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Paper Covid 1

This study analyzed 11,580 contacts of COVID-19 cases in Guangdong Province to identify risk factors and attack rates of infection. It found that children, older adults, and females had higher infection risks, particularly those with close relationships to index cases. The findings aim to inform targeted prevention strategies for COVID-19.
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0% found this document useful (0 votes)
22 views10 pages

Paper Covid 1

This study analyzed 11,580 contacts of COVID-19 cases in Guangdong Province to identify risk factors and attack rates of infection. It found that children, older adults, and females had higher infection risks, particularly those with close relationships to index cases. The findings aim to inform targeted prevention strategies for COVID-19.
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© © All Rights Reserved
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Emerging Microbes & Infections

2020, VOL. 9
https://doi.org/10.1080/22221751.2020.1787799

Risk factors associated with COVID-19 infection: a retrospective cohort study


based on contacts tracing
Tao Liua*, Wenjia Liangb*, Haojie Zhongb*, Jianfeng Heb*, Zihui Chena*, Guanhao Hea*, Tie Songb,
Shaowei Chena, Ping Wanga, Jialing Lib, Yunhua Lanb, Mingji Chengb, Jinxu Huangb, Jiwei Niub, Liang Xiab,
Jianpeng Xiaoa, Jianxiong Hua, Lifeng Linb, Qiong Huangb, Zuhua Ronga, Aiping Dengb, Weilin Zenga,
Jiansen Lib, Xing Lia, Xiaohua Tanb, Min Kangb, Lingchuan Guoa, Zhihua Zhua, Dexin Gonga, Guimin Chena,
Moran Donga and Wenjun Maa
a
Guangdong Provincial Institute of Public Health, Guangdong Provincial Center for Disease Control and Prevention, Guangzhou, People’s
Republic of China; bGuangdong Provincial Center for Disease Control and Prevention, Guangzhou, People’s Republic of China

ABSTRACT
This study aimed to estimate the attack rates, and identify the risk factors of COVID-19 infection. Based on a retrospective
cohort study, we investigated 11,580 contacts of COVID-19 cases in Guangdong Province from 10 January to 15 March
2020. All contacts were tested by RT-PCR to detect their infection of SARS-COV-2. Attack rates by characteristics were
calculated. Logistic regression was used to estimate the risk factors of infection for COVID-19. A total of 515 of 11,580
contacts were identified to be infected with SARS-COV-2. Compared to young adults aged 20–29 years, the infected
risk was higher in children (RR: 2.59, 95%CI: 1.79–3.76), and old people aged 60–69 years (RR: 5.29, 95%CI: 3.76–7.46).
Females also had higher infected risk (RR: 1.66, 95%CI: 1.39–2.00). People having close relationship with index cases
encountered higher infected risk (RR for spouse: 20.68, 95%CI: 14.28–29.95; RR for non-spouse family members: 9.55,
95%CI: 6.73–13.55; RR for close relatives: 5.90, 95%CI: 4.06–8.59). Moreover, contacts exposed to index case in
symptomatic period (RR: 2.15, 95%CI: 1.67–2.79), with critically severe symptoms (RR: 1.61, 95%CI: 1.00–2.57), with
symptoms of dizzy (RR: 1.58, 95%CI: 1.08–2.30), myalgia (RR: 1.49, 95%CI: 1.15–1.94), and chill (RR: 1.42, 95%CI: 1.05–
1.92) had higher infected risks. Children, old people, females, and family members are susceptible of COVID-19
infection, while index cases in the incubation period had lower contagiousness. Our findings will be helpful for
developing targeted prevention and control strategies to combat the worldwide pandemic.

