The impact of environmental variables on the spread of COVID-19 in the Republic of Korea

Corona virus disease 2019 (COVID-19) has been declared a global pandemic and is a major public health concern worldwide. In this study, we aimed to determine the role of environmental factors, such as climate and air pollutants, in the transmission of COVID-19 in the Republic of Korea. We collected epidemiological and environmental data from two regions of the Republic of Korea, namely Seoul metropolitan region (SMR) and Daegu-Gyeongbuk region (DGR) from February 2020 to July 2020. The data was then analyzed to identify correlations between each environmental factor with confirmed daily COVID-19 cases. Among the various environmental parameters, the duration of sunshine and ozone level were found to positively correlate with COVID-19 cases in both regions. However, the association of temperature variables with COVID-19 transmission revealed contradictory results when comparing the data from SMR and DGR. Moreover, statistical bias may have arisen due to an extensive epidemiological investigation and altered socio-behaviors that occurred in response to a COVID-19 outbreak. Nevertheless, our results suggest that various environmental factors may play a role in COVID-19 transmission.


Results
During our study period, from February 2020 to July 2020, a total of 12,031 confirmed locally-transmitted COVID-19 cases were identified. Among these cases, 3010 (25.0%) and 7998 (66.5%) were from SMR and DGR, respectively. Figure 1 shows daily confirmed cases in SMR and DGR. An explosive outbreak was observed in DGR following religious gatherings between February and March. Meanwhile, there were several major cases of local cluster infections in SMR, and the number of confirmed cases has remained relatively constant in SMR since April. Table S1 summarizes monthly variations in various environmental parameters in SMR and DGR. A large variation in temperature was noted between the months, with no significantly different meteorological parameters noted between SMR and DGR, except in July. The levels of atmospheric carbon monoxide, nitrogen dioxide, and sulfur trioxide were higher in SMR, and ozone was higher in DGR. However, significant differences were not observed in the PM 10 and PM 2.5 levels between the two regions, save for in March when both were significantly increased in SMR. Table 1 summarizes the relationship between environmental factors and daily confirmed COVID-19 cases. Among the 16 environmental parameters, 11 and 10 were found to be significantly correlated with confirmed COVID-19 cases in SMR and DGR, respectively. However, the duration of sunshine and the ozone level were the only parameters determined to affect COVID-19 in both regions. Meanwhile, contradictory results were obtained regarding the relationship between cases and temperature variables and atmospheric pressure in the two regions. Specifically, all temperature related variables were positively correlated, and atmospheric pressure was inversely correlated with COVID-19 cases in SMR, while the opposite trend was observed in DGR.

