Photochemistry and Photobiology, 2020, 96: 731–737
Estimated Inactivation of Coronaviruses by Solar Radiation With Special
Reference to COVID-19
Rapid Communication
Jose-Luis Sagripanti1* and C. David Lytle2
1US Department of Defense Ringgold Standard Institution-US Army, RETIRED, Annapolis, MD, USA
2Department of Health and Human Services Ringgold Standard Institution – Food and Drug Administration, RETIRED,
Albuquerque, NM, USA
Received 19 May 2020, accepted 1 June 2020, DOI: 10.1111/php.13293
ABSTRACT
Using a model developed for estimating solar inactivation of
viruses of biodefense concerns, we calculated the expected
inactivation of SARS-CoV-2 virus, cause of COVID-19 pandemic,
by articial UVC and by solar ultraviolet radiation in
several cities of the world during different times of the year.
The UV sensitivity estimated here for SARS-CoV-2 is compared
with those reported for other ssRNA viruses, including
inuenza A virus. The results indicate that SARS-CoV-2
aerosolized from infected patients and deposited on surfaces
could remain infectious outdoors for considerable time during
the winter in many temperate-zone cities, with continued
risk for re-aerosolization and human infection. Conversely,
the presented data indicate that SARS-CoV-2 should be inactivated
relatively fast (faster than inuenza A) during summer
in many populous cities of the world, indicating that
sunlight should have a role in the occurrence, spread rate
and duration of coronavirus pandemics.
INTRODUCTION
The current (2019-2020) COVID-19 world pandemic is caused
by a member of the Coronaviridae family [Reviewed in (1)].
Coronaviruses have a lipid-containing envelope with the genome
consisting of a single-stranded, positive-sense RNA genome that
is not segmented (2–5). Coronaviruses have the largest genomes
of all ssRNA viruses which will become of relevance latter in
this work. In the absence of pandemics, coronaviruses cause
about 15–20% of all upper respiratory infections in humans (6).
Previous pandemics like Severe Acute Respiratory Syndrome
(caused by SARS-CoV during 2002–2003), and Middle East
Respiratory Syndrome (caused by MERS-CoV during 2012)
indicate that pandemics caused by coronaviruses should be
expected to occur with frequency (7,8). Additional coronaviruses
are known to cause disease in animals closely associated to
humans like cat and dog, rat and mouse, cow, swine, chicken
and turkey (6).
Although clusters of infected family members and medical
workers have conrmed direct, person-to-person transmission
(9), the rapid expansion of COVID-19, that progressed
unquenched even after quarantine of nearly one-third of the
world population and major social distancing measures, suggests
that an environmental component (with the virus remaining
infectious outside the host) plays a role in disease transmission.
Of relevance here is the amount of infectious virus present in the
aerosolized droplets produced by COVID-19 symptomatic
patients or nonsymptomatic carriers. This amount is not well
established for coronaviruses, but it has been reported that nasal
secretions contain up to 107 infectious inuenza viral particles
per ml (10), from which aerosolized droplets generated by
coughing, sneezing and talking can contain several hundred
infectious virions (11). These micro droplets can reach distances
of 12.5 meters (over 40 feet, (12)). SARS-CoV has been reported
to persist on contaminated surfaces with risk of disease transmission
for up to 96 h (13) and other coronaviruses for up to 9 days
(14). SARS-CoV-2 persisted viable from 3 h to 3 days depending
on the type of surface on which it was deposited (15). Inuenza
virus was readily re-aerosolized by sweeping oors without
much loss in infectivity (16). It must be assumed that SARSCoV-
2 will be re-aerosolized in a similar manner.
Three main physical factors generally considered with a
potential effect on virus persistence outdoors, include temperature,
humidity and the contribution of sunlight. The survival of
inuenza virus, a member of the Orthomyxoviridae family, also
with ssRNA and a lipid–containing envelope, only varied up to
9% when the relative humidity changed between 50% and 70%
(17). Rather extreme changes in relative humidity between 15%
and 90% varied survival of inuenza 12.5–fold [1.1 Log10, (18)].
In these studies, virus survival was even less inuenced by
changes in temperature. A recent study where virus infectivity
was corrected by aerosol losses and natural decay, demonstrated
that aerosolized inuenza A virus remained equally infectious at
all relative humidity tested, ranging from 23% to 98% (19). In
agreement with the relatively small effect of humidity and temperature
on inuenza virus inactivation, epidemiological studies
concluded that the mortality increase in winter was largely independent
of temperature and humidity (20,21).
If the limited role of relative humidity and temperature (within
the range encountered in the environment) reported for inuenza
A parallels that for SARS-CoV-2 then, the effect of articial and
natural UV radiation on SARS-CoV-2 inactivation should be preeminent.
The pre-eminent effect indoors of germicidal UV
*Corresponding author email:
gripan889@gmail.com (Jose-Luis Sagripanti) (UVC, 254 nm) radiation is clearly conrmed by a report
© 2020 American Society for Photobiology
731
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whereby inactivation of air-borne virions by UV radiation virtually
prevented the spread of inuenza among patients in a veterans
hospital, during the same time that an epidemic of inuenza
ravaged similar patients in nearby nonirradiated rooms (22).
There are published reports indicating that very high doses of
UVC are effective for inactivating SARS-CoV-2 or SARS-CoV
that had been added to different blood products or remaining in
virus culture medium (23–28) but there is no data on the viral
sensitivity to UVC in UV-transparent liquids or in absence of
protective substances, as needed to estimate UVC sensitivity.
Nor is there information for UVC inactivation of the virus suspended
in aerosols or deposited on surfaces as needed for environmental
risk assessment.
