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Aerosol transmission, an indispensable route of COVID-19 spread: case study of a department-store cluster

Aerosol transmission, an indispensable route of COVID-19 spread: case study of a department-store... Front. Environ. Sci. Eng. 2021, 15(3): 46 https://doi.org/10.1007/s11783-021-1386-6 RESEARCH ARTICLE Aerosol transmission, an indispensable route of COVID-19 spread: case study of a department-store cluster 1,2 1,2 1,2 3 3 4 4 Guanyu Jiang , Can Wang (✉) , Lu Song , Xing Wang , Yangyang Zhou , Chunnan Fei , He Liu 1 School of Environmental Science and Engineering, Tianjin University, Tianjin 300350, China 2 Tianjin Key Laboratory of Indoor Air Environmental Quality Control, Tianjin 300350, China 3 Tianjin Haihe Hospital, Tianjin 300350, China 4 Tianjin Centers for Disease Control and Prevention, Tianjin 300350, China HIGH LIGHTS GRAPHIC A BSTRA CT � Aerosol transmission is an indispensable route of COVID-19 spread. � Different outbreak sites have different epidemio- logic feature. � SRAS-CoV-2 can exist for a long time in aerosol. � SRAS-CoV-2 RNA can be detected in aerosol in diverse places. � Some environmental factors can impact SARS- CoV-2 transportation in aerosol. ABSTRA CT AR TICL E IN F O Patients with COVID-19 have revealed a massive outbreak around the world, leading to widespread concerns in global scope. Figuring out the transmission route of COVID-19 is necessary to control Article history: further spread. We analyzed the data of 43 patients in Baodi Department Store (China) to supplement Received 17 June 2020 the transmission route and epidemiological characteristics of COVID-19 in a cluster outbreak. Incubation median was estimated to endure 5.95 days (2–13 days). Almost 76.3% of patients sought Revised 15 November 2020 medical attention immediately upon illness onset. The median period of illness onset to hospitalization Accepted 17 November 2020 and confirmation were 3.96 days (0–14) and 5.58 days (1–21), respectively. Patients with different Available online 25 December 2020 cluster case could demonstrate unique epidemiological characteristics due to the particularity of outbreak sites. SRAS-CoV-2 can be released into the surrounding air through patient’s respiratory tract activities, and can exist for a long time for long-distance transportation. SRAS-CoV-2 RNA can be Keywords: detected in aerosol in different sites, including isolation ward, general ward, outdoor, toilet, hallway, SARS-CoV-2 and crowded public area. Environmental factors influencing were analyzed and indicated that the COVID-19 SARS-CoV-2 transportation in aerosol was dependent on temperature, air humidity, ventilation rate and inactivating chemicals (ozone) content. As for the infection route of case numbers 2 to 6, 10, 13, Environmental factor 16, 17, 18, 20 and 23, we believe that aerosol transmission played a significant role in analyzing their Aerosol transmission exposure history and environmental conditions in Baodi Department Store. Aerosol transmission Epidemiologic characteristic could occur in some cluster cases when the environmental factors are suitable, and it is an indispensable route of COVID-19 spread. © The Author(s) 2021. This article is published with open access at link.springer.com and journal.hep. com.cn 19 with the novel coronavirus (SARS-CoV-2) has been 1 Introduction occurred at large scale. Then, the COVID-19 epidemic was rapidly spread the world (Bassetti, et al., 2020; Wang et al., Since December 2019, the fulminant epidemic of COVID- 2020;Zhu et al., 2020). The World Health Organization (WHO) has announced that COVID-19 outbreak has ✉ Corresponding author become pandemic from March 11, 2020. Excitingly, the E-mail: wangcan@tju.edu.cn increasing population of confirmed patients with COVID- Special Issue—Bioaerosol, Environment and Health (Responsible 19 in China was well controlled after series of strict control Editors: Can Wang, Jungho Hwang, Jingkun Jiang & Maosheng Yao) measures. But on the contrary, patients with COVID-19 2 Front. Environ. Sci. Eng. 2021, 15(3): 46 were also increasing sharply in many other countries, surveillance videos of Baodi Department Store from leading to widespread concerns in global scope (Bhaga- 20th–25th, January to determine whether the confirmed vathula et al., 2020; Lau et al., 2020; Liu et al., 2020a; salespersons contact directly. We made further result Phan et al., 2020; Rothe et al., 2020). The transmission analysis of results in this study based on the complete modes and epidemiological characteristics of COVID-19 epidemiological investigation results and the preliminary should be urgently explored to control its development. clinical diagnosis data. To protect personal privacy, we Droplet and contact transmission are confirmed ways of omitted identity information and replaced it with numbers. COVID-19 transmission, whereas aerosol transmission as a potential route requires further confirmation (Jiang et al., 2.2 Study population 2020a). In addition, the relative importance of the mode of these transmissions is still unclear (Tellier et al., 2019). We carefully screened out 43 cases that related to Baodi Case cluster exposure in hospitals, communities, depart- Department Store out of 131 confirmed cases based on the ment stores, and public transportation have continuously results of the epidemiological investigation. We retro- increased during the epidemic. These cases have counted a spectively analyzed the epidemiological characteristics of great number of available data. A cluster outbreak in Baodi confirmed 43 patients with COVID-19 who were in direct Department Store in Tianjin affected more than 40 persons, and indirect contact with Baodi Department Store, including salespersons, customers, and their close contacts. typically including: 6 salespersons (case numbers 1 to 6), However, a report that provides a satisfactory explanation 18 customers (case numbers 7 to 24), and 19 of their close of the feature of the epidemic outbreak in the area is not contacts (case numbers 25 to 43). The salespersons had currently available. Thus, the epidemiological character- sustained exposure in Baodi Department Store. The istics of COVID-19 in cluster case should be urgently customers were only present in the specific area for a explored, and its transmission routes in various cluster short-term, and their close contacts have realistically been cases should be analyzed. second-generation infections without potential exposure to Herein, we provide an analysis of available data on the Baodi Department Store. 43 confirmed patients of Baodi Department Store (China) cluster outbreak to clarify epidemiological characteristics 2.3 Epidemiologic analysis and transmission routes of COVID-19 explored in this typical cluster outbreak. We drew a Baodi Department Store plan with the accurate exposure site of salespersons and customers to describe the distribution of each functional zone and the infected area of 2 Methods patients in this store. We illustrated the ventilated conditions and the outbreak process of COVID-19 of 2.1 Data collection Baodi Department Store. We described the characteristics, including demographic characteristics, exposures, and Tianjin Centers for Disease Control and Prevention clinical diagnosis, of the infected patients onto a (TCDC) and Tianjin Haihe Hospital (THH) were author- standardized table. We drew a diagram to expound the itative organizations for the prevention and control of key date points relating to the epidemic identification of the COVID-19 epidemic in Tianjin, China. TCDC is in charge patients during the timeline of illness. We drew a box-plot of epidemiological investigations of suspected and con- to analyze the key periods of these patients from infection firmed patients. A detailed epidemiological investigation to illness, including incubation, the onset to the first will be carried out as soon as the suspected/confirmed medical therapy, onset to hospitalization, and onset to patient was admitted to the THH. confirmed date, confirmed utilizing the GRAPHPAD Through interviews with patients, relatives, close software. We combined surveillance video analysis and contacts and health care workers, as well as the compila- epidemiological investigation results to determine the tion of patient’s medical records, we collected the infection route of 43 patients, and draw conclusions information of patient’s age, gender, occupation, clinical about transmission relation and route among patients. symptoms, onset date, first medical treatment date, first hospital visit date, hospitalization date and clinical results. Investigators interviewed patient’s relatives as necessary to 3 Results determine the contact history two weeks before the onset of epidemic. To detect the infection source of the patients in Functional areas were divided into nine parts, including accurate ways as possible, we investigated the particular ornament, costume, shoes, jewelry, clock, small appliance, households and places where the patients went to visit for cosmetic, headwear and luggage areas in Baodi Depart- two weeks before outbreak onset and cross-analyzed the ment Store. The adjacent areas were separated at least exposure history of all patients. Specially, in the initial 1.5 m by a corridor, except for the costume and shoes area traceability work, TCDC immediately retrieved the and the jewelry and clock area. No distinct boundary was Guanyu Jiang et al. Aerosol transmission, an indispensable route of COVID-19 spread 3 present between the costume and shoes area and the number 1 showed infection during the incubation period jewelry and clock area (Fig. 1). Six salespersons were on January 20th (Fig. 2). Case numbers 2 and 3 were affected, and four of them (case numbers: 1, 4, 5, and 6) infected through long-term exposure to aerosol containing were working at the costume and shoes area, one (case SARS-CoV-2 released by the case number 1. Then, they number 3) was at the jewelry area, and one (case number 2) became the other major providers of airborne SARS-CoV- was assigned to the small appliance area. Eleven of the 2 starting two days before they showed clinical symptoms. customers (case numbers: 7, 8, 10, 11, 13, 14, 17, 18, 19, With the exception of case number 1, we explored the 20 and 23) have been to the costume and shoes area. Two infection route of other 42 patients and divided them into 3 groups: group 1: most likely infected through aerosol (cases numbers: 7 and 17) were to the jewelry area, and one transmission (case numbers: 2–6, 10, 13, 16, 17, 18, 20 and (case number 7) was to the headwear area. In addition, we 23), group 2: most likely infected through droplet or did not determine the accurate exposure areas of eight infected customers (case numbers: 9, 12, 15, 19, 21 and 24) contact transmission (case numbers: 7, 8, 11, 14 and 22), (Fig. 1). The Baodi Department Store exposure date of and group 3: infected through unclear transmission which salespersons and customers were marked as blue block and means patients possibly infected by all routes (case green circle, respectively. numbers: 9, 12, 15, 19, 21, 24, and 25–43). The median ages were 50 years (range: 10–90) for the Given that all of the salespersons, were infected through patients, 42 years (range: 34–52) for the salespersons, 50 prolonged exposure in Baodi Department Store (case years (range: 26–69) for the customers, and 51 years (range numbers 2 to 6), except for case number 1. Case number 43 10–90) for their close contacts. Among the 43 patients, 28 was an asymptomatic infected patient, and case number 33 (65.1%) were female. Among the 20 customers, 16 (80%) did not have a clear source, we could not concretely were female, and all of the infected salespersons were determine their infection time and incubation period. women. The patients infected in this case were middle- Therefore, we only analyzed the incubation of all patients, aged and elderly, major to report exposure to the costume except case numbers 2, 3, 4, 5, 6, 33, and 43. and shoes area, and major to be female. The clinical The median of incubation was estimated to be 5.95 days outcome was primarily slight and common types, whereas (2–13; Fig. 3(a)). Almost 76.3% of the patients immedi- few cases revealed a severe type (Tables 1(a) and 1(b)). ately sought for medical therapy as the outbreak onset, Case number 1 was regarded as the imported source of except for the patients who showed onset during an infection in this cluster outbreak. Case number 1 contacted isolation period (case numbers: 33, 34, 35, 38, and 43; Fig. 3(b)). The median periods of illness onset to with a hyperpyrexia patient on business from January 12 to hospitalization and to confirmation were 3.96 (0–14) and January 13, showed clinical symptoms on January 21st. 5.85 days (1–21), respectively (Figs. 3(c) and 3(d)). The Since all of the customers who had been to the store before January 20th had not been infected, we believed that result of this distribution period of customers, salespersons SARS-CoV-2 began to spread in the environment of Baodi and their close contacts were similar across all of the Department Store from January 20th. Therefore, case patients without a significant difference. Fig. 1 Functional areas division and patients’ exposure places in Baodi Department Store. The distance between two adjacent areas is at least 1.5 m, except that there is no distinct boundary between the costume and shoes area, the jewelry and clock area. Case numbers 9, 12, 15, 19, 23, 24, and 26 did not provide their accurate exposure area. 4 Front. Environ. Sci. Eng. 2021, 15(3): 46 Table 1(a) Characteristics of patients with COIVD-19 in Baodi Department Store Characteristic Total (N = 43) Salespersons (N = 6) Customers (N = 20) Close contacts (N = 17) Median age (range) — yr 50(10–90) 42(34–52) 50(26–69) 51(10–90) Age group — No./total No. (%)< 15 yr 1/43(2.3) 0/6(0) 0/20(0) 1/17(5.9) Age group — No./total No. (%)15–44 yr 16/43(37.2) 4/6(66.7) 6/20(30) 6/17(35.3) Age group — No./total No. (%)45–64 yr 17/43(39.5) 2/6(33.3) 11/20(55) 4/17(23.5) Age group — No./total No. (%)≥65 yr 9/43(20.9) 0/6(0) 3/20(15) 6/17(35.3) Female sex — No./total No. (%) 28/43(65.1) 0/6(0) 16/20(80) 6/17(35.3) Clinical outcome — No./total No. (%) Severe type 3/43(7.0) 2/6(33.3) 0/20(0) 1/17(5.9) Clinical outcome — No./total No. (%) Common 20/43(46.5) 2/6(33.3) 10/20(50) 8/17(47.1) type Clinical outcome — No./total No. (%) Slight type 20/43(46.5) 2/6(33.3) 10/20(50) 8/17(47.1) Table 1(b) Patients’ exposure in Baodi Department Store Exposure to Baodi Department Store Total (N = 26) Salespersons (N = 6) Customers (N = 20) Costume and shoes area— No./total No. (%) 13/26(50) 4/6(66.7) 9/20(45) Home appliance area — No./total No. (%) 1/26(3.8) 1/6(1.67) 0/20(0) Jewelry area — No./total No. (%) 3/26(11.5) 1/6(1.67) 2/20(10) Headwear area — No./total No. (%) 1/26(3.8) 0/6(0) 1/20(5) Unknown area — No./total No. (%) 10/26(38.5) 0/6(0) 10/20(50) Notes: Reduced denominators indicate missing data; Percentages may not total 100 because of rounding. Moreover, we have summarized some airborne SARS- is slightly different from the earlier researches, where they CoV-2 detection results in multiple environment air found that more males were infected rather than females samples, which proved that SARS-CoV-2 could be truly (Chen et al., 2020; Huang et al., 2020; Li et al., 2020; Xu carried by air and cause the possibility of aerosol et al., 2020a). Notably, the 22 out of all 26 infected transmission. salespersons and customers were female (84.6%), and half of them was in the costume area in Baodi Department Store. Out of the 17 close contacts of infected salespersons 4 Discussion and customers, 11 (58.8%) were males. The cluster outbreak of COVID-19 that occurred in Baodi Department, Although the previous retrospective studies have described a place where it showed more attractive to women. This the epidemiological, clinical, and transmission dynamics was a satisfactory explanation for the abnormal gender of COVID-19 patients in metropolitan areas, these proportion. characteristics have not also been analyzed in public Most of the patients were classified in middle- aged and cluster outbreak cases at the national level (Chan et al., older people, but no older than 65 years (76.7%). The 2020; Chen et al., 2020; Huang et al., 2020; Li et al., 2020; infected salespersons were generally young (Table 1). The McMichael et al., 2020;Pan et al., 2020; Xu et al., 2020a). clinical outcome was also consistent with other retro- Here, we make the supplemental transmission route spective studies: a large proportion of the patients had evaluation, dynamics and the epidemiological character- slight and common symptoms (Table 1) (Chen et al., 2020; istics of COVID-19 in a cluster outbreak. What we found, Huang et al., 2020; Li et al., 2020; Xu et al., 2020a). The it could supply a couple of significant points for further two severe cases were identified, which both appeared in analysis in a cluster outbreak, including elucidate routes of salespersons, indicating that long-term and stuffiness transmission, control further spread, assess the effective- exposure may increase the risk of infection with severe ness of control measures and predict the spread of infection symptoms. in the future. Although the time interval in illness onset to first medicine therapy were generally short (81.4% of patients 4.1 Epidemiological characteristics in this public cluster choosing to self-medicate within two days of symptoms), outbreak the time interval for hospitalization was long (average number of days was 4). Half of the patients were not Among the 43 COVID-19 patients in this cluster outbreak, hospitalized until at least 5 days of illness onset, and 23.3% we observed more females than males (Table 1). The result of the patients were confirmed after detection in multiple Guanyu Jiang et al. Aerosol transmission, an indispensable route of COVID-19 spread 5 Fig. 2 The key dates relating to the epidemic identification of COVID-19. The infection time was consistent with exposure time in Baodi Department Store for customers, because all of them had the single dangerous exposure place before the first onset. The infection time of salespersons was not confirmed due to their long-term exposure in Baodi Department Store, except case number 1. Case number 43 was an asymptomatic infected patient and case number 33 did not have a clear source, we could not determine their infection time and incubation period in a conclusive way. A circle with two colors means the two events happening on the same day. respiratory specimens (Fig. 3). Our finding suggests that in care, which increases the difficulty of case screening, and the early stages of illness, the identification and isolation of transmission risk. Increasing the awareness on actively the disease cases are difficult. Nine-tenths of patients prefer seeking medical attention is also important in the to self-medicating rather than seeking professional medical prevention and control of COVID-19. 