Coronavirus disease 2019 (COVID-19), caused by the emergence of the novel pathogen severe acute respiratory syndrome coronavirus 2 (SARS-COV-2), has spread with alarming speed and on an extensive scale since it was first reported in Wuhan, Hubei Province, China, in late December 2019 [1]. On March 11^th, 2020, following the outbreak of COVID-19, World Health Organization (WHO) declared the current situation as a pandemic [2]. So far, 476,374,234 cases have been confirmed, causing 6108,976 deaths (WHO) [3].

A great deal of studies have confirmed that the two primary transmission routes of SARS-CoV-2 spread are through contact (direct and indirect contact) or droplets [4-6]. The official reports of WHO announced that virions through airborne transmission in droplet nuclei with a particle size of < 5 µm can exist for long periods of time, with travel distances > 1 m [7]. These aerosols with virions attached may travel through ventilation systems in buildings and enclosed spaces, eventually invading other areas away from any infected individual [5]. Furthermore, a recent study has even suggested that airborne transmission may be the dominant mode of transportation [6].

Multiple studies have shown that novel coronavirus transmission may be travel-related [8-10]. The human infection risk could be extremely high due to the length of the exposure time window, transmission routes, and structural characteristics during travel or work [11, 12]. Public transport might have been less safe to use during the COVID-19 pandemic due to the enclosed space and the difficulty to maintain social distancing [8]. Zhu's investigation in the early periods of the COVID-19 outbreak showed that high-speed rail (HSR) and air connectivity with Wuhan resulted in 25.4% and 21.2% increases in the average number of daily new confirmed cases, respectively, while their suspension led to 18.6% and 13.3% decreases in that number [13]. Researchers performed correlation analysis based on the data released by the Chinese National Health Commission, and showed that the incidence rate was higher in the regions receiving the largest number of travelers during this period, further confirming the epidemiological characteristics [14]. Travel restrictions have been used in many countries around the world to stop the epidemic, and a combination of non-pharmaceutical interventions, such as early detection, isolation of cases, and travel restrictions, has been found to be more effective [14-16].

Recent studies have indicated SARS-CoV-2 to demonstrate 10-20 times greater affinity to angiotensin-converting enzyme 2 (ACE2) receptors compared to SARS-CoV-1, making it a much more virulent virus [17, 18]. This means fewer SARS-CoV-2 virions are necessarily needed to establish a successful infection in humans. Currently, the most common novel coronavirus strain is the Delta variant, which is characterized by strong infectivity, high viral load, and shortened incubation period [19], and is gradually becoming the main cause of the high incidence of COVID-19. It has been reported that the Delta strain can infect even after 14 seconds without contact [16]. Individuals infected with Delta variant could develop typical clinical symptoms 2 to 3 days after infection and could cause five generations of cases within 10 days with a R₀ (basic infected population) of 4.04 to 5.0. This has been reported to be much higher than that of the prototype strain that was isolated in Wuhan (2.2 to 3.77) [19, 20].

The current outbreak has spread rapidly, but the causes of the rapid occurrence of the outbreak and its spread to several provinces have not been reported. Therefore, the purpose of this study is to understand the epidemiological characteristics of COVID-19 cases in a typical tourist-related outbreak and explore the possible route for its transmission, so as to provide a reference for the prevention and control of COVID-19 in the post-pandemic era.

The COVID-19 virus sequencing results from the provincial CDC in China showed the virus responsible for the spread of the outbreak to be a Delta variant strain (B.1.617.2 evolutionary branch). Previously, no strains of this type of mutant virus have been found in China's indigenous new coronaviruses, suggesting the outbreak to be caused by the spread of an imported virus from outside China. Information on the local trajectory of confirmed cases in Ejin Banner, Inner Mongolia, pointed to the Cek port (a bilateral year-round land port open to China and Mongolia), which is a well-known tourist attraction, and multiple local coal drivers have been diagnosed.

Fig. (6). Schematic diagram of the transmission chains of the relevant parts of the COVID-19 tourist groups within three generations of cases in China.

The National Day holiday of China ushered in the peak of tourism in the area, and frequent activities of foreign tourists, who traveled between various scenic spots, hotels and restaurants, exacerbated the local epidemic. There were 50 cases (16.0%) with Ejin Banner tourism history, resulting in 68 second-generation cases, which accounted for about 1/3 of the total confirmed cases. The rest 2/3 were spread by subsequent crowd activities, so it can be seen that timely isolation of the source of infection is a significant prevention and control measure. In addition, the weather during that period was cooler and dryer, which may also have accelerated this outbreak, since cooler and dryer environments may possibly prolong the viruses' survival [1].

