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Preplanned Studies: Characteristics and Containment of 74 Imported COVID-19 Outbreaks: Experiences, Lessons, and Implications — China, 2020–2021

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  • Summary

    What is already known about this topic?

    After the initial coronavirus disease 2019 (COVID-19) outbreak in Wuhan, China, the outbreaks during the dynamic-zero policy period in the mainland of China have not been systematically documented.

    What is added by this report?

    We summarized the characteristics of 74 imported COVID-19 outbreaks between March 19, 2020 and December 31, 2021. All outbreaks of early severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants were successfully contained with the aid of nucleic acid testing, modern communication technologies, and non-pharmacological interventions.

    What are the implications for public health practice?

    These findings provide us with confidence for the containment of future emerging infectious diseases alike at early stages to prevent pandemics or to win time to gain experience, develop vaccines and drugs, vaccinate people, and wait for the possible lessening of the virus’ pathogenicity.

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  • Funding: Supported by the Shenzhen Science and Technology Programs (RKX20210901150004012, KQTD20190929172835662, JSGG20220301090202005)
  • [1] Canjun Zheng, Zhaorui Chang, Fengfeng Liu, Mengjie Geng, Hui Chen, Jingwei Jiang, Sheng Zhou, Lu Ran, Zhongjie Li, Zijian Feng, George F. Gao, Liping Wang. Interpretation of the Protocol for Prevention and Control of COVID-19 in China (Edition 7)[J]. China CDC Weekly, 2020, 2(47): 902-905. doi: 10.46234/ccdcw2020.245CrossRef
    [2] Fengfeng Liu, Canjun Zheng, Liping Wang, Mengjie Geng, Hui Chen, Sheng Zhou, Lu Ran, Zhongjie Li, Yanping Zhang, Zijian Feng, George F. Gao, Zhaorui Chang. Interpretation of the Protocol for Prevention and Control of COVID-19 in China (Edition 8)[J]. China CDC Weekly, 2021, 3(25): 527-530. doi: 10.46234/ccdcw2021.138CrossRef
    [3] Tang JL, Li LM. Importance of public health tools in emerging infectious diseases. BMJ 2021;375:n2374. http://dx.doi.org/10.1136/BMJ.N2374CrossRef
    [4] Zhou YB, Jiang HL, Wang QY, Yang MX, Chen Y, Jiang QW. Use of contact tracing, isolation, and mass testing to control transmission of covid-19 in China. BMJ 2021;375:n2330. http://dx.doi.org/10.1136/BMJ.N2330CrossRef
    [5] Tu HW, Hu KQ, Zhang M, Zhuang YL, Song T. Effectiveness of 14 day quarantine strategy: Chinese experience of prevention and control. BMJ 2021;375:e066121. http://dx.doi.org/10.1136/BMJ-2021-066121CrossRef
    [6] An ZJ, Wang FZ, Pan A, Yin ZD, Rodewald L, Feng ZJ. Vaccination strategy and challenges for consolidating successful containment of covid-19 with population immunity in China. BMJ 2021;375:e066125. http://dx.doi.org/10.1136/bmj-2021-066125CrossRef
    [7] Li YY, Liu HX, Xia W, Wong GWK, Xu SQ. Cold chain logistics: a possible mode of SARS-CoV-2 transmission? BMJ 2021;375:e066129. http://dx.doi.org/10.1136/bmj-2021-066129.http://dx.doi.org/10.1136/bmj-2021-066129
    [8] Liu YJ, Yang BW, Liu LP, Jilili M, Yang A. Occupational characteristics in the outbreak of the COVID-19 delta variant in Nanjing, China: rethinking the occupational health and safety vulnerability of essential workers. Int J Environ Res Public Health 2021;18(20):10734. http://dx.doi.org/10.3390/ijerph182010734CrossRef
    [9] Chen ZY, Deng XW, Fang LQ, Sun KY, Wu YP, Che TL, et al. Epidemiological characteristics and transmission dynamics of the outbreak caused by the SARS-CoV-2 Omicron variant in Shanghai, China: a descriptive study. Lancet Reg Health West Pac 2022; 100592. 10.1101/2022.06.11.22276273.CrossRef
  • FIGURE 1.  Occurrence and size of outbreaks by region and time in the mainland of China between March 19, 2020 and December 31, 2021.