Discussion
Numerous variables were included in the analysis for this study to clarify the relationship between the environment and confirmed COVID-19 cases. We found that the duration of sunshine and the ozone level were positively correlated with the spread of SARS-CoV-2 in the two selected regions, which contradicts the results of Ratnesar-Shumate et al. who reported that sunlight rapidly inactivates SARS-CoV-2 on surfaces 13 . We postulate that one potential explanation for our results is the increased risk of SARS-CoV-2 exposure associated with outdoor activities during days with a longer duration of sunlight 14 , resulting in increased transmission prior to inactivation of the virus by sunlight. Additionally, Daniele et al. reported that atmospheric pollution may influence the SARS-CoV-2 outbreak in Italy 15 . We, therefore, also analyzed the effect of air pollutants on the spread of SARS-CoV-2 and found no correlation between SARS-CoV-2 transmission and air pollutants, with the exception of ozone, suggesting that air pollutants do not represent a significant environmental driver of SARS-CoV-2 transmission in the Republic of Korea. The ozone level significantly affected the transmission of SARS-CoV-2, www.nature.com/scientificreports/ and we hypothesize that the ozone level would disrupt the respiratory epithelial barrier 16,17 , making the public more susceptible to the SARS-CoV-2 infection. Numerous studies have also reported a strong association between COVID-19 transmission and temperature 3,5,11,18 . We, therefore, selected two regions that showed similar temperature fluctuations during the study period; however, contradictory results were observed for all temperature variables between the two regions. Specifically, SARS-CoV-2 transmission increased as the temperature increased in SMR; whereas, we observed an increase in the number of cases with a decrease in temperature in DGR. The large outbreak that occurred following religious events in DGR between February and March 2020 may have contributed to these conflicting results. Moreover, in response to these outbreaks, an extensive epidemiological investigation was performed for members who participated in this event and for their close immediate contacts. Moreover, after this outbreak between February and March, strict measures were set in place to ensure proper maintenance of personal hygiene, including wearing of masks, use of hand sanitizers, and social distancing 19 , resulting in only a few cases of local clustering and sporadic infections reported in SMR and DGR. We could, therefore, assume that changes in socio-behavioral factors in response to the outbreaks had a greater impact than the environmental factors on the spread of SARS-CoV-2. However, extensive and rapid epidemiological investigations would also lead to an increase in the number of confirmed cases within a short period of time, which would subsequently skew the statistical results related to the effects of temperature variables. Therefore, one should consider that a large number of confirmed cases identified in these types of situations would greatly influence the correlation analysis between environmental factors and disease transmission, resulting in false negative or positive results.
Despite the significant results demonstrating the effect of environmental factors on COVID-19, there were several limitations noted in our study. First, the classification of locally infected cases and imported cases may have been affected by the extensive epidemiological investigation. Therefore, the number of confirmed cases due to community infection may be inaccurate, although we collected the epidemiological data from Korea Centers for Disease Control and Prevention (KCDC). Second, in the early days of the COVID-19 pandemic, there was a shortage of molecular tests for COVID-19 diagnosis, therefore, the impact of the environmental factors might not be accurately reflected. Third, we could not consider individual health factors, such as personal hygiene or exposure risk to SARS-CoV-2, in the statistical analyses.
The environment plays a significant role in the regional spread of COVID-19, and our results demonstrated that the duration of sunshine and ozone level were positively correlated with SARS-CoV-2 transmission. However, the number of confirmed COVID-19 cases may have also been impacted by various additional factors, including the completion of a large epidemiological investigation within the study period or changing sociobehaviors based on cluster outbreaks. Hence, these factors could create a bias in the statistical results. For these reasons, further studies should be conducted to confirm the relationship between environmental factors and SARS-CoV-2 transmission with sufficient epidemiological data generated over an extended period of time. Meteorological and air pollution data. The meteorological data were collected from the database of Korea Meteorological Administration (KMA; https:// data. kma. go. kr/). The KMA provides high-resolution meteorological information for specific areas on a flexible web-based platform 20,21 . Additionally, we collected the daily records on ten basic meteorological factors, including average temperature, maximum temperature, minimum temperature, ground temperature, diurnal temperature variation, amount of rainfall, wind speed, relative humidity, atmospheric pressure, and duration of sunshine. Information on air pollution across the country was collected from AIRKOREA (http:// airko rea. or. kr), which was launched by the Korean Ministry of Environment and is a database that provides an account of daily air pollutant levels including carbon monoxide, nitrogen dioxide, ozone, sulfur trioxide, PM 10 , and PM 2.5 .
Ethical statement. Data on environmental conditions and COVID-19 confirmed cases were obtained from official reports provided in a public database, therefore ethical review was not required.
Statistics. Datasets were analyzed using R version 3.6.3 (http:// www.R-proje ct. org/). Descriptive analyses for monthly meteorological factors and air pollutants during the study period were performed for both regions (SMR, DGR). Student's t-test was used to determine the statistical difference in monthly environmental variables between the regions. P-values < 0.05 were considered significant. To examine the relationship between environmental factors and daily COVID-19 confirmed cases, we conducted Spearman rank correlation test and Kendall rank correlation test. Factors were considered to affect SARS-CoV-2 if significant differences were observed in both statistical tests.

Data availability
The data analyzed in this study are available on GitHub at https:// github. com/ yoorer/ COVID_ ENV.