Asymptomatic SARS-CoV-2 Infections Among Persons Entering China From April 16 to October 12, 2020 | Global Health | JAMA | JAMA Network
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Figure.  International Entrants to China From April 16, 2020, to October 12, 2020
International Entrants to China From April 16, 2020, to October 12, 2020

aTested positive for SARS-CoV-2 infection via a polymerase chain reaction test.

bDid not have symptoms throughout the 14-day quarantine.

cHad symptoms throughout the 14-day quarantine.

dDeveloped symptoms during the 14-day quarantine.

Table.  Characteristics of International Entrants to China From April 16, 2020, to October 12, 2020
Characteristics of International Entrants to China From April 16, 2020, to October 12, 2020
1.
Wu  Z, McGoogan  JM.  Asymptomatic and pre-symptomatic COVID-19 in China.   Infect Dis Poverty. 2020;9(1):72. doi:10.1186/s40249-020-00679-2PubMedGoogle ScholarCrossref
2.
Zhou  L, Wu  Z, Li  Z,  et al; China COVID-19 Task Force.  One hundred days of COVID-19 prevention and control in China.   Clin Infect Dis. Published online June 5, 2020. doi:10.1093/cid/ciaa725PubMedGoogle Scholar
3.
World Health Organization. WHO COVID-19 case definition. Accessed September 19, 2020. https://www.who.int/ publications/i/item/WHO-2019-nCoV-Surveillance_Case_Definition-2020.1
4.
Davies  NG, Klepac  P, Liu  Y, Prem  K, Jit  M, Eggo  RM; CMMID COVID-19 Working Group.  Age-dependent effects in the transmission and control of COVID-19 epidemics.   Nat Med. 2020;26(8):1205-1211. doi:10.1038/s41591-020-0962-9PubMedGoogle ScholarCrossref
5.
Stokes  EK, Zambrano  LD, Anderson  KN,  et al.  Coronavirus disease 2019 case surveillance—United States, January 22–May 30, 2020.   MMWR Morb Mortal Wkly Rep. 2020;69(24):759-765. doi:10.15585/mmwr.mm6924e2PubMedGoogle ScholarCrossref
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Research Letter
February 2, 2021

Asymptomatic SARS-CoV-2 Infections Among Persons Entering China From April 16 to October 12, 2020

Author Affiliations
  • 1Chinese Center for Disease Control and Prevention, Beijing, China
JAMA. 2021;325(5):489-492. doi:10.1001/jama.2020.23942

The magnitude of asymptomatic severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection is a question of global concern. Individuals who test positive for SARS-CoV-2 infection via a polymerase chain reaction (PCR) test but lack coronavirus disease 2019 (COVID-19)–like symptoms must be followed up through the incubation period to distinguish individuals with asymptomatic infection from those with presymptomatic infection.1

China successfully controlled its initial COVID-19 epidemic in March 20202 and has since focused on preventing importation of SARS-CoV-2 infection. Beginning April 1, 2020, persons entering China via air, sea, or land have been mandatorily tested for SARS-CoV-2 infection by PCR test at border checkpoints. Individuals who have tested positive have been hospitalized in isolation and those who have tested negative have been quarantined for 14 days at centralized facilities and then retested on day 13. We assessed the proportion of international entrants to China with asymptomatic SARS-CoV-2 infection.

Methods

This retrospective cohort study was approved by the institutional review board of the Chinese Center for Disease Control and Prevention; informed consent was not required. All international entrants found to have SARS-CoV-2 infection via a positive PCR test result at China’s border checkpoints from April 16 to October 12 were included in this study. This allowed 15 days for full policy implementation (April 1-15) and 13 days of follow-up for the last enrolled participant (October 13-25).

Participants were categorized as either confirmed COVID-19 cases (ie, positive test results for SARS-CoV-2 infection plus being symptomatic or presymptomatic) or asymptomatic SARS-CoV-2 infection cases (ie, positive test results for SARS-CoV-2 infection but having no symptoms throughout the 14-day quarantine).1 Although different from the that of the World Health Organization,3 this case definition is standard in China.1 Fifteen-day intervals during the study were used to investigate changes over time.

The χ2, Cochran-Mantel-Haenszel, and Jonckheere-Terpstra nonparametric trend tests were used. A 2-sided P< .05 was considered statistically significant. All analyses were performed using SAS software version 9.2 (SAS Institute Inc).

Results

Of the 19 398 384 international travelers who entered China during the study period, 3103 had SARS-CoV-2 infection. Most were male (75.5%) and were aged 20 to 49 years (80.8%) (Table). Among all SARS-CoV-2–positive entrants, 1354 (43.6%) had symptoms at entry (symptomatic) and 137 (4.4%) developed symptoms (presymptomatic; median time to symptom onset, 1 day; interquartile range [IQR], 0-5 days; 95th percentile, 10 days) and were categorized as confirmed COVID-19 cases, whereas 1612 (51.9%) never developed symptoms through day 13 and were considered to have asymptomatic SARS-CoV-2 infection.