6 Front. Environ. Sci. Eng. 2021, 15(3): 46 Fig. 3 Key periods distribution of epidemic development: (a) Incubation period; (b) Onset to the first medicine therapy; (c) Onset to hospitalization; (d) Onset to confirmation. The incubation period was analyzed through all customers, close contacts and case number 1 in Panel A, because the incubation of salespersons was unknown, except case number 1. The onset to medicine therapy in patient is shown in Panel B, except case numbers: 33, 34, 35, 38 and 43 (they were onset during isolation period). The period of onset to hospitalization is shown in Panel C. The period of onset to confirmation is shown in Panel D. 4.2 Transmission routes of SARS-CoV-2 in cluster from< 0.1–100 µm, while it can be dispersed large droplet outbreak particles (>100 µm) into air in more violent coughing, sneezing and talking activities. 3) The number of particles COVID-19 has been defined as a respiratory infectious produced by different respiratory activities is quite disease, and SARS-CoV-2 as a novel type of coronavirus is different: a cough can produce 3500 infectious particles, mainly released from a patient’s body into the air through which is equivalent to 5 minutes of normal breath the respiratory tract, and it could load on exhaled droplets emissions, and a sneeze can emit 1 million particles into for more isolated transportation (familiar with SARS-CoV the surrounding air. 4) Some pathogenic microorganism and MERS-CoV) (Rockx et al., 2020). Therefore, the can be emitted into the air via respiratory activities. droplets that emitted from the respiratory tract are used as Respiratory tract infectious diseases may exist in the starting point for the transmission of infectious multiple routes of transmission in many closed indoor diseases, and exploring its characteristics in the air is of environments, such as in ICU ward, steamship, department great significance for the analysis of disease transmission store and so on. In Baodi Department Store cluster routes. outbreak, the main potential transmission routes will be At present, there has been many studies clarifying the droplet transmission, contact transmission, and aerosol exhaled particle amount and size distribution of droplets transmission, if we do not take into account the use of the that discharged through the respiratory tract (Roy and toilet places and concentrate on the shopping area. In Milton, 2004; Fabian et al., 2008; Gralton et al., 2011; droplet transmission, the particle size is larger, and the Gralton et al., 2013; Milton et al., 2013). It could be propagation range is smaller (< 1.5 m) compared with that concluded as follows: 1) The size range of the droplets occurs in aerosol transmission (small particle size, and discharged through natural respiratory activities is less lager transportation range). But there is no specific affected by health status, gender, age and sex. 2) Almost all boundary between the droplet transmission and aerosol of respiratory activities (breathing, coughing, sneezing and transmission. According to the droplet size of 5 µm, WHO talking) can release droplets with a particle size ranging distinguishes the long-distance aerosol transmission Guanyu Jiang et al. Aerosol transmission, an indispensable route of COVID-19 spread 7 (£5 µm) and close-range droplet transmission (>5 µm) could be easily inhaled by the susceptible population or (Siegel et al., 2007;World Health Organization., 2014), deposit on the eyes, mouth or nasal mucosa thereby which is different with the 10 µm boundary defined by the causing the susceptible population being sick by droplet Infectious Diseases Society of America (IDSA) on whether transmission. 2) The susceptible population may contain the particles can be deposited in the lower respiratory tract the virus in their own hands by directly (contacting like, (Tellier et al., 2019). IDSA defines “respirable particles” as shaking hands) or indirectly (touching virus droplets having a diameter of 10 µm or less and the diameter of deposited on the object’s surface) ways, then, the virus “inspirable particles” is between 10 µm and 100 µm, while travels through the hands and inoculates themselves into the mucous membranes (eyes, nose and mouth), causing an almost of “inspirable particles” are deposited in the upper infection (Fig. 4). respiratory tract. Bioaerosol is a mixing decentralized system with aerodynamic diameter within 100 µm suspended in the 4.3 Aerosol transmission in the cluster outbreak air, which containing numbers of droplets, droplet nuclei and multiple inorganic compositions. Infectious particles Baodi Department Store is a 40-year-old commercial place no larger than 100 µm (such as respirable particles and located in the triangular region of Beijing, Tianjin, inspirable particles), could be spread over long distances Tangshan. Baodi Department Store opened as usual before th by bioaerosol. The susceptible population has infected by January 26th, 2020, and has been closed since January 26 , inhaling the pathogenic particles in the aerosol without due to the COVID-19 epidemic outbreak (Fig. 2). Chinese closing contact with the infected person, thus completing Center for Disease Control and Prevention published a the process of aerosol transmission. During the close report indicating that infectivity in the incubation period of contact between virus carriers and susceptible population, COVID-19 may occur in two days earlier before the first droplet transmission and contact transmission may happen: clinical onset of symptoms. This condition may seem to be 1) The large droplet particles have a better settling the reason of the minimum time interval between the performance and relative strong pathogenicity, which contact date and the onset date, endure three days in the Fig. 4 The transmission of exhaled virus between infected and susceptible population. Infected salesperson could release the virus into the environment by violent expiration (cough, sneeze, talk) or simply exhalation. Customer-I are infected through close encounter (occurred droplet transmission or contact transmission). Customer-II are infected through sniffing airborne SARS-CoV-2 (aerosol transmission). The transportation distance of droplet particles usually less than 1.5 meters. Inspirable and respirable particles could spread through the aerosol for long distances, while droplet particles could transform into inspirable or respirable by evaporation. Deposited droplet particles could be re-suspended through human activity and air agitation. 8 Front. Environ. Sci. Eng. 2021, 15(3): 46 infected customers (Fig. 2). The exposure of the 18 of 43 patients were most likely infected through aerosol infected customers in Baodi Department Store was transmission in this cluster outbreak. In the absence of concentrated from January 20–25th, 2020, it was the indirect infection, the half of persons (12/24) were highly period that the first three confirmed salespersons (case possible infected through aerosol transmission among the numbers: 1, 2 and 3) showed infectivity, and it was a time patients who were directly infected in Baodi Department for purchasing goods for the people in preparation for the Store. It suggested that aerosol transmission was an Spring Festival, suggesting a high population density indispensable and important route for the proliferation of (Fig. 2). COVID-19. Moreover, it is necessary to study the infection risk After analyzing the working dates and onset date of assessment of aerosol transmission for establishing these salespersons, we found that three salespersons (case prevention measures of COVID-19. Some previous reports numbers: 4, 5 and 6) showed clinical symptoms after January 29th, which suggested they were not infectious have performed the theoretical analysis for the health risk during January 20th–25th. Consequently, the only half of assessment on aerosol transmission (Buonanno et al., them could meet the requirements as the source of 2020; Zhang et al., 2020). In our subsequent research, the infection (from January 20th–22nd for case number 1, estimation of the infection risk together with the model January 20th–23rd for case number 2, and January 23rd– development of aerosol transmission will be performed. 24th for case number 3) during the period of January 20th– 24th. Therein, case number 1 was the first onset sales- 4.4 Detected SARS-CoV-2 in aerosol person and possessed the capacity to infect susceptible th from January 20 , 2020. Case numbers 2 and 3 were Many types of coronaviruses can survive and maintain working in diverse areas with the case number 1. Through their viral properties in the environment for 9 days (such as field visits, case numbers 1, 2 and 3 did not retain any MERS-CoV and SARS-CoV) (Kampf et al., 2020). relationship by each other, and any close contact behaviors Nowadays, multiple research teams have detected nucleic had not been recorded by the surveillance video (including, acid positive for SARS-CoV-2 RNA in aerosol in different talking, eating at the same place, and using the common sites (Table 2). toilet). Therefore, the routes of the droplet and contact Jiang et al. detected SARS-CoV-2 in the air where transmission can be essentially eliminated when speculated critically ill-patients were present (Jiang et al., 2020b). the infection routes of the case numbers 2 and 3. Guo et al. tested the air and surface swatches for the Case number 1 released SARS-CoV-2 that living in his purpose of confirming the distribution of SARS-CoV-2 in nasopharynx, respiratory tract and pulmonary to atmo- hospital wards. They found that the intensive-care unit was sphere by violent expiration (cough, sneeze, talk) or simply more polluted than the normal ward (Guo et al., 2020). The exhalation when infectivity was immediately shown. A airborne SARS-CoV-2 could not only be detected in part of SARS-CoV-2 which attached to nuclei particles in indoor, but also in the outdoor environment. Setti et al. aerosols could travel considerable distance (over several collected 34 of outdoor PM