Highlights
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Household settings related to a higher asymptomatic SARS-CoV-2 transmission risk
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Lower transmission potential for asymptomatic than (pre)symptomatic infections
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Asymptomatic transmission rate lower in China than other countries included
Keywords: SARS-CoV-2, Asymptomatic, Transmission rate, Systematic review, Meta-analysis
Abstract
Background
Global evidence on the transmission of asymptomatic SARS-CoV-2 infection needs to be synthesized.
Methods
A search of 4 electronic databases (PubMed, EMBASE, Cochrane Library, and Web of Science databases) as of January 24, 2021 was performed. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were followed. Studies which reported the transmission rate among close contacts with asymptomatic SARS-CoV-2 cases were included, and transmission activities occurred were considered. The transmission rates were pooled by zero-inflated beta distribution. The risk ratios (RRs) were calculated using random-effects models.
Results
Of 4923 records retrieved and reviewed, 15 studies including 3917 close contacts with asymptomatic indexes were eligible. The pooled transmission rates were 1.79 per 100 person-days (or 1.79%, 95% confidence interval [CI] 0.41%–3.16%) by asymptomatic index, which is significantly lower than by presymptomatic (5.02%, 95% CI 2.37%–7.66%; p<0.001), and by symptomatic (5.27%, 95% CI 2.40%–8.15%; p<0.001). Subgroup analyses showed that the household transmission rate of asymptomatic index was (4.22%, 95% CI 0.91%–7.52%), four times significantly higher than non-household transmission (1.03%, 95% CI 0.73%–1.33%; p=0.03), and the asymptomatic transmission rate in China (1.82%, 95% CI 0.11%–3.53%) was lower than in other countries (2.22%, 95% CI 0.67%–3.77%; p=0.01).
Conclusions
People with asymptomatic SARS-CoV-2 infection are at risk of transmitting the virus to their close contacts, particularly in household settings. The transmission potential of asymptomatic infection is lower than symptomatic and presymptomatic infections. This meta-analysis provides evidence for predicting the epidemic trend and promulgating vaccination and other control measures. Registered with PROSPERO International Prospective Register of Systematic Reviews, CRD42021269446; https://www.crd.york.ac.uk/prospero/display_record.php?RecordID=269446.
Graphical abstract
1. Introduction
People who become infected with acute respiratory syndrome coronavirus 2 (SARS-CoV-2) may remain asymptomatic throughout the course of infection. Asymptomatic SARS-CoV-2 infection plays a unique role in the spread of the virus. Of all SARS-CoV-2 infections including symptomatic coronavirus disease 2019 (COVID-19) cases, asymptomatic infections accounted for 20% [1], even more among subgroup populations such as obstetric patients and nursing home residents [2]. The significant proportion of asymptomatic infections contributes to the difficulty of early detection of infected individuals and quarantine of transmission sources [3]. Accurate estimation of the transmission risk of asymptomatic infection is needed for: (1) early screening and detection of infected individuals; (2) quarantine and border control for international travels; (3) prediction of epidemic trends; and (4) comparison of the relative risk by different stages of infection for implementing appropriate strategies of epidemic control [4].
Numerous systematic reviews on asymptomatic transmission have been published [1,2,[5], [6], [7], [8]]. For example, two are systematic reports of the transmission potential of asymptomatic infection [2,5], two estimated a pooled household transmission rate of both asymptomatic and presymptomatic infections but not the transmission rate solely from asymptomatic infection [7,8], and two only calculated the relative risk of transmission rates between asymptomatic and symptomatic infections [1,6]. There is no meta-analysis providing a pooled transmission rate of asymptomatic infections. We conducted a systematic review and meta-analysis of global literature with three purposes: (1) estimating the transmission rate of asymptomatic infection; (2) comparing the transmission rates of asymptomatic infection in different subpopulations of close contacts; (3) comparing the relative risks of asymptomatic transmission with presymptomatic and symptomatic transmissions.
2. Methods
This systematic review and meta-analysis was reported following PRISMA guidelines [9].
