key: cord-1046597-az7f7zgr authors: Sagripanti, Jose‐Luis; Lytle, C. David title: Estimated Inactivation of Coronaviruses by Solar Radiation With Special Reference to COVID‐19 date: 2020-06-05 journal: Photochem Photobiol DOI: 10.1111/php.13293 sha: fb6bb02cb4e8298500b6ed22e834d198c227e299 doc_id: 1046597 cord_uid: az7f7zgr 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 artificial 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 influenza 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 influenza 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. 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) (3) (4) (5) . Coronaviruses have the largest genomes of all ssRNA viruses which will become of relevance latter This article is protected by copyright. All rights reserved 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 confirmed 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 non-symptomatic carriers. This amount is not well established for coronaviruses, but it has been reported that nasal secretions contain up to 10 7 infectious influenza 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 hours to 3 days depending on the type of surface on which it was deposited (15). Influenza virus was readily reaerosolized by sweeping floors without much loss in infectivity (16). It must be assumed that SARS-CoV-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 influenza 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 influenza 12. 5 This article is protected by copyright. All rights reserved tested, ranging from 23% to 98% (19). In agreement with the relatively small effect of humidity and temperature on influenza 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 influenza A parallels that for SARS-CoV-2 then, the effect of artificial and natural UV radiation on SARS-CoV-2 inactivation should be preeminent. The preeminent effect indoors of germicidal UV (UVC, 254nm) radiation is clearly confirmed by a report whereby inactivation of air-borne virions by UV radiation virtually prevented the spread of influenza among patients in a veterans hospital, during the same time that an epidemic of influenza ravaged similar patients in nearby non-irradiated 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 UVtransparent 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 influenza incidence in hospital admission records and solar UV-blocking by smoke during the burning season (32). The reports on influenza 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 two-fold, i) to estimate the sensitivity of SARS-CoV-2 to inactivation by germicidal UV (UVC) and ii) 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 influenza viruses at various times in numerous locations in the U.S. and globally (34). here should be useful in evaluating the persistence of SARS-CoV-2 in environments exposed to solar radiation. 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 influenza A virus (34) SARS-CO V2 virus UV 254 sensitivity. The UVC sensitivity is reported here as D 37 which corresponds to the UV fluence that produces, on average, one lethal hit to the virus, resulting in 37% survival. D 37 equals the reciprocal of the slope on the semi-logarithmic graph of viral survival versus dose and can be calculated by dividing the fluence that results in 1 Log 10 reduction of virus load by 2.3 (the natural logarithmic base). A lower value of D 37 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, i.e., the larger the genome "target", the more sensitive (and lower D 37 ). This results in the product of the genome size and the D 37 , defined 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 determined that 35% of the total daily UVB occurs in the two-hour period (120 minutes) around solar noon (37). Thus 35% of the total daily UVB fluence divided by 120 minutes yields the noontime UVB flux (in J/m 2 /min) at the locations and times of the year presented in Tables 2 and 3 . It should be noted that the solar UVB flux used in the present study assumed no atmospheric influence, 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) . In Table 1 Table 1 , the median value for the SARS-CoV-2 D 37 was 5.0 J/m2. The D 37 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; D 10 (6.9 J/m 2 ) 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, This article is protected by copyright. All rights reserved 36, [40] [41] [42] . This resulted in a change of slope of approximately 4-fold in experiments with Ebola and Lassa viruses and affected several percent of the virus population (33, 42). Therefore, for survival beyond 10%, a UV fluence of 4 times the chosen D 10 (28 J/m 2 ) 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/m 2 ; sterilization level inactivation (10 -6 survival) would require 140 J/m 2 .