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Rapid and complete inactivation of SARS-CoV-2 by ultraviolet-C irradiation

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Abstract

The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic has devastated global public health systems and economies, with over 23 million people infected, millions of jobs and businesses lost, and more than 800 000 deaths recorded to date. Contact with surfaces contaminated with droplets generated by infected persons through exhaling, talking, coughing and sneezing is a major driver of SARS-CoV-2 transmission, with the virus being able to survive on surfaces for extended periods of time. To interrupt these chains of transmission, there is an urgent need for devices that can be deployed to inactivate the virus on both recently and existing contaminated surfaces. Here, we describe the inactivation of SARS-CoV-2 in both wet and dry format using radiation generated by a commercially available Signify ultraviolet (UV)-C light source at 254 nm. We show that for contaminated surfaces, only seconds of exposure is required for complete inactivation, allowing for easy implementation in decontamination workflows.
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Rapid and complete inactivation of SARS-CoV-2 by
ultraviolet-C irradiation
Nadia Storm
Boston University
Lindsay McKay
Boston University
Sierra Downs
Boston University
Rebecca Johnson
Boston University
Dagnachew Birru
Signify Research
Marc de Samber
Signify Research
Walter Willaert
Signify Research
Giovanni Cennini
Signify Research
Anthony Griths ( ahgriff@bu.edu )
Boston University https://orcid.org/0000-0001-5435-8364
Article
Keywords: SARS-CoV-2, radiation, Signify ultraviolet (UV)-C light, decontamination
DOI: https://doi.org/10.21203/rs.3.rs-65742/v2
License: This work is licensed under a Creative Commons Attribution 4.0 International License. 
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Abstract
The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic has devastated global
public health systems and economies, with over 23 million people infected, millions of jobs and
businesses lost, and more than 800 000 deaths recorded to date. Contact with surfaces contaminated
with droplets generated by infected persons through exhaling, talking, coughing and sneezing is a major
driver of SARS-CoV-2 transmission, with the virus being able to survive on surfaces for extended periods
of time. To interrupt these chains of transmission, there is an urgent need for devices that can be
deployed to inactivate the virus on both recently and existing contaminated surfaces. Here, we describe
the inactivation of SARS-CoV-2 in both wet and dry format using radiation generated by a commercially
available Signify ultraviolet (UV)-C light source at 254 nm. We show that for contaminated surfaces, only
seconds of exposure is required for complete inactivation, allowing for easy implementation in
decontamination workows.
Introduction
Towards the end of 2019, an outbreak of life-threatening pneumonia caused by a novel betacoronavirus
occurred in the Hubei Province of China1. The virus, named severe acute respiratory syndrome
coronavirus 2 (SARS-CoV-2), has since spread across the world at an alarming rate to cause a debilitating
and ongoing pandemic, with only a few islands not reporting any cases to date. While SARS-CoV-2 is
thought to be of zoonotic origin2, intense and extensive human-to-human transmission has mainly been
driven by the inhalation of respiratory droplets and virus-bearing particles spread through the air3, or by
contact with surfaces contaminated with settled droplets4. Although academic institutions and
pharmaceutical organizations worldwide have banded together to develop countermeasures against the
virus, there are still no licensed vaccines or therapeutics available. The disruption of transmission chains
is therefore crucial for managing the outbreak and preventing additional infections.
Ultraviolet (UV) irradiation is an extensively tested, widely used and effective no-contact method for
inactivating viral pathogens5–7. There are three types of UV, including UV-A (315–400nm), UV-B (280–
315nm) and UV-C (100–280nm), of which UV-C is most commonly employed in germicidal applications.
At a wavelength of 254nm, viral inactivation can be attributed to direct UV-C light absorption and
photochemical damage to nucleic acid, leading to the disruption of viral replication8. Despite its wide use,
limited data exists on the effectiveness of UV-C on inactivating wet and dried SARS-CoV-2 on
contaminated surfaces. In particular, the ecacy of UV-C for inactivating SARS-CoV-2 in uids needs to
be determined, as the UV absorbance characteristics of uid constituents may inuence the dose required
to achieve complete viral inactivation.
In this paper, we describe the complete and rapid inactivation of SARS-CoV-2 in both wet and dried
droplets using 254nm UV-C irradiation. Our results suggest that UV-C is an affordable and effective tool
for preventing SARS-CoV-2 contact transmission that can easily be deployed to manage the coronavirus
disease outbreak.