2.1. Selection Criteria
The target population was defined as people who were confirmed as SARS-CoV-2 infection by laboratory testing and those who had no symptoms during follow-up from diagnosis to the first negative laboratory test. Studies were eligible if they reported data that can be used for calculating the transmission rate of asymptomatic infection (transmission rate = [total number of new infections among close contacts with asymptomatic index cases] / [total number of close contacts]). The close contacts were defined as any persons living in the same household with a confirmed case-patient (the household contacts) or persons who had been within 1 meter of a confirmed asymptomatic SARS-CoV-2 case in an enclosed space (the non-household contacts). The studies included in this meta-analysis must have a defined period of follow-up of the close contacts to ascertain secondary infections. Studies were excluded if they were pre-print manuscripts without peer review, case reports, small clusters, modelling studies, qualitative studies or duplicated studies, if they had no clear sampling frame of at-risk population, if they did not report the specific number of close contacts with index asymptomatic cases [10], [11], [12], [13], if they included index cases as mixed asymptomatic and symptomatic infections [14,15], or if they were not original research such as reviews, commentaries, and editorials. The language was limited to English.
2.2. Search Strategy
We searched 4 electronic databases (PubMed, EMBASE, Cochrane Library, and Web of Science databases) for publications from January 1, 2019 to January 24, 2021. Our search terms included (2019 novel coronavirus OR 2019-nCov OR covid-19 OR coronavirus disease 2019 OR SARS-CoV-2 OR severe acute respiratory syndrome coronavirus 2) AND (asymptomatic OR covert OR latent OR preclinical OR pre-clinical OR presymptomatic OR pre-symptomatic OR subclinical OR “without symptoms” OR “no symptoms” OR “free of symptoms” OR non-symp* OR nonsymp* OR symptom-free OR symptomfree) AND (transmission* OR “secondary infection*” OR “secondary attack rate”).
We manually checked the reference list of each selected paper for additional studies. Records were managed by EndNote 20.0 software to exclude duplicates. Figure 1 describes the literature search and study selection procedures.
Fig. 1.
Flow chart of study selection (no specific request for color in print)
2.3. Data Screening and Extraction
Two investigators performed the literature search and extracted the data from the included studies independently. A standard data extraction form was used to extract variables from the included studies, including publication year, country/city, study period, follow up of close contacts, mean age, whether wearing face mask, diagnosis method, type of close contacts, number of index asymptomatic infection cases, transmission rate of asymptomatic cases, number of index presymptomatic infection cases, transmission rate of presymptomatic cases, number of index symptomatic infection cases, transmission rate of symptomatic cases, and quality score of the studies (Table 1). Disagreements were resolved through discussion with a third investigator.
Table 1.
Characteristics of included studies reporting the transmission rates of asymptomatic SARS-CoV-2 infection.
Study ID | Study country /city | Study period | Days of follow-up of close contacts | Mean age | Wearing face mask | Diagnosis method | Number of index AI cases, n | Transmission rate of AI, per 100 close contacts (n/N) | Number of index PI cases, n | Transmission rate of PI, per 100 close contacts (n/N) | Number of index SI cases, n | Transmission rate of SI, per 100 close contacts (n/N) | Quality score of the study |
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Cao et al. [21] | China, Wuhan | 2020.5.14-2020.6.1 | ≥14 | NA | NA | RT-PCR | 300 | 0.0 (0/1174) | NA | NA | NA | NA | 9 |
Blaisdell et al. [22] | USA | 2020.6-2020.8 | 8-10 | NA | NA | RT-PCR | 3 | 0.0 (0/41) | NA | NA | NA | NA | 8 |
Chaw et al. [23] | Brunei | NA | ≤14 | NA | NA | RT-PCR | 4 | 2.8 (3/106) | 7 | 2.1 (12/585) | 8 | 2.8 (28/1010) | 9 |
Yin G and Jin H [24] | China, Ningbo | 2020.1.21-2020-3.6 | ≥14 | NA | NA | RT-PCR | 30 | 4.1 (6/146) | NA | NA | 157 | 6.3 (126/2001) | 9 |
Gao et al. [25] | China, Guangzhou | 2020.2.11.-2020.3.2 | ≥14 | NA | Yesa | RT-PCR | 1 | 0.0 (0/455) | NA | NA | NA | NA | 9 |
