Does the environment matter?; Effect of environmental factors on COVID-19 transmission in the Republic of Korea


 Background: Corona virus disease 2019 (COVID-19) has been declared a global pandemic and is a major concern of public health 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.Methods: 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. Further, we analyzed the data to identify the correlation of each environmental factor with the confirmed cases of COVID-19 on a daily basis.Results: Among the various environmental parameters, duration of sunshine and ozone level were found to be positively correlated with COVID-19 in both regions. However, the association of temperature variables with COVID-19 transmission showed contradictory results upon comparing the data from SMR and DGR.Conclusions: In conclusion, our results suggest that the environmental factors could play a crucial role in the transmission of COVID-19. However, it should be noted that statistical bias could arise due to the disease outbreak being confined to a specific area and extensive epidemiological investigation.


Introduction
Since the identi cation of novel coronavirus (SARS-CoV-2) infection in Wuhan, China in December 2019, it has become the greatest concern among public health issues 1 . A total of 17 million con rmed cases has been reported worldwide as of 31 st July, 2020. Over 200,000 novel cases of COVID-19 are being reported every day 2 . SARS-CoV-2 has similar or slightly higher reproduction number compared to the Middle East Respiratory Syndrome Coronavirus (MERS) and severe acute respiratory syndrome coronavirus 1 (SARS-CoV-1) 3 . SARS-CoV-2 infection has spread worldwide due to its highly contagious nature. SARS-CoV-2 infection, also known as coronavirus disease 2019 , is characterized by di culty in breathing and pneumonia. COVID-19 has also been reported to cause kidney failure and even death in severe cases 4 .
Similar to that of other viral respiratory infections, the transmission of COVID-19 could also be affected by environmental factors including climate. Numerous studies have been performed to investigate the effect of meteorological factors on the transmission of COVID-19 in various countries including Brazil 5 , China 6,7 , Iran 8 , Singapore 3 , and USA 9 . However, the effect of climate factors on the transmission of COVID-19 remains unclear 10 .
Since the rst con rmed case of COVID-19 in the Republic of Korea, on 20 January, 2020, a total of 14,305 con rmed cases has been reported as of July 31, 2020. The majority of con rmed cases were classi ed as domestic cases caused due to communal spread. The wide range of climate parameters such as temperature variables, amount of rainfall and relative humidity in the Republic of Korea makes it a suitable place to study the effect of the environment on the spread of COVID-19. Therefore, in this study, we aimed to investigate the role of environmental factors, such as climate and air pollutants in the transmission of COVID-19 by analyzing the relationship between these variables with the con rmed COVID-19 cases in the Republic of Korea on a daily basis.

Results
During our study period, a total of 12,031 con rmed cases of COVID-19 were reported to be caused due to communal spread. Among these cases, 3,010 (25.0%) and 7,998 (66.5%) cases were from SMR and DGR, respectively. Figure 1 shows daily con rmed cases in SMR and DGR. An explosive epidemic outbreak occurred due to religious gatherings between February and March in DGR. Apart from DGR, there were several major cases of local cluster infections in SMR, and the number of con rmed cases has remained relatively constant in SMR since April. Table 1 summarizes monthly variations in various environmental parameters in SMR and DGR. As mentioned previously, there was a large difference in temperature between months. There was no signi cant difference in meteorological parameters between SMR and DGR with the exception of the month of July. The levels of carbon monoxide, nitrogen dioxide, and sulfur trioxide in the air were higher in SMR, and ozone was higher in DGR. However, there was almost no difference in the levels of PM 10 and PM 2.5 between two regions. Table 2 summarizes the relationship between the environmental factors and daily con rmed cases of COVID-19.
Among the 16 environmental parameters, 11 and 10 parameters were found to be signi cantly correlated with con rmed COVID-19 cases in SMR and DGR, respectively. Further, duration of sunshine and ozone, were the only two parameters to commonly affect COVID-19 in both regions. When we compared the data from SMR and DGR, we obtained contradictory results in case of temperature variables and atmospheric pressure.