    Note: The number next to each outbreak refers to the unique ID number assigned for each outbreak in Supplementary Table S1. Cases with the same numbers belong to the same outbreak.

    Abbreviation: PLADs=provincial-level administrative divisions.

    TABLE 1.  Characteristics of the 74 outbreaks according to the three periods of study.

    Study periodLength of period (days)Number of outbreaks (n, %)Number of outbreaks involving ≥2
    PLADs (n, %)
    Number of outbreaks detected via proactive surveillance (n, %)Average number of cases per outbreak (median, range)Total number of cases (n, %)Duration of outbreaks (days) (median, range)Ratio of daily number of close contacts over that of cases (median, range)
    Period 1:
    2020/3/19–2020/9/30
    19614 (18.9)5 (35.7)2 (14.3)7 (1, 827)1,457 (14.5)11.5 (1, 39)29 (4, 2,807)
    Period 2:
    2020/10/1–2021/5/31
    24225 (33.8)4 (16.0)14 (56.0)13 (1, 1,055)2,632 (26.1)12.0 (1, 44)116 (8, 2,830)
    Period 3:
    2021/6/1–2021/12/31
    21335 (47.3)8 (22.9)27 (77.1)6 (1, 1,506)5,993 (59.4)7.0 (1, 62)68 (8, 1,737)
    P*0.386P<0.0010.8050.668P<0.001
    P for trend0.6100.0300.3920.7170.300
    Entire period65074 (100.0)17 (23.0)43 (58.1)10 (1, 1,506)10,082 (100.0)10.0 (1, 62)60 (4, 2,830)
    Abbreviation: PLADs=provincial-level administrative divisions.
    * P value for comparisons among the three study periods. Kruskal-Wallis test was used for comparisons in skewed continuous variables, Fisher’s exact Chi-square test for categorical variables, and linear regression and Cochran-Armitage trend test for assessing trend for the two types of variables, respectively.
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    TABLE 2.  Characteristics of the 74 outbreaks according to the source of the first case(s).

    Source of the first case (s)Number of outbreaks
    (n, %)
    Number of outbreaks involving ≥2 PLADs
    (n, %)
    Number of outbreaks detected via proactive surveillance (n, %)Average number of cases per outbreak (median, range)Total number of cases
    (n, %)
    Duration of outbreaks (days) (median, range)
    First frontier: cross border entrances35 (47.3)9 (25.7)23 (65.7)8 (1, 1,056)5,654 (56.1)8 (1, 62)
    Land borders15 (20.3)3 (20.0)11 (73.3)20 (1, 636)1,702 (16.9)11 (1, 62)
    Airports14 (18.9)5 (35.7)8 (57.1)5 (1, 1,506)3,551 (35.2)5 (1, 44)
    Ports6 (8.1)1 (16.7)4 (66.7)19 (1, 308)401 (4.0)8 (1, 24)
    Second frontier: Quarantine related 23 (31.1)1 (4.3)15 (65.2)2 (1, 468)805 (8.0)1 (1, 32)
    Possibly via quarantined inbound visitors13 (17.6)1 (7.7)7 (53.8)3 (1, 468)595 (5.9)1 (1, 32)
    Designated care hospitals5 (6.8)0 (0.0)4 (80.0)2 (1, 167)193 (1.9)7 (1, 24)
    Quarantine places5 (6.8)0 (0.0)4 (80.0)1 (1, 13)17 (0.2)1 (1, 11)
    Local community (eg, markets & malls)16 (21.6)7 (43.8)5 (31.3)92 (1, 1,055)3,623 (35.9)21 (1, 39)
    Possibly via cold chain5 (6.8)2 (40.0)2 (40.0)99 (10, 826)1,333 (13.2)25 (16, 31)
    Uncertain11 (14.9)5 (45.5)3 (27.3)89 (1, 1,055)2,290 (22.7)20 (1, 39)
    P*0.0080.055<0.001P<0.001
    All74 (100.0)17 (23.0)43 (58.1)10 (1, 1,056)10,082 (100.0)10 (1,62)
    Abbreviations: PLADs=provincial-level administrative divisions.
    * P value for comparisons among the three categories of sources of first cases. Kruskal-Wallis test was used for comparisons in skewed continuous variables, Fisher’s exact Chi-square test for categorical variables.
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Characteristics and Containment of 74 Imported COVID-19 Outbreaks: Experiences, Lessons, and Implications — China, 2020–2021