Gupta et al. [26] | India | NA | ≥9 | 6 (4-9) | NA | Laboratory testing | 19 | 5.7 (7/122) | NA | NA | NA | NA | 9 |
Han [27] | South Korea | 2020.3.28-2020.4.3 | ≥14 | 51.5 | No | RT-PCR | 2 | 0.0 (0/52) | NA | 8.0 (7/88) | 8 | 0.0 (0/52) | 8 |
Han et al. [28] | China, Wuhan | 2020.3.13-2020.4.25 | ≥14 | 30.5 | NA | RT-PCR | 18 | 0.0 (0/41) | NA | NA | NA | NA | 8 |
Jiang et al. [29] | China, Shandong | 2020.1.11-2020.2.17 | ≥14 | 40.1 | No | RT-PCR | 2 | 0.6 (1/174) | NA | NA | 5 | 3.8 (5/130) | 8 |
Cheng et al. [30] | China, Taiwan | 2020.1.15-3.18 | 14 | NA | No | RT-PCR | 9 | 0.0 (0/91) | NA | NA | 91 | 0.8 (22/2644) | 8 |
Liu et al. [31] | China, Anhui | NA | 14 | NA | NA | RT-PCR | 131 | 2.6 (24/914) | 16 | 9.7 (23/236) | NA | NA | 9 |
Luo et al. [32] | China, Guangzhou | 2020.1.13-2020.3.6 | ≥14 | NA | NA | RT-PCR | NA | 0.3 (1/305) | NA | NA | NA | 5.1 (117/2305) | 9 |
Shi et al. [33] | China, Wenzhou | 2020.1.21-2020.4.10 | 28 | NA | Yes† | RT-PCR | NA | 9.2 (16/173) | NA | 5.1 (47/922) | NA | 4.2 (20/471) | 9 |
Park et al. [34] | South Korea | 2020.2.21-2020.3.31 | 14 | NA | NA | RT-PCR | 4 | 0.0 (0/4) | 4 | 0.0 (0/11) | 89 | 16.2 (34/210) | 7 |
Zhang et al. [35] | China, Guangzhou | 2020.3.15-3.29 | 14 | NA | No | RT-PCR | 12 | 0.8 (1/119) | 71 | 4.4 (11/250) | NA | NA | 9 |
Transmission rate of AI = (total number of infections among the contacts of asymptomatic index cases) / (total number of the contacts of asymptomatic index cases); Transmission rate of PI = (total number of infections among the contacts of presymptomatic index cases) / (total number of the contacts of presymptomatic index cases); Transmission rate of SI = (total number of infections among the contacts of symptomatic index cases) / (total number of the contacts of symptomatic index cases).
AI, asymptomatic infection; PI, presymptomatic infection; SI, symptomatic infection; NA, not available; RT-PCR, real time polymerase chain reaction testing.
The contacts wore face masks except during eating and drinking. † The contacts were required to wear masks outside the home and minimize interactions with family members during home quarantining.i
2.4. Quality Assessment
Quality assessment of the included studies was conducted using the Joanna Briggs Institute (JBI) Critical Appraisal Checklist for Prevalence Studies [16] by two independent reviewers (CiZ and ChZ) (Supplemental Table S1). The checklist has nine items, and the score for each study ranged from 0 to 9. The disagreements were resolved by the discussion with a third investigator (HZQ).
2.5. Statistical Analysis
We calculated the pooled transmission rates under different scenarios using R software version 4.0.3. To include studies with zero event into analysis, the two-part zero-inflated beta (ZIB) distribution was used to calculate the pooled transmission rates [17]. ZIB distribution was used to model transmission rates that are skewed proportional data with a large proportion of zero values and a range between 0 and 1. We also simulated the transmission rate for 1000 times using ZIB distribution with estimated parameters and used the standard errors of these simulated samples to calculate 95% confidence intervals (CI) of the pooled transmission rates. Sensitivity analyses were performed to assess the impacts of each individual study on the pooled rates through a repeating procedure of removing one study from the analysis each time. The two-sample proportion test was used to evaluate the significance of the difference in transmission rate between groups or subgroups.
If the included studies also reported transmissions from presymptomatic and symptomatic infections, we compared the transmission risks between index asymptomatic and presymptomatic or symptomatic cases. STATA MP version 13.0 was used to calculate the risk ratios (RRs) between asymptomatic and presymptomatic transmission rates, between asymptomatic and symptomatic rates and between asymptomatic and presymptomatic or symptomatic transmission rates. DerSimonian-Laird random-effects models were used to calculate RRs and 95% CIs [18,19]. If there was no event in one group, 0.5 was added to each cell in the 2 × 2 table in the pooled analysis [20]. If there were no event in both group pairs, the data from these group pairs were excluded from the analysis.
