Epidemiological clustered characteristics of coronavirus disease 2019 (COVID-19) in three phases of transmission in Jilin Province, China

Discussion

COVID-19 has posed great challenges to all health professionals worldwide. China has experienced a large outbreak, and its economy is gradually stabilizing; however, the cumulative number of overseas imported infections is slowly increasing. Except in Wuhan, China, the initial cases were mainly imported cases, and the number of infections eventually increased due to the occurrence of cluster events. During the Spring Festival, China adopted measures such as sealing off the city, prohibiting the entry of foreign populations, closing public places, and extending holidays to reduce the incidence of imported and cluster cases, which achieved good results [ 19 ]. In Beijing, Shanghai, and other provinces and cities in China, the number of cluster cases accounted for the number of confirmed cases (50%–80%) [ 20 , 21 ]. The aggregated cases in Jilin Province suggested that most of the aggregated outbreaks involved family aggregation.

The COVID-19 outbreak in Jilin Province can be divided into three phases according to temporal distribution. The first phase of the outbreak involved 17 aggregated outbreaks, the second phase involved one aggregated outbreak, and the third phase involved one aggregated outbreak. The median incubation periods of the cases in all three phases of the outbreak in Jilin Province were 10 days, 8 days, and 5 days, respectively, with the longest of all cases being 19 days and the shortest being 0 days; that is, the symptoms appeared on the day of exposure. Based on previous studies, the longest incubation period for COVID-19 is 19 days [ 22 ]. As most of the first cases were imported, data on their exposure time were difficult to obtain; therefore, the incubation period of the renewed cases is more representative of the actual situation of COVID-19 in Jilin Province. Previous studies have indicated that the average incubation period of COVID-19 is 5 days [ 7 ]. The differences between the present study and previous studies may be due to the different strains of the transmitted viruses across regions. Results of statistical tests showed that the incubation period of the third stage of the epidemic differs from those of the first two stages, presumably due to the differences in the source of virus, thus leading to the variations in the incubation period of the infected cases [ 23 ].

The third stage of the outbreak was discovered through a flow survey, in which a lecturer who had already been infected with COVID-19 conducted a health promotion class and caused mass transmission of COVID-19 to the audience. Since the outbreak occurred during the winter, the lecture room was not properly ventilated as it was extremely cold outside; hence, most of the people who attended the lecture were infected. In addition, because the topic of the lecture was health related, most of the older adults were interested to listen as they were overly concerned about their health and had sufficient time to attend the event; hence, most of the attendees were unemployed or retired, which explains the difference in age and occupation between the third and first two stages of the epidemic.

This study found that most cases had the ability to transmit to the next generation of cases 2–7 days prior to the onset of symptoms; that is, they were infectious during the incubation period, which was similar to the findings of other studies related to aggregated outbreaks [ 10 , 24 ]. The epidemiological survey data of patients showed that most people during the aggregated outbreak had not been exposed to the infected area and had no contact with symptomatic patients, yet they still had the possibility of being infected; this finding confirmed the hypothesis that some asymptomatic patients also had the ability to spread the infection. Thus, the neglect of the detection and management of asymptomatic infected persons in the early stages of the COVID-19 outbreak resulted in the widespread transmission. At the first sign of the epidemic, the close contacts of the infected population should be identified, and the management and isolation of the closely connected and sub-closely connected populations should be strengthened to effectively limit the spread of the epidemic. The detection methods used between the first and subsequent cases differed. The predominance of active screening as a detection method for sequel cases suggests that active screening can detect patients who may still be in the incubation period and is an effective method of controlling the spread of the disease. Aggregate cases had a higher rate of active screening than non-aggregate cases. Among the aggregated cases, the proportion of active screening was higher among renewed cases than among first cases, indicating that the local health authorities monitored and managed the close contacts in a timely manner. Furthermore, most of the renewed cases were detected through active testing, effectively controlling latent cases and avoiding the spread of the virus in mostly unknown situations. At the same time, significant differences were observed in the length of hospital stay between the aggregated cases and non-aggregated cases. All patients were discharged with a negative nucleic acid test over a period of time, and the aggregated cases were hospitalized for a longer period of time, which indicates that the aggregated outbreaks involved earlier admissions. This laterally proves that the local health department isolated their close contacts in a timely manner, allowing the source of infection to be detected early through active screening. The largest proportion of imported cases was detected in the first phase of the cluster outbreak, and the population size per cluster outbreak was smaller than that in the last two phases of the outbreak. This is due to the fact that during the first phase of the COVID-19 outbreak in Jilin Province, there was an inflow of a large number of cases from outside the province flowed into Jilin Province due to uncertainty and inexperience in the mode of transmission of the disease, and the failure to adopt contact avoidance methods such as city closures and travel restrictions in the first hours of the epidemic. However, when the disease was confirmed to be contagious, the relevant health authorities immediately implemented mandatory quarantine and city closure measures; hence, each cluster of outbreaks only involved a relatively small number of people. The cases in the latter two phases of the outbreak were all related to each other and were found in close and sub-close contacts of the same imported case, suggesting that sealing the city was effective in avoiding the inflow of cases from outside the province. The outbreaks in both phases were found to be caused by gatherings in public places and therefore involved a large number of people; although the outbreaks were effectively controlled at this stage, the focus of prevention and control should shift to the restriction of large gatherings in public places. For imported cases where various conditions permit (e.g., time and money), if you live with your relatives, home isolation is not recommended, or the family members need to take protective measures when they are at home. Infections during gatherings and common exposures occur mainly in places with a high population density and within a short period of time. Therefore, effective measures, such as controlling the flow of people, should be implemented in densely populated areas. Therefore, it is necessary to abolish any type of in-person gatherings [ 25 ]. For example, the conduct of online classes at home significantly reduced the spread of COVID-19. However, as the mobility of people returning to work and classes increases, this also increases the possibility of spreading the infection. The second and third phases of the outbreak in Jilin Province were caused by gatherings in public places under strict control of imported cases; therefore, it is even more important to avoid gatherings in the current epidemic situation to avoid the possibility of outbreaks caused by mass gatherings.