View author affiliations

Summary

What is already known about this topic?

After the initial coronavirus disease 2019 (COVID-19) outbreak in Wuhan, China, the outbreaks during the dynamic-zero policy period in the mainland of China have not been systematically documented.

What is added by this report?

We summarized the characteristics of 74 imported COVID-19 outbreaks between March 19, 2020 and December 31, 2021. All outbreaks of early severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants were successfully contained with the aid of nucleic acid testing, modern communication technologies, and non-pharmacological interventions.

What are the implications for public health practice?

These findings provide us with confidence for the containment of future emerging infectious diseases alike at early stages to prevent pandemics or to win time to gain experience, develop vaccines and drugs, vaccinate people, and wait for the possible lessening of the virus’ pathogenicity.

  • 1. Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen City, Guangdong Province, China
  • 2. Division of Epidemiology, JC School of Public Health and Primary Care, the Chinese University of Hong Kong, Hong Kong Special Administrate Region, China
  • 3. Department of Clinical Data Center, Guangzhou Women, and Children's Medical Center, Guangzhou Medical University, Guangzhou City, Guangdong Province, China
  • Corresponding authors:

    Zuyao Yang, zyang@cuhk.edu.hk

    Feng Sha, feng.sha@siat.ac.cn

  • Funding: Supported by the Shenzhen Science and Technology Programs (RKX20210901150004012, KQTD20190929172835662, JSGG20220301090202005)
  • Online Date: December 16 2022
    Issue Date: December 16 2022
    doi: 10.46234/ccdcw2022.228
  • After the successful containment of the initial coronavirus disease 2019 (COVID-19) outbreak in Wuhan, China adopted a dynamic-zero policy in March 2020 aimed at eradicating all imported outbreaks. In this report, we provided a comprehensive documentation and analyses of all the imported outbreaks before 2022. Data on daily COVID-19 infections were retrieved from the website of the National Health Commission of China. Results of epidemiological investigations of the outbreaks were retrieved from 1,504 publications by local governments or mainstream social media. Seventy-four outbreaks were identified consisting of 10,082 symptomatic cases and all were successfully contained. Characteristics of the outbreaks were summarized including source of the first case(s), time, place, scale, and duration. These data were then analyzed to identify potential problems and plan for future emerging infectious diseases alike. China’s experience in successfully containing 74 consecutive outbreaks provides important evidence that COVID-19 or newly emerging infectious diseases alike can be contained at their early stage to prevent the occurrence of pandemics, or at least gain experiences and win time for the development of vaccines and drugs.

    Data on daily number of imported cases, domestic cases, symptomatic domestic cases, and close contacts from March 19, 2020 to December 31, 2021 were retrieved from the official reports of Daily Briefing on Novel Coronavirus Cases. Our analyses of outbreaks only included symptomatic domestic cases from all the outbreaks; cases found in quarantined inbound cross-border travelers were excluded. For each symptomatic case, epidemiological investigations were traced via official reports from local governments. A total of 1,504 reports were retrieved and scrutinized. The definitions for outbreaks are presented in Supplementary Figure S1, available in https://weekly.chinacdc.cn/.

