The Journal of Infectious Diseases MAJOR ARTICLE Rapid SARS-CoV-2 Inactivation in a Simulated Hospital Room Using a Mobile and Autonomous Robot Emitting Ultraviolet-C Light Cristina Lorca-Oró,1 Jordi Vila,2,3 Patricia Pleguezuelos,1 Júlia Vergara-Alert,1 Jordi Rodon,1 Natàlia Majó,1,4 Sergio López,1 Joaquim Segalés,1,4 Francesc Saldaña-Buesa,5 Maria Visa-Boladeras,6 Andreu Veà-Baró,2,5 Josep Maria Campistol,2,3 and Xavier Abad1 1 Centre de Recerca en Sanitat Animal, Institut de Recerca i Tecnologia Agroalimentàries, Campus de la Universitat Autònoma de Barcelona, Barcelona, Spain, 2Hospital Clínic, University of Barcelona, August Pi i Sunyer Biomedical Research Institute, Barcelona, Spain, 3Institute for Global Health (ISGlobal) - Hospital Clinic, Universitat de Barcelona, Barcelona, Spain 4Departament de Sanitat i Anatomia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, Barcelona, Spain, 5CovidWarriors, Barcelona, Spain, and 6MTS Tech, Barcelona, Spain The spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) since 2019 has made mask-wearing, physical distancing, hygiene, and disinfection complementary measures to control virus transmission. Especially for health facilities, we evaluated the efficacy of an UV-C autonomous robot to inactivate SARS-CoV-2 desiccated on potentially contaminated surfaces. ASSUM (autonomous sanitary sterilization ultraviolet machine) robot was used in an experimental box simulating a hospital in- tensive care unit room. Desiccated SARS-CoV-2 samples were exposed to UV-C in 2 independent runs of 5, 12, and 20 minutes. Residual virus was eluted from surfaces and viral titration was carried out in Vero E6 cells. ASSUM inactivated SARS-CoV-2 by ≥ 99.91% to ≥ 99.99% titer reduction with 12 minutes or longer of UV-C exposure and onwards and a minimum distance of 100 cm between the device and the SARS-CoV-2 desiccated samples. This study demonstrates that ASSUM UV-C device is able to inactivate SARS-CoV-2 within a few minutes. Keywords. SARS-CoV-2 inactivation; UV-C radiation; autonomous robots; exponential viral-load reduction; virus inactivation. The coronavirus disease 2019 (COVID-19) pandemic con- coughing, sneezing, and breathing near to another person or tinues to make necessary the collaboration of researchers, med- by aerosols. However, the virus in aerosols and droplets depos- ical professionals, technologists, and industry to find rapid and ited on surfaces has been demonstrated to remain infectious for reliable solutions until we reach herd immunity conferred by a few days, especially in cold environments, and can be a risk globally available vaccines. Up to 7 October 2021, severe acute for infection [3–5]. In places such as hospitals and health care respiratory syndrome coronavirus 2 (SARS-CoV-2) has caused facilities, disinfection of surfaces is especially required to avoid more than 235 million confirmed COVID-19 cases and 4.8 mil- SARS-CoV-2 nosocomial transmission [6–8]. lion deaths, and over 6000 million vaccine doses have been ad- SARS-CoV-2 has a lipid-containing envelope with a ministered [1]. The rapid spread of SARS-CoV-2 since the end nonsegmented positive-sense RNA genome [9], and is rela- of 2019, and the challenge of world population immunity, make tively easy to inactivate by heat, chemical disinfectants, deter- other prevention measures still crucial to control SARS-CoV-2 gents, gamma irradiation, or UV light [10, 11]. UV irradiation transmission. works as a virucidal agent by cellular damage (photohydration, In respiratory diseases, spread occurs primarily through di- photosplitting, photodimerization, and photocross-linking) rect patient contact, droplet transmission, or by the airborne and thereby inhibiting cellular replication [12]. The disinfection route [2]. In the case of SARS-CoV-2, transmission has been of medical and laboratory objects using UV light is widely used mainly reported to be from infective droplets produced by as a germicidal method for certain bacteria, fungi, and viruses without the use of harmful chemicals or heat [13]. UV-C light (100–280 nm wavelength) can be artificially generated from Received 6 September 2021; editorial decision 23 October 2021; accepted 18 November 2021; published online 20 November 2021. low-pressure