key: cord-0877098-hdwkphnb
authors: Tang, Liwei; Liu, Min; Ren, Bingyu; Wu, Zongting; Yu, Xunci; Peng, Chen; Tian, Jing
title: Sunlight ultraviolet radiation dose is negatively correlated with the percent positive of SARS-CoV-2 and four others common human coronaviruses in the U.S.
date: 2020-08-19
journal: Sci Total Environ
DOI: 10.1016/j.scitotenv.2020.141816
sha: 4503af28d0c1e41a582c751e32eae5f46b8be523
doc_id: 877098
cord_uid: hdwkphnb

Abstract Human coronaviruses are RNA viruses that are sensitive to ultraviolet (UV) radiation. Sunlight contains UVA (320–400 nm), UVB (260–320 nm) and UVC (200–260 nm) action spectra. UVC can inactivate coronaviruses, including severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2). The incidence and mortality of coronavirus disease 2019 (COVID-19) are considered to be correlated with vitamin D levels. Vitamin D synthesis in human skin is closely related to exposure to UVB radiation. Therefore, the incidence and mortality of COVID-19 are also considered to be correlated with Vitamin D levels. In this study, Spearman and Kendall rank correlation analysis tests were used to analyze the correlation between the average percent positive of five human coronaviruses (SARS-CoV-2, CoVHKU1, CoVNL63, CoVOC43, and CoV229E) in the U.S. and the corresponding sunlight UV radiation dose The results indicated that the monthly average percent positive of four common coronaviruses was significantly negatively correlated with the sunlight UV radiation dose. The weekly percent positive of SARS-CoV-2 during April 17, 2020 to July 10, 2020 showed a significant negative correlation with the sunlight UV radiation dose in census regions 1 and 2 of the U.S. while no statistical significance in the other regions. Additionally, sunlight UV radiation also showed some negative effects with respect to the early SARS-CoV-2 transmission.

Coronavirus disease 2019 is an emerging infectious disease that has caused a global pandemic. Its causing agent is severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2), which belongs to betacoronavirus (Wiersinga et al., 2020) . Droplet and aerosol modes are considered the transmission routes of COVID-19 (Shereen et al., 2020; Wiersinga et al., 2020) . Seven coronaviruses have been reported to have the ability to cause human diseases, and they show great similarities in species types and transmission patterns . Four human coronaviruses, including CoVHKU1, CoVNL63, CoVOC43, and CoV229E, were reported to cause seasonal epidemics commonly in the U.S. and some other countries (Gaunt et al., 2010; Killerby et al., 2018) . Although the seasonality of the COVID-19 epidemic remains unclear, the epidemics caused by other four common human coronaviruses have been confirmed to be correlated with season; the incidence rates of the epidemics caused by these four common human coronaviruses are higher in winter and lower in summer (Friedman et al., 2018; Gaunt et al., 2010; Killerby et al., 2018) . However, the cause of seasonality is still not fully understood (Fisman, 2012) .

The wavelength of ultraviolet (UV) radiation in sunlight ranges from 100 nm to 400 nm, which are largely divided into three parts, including UVA (320-400 nm), UVB (260-320 nm) and UVC (200-260 nm) (D'Orazio et al., 2013) . Human J o u r n a l P r e -p r o o f Journal Pre-proof coronaviruses, including SARS-CoV and SARS-CoV-2, are sensitive to UV radiation (Duan et al., 2003; Hessling et al., 2020) . The UVC is thought to be able to inactivate pathogens in aerosol and skin surface by forming pyrimidine dimers and causing DNA or RNA damage (Welch et al., 2018) . Previous studies had suggested that more than 90% of the SARS-CoV-2 virus load will be inactivated after exposure to summer midday sunlight in the summer for 34 minutes (Sagripanti and Lytle, 2020) . Moreover, more evidences have indicated the important role of vitamin D levels in the COVID-19 epidemic. Vitamin D, including vitamins D2 and D3, is a group of nutrients essential for human beings (Lips, 2006) . COVID-19 confirmed cases and mortality rate in some European countries were reported to be negatively correlated with the mean vitamin D level (Hastie et al., 2020; Ilie et al., 2020) . The same association was also been observed in countries 35 degrees south of latitude (Mansur, 2020; Rhodes et al., 2020) . Further, lower vitamin D levels were linked to higher mortality, and vitamin D supplementation could reduce the mortality rate of COVID-19 patients (Grant et al., 2020) . Considering that vitamin D3 is mainly synthesized from 7-dehydrocholesterol in the skin under sunlight UVB (Holick et al., 2007; Lips, 2006) , the above-mentioned correlations suggested that sunlight UV radiation might affect the COVID-19 epidemic.