    The national daily numbers of cases, which included data on location and magnitude of these outbreaks, were described chronologically and geographically. Characteristics of the outbreaks were compared among 3 study periods divided according to the announcement dates of the 7th and 8th editions of the Protocol on Prevention and Control of COVID-19 and the source of the first case (1-2). All statistical analyses were performed by using R software version 3.6.2. A full description of methods is in Supplementary Materials, available in https://weekly.chinacdc.cn/.

    Overall, the study identified 74 outbreaks with a total of 10,082 symptomatic cases between March 19, 2020 and December 31, 2021 (Figure 1). The median number of cases in an outbreak was 10, ranging from 1 to 1,506. Out of the 74 outbreaks, 43 (58.1%) were detected via proactive surveillance, and 57 (77.0%) were contained at their origin within the provincial-level administrative divisions (PLADs) (Table 1). The outbreaks on average lasted for 10 days, ranging from 1 to 62 days. The ratio of daily number of close contacts over daily number of cases, an approximate indicator of people quarantined per case, was 60, ranging from 4 to 2,830. Detailed characteristics for each outbreak were presented in Supplementary Table S1 available in https://weekly.chinacdc.cn/.

    Study periodLength of period (days)Number of outbreaks (n, %)Number of outbreaks involving ≥2
    PLADs (n, %)
    Number of outbreaks detected via proactive surveillance (n, %)Average number of cases per outbreak (median, range)Total number of cases (n, %)Duration of outbreaks (days) (median, range)Ratio of daily number of close contacts over that of cases (median, range)
    Period 1:
    2020/3/19–2020/9/30
    19614 (18.9)5 (35.7)2 (14.3)7 (1, 827)1,457 (14.5)11.5 (1, 39)29 (4, 2,807)
    Period 2:
    2020/10/1–2021/5/31
    24225 (33.8)4 (16.0)14 (56.0)13 (1, 1,055)2,632 (26.1)12.0 (1, 44)116 (8, 2,830)
    Period 3:
    2021/6/1–2021/12/31
    21335 (47.3)8 (22.9)27 (77.1)6 (1, 1,506)5,993 (59.4)7.0 (1, 62)68 (8, 1,737)
    P*0.386P<0.0010.8050.668P<0.001
    P for trend0.6100.0300.3920.7170.300
    Entire period65074 (100.0)17 (23.0)43 (58.1)10 (1, 1,506)10,082 (100.0)10.0 (1, 62)60 (4, 2,830)
    Abbreviation: PLADs=provincial-level administrative divisions.
    * P value for comparisons among the three study periods. Kruskal-Wallis test was used for comparisons in skewed continuous variables, Fisher’s exact Chi-square test for categorical variables, and linear regression and Cochran-Armitage trend test for assessing trend for the two types of variables, respectively.

    Table 1.  Characteristics of the 74 outbreaks according to the three periods of study.

    Figure 1. 

    Occurrence and size of outbreaks by region and time in the mainland of China between March 19, 2020 and December 31, 2021.

    Note: The number next to each outbreak refers to the unique ID number assigned for each outbreak in Supplementary Table S1. Cases with the same numbers belong to the same outbreak.

    Abbreviation: PLADs=provincial-level administrative divisions.

    Due to heavy international air traffic, it was anticipated that the earliest imported outbreaks occurred in Guangdong, Beijing, Shanghai, and PLADs near them. These outbreaks were generally small and quickly contained. However, as outbreaks continued to spread, an increasing trend emerged including a higher frequency of outbreaks and higher number of PLADs involved (Figure 1). By December 31, 2021, all PLADs in the mainland of China had been involved in at least one outbreak except Xizang (Tibet). No seasonal trends were observed.