mercury lamps or from pulsed xenon lamps [12]. Correspondence: Cristina Lorca-Oró, PhD, Centre de Recerca en Sanitat Animal (CReSA, Previous studies reported that high doses of UV-C are effective IRTA-UAB), Campus de la Universitat Autònoma de Barcelona, 08193 Barcelona, Spain (cristina. for inactivating SARS-CoV-2 and SARS-CoV in blood products lorca@irta.cat). The Journal of Infectious Diseases®  2021;XX:1–6 or in culture medium [10]. Thus, UV disinfection is an envi- © The Author(s) 2021. Published by Oxford University Press for the Infectious Diseases ronmentally friendly method that does not leave a residue or Society of America. This is an Open Access article distributed under the terms of the Creative require ventilation after treatment. Although the efficacy of UV Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/ by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any irradiation on the inactivation of pathogens, and particularly medium, provided the original work is not altered or transformed in any way, and that the work is SARS-CoV-2, has been previously described [14–16], there is properly cited. For commercial re-use, please contact journals.permissions@oup.com https://doi.org/10.1093/infdis/jiab551 little scientific evidence of similar studies in realistic scenarios. Effective SARS-CoV-2 Inactivation by UV-C • JID 2021:XX (XX XX) • 1 Hence, the aim of the present work was to explore the efficacy positions were located throughout the room for each run. In each of an autonomous and mobile UV-C robot (ASSUM, autono- position, next to the plates with desiccated SARS-CoV-2, 2 ad- mous sanitary sterilization ultraviolet machine; MTS Tech), hesive chemical indicators were placed to record the actual cu- equipped with 4 UV-C lamps of 254 nm wavelength arranged mulative UV-C radiation dose received per sample site. One of in 360°, for application to high-touch surfaces potentially con- the indicators ranged from 0 to 200 mJ/cm2 (ASSUM stickers) taminated with SARS-CoV-2. and the other from 500 to 1000 mJ/cm2 (Chemdye ChemDose). Four of the 6 SARS-CoV-2 desiccated plates used for each ex- METHODS posure time were located at 100 cm height on the 4 room walls Ultraviolet-C Light Device (1 on each wall). Another plate was located under the closest A mobile UV-C robot, ASSUM, was used. This device is to ASSUM robot corner of a table and the remaining plate was equipped with 4 UV-C Phillips lamps of 254 nm arranged placed on the floor at one of the room’s corners (Figure 1 and in 360° and its dimensions are 600 × 900 × 1500 mm, width, Supplementary Video). For all replicates, the ASSUM robot was length, and height. ASSUM scans and moves throughout the set to keep a minimum distance of 1 m from the UV-C exposed space always respecting a programmed distance from any ob- samples when freely moving around the box. stacle or surface, reaching a maximum UV-C efficiency. SARS-CoV-2 Detection and Titration Cells and Virus After each exposure time, all plates were eluted with 1 mL of Vero E6 cells (Vero C1008; American Type Culture Collection DMEM (1% FCS) and stored at −75°C until titration. One day CRL-1586) were cultured in Dulbecco’s Modified Eagle’s before titration, 96-well plates with 1.5 × 104 Vero E6 cells/ Medium (DMEM) supplemented with 10% fetal calf serum well (in 100 µL of DMEM-10% FCS) were seeded. Prior to (FCS). SARS-CoV-2 (lineage B.1) was isolated from a nasopha- infection, cells were checked under an inverted light micro- ryngeal swab collected from an 89-year-old man from the first scope. On the day of titration, 2 replicates of five 10-fold se- patient cluster in Catalonia, Spain (Global Initiative on Sharing rial dilutions of each sample were prepared. A total of 20 µL Avian Influenza Data ID EPI_ISL_510689) as previously de- scribed in detail [17]. Working virus stocks with a titer of 106 50% tissue culture infectious dose (TCID50)/mL were gener- A ated by infecting Vero E6 cells at a multiplicity of infection of 0.01 in the presence of 5% FCS. Cell culture supernatants were 3 collected at 72 hours postinfection, clarified for 10 minutes at 4 2 3000g, aliquoted, and stored at −75°C until required. For this 5 study, virus was thawed immediately before the experiment and 6 100 cm sterile plastic