Ultraviolet radiation in sunlight is the primary virucidal agent
in the environment (29–31). This notion is supported by the correlation
found in Brazil between increased inuenza incidence in
hospital admission records and solar UV-blocking by smoke during
the burning season (32). The reports on inuenza A warrant
the present study to estimate UV sensitivity of SARS-CoV-2 and
its possible role in the COVID-19 pandemic.
The purpose of this study was twofold, (1) to estimate the
sensitivity of SARS-CoV-2 to inactivation by germicidal UV
(UVC) and (2) to predict the inactivation of the virus by the
UVB in sunlight for various populous cities of the world at different
times of the year. These goals were achieved by utilizing
a model developed for biodefense purposes for estimating solar
UVB inactivation of dangerous viruses (30). This methodology
has been validated with Ebola and Lassa viruses (33). The model
has also been used to estimate inactivation of inuenza viruses at
various times in numerous locations in the U.S. and globally
(34).
Estimation of the time required for inactivation of 90% and
99% of infectious virus reported here should be useful in evaluating
the persistence of SARS-CoV-2 in environments exposed
to solar radiation.
MATERIALS AND METHODS
We estimated SARS-CoV-2 virus UV (254 nm) sensitivity and inactivation
at different U.S. and global locations by an approach originally developed
to predict the survival of viruses of interest in biodefense (30) and later
employed to estimate persistence of inuenza A virus (34).
SARS-CO V2 virus UV254 sensitivity. The UVC sensitivity is reported
here as D37 which corresponds to the UV uence that produces, on
average, one lethal hit to the virus, resulting in 37% survival. D37 equals
the reciprocal of the slope on the semi-logarithmic graph of viral survival
versus dose and can be calculated by dividing the uence that results in
1 Log10 reduction of virus load by 2.3 (the natural logarithmic base). A
lower value of D37 indicates a higher sensitivity to inactivation by UV
radiation. Comparison of a virus of unknown UVC sensitivity to that of
other viruses of similar genomic structure allows an estimate to be
determined (30). An important part of the method is the fact that UVC
sensitivities of viruses depends proportionally on genome size, especially
with single-stranded RNA or DNA, that is, the larger the genome
“target”, the more sensitive (and lower D37). This results in the product
of the genome size and the D37, dened as size normalized sensitivity
(SnS), being relatively constant for a given type of viral genome (30)
and it is used in this study to compare viruses with ssRNA genomes.
This approach has been used successfully to estimate the UVC
sensitivities of Ebola and Lassa viruses, later conrmed experimentally in
the laboratory (33), thus validating the method.
Solar intensity at different locations and times of year. Solar UVB
ux measured by the USDA UVB Monitoring and Research Program
(35) have been used in the development and testing of the method (30).
Maximum daily solar UVB uence values for the selected locations at
specic times of year have been presented in a previous article predicting
the inactivation of inuenza A by solar UVB (34). Those daily solar ux
values were normalized using a virucidal action spectrum to 254 nm
equivalent levels (30). Whereas the total UV254 equivalent uence per
full day was previously used in the inuenza A inactivation study (34),
the ux values at solar noon are preferable and are used here because
they are essentially constant during two hours (36,37). It has been
previously determined that 35% of the total daily UVB occurs in the
two-hour period (120 min) around solar noon (37). Thus 35% of the total
daily UVB uence divided by 120 min yields the noontime UVB ux
(in J m2 min1) at the locations and times of the year presented in
Tables 2 and 3. It should be noted that the solar UVB ux used in the
present study assumed no atmospheric inuence, whether by haze, clouds
or air pollution. Also, there was no correction for an increase in the solar
virucidal effect due to the elevation of the urban sites (38).
RESULTS
UVC sensitivity of SARS-CoV-2
In Table 1 we compare the genomic and UV254 characteristics of
SARS-CoV-2 (causing COVID-19) with those of other coronaviruses
and viruses that have similar nucleic acid composition.
The rst three coronaviruses cause disease in humans. Studies
with MHV and EtoV have found similar values for D37s (36,39).
Therefore, a reasonable estimate for the D37s for the SARSs and
MERS-CoV viruses would be 3.0 J m2. Comparison with other
ssRNA viruses yields a similar D37 value. Since the inuenza A
genomes are 2.2 times shorter than those of the coronaviruses, it
is further reasonable that the coronaviruses (larger UV targets)
would be at least twice as sensitive to UVC; the reciprocal ratio
of the genome sizes times the D37 for the inuenza viruses yields
an estimated D37 for SARS-CoV-2 of 4.7 J m2 . When a similar
comparison is done with the viruses of the other ssRNA families
in Table 1, the median value for the SARS-CoV-2 D37 was
5.0 J m2. The D37 value of 3.0 J m2 was used in the following
calculations because it follows from values derived directly
from members of the same Coronaviridae family; D10
(6.9 J m2) was used as it represents 10% survival (90% inactivation).
It may be useful to estimate the solar exposure for 99% virus
inactivation (1% survival) or for even lower levels of survival.
Because the material in aerosols created by COVID-19 patients
and carriers may shield the virus from the UV as has been
shown in laboratory experiments with viruses in culture medium,
the virus survival curves indicate that the virus apparently
becomes less UV sensitive (33,36,40–42). This resulted in a
change of slope of approximately 4-fold in experiments with
Ebola, Lassa and inuenza A viruses and affected several percent
of the virus population (33,42). Therefore, for survival beyond
10%, a UV uence of 4 times the chosen D
10 (28 J m2) was
assumed. This value was used to estimate the solar exposure
needed for 99% inactivation. Assuming that the survival curve
maintains that 4-fold greater UV resistance at lower survival
levels, 99.9% inactivation (disinfection level) would require
56 J m2 ; sterilization level inactivation (10-6 survival) would
require 140 J m2.
