussed in this manuscript. disinfection carried out by trained and audited cleaning staff. However, there is huge potential in this technology Received: 2 December 2020 Accepted: 26 February 2021 once it is further developed. Abbreviations References C. auris: Candida auris; C&D: Cleaning and disinfection; CFU: Colony‑Forming 1. Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, Unit; ENT: Ear, nose and throat; IPC: Infection prevention and control; HAI: et al. Multistate point‑prevalence survey of health care ‑associated infec‑ Healthcare‑associated infection; MRSA: Methicillin‑resistant Staphylococcus tions. N Engl J Med. 2014;370(13):1198–208. aureus; SDA: Sabouraud Dextrose Agar; SOP: Standard operating procedure; 2. WHO. Report on the endemic burden of healthcare‑associated infection STC&D: Standard terminal room cleaning and disinfection; TSA: Tryptic Soy worldwide. 2011. https:// www. who. int/ infec tion‑ preve ntion/ publi catio Agar; UV‑ C: Ultraviolet‑ C; VRE: Vancomycin‑resistant Enterococcus. ns/ burden_ hcai/ en/. 05 Nov 2020. 3. Dancer SJ. 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Carling PC. Evaluating the thoroughness of environmental cleaning in hospitals. J Hosp Infect. 2008;68(3):273–4. Acknowledgements 9. Carling PC, Parry MM, Rupp ME, Po JL, Dick B, Von Beheren S. Improv‑ We would like to thank Clean Room Solutions for providing their Ultra Violet ing cleaning of the environment surrounding patients in 36 acute care Disinfection Robot (UVD‑R) as well as technical support during the study hospitals. Infect Control Hosp Epidemiol. 2008;29(11):1035–41. period. Clean Room Solutions did not provide any funding for the study and 10. Kampf G, Scheithauer S, Lemmen S, Saliou P, Suchomel M. COVID‑ did not contribute to the study design or writing of the manuscript. We would 19‑associated shortage of alcohol‑based hand rubs, face masks, medical also like to thank Thi Lan Vi Tran for assisting with the statistical analysis as gloves and gowns—proposal for a risk‑adapted approach to ensure well as the ESCMID Study Group for Nosocomial Infections (ESGNI) for their patient and healthcare worker safety. J Hosp Infect. 2020;105(3):424–7. valuable input. 11. Misovic M, Milenkovic D, Martinovic T, Ciric D, Bumbasirevic V, Kravic‑Ste ‑ vovic T. Short‑term exposure to UV ‑A, UV ‑B, and UV ‑ C irradiation induces Authors’ contributions alteration in cytoskeleton and autophagy in human keratinocytes. DM and PE designed the study. ZB prepared the Candida auris samples and Ultrastruct Pathol. 2013;37(4):241–8. summarized the results regarding Candida auris growth inhibition as a result of 12. Liscynesky C, Hines LP, Smyer J, Hanrahan M, Orellana RC, Mangino JE. UV‑ C exposure. NM and EJ assisted in the execution of the study. 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