Discussion
In our study, various variables were included to clarify the relationship between the environment and con rmed COVID-19 cases. We found that duration of sunshine and ozone level were found to be positively correlated with the spread of COVID-19 in two selected regions. Ratnesar-Shumate et al. reported that sunlight rapidly inactivates SARS-CoV-2 on surfaces 11 . However, our ndings contradicted the results of the previous study. Although we were unsure about how sunlight affected the spread of COVID-19, we hypothesized that the increase in the risk of exposure to SARS-CoV-2 could be attributed to the increase in outdoor activity 12 , resulting in an increase in spread rather than inactivation of the virus by sunlight. Further, we analyzed the effect of air pollutants on the spread of COVID-19, and found that there was no or inverse correlation between COVID-19 transmission and air pollutants with the exception of ozone. This suggests that air pollutants could not be the environmental drivers of COVID-19 transmission.
Numerous studies have reported the strong association between COVID-19 transmission and temperature 3,5,13 . We selected two regions that showed almost similar temperature during the study period; however, contradictory results were observed in temperature variables between the two regions. COVID-19 transmission increased as the temperature increased in SMR; however, we observed an increase in the number of cases with a decrease in temperature in DGR. As mentioned earlier, there was huge outbreak occurred due to religious events in DGR between February and March, 2020. An extensive epidemiological investigation was performed for members who participated in this event and for individuals who were in close contact with this group. Following the outbreak in DGR, Koreans have been strictly following strategies to maintain personal hygiene, including wearing a mask, use of hand sanitizers, and social distancing, and only a few cases of local cluster and sporadic infections in SMR and DGR were reported. Extensive epidemiological investigation revealed a large number of con rmed cases in DGR. This sudden increase in the number of con rmed cases during a short period of time would result in a bias in the statistical results with respect to temperature variables. Due the rapid transmission of COVID-19 and extensive epidemiological surveillance 14,15 , numerous outbreaks could occur due to religious events or social gatherings. Therefore, one should consider that a large number of con rmed cases identi ed due to the above situations would have a great in uence on the analysis of correlation between the environmental factors and the transmission of the disease, resulting in false negative results.
Despite the signi cant results demonstrating the effect of environmental factors on COVID-19, there were several limitations in our study. First, the classi cation of locally infected cases and imported cases could have been affected by the process used for epidemiological investigation. Therefore, the number of con rmed cases due to communal infection may not be accurate, although we collected the epidemiological data from KCDC. Second, in the early days of the COVID-19 spread, there were not enough molecular tests to diagnose COVID-19, therefore, the impact of the environmental factors might not be effectively re ected. Third, we could not consider individual health factors in statistical analyses, such as personal hygiene or exposure risk to COVID-19.
The environment plays a signi cant role in the regional spread of COVID-19, and our results demonstrated that the duration of sunshine and ozone level were positively correlated to the transmission of COVID-19. However, due to of the infection rate of COVID-19 and massive global efforts in terms of epidemiological investigations, outbreaks or large cluster infection can be identi ed in multiple population groups in a speci c area, which can create a bias in statistical results. Although COVID-19 epidemiological data have been collected globally, we have been exposed to this pandemic for only eight months. For the aforementioned reasons, further studies should be conducted to con rm the relationship between the environmental factors and transmission of COVID-19 with su cient epidemiological data over a longer duration of time.

Study area and con rmed COVID-19 cases
The Republic of Korea lies between latitudes 33° and 39°N, and longitudes 124° and 130°E. It tends to have a humid continental and subtropical climate, and typically exhibits large seasonal temperature differences. We selected two regions in the Republic of Korea, namely Seoul metropolitan region (SMR) and Daegu-Gyeongbuk region (DGR), which had relatively higher cases of COVID-19. The data for daily con rmed cases of COVID-19 from February 1, 2020 to July 31, 2020 were obtained from the website of Korea Centers for Disease Control and Prevention (KCDC; http://www.cdc.go.kr). Our study aimed to exclusively investigate the effect of environmental factors on COVID-19 transmission, therefore, we have only included the con rmed cases caused due to communal spread.

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 speci c areas on a exible web-based platform 16,17 . Additionally, we collected the daily records on 10 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. Further, information on air pollution across the country was collected from AIRKOREA (http://airkorea.or.kr), which was launched by the Korean Ministry of Environment. This database 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 con rmed cases were from o cial reports provided by public database, therefore ethical review was not required.

Statistics
Datasets were analyzed using R version 3.6.3 (http://www.R-project.org/). Descriptive analyses of monthly meteorological factors and air pollutants during the study period were performed for both the regions (SMR, DGR).
Student's t-test was used to determine the statistical difference in monthly environmental variables between the regions. P-value less than 0.05 was considered signi cant. To examine the relationship between environmental factors and daily COVID-19 con rmed cases, we conducted Spearman rank correlation test and Kendall rank correlation test. Factors were considered to affect COVID-19, if signi cant difference was observed in both the statistical tests.

Data availability
The data analyzed in this study are available on GitHub at https://github.com/yoorer/COVID_ENV.    Figure 1 Daily con rmed cases (grey box) and total con rmed cumulative cases (solid line) of COVID-19 in Seoul metropolitan region (A) and Daegu-Gyeongbuk region (B).