Estimated time for inactivation of SARS-Co V-2 virus
Table 2 shows reported solar virucidal ux at solar noon together
with the estimated minutes of sunlight exposure needed at various
populous North American metropolitan areas to inactivate
90% of SARS-CoV-2. The (+) sign in Table 2 indicates that
99% of SARS-CoV-2 may be inactivated within the two hours
732 Jose-Luis Sagripanti and C. David Lytle
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period around solar noon during summer in most US cities
located south of Latitude 43°N. Also 99% of the virus will be
inactivated during two hours midday in several cities south of
latitude 35°N in Fall, but only Miami and Houston will receive
enough solar radiation to inactivate 99% of the virus in spring.
During winter, most cities will not receive enough solar radiation
to produce 90% viral inactivation during 2-hour midday exposure
(underlined values in Table 2).
Table 3 presents germicidal solar ux values and resulting
inactivation of SARS-CoV-2 for populous metropolitan areas on
other continents. The values in Tables 2 and 3 clearly illustrate
that SARS-CoV-2 in environments exposed to sunlight will be
differentially inactivated in different cities and at different times
of the year. For example, at winter solstice (December, in the
northern hemisphere), just at the beginning of the COVID-19
pandemic, virus exposed to full midday sunlight would be
reduced by at least 90% (1 Log10) during 22 min in Mexico
City, and will be receiving enough germicidal solar ux to inactivate
99% of virus as indicated by (+) in Table 3. A 90% inactivation
of SARS-CoV-2 in December should have taken
considerably longer time in Shanghai (99 min), and Cairo
(86 min). Nearly full virus persistence should occur in winter
(December) in the European cities listed in Table 3 (where
COVID-19 was severe). Of course, the same trend applies to the
Southern Hemisphere where winter begins in June and 90% of
SARS-CoV-2 should be inactivated in 41 min in Sao Pablo (Brazil),
but not within the 2 hours solar noon period in Buenos
Aires (Argentina) or Sydney (Australia) in the incoming winter
season.
DISCUSSION
The transmission of viral infections and evolution of pandemics
is a multi-factorial process involving, among others, properties of
the viral agent, health condition of the host and available health
care, viral inactivation in the environment, social dynamics and
political decisions. It is well known that there is direct transmission
of infectious virions by inhalation of contaminated aerosols
exhaled, coughed or sneezed from infected persons, allowing for
little time and opportunity for environmental viral inactivation,
unless the virions settle on some surface. Although direct (person-
to-person) transmission is important between nearby individuals
(9), it is remarkable that the COVID-19 pandemic
progressed at a sustained rate even after one-third of the world
population was in quarantine or in-house lock-down (50). The
rapid progression of the COVID-19 pandemic, in spite of greatly
hindered direct transmission, supports elucidating the relevance
of indirect infection through aerosolized virus, contact with contaminated
surfaces and other fomites, and the inactivation
thereof.
Changes in relative humidity and ambient temperature have
been reported as having a rather limited effect on environmental
virus survival and disease transmission (17–21). In contrast,
UVC radiation has considerable virucidal effect (22). The
methodology employed in the present study has been used previously
to estimate the UVC sensitivity of Lassa virus and other
viruses of relevance in biodefense (30). A close agreement was
obtained between UVC D37 values predicted for Lassa virus
(member of the Arenavirus family) (13 J m2, table 4 in Ref 30)
and measured years later in the laboratory (16 J m2) (33).
These results suggest that the accuracy of the methodology used
here to estimate the UV sensitivity of the SARS-CoV-2 virus
from data obtained for members of the same family may be
within 20%.
The relevance of sunlight in viral inactivation contrasts with
and is supported by the (1) long-term persistence in darkness of
smallpox (an Orthopoxivirus) in scabs and surfaces (51), (2) with
laboratory results where pathogenic viruses in the dark survived
Table 1. UVC sensitivity of SARS-CoV-2 and selected viruses.*
Virus family Genome Size† (Knt)
Measured‡
D37 (J m2)
SNS§
(J m2 Knt)
Predicted
D37 (J m2) References
Coronaviridae
SARS-CoV-2 ssRNA+ 29.8 89 3.0
SARS-CoV ssRNA+ 29.7 89 3.0
MERS ssRNA+ 30.1 89 3.0
MHV ssRNA+ 31.6 2.9 91 (36)
EToV ssRNA+ 28.5 3.1 88 (39)
Togaviridae
SINV ssRNA+ 11.7 19 220 (43)
VEEV ssRNA+ 11.4 23 260 (44)
SFV ssRNA+ 13.0 7.2 94 (39)
Paramyxiviridae
NDV ssRNA- 15.2 11-13.5 170-210 (45,46)
MeV ssRNA- 15.9 8.8-10.9 140-170 (47)
Orthomyxoviridae
FLUAV ssRNA- 13.6
Melbourne H1N1 10.2 139 (48)
NIB-4 H3N2-3 11 150 (40)
NIB-6 H1N1 9.6 131 (40)
ISAV ssRNA- 14.5 4.8 70 (49)
Rhabdoviridae
RABV ssRNA- 11.9 4.3 51 (39)
*Selected viruses of different genetic Families having ssRNA as the genome.
†
Size of the genome expressed as thousands of nucleotide bases
(Knt).
‡
UVC uence that causes one lethal event per virus on average, resulting in 37% survival.
§
Size-normalized sensitivity dened as the product of
the D37 and the genome size in thousands of bases is relatively constant for a given genome type, but can be vastly different for different genomic types.
