key: cord-0835090-xx35dq00
authors: Liu, Tao; Gong, Dexin; Xiao, Jianpeng; Hu, Jianxiong; He, Guanhao; Rong, Zuhua; Ma, Wenjun
title: Cluster infections play important roles in the rapid evolution of COVID-19 transmission: a systematic review
date: 2020-08-05
journal: Int J Infect Dis
DOI: 10.1016/j.ijid.2020.07.073
sha: efb9f735e0085fdd42d4d94d8d8303897d5dbf02
doc_id: 835090
cord_uid: xx35dq00

OBJECTIVES: To summarize the major types of cluster infections of SARS-CoV-2 all over the world through a comprehensive systematic review. METHODS: We searched all of the studies published between January 1, 2020 and June 15, 2020, on the cluster infections of COVID-19 in the English electronic databases including PubMed, Embase, Web of Knowledge, and Scopus. All included studies were independently screened and evaluated by two authors, and information of each study was extracted using a standard form. RESULTS: A total of 65 studies were included in this study which involved 108 cluster infections from 13 countries, areas or territories. Out of the cluster infections, 72(66.7%) were reported in China. The major types of cluster infections include family cluster, community transmission, nosocomial infection, transmission in gathering activities, on transportations, in shopping malls, on conference, among tourists, in religious organizations, among workers, in prisons, office, and in nursing home. CONCLUSIONS: The SARS-CoV-2 can be transmitted in various circumstances, and cluster infection plays important roles in the rapid evolution of COVID-19 transmission. Prevention and control measures such as social distance must be strictly implemented to contain the cluster infections.

In December of 2019, an emerging infectious disease named as COVID-19 caused by SARS-CoV-2 virus was first reported in Wuhan, Hubei Province, China (Epidemiology Working Group for NCIP Epidemic Response, 2020). Since then, more and more countries also reported COVID-19 all over the world . The World Health Organization (WHO) has declared the COVID-19 a public health emergency of international concern January 30, 2020 (WHO, 2020a) , and further declared the COVID-19 a pandemic on March 11,2020 (WHO, 2020b . As of June 24, 2020, a total of 9,273,773 confirmed cases with 477,807 deaths were in more than 210 countries, areas or territories (Hopkins, 2020) .

Although the whole world is endeavoring to contain COVID-19, and several countries have successfully controlled the epidemic, this novel norovirus is still widely spreading in many countries.

Since the late of May 2020, daily confirmed cases excessed 100,000, and had an increase trend worldwide, which indicates that epidemic of COVID-19 is still serious. Additionally, studies have reported characteristics of SARS-CoV-2 different from other coronaviruses (Tan et al., 2005) . For example, people could be infected with SARS-CoV-2 by asymptomatic carries and presymptomatic patients , which could prolong the infectious period.

Meteorological factors including temperature and UV radiation may not impact the transmission risk of SARS-CoV-2 (Yao and Pan, 2020) . Several super-spreaders of COVID-19 were reported in settings such as religious organizations (Wikipedia, 2020) . These characteristics partially contribute the high transmission risk of SARS-CoV-2, and indicate that more research workers are needed to further understand this infectious disease.

J o u r n a l P r e -p r o o f eligible records and be further assessed. Reference lists of full-text articles were also screened for additional publications. Two authors (T. L and DX. G) searched and screened independently to identify eligible studies. Disagreement between them were reconciled by a third author.

Studies were included if they reported an aggregation of COVID-19 cases in any settings, such as in household, vehicle, shopping mall, community, etc. The exclusion criteria were editorial, comment, and letter or articles with irrelevant topics. For studies sharing a same case series, the one with the most meaningful information was included.

The following information were independently extracted by two authors: author names, time of publish, study setting, type of cluster infection, and number of infections involved. Differences were addressed by a third author. Authors of studies with unclarified data were contacted to update information.

The search strategy initially identified 981 records and 5 reference was added by referring to reference sections. We excluded 500 duplicated articles through screening their titles and abstracts.