plates (35 mm; SPL, Ref. PLC20035) were used as 100 cm 1 the surface to desiccate 100 µL/plate of SARS-CoV-2 in a period of 90–100 minutes under airflow in a class 2 biosafety cabinet. All infectious work was carried out using the appropriate per- sonal protective equipment (double gloves, double gown, and B powered air-purifying respirator Sundström equipment) at Institut de Recerca i Tecnologia Agroalimentàries-Centre de Recerca en Sanitat Animal High Biocontainment Unit (bio- safety level 3 facilities). Study Design The study was carried out in and experimental box with floor area 11-m2 mimicking a hospital room. A total of 42 sterile plastic plates were prepared with 100 µL/plate of SARS-CoV-2 at 106 TCID50/mL. Thirty-six of the 42 plates with desiccated SARS- CoV-2 were irradiated by the ASSUM UV-C robot for different Figure 1. Schematic representation of the autonomous sanitary sterilization ul- time periods (5, 12, and 20 minutes). In addition, 2 plates per ex- traviolet machine (ASSUM) UV-C device. A, Position of tested desiccated severe posure time were left in the laboratory as a negative control (plate acute respiratory syndrome coronavirus 2 (SARS-CoV-2) samples and chemical in- dicators in the experimental box. Black numbers indicate positions of samples at with culture medium) and positive control (plate with desiccated, 100 cm height on the 4 room walls and sample 5 located under the edge of a table. non–UV-C exposed SARS-CoV-2). Two independent runs for Sample 6 was located on the floor in a corner of the room. B, Simulation of ASSUM each exposure time were performed, and 6 plates in different running in an operating room of a hospital. 2 • JID 2021:XX (XX XX) • Lorca-Oró et al of each diluted sample was added per well. A bulk titration plates not exposed to UV-C showed a mean viral load between was also performed for each sample. For this purpose, 20 µL 3.49 and 4.19 log10 TCID50/mL in 2 consecutive runs, which of each undiluted sample was added in 24 wells containing were analyzed independently. The detection limit of the tech- Vero E6 cells (a total volume of 480 µL/sample was titrated). nique was 0.45 log10 TCID50/mL. All plates were incubated for 1 hour at 37°C in 5% CO2. After The minimum distance between the ASSUM robot and the incubation, 130 µL of DMEM-10% FCS was added per well. desiccated samples was set at 1 m and the maximum was regis- Plates were incubated at 37°C in 5% CO2 for 6−7 days and tered close to 3 m to the opposed wall. As expected, the highest then the SARS-CoV-2–induced cytopathic effect was deter- reductions of infectious SARS-CoV-2 were observed particu- mined. Viral titers were calculated as 50% tissue culture infec- larly in the positions that were in direct line of sight (samples tious doses (TCID50) according to Spearman-Kärber methods located at 100 cm height on the walls). Samples located on the [18, 19]. walls or on the floor showed statistically significant differences (P < .01) compared to the SARS-CoV-2 controls not exposed to Statistical Analysis UV-C. This was not the case for the samples located under the The 2 runs performed for each exposure time (5, 10, and 20 edge of a table (P > .05). minutes) were considered as independent runs. To analyze the At 20 and 12 minutes of UV-C exposure, samples located on differences between the different sample position with UV-C the walls showed reduction ranging between ≥ 99.91% and ≥ exposure and the control not exposed to UV-C, Tukey mul- 99.99%. At 20 minutes, the sample located on the floor in the tiple comparisons test (ANOVA) was used to compare the viral corner showed the same reduction percentage. The infectivity titer means obtained at all positions and P values lower than reduction of samples located on the floor ranged from 99.47% .05 were accepted as statistically significant. Calculations were to 99.93% after 12 minutes of UV-C exposure. Finally, with done using Graphpad Prism 9. 