If the size and genome type is known for an untested virus, the D37 can be predicted from the SNS.
Photochemistry and Photobiology, 2020, 96 733
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for much longer times (T37 [time to 37% survival)]between 15
and 43 h for the different viruses studied) (52), and (3) with the
rapid inactivation of vaccinia virus exposed to direct sunlight or
simulated solar UVB (42).
The solar germicidal ux shown in Tables 2 and 3 allows
estimating SARS-CoV-2 inactivation outdoors for the cities presented,
as well as for almost any other location for which latitude
is known, from sun exposure under clear skies. Modeling of
viruses suspended in the atmosphere indicates that the diffuse
(scatter) component of sunlight may still have approximately
50% of the virucidal efcacy exerted by direct solar radiation
(38,53). These ndings demonstrate that viral inactivation by
sunlight continues outdoors (albeit at half the rate or less) even
in the shade or in polluted air or partially cloudy days.
Although the solar zenith angle at a given location is the same
at the spring and fall equinoxes, the solar UV radiation received
in the northern hemisphere was generally greater in the fall than
in the spring, except for the location furthest south, Hawaii (latitude
19.5 °N). Data for Alexandra, New Zealand, in the southern
hemisphere where the seasons are reversed, demonstrated the
same trend with spring UVB radiation being lower than fall UV
radiation (data not shown). This differential solar germicidal uence
between spring and summer has been previously discussed
(30).
Data for the COVID-19 pandemics from the World Health
Organization and from Johns Hopkins’ Center for Systems
Science and Engineering (as of May 7, 2020) indicates that of
the 30 countries with highest infections per million inhabitants,
28 were north of the Tropic of Cancer (the two exceptions being
Qatar and Mayotte) (54). Any correlation between solar ux during
December- March 2019/20, (when COVID-19 was in expansion)
and infection rate is limited by inaccuracy and availability
of testing, different numbers of infected travelers, as well as vast
differences on each country demographics and response. However,
the statistical data [as of May 7 2020 (54)] suggest that
COVID-19 may have progressed differently in countries at northern
latitudes where it was winter and sun exposure was limited
at the onset of the pandemic, than in countries in the southern
latitudes where summer sunlight was abundant.
Considering that SARS-CoV-2 is three times more sensitive
to UV than inuenza A (as presented in Table 1 and discussed
in RESULTS) it should be inferred that sunlight should have an
effect on coronaviruses transmission at least similar to that previously
established for the evolution of inuenza epidemics
(22,32) If we accept a possible virucidal role of sunlight during
coronavirus pandemics, then forcing people to remain indoors
may have increased (or assured) contagion of COVID-19 among
same house-hold dwellers and among patients and personnel
inside the same hospital or geriatric facilities. In contrast, healthy
people outdoors receiving sunlight could have been exposed to
lower viral dose with more chances for mounting an efcient
immune response. This argument supports considering the results
of two opposed containment approaches to deal with the
COVID-19 crisis.
Almost all countries and territories affected with COVID-19
have closed their borders, mandated the use of masks and promoted
social distancing. By 26 March, 2020, 1.7 billion people
worldwide were under some form of lock-down, which increased
to 3.9 billion people by the rst week of April, amounting to
more than half of the world’s population (55). Schools, universities
and colleges have closed either on a nationwide or local
basis in 177 countries, affecting approximately 98.6 percent of
the world’s student population (56). In addition to these measures,
some countries (for example: Italy, Spain, the UK, Peru,
Chile, Argentina and Rep South Africa) implemented nationwide
strict quarantine and in-house lock-down measures, often
enforced by police, that decreased the time individuals could
spent outdoors thus preventing potential exposure to sunlight.
Most countries (like USA, Finland and Brazil) implemented
regional less stringent lock-down measures at varying degrees. A
third group of countries (for example: Sweden, Belorussia, Nicaragua,
Uruguay, Indonesia, South Korea and Namibia) did not
mandate lock-downs that prevented healthy individuals to remain
outdoors with potential exposure to sunlight (57). These “ unlock”
countries have not enforced any strict lock-downs but have
Table 2. Calculated maximum* virucidal (254-nm equivalent†) UV ux
during two-hour period around solar noon for populous metropolitan
areas in North America at specied times of year. Effectiveness estimated
for inactivation of SARS-CoV-2 virus
Metropolitan
area Latitude
Solar virucidal UV ux (J/m2
254
2/min)‡ /Time
for 90% Infectivity reduction (min)§
Summer
Solstice
Equinox
Winter
Spring Fall Solstice
Miami, FL 25.8 °N 0.51/14 +k 0.34/20 + 0.41/17 + 0.13/53
Houston,
TX
29.8 °N 0.44/16 + 0.25/28 + 0.33/21 + 0.08/86
Dallas, TX 32.8 °N 0.39/18 + 0.20/34 0.28/25 + 0.06/115
Phoenix, AZ 33.4 °N 0.39/18 + 0.19/36 0.26/27 + 0.05/138¶
Atlanta, GA 33.7 °N 0.39/18 + 0.18/38 0.26/27 + 0.05/138
Los
Angeles,
CA
34.1 °N 0.38/18 + 0.18/38 0.26/27 + 0.05/138
San
Francisco,
CA
37.7 °N 0.34/20 + 0.13/53 0.20/34 0.03/230
Washington,
D.C.
