Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the etiological agent of coronavirus disease 2019 (COVID-19), is constantly mutating under the different circumstances of global transmission (1). The emerging SARS-CoV-2 variants may have potential adverse impacts on epidemic traits and severity. To some extent, it is also capable of escaping natural and vaccine-induced immunity (2-3). Some of them were designated as variants of concern (VOCs) by the World Health Organization (WHO) (4). Therefore, robust surveillance is essential to assess the evolution of viruses in real time.
After the epidemic in Wuhan City was brought under control in 2020, several COVID-19 outbreaks in the mainland of China have been proven to relate to SARS-CoV-2 contaminated cold-chain products (5-7), while most were caused by transmission through imported cases on flights, at isolation facilities, or in designated hospitals (8-9). Therefore, genomic surveillance for SARS-CoV-2 from imported cases is of great significance for monitoring the risk of different variants that were imported into the mainland of China, assessing the risk of importation-associated domestic spread, and helping guide public health interventions. On March 17, 2020, the China CDC released a notice and launched genomic surveillance for SARS-CoV-2 from imported COVID-19 cases nationwide. The laboratories of provincial CDCs were required to conduct SARS-CoV-2 whole-genome sequencing for samples from imported cases and submit the genomic sequences to the China CDC in time. This study includes the analysis of genomic surveillance data of imported SARS-CoV-2 cases of 2021 from the mainland of China.
The SARS-CoV-2 genomic sequences of 3,355 imported COVID-19 cases were submitted to the China CDC from January 1 to December 31, 2021 (upon validation, one sequence of them was submitted on December 25, 2020). Except for Xizang (Tibet) Autonomous Region and Qinghai Province, the remaining provincial-level administrative divisions (PLADs) had sequences submitted in various amounts (Figure 1A). The 3 PLADs with the largest submitted sequences were Shanghai Municipality (23.9%, 803/3,355), Yunnan Province (22.9%, 768/3,355), and Guangdong Province (16.9%, 568/3,355), followed by Tianjin Municipality, Fujian Province, Sichuan Province, and Henan Province, which submitted more than 100 sequences each. There were 8 PLADs that submitted 30–100 sequences. The remaining 14 PLADs submitted fewer than 30 sequences each.Figure 1. The surveillance of SARS-CoV-2 genome of imported cases in the mainland of China, 2021. (A) The number of genomic sequences of imported cases submitted by PLADs. (B) The median sequence deposition time of each PLAD from sample collection to sequence submission.
Note: Data as of December 31, 2021. Grey part means no data.
Abbreviation: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2; PLAD=provincial-level administrative division.
To validate the timeliness of the sequence submission, the deposition time of each sequence was calculated according to the date of sample collection and sequence submission. The results showed that Shaanxi Province had the longest median time of sequence deposition with 67 days (Q3-Q1=109-8), followed by Fujian with 23 days (Q3-Q1=44-11). The remaining PLADs submitted sequences within 3 weeks of sample collection (Figure 1B).
Of the 3,355 sequences, 3,309 sequences were collected in 2021. Of the 3,309 sequences, 2,388 (72.2%) had a genomic coverage of >90%, allowing for further lineage analysis (Figure 2A). From January to April, the number of submitted sequences was less than 100 available sequences per month. Since May, the number had increased, with more than 100 available sequences per month. July and August had the highest numbers, with 548 and 407 available sequences, respectively. All five VOCs (Alpha, Beta, Gamma, Delta, and Omicron) were identified in the imported cases. The proportion of the Alpha variant was the highest from February to May. Subsequently, the Delta variant gradually replaced Alpha, becoming dominant in June and overwhelmingly dominant from August to November (more than 95% per month). In December, Omicron variants were detected, accounting for 54.3% (151/278) of the sequences, including BA.1 and BA.2 lineages.Figure 2. The proportion of SARS-CoV-2 VOCs in the imported SARS-CoV-2 surveillance and in GISAID, 2021. (A) The imported SARS-CoV-2 surveillance in the mainland of China (Data as of December 31, 2021). (B) GISAID (Data as of March 19, 2022). Abbreviation: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2; VOC=variant of concern; GISAID=the Global Initiative of Sharing All Influenza Data.
The pattern of prevalence of the VOCs from the imported SARS-CoV-2 surveillance was similar to that in GISAID (Figure 2B). However, the relative proportions of VOCs were different, particularly for the Beta and Gamma variants. From January to May, the proportion of the Beta variant in the imported SARS-CoV-2 surveillance was more than 10% per month, compared to the data of 1.2%–2.2% in GISAID. The proportion of Gamma variant was the highest in April (5.1%, 2/39) and decreased to 1.4% (2/141) and 1.2% (3/259) in May and June, respectively, in the imported SARS-CoV-2 surveillance. In GISAID, the proportion of Gamma variant was 5.9% (26,530/449,653) in April, which increased to 7.5% (25,933/347,752) in May, and reached a maximum of 7.9% (22,660/285,518) in June.
To assess the sensitivity of the surveillance, the time of each VOC for sample collection of the first record, the initial local transmission in the mainland of China as well as its designation by the WHO as a VOC were recorded (Table 1). The time intervals for Alpha, Delta, and Omicron variants between sample collection of their first record in the surveillance and WHO designation were less than one month. Except for Gamma, the time period for the remaining VOCs causing local transmission in the mainland of China was later than that of the sample collection of their first records in the surveillance. There was no local transmission caused by the Gamma variant in the mainland of China.
VOC Earliest recorded sequence in the imported
Date of first local
samples in the world†
Date of designation
by the WHO†
Submitted PLAD Submission date Alpha Shanghai 2020-12-25
VOC: 2020-12-18 Beta Hunan 2021-2-7
VOC: 2020-12-18 Gamma Jiangsu 2021-3-30
VOC: 2021-1-11 Delta Chongqing 2021-4-28
Omicron (BA.1*) Tianjin 2021-12-13
Omicron (BA.2*) Guangdong 2021-12-29
* Includes the descendent lineages.
† According to the official information published by the World Health Organization (4).
Abbreviation: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2; WHO=World Health Organization; VOC=variant of concern; VOI=variant of interest; VUM=variant under monitoring; PLAD=provincial-level administrative division.
Table 1. The detection of SARS-CoV-2 VOCs in the mainland of China and the world.