swatches from an industrial meters) by aerosol transmission. Therefore, we believed base in Bergamo Province, and 5 of them presented the that case numbers 2 and 3 were infected through long-term significant results of positivity after nucleic acid assay exposure to aerosol containing SARS-CoV-2. They were (Setti et al., 2020). They suggested outdoor air particles also the major providers of SARS-CoV-2 in aerosols after would be combined with airborne SARS-CoV-2 to form a confirmed COVID-19 infection and showing infectivity. polymer. This polymer had a low diffusion coefficient and Other patients in group 1 were similar with case numbers propagation durability under stable atmospheric condi- 2 and 3: any direct, in-plant, or indirect contact did not tions. Santarpia et al. have recently clarified that the definitely occur. Nevertheless, patients in group 1 were percent positive of air samples collected from the hallway infected through exposure to the aerosol and draw-in a and personal zone were 66.7% and 100%, respectively. number of SARS-CoV-2. Although the infectious char- And SARS-CoV-2 might be scattered in the environment acteristics of the incubation period of patients with in the form of expired particles when going to the toilet and COVID-19 were ambiguous, whether there was direct in contact with pollutants (Santarpia et al., 2020). As for contact between salespersons and customers could be the granulometric distribution of SARS-CoV-2 in an determined through exposure history analysis. Therefore, indoor air environment, Chia et al. sampled from three thetransmission routeofgroup2and3couldbe airborne infection isolation rooms in the general ward, and confirmed: there occurred in-plant or direct contact with SARS-CoV-2 positive particles with a particle size of an infection source in group 2; customers in group 3 did > 4 µm and 1–4 µm were detected in 2 of 3 general not provide their clear exposure area in the Baodi wards with 12 times for ventilation per hour (Chia et al., Department Store and close contacts may show various 2020). It provided that SARS-CoV-2 could exist in the air contact forms during their daily life (Fig. 5). and possess the capacity for long-term aerosol transmis- In summary, there is the evidence suggested that 12 out sion. Guanyu Jiang et al. Aerosol transmission, an indispensable route of COVID-19 spread 9 Fig. 5 The transmission chain in salespersons, customers and their close contacts Case numbers 1, 2 and 3 are not only salespersons, but also providers of SARS-CoV-2 in aerosols. Group 1 consists of case numbers: 2–6, 10, 13, 16, 17, 18, 20 and 23; Group 2 is composed by case numbers: 7, 8, 11, 14 and 22; Group 3 is constituted by case numbers: 9, 12, 16, 15, 19, 21, 24 and 27 to 43. Various modes of transmissions between salespersons and customers mean that these customers exposure areas in Baodi Department Store were unclear, while aerosol, droplet or contact transmission are all possible Table 2 Positive SARS-CoV-2 RNA in aerosol at several sites Sites Environmental description Positivity/Total Rate of positivity References Isolation ward Patients in isolation underwent tracheal intubation the day 1/20 – 5% Jiang et al., 2020b before the samples Intensive care unit Indoor air near the air outlet 5/14 – 35.7% Guo et al., 2020 Indoor air near the patients 8/18 – 44.4% Indoor air near the doctors’ office area 1/8 – 12.5% General ward Indoor air under the air inlet 2/13 – 15.4% An industrial site of Bergamo Province PM samples 5/34 – 14.7% Setti et al., 2020 Isolation ward Isolation of asymptomatic or mildly ill 80/107 – 74.8% Santarpia et al., 2020 Personal care unit For individuals requiring hospital care 34/40 – 85.0% Hallway Air Samples Sampling at the same time as the ward sample collection -/- – 66.7% Personal Air Samples low volume personal air samples around patients 7/7 – 100% Isolation ward Sampling at three isolation wards; 2/3 – 66.7% Chia et al., 2020 Samples from each room were pooled prior to analysis 4.5 Environmental factors impact on SARS-CoV-2 suitable environmental conditions such as worm, wet and transmission stuffiness could lengthen the concentration and survival time of airborne SARS-CoV-2. Liu et al. detected that The virus survival time in the environment is affected by airborne SARS-CoV-2 RNA concentration around the salinity, humidity, temperature, pH, solar radiation and air patients’ toilet, air was much higher than that in common pollution (Sooryanarain and Elankumaran, 2015), while wards with regular ventilation and in isolation units. They 10 Front. Environ. Sci. Eng. 2021, 15(3): 46 also found it was difficult to detect airborne SARS-CoV-2 symptoms, the incubation period and treatment time) are RNA in most public places, except for two department not significantly different among the epidemiological stores which tend to get crowded (Liu et al., 2020b). investigations in special cluster outbreak and large-scale Bukhari and Jameel found that 90% of the spread of areas. Based on the identification, the personal character- COVID-19 within a certain temperature (3°C–17°C) and istics (such as age, sex and occupation) indicated its 3 3 absolute humidity (4 g/m –9 g/m ) (Bukhari and Jameel, uniqueness due to the particularities of the outbreak site. 2020). They speculated that the high-level temperature and Most of the infected customers are females, and the age absolute humidity were to the disadvantage of SARS-CoV- range is relatively large, and the severe ill-patients are all 2 transmission. Similarly, the finding of Ma et al. who salespersons in Baodi Department Store cluster outbreak. showed the risk of SARS-CoV-2 was inversely propor- Droplet transmission, contact transmission, and aerosol tional to the relative humidity and directly proportional to transmission are main transmission routes in Baodi the diurnal temperature range (Ma et al., 2020). These Department Store cluster outbreak, if we ignore the toilet studies have strongly demonstrated that the transmission of places and focus on the shopping area. SRAS-CoV-2 can SARS-CoV-2 is influenced by ambient temperature and be released into the surrounding air through the patient’s humidity. respiratory tract activities and can exist for a long time for Moreover, the weather conditions and ambient air long-distance transportation. SRAS-CoV-2 RNA can be pollution could also impact SARS-CoV-2 transmission. detected in aerosol at several sites, such as in isolation Xu et al. found that a U-shaped association among the ward, general ward, outdoor, toilet, hallway, and a crowded estimated reproduction amount of COVID-19, outdoor UV public area. The influence of environmental factors was contact, wind speed, sediments, diurnal changed tempera- analyzed and indicated that the SARS-CoV-2 transporta- ture, SO and ozone (Xu et al., 2020b). Yao et al. tion in aerosol was dependent on the temperature, air deliberated the influence of local environmental factors on humidity, ventilation rate and inactivating chemicals the number of confirmed COVID-19 cases in 31 various (ozone) content. Indeed, the aerosol transmission is an regions of China, and the results suggested that the important route, leading to the infection of a part of environmental diffusion coefficient of SARS-CoV-2 patients in Baodi Department Store cluster case. continued to decrease following the ambient ozone concentration increases (Yao et al., 2020). Acknowledgements This research was supported by the Key Technologies In another research, the indoor virus concentration was R & D Program of Tianjin (No. 20ZXGBSY00100) affected by ventilation efficiency, and low-level ventilation rate would increase the danger of contact with potentially Conflicts of Interest All authors of this article have no conflicts of interest. infectious droplet nuclei (Myatt et al., 2004). No air Open Access This article is licensed under a Creative Commons conditioning system which was installed in Baodi Depart- Attribution 4.0 International License, which permits use, sharing, adaptation, ment Store, indicating no good ventilation conditions. distribution and reproduction in any medium or format, as long as you give They had to keep the door closed and interdict the natural appropriate credit to the original author(s) and the source, provide a link to the ventilation (thick windshield clothes were installed on the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative doors) to keep indoor rooms warm in the winter, which Commons licence, unless indicated otherwise in a credit line to the material. provided a suitable condition for the aerosol transmission If material is not included in the article’s Creative Commons licence and your of COVID-19. There also was no enough sunlight for intended use is not permitted by statutory regulation or exceeds the permitted indoor sterilization. No timely and regular sterilization has use, you will need to obtain permission directly from the copyright holder. To been conducted using disinfectants before the level 1 view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. warning implemented on January 24th, in Tianjin. However, the people were not aware or informed how to wear the mask during the period of this cluster outbreak, References even though some types of masks such as N95, KF94, medical, surgical masks could limit the transportation of Bassetti M, Vena A, Giacobbe D R (2020). The novel Chinese SARS-CoV-2 emitted by patient’s respiratory activities coronavirus (2019-nCoV) infections: Challenges for fighting the (Leung et al., 2020). Therefore, SARS-CoV-2 discharged storm. 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Aerosol transmission, an indispensable route of COVID-19 spread: case study of a department-store cluster