In the left 486 articles, 417 articles were excluded because these articles are related to epidemiological characteristics of COVID-19 cases (n=90), clinical characteristics or therapy (n=115), spatial analysis (n=10), policies or recommendations (n=54), genome and phylogeny J o u r n a l P r e -p r o o f (n=25), testing/screening/immunity (n=14), or others such as review, comment (n=109). In the 69 potentially eligible studies, we further excluded four repeated studies, and 65 studies were finally included in this study (Figure 1) . The included 65 studies involved 108 cluster infections in 13 regions. Out of the cluster infections, 72(66.7%) were reported in China, and 58(53.7%) were family clusters ( Table 1 ). The major types of clusters are family cluster (62), in community (4), nosocomial infection (3), transmission in gathering activities (15), on transportations (6), in shopping malls (3), on conference (4), during tourists (6), and in religious organizations (5).

Family is the dominated circumstance where the cluster of SARS-CoV-2 infection occurs. World

Health Organization reported that 78-85% of infection clusters occurred in families in the early stage of COIVD-19 epidemic in China (Mission, 2020) . The first family cluster was reported as early as on January 24, 2020 in Shenzhen, China, in which a household member who had no travel history to Wuhan or exposure to wild animals were infected by a COVID-19 case who traveled from Wuhan (Chan et al., 2020) . This is the first study that confirmed the transmission of SARS-CoV-2 from human to human. Since then, many family clusters of COVID-19 were reported across the world , Chan et al., 2020 , Wolf et al., 2020 , Chiu et al., 2020 , Qiu et al., 2020a , Ji et al., 2020 , Phan et al., 2020 , Du et al., 2020 , Jiang et al., 2020a , Liu et al., 2020c , Gao et al., 2020a , Yu et al., 2020 , Tong et al., 2020 , Qiu et al., 2020b , Luo et al., 2020 , Lu et al., 2020a J o u r n a l P r e -p r o o f 7 2020b, Huang et al., 2020c , Gao et al., 2020b , Bai et al., 2020a , Liu et al., 2020d , Bai et al., 2020b , Jiang et al., 2020b , Ghinai et al., 2020 , Zhang et al., 2020c , Lu et al., 2020b , Cao et al., 2020 . Family cluster usually has higher risk of infection in household members due to their close and frequent contacts (Bi et al., 2020) . Hence, prevention of infection among household members is an important strategy to contain the transmission of COVID-19 worldwide. For example, it is crucial to quarantine their close contacts in families of confirmed COVID-19 cases and detect SARS-CoV-2 as early as possible.

Community transmission is one of the most important modes facilitating the widespread of COVID-19. Several studies have reported community transmission cases (Ghinai et al., 2020 , Lu et al., 2020b , Liu et al., 2020e, Kim et al., 2020 , The Centre for Health Protection, 2020). For example, the Centers for Disease Control and Prevention (CDC) reported community transmissions occurred in Chicago in April, in which 16 COVID-19 cases were infected in nonhousehold gatherings (a birthday party, funeral and church attendance) (Ghinai et al., 2020) . These cases indicate the importance of social distancing for prevention of COVID-19 transmission. Additionally, studies showed extensive environmental contamination of SARS-CoV-2 (Jiang et al., 2020a , Ong et al., 2020 , suggesting the contaminated environments as a potential medium of virus transmission among families in the communities. Environmental management and disinfection are also important for preventing the community transmission of COVID-19.

Nosocomial infection is also an important mode of COVID-19 transmission, which is similar to Severe Acute Respiratory Syndrome (SARS) and Middle East Respiratory Syndrome (MERS) (Tsang et al., 2003 , Assiri et al., 2013 , Sina News, 2020 . It was reported that as of February 11, 2020, a total of 3,019 healthcare workers have been infected by SARS-CoV-2 in China, with 1,716 confirmed cases and 5 have died (0.3%) (The Novel Coronavirus Pneumonia Emergency Response Epidemiology, 2020). Another report on 138 COVID-19 cases in Zhongnan Hospital of Wuhan University in Wuhan during the early period of COVID-19 outbreak presumed that nosocomial transmission of 2019-nCoV was suspected in 41% (57/138) of patients, including 40 healthcare workers and 17 patients who were already hospitalized for other reasons .