    Geographically, PLADs including Beijing, Shanghai, Guangdong, and their neighboring regions had the highest frequency of outbreak attacks (Supplementary Table S2). Five PLADs with the highest number of outbreaks included Beijing (11), Shanghai (10), Liaoning (10), Guangdong (9), and Heilongjiang (9). The 5 regions with the largest number of cases accumulated were Shaanxi (1,494 cases), Heilongjiang (1,145 cases), Hebei (1,103 cases), Xinjiang (906 cases) and Jiangsu (826 cases), totally accounting for 54.3% (5,474/10,082) of all cases.

    Chronologically, the daily number of imported cases that were diagnosed during quarantine and did not cause community outbreaks considerably fluctuated during the study period. Although there was no clear increasing trend with time, there was a slight elevation after June 2021 (Supplementary Figure S2). The daily number of symptomatic domestic cases and close contacts showed a similar pattern.

    In addition, the average size and duration of outbreaks and the average number of PLADs involved in each outbreak are shown in Table 1. Although the number of outbreaks and that of cases accumulated were chronologically increasing during the 3 periods of study, the last period had the highest proportion of outbreaks detected via active surveillance (77.1%), the smallest number of patients per outbreak (6 cases), shortest duration of outbreaks (7 days), the largest proportion of outbreaks involving only one PLAD (77.1%), and an average number of 68 close contacts quarantined per patient. These findings showed that the number of outbreaks and thus prevention and control intensity increased over time, but the effect and efficiency of response actions also increased. As a result, the situation remained largely controllable.

    Regarding the source of the first case(s) or the origin of an outbreak, 35 (47.3%) of the 74 outbreaks occurred at areas labeled as the first frontier, i.e., land borders, airports, and ports (Table 2). These outbreaks contributed 5,654 (56.1%) cases to the total number of cases from the 74 outbreaks (Supplementary Figure S3).

    Source of the first case (s)Number of outbreaks
    (n, %)
    Number of outbreaks involving ≥2 PLADs
    (n, %)
    Number of outbreaks detected via proactive surveillance (n, %)Average number of cases per outbreak (median, range)Total number of cases
    (n, %)
    Duration of outbreaks (days) (median, range)
    First frontier: cross border entrances35 (47.3)9 (25.7)23 (65.7)8 (1, 1,056)5,654 (56.1)8 (1, 62)
    Land borders15 (20.3)3 (20.0)11 (73.3)20 (1, 636)1,702 (16.9)11 (1, 62)
    Airports14 (18.9)5 (35.7)8 (57.1)5 (1, 1,506)3,551 (35.2)5 (1, 44)
    Ports6 (8.1)1 (16.7)4 (66.7)19 (1, 308)401 (4.0)8 (1, 24)
    Second frontier: Quarantine related 23 (31.1)1 (4.3)15 (65.2)2 (1, 468)805 (8.0)1 (1, 32)
    Possibly via quarantined inbound visitors13 (17.6)1 (7.7)7 (53.8)3 (1, 468)595 (5.9)1 (1, 32)
    Designated care hospitals5 (6.8)0 (0.0)4 (80.0)2 (1, 167)193 (1.9)7 (1, 24)
    Quarantine places5 (6.8)0 (0.0)4 (80.0)1 (1, 13)17 (0.2)1 (1, 11)
    Local community (eg, markets & malls)16 (21.6)7 (43.8)5 (31.3)92 (1, 1,055)3,623 (35.9)21 (1, 39)
    Possibly via cold chain5 (6.8)2 (40.0)2 (40.0)99 (10, 826)1,333 (13.2)25 (16, 31)
    Uncertain11 (14.9)5 (45.5)3 (27.3)89 (1, 1,055)2,290 (22.7)20 (1, 39)
    P*0.0080.055<0.001P<0.001
    All74 (100.0)17 (23.0)43 (58.1)10 (1, 1,056)10,082 (100.0)10 (1,62)
    Abbreviations: PLADs=provincial-level administrative divisions.
    * P value for comparisons among the three categories of sources of first cases. Kruskal-Wallis test was used for comparisons in skewed continuous variables, Fisher’s exact Chi-square test for categorical variables.