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Front. Environ. Sci. Eng. 2021, 15(3): 46 https://doi.org/10.1007/s11783-021-1386-6 RESEARCH ARTICLE Aerosol transmission, an indispensable route of COVID-19 spread: case study of a department-store cluster 1,2 1,2 1,2 3 3 4 4 Guanyu Jiang , Can Wang (✉) , Lu Song , Xing Wang , Yangyang Zhou , Chunnan Fei , He Liu 1 School of Environmental Science and Engineering, Tianjin University, Tianjin 300350, China 2 Tianjin Key Laboratory of Indoor Air Environmental Quality Control, Tianjin 300350, China 3 Tianjin Haihe Hospital, Tianjin 300350, China 4 Tianjin Centers for Disease Control and Prevention, Tianjin 300350, China HIGH LIGHTS GRAPHIC A BSTRA CT � Aerosol transmission is an indispensable route of COVID-19 spread. � Different outbreak sites have different epidemio- logic feature. � SRAS-CoV-2 can exist for a long time in aerosol. � SRAS-CoV-2 RNA can be detected in aerosol in diverse places. � Some environmental factors can impact SARS- CoV-2 transportation in aerosol. ABSTRA CT AR TICL E IN F O Patients with COVID-19 have revealed a massive outbreak around the world, leading to widespread concerns in global scope. Figuring out the transmission route of COVID-19 is necessary to control Article history: further spread. We analyzed the data of 43 patients in Baodi Department Store (China) to supplement Received 17 June 2020 the transmission route and epidemiological characteristics of COVID-19 in a cluster outbreak. Incubation median was estimated to endure 5.95 days (2–13 days). Almost 76.3% of patients sought Revised 15 November 2020 medical attention immediately upon illness onset. The median period of illness onset to hospitalization Accepted 17 November 2020 and confirmation were 3.96 days (0–14) and 5.58 days (1–21), respectively. Patients with different Available online 25 December 2020 cluster case could demonstrate unique epidemiological characteristics due to the particularity of outbreak sites. SRAS-CoV-2 can be released into the surrounding air through patient’s respiratory tract activities, and can exist for a long time for long-distance transportation. SRAS-CoV-2 RNA can be Keywords: detected in aerosol in different sites, including isolation ward, general ward, outdoor, toilet, hallway, SARS-CoV-2 and crowded public area. Environmental factors influencing were analyzed and indicated that the COVID-19 SARS-CoV-2 transportation in aerosol was dependent on temperature, air humidity, ventilation rate and inactivating chemicals (ozone) content. As for the infection route of case numbers 2 to 6, 10, 13, Environmental factor 16, 17, 18, 20 and 23, we believe that aerosol transmission played a significant role in analyzing their Aerosol transmission exposure history and environmental conditions in Baodi Department Store. Aerosol transmission Epidemiologic characteristic could occur in some cluster cases when the environmental factors are suitable, and it is an indispensable route of COVID-19 spread. © The Author(s) 2021. This article is published with open access at link.springer.com and journal.hep. com.cn 19 with the novel coronavirus (SARS-CoV-2) has been 1 Introduction occurred at large scale. Then, the COVID-19 epidemic was rapidly spread the world (Bassetti, et al., 2020; Wang et al., Since December 2019, the fulminant epidemic of COVID- 2020;Zhu et al., 2020). The World Health Organization (WHO) has announced that COVID-19 outbreak has ✉ Corresponding author become pandemic from March 11, 2020. Excitingly, the E-mail: wangcan@tju.edu.cn increasing population of confirmed patients with COVID- Special Issue—Bioaerosol, Environment and Health (Responsible 19 in China was well controlled after series of strict control Editors: Can Wang, Jungho Hwang, Jingkun Jiang & Maosheng Yao) measures. But on the contrary, patients with COVID-19 2 Front. Environ. Sci. Eng. 2021, 15(3): 46 were also increasing sharply in many other countries, surveillance videos of Baodi Department Store from leading to widespread concerns in global scope (Bhaga- 20th–25th, January to determine whether the confirmed vathula et al., 2020; Lau et al., 2020; Liu et al., 2020a; salespersons contact directly. We made further result Phan et al., 2020; Rothe et al., 2020). The transmission analysis of results in this study based on the complete modes and epidemiological characteristics of COVID-19 epidemiological investigation results and the preliminary should be urgently explored to control its development. clinical diagnosis data. To protect personal privacy, we Droplet and contact transmission are confirmed ways of omitted identity information and replaced it with numbers. COVID-19 transmission, whereas aerosol transmission as a potential route requires further confirmation (Jiang et al., 2.2 Study population 2020a). In addition, the relative importance of the mode of these transmissions is still unclear (Tellier et al., 2019). We carefully screened out 43 cases that related to Baodi Case cluster exposure in hospitals, communities, depart- Department Store out of 131 confirmed cases based on the ment stores, and public transportation have continuously results of the epidemiological investigation. We retro- increased during the epidemic. These cases have counted a spectively analyzed the epidemiological characteristics of great number of available data. A cluster outbreak in Baodi confirmed 43 patients with COVID-19 who were in direct Department Store in Tianjin affected more than 40 persons, and indirect contact with Baodi Department Store, including salespersons, customers, and their close contacts. typically including: 6 salespersons (case numbers 1 to 6), However, a report that provides a satisfactory explanation 18 customers (case numbers 7 to 24), and 19 of their close of the feature of the epidemic outbreak in the area is not contacts (case numbers 25 to 43). The salespersons had currently available. Thus, the epidemiological character- sustained exposure in Baodi Department Store. The istics of COVID-19 in cluster case should be urgently customers were only present in the specific area for a explored, and its transmission routes in various cluster short-term, and their close contacts have realistically been cases should be analyzed. second-generation infections without potential exposure to Herein, we provide an analysis of available data on the Baodi Department Store. 43 confirmed patients of Baodi Department Store (China) cluster outbreak to clarify epidemiological characteristics 2.3 Epidemiologic analysis and transmission routes of COVID-19 explored in this typical cluster outbreak. We drew a Baodi Department Store plan with the accurate exposure site of salespersons and customers to describe the distribution of each functional zone and the infected area of 2 Methods patients in this store. We illustrated the ventilated conditions and the outbreak process of COVID-19 of 2.1 Data collection Baodi Department Store. We described the characteristics, including demographic characteristics, exposures, and Tianjin Centers for Disease Control and Prevention clinical diagnosis, of the infected patients onto a (TCDC) and Tianjin Haihe Hospital (THH) were author- standardized table. We drew a diagram to expound the itative organizations for the prevention and control of key date points relating to the epidemic identification of the COVID-19 epidemic in Tianjin, China. TCDC is in charge patients during the timeline of illness. We drew a box-plot of epidemiological investigations of suspected and con- to analyze the key periods of these patients from infection firmed patients. A detailed epidemiological investigation to illness, including incubation, the onset to the first will be carried out as soon as the suspected/confirmed medical therapy, onset to hospitalization, and onset to patient was admitted to the THH. confirmed date, confirmed utilizing the GRAPHPAD Through interviews with patients, relatives, close software. We combined surveillance video analysis and contacts and health care workers, as well as the compila- epidemiological investigation results to determine the tion of patient’s medical records, we collected the infection route of 43 patients, and draw conclusions information of patient’s age, gender, occupation, clinical about transmission relation and route among patients. symptoms, onset date, first medical treatment date, first hospital visit date, hospitalization date and clinical results. Investigators interviewed patient’s relatives as necessary to 3 Results determine the contact history two weeks before the onset of epidemic. To detect the infection source of the patients in Functional areas were divided into nine parts, including accurate ways as possible, we investigated the particular ornament, costume, shoes, jewelry, clock, small appliance, households and places where the patients went to visit for cosmetic, headwear and luggage areas in Baodi Depart- two weeks before outbreak onset and cross-analyzed the ment Store. The adjacent areas were separated at least exposure history of all patients. Specially, in the initial 1.5 m by a corridor, except for the costume and shoes area traceability work, TCDC immediately retrieved the and the jewelry and clock area. No distinct boundary was Guanyu Jiang et al. Aerosol transmission, an indispensable route of COVID-19 spread 3 present between the costume and shoes area and the number 1 showed infection during the incubation period jewelry and clock area (Fig. 1). Six salespersons were on January 20th (Fig. 2). Case numbers 2 and 3 were affected, and four of them (case numbers: 1, 4, 5, and 6) infected through long-term exposure to aerosol containing were working at the costume and