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Results And Discussion
Estimation of viral decay time
To examine the inactivation ecacy of UV-C on SARS-CoV-2, virus was applied to 60 mm plastic dishes
and exposed to UV radiation as either wet or dried droplets for varying amounts of time ranging from 0.8
to 120 seconds. Under a UV-C irradiance of 0.849 mW/cm2, partial inactivation occurred from 0.8
seconds of exposure, while SARS-CoV-2 virus infectivity was reduced to below detectable levels in as few
as 9 seconds for dried virus (Figure 1A) and 4 seconds for wet virus (Figure 1B). Virus inactivation by UV
light is expected to be an exponential process9. Therefore, to estimate the decay time, we used linear
regression methods with single and double exponential decay functions (Figure 1). The single
exponential decay function has the form , while the double exponential function has the
form are the decay times of the linear regressions. In
case of double exponential decay,
f
is the fraction of the viruses that survive the rst decay. For the
analysis, data points were normalized so that the initial condition
t
= 0 corresponds to 100% infectivity
with no irradiance.
In the linear regression of dried droplets, the reduced χ2 for double exponential decay (0.36) was lower
than the one corresponding to single exponential decay (0.52). The R2 for double exponential was higher
than the R2 of the single exponential. Hence, we used the double exponential decay to estimate the decay
times, obtaining In case of wet
droplets, we observed the opposite: the χ2 for the double exponential (1.0) was higher than the one
corresponding to the single exponential (0.8). The R2 for the double exponential and the single
exponential was the same (0.9). We therefore used the single exponential decay as a best t of the data
to estimate the decay time, translating into an average decay time of Within
one standard deviation, the decay times of wet and dried droplets are congruent. This is most likely due
to the limited resolution of the measurements. In addition, this indicates that given the observation limits,
UV-C absorption by media constituents did not signicantly affect virus inactivation at a wavelength of
254 nm.
It should be noted that the experiments for this study were performed under specic and controlled
conditions. Factors such as humidity, textured surfaces and the presence of dust and other particles may
reduce the effectiveness of UV-C and inuence the dose required to achieve complete viral inactivation6. It
is also important to consider the composition of respiratory droplets when evaluating the effectiveness of
254 nm UV-C irradiation. Droplets are likely to be in solvent with a variety of other biological uids such
as respiratory mucus (phlegm) which may include viral glycoproteins, and UV-C absorption of these uids
and particles may result in a reduction in viral inactivation eciencies. The results obtained in this study
should therefore be interpreted as the minimum dose of radiation required to achieve viral inactivation.
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Although beyond the scope of this study, future studies should address the effects of humidity, surface
conformation and the natural matrices in which the virus may exist on the required UV-C inactivation
doses.
Direct exposure of the skin and eyes to 254 nm UV-C light presents a serious health hazard10 and as
such, 254 nm UV-C light should only be used with proper training or where people are not at risk of being
exposed. Forthcoming studies will explore the viral inactivation effectiveness of far UV-C wavelengths
(207-222 nm) that have been proposed to be a safer alternative to 254 nm UV-C light7.
Although several techniques exist for inactivating SARS-CoV-2, the lack of proven effective tools and
interventions have allowed for the unmanageable spread of the virus in the human population. Our
results show that UV-C is a powerful tool that can be applied extensively in a wide range of public
institutions including hospitals, nursing homes, workplaces, schools, airports and shopping centers to
disinfect contaminated equipment and surfaces to prevent and reduce SARS-CoV-2 contact transmission.
Methods
UV-C device
A test apparatus was designed, optimized, fabricated and calibrated to enable accurate and controlled
UV-C treatment of test samples. A collimated beam setup was fabricated based on a dual chamber
construction. The top chamber contains the UV-C light source, the electronic driver, and a shutter system
to control the exposure times of the samples while keeping the lamp output stable. Samples were treated
in the bottom chamber using deep UV-C light generated with a classical Mercury type TUV PLL 35W light
source, generating a peak wavelength at 254 nm. Multiple sensor-based safety measures were applied to
protect the user against incidental exposure to the UV-C radiation. The irradiance level for three different
lamps inside the treatment chamber was measured using a calibrated UV-C sensor system
(Spectroradiometer GL Optic Spectis 5.0 Touch with detector GL Opti Probe 5.1.50), which provided
irradiance patterns and levels from which optimal treatment locations could be deduced.