No spatial correlation was found between the differences in COVID-19 incidence rates across urban areas for the other two phases of the epidemic, except for the second phase; this result implies that during the first and third phases of the COVID-19 outbreak, cases showed a random distribution across municipalities and were not regionally clustered, which may be due to the fact that the epidemic had been spreading across municipalities in Jilin Province for several days by the time cases were detected. By contrast, the second phase of the epidemic in Jilin City, Jilin Province, was detected early at the beginning, and prevention and control measures were implemented quickly; thus, few cases spilled over from Shulan City, showing high-low aggregation in Shulan City and implying the risk of spreading the epidemic from Shulan City to the surrounding municipalities. The results of this spatiotemporal analysis are consistent with the epidemiological distribution of this study.

The proportion of imported cases in the first phase of the cluster epidemic was relatively high, while the size of the population per cluster epidemic was smaller than that in the last two phases of the epidemic, which was due to the fact that during the first phase of the COVID-19 epidemic in Jilin Province, there was an inflow of a large number of cases from outside the province into the Jilin Province due to uncertainty and inexperience with the mode of transmission of the disease and the failure to adopt contact avoidance methods such as city closures and travel restrictions in the first hours of the epidemic. However, after confirming that the disease was contagious, the relevant health authorities immediately implemented mandatory quarantine and city closure measures; hence, each cluster of outbreaks only involved a relatively small number of people. The cases in the second and third phases of the outbreak were linked to each other, with cases found in close and sub-close contacts of the same imported case, indicating that the closure of the city was effective in avoiding the inflow of cases from outside the province. The outbreak of the second and third phases of the epidemic was caused by gatherings in public places, thus involving a large number of people; although the outbreak was effectively controlled at this stage, the focus of prevention and control should shift to the avoidance of large gatherings in public places.

Infections and general exposure at gatherings occur mainly in areas with a high population density. Therefore, effective measures, such as crowd control, should still be implemented in densely populated areas. Gatherings must be eliminated [ 25 ]. For example, the conduct of online class at home significantly reduced the spread of COVID-19. However, with the increased movement to and from home and tourist travel during holidays, this made it possible for the outbreak to spread. The second and third phases of the epidemic in Jilin Province were caused by gatherings in public places under the strict control of imported cases. Therefore, in the current epidemic situation, gatherings should be restricted to avoid the occurrence of an epidemic caused by mass gatherings.

Conclusion

Cluster cases comprised the highest component of the total number of cases. Surveillance of outbreaks is of utmost importance. In addition, family gatherings and high traffic areas should be avoided. Simultaneously, as the number of people returning to work and school increases, precautions should be taken to avoid the possibility of secondary outbreaks.

Acknowledgments

Funding Statement

The author(s) received no specific funding for this work.

Data Availability

All relevant data are within the manuscript and its Supporting Information files.

References