The transmission of the current outbreak spread between different tourist groups was mainly through public transport, involving multiple flights and trains. Among them, train D2746 had the largest number of cases, mainly found in carriage 6 with 18 confirmed cases and carriage 8 with 3 confirmed cases. Considering the ventilation system of trains [25], it is reasonable to believe that all these cases in carriage 8 were infected in the tourist area or waiting hall at the train station. Six ordinary passengers in carriage 6 who were not part of tourist groups were infected in the carriage. Experimental work by Doremalen et al. suggested that aerosol transmission of SARS-CoV-2 is plausible because the virus could survive in aerosols for hours and remain infectious on the surface of objects for up to several days, causing more severe transmission, especially in confined spaces [26]. Tourists from the same group often stayed in the same confined spaces, such as attractions, public transport means, hotels and restaurants, which led to the rapid spread of COVID-19. Besides, during train rides, passengers would like to talk, eat, and move, which may promote virus transmission in such proximity to viruses attached to aerosols and droplets [27]. In addition, frequent contact with surfaces, such as armrests and seats, could also be a potential route for COVID-19 infection [28]. The study by Hu et al. showed that the limited time interval between repeated seat use, disinfecting seats, and improving hand hygiene may help reduce the risk of transmission [29]. All of the evidence suggests the possibility and danger of COVID-19 transmission in public transportation, like train carriages. But whether or not being infected in the carriages could be related to many factors, such as indoor airflow, virus-specific factors, aerosol properties, host-specific factors, and so on [30]. The cases in carriage 8 did not cause secondary cases. We suspect that the ventilation system of the carriage was in continuous operation, which cause the indoor airflow to be in a state of circulation, making the virus concentration low and the masks and the bodies' own immunity sufficient to resist.

Fig. (7). 312 SARS-COV-2 exposure and timing of symptom onset in confirmed cases of China.

The median incubation period for the generation of cases in the current COVID-19 outbreak was 5 days, similar to pneumonia with β-attributable novel coronavirus infection [20]. Generally, the incubation period depends on the amount of virus reaching the body. The higher the viral load in the body, the shorter the incubation period [31]. Cases with no travel or residence history in the Ejin Banner tended to experience a longer incubation period and more dispersed distribution, whereas cases with a history of travel and residence in the Ejin Banner showed a shorter incubation period. This may be explained by their repeated exposure to the source of infection during their stay. As the number of infectious generations increased, the incubation period gradually lengthened, reaching about 9 days by the third generation of cases, and the longest incubation period reached 19 days, suggesting that the pathogenicity of the virus would become weaker generation by generation [32].

As the outbreak began in elderly tourist groups, the majority of infected in the early stages of the outbreak were aged 50 and older. Some studies have shown that the elderly population and those with an underlying disease are generally more susceptible to the virus [33]. The response and course of infectious diseases may be altered in the elderly due to immune senescence and the common occurrence of secondary immuno-deficiencies in old age [34]. Moreover, our study showed aged females to be more infected than males. This may have something to do with more females in the infected tourist groups. Some studies have investigated the population in mainland China, and the results showed females to be more susceptible than males [35]. In general, females are more susceptible to SARS-CoV-2 infection, especially in certain age groups. Infection with SARS-CoV-2 occurs primarily through the angiotensin-converting enzyme 2 (ACE2) receptor, which acts as a gateway for the virus to enter tissues [36]. ACE2 gene is located on the X chromosome. Therefore, female individuals should have a higher ACE2 level [37], which may be the reason why they are more likely to be infected with SARS-CoV-2 compared to males. Further studies on sex-related ACE2 enzyme activity are needed to test this hypothesis. In China, 90% of COVID-19 deaths occur in people over 60 years of age, and 20% of deaths are in people over 80 years of age [38]. But with the inter-generational spread of the epidemic, there is a tendency to infect younger people, even children under the age of 1. This is most likely related to the infection of their parents or family members [39, 40].

The limitations of this study mainly come from three aspects. First, although the sample size of 312 cases could meet the basic needs of estimating the incubation period, a more effective sample size would be stronger in inferring the conclusion. Second, the classification of a case as a primary or secondary case was based only on the time of symptom onset, which might lead to misclassification due to delayed symptom onset for some primary cases than that of secondary cases. Third, all the data were collected from the publicly available epidemiological survey and supplementary materials in the journal literature. Thus, there may be recall bias over the exposure time and onset time of cases.Finally, this study has analyzed a typical COVID-19 outbreak spread by tourist groups, which may give us some tips for future COVID-19 prevention to some degree.

In conclusion, the current outbreak occurred in Ejin Banner, suggesting it to be caused by an imported virus from abroad and spread throughout the country by tourist groups, making it a typical infection outbreak promoted by travel. Considering the faster spread and stronger infection rate, the regular surveillance of the epidemic situation should be strengthened so as to cut off the routes of mobile clusters of infection in a timely manner. Besides, data have proved the lower rate of serious illness among the newly infected COVID-19 cases, so there is a necessity to readjust the prevention and control measures in order to adapt the economic development, like higher precision of surveillance and prevention, strengthening effective ventilation in public places, and so on [21]. Our results further confirm that travel needs to be more strictly weighed in pandemics like COVID-19, and people need to pay more attention to the prevention against infectious diseases, particularly when traveling in a tourist group.