Virus inactivation procedures
All experiments were performed in the biosafety level 4 laboratory of the National Emerging Infectious
Diseases Laboratories of Boston University. A volume of 100 µl SARS-CoV-2 (7.33 x 103 PFU/ml)
(USA/WA1-2020)11 was plated onto the surface of 60 mm plastic tissue culture dishes (TPP) in 5 µl
aliquots. The virus was allowed to dry for approximately 2 hours on a subset of the dishes while the rest
were processed immediately in the prototype UV-C device. Briey, a pair of dishes (one to be treated and
one control wrapped tightly in aluminum foil) were placed in the center of the device at an irradiance level
of 0.849 mW/cm2, and towards the side of the UV-C device, respectively. The dishes were UV-C-treated for
either 0.8, 2, 3, 4, 5, 6, 9, 15, 30 or 120 seconds, with each treatment time tested in triplicate. Dishes
containing dried virus were treated in the same manner. Following treatment, the wet and dried virus were
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resuspended in 1.9 ml or 2 ml, respectively, of high glucose Dulbecco's Modied Eagle Medium (DMEM)
(Gibco) containing 0.04 mM phenol red, 1 x antibiotic-antimycotic (Gibco), 1 x non-essential amino acids
(Gibco), 1 x GlutaMAX-I (Gibco), 1 mM sodium pyruvate (Gibco) and 2% fetal bovine serum (FBS)(Gibco).
The resuspended virus was then serially diluted from 1 x 100 to 1 x 10-2.5 using half-logarithmic dilutions
for the crystal violet plaque assay, or from 1 x 100 to 1 x 10-5 using 10-fold dilutions for the anti-SARS-
CoV-2 antibody plaque assay. A back-titration of the virus was included for each experiment.
Conrmation of virus inactivation by plaque assay
a) Plaque identication using crystal violet
Vero E6 cells maintained in high glucose DMEM (Gibco) supplemented with 1 x GlutaMAX-I, 1 mM
sodium pyruvate, 10% FBS (Gibco) and 1 x non-essential amino acids (Gibco) were seeded into 6-well
CellBIND plates (Corning) at a density of 8.0 x 105 cells per well. The cells were incubated at 37°C and 5%
CO2 overnight. The media was removed from each well and 200 µl of each dilution prepared from
resuspended virus was added to the respective wells of a 6-well plate. One well containing only DMEM
with 2% FBS was included as a control on each plate. A back-titer of the virus used to prepare the 60 mm
dishes was performed in triplicate by inoculating each well of a 6-well plate with 1 x 10-2 to 1 x 10-6
dilutions of the virus, respectively. Plates were incubated at 37°C and 5% CO2 for 1 hour with intermittent
rocking. Cells were then overlaid with 2 ml of a 1:1 solution of 2.5% Avicel RC-591 (DuPont Nutrition and
Health) and 2 x Temin's Modied Eagle Medium (Gibco) without phenol red, supplemented with 10% FBS
(Gibco), 2 x antibiotic-antimycotic (Gibco) and 2 x GlutaMAX-I (Gibco). The cells were incubated at 37°C
and 5% CO2 for 2 days. Plates were xed in 10% neutral buffered formalin (ThermoFisher Scientic),
followed by staining with 0.2% Gentian Violet (Ricca Chemical) in 10% neutral buffered formalin. The
number of plaques per virus dilution were determined by eye and used to calculate the titer of the virus
using the following formula:
Virus titer in PFU/ml = Number of plaques / (virus dilution in well x volume plated in ml)
Statistical analysis
The statistical package Microcal Origin® was used to analyze the data. A detailed explanation of the
statistical methods used is provided with the results.
Data availability
Additional data supporting the ndings of this study are available from the corresponding author upon
request.
Declarations
Acknowledgements
Page 6/7
The authors acknowledge Lauren E. Malsick for technical assistance. This work was supported by
Signify Research.
Author Contributions
AG, SND, NS and LGAM conceptualized the study design. SND, NS, LGAM and RIJ performed the
experiments. NS, SND, LGAM, GC and AG analyzed the data and wrote the rst draft of the paper with
input from DB, MdS and WW. All authors read, revised and approved the nal paper.
Competing interests
AG, NS, LGAM, SND, and RIJ have no competing interests to declare. MdS, GC, DB, and WW are
employees of Signify Research.
Materials and correspondence
Correspondence and materials requests should be addressed to AG.
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Figures
Figure 1
Reduction in infectivity of SARS-CoV-2 after exposure to UV-C irradiation. The virus was exposed to UV-C
as dried droplets (A) or wet droplets (B). Each set of data (dry samples and wet samples) shows a
decrease of the remaining infectivity as a function of time, normalized to 1. Blue lines indicate single
exponential decay functions while red lines indicate double exponential decay functions.
... UVGI applications use low-pressure mercury discharge lamps that emit shortwave ultraviolet-C (UV-C) radiation. UV-C radiation inactivates viral pathogens by damaging their deoxyribonucleic acid (DNA) [129,130,131]. ...
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Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV
  • M E R Darnell
Darnell, M.E.R. et al. Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV. J Virol Methods 121, 85-91, https://doi.org/10.1016/j.jviromet.2004.06.00 (2004).