5 minutes of UV-C exposure, 2 of the 4 samples on the walls reached a percentage of SARS-CoV-2 reduction comparable to those at 12 and 20 minutes, but the other 2 samples located RESULTS on the walls showed a 94.11% reduction. At 5 minutes, sam- Results of virus inactivation from the present study are sum- ples on the floor achieved 97.43%–98.00% infectivity decrease. marized in Table 1. All control samples without desiccated virus The samples located under the edge of a table showed the lowest were negative for each replicate and exposure time. Control viral reduction (63.7%–98.41%). Table 1. SARS-CoV-2 Titration Results Expressed as TCID50/mL Sample Location SARS-CoV-2 Titer, Mean log10 TCID50/mL Titer Reduction Range, logR Reduction Range, % UV-C robot working time 20 min Wall 1, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Wall 2, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Wall 3, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Wall 4, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 On the floor ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Under the edge of a table 2.69 0.49 to 1.81 67.64 to 98.41 UV-C robot working time 12 min Wall 1, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Wall 2, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Wall 3, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Wall 4, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 On the floor 1.14 2.27 to 3.14 99.47 to 99.93 Under the edge of a table 2.58 0.84 to 1.69 85.54 to 98.00 UV-C robot working time 5 min Wall 1, at 100 cm height 2.27 1.22 to ≥3.74 94.11 to ≥ 99.99 Wall 2, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Wall 3, at 100 cm height ≤0.45 ≥3.04 to ≥3.74 ≥ 99.91 to ≥ 99.99 Wall 4, at 100 cm height 0.45 3.04 to ≥3.74 99.91 to ≥ 99.99 On the floor 2.20 1.59 to 1.69 97.43 to 98.00 Under the edge of a table 3.37 0.44 to 0.51 63.70 to 69.80 SARS-CoV-2 infectious titer was calculated from serial dilutions and bulk titration mean (log10 TCID50/mL). Titer reduction range (logR) is shown compared to the SARS-CoV-2 desiccated stocks (3.49 and 4.19 log10 TCID50/mL) and the percentage of viral reduction range was obtained from both independent experimental runs. Abbreviations: SARS-CoV-2, severe acute respiratory syndrome coronavirus 2; TCID50, 50% tissue culture infectious dose. Effective SARS-CoV-2 Inactivation by UV-C • JID 2021:XX (XX XX) • 3 After allowing the robot to freely move around the experi- The risk of COVID-19 transmission by fomites has been mental box, the UV-C radiation dose at the different positions questioned, with the argument that most of the published ranged between 50 mJ/cm2 and 500 mJ/cm2, according to the studies have been carried out with high viral titers compared UV-C dosimeters (stickers placed next to the sample). After to those in natural aerosols or droplets from infected patients. both 12 and 20 minutes of UV-C exposure, samples located at As a consequence, it is believed that the risk of transmission by 100 cm height on the walls showed an accumulative UV-C ra- fomites is lower compared to aerosol or droplet transmission diation dose of 500 mJ/cm2 approximately, for both runs. For [22]. However, the number of viral particles present in aerosols these 2 exposure times, samples located on the floor and under or contaminated surfaces is not well known and the risk of in- the table received a UV-C radiation dose of 150 mJ/cm2 and 50 fection from fomites cannot be ruled out. Therefore, stringent mJ/cm2, respectively. preventive measures should be taken, especially in high-risk lo- After 5 minutes of UV-C exposure, samples at 100 cm height cations such as health care settings, to avoid this possible route on the walls received an accumulated UV-C radiation dose be- of transmission [6–8]. tween 200 and 500 mJ/cm2, while samples underneath the table There have been no previous studies on the use of autono- and on the floor received around 50 mJ/cm2. None of the posi- mous UV-C robots, which can freely move around ICU and tive or negative controls received UV-C radiation. other health care rooms where COVID-19 patients have been treated, to inactivate SARS-CoV-2 on contaminated surfaces. DISCUSSION Our work simulates an actual hospital scenario, including room With herd immunity as a huge challenge in the current COVID- obstacles, and the robot was set to maintain a minimum dis- 19 pandemic, all preventive measures are still crucial to mini- tance of 100 cm to all objects. Previous reports with this and mize SARS-CoV-2 spread. This study provides useful baseline other coronaviruses