38.9 °N 0.33/21 + 0.12/57 0.19/36 0.02/ 300
Philadelphia,
PA
39.9 °N 0.32/22 + 0.11/63 0.18/38 0.02/ 300
New York
City, NY
40.7 °N 0.32/22 + 0.10/69 0.17/41 0.02/ 300
Chicago, IL 41.9 °N 0.31/22 + 0.10/69 0.16/43 0.01/ 00
Boston, MA 42.3 °N 0.30/23 + 0.09/77 0.15/46 0.01/ 00
Detroit, MI 42.3 °N 0.30/23 + 0.09/77 0.15/46 0.01/ 00
Toronto,
Ontario
43.6 °N 0.29/24 0.08/86 0.14/49 0.01/ 300
Minneapolis,
MN
45.0 °N 0.28/25 0.07/99 0.13/53 0.01/ 300
Seattle, WA 47.6 °N 0.26/27 0.06/115 0.11/63 0.01/>300
*Maximum solar exposure with no clouds, haze, air pollution or shadows
to reduce exposure, independent of site elevation.
†
Obtained using the
virus inactivation action spectrum normalized to unity at 254 nm
(30).
‡
Methodology: Maximum daily solar UVB uence values for the
selected locations at specic times of year have been represented in
Tables 1 and 2 in the previous article on predicted Inuenza inactivation
by solar UVB (34). 35% of the total daily UVB uence divided by
120 min yields the noontime UVB ux in J m2 min1 at the locations
and times in Tables 2 and 3.
§
The UVB uence D10 to inactivate SARSCoV-
2 90% (10% survival) was estimated as 6.9 J m2 .
k
"+" denotes that
under ideal conditions, solar UV could inactivate SARS-CoV-2 99% (1%
survival) during 2-hour period around solar noon. Four times the D10
was chosen to account for the likely biphasic inactivation due to protective
elements surrounding the virus.
¶
Underlined values indicate solar
UVB is likely not enough to inactivate SARS-CoV-2 90% (10% survival)
during two-hour period around solar noon.
734 Jose-Luis Sagripanti and C. David Lytle
Printed by [Wiley Online Library - 093.034.091.251 - /doi/epdf/10.1111/php.13293] at [14/04/2021].
rather implemented large-scale social distancing, face mask wearing
measures and/or instituted quarantine mainly for travelers
and infected patients (57).
Analyzing the value (if any) of whole-population quarantine
or in-house lock-down of healthy individuals is beyond the scope
of the present work. However, the freely available epidemiological
data (as of May 29, 2020 (54)) demonstrates that lock-down
measures preventing healthy individuals from remaining outdoors
have not resulted in an obvious and statistically signicant difference
on infections per million inhabitants when compared to
countries where healthy individuals were free to stay outdoors,
with potential exposure to sunlight radiation. If lock-down of
healthy citizens may not be determinant as these statistics suggest,
then the potential role of being outside exposed to direct or
scattered sunlight in COVID-19 pandemic should not be underestimated.
CONCLUSION
The data presented estimates the sensitivity to UVC (254 nm) of
the SARS-CoV-2 virus with a D37 of 3.0 J m 2 , corresponding
to 90% inactivation (D10) after a dose of 7 J m2 . Inactivation
of 99% viral load (D1) was estimated to be 28 J m2 (49 D10)
due to the biphasic nature of the virus inactivation curve found
for other viruses shielded by culture media and other components
that accompany virus infections.
90% or more of SARS-CoV-2 virus will be inactivated after
being exposed for 1134 min of midday sunlight in most US and
world cities during summer. In contrast, the virus will persist
infectious for a day or more in winter (December–March), with
risk of re-aerosolization and transmission in most of these cities.
Although latitude, population size, public health and control
measures vastly vary among countries, the viral persistence estimated
here for cities at northern latitudes where COVID-19
expanded rapidly during winter 2019–2020 and relatively higher
viral inactivation in more southern latitudes receiving high solar
radiation during the same period, suggests an environmental role
for sunlight in the COVID-19 pandemic.
Acknowledgements—The authors appreciate the encouragement to initiate
this study received from Ms. Jessica Seigel (journalist, New York
University).
Table 3. Calculated maximum* virucidal (254-nm equivalent†) UV ux for two-hour period around solar noon for selected major world cities at speci-
ed times of year: Effectiveness estimated for inactivation of SARS-CoV-2 virus
City Latitude
Solar virucidal UV ux (J/m2
254
2/min) ‡/Time for 90% Infectivity reduction (min)§
Summer Solstice
Equinox
Spring Fall Winter Solstice
Central and South America
Bogota, Colombia 4.6 °N 0.64 #/11+k 0.64/11+ 0.64/11+ 0.64/11+
Mexico City, Mexico 19.5 °N 0.64/11+ 0.62/11+ 0.62/11+ 0.31/22+
S
~
ao Paulo, Brazil 23.3 °S 0.55/13+ 0.40/17+ 0.48/14+ 0.17/41
Buenos Aires, Argentina 34.6 °S 0.37/19+ 0.17/41 0.24/29 0.04/172¶
Europe
Barcelona, Spain 41.4 °N 0.31/22+ 0.10/69 0.16/43 0.01/>300
Paris, France 48.9 °N 0.25/28+ 0.05/138¶ 0.10/69 0.00/>300
London, UK 51.5 °N 0.23/30 0.04/173 0.09/77 0.00/>300
Moscow, Russia 55.7 °N 0.20/34 0.03 /230 0.07/99 0.00/>300
Middle East
Baghdad, Iraq 33.3 °N 0.39/18+ 0.19/36 0.26/27+ 0.05/138
Tehran, Iran 35.7 °N 0.36/19+ 0.16/43 0.23/30 0.04/172
Istanbul, Turkey 41.0 °N 0.31/22+ 0.10/69 0.16/43 0.02/>300
Africa
Kinshasa, Congo 4.3 °S 0.64/11+ 0.64/11+ 0.64/11+ 0.64/11+
Lagos, Nigeria 6.4 °N 0.64/11+ 0.64/11+ 0.64/11+ 0.64/11+
Khartoum, Sudan 15.6 °N 0.64/11+ 0.64/11+ 0.64/11+ 0.32/22+
Cairo, Egypt 30.0 °N 0.43/16+ 0.25/28+ 0.32/22+ 0.08/86
Asia
Mumbai (Bombay), India 19.0 °N 0.64/11+ 0.62/11+ 0.62/11+ 0.32/22+
Shanghai, China 31.2 °N 0.42/16+ 0.22/31 0.31/22+ 0.07/99
Seoul, Republic of Korea 33.5 °N 0.38/18+ 0.19/36 0.26/27+ 0.05/138
Tokyo, Japan 35.7 °N 0.36/20+ 0.16/43 0.23/30 0.04/172
Australia
Sydney, Australia 33.9 °S 0.38/18+ 0.18/38 0.26/27+ 0.05/138
*Maximum solar exposure with no clouds, haze, air pollution or shadows to reduce exposure, independent of site elevation.