ARTICLE HISTORY Received 18 May 2020; Revised 21 June 2020; Accepted 22 June 2020

KEYWORDS COVID-19; attack rate; risk factors; close contact; China

Introduction syndrome (SARS), Ebola virus disease, and Middle


East respiratory syndrome (MERS) [4–7]. Report of
Since the Coronavirus Disease 2019 (COVID-19) out- the WHO-China Joint Mission on COVID-19 pointed
break on 31 December 2019 [1], it has hit more than out that China has a policy of meticulous case and con-
200 countries, areas or territories with 8,525,042 cases tact identification for COVID-19 [8]. Previous studies
and 456,973 deaths as of 20 June 2020 [2]. World Health using mathematical modeling also theoretically
Organization (WHO) has declared COVID-19 as a pan- demonstrated that contact tracing and quarantine
demic on 11 March 2020 [3]. Owing to the effective play important roles in controlling the spreading of
measure taken in China, the chain of transmission has COVID-19 [9,10]. In addition to this, contact tracing
been broken and the epidemic has been under control. also provides a unique opportunity to investigate the
Contact tracing is a major public health response to epidemiological features of COVID-19.
imports of rare or emerging infectious diseases. The Previous researches have analysed the data of
main objectives of contact tracing are to identify poten- COVID-19 patients and found some risk factors of
tially infected individuals before the onset of severe mortality, such as older age, pre-existing cardiovascular
symptoms, and to prevent onward transmission from or cerebrovascular diseases, low levels of CD3+CD8+ T-
the secondary cases. Contact tracing has decisively con- cells, high levels of cardiac troponin I, higher Sequen-
tributed to the control of many infectious diseases tial Organ Failure Assessment score and d-dimer
worldwide including severe acute respiratory [11,12]. Unfortunately, limited study has paid attention

CONTACT Wenjun Ma mawj@gdiph.org.cn Guangdong Provincial Institute of Public Health, Guangdong Provincial Center for Disease Control and
Prevention, Guangzhou 511430, People’s Republic of China
*These authors contributed equally to this work.
Supplemental data for this article can be accessed https://doi.org/10.1080/22221751.2020.1787799
© 2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, on behalf of Shanghai Shangyixun Cultural Communication Co., Ltd
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided the original work is properly cited.
Emerging Microbes & Infections 1547

to the risk factors related to COVID-19 infection. contacts was collected by CDC using a standardized
Recent studies conducted among 1286 close contacts questionnaire, including general demographic charac-
(98 of them were infected by SARS-CoV-2) in Shenz- teristics, relationships with the index case, and patterns
hen and among 2098 close contacts in Guangzhou and frequency of contract. Meanwhile, their throat
(134 of them were infected by SARS-CoV-2) explored swabs were collected and detected by real-time reverse
the risk factors for COVID-19 infection, like older age, transcriptase polymerase chain reaction assay (RT-
travelling to Hubei, etc. [13,14]. Another recent study PCR). During the quarantine, health status of all con-
among 2761 close contact of 100 selected index cases tacts was monitored, and their throat swabs were col-
in Taiwan identified exposure to index case with severe lected every several days to test their infection status.
symptoms as a risk factor [15]. However, their limited Once they were identified with positive of severe acute
sample size, especially the limited cases, may restrict respiratory syndrome coronavirus 2 (SARS-COV-2),
their ability to perform detailed analysis, and reduce they would be transferred to a designated hospital for
the power to detect significant risk factors. Addition- diagnosis and treatment. Clinical symptoms and severity