These nosocomial infections were mainly due to the lack of understanding on the novel coronavirus, and insufficient personal protection equipment (PPE) in the early stage of epidemic. As knowledge of COVID-19 increases, nosocomial infections dramatically decreased in China. For example, more than 42,000 healthcare workers were sent to assist Wuhan from other provinces in China, but none of them was infected (Liu et al., 2020f) . Nosocomial infections were also reported in many other studies (Cao et al., 2020 , von Freyburg et al., 2020 , Hara et al., 2020 , WHO, 2020c . It was reported that over 90,000 health workers were infected with COVID-19 worldwide (Mantovani, 2020) . Healthcare workers play an essential role in containing the COVID-19 outbreak.

They provide care for patients during routine health service, offer critical care to severe patients, and ensure that the infection prevention and control measures are implemented and adhered to in healthcare facilities in order to limit nosocomial infections. Before a vaccine of SARS-CoV-2 available, healthcare workers remain susceptible to COVID-19. However, evidence from Wuhan, J o u r n a l P r e -p r o o f China illustrated that appropriate personal protective equipment in addition to adhering to standard recommendations could effectively protect them from SARS-CoV-2 infection even in the clinical settings with higher risk of exposure (Liu et al., 2020f) . Hence, healthcare workers must be given priority to procurement and distribution of PPEs, and provided adequate training of protecting themselves from infection.

Indoor gathering activities could also lead to cluster infections of COVID-19. Transmission in gathering activities were reported in several studies (Jiang et al., 2020b , Emma, 2020 , Danis et al., 2020 , Jang et al., 2020 . For example, Danis et al. reported a confirmed case infected in a chalet in France (Danis et al., 2020) . The index case had attended an international conference in Singapore linked to COVID-19 confirmed cases. He flighted to France and had a gathering activity with several English tourists and French residents, which led to 11 people infected. Such transmissions also occurred in other countries (Jang et al., 2020 , Takeuchi, 2020 . People in gathering activities rarely wear PPEs such as face masks, which make them in higher risk of infection. These transmissions further support the WHO recommendations to stay at home during the epidemic, and avoid any gatherings with persons from multiple households.

Transportation is another circumstance occurring the transmission of COVID-19, including flight, train, taxi, bus, cruise, etc. (Qiu et al., 2020a , Pongpirul et al., 2020 , Shen et al., 2020 , Eldin et al., 2020 , Kakimoto et al., 2020 For example, Yang et al. reported that ten out of 325 passengers and crew members were infected in a flight from Singapore to Hangzhou, China (Shen et al., 2020) .

have an enclosed space. Passengers usually have close contacts, and droplets can be easily generated in the enclosed space, which may transmit the SARS-CoV-2 from those carriers. Previous studies have demonstrated that SARS-CoV transmission in transportations was more likely through airborne (Chan et al., 2020) , small-particle (Setti et al., 2020) , and close contacts (Olsen et al., 2003) . Therefore, travelers should avoid all nonessential travels during the epidemic, and must implement strict measures to protect themselves on the transportations once they have to travel, such as wearing face masks, sanitation and disinfection.

A shopping mall is a place with high density of people, which can increase the transmission risk of SARS-CoV-2. Cai et al. reported a cluster of 35 confirmed cases associated with a shopping mall in Wenzhou, China (Cai et al., 2020) . A similar cluster of COVID-19 was reported in a shopping mall in Tianjin, China, which has caused 42 confirmed cases by February 22 (Tianjin Health Commission, 2020) . It was proposed that SARS-CoV-2 in shopping mall may spread via fomites (e.g., elevator buttons or restroom taps) or virus aerosolization in confined public places (e.g., restrooms or elevators) (Cai et al., 2020) . A report from Guangzhou, China also detected the nucleic acid of SARS-CoV-2 on a doorknob at a patient's house (Guo, 2020) , which further clarified the transmission of SARS-CoV-2 in the shopping mall. In addition, close contacts among people in the shopping mall may also lead to low intensity transmission. In order to prevent the spread of COVID-In addition, customers are suggested to wear face mask, practice social distancing while shopping, and wash hands.