shoes area, one (case SARS-CoV-2 released by the case number 1. Then, they number 3) was at the jewelry area, and one (case number 2) became the other major providers of airborne SARS-CoV- was assigned to the small appliance area. Eleven of the 2 starting two days before they showed clinical symptoms. customers (case numbers: 7, 8, 10, 11, 13, 14, 17, 18, 19, With the exception of case number 1, we explored the 20 and 23) have been to the costume and shoes area. Two infection route of other 42 patients and divided them into 3 groups: group 1: most likely infected through aerosol (cases numbers: 7 and 17) were to the jewelry area, and one transmission (case numbers: 2–6, 10, 13, 16, 17, 18, 20 and (case number 7) was to the headwear area. In addition, we 23), group 2: most likely infected through droplet or did not determine the accurate exposure areas of eight infected customers (case numbers: 9, 12, 15, 19, 21 and 24) contact transmission (case numbers: 7, 8, 11, 14 and 22), (Fig. 1). The Baodi Department Store exposure date of and group 3: infected through unclear transmission which salespersons and customers were marked as blue block and means patients possibly infected by all routes (case green circle, respectively. numbers: 9, 12, 15, 19, 21, 24, and 25–43). The median ages were 50 years (range: 10–90) for the Given that all of the salespersons, were infected through patients, 42 years (range: 34–52) for the salespersons, 50 prolonged exposure in Baodi Department Store (case years (range: 26–69) for the customers, and 51 years (range numbers 2 to 6), except for case number 1. Case number 43 10–90) for their close contacts. Among the 43 patients, 28 was an asymptomatic infected patient, and case number 33 (65.1%) were female. Among the 20 customers, 16 (80%) did not have a clear source, we could not concretely were female, and all of the infected salespersons were determine their infection time and incubation period. women. The patients infected in this case were middle- Therefore, we only analyzed the incubation of all patients, aged and elderly, major to report exposure to the costume except case numbers 2, 3, 4, 5, 6, 33, and 43. and shoes area, and major to be female. The clinical The median of incubation was estimated to be 5.95 days outcome was primarily slight and common types, whereas (2–13; Fig. 3(a)). Almost 76.3% of the patients immedi- few cases revealed a severe type (Tables 1(a) and 1(b)). ately sought for medical therapy as the outbreak onset, Case number 1 was regarded as the imported source of except for the patients who showed onset during an infection in this cluster outbreak. Case number 1 contacted isolation period (case numbers: 33, 34, 35, 38, and 43; Fig. 3(b)). The median periods of illness onset to with a hyperpyrexia patient on business from January 12 to hospitalization and to confirmation were 3.96 (0–14) and January 13, showed clinical symptoms on January 21st. 5.85 days (1–21), respectively (Figs. 3(c) and 3(d)). The Since all of the customers who had been to the store before January 20th had not been infected, we believed that result of this distribution period of customers, salespersons SARS-CoV-2 began to spread in the environment of Baodi and their close contacts were similar across all of the Department Store from January 20th. Therefore, case patients without a significant difference. Fig. 1 Functional areas division and patients’ exposure places in Baodi Department Store. The distance between two adjacent areas is at least 1.5 m, except that there is no distinct boundary between the costume and shoes area, the jewelry and clock area. Case numbers 9, 12, 15, 19, 23, 24, and 26 did not provide their accurate exposure area. 4 Front. Environ. Sci. Eng. 2021, 15(3): 46 Table 1(a) Characteristics of patients with COIVD-19 in Baodi Department Store Characteristic Total (N = 43) Salespersons (N = 6) Customers (N = 20) Close contacts (N = 17) Median age (range) — yr 50(10–90) 42(34–52) 50(26–69) 51(10–90) Age group — No./total No. (%)< 15 yr 1/43(2.3) 0/6(0) 0/20(0) 1/17(5.9) Age group — No./total No. (%)15–44 yr 16/43(37.2) 4/6(66.7) 6/20(30) 6/17(35.3) Age group — No./total No. (%)45–64 yr 17/43(39.5) 2/6(33.3) 11/20(55) 4/17(23.5) Age group — No./total No. (%)≥65 yr 9/43(20.9) 0/6(0) 3/20(15) 6/17(35.3) Female sex — No./total No. (%) 28/43(65.1) 0/6(0) 16/20(80) 6/17(35.3) Clinical outcome — No./total No. (%) Severe type 3/43(7.0) 2/6(33.3) 0/20(0) 1/17(5.9) Clinical outcome — No./total No. (%) Common 20/43(46.5) 2/6(33.3) 10/20(50) 8/17(47.1) type Clinical outcome — No./total No. (%) Slight type 20/43(46.5) 2/6(33.3) 10/20(50) 8/17(47.1) Table 1(b) Patients’ exposure in Baodi Department Store Exposure to Baodi Department Store Total (N = 26) Salespersons (N = 6) Customers (N = 20) Costume and shoes area— No./total No. (%) 13/26(50) 4/6(66.7) 9/20(45) Home appliance area — No./total No. (%) 1/26(3.8) 1/6(1.67) 0/20(0) Jewelry area — No./total No. (%) 3/26(11.5) 1/6(1.67) 2/20(10) Headwear area — No./total No. (%) 1/26(3.8) 0/6(0) 1/20(5) Unknown area — No./total No. (%) 10/26(38.5) 0/6(0) 10/20(50) Notes: Reduced denominators indicate missing data; Percentages may not total 100 because of rounding. Moreover, we have summarized some airborne SARS- is slightly different from the earlier researches, where they CoV-2 detection results in multiple environment air found that more males were infected rather than females samples, which proved that SARS-CoV-2 could be truly (Chen et al., 2020; Huang et al., 2020; Li et al., 2020; Xu carried by air and cause the possibility of aerosol et al., 2020a). Notably, the 22 out of all 26 infected transmission. salespersons and customers were female (84.6%), and half of them was in the costume area in Baodi Department Store. Out of the 17 close contacts of infected salespersons 4 Discussion and customers, 11 (58.8%) were males. The cluster outbreak of COVID-19 that occurred in Baodi Department, Although the previous retrospective studies have described a place where it showed more attractive to women. This the epidemiological, clinical, and transmission dynamics was a satisfactory explanation for the abnormal gender of COVID-19 patients in metropolitan areas, these proportion. characteristics have not also been analyzed in public Most of the patients were classified in middle- aged and cluster outbreak cases at the national level (Chan et al., older people, but no older than 65 years (76.7%). The 2020; Chen et al., 2020; Huang et al., 2020; Li et al., 2020; infected salespersons were generally young (Table 1). The McMichael et al., 2020;Pan et al., 2020; Xu et al., 2020a). clinical outcome was also consistent with other retro- Here, we make the supplemental transmission route spective studies: a large proportion of the patients had evaluation, dynamics and the epidemiological character- slight and common symptoms (Table 1) (Chen et al., 2020; istics of COVID-19 in a cluster outbreak. What we found, Huang et al., 2020; Li et al., 2020; Xu et al., 2020a). The it could supply a couple of significant points for further two severe cases were identified, which both appeared in analysis in a cluster outbreak, including elucidate routes of salespersons, indicating that long-term and stuffiness transmission, control further spread, assess the effective- exposure may increase the risk of infection with severe ness of control measures and predict the spread of infection symptoms. in the future. Although the time interval in illness onset to first medicine therapy were generally short (81.4% of patients 4.1 Epidemiological characteristics in this public cluster choosing to self-medicate within two days of symptoms), outbreak the time interval for hospitalization was long (average number of days was 4). Half of the patients were not Among the 43 COVID-19 patients in this cluster outbreak, hospitalized until at least 5 days of illness onset, and 23.3% we observed more females than males (Table 1). The result of the patients were confirmed after detection in multiple Guanyu Jiang et al. Aerosol transmission, an indispensable route of COVID-19 spread 5 Fig. 2 The key dates relating to the epidemic identification of COVID-19. The infection time was consistent with exposure time in Baodi Department Store for customers, because all of them had the single dangerous exposure place before the first onset. The infection time of salespersons was not confirmed due to their long-term exposure in Baodi Department Store, except case number 1. Case number 43 was an asymptomatic infected patient and case number 33 did not have a clear source, we could not determine their infection time and incubation period in a conclusive way. A circle with two colors means the two events happening on the same day. respiratory specimens (Fig. 3). Our finding suggests that in care, which increases the difficulty of case screening, and the early stages of illness, the identification and isolation of transmission risk. Increasing the awareness on actively the disease cases are difficult. Nine-tenths of patients prefer seeking medical attention is also important in the to self-medicating rather than seeking professional medical prevention and control of COVID-19. 6 Front. Environ. Sci. Eng. 2021, 15(3): 46 Fig. 3 Key periods distribution of epidemic development: (a) Incubation period; (b) Onset to the first medicine therapy; (c) Onset to hospitalization; (d) Onset to confirmation. The incubation period was analyzed through all customers, close contacts and case number 1 in Panel A, because the incubation of salespersons was unknown, except case number 1. The onset to medicine therapy in patient is shown in Panel B, except case numbers: 33, 34, 35, 38 and 43 (they were onset during isolation period). The period of onset to hospitalization is shown in Panel C. The period of onset to confirmation is shown in Panel D. 4.2 Transmission routes of SARS-CoV-2 in cluster from< 0.1–100 µm, while it can be dispersed large droplet outbreak particles (>100 µm) into air in more violent coughing, sneezing and talking activities. 