ally, findings within a single city or selected sample of these infected contacts were followed up and recorded
may restrict its ability of generalization. by clinical workers. After 14 days’ quarantine, contacts
In the current study, we employed a large dataset with negative SARS-COV-2 were released.
including 11,686 close contacts of COVID-19 cases
(449 of them were infected) in Guangdong Province,
China to estimate the attack rates, and identify risk fac- Statistical analysis
tors for infection of COVID-19. Under the context of Categorical variables were described using percentage
worldwide pandemic, understanding this issue can (%), and a Chi-square test was used to test the differ-
identify high-risk groups and provide evidence to ences in distributions of categorical variables between
develop targeted prevention. index and secondary cases. If conditions for Chi-square
test were not satisfied, Fisher’s exact test was used.
Attack rate was calculated as the percentage of contacts
Methods
who were later confirmed to be infected with SARS-COV-
Setting and definitions 2. We estimated the attack rates of contacts by gender, age,
relationships to index cases (household members, rela-
Guangdong, a province with a large population size
tives, social activities, etc.), transportations (flight, train,
located in Southern China, is a place early affected by
public transportation, provide car, and the Dream Cruise)
COVID-19. The first confirmed case was reported on
where infection occurred, course of disease (incubation
15 January 2020, and a total of 1361 confirmed cases
period, symptomatic period, and different days from
were reported by 15 March 2020. Since the very early
symptom onset) ofindex cases when the contact occurred,
stage of COVID-19 outbreak, an intensified surveillance
severity of index cases (mild, moderate, severe, and criti-
was implemented across Guangdong Province to detect
cally severe), and clinical symptoms of index cases.
suspected and confirmed COVID-19 cases, and their
These attack rates were calculated only using sub-datasets
close contacts following standardized protocols released
of the index cases and contacts with detailed information
by the National Health Commission of China. Sus-
because some cases had no complete information for an
pected and confirmed COVID-19 cases were defined
estimate. Logistic regression was also conducted to esti-
based on the Diagnosis and Treatment scheme of
mate the risk factors of COVID-19. All data analyses
COVID-19, and close contacts were defined by the Pre-
were conducted by R software (version 3.5.0, R Foun-
vention and Control Scheme of COVID-19. These two
dation for Statistical Computing).
schemes were released by the National Health Commis-
sion of China (Supplementary materials) [16,17].
Results
Identification and quarantine of contacts General characteristics of contacts
Once a suspected or confirmed COVID-19 case was As of 15 March 2020, a total of 11,686 contacts were
identified, the case would be reported as an index case traced and quarantined. The first contact was identified
and isolated, and the Center for Diseases Control and on 10 January 2020. Contacts (n = 106) without key
Prevention (CDC) will conduct a field investigation. formation were excluded, and 11,580 contacts were
Information of index cases was collected by clinical finally included in the analysis. Figure 1 showed the
workers, including demographic information, exposure daily number of quarantined contacts, which peaked
history, clinical symptoms, date of symptom onset, lab- (n = 574) on 31 January. Of total contacts, 6183
oratory test results, and the severity. This information (53.4%) were males; 8419 (72.7%) were adults aged
was directly reported to the National Internet-Based 20–59 years, and 9725 (84.0%) contacts were quaran-
Infectious Diseases Reporting System. Information of tined in centralized stations. The number of contacts
1548 T. Liu et al.