Among all international entrants (part A in the Figure), the proportion of SARS-CoV-2–positive persons screened remained stable at 0.01% to 0.03% (part B), but the proportion of individuals with symptomatic, presymptomatic, and asymptomatic SARS-CoV-2 infection did not remain stable (part C). Among all SARS-CoV-2–positive entrants, the proportion of asymptomatic infections increased significantly over time from 27.8% during April 16 to April 30 to 59.4% during September 28 to October 12 (P < .001) (Table).

No association was found between presence of symptoms and sex (P = .61). A significant association was found between presence of symptoms and age (P < .001) (Table). Although median age was highest in the April 16-30 period at 38 years (IQR, 23-45 years), it decreased to 24 years (IQR, 20-33 years) in the May 1-15 period, then significantly increased, reaching 35 years (IQR, 29-46 years) in the September 28–October 12 period. Of SARS-CoV-2–positive entrants, 43.7% arrived from just 4 of 86 countries (Table). Among confirmed COVID-19 cases, the proportion who were symptomatic (median, 95.4%; range, 93.0%-98.7%) vs presymptomatic (median, 4.6%; range, 1.3%-5.6%) did not change significantly over time (P = .27).

Discussion

The finding of a high and increasing proportion of asymptomatic infections among all SARS-CoV-2–positive international entrants to China may signal an increase in asymptomatic infection globally. Because asymptomatic SARS-CoV-2 infection is thought to be more common in young people,4 and severe and critical case status is more common in older adults,5 the finding of increasing age in the population over time indicates that the results were not biased by age. Moreover, the unchanging proportion of symptomatic cases among all confirmed cases suggests that the increase in asymptomatic infections over time was not due to symptomatic persons being screened out before travel.

The main limitation was the inability to directly ascertain how many symptomatic individuals were screened out or whether any individuals were screened in because of prior infection and prolonged viral shedding. Nevertheless, this study has implications for traveler screening policies and procedures.

Section Editor: Jody W. Zylke, MD, Deputy Editor.
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Article Information

Accepted for Publication: November 16, 2020.

Corresponding Author: Zunyou Wu, MD, PhD, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, 155 Changbai Rd, Changping District, Beijing 102206, China (wuzy@263.net).

Author Contributions: Dr Wu had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Wu.

Acquisition, analysis, or interpretation of data: Ren, Zhang, Li, McGoogan, Feng, Gao, Wu.

Drafting of the manuscript: Ren, Wu.

Critical revision of the manuscript for important intellectual content: Zhang, Li, McGoogan, Feng, Gao, Wu.

Statistical analysis: Ren, Wu.

Obtained funding: Wu.

Administrative, technical, or material support: Li, McGoogan, Feng, Gao, Wu.

Supervision: Zhang, Wu.

Conflict of Interest Disclosures: None reported.

Funding/Support: This study was supported by grant 2020YFC0846300 from the Chinese Ministry of Science and Technology and grant 1G11TW010941 from the Fogarty International Center at the US National Institutes of Health.

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Disclaimer: The opinions expressed herein reflect the collective views of the authors and do not necessarily represent the official position of the Chinese Center for Disease Control and Prevention.

References
1.
Wu  Z, McGoogan  JM.  Asymptomatic and pre-symptomatic COVID-19 in China.   Infect Dis Poverty. 2020;9(1):72. doi:10.1186/s40249-020-00679-2PubMedGoogle ScholarCrossref
2.
Zhou  L, Wu  Z, Li  Z,  et al; China COVID-19 Task Force.  One hundred days of COVID-19 prevention and control in China.   Clin Infect Dis. Published online June 5, 2020. doi:10.1093/cid/ciaa725PubMedGoogle Scholar
3.
World Health Organization. WHO COVID-19 case definition. Accessed September 19, 2020. https://www.who.int/ publications/i/item/WHO-2019-nCoV-Surveillance_Case_Definition-2020.1
4.
Davies  NG, Klepac  P, Liu  Y, Prem  K, Jit  M, Eggo  RM; CMMID COVID-19 Working Group.  Age-dependent effects in the transmission and control of COVID-19 epidemics.   Nat Med. 2020;26(8):1205-1211. doi:10.1038/s41591-020-0962-9PubMedGoogle ScholarCrossref
5.
Stokes  EK, Zambrano  LD, Anderson  KN,  et al.  Coronavirus disease 2019 case surveillance—United States, January 22–May 30, 2020.   MMWR Morb Mortal Wkly Rep. 2020;69(24):759-765. doi:10.15585/mmwr.mm6924e2PubMedGoogle ScholarCrossref
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