To the Editor—Since identification and initial characterization of COVID-19 in late December 2019 and early January 2020, China’s containment goal has been complete interruption of local transmission of the coronavirus SARS-CoV-21. The nationwide epidemic wave centered on Wuhan was contained by April 2020 with non-pharmaceutical interventions alone but was associated with economic loss: China’s first-quarter gross domestic product fell 6.8% compared with that in the first quarter of 2019 (ref. 2). Since containment, there have been numerous outbreaks in China caused by imported viruses with local spread, varying in size from several cases to about 1,000 cases, all stopped with non-pharmaceutical interventions alone3. Sustained containment has high socioeconomic value: economic activities recovered rapidly, with an increase in gross domestic product of 3.2% during April through June 2020, and of 4.9% during July through September 2020 (ref. 2); the government’s response to the pandemic was perceived positively by the Chinese public4. In this Correspondence, we describe two large-scale PCR-based testing strategies that have played critically important roles in sustaining containment since April 2020 in mainland China: routine, active, PCR-based screening, and mass PCR testing during the outbreak response.

With almost all of China’s population being susceptible to SARS-CoV-2 before the induction of any vaccine-induced population immunity5, imported viruses posed an enormous threat to containment. All incoming international travelers, workers handling imported goods, medical-center outpatients with fever or respiratory symptoms, and medical staff caring for patients with fever or infectious diseases are actively screened with PCR to determine if they are infected. Incoming travelers have been required to quarantine at designated hotels for 14 days after entry into China, during which time they are tested at least twice. As of 30 November 2020, 3,866 SARS-CoV-2-infected travelers had been diagnosed, which prevented seeding of the virus in susceptible communities (Fig. 1).

Fig. 1: Local and imported COVID-19 cases from 1 April 2020 to 30 November 2020.
figure1

Light blue wide bars indicate outbreaks (key) and adjacent labels indicate mass PCR testing strategies.

Outbreak investigations in Beijing and Dalian found that food contamination could potentially transmit SARS-CoV-26,7. Isolation of viable virus in the outer packages of imported seafood in Qingdao strengthened the evidence for such transmission. Workers handling imported goods are now required to be tested weekly for SARS-CoV-2, which has prevented several importation-related outbreaks—for example, four dockworkers were found to have become infected in December 2020 in Dalian, and an outbreak investigation in Kashgar, Xinjiang, found importation of SARS-CoV-2 via a contaminated cross-border truck.

Fever clinics have long been established in secondary and tertiary hospitals. Anyone with fever seeking healthcare is screened by PCR. Medical facilities admit anyone with suspected COVID-19, unexplained pneumonia, or severe, acute respiratory-tract infection, and they test the patients and accompanying people by PCR. This screening strategy has identified index cases of several outbreaks: the Xinfadi market in Beijing; Dalian; Pudong airport8; Qingdao9; and Manchuria.

Routine testing requires many PCR tests. Laboratories combine five or ten specimens and test the combination for SARS-CoV-2 RNA as an efficiency and cost-saving measure. If the combination tests have a positive result, people whose samples were combined are tested separately to identify the infected person (or people). With a 10:1 pooled sampling approach, the average cost per person tested is approximately 9 RMB yuan (US$ 1.50) in China.

Routine PCR testing is augmented with testing of all close contacts of an infected person. Since September 2020, all close contacts of infected people have been required to be tested three times during a 14-day centralized quarantine period: at day 1 or 2; 1 day later; and at day 14.

Mass, community-wide PCR testing during or after an outbreak response has proven to be a useful strategy for identifying infected people, including those with no symptoms, and for determining whether a community is free of SARS-CoV-2. Once a local outbreak is identified, geographic jurisdictions are classified by epidemiologists into regions at low, moderate or high risk of transmitting the virus. People in high-risk settings are tested individually. In moderate-risk areas, a 5:1 or 10:1 pooled sampling approach is used to reduce the number of tests.

The first city-wide mass screening was performed between 14 May and 1 June 2020 in Wuhan city; nearly 10 million people were tested by PCR, and 300 asymptomatically infected people were identified for quarantine. The testing results were used to support full reopening of local socioeconomic activities10. Large screening programs have been implemented following local case reports that indicated possible community transmission. For instance, during the outbreak in Beijing’s Xinfadi market, 11.9 million people were tested between 11 June and 14 July 2020; in Dalian, 4.5 million people were tested between 26 July and 31 July 2020; and in Qingdao, 10.9 million people were tested between 11 October and 16 October 2020 (ref. 9). These risk-based, large-scale, population-wide screenings contributed to case finding and rapid control of epidemics and provided evidence for the government to reopen economic activities.

The timeliness of PCR test results varies by testing purpose and epidemiological situation. For members of the public who request PCR testing but have no symptoms or exposure history, results are to be reported within 24 hours. Results for outpatients, inpatients, caregivers, close contacts of confirmed cases and people residing in high-risk areas in a local outbreak setting are to be reported within 12 hours. Results for patients in fever clinics and emergency departments are to be reported within 6 hours.

In China’s ‘new-normal’ situation, comprehensive, active and innovative PCR testing strategies are performed for targeted groups and in outbreak settings; this ensures timeliness of early case detection and interruption of local outbreaks—essential ingredients in the prevention and control strategy. Maintenance of containment has greatly reduced the impact of COVID-19 in terms of suffering, lives lost and socioeconomic progress.

The introduction of vaccines against COVID-19 globally and in China will undoubtedly improve epidemiological situations. PCR testing strategies will be adjusted to fit the changing epidemiological situation in China—probably one in which few or fewer non-pharmaceutical interventions will be needed for effective epidemic control. Inexpensive, readily available and rapid PCR testing will continue to be essential for sensitive surveillance of SARS-CoV-2 well into the future. Throughout 2020, PCR testing served the public well, helping to make and keep China nearly free of SARS-CoV-2, and providing socioeconomic space and time for vaccine development and long-term prevention and control of COVID-19.

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Acknowledgements

We thank L. Rodewald for contributions to the content and improvement to the text of this Correspondence.

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Z.L., Z.F. and G.F.G. designed and supervised the study; Z.L. and F.L. wrote the manuscript; J.C. designed and drew the figure; Z.P., Z.C., Q.C. and L.W. participated in literature review and data collection; and S.L. and G.F.G. commented on and revised drafts of the manuscript.

Corresponding author

Correspondence to
Zijian Feng.

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The authors declare no competing interests.

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Li, Z., Liu, F., Cui, J. et al. Comprehensive large-scale nucleic acid–testing strategies support China’s sustained containment of COVID-19.
Nat Med (2021). https://doi.org/10.1038/s41591-021-01308-7

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