Figure 1. Daily numbers of quarantined contacts, and confirmed cases or asymptomatic infections identified from the quarantined
contacts in Guangdong Province.

occurred at home, in social activities, on transpor- from five days prior to the symptom onset of index
tations, and in health care settings were 4893 cases (1.7%), to a peak during 3–4 days (10.1%) after
(40.9%), 2016 (16.8%), 3198 (26.7%) and 1348
(11.3%), respectively. Many contacts were from family
Table 1. General characteristics of contacts to COVID-19 cases
members of index cases (4707, 40.7%), social activity in Guangdong Province.
contacts (3344, 28.9%), transportation contacts (2778, n %
24.0%), and health care workers (573, 4.9%) Sex
(Table 1). All contacts were linked to 1158 index Male 6183 53.4
Female 5397 46.6
cases, with a mean of 7.8 (95%CI: 7.0–8.7) close con- Age (years)
tacts per index case. The average contacts per index 0–9 1048 9.0
10–19 819 7.1
case varied with contact circumstances and relation- 20–29 2420 20.9
ships to the index cases (Table S1). The average period 30–39 2601 22.5
from exposure to quarantine was 6.4 days, and the 40–49 1878 16.2
50–59 1520 13.1
average duration of quarantine was 9.7 days (Table S1). 60–69 831 7.2
70–79 314 2.7
≥80 149 1.3
Places of quarantine
Attack rates of COVID-19 At home 1855 16.0
Centralized stations 9725 84.0
Until 15 March 515 (4.4%) contacts were identified to Contact circumstances
be infected with SARS-COV-2. The attack rates varied Family 4893 40.9
Social activities 2016 16.8
by age groups with the highest for the group aged 60– Transportation 3198 26.7
69 years (11.1%), and the lowest for the group of 20–29 Flight 695 5.8
Train 902 7.5
years (2.3%) (Table 2). The attack rate of children <10 Public transportation* 229 1.9
years was 5.7%, and the attack rates were higher in chil- Private car 213 1.8
The Dream Cruises 64 0.5
dren whose index cases aged 30–39 years (8.5%), and Unknown 1095 9.2
50–59 years (7.0%) (Table S3). Health care institutes 1348 11.3
We also observed a higher attack rate in females Others 519 4.3
Relationship with index cases
(5.6%) than in males (3.5%). In addition, contacts hav- Family members 4707 40.7
ing a close relationship with index cases had higher Spouse 563 4.9
Family members (non-spouse) 1878 16.2
attack rate (attack rate: 23.3% for spouse; 10.6% for Close relatives 1341 11.6
non-spouse family members; 7.0% for close relatives; Other relatives 925 8.0
Social activity contacts 3344 28.9
4.1% for other relatives, 1.3% for social activity con- Transportation contacts 2778 24.0
tacts, etc.). Different attack rates also occurred in var- Health care workers 573 4.9
Others 178 1.5
ious transportations where infection occurred. Attack Infection spectrum of contacts
rates were 0.8% on flight, 1.2% on train, 2.1% on public No infection 11065 95.6
transportation, 4.2% on private car, and 9.5% on the Asymptomatic infections 66 0.6
Mild confirmed cases 104 0.9
Dream Cruise. Moderate confirmed cases 300 2.6
When considering the time contacting with the Severe confirmed cases 31 0.2
Critically severe confirmed cases 12 0.1
index cases, attack rates were 3.3% and 7.0% when con- Dead cases 2 <0.01
tacts occurred in the index cases’ incubation period and *Indicate other public transportations mainly including bus, taxi, subway,
symptomatic period. In detail, attack rate increased ferry, etc.
Emerging Microbes & Infections 1549