3) The number of particles COVID-19 has been defined as a respiratory infectious produced by different respiratory activities is quite disease, and SARS-CoV-2 as a novel type of coronavirus is different: a cough can produce 3500 infectious particles, mainly released from a patient’s body into the air through which is equivalent to 5 minutes of normal breath the respiratory tract, and it could load on exhaled droplets emissions, and a sneeze can emit 1 million particles into for more isolated transportation (familiar with SARS-CoV the surrounding air. 4) Some pathogenic microorganism and MERS-CoV) (Rockx et al., 2020). Therefore, the can be emitted into the air via respiratory activities. droplets that emitted from the respiratory tract are used as Respiratory tract infectious diseases may exist in the starting point for the transmission of infectious multiple routes of transmission in many closed indoor diseases, and exploring its characteristics in the air is of environments, such as in ICU ward, steamship, department great significance for the analysis of disease transmission store and so on. In Baodi Department Store cluster routes. outbreak, the main potential transmission routes will be At present, there has been many studies clarifying the droplet transmission, contact transmission, and aerosol exhaled particle amount and size distribution of droplets transmission, if we do not take into account the use of the that discharged through the respiratory tract (Roy and toilet places and concentrate on the shopping area. In Milton, 2004; Fabian et al., 2008; Gralton et al., 2011; droplet transmission, the particle size is larger, and the Gralton et al., 2013; Milton et al., 2013). It could be propagation range is smaller (< 1.5 m) compared with that concluded as follows: 1) The size range of the droplets occurs in aerosol transmission (small particle size, and discharged through natural respiratory activities is less lager transportation range). But there is no specific affected by health status, gender, age and sex. 2) Almost all boundary between the droplet transmission and aerosol of respiratory activities (breathing, coughing, sneezing and transmission. According to the droplet size of 5 µm, WHO talking) can release droplets with a particle size ranging distinguishes the long-distance aerosol transmission Guanyu Jiang et al. Aerosol transmission, an indispensable route of COVID-19 spread 7 (£5 µm) and close-range droplet transmission (>5 µm) could be easily inhaled by the susceptible population or (Siegel et al., 2007;World Health Organization., 2014), deposit on the eyes, mouth or nasal mucosa thereby which is different with the 10 µm boundary defined by the causing the susceptible population being sick by droplet Infectious Diseases Society of America (IDSA) on whether transmission. 2) The susceptible population may contain the particles can be deposited in the lower respiratory tract the virus in their own hands by directly (contacting like, (Tellier et al., 2019). IDSA defines “respirable particles” as shaking hands) or indirectly (touching virus droplets having a diameter of 10 µm or less and the diameter of deposited on the object’s surface) ways, then, the virus “inspirable particles” is between 10 µm and 100 µm, while travels through the hands and inoculates themselves into the mucous membranes (eyes, nose and mouth), causing an almost of “inspirable particles” are deposited in the upper infection (Fig. 4). respiratory tract. Bioaerosol is a mixing decentralized system with aerodynamic diameter within 100 µm suspended in the 4.3 Aerosol transmission in the cluster outbreak air, which containing numbers of droplets, droplet nuclei and multiple inorganic compositions. Infectious particles Baodi Department Store is a 40-year-old commercial place no larger than 100 µm (such as respirable particles and located in the triangular region of Beijing, Tianjin, inspirable particles), could be spread over long distances Tangshan. Baodi Department Store opened as usual before th by bioaerosol. The susceptible population has infected by January 26th, 2020, and has been closed since January 26 , inhaling the pathogenic particles in the aerosol without due to the COVID-19 epidemic outbreak (Fig. 2). Chinese closing contact with the infected person, thus completing Center for Disease Control and Prevention published a the process of aerosol transmission. During the close report indicating that infectivity in the incubation period of contact between virus carriers and susceptible population, COVID-19 may occur in two days earlier before the first droplet transmission and contact transmission may happen: clinical onset of symptoms. This condition may seem to be 1) The large droplet particles have a better settling the reason of the minimum time interval between the performance and relative strong pathogenicity, which contact date and the onset date, endure three days in the Fig. 4 The transmission of exhaled virus between infected and susceptible population. Infected salesperson could release the virus into the environment by violent expiration (cough, sneeze, talk) or simply exhalation. Customer-I are infected through close encounter (occurred droplet transmission or contact transmission). Customer-II are infected through sniffing airborne SARS-CoV-2 (aerosol transmission). The transportation distance of droplet particles usually less than 1.5 meters. Inspirable and respirable particles could spread through the aerosol for long distances, while droplet particles could transform into inspirable or respirable by evaporation. Deposited droplet particles could be re-suspended through human activity and air agitation. 8 Front. Environ. Sci. Eng. 2021, 15(3): 46 infected customers (Fig. 2). The exposure of the 18 of 43 patients were most likely infected through aerosol infected customers in Baodi Department Store was transmission in this cluster outbreak. In the absence of concentrated from January 20–25th, 2020, it was the indirect infection, the half of persons (12/24) were highly period that the first three confirmed salespersons (case possible infected through aerosol transmission among the numbers: 1, 2 and 3) showed infectivity, and it was a time patients who were directly infected in Baodi Department for purchasing goods for the people in preparation for the Store. It suggested that aerosol transmission was an Spring Festival, suggesting a high population density indispensable and important route for the proliferation of (Fig. 2). COVID-19. Moreover, it is necessary to study the infection risk After analyzing the working dates and onset date of assessment of aerosol transmission for establishing these salespersons, we found that three salespersons (case prevention measures of COVID-19. Some previous reports numbers: 4, 5 and 6) showed clinical symptoms after January 29th, which suggested they were not infectious have performed the theoretical analysis for the health risk during January 20th–25th. Consequently, the only half of assessment on aerosol transmission (Buonanno et al., them could meet the requirements as the source of 2020; Zhang et al., 2020). In our subsequent research, the infection (from January 20th–22nd for case number 1, estimation of the infection risk together with the model January 20th–23rd for case number 2, and January 23rd– development of aerosol transmission will be performed. 24th for case number 3) during the period of January 20th– 24th. Therein, case number 1 was the first onset sales- 4.4 Detected SARS-CoV-2 in aerosol person and possessed the capacity to infect susceptible th from January 20 , 2020. Case numbers 2 and 3 were Many types of coronaviruses can survive and maintain working in diverse areas with the case number 1. Through their viral properties in the environment for 9 days (such as field visits, case numbers 1, 2 and 3 did not retain any MERS-CoV and SARS-CoV) (Kampf et al., 2020). relationship by each other, and any close contact behaviors Nowadays, multiple research teams have detected nucleic had not been recorded by the surveillance video (including, acid positive for SARS-CoV-2 RNA in aerosol in different talking, eating at the same place, and using the common sites (Table 2). toilet). Therefore, the routes of the droplet and contact Jiang et al. detected SARS-CoV-2 in the air where transmission can be essentially eliminated when speculated critically ill-patients were present (Jiang et al., 2020b). the infection routes of the case numbers 2 and 3. Guo et al. tested the air and surface swatches for the Case number 1 released SARS-CoV-2 that living in his purpose of confirming the distribution of SARS-CoV-2 in nasopharynx, respiratory tract and pulmonary to atmo- hospital wards. They found that the intensive-care unit was sphere by violent expiration (cough, sneeze, talk) or simply more polluted than the normal ward (Guo et al., 2020). The exhalation when infectivity was immediately shown. A airborne SARS-CoV-2 could not only be detected in part of SARS-CoV-2 which attached to nuclei particles in indoor, but also in the outdoor environment. Setti et al. aerosols could travel considerable distance (over several collected 34 of outdoor PM swatches from an industrial meters) by aerosol transmission. Therefore, we believed base in Bergamo Province, and 5 of them presented the that case numbers 2 and 3 were infected through