This study is aimed to determine the correlation between the percent positive of human coronaviruses, including SARS-CoV-2 in the U.S. and the sunlight UV radiation dose. Since the ongoing COVID-19 epidemic will possibly become a long-term seasonal disease like other common human coronavirus diseases, our J o u r n a l P r e -p r o o f research may contribute to the deeper understanding of the mechanism underlying the seasonality and transmission processes in human coronavirus diseases.

To better understand the incidence of human coronavirus diseases in different areas of the U.S., the U.S. was divided into four census regions, as suggested by the U.S. Census Bureau suggested (Fig. 1) J o u r n a l P r e -p r o o f

To analyze the correlation between the sunlight UV radiation dose and the human coronavirus diseases, Spearman and Kendall rank correlation tests were used to examine and determine the nonlinear relationships between the percent positive of the human coronaviruses and sunlight UV radiation dose. Spearman and Kendall rank correlation tests are non-parametric tests, which are not depending on the concrete values and distributions of the data (Dalmay et al., 2003; Kahraman et al., 2004) .

Spearman rank correlation is mainly used to measure the strength of the association between two variables, while Kendall rank correlation is mainly used to measure the ordinal association between two measured variables (Bonett and Wright, 2000; Menebo, 2020; Pani et al., 2020) . Both those tests are sensitive to the rank and consistency, instead of the precise value of the variables (Bonett and Wright, 2000; Dalmay et al., 2003) .

The percent positive is the proportion of positive individuals in the total number of tested individuals. The monthly average percent positive of four common human coronaviruses was calculated from the weekly data obtained from NREVSS while the weekly average percent positive of SARS-CoV-2 was estimated from the weekly total tests and confirmed cases obtained from JHU CSSE.

Due to the data of total COVID-19 test cases were absence in early transmission period in the U.S., percent positive of SARS-CoV-2 in the U.S. during that period was unavailable. We approximated the infectivity of COVID-19 during the early transmission period as follows (Wallinga and Lipsitch, 2007) J o u r n a l P r e -p r o o f

where C(t) represents the number of confirmed cases at time point t, Δg represents the generation interval, and R average represents the approximation of infectivity. We set the generation interval as 5, 6, and 7 days, according to previous studies on the incubation period of COVID-19 (Guan et al., 2020; Wiersinga et al., 2020) . The monthly average percent positive of four common human coronaviruses (CoVHKU1, CoVNL63, CoVOC43, and CoV229E) and the corresponding monthly total erythemal UV dose are shown in Fig. 3 . The erythemal UV dose includes UVA and UVB doses, and it is considered the most commonly used standard for UV radiation dose (Fioletov et al., 2009; Webb et al., 2011) . The monthly total erythemal UV dose from July 2018 to June 2020 in the U.S. largely ranged from 11.223 kJ/m 2 (in December 2018, census region 1) to 176.855 kJ/m 2 (in June 2020, census region 3).

The results of the Spearman and Kendall rank correlation tests indicated that the monthly average percent positive of human coronaviruses and the corresponding erythemal UV dose showed significant negative association, as shown in Table. 1 (the same association was also indicated from vitamin D UV dose and DNA-damage UV dose, as shown in supplementary materials, Fig. S1, Fig. S2 , Table. S2, and Table. S3).