Table 2. Attack rates of COVID-19 in contacts with different Risk of infection for COVID-19
characteristics.
Total Total Attack Rate Compared with people aged 20–29 years, children <10
Characteristics contacts infections (%) years (RR: 2.59, 95%CI: 1.79–3.76) and children aged
Age of contacts (years) 10–19 (RR: 1.81, 95%CI: 1.17–2.81) had higher risk
0–9 1048 60 5.7
10–19 819 33 4.0
to be infected with COVID-19 (Figure 2A). The risks
20–29 2420 56 2.3 were also higher in people aged 30–39 years (RR:
30–39 2601 113 4.4 1.96, 95%CI: 1.41–2.71), 50–59 years (RR: 2.30, 95%
40–49 1878 56 3.0
50–59 1520 76 5.0 CI: 1.65–3.27), 60–69 years (RR: 5.29, 95%CI: 3.76–
60–69 831 92 11.1 7.46) and 70–79 years (RR: 3.03, 95%CI: 1.81–5.08).
70–79 314 21 6.7
≥80 149 7 4.7 Moreover, young adults (aged 30–39 years), whose
Sex index cases aged <20 years, 30–39 years, and 50–69
Male 6183 213 3.4
Female 5397 302 5.6 years, had higher infected risk (Table S4). We also
Relationship to the index case observed a higher risk in females than in males (RR:
Spouse 563 131 23.3
Family members (non- 1878 199 10.6
1.66, 95%CI: 1.39–2.00) (Figure 2B). In addition,
spouse) people having close relationship with index cases
Close relatives 1341 94 7.0 encountered higher risk to be infected (RR and 95%
Other relatives 925 38 4.1
Social activity contacts 3344 41 1.3 CI: 20.68 [14.28–29.95] for spouse; 9.55 [6.73–13.55]
Transportation contacts 2778 10 0.3 for non-spouse family members; 5.90 [4.06–8.59] for
Health care workers 573 2 0.3
Others 178 0 0.0 close relatives; 3.37 [2.15–5.28] for other relatives)
Contacts on different transportations (Figure 2C). In terms of the infected risk in transpor-
Flight 695 6 0.8
Train 901 11 1.2 tations, we did not observe significant difference across
Public transportation* 229 5 2.1 various transportations except in the Dream Cruises
Private car 213 9 4.2
The Dream Cruises 63 6 9.5
(RR: 4.19, 95%CI: 1.21–14.50) (Figure 2D).
Unknown 1104 14 1.3 When considering time contacting with index cases,
*Indicate other public transportations mainly including bus, taxi, subway, the risk of exposure to index cases in the symptomatic
ferry, etc.
period was higher than in the incubation period (RR:
Disease history of confirmed index cases#
Incubation period 2211 72 3.3 2.15, 95%CI: 1.67–2.79) (Figure 2E). More specifically,
Symptomatic period 5904 411 7.0 the infected risk increased from five-plus days prior to
Contacts to the index cases at different time (days to the symptom onset)*
≤−5 522 9 1.7
the symptom onset of index cases (RR: 0.30, 95%CI:
−4 to −3 283 6 2.1 0.15–0.60), to a peak during 3–4 days (RR: 1.87, 95%
−2 to −1 974 25 2.5 CI: 1.33–2.61) after onset, and then decreased to 0.30
0 1020 61 5.6
1–2 1036 81 7.3 (95%CI: 0.12–0.77) after 17 days of the onset
3–4 865 97 10.1 (Figure 2F). Moreover, contact with index cases with
5–6 702 61 8.0
7–8 371 31 7.7 critically severe symptoms was associated with a higher
9–10 223 16 6.7 infected risk (RR: 1.61, 95%CI: 1.00–2.57) (Figure 2G).
11–12 106 6 5.4
13–14 109 4 3.5 Figure 2H shows the infected risk for the contacts of
15–16 188 10 5.1 index cases with different clinical symptoms compared
≥17 265 11 4.0
Clinical severity of index case
to fever, and there were higher risks in index cases
Mild 1244 57 4.6 with dizzy (RR: 1.58, 95%CI: 1.08–2.30), myalgia
Moderate 5637 344 6.1 (RR: 1.49, 95%CI: 1.15–1.94), and chill (RR: 1.42,
Severe 812 52 6.4
Critically severe 371 28 7.5 95%CI: 1.05–1.92).
*Minus number indicates days before the symptom onset, plus number
indicates the days after the symptom onset in confirmed cases, and
zero indicates the day of symptom onset. In order to precisely estimate
the contacting time, only the pairs with only one index case and one sec- Discussion
ondary case were included.
After reporting the first case on 15 January 2020,
Guangdong Provincial government mobilized enor-
mous resources to respond to the COVID-19 epi-
onset, and then decreased to 4.0% after 17 days of the demic. More than 11,000 close contacts of COVID-
onset. In addition, attack rates increased from 4.6% for 19 were traced and quarantined. One-third of the
the contacts of mild cases to 7.5% for the contacts of total cases reported in Guangdong Province were
critically severe cases. Table S2 shows attack rates for identified from these contacts, which indicate that
the contacts of index cases with different clinical contact tracing strategy has played an important
symptoms, and higher attack rates were observed in role in containing the spreading of COVID-19. The
index cases with dyspnea (11.2%), dizzy (10.6%), analysis of index cases and their close contacts pro-
muscle soreness (10.4%), and shortness of breath vides insight into the attack rates and risk factors
(10.0%). of infection for COVID-19.
1550 T. Liu et al.