are in line with the results of our study and data towards securing a safer environment where surfaces are showed viral reduction mediated by UV-C irradiation in a lab- potentially contaminated with this and other pathogens sen- oratory enclosed within biosafety cabinet conditions. However, sitive to UV-C radiation. This is especially focused on health most of the published studies were performed with shorter care facilities where viral loads can be high. Here, we demon- exposure distances (a few cm) between the UV source and strated for the first time under comparable hospital intensive SARS-CoV-2 samples [14, 16, 23, 24]. Darnell and colleagues care unit (ICU) room conditions (not within a biosafety cab- [23] showed that after 15 minutes of UV-C irradiation at 3 cm inet) that SARS-CoV-2 load can be drastically reduced within a from the virus plate and a UV-C dose emitted of 4016 µW/cm2, few minutes using UV-C irradiated by the ASSUM autonomous SARS-CoV was inactivated below the detection limit (≤1.0 log10 robot. A preliminary assay was carried out to set the optimal TCID50/mL). Moreover, Heilingloh and colleagues [14] also timing and distance conditions for the UV-C mobile ASSUM showed complete inactivation of SARS-CoV-2 after 9 minutes robot. Results from this preliminary assay showed that 20 min- of irradiation and with a UV-C dose emitted of 1048 mJ/cm2 utes were enough to inactivate desiccated SARS-CoV-2 from at 3 cm. In both cases, the total inactivation implied about a surfaces at a distance between 1 and 2 m from the ASSUM de- 5-log reduction. These data on SARS-CoV and SARS-CoV-2 vice (data not shown). The results of the present assay showed indicting total viral inactivation were obtained under ideal con- infectious virus reduction ≥ 99.91% after 12 minutes of UV-C ditions with short UV exposure distances, which differ consid- exposure with a minimum distance of 100 cm from the UV-C– erably from our attempt to model a more realistic setting for exposed samples placed at 100 cm height and a cumulative testing SARS-CoV-2 UV-C inactivation. UV-C radiation dose between 50 and 500 mJ/cm2. As expected, Besides its efficiency, an advantage of the UV-C robot is its in shadowed positions, viral reduction was less evident, and self-autonomy and capability to freely move and maintain a the lowest viral reduction was observed for the samples located desired distance from room obstacles. This UV-C device may under a table; however, this location is also less likely to be con- be especially useful to avoid excessive exposure of cleaning or taminated with SARS-CoV-2. health care personnel to SARS-CoV-2 contaminated surfaces in Considering that the main route of SARS-CoV-2 transmis- hospital facilities, where high numbers of COVID-19 patients sion occurs from infectious droplets, which are very diverse in may shed large amounts of virus. Moreover, the ASSUM UV-C size, and produced by coughing, sneezing, and breathing near robot may inactivate other pathogens even more environmen- another person [20], SARS-CoV-2 nosocomial transmission tally resistant than SARS-CoV-2. has been reported over longer distances, principally due to high Taken together, the present study demonstrated that UV-C ir- air fluxes inside health care facilities [21]. So far as it is known, radiation is a highly effective method to inactivate high titers of human coronaviruses, including SARS-CoV and SARS-CoV-2, infectious SARS-CoV-2 from surrogate surfaces, mimicking a can remain infectious in aerosols for 3 to 16 hours and can sur- natural health care center environment and high touch surfaces. vive on surfaces at room temperature and relative humidity of This technology would be reliable not only for disinfection pur- 65% for a few days [3]. poses in health care rooms but also for other applications and 4 • JID 2021:XX (XX XX) • Lorca-Oró et al equipment or spaces with high risk of transmission, such as 4. Kratzel A, Steiner S, Todt D, et al. Temperature-dependent public transport facilities. Further studies regarding the efficacy surface stability of SARS-CoV-2. J Infect 2020; 81:452–82. of UV-C irradiation in other situations and other viruses will 5. Aboubakr HA, Sharafeldin TA, Goyal SM. 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