2.6. Registration
The study protocol was registered with the International Prospective Register of Systematic Reviews (PROSPERO) (https://www.crd.york.ac.uk/PROSPERO/, ID: CRD42021269446).
3. Results
3.1. Search Results and Characteristics of Included Studies
We retrieved 4670 publications from electronic database searches. After removing duplicates, 2443 records were retained. Then 418 records were excluded through reviewing the titles or abstracts, and 2025 articles were further excluded through reviewing the full texts, leaving 14 eligible publications. In addition, 253 citations from the included studies were reviewed and 1 article was eligible (Figure 1). Hence, 15 studies were included in the meta-analysis [21], [22], [23], [24], [25], [26], [27], [28], [29], [30], [31], [32], [33], [34], [35].
These 15 included studies were conducted between January to August, 2020, and published in 2020 (Table 1). They were conducted in five countries including ten in China (67%, 10/15) [21,24,25,[28], [29], [30], [31], [32], [33]] and two in South Korea (13%) [27,34].
The duration of follow-up to assess secondary transmission among the close contacts with index asymptomatic cases ranged from 8–28 days. Four studies reported the mean age of index cases [26], [27], [28], [29], with one study conducted among children [26]. Four studies (27%) reported that index cases and close contacts did not wear face masks [27,29,30,35], one study (7%) reported that index cases and close contacts wore mask except for eating and drinking [25], and one study (7%) reported the contacts were required to wear masks outdoors and to minimize interactions with family members during home quarantining [33]. Most studies (93%) reported that SARS-CoV-2 infection was determined by reverse transcription polymerase chain reaction (RT-PCR) testing. The methodological quality was scored as 9 in nine studies (60%), 8 in five studies (33.3%), and 7 in one study (6.7%) (Supplemental Table S1).
The number of asymptomatic index cases in the included studies ranged from 1 to 300 and the sample size of close contacts ranged from 4 to 1174. The reported transmission rate of asymptomatic cases ranged from 0 to 9.2 per 100 person-days (9.2%). Six studies (40%) also reported the transmission rate of presymptomatic cases [23,27,31,[33], [34], [35]], which ranged from 0 to 9.7%. Eight studies (52.3%) reported the transmission rate of symptomatic cases as well [23,24,27,29,30,[32], [33], [34]], which ranged from 0 to 16.2% (Table 1). Five studies (33.3%) reported household transmission [23,[25], [26], [27], 34] and four studies (26.7%, 4/15) reported non-household transmission of asymptomatic cases [23,[25], [26], [27]] (Supplemental Table S2). Household and non-household transmission rates were 0%–11.9% and 0%–2.5%, respectively.
3.2. Primary and Secondary Outcomes
The pooled transmission rates are 1.79% (95% CI 0.41%–3.16%) for asymptomatic cases, 5.02% (2.37%–7.66%) for presymptomatic cases, and 5.27% (2.40%–8.15%) for symptomatic cases (Table 2). We found that the transmission rate by asymptomatic infection was significantly less than presymptomatic (p<0.001) and symptomatic (p<0.001), while no significant difference was observed between presymptomatic and symptomatic infection (p=0.17). The ZIB models fit well and provide stable estimates for the asymptomatic, presymptomatic, and symptomatic pooled transmission rates (Supplemental Figure S1).
Table 2.
Pooled transmission rate of asymptomatic COVID-19 infection, presymptomatic COVID-19 infection, and symptomatic COVID-19 infection and subgroup analysis for asymptomatic infection.
Type of COVID-19 transmission source | No. of included studies | No. of studies with zero event | Total number of transmissions/ total number of contacts | Pooled transimission rate % (95% CI)* |
---|---|---|---|---|
Asymptomatic infection | 15 | 7 | 59/3917 | 1.79 (0.41, 3.16) |
Subgroup analysis | ||||
Sample of close contacts | ||||
Household | 5 | 3 | 7/301 | 4.22 (0.91, 7.52) |
Non-household | 4 | 2 | 3/438 | 1.03 (0.73, 1.33) |
Country | ||||
China | 10 | 4 | 49/3592 | 1.82 (0.11, 3.53) |
Other | 5 | 3 | 10/325 | 2.22 (0.67, 3.77) |
Presymptomatic infection | 6 | 1 | 100/2092 | 5.02 (2.37, 7.66) |
Symptomatic infection | 8 | 1 | 352/8823 | 5.27 (2.40, 8.15) |
Zero-inflated beta distribution was used to calculate the pooled rates.