†
Obtained using the virus
inactivation action spectrum normalized to unity at 254 nm (30).
‡
Methodology: Maximum daily solar UVB uence values for the selected locations at
specic times of year have been represented in Tables 1 and 2 in the previous article on predicted Inuenza inactivation by solar UVB (34). 35% of the
total daily UVB uence divided by 120 min yields the noontime UVB ux in J m2 min1 at the locations and times in Tables 2 and 3.
§
The UVB uence
D10 to inactivate SARS-CoV-2 90% (10% survival) was estimated as 6.9 J m2 .
k
Under ideal conditions, solar UV could inactivate SARS-CoV-2
99% (1% survival) during 2-h period around solar noon. Four times the D10 was chosen to account for the likely biphasic inactivation due to protective
elements surrounding the virus.
¶
Underlined values indicate solar UVB is likely not enough to inactivate SARS-CoV-2 90% (10% survival) during twohour
period around solar noon.
#
Flux values above 0.62 are likely underestimates. Therefore, the time for 90% and 99% inactivation are possibly overestimates.
Photochemistry and Photobiology, 2020, 96 735
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REFERENCES
1. Harapan, H., N. Itoh, A. Yuka, W. Winardi, S. Keam, H. Te, D.
Megawati, Z. Hayati, A. L. Wagner and M. Mudatsir (2020) Coronavirus
disease 2019 (COVID-19) A literature review. J. Infect Public
Health. 13(5), 667–673.
https://doi.org/10.1016/j.jiph.2020.03.019
2. Sturman, L. S. and K. V. Holmes (1983) The molecular biology of
corona viruses. Adv. Virus Res. 28, 35–112.
3. Van Regenmortel, M. H. V., C. M. Fauquet, D. H. L. Bishop, E. B.
Carstens, M. K. Estes, S. M., Lemon, D. J., McGeogh, J., Maniloff,
M. A., Mayo, C. R., Pringle and R. B., Wickner (2000) Classication
and nomenclature of viruses. Seventh report of the International
Committee on Taxonomy of viruses. Academic Press, San Diego,
CA.
4. Knipe Condit, R. C. (2001) Principles of virology. In Fields Virology
(Edited by D. M. Knipe and P. M. Howley), 4th ed. Vol 1, Chapter
2, pp. 19–51. Lippincot Williams & Wilkins, Philadelphia, PA.
5. Woo, P. C. Y., S. K. P. Lau, C-m Chu, K-h Chan, Y. H-w Tsoi, B.
H. L. Huang, R. W. S. Wong, J. J. Cai Poon, L. L. M. W-k Luk, S.
S. Y. Poon, Y. Wong, , J. S. M. Peiris and K.-Y. Yuen (2005) Characterization
and complete genome sequence of a novel coronavirus,
Coronavirus HKU1, from patients with pneumonia. J. Virol. 79,
884–895.
6. Holmes, K. V. (1990) Coronaviridae and their replication. In Fields
Virology (Edited by B. N. Fields and D. M. Knipe), 2nd edn. Vol 1,
Chapter 29, pp. 841–856. Raven Press, New York, NY
7. Peiris, J. S. M., S. T. Lai, L. L. M. Poon, Y. Guan, L. Y. C., Yam,
W., Lim, J., Nicholls, W. K. S., Yee, W. W., Yan, M. T., Cheung,
V. C. C., Cheng, K. H., Chan, D. N. C., Sang, R. W. H., Yung, T.
K., Ng, K. Y., Yuen and members of the SARS study group (2003)
Coronavirus as a possible cause of severe acute respiratory syndrome.
Lancet 361, 1319–1325.
8. Ramadan, N. and H. Shaib (2019) Middle east respiratory syndrome
corona virus (MERS-CoV): a review. Germas 9, 35–42.
9. Chan, J. F., S. Yuan, K. H. Kok, K. K. To, H. Chu, J. Yang, F.,
Xing, J., Liu, C. C., Yip, R. W., Poon, H., Tsoi, S. K., Lo, K., Chan,
V. K., Poon, W., Chan, J., Daniel Ip, J., Cai, V. C., Cheng, H.,
Chen, C. K., Hui and K. Y., Lancet (2020) A familial cluster of
pneumonia associated with the 2019 novel corona virus indicating
person-to-person transmission: a study of a familial cluster. Lancet.
10. Couch, R. B. (1995) Medical Microbiology, pp. 1–22. University of
Texas Medical Branch, Galveston.