    Table 2.  Characteristics of the 74 outbreaks according to the source of the first case(s).

    Surprisingly, 23 (31.1%) outbreaks occurred at the second frontier, including those at designated care hospitals, quarantine places, and among inbound travelers whose incubation time might be longer than the quarantine time or who got infected during quarantine (Table 2). However, these outbreaks were relatively small in size, quickly contained, and accounted for only 8.0% of the total number of symptomatic cases from the 74 outbreaks.

    Lastly, 16 (21.6%) outbreaks were identified in communities such as shopping malls and food markets. Some were possibly caused via cold-chain logistics, while the rest had no clearly identifiable source of infection (Table 2). These outbreaks were most difficult to control when detected as well as difficult to detect once occurred, as only 31.3% (5 out of 16) were detected by proactive surveillance. As a result, they were most likely (43.8%) to involve 2 or more PLADs, resulting in more cases and longer durations per outbreak.

    • Under the dynamic-zero policy after the Wuhan outbreak, a total of 74 imported outbreaks were observed and successfully contained in the mainland of China before 2022. The success made in China, which was also demonstrated in economically less developed PLADs, proved that outbreaks of such highly infectious diseases could be rapidly contained by non-pharmacological interventions with the aid of nucleic acid testing and modern communication technologies.

      The first and most important lesson is to put prevention first. Second, effective surveillance and early detection of domestic cases are keys to controlling outbreaks. On the technical front, prevention and control tactics are nothing more than the three conventional methods in the control of infectious diseases, namely controlling infection sources, blocking transmission routes, and protecting susceptible populations (3-4).

      For controlling infection sources, quarantining inbound cross-border travelers is the first step (5). Due to limited quarantine facilities, international traveling also needs to be reduced. Routine nucleic acid testing in high-risk groups and general populations when deemed necessary is crucial for identifying new domestic cases. For blocking transmission routes, fast epidemiological investigations are possible with the aid of modern technologies and are important for the quick isolation of close contacts (4). For protecting susceptible populations, vaccination plays an important role but is far from enough due to fast waning of the protective effect of vaccines (6). When a community outbreak occurred, some restrictions on people’s movability could be implemented on top of all the above measures. In addition, social distancing and mask-wearing are always part of the policy (4).

      Another important lesson is to keep finding and closing the loopholes in current measures, which have been embodied in the 7th and 8th revisions of Chinese national guides for the prevention and control of COVID-19 (1-2). For instance, imported frozen goods from key areas were put under surveillance after outbreaks potentially related to cold chain logistics occurred in June 2020 (7). Another example is the complete separation of international and domestic passengers within the airport after a large outbreak that started in Nanjing Airport in July 2021 (8). The increasing number of proactively detected outbreaks over time reflected improvements in surveillance. The effects of these experiences were further confirmed in the recent large Omicron outbreak in Shanghai which caused over 626,000 cases but was eventually contained (9).

      The limitations of this study were discussed in Supplementary Materials.

      Although the strategy was overall effective, outbreaks and PLADs involved both increased over time. This may be partly because of 1) the increasing transmissibility of the new variants; 2) the efforts to resume work and life orders, which inevitably increased people’s movability, cross-border traveling, and imported goods, and caused shortening of quarantine time; and 3) the “pandemic fatigue” since people are becoming tired of the sustained pressure of the pandemic. After all, the strategy has successfully won time for China to gain experiences, develop vaccines and drugs, vaccinate people, and wait for the possible lessening of pathogenicity of the virus so that a massive number of hospitalizations and deaths from COVID-19 can be avoided, even if large outbreaks inevitably occur in the future.

    • No conflicts of interest.

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