Conference is also a circumstance favoring the transmission of SARS-CoV-2. A typical case was reported in Singapore where 109 persons from several countries attended an international conference, which led to at least seven confirmed cases (WHO, 2020d). More importantly, these infected cases spread the SARS-CoV-2 to many other countries including Malaysia, UK, France, and Spain through international flight. Therefore, many countries firstly stopped the international flights to and from those epidemic regions.

Tourists usually have close contacts, such as taking the same transportation, having meals together, staying in the same hotel. Hence, the infection risk is high once anyone of them was a virus carrier.

A such cluster of cases was reported in India. A group of 23 Italian tourists along with three Indians visited several tourist places, and the index case infected 16 tourists with an attack rate of 65.4% (Vivian et al., 2020) , which was higher than existing literature such as 5.7% in Shenzhen, China (Bi et al., 2020) . Another study also reported a cluster of eight cases infected in a hotel in Spain (Hoefer et al., 2020) . These studies illustrated the high risk of infections among tourists, and protection measures must be strictly implemented among those tourists.

Outbreak of COVID-19 was also reported in religious organizations (Qian et al., 2020, Wei et al., J o u r n a l P r e -p r o o f Others Cluster infections of SARS-CoV-2 were also reported in other circumstances, including prisons (Xinhuanet, 2020) , office , nursing home (The Beijing News, 2020). For example, five prison epidemics of COVID-19 including 511 confirmed cases were reported in China at the end of February 2020. (Xinhuanet, 2020) A cluster of cases infected in an office were reported in a German company (Rothe et al., 2020 , Böhmer et al., 2020 . Nursing home is another important setting with high risk of SARS-CoV-2. It has been demonstrated that older people are more susceptible to SARS-CoV-2, and older COVID-19 patients had poorer prognosis (Guan et al., 2020) . Statistics from the Swedish Board of Health and Welfare showed that 90% of COVID-19 patients who had died as of April 28 were over the age of 70, and half were nursing home residents (Bangkok Post, 2020) . These results suggest that transmission of SARS-CoV-2 could occur in various circumstances, which increases in the difficulties of control and prevention on the spread of COVID-19. These characteristics of COVID-19 also differ from SARS and MERS (Kwok et al., 2019) . The majority of SARS and MERS cases occurred in healthcare setting. While most SARS cases were among health care workers, substantial number of MERS cases were patients.

Studies have demonstrated that SARS-CoV-2 had a stronger transmissibility than other coronaviruses including SARS-CoV and MERS-CoV (Petrosillo et al., 2020) . Out of the many driving factors of the strong transmissibility, cluster infections play critical roles in the rapid evolution of COVID-19 transmission, which exponentially increases the number of cases and drive the new emerging disease to spread worldwide through modern transportation.

J o u r n a l P r e -p r o o f COVID-19 is still spreading over the world, countries that are in pandemic should be particularly cautious about cluster infectious in various settings. Governments are advised to track COVID-19 cases and conduct extensive epidemiological investigation as early as possible. Additionally, proper and effective risk communication are essential when taking social restrictions to minimize people's gatherings (meals, religions, etc.) and journeys outside home. Preventing and controlling the cluster infections of SARS-CoV-2 is an important strategy to contain the spread and to flatten the curve of COVID-19. As we continue to face many challenges on containing this infectious disease, collaboratively work and efforts from global community to reduce cluster infections are particularly important to suppress its spreading.

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical approval: Not required.

nursing staff who assisted in the care of patients.

TL and DG performed the database research, done the statistical analysis, and wrote the first draft of the manuscript; JX, JH, GH and ZR reviewed the manuscript critically for contents; WM concepted and guaranteed this study. All authors are in agreement with the content of the manuscript and approved the final manuscript.

Competing interests: None declared. 

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This study was supported by the Science and Technology Program of Guangdong Province (2018B020207006, 2019B020208005, 2019B111103001); and Guangzhou Science and technology Plan Project (201804010383). We thank the members from health departments and CDCs for their contribution in information collection, COVID-19 control and prevention, and all the medical and