11. Gustin, K. M., J. M. Katz, T. M. Tumpey and T. R. Maines (2013)
Comparison of the levels of infectious virus in respirable aerosols
exhaled by ferrets infected with Inuenza viruses exhibiting diverse
transmissibility phenotypes. J Virol. 87(14), 7864–7873.
12. Reiling, J. (2000) Dissemination of bacteria from mouth during
speaking coughing and otherwise. J. Am. Med. Assoc. 284, 156.
13. Kramer, A., I. Schwebke and G. Kampf (2006) How long do nosocomial
pathogens persist on inmate surfaces? A systematic review.
BMC Infect Dis. 6, 130.
14. Kampf, G., D. Todt, S. Pfaender and E. Steinmann (2020) Persistence
of corona viruses on inmate surfaces and its inactivation with
biocidal agents. J. Hosp. Infect. 104(3), 246-251.
https://doi.org/10.
1016/j.jhin.2020.01.022
15. Van Doremalen, N., T. Bushmaker, D. H. Morris, M. G. Holbrook,
A., Gamble, B. N., Williamson, A., Tamin, J. L., Harcourt, N. J.,
Thornburg, S. I., Gerber, J. O., Lloyd-Smith, E., de Wit and V. J.,
Munster (2020) Aerosol and surface stability of SARS-CoV-2 as
compared to SARS-CoV-1. N Engl J Med.
https://doi.org/10.1056/
NEMJc2004973
16. Loosli, C. G., H. M. Lemon, O. H. Robertson and E. Appel (1943)
Experimental airborne inuenza infection. I. Inuence of humidity
on survival of virus in air. Proc. Soc. Exp. Biol. 53, 205–206.
17. Schaffer, F. L., M. E. Soergel and D. C. Straube (1976) Survival of
airborne inuenza virus: effects of propagating host, relative humidity,
and composition of spray uids. Arch. Virol. 51, 263–273.
https://doi.org/10.1056/NEJMc2004973
18. Hemmes, J. H., K. C. Winkler and S. M. Kool (1960) Virus survival
as a seasonal factor in inuenza and poliomyelitis. Nature 188, 430–
431.
19. Kormuth, K. A., K. Lin, A. Prussin, E. P. Vejerano, A. J., Tiwari, S.
S., Cox, M. M., Myerburg, S. S., Lakdawala and L. C., Marr (2018)
Inuenza virus infectivity is retained in aerosols and droplets
independent of relative humidity. J. Infect Dis. 218(5), 739–747.
https://doi.org/10.1093/infdis/jiy221
20. Tiller, H. E., J. W. Smith and C. D. Gooch (1983) Excess deaths
attributable to inuenza in England and Wales. Im. J. Epidemiol. 12,
344–352.
21. Reichert, T. A., L. Somonsen, A. Sharma, S. A. Pardo, D. Fedson
and M. A. Miller (2004) Inuenza and the winter increase in mortality
in the United States, 1959–1999. Am. J. Epidemiol. 180(5), 492–
502.
22. McLean, R. L. (1956) Comments on reducing inuenza epidemics
among hospitalized veterans by UV irradiation of droplets in the air.
Amer. Rev. Respiratory Dis. 83(Suppl), 36–38.
23. Duan, S.-M., X.-S. Zhao, R.-F. Wen, J.-J. Huang, G.-H. Pi, S.-X.
Zhang, J. Han, S.-L. Bi, L. Ruan, X.-P. Dongand SARS Research
Team (2003) Stability of SARS coronavirus in human specimens
and environment and its sensitivity to heating and UV irradiation.
Biomed. Environ. Sci. 16, 246–255.
24. Kariwa, H., N. Fujii and I. Takashima (2004) Inactivation SARS
coronavirus by means of povidone-iodine, physical conditions, and
chemical reagents. Jpn. J. Vet. Res. 52, 105–112.
25. Darnell, M. E. R., K. Subbarao, S. M. Feinstone and D. R. Taylor
(2004) Inactivation of the coronavirus that induces severe respiratory
syndrome. SARS-CoV. J. Virol. Methods 121, 85–91.
26. Darnell, M. E. R. and D. R. Taylor (2006) Evaluation of inactivation
methods for severe acute respiratory syndrome coronavirus in noncellular
blood products. Transfusion 46, 1770–1777.
27. Eickmann, M., U. Gravemann, W. Handke, F. Tolksdorf, S.
Reichenberg, T. H. Muller and A. Seltsam (2018) Inactivation of
Ebola and Middle East respiratory syndrome corona virus in platelet
concentratess and plasma by ultraviolet C light and methylene blue
plus visible light, respectively. Transfusion 58(9), 2202–2207.
28. Eickmann, M., U. Gravemann, W. Handke, F. Tolksdorf, S.
Reichenberg, T. H. Muller and A. Seltsam (2020) Inactivation of
three emerging viruses-severe acute respiratory syndrome corona
virus, Crimean-Congo hemorrhagic fever virus and Nipah virus-in
platelet concntrates by ultraviolet C light and in plasma by methylene
blue plus visible light. Vox Sang. 115(3), 146–151.
29. Giese, A. C. (1976) Living with Our Sun’s Ultraviolet Rays, Chapter
3, pp. 33–34. Plenum Press, New York.
30. Lytle, C. D. and J.-L. Sagripanti (2005) Predicted inactivation of
viruses of relevance to biodefense by solar radiation. J. Viol. 79,
14244–14252.
31. Coohill, T. P. and J.-L. Sagripanti (2009) Bacterial inactivation by
solar ultraviolet radiation compared with sensitivity to 254 nm radiation.
Photochem. Photobiol. 85, 1043–1052.