long-term significant results of positivity after nucleic acid assay exposure to aerosol containing SARS-CoV-2. They were (Setti et al., 2020). They suggested outdoor air particles also the major providers of SARS-CoV-2 in aerosols after would be combined with airborne SARS-CoV-2 to form a confirmed COVID-19 infection and showing infectivity. polymer. This polymer had a low diffusion coefficient and Other patients in group 1 were similar with case numbers propagation durability under stable atmospheric condi- 2 and 3: any direct, in-plant, or indirect contact did not tions. Santarpia et al. have recently clarified that the definitely occur. Nevertheless, patients in group 1 were percent positive of air samples collected from the hallway infected through exposure to the aerosol and draw-in a and personal zone were 66.7% and 100%, respectively. number of SARS-CoV-2. Although the infectious char- And SARS-CoV-2 might be scattered in the environment acteristics of the incubation period of patients with in the form of expired particles when going to the toilet and COVID-19 were ambiguous, whether there was direct in contact with pollutants (Santarpia et al., 2020). As for contact between salespersons and customers could be the granulometric distribution of SARS-CoV-2 in an determined through exposure history analysis. Therefore, indoor air environment, Chia et al. sampled from three thetransmission routeofgroup2and3couldbe airborne infection isolation rooms in the general ward, and confirmed: there occurred in-plant or direct contact with SARS-CoV-2 positive particles with a particle size of an infection source in group 2; customers in group 3 did > 4 µm and 1–4 µm were detected in 2 of 3 general not provide their clear exposure area in the Baodi wards with 12 times for ventilation per hour (Chia et al., Department Store and close contacts may show various 2020). It provided that SARS-CoV-2 could exist in the air contact forms during their daily life (Fig. 5). and possess the capacity for long-term aerosol transmis- In summary, there is the evidence suggested that 12 out sion. Guanyu Jiang et al. Aerosol transmission, an indispensable route of COVID-19 spread 9 Fig. 5 The transmission chain in salespersons, customers and their close contacts Case numbers 1, 2 and 3 are not only salespersons, but also providers of SARS-CoV-2 in aerosols. Group 1 consists of case numbers: 2–6, 10, 13, 16, 17, 18, 20 and 23; Group 2 is composed by case numbers: 7, 8, 11, 14 and 22; Group 3 is constituted by case numbers: 9, 12, 16, 15, 19, 21, 24 and 27 to 43. Various modes of transmissions between salespersons and customers mean that these customers exposure areas in Baodi Department Store were unclear, while aerosol, droplet or contact transmission are all possible Table 2 Positive SARS-CoV-2 RNA in aerosol at several sites Sites Environmental description Positivity/Total Rate of positivity References Isolation ward Patients in isolation underwent tracheal intubation the day 1/20 – 5% Jiang et al., 2020b before the samples Intensive care unit Indoor air near the air outlet 5/14 – 35.7% Guo et al., 2020 Indoor air near the patients 8/18 – 44.4% Indoor air near the doctors’ office area 1/8 – 12.5% General ward Indoor air under the air inlet 2/13 – 15.4% An industrial site of Bergamo Province PM samples 5/34 – 14.7% Setti et al., 2020 Isolation ward Isolation of asymptomatic or mildly ill 80/107 – 74.8% Santarpia et al., 2020 Personal care unit For individuals requiring hospital care 34/40 – 85.0% Hallway Air Samples Sampling at the same time as the ward sample collection -/- – 66.7% Personal Air Samples low volume personal air samples around patients 7/7 – 100% Isolation ward Sampling at three isolation wards; 2/3 – 66.7% Chia et al., 2020 Samples from each room were pooled prior to analysis 4.5 Environmental factors impact on SARS-CoV-2 suitable environmental conditions such as worm, wet and transmission stuffiness could lengthen the concentration and survival time of airborne SARS-CoV-2. Liu et al. detected that The virus survival time in the environment is affected by airborne SARS-CoV-2 RNA concentration around the salinity, humidity, temperature, pH, solar radiation and air patients’ toilet, air was much higher than that in common pollution (Sooryanarain and Elankumaran, 2015), while wards with regular ventilation and in isolation units. They 10 Front. Environ. Sci. Eng. 2021, 15(3): 46 also found it was difficult to detect airborne SARS-CoV-2 symptoms, the incubation period and treatment time) are RNA in most public places, except for two department not significantly different among the epidemiological stores which tend to get crowded (Liu et al., 2020b). investigations in special cluster outbreak and large-scale Bukhari and Jameel found that 90% of the spread of areas. Based on the identification, the personal character- COVID-19 within a certain temperature (3°C–17°C) and istics (such as age, sex and occupation) indicated its 3 3 absolute humidity (4 g/m –9 g/m ) (Bukhari and Jameel, uniqueness due to the particularities of the outbreak site. 2020). They speculated that the high-level temperature and Most of the infected customers are females, and the age absolute humidity were to the disadvantage of SARS-CoV- range is relatively large, and the severe ill-patients are all 2 transmission. Similarly, the finding of Ma et al. who salespersons in Baodi Department Store cluster outbreak. showed the risk of SARS-CoV-2 was inversely propor- Droplet transmission, contact transmission, and aerosol tional to the relative humidity and directly proportional to transmission are main transmission routes in Baodi the diurnal temperature range (Ma et al., 2020). These Department Store cluster outbreak, if we ignore the toilet studies have strongly demonstrated that the transmission of places and focus on the shopping area. SRAS-CoV-2 can SARS-CoV-2 is influenced by ambient temperature and be released into the surrounding air through the patient’s humidity. respiratory tract activities and can exist for a long time for Moreover, the weather conditions and ambient air long-distance transportation. SRAS-CoV-2 RNA can be pollution could also impact SARS-CoV-2 transmission. detected in aerosol at several sites, such as in isolation Xu et al. found that a U-shaped association among the ward, general ward, outdoor, toilet, hallway, and a crowded estimated reproduction amount of COVID-19, outdoor UV public area. The influence of environmental factors was contact, wind speed, sediments, diurnal changed tempera- analyzed and indicated that the SARS-CoV-2 transporta- ture, SO and ozone (Xu et al., 2020b). Yao et al. tion in aerosol was dependent on the temperature, air deliberated the influence of local environmental factors on humidity, ventilation rate and inactivating chemicals the number of confirmed COVID-19 cases in 31 various (ozone) content. Indeed, the aerosol transmission is an regions of China, and the results suggested that the important route, leading to the infection of a part of environmental diffusion coefficient of SARS-CoV-2 patients in Baodi Department Store cluster case. continued to decrease following the ambient ozone concentration increases (Yao et al., 2020). Acknowledgements This research was supported by the Key Technologies In another research, the indoor virus concentration was R & D Program of Tianjin (No. 20ZXGBSY00100) affected by ventilation efficiency, and low-level ventilation rate would increase the danger of contact with potentially Conflicts of Interest All authors of this article have no conflicts of interest. infectious droplet nuclei (Myatt et al., 2004). No air Open Access This article is licensed under a Creative Commons conditioning system which was installed in Baodi Depart- Attribution 4.0 International License, which permits use, sharing, adaptation, ment Store, indicating no good ventilation conditions. distribution and reproduction in any medium or format, as long as you give They had to keep the door closed and interdict the natural appropriate credit to the original author(s) and the source, provide a link to the ventilation (thick windshield clothes were installed on the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative doors) to keep indoor rooms warm in the winter, which Commons licence, unless indicated otherwise in a credit line to the material. provided a suitable condition for the aerosol transmission If material is not included in the article’s Creative Commons licence and your of COVID-19. There also was no enough sunlight for intended use is not permitted by statutory regulation or exceeds the permitted indoor sterilization. No timely and regular sterilization has use, you will need to obtain permission directly from the copyright holder. To been conducted using disinfectants before the level 1 view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. warning implemented on January 24th, in Tianjin. However, the people were not aware or informed how to wear the mask during the period of this cluster outbreak, References even though some types of masks such as N95, KF94, medical, surgical masks could limit the transportation of Bassetti M, Vena A, Giacobbe D R (2020). The novel Chinese SARS-CoV-2 emitted by patient’s respiratory activities coronavirus (2019-nCoV) infections: Challenges for fighting the (Leung et al., 2020). Therefore, SARS-CoV-2 discharged storm. 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Journal

Frontiers of Environmental Science & Engineering – Springer Journals

Published: Jun 1, 2021

Keywords: SARS-CoV-2; COVID-19; Environmental factor; Aerosol transmission; Epidemiologic characteristic

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