Since COVID-19 has spread further in the US, the number of total confirmed cases in the four census regions of the U.S. from April 17, 2020 to July 10, 2020 has shown different growth trends (Fig. 4) . The association between the weekly average percent positive of SARS-CoV-2 in the four census regions and the corresponding weekly total sunlight UV radiation dose is shown in Fig. 5 and Table. 

The infectivity of COVID-19 from April 17, 2020 to April 30, 2020 in the U.S. was investigated to study the relationship between the sunlight UV radiation dose and COVID-19 early transmission. The 11-, 13-, and 15-day total sunlight erythemal UV doses and the corresponding R average values at the different generation intervals are shown in Fig. 6 . Spearman and Kendall rank correlation tests indicated significant negative association between sunlight UV radiation and COVID-19 infectivity during the early transmission period outside the State of New York, as shown in Table. 3.

Despite the sunlight UV radiation dose variations can be caused by latitude or seasonal reason, similar negative correlation between sunlight UV radiation and the Fig. 6 The R average values at the different generation intervals (Δg selected as 5, 6, and 7 days) and the corresponding total sunlight erythemal UV doses (11-, 13-, and 15-day durations, respectively)

Our study mainly aimed to provide evidence on the correlation between the sunlight UV radiation dose and human coronaviruses. According to our analyses based on the data from the U.S. during 2018-2020, the sunlight UV radiation dose showed significant negative correlation with four common human coronaviruses (CoVHKU1, CoVNL63, CoVOC43, and CoV229E). The seasonal variation in sunlight UV radiation dose could partly explain the seasonality of four common human coronaviruses which were reported in previous studies (Friedman et al., 2018; Killerby et al., 2018) . Recent studies have suggested that the severity of the COVID-19 epidemic may be closely related to climatic factors, including the UV radiation dose (Babu et al., 2020;  J o u r n a l P r e -p r o o f Sfîcă et al., 2020; Suhaimi et al., 2020) . And the role of particulate matter (PM) and aerosol in COVID-19 transmission has been increasingly recognized (Hsiao et al., 2020; Mutuku et al., 2020; Razzini et al., 2020) . Severe COVID-19 outbreaks in some areas may be associated with lower UV radiation dose in those areas (Sfîcă et al., 2020) . A study of the provincial-level regions in China from December 2019 to April 2020 showed a negative correlation between the number of infections and the latitude (Sun et al., 2020) . The results of these existing studies supported our finding that the UV radiation dose might play an important role in COVID-19 transmission.

Additionally, PM and aerosol were reported to be important vectors for COVID-19

transmission, and the chemical properties of aerosols might affect SARS-CoV-2 survival and transmission (Razzini et al., 2020; Tung et al., 2020; Wathore et al., 2020) . According to a previous study in Italy, the average concentration of PM on the ground in Milan was strongly associated with the number of COVID-19 confirmed cases (Zoran et al., 2020) . Inactivation of pathogens in aerosols and PM by sunlight UV radiation might be the underlying mechanism for this correlation.

However, our study still had some limitations. First, the sunlight UV radiation dose is the cumulative total of the effective UV irradiance received from sunlight over a period. For areas with different sunshine intensities, higher UV radiation dose did not necessarily correspond to higher UV radiation intensity. Therefore, the relationship between the UV radiation intensity and human coronaviruses remains to be studied further. Second, the study on the role of sunlight UV radiation in the early transmission of COVID-19 is limited to the source of the data, which was not 

This study provided some evidence on the possible negative correlations between the sunlight UV radiation dose and the percent positive of five human coronaviruses (SARS-CoV-2, CoVHKU1, CoVNL63, CoVOC43, and CoV229E). Our study indicated significant negative correlation between the percent positive of four common human coronaviruses (CoVHKU1, CoVNL63, CoVOC43, and CoV229E) and the sunlight UV radiation dose in the U.S. Higher sunlight UV radiation dose might be related to lower percent positive of human coronaviruses. However, although SARS-CoV-2 might show a similar negative correlation with the sunlight UV radiation dose, further research and verification based on the update data in the future are needed to account for the variations in the seasonal cycles. We will continue to focus on this study area in future studies, since they may be beneficial for providing more insights into COVID-19 prevention and treatment.