Subgroup analyses for secondary transmission by asymptomatic infections found that the household transmission rate (4.22%, 95% CI 0.91%–7.52%) is four times higher than non-household transmission (1.03%, 0.73%–1.33%, p=0.03). The transmission rates in China (1.82%, 0.11%–3.53%) is significantly lower than in other countries (2.22%, 0.67%–3.77%, p=0.01) (Table 2).
Studies reporting transmission rates by different types of index cases were included in analyses for pooled relative risk (RR), including five for asymptomatic versus presymptomatic infection [23,27,31,33,35], seven for asymptomatic versus symptomatic infection [23,24,29,30,[32], [33], [34]], and 12 pairs of data from nine studies for asymptomatic versus presymptomatic or symptomatic infections [23,24,27,29,30,[32], [33], [34], [35]]. Individuals with asymptomatic infection have 46% lower risk of transmitting the virus than those with presymptomatic infection (RR 0.54, 95% CI 0.17–1.78, I2=85.6%), 42% lower risk than those with symptomatic infection (0.58, 0.22–1.56, I2=72.6%), and 42% lower risk than those with either asymptomatic or presymptomatic infection (0.58, 0.29–1.17, I2=77.8%) (Figure 2).
Fig. 2.
Forest plot of the risk ratio and 95% confidence interval of the transmission rates among the close contacts of asymptomatic index cases versus presymptomatic and/or symptomatic index cases.
AI, asymptomatic index cases; PI, presymptomatic index cases; SI, symptomatic index cases.
3.3. Sensitivity Analysis
Sensitivity analysis of the transmission rate of asymptomatic cases indicated that two studies had larger impacts on the pooled transmission rate. The transmission rates are reduced to 1.45% and 1.18% after excluding the studies by Gupta et al. [26] and by Shi et al. [33], respectively (Supplemental Table S3).
4. Discussion
This systematic review and meta-analysis provided summary estimation of transmission rates by asymptomatic, presymptomatic, and symptomatic SARS-CoV-2 infections. The pooled transmission rate of asymptomatic infection is 1.79%, which is significantly lower than those of presymptomatic (5.02%) and symptomatic infections (5.27%). SARS-CoV-2 is primarily transmitted from person-to-person through respiratory droplets, which are released when an individual with COVID-19 sneezes, coughs or talks [36]. Symptomatic patients are more likely to spread the virus and have a higher transmission rate than asymptomatic individuals. Infected individuals have the highest virus load and infectivity during numerous days before and after the onset of symptoms [37], thus presymptomatic individuals also have a higher transmission rate than asymptomatic ones. Another finding from our analysis is that the household transmission rate by asymptomatic infection (4.22%) is higher than non-household transmission rate (1.03%). A previous study indicated that compared to in non-household environments, exposure to continuous close contact and conversations with infected individuals in the crowded indoor environments substantially increased the transmission risk than in non-household environments [38].
Numerous systematic reviews and meta-analyses were published to explore the transmission of asymptomatic infections [1,2,[5], [6], [7], [8]]. One review reported SARS-CoV-2 transmission from asymptomatic cases among a wide scope of studies, including case reports, viral kinetic studies and serial interval studies [5]. Two meta-analyses reported the proportion of asymptomatic transmission among the contacts ranged from 0% to 80% [2,8], where the acquired range is much wider than our results (0%–9.2%). Among five studies included in this systematic review [2], four showed that the index SARS-CoV-2 cases became symptomatic during the follow-up for assessing secondary transmission. The difference in pooled transmission rates might be explained by the inclusion criterion of each study. Two meta-analyses compared the relative risks of transmission by asymptomatic versus by symptomatic infections (RR, 0.35 & 0.31) [1,6], which were smaller than the finding in our analysis ((RR, 0.58). This difference may be due to underestimation of asymptomatic transmission in early publications or due to the increase of asymptomatic transmissions of new SARS-CoV-2 variants as the epidemic continued to evolve. Our analysis also provides the additional relative risk of transmission for asymptomatic versus presymptomatic infections. The fifth meta-analysis reported the pooled household transmission rate without differentiating asymptomatic and presymptomatic index cases [7]. In comparison with these systematic reviews, our meta-analysis provided both absolute measure of pooled transmission rates and relative measure of the transmission risk by asymptomatic, presymptomatic and symptomatic infections.