Figure 2. Infected risks of COVID-19 in contacts with different characteristics. (A) In contacts with different ages; (B) In males and
females; (C) In contacts who had different relationships to the index case; (D) In contacts exposed to the index cases on different
transportations; (E) In contacts exposed to the index cases at different time; (F) In contacts exposed to the index cases in different
course of disease; (G) In contacts exposed to the index cases with different clinical severity; (H) In contacts exposed to the index
cases with different clinical symptoms. Adjusted for age and/or sex.

We found that attack rates were higher in the elderly Meanwhile, the immunity of the age may be weaker
with the highest in the group aged 60–69 years, and than younger adults, making them more susceptible
logistic regression demonstrated the statistical signifi- to infection. Therefore, more efforts are needed to pro-
cance. These findings are consistent with the results tect the elderly from the infection of COVID-19.
for SARS in Beijing [7]. Recent studies also reported The susceptibility of children to COVID-19 is con-
that elderly contacts were more likely to encounter troversial [8,18]. Clinical data of COVID-19 showed
COVID-19 infection [13,14]. However, another recent much lower percentage of children aged <10 years
article in Taiwan did not observe significant higher [19,20]. A recent systematic review considering litera-
infected risk of elderly contacts, which may ascribe tures of COVID-19 in children pointed out that chil-
its insufficient sample size [15]. Our findings thus dren cases are usually less severe than adult cases,
confirmed the greater vulnerability of the elderly. and more children cases are asymptomatic infection,
Those contacts aged 60–69 years could have more which makes them less opportunity to be tested and
physical activities than older people, which may cause identified [21]. However, we found the higher infected
closer contact with index case for a longer period [7]. risk of COVID-19 in children <10 years that their RR
Emerging Microbes & Infections 1551

were larger than contacts aged 10–59 years, which indi- place like washing hands and wearing mask, but
cates that children were also susceptible to COVID-19. neglect personal protection at home. This indicates
Furthermore, we observed a higher attack rate in chil- the necessity for public to pay attention to personal
dren whose index cases aged 30–39 and 50–59 years. protective at home especially when family members
Although limited sample size may cause insignificant develop symptom or have travel history of epidemic
RR, our results still implicated that the children may areas.
be mainly infected by their parents and grandparents. We also compared attack rates occurred on different
Two recent studies reported consistent results with transportations, and found lower attack rates occurred
our study [13,22]. For instance, Dong et al. analysed on trains or flights. This result indicates that the possi-
2143 pediatric COVID-19 patients across China, and bility of transmission of SARS-COV-2 on flight and
found that children were susceptible to COVID-19 train was low, which may be related to the advanced
[22]. Additionally, young adults (30–39 years) were air purification system and sanitation in these trans-
more likely to be infected by children aged < 20 portations. However, after controlling for age and
years, their peers aged 30–39 years, as well as people sex, the results of logistic regression did not find signifi-
aged 50–69 years. These findings may be attributed cant difference across various transportations except in
to the status that young adults are the primary care- the Dream Cruises. The insignificance may be attribu-
givers once their children and parents got sick, and ted to the limited sample size and the risk difference
they are also the individuals who have many social may actually exist. Future studies with a larger sample
activities with their peers. These findings suggested should be conducted to explore this issue and provide
that people should performed strict personal protec- evidence to guide the development of prevention in
tion both at home and in public places. Compared transportations.
with previous studies, our study prospectively collected Although previous studies reported that both
data based on contacts tracing, which had explicit tem- asymptomatic and symptomatic cases could infect
porality for causal inference and reduced recall bias, other persons [26–28], the differences in contagious-
and therefore provide more reliable evidence. Our ness at different phases of COVID-19 remain unclear.
finding is helpful for preventing people from being Our study shows the contagiousness peaked during
infected with COVID-19. 3–4 days after symptom onset, which is consistent
We observed that female contacts were more likely with previous studies, which showed higher virus shed-
to be infected by SARS-CoV-2 than male contacts, ding during several days after the onset of symptoms
which is consistent with previous studies [13,14]. For [29–31]. For example, To et al. found that salivary
example, a recent study conducted in Guangzhou viral load in COVID-19 cases was highest during the
also found higher attack rates in females than in first week after symptom onset, and the viral RNA
males [14]. This difference in attack rate between sex was detected 25 days after symptom onset [31]. In
may be due to several reasons: (1) females play predo- addition, we found contacts before the symptom
minant roles as caregivers within the family and may onset could also lead to infection, which indicates the
have closer contact and longer contact period with transmission of COVID-19 in incubation period.
the index cases [23]; (2) females comprise a large pro- Although viral shedding before symptom onset is still
portion of health care workers [24]. Therefore, our limited, Zou et al. reported an asymptomatic patient
findings suggest more prevention measures specifically who had a similar amount of virus to those sympto-
implemented to protect females from infection during matic cases [30]. Another study conducted in children
the epidemic of COVID-19. also detected positive virus before the onset of symp-
We observed that the relationships between contacts toms in several children cases [20]. These findings
and index cases significantly affected the infected risks. suggested COVID-19 could be transmitted before the
Compared with the social activity contacts, the risk of onset of symptoms.
being infected was more than 20 times higher among The present study found that severe index cases
the spouse and more than nine times higher among could cause higher attack rates than mild cases. In
other family members, which was consistent with pre- addition, compared with cases with fever, dizzy, myal-
vious studies on SARS and H1N1 [7,25]. A newly pub- gia, and chill caused higher infected risks to their con-
lished research also found that more infections were tacts, while cases with rhinorrhea, expectoration, and
acquired in household [15]. Family members are chest tightness caused lower infected risks. To et al.’s
more likely to have closer contact with index case for study showed higher virus load in specimens of severe
a longer contact period with the shorter distance. patients than mild patients [31], which verified our
Another possible reason is that family members may findings. However, studies are needed to detect the
have some certain linkage with index cases in living virus load in cases with different clinical symptoms
habits which may cause higher predisposition in infec- for assessing their contagiousness.
tion than other close contacts. Unfortunately, individ- This study has several strengths. First, our study
uals commonly take protective measures in public includes the largest number of close contacts of
1552 T. Liu et al.