The authors declare that they have no conflict of interest.

Liu, Bingyu Ren, Zongting Wu, Xunci Yu, Chen Peng, and Jing Tian.

All authors read and approved the final manuscript.

We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled. -0.612 ** 0.001 -0.42 ** 0.004 p Significance level of the two-tailed test. ** Correlation is significant at the 0.01 level; * Correlation is significant at the 0.05 level.

Plausible Role of Environmental Factors on COVID-19 Transmission in the Megacity Delhi

Sample size requirements for estimating Pearson, Kendall and Spearman correlations

UV Radiation and the Skin

Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation

On the relationship between erythemal and vitamin D action spectrum weighted ultraviolet radiation

Seasonality of viral infections: mechanisms and unknowns

Human Coronavirus Infections in Israel: Epidemiology, Clinical Symptoms and Summer

Epidemiology and clinical presentations of the four human coronaviruses 229E, HKU1, NL63, and OC43 detected over 3 years using a novel multiplex real-time PCR method

Evidence that Vitamin D Supplementation Could Reduce Risk of Influenza and COVID-19 Infections and Deaths

Clinical Characteristics of Coronavirus Disease 2019 in China

Vitamin D concentrations and COVID-19 infection in UK Biobank

Ultraviolet irradiation doses for coronavirus inactivation -review and analysis of coronavirus photoinactivation studies

Vitamin D and skin physiology: A D-lightful story

COVID-19: An Aerosol's Point of View from Expiration to Transmission to Viral-mechanism

The role of vitamin D in the prevention of coronavirus disease J o u r n a l P r e -p r o o f Journal Pre-proof 2019 infection and mortality

Fuzzy sets approaches to statistical parametric and nonparametric tests

Human coronavirus circulation in the United States

Vitamin D physiology

Letter: low population mortality from COVID-19 in countries south of latitude 35 degrees North supports vitamin D as a factor determining severity

Temperature and precipitation associate with Covid-19 new daily cases: A correlation study between weather and Covid-19 pandemic in Oslo

An Overview of Experiments and Numerical Simulations on Airflow and Aerosols Deposition in Human Airways and the Role of Bioaerosol Motion in COVID-19 Transmission

Association of COVID-19 pandemic with meteorological parameters over Singapore

SARS-CoV-2 RNA detection in the air and on surfaces in the COVID-19

Letter: low population mortality from severity. Authors' reply

Estimated Inactivation of Coronaviruses by Solar Radiation With Special Reference to COVID-19

Weather Conditions (with focus on UV radiation) Associated with COVID-19 Outbreak and Worldwide Climate-based Prediction for Future Prevention

COVID-19 infection: Origin, transmission, and characteristics of human coronaviruses

Demystifying a Possible Relationship between COVID-19, Air Quality and Meteorological Factors: Evidence from Kuala Lumpur

Impacts of geographic factors and population density on the COVID-19 spreading under the lockdown policies of China

Particulate matter and SARS-CoV-2: A possible model of COVID-19 transmission

How generation intervals shape the relationship between growth rates and reproductive numbers

Understanding air and water borne transmission and survival of coronavirus: Insights and way forward for SARS-CoV-2

Know your standard: clarifying the CIE erythema action spectrum

Far-UVC light: A new tool to control the spread of airborne-mediated microbial diseases

Transmission, Diagnosis, and Treatment of Coronavirus Disease 2019 (COVID-19): A Review

Origin and evolution of the 2019 novel coronavirus

Assessing the relationship between surface levels of PM2.5 and PM10 particulate matter impact on COVID-19 in

We would like to thank Dr. Jari Hovila from Finnish Meteorological Institute for his useful suggestions on collecting UV radiation dose data. We would also like to thank the three anonymous reviewers and the editors for their helpful and constructive comments.This study was financially supported by grants from the Science and Technology Innovation Committee of Shenzhen Municipality (JCYJ20190808152613121), Shenzhen-HongKong Institute of Brain Science-Shenzhen Fundamental Research