5. Conclusions
Our review provides a comprehensive assessment of transmission risk of asymptomatic infections. Rigorous inclusion criteria for selecting eligible studies were applied to ensure the quality and homogeneity of the studies involved. All included studies had a defined period of follow-up to assess secondary transmission among close contacts with asymptomatic index cases, all studies had a clear sampling frame of at-risk population to ensure the homogeneity of the target population, and all studies had been peer reviewed. An additional strength of our study is that the studies with zero event of transmission were included in the meta-analysis by using the zero-inflated beta distribution approach.
This study also has limitations. First, only English studies were included, and this inclusion criterion might introduce potential bias. Second, heterogeneity assessment could not be performed, as studies with zero events could not be included in the heterogeneity tests; however, rigorous inclusion and exclusion criteria were used to minimize heterogeneity of the included studies. Third, the exposure time of the close contacts with their index cases was not reported in original studies, so its impact on asymptomatic transmission could not be assessed. COVID-19 is a fast-evolving pandemic with the emergence of new variants. By the end of October 2021, World Health Organization has designated 4 SARS-CoV-2 variants of concern and 2 variants of interest. People carrying different variants may have different infectivity and transmission risks. For example, the current dominant strain Delta is more infectious than the ancestral strains [39]. Our analysis only included the studies conducted in 2020 when Delta and Omicron had not become prevalent strains [40,41]. Few original studies have been conducted after 2020 [42]. For example, the study conducted during September 2020 and March 2021 in Canada showed that the odd of transmission from asymptomatic index patient to household contacts was slightly lower that from symptomatic index patients (0.6 vs. 0.9, with overlapping 95% confidence intervals) [42]. As more infectious strains such as Delta and Omicron become dominant, the transmission rate among susceptible close contacts may increase. Another factor of determining the transmission rate among close contacts with infected individuals is infection-induced or vaccination-induced seropositivity in the general population. As more people are infected with the virus or are vaccinated, population seroprevalence will become higher and the transmission rate will decline. Age may also play a key role in the transmission rate. Infected children with SARS-CoV-2 are less likely to develop symptoms than adults [3]. Our analysis included only one study among children. As most countries have opened schools in the fall semester of 2021, there is an increasing concern about the risk of transmission among children, particularly among those with asymptomatic infection. Moreover, wearing face masks can significantly reduce the risk of infection [43]. Of 15 studies included in our analysis, only two studies provided data on mask wearing [25,33], thus the impact of wearing masks on the transmission risk is not focused in this review. For the consideration of all these factors, continuing meta-analyses will be needed to provide updated estimates of transmission risk under new scenarios of epidemic, vaccination and population-level immunity and in special subgroup populations.
There are some strengths and limitations of this study. We focused on the asymptomatic transmission during a clearly defined period of follow-up in an early phase of the epidemic. And we used zero-inflated beta distribution to take the zero transmission rates into consideration. However, only English studies were included, and this inclusion criteria might introduce bias. Included studies were conducted prior to the emerging of SARS-CoV-2 variants delta and omicron, further meta-analysis may be needed to assess asymptomatic transmission of these new variants.
Funding
None declared.
Author contributions
HZQ, CiZ, and ChZ conceptualized the study. HZQ, CiZ, ChZ, XW, FQ, XL, HW, HuZ, TW, HL, HoZ, and SHV developed the study protocol. HZQ, CiZ, ChZ, XW, YG, PL, LD, XZ, and QJ developed the search strategy. CiZ and ChZ searched for relevant records. CiZ and ChZ assessed eligibility and extracted data under the supervision of HZQ. CiZ and ChZ analyzed the data. YX and SZ assisted with data analyses. HZQ, CiZ and ChZ interpreted the data. CiZ and ChZ wrote the first draft of manuscript. All authors critically revised the manuscript and approved the final version of the manuscript. Data were available to all authors. The corresponding author HZQ had final responsibility for the decision to submit for publication.
Acknowledgements
Not applicable.
Declaration of Competing Interest
None.
Data available statement
The data analyzed in this meta-analysis are from previously published studies, which have been cited. The R script is available at: https://github.com/ZRChao/Rscript_for_meta_analysis_of_COVID19_tranmission_rate.
Ethics statement
Ethics statement was waived cause no patients’ data was involved.
Informed consent
Informed consent was waived cause no patients’ data was involved.
Footnotes
Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.imj.2022.12.001.
Appendix. Supplementary materials
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