COVID-19 to date. Second, our study is a retrospective No study participants were involved in the prep-
cohort study, which provides information with explicit aration of this article. The results of the article will be
temporality for causal inference, and the recall bias was summarized in media press releases from the Guang-
reduced. Third, we estimated the attack rates and dong Provincial Center for Disease Control and
infected risks for different contacts, which is helpful Prevention.
for identifying susceptible groups to develop specific
protection. Fourth, we estimated the contagiousness
across the course of COVID-19. Authors contribution
Some limitations also need to be noted. First, T.L., W.J.L., H.J.Z., J.F.H., Z.H.C. and G.H.H. contrib-
although we used a large dataset with more than uted equally to this article. W.J.L., H.J.Z. and W.J.M.
10,000 of contacts, the sample size of cases was limited conceptualized the paper. T.L., J.F.H., Z.H.C. and
in some subgroups, which may lead to insufficient G.H.H. analysed the data, with input from T.S.,
power to identify the statistical significance. Second, a S.W.C., P.W., J.L.L., Y.H.L., M.J.C., J.X.H., J.W.N.,
number of asymptomatic infections may be missed L.X., J.P.X., J.X.H., L.F.L., Q.H., Z.H.R., A.P.D.,
and their close contacts cannot be identified. Third, W.L.Z., J.S.L., X.L., X.H.T., M.K., L.C.G., Z.H.Z.,
since the imperfect sensitivity of the RT-PCR test, D.X.G., G.M.C., and M.R.D. T.L., W.J.L., H.J.Z., T.S.,
some potential infections among close contacts may J.F.H., Z.H.C., G.H.H. and W.J.M. wrote the initial
be missed. Fourth, the data were collected by a variety draft with all authors providing critical feedback and
of epidemiological investigation groups across Guang- edits to subsequent revisions. All authors approved
dong Province. Despite using the same protocol, the the final draft of the manuscript. W.J.M. is the guaran-
implementation may have inconsistence and some tor. The corresponding author attests that all listed
noise may be introduced. authors meet authorship criteria and that no others
meeting the criteria have been omitted.
Conclusions
Children, old people, females, and family members are Disclosure statement
susceptible to be infected with COVID-19, while index No potential conflict of interest was reported by the authors.
cases in the incubation period had lower contagious-
ness. Our findings will be helpful for developing tar-
geted prevention and control strategies to combat the Funding
worldwide pandemic.
This study was supported by Key-Area Research and Devel-
opment Program of Guangdong Province #1 under [grant
number 2019B111103001]; the Science and Technology Pro-
Acknowledgements gram of Guangdong Province#2 under [grant number
We thank all members from health departments and CDCs 2018B020207006, 2019B020208005]; the National Key
in Guangdong Province for their contribution in data collec- Research and Development Program of China#3 under
tion, COVID-19 control, and prevention. [grant number 2018YFA0606200, 2018YFA0606202]; and
Guangzhou Science and Technology Plan Project#4 under
[grant number 201804010383].
Funding
This study was supported by Key-Area Research and Devel- References
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