32. Mims, F. M. (2005) Avian inuenza and UV-B blocked by biomass
smoke. Environ. Health Perspect. 113(12), A806–A807.
33. Sagripanti, J.-L. and C. D. Lytle (2011) Sensitivity to ultraviolet
radiation of Lassa, Vaccinia, and Ebola viruses dried on surfaces.
Arch. Virol. 156, 489–494.
34. Sagripanti, J.-L. and C. D. Lytle (2007) Inactivation of Inuenza
virus by solar radiation. Photochem. Photobiol. 83, 1278–1282.
35. USDA UV-B Monitoring and Research Program (http://uvb.nrel.-
colostate.edu/UVB/).
36. Walker, C. M. and G. P. Ko (2007) Effect of ultraviolet irradiation
on viral aerosols. Environ. Sci. Technol. 41, 5460–5465.
37. Sagripanti, J.-L., A. Levy, J. Robertson, A. Merritt and T. J. J. Inglis
(2009) Inactivation of virulent Burkholderia pseudomallei by sunlight.
Photochem. Photobiol. 85, 978– 986.
38. Ben-David, A. and J.-L. Sagripanti (2010) A model for inactivation
of microbes suspended in the atmosphere by solar ultraviolet radiation.
Photochem Photobiol. 86, 895–908.
39. Weiss, M. and M. C. Horzinek (1986) Resistance of Berne virus to
physical and chemical treatment. Vet. Microbiol. 11, 41–49.
40. Budowsky, E. I., S. E. Bresler, E. A. Friedman and N. V. Zheleznova
(1981) Principles of selective inactivation of viral genome. I. UV-induced
inactivation of Inuenza virus. Arch. Virol. 68, 239–247.
41. Budowsky, E. I., G. V. Kostyuk, A. A. Kost and F. A. Savin (1981)
Principles of selective inactivation of viral genome. II. Inuence of
stirring and optical density of the layer to be irradiated upon UV-induced
inactivation of viruses. Arch. Virol. 68, 249–256.
42. Sagripanti, J.-L., L. Voss, H.-J. Marschall and C. D. Lytle (2013)
Inactivation of Vaccinia virus by natural sunlight and by articial
UVB radiation. Photochem. Photobiol. 89, 132–138.
736 Jose-Luis Sagripanti and C. David Lytle
Printed by [Wiley Online Library - 093.034.091.251 - /doi/epdf/10.1111/php.13293] at [14/04/2021].
43. Zavadoba, Z. and H. Libikova (1975) Comparison of the sensitivity
to ultraviolet radiation of reovirus 3 and some viruses of the Kamerovo
group. Acta Virol. 19, 88–90.
44. Simirnov, Y., S. P. Kapitulez and N. V. Kaverin (1992) Effects of
UV-irradiation upon Venezuelean equine encephalomyelitis virus.
Virus Res. 22, 151–158.
45. Kohase, M. and J. Vilcek (1979) Interferon induction with Newcastle
disease virus in FS-4 cells: effect of priming with priming with interferon
and of virus inactivating treatments. Jpn. J. Med. Sci. Biol. 32,
281–294.
46. Levinson, W. and R. Rubin (1966) Radiation studies of avian tumor
viruses and of Newcastle disease virus. Virol. 28, 533–542.
47. DiStefano, R., G. Burgio, P. Ammatuna, A. Sinatra and A. Chiarini
(1976) Thermal and ultraviolet inactivation of plaque puried
measles virus clones. G. Batteriol. Virol. Immunol. 69, 3–11.
48. Powell, W. F. and R. B. Setlow (1956) The effect of monochromatic
ultraviolet radiation on the interfering property of inuenza virus.
Virology 2, 337–343.
49. Oye, A. K. and E. Rimstad (2001) Inactivation of infectious salmon
anemia virus, viral hemorrhagic septicaemia virus and infectious pancreatic
necrosis virus in water using UVC radiation. Dis Aquat.
Organ. 48, 1–5.
50. Kaplan, J., L. Frias and M. McFall (2020) A third of the
global world population is in coronavirus lockdown. Business Insider
May 6.
51. Downie, A. W. and K. R. Dumbell (1947) Survival of variola virus
in dried exudates and crusts from smallpox patients. Lancet 1, 550–
553.
52. Sagripanti, J.-L., A. M. Rom and L. E. Holland (2010) Persistence
in darkness of virulent alpha viruses, Ebola virus, and Lassa virus
deposited on solid surfaces. Arch Virol 155, 2035–2039.
53. Ben-David, A. and J.-L. Sagripanti (2013) Regression model for estimating
inactivation of microbial aerosols by solar radiation. Photochem
Photobiol 89, 995–999.
54. Coronavirus Statistics (2020) Stats real time. www.epidemic-stats.-
com consulted May 7, 2020.
55. Coronavirus: Half of humanity now on lockdown as 90 countries
call for connement. Euronews. 3 April 2020.
56. UNESCO. 4 March 2020 COVID-19 Educational Disruption and
Response.
https://reliefweb.int/sites/reliefweb.i ... /en.unesco.
org-COVID-19%20Educational%20Disruption%20and%
20Response.pdf. Retrieved 28 March 2020.
57. Wikipedia, the free encyclopedia/COVID-19 pandemic lockdowns.
https://en.wikipedia.org/wiki/COVID-19_ ... downs#Coun
tries_and_territories_without_lockdowns. Retrieved May 29, 2020.
Photochemistry and Photobiology, 2020, 96 737
Printed by [Wiley Online Library - 093.034.091.251 - /doi/epdf/10.1111/php.13293] at [14/04/2021].
