Vital Surveillances: Genomic Surveillance for SARS-CoV-2 — China, September 26, 2022 to January 29, 2023

In this study, SARS-CoV-2 variant genome data was included for all cases of COVID-19 that had been sequenced in the SARS-CoV-2 laboratory network from September 26, 2022 to January 29, 2023 in China (the data from Hong Kong and Macau Special Administrative Regions and Taiwan, China were not included. Data was reported in real time by 31 provincial-level administrative divisions (PLADs) and Xinjiang Production and Construction Corps (XPCC) to the COVID-19 Notifiable Surveillance System of the National Institute for Virus Disease Control and Prevention, covering all regions in China.

The China COVID-19 Case Database is a laboratory-based surveillance system that receives real-time electronic data on laboratory-confirmed cases of SARS-CoV-2 from PLADs in China.

Data collection criteria included selecting three sentinel hospitals in three different regions of 31 PLADs and XPCC, with no fewer than 25 valid sequence tests completed weekly for each sentinel hospital in each PLAD. Additionally, surveillance of SARS-CoV-2 variants among inbound people was conducted at land, water, and airport ports.

The complete genome sequence of SARS-CoV-2 was obtained using Oxford Nanopore, Illumina, and BGI sequencing systems. Genomic analysis of all files was performed using CLC Genomics Workbench (version 21.0.4; Qiagen, Germany) and Nextclade webservers. The whole genome spliced sequence, sequence quality test, mutation sites, and the number of mutation sites were obtained.

From September 26, 2022 to January 29, 2023, 20,013 valid genome sequences of COVID-19 from domestic cases were reported by all 31 PLADs and XPCC, with 72 lineages. The predominant lineages were BA.5.2.48 (52.42%), BF.7.14 (22.70%), and BA.5.2.49 (16.30%), followed by 15 other lineages with proportions ranging from 0.11% to 2.46%, including BA.5.2, BA.2.76, BF.7, BA.5.1, BA.5.2.1, BA.2.75.2, BF.21, BN.1.3, BA.2.3, BA.5.2.20, BQ.1.10, BA.2.12.1, BF.11, BM.2, and BA.2.2. Additionally, 54 minority lineages with proportions below 0.10% accounted for 1.07% (Figure 1A). The proportion of BA.5.2.48 gradually increased from 7.14% (September 26–October 2, 2022) to 68.71% (January 23–28, 2023), while the proportion of BA.5.2.49 declined from 44.16% (October 3–9, 2022) to approximately 6%. Additionally, the proportion of BF.7.14 rose from 7.58% (October 17–23, 2022) to 34.07% (December 5–11, 2022), before decreasing to 22.70% (January 23–28, 2023) (Figure 1A).

Figure 1. 

Dynamic trends of SARS-CoV-2 lineages of domestic cases in China. (A) All lineages; (B) BA.5.2 and descendent lineages, and BF.7 and descendent lineages.

Note: Collection date interval was from September 26, 2022 to January 28, 2023. The data were derived from valid SARS-CoV-2 genome sequences of domestic and imported cases submitted by PLADs with a deadline date of January 29, 2023. The numbers marked on the right of the figure represent the number of valid genome sequences per week for all lineages. “Other” refers to lineages with proportions of Omicron variants less than 0.1% of domestic cases. The other 54 lineages include BA.2.75.1, XBB.1, BN.1.5, BY.1, BS.1.1, BA.5.2.27, BQ.1.1, BA.2, BA.5.1.7, BQ.1.2, BA.5.9, BE.1, BA.5.1.23, BF.5, BN.1.2, BA.5.2.26, BE.1.1, BQ.1.8, BQ.1.23, BA.5, BF.23, BQ.1, BF.4, BA.5.6, BE.4, BN.2, BQ.1.5, BF.7.5, BM.1.1, BF.18, BN.1, BA.5.2.34, BF.26, BA.5.2.6, BN.1.9, BA.5.2.28, BA.2.75.8, BA.5.2.16, BA.2.38, BS.1, XBB.1.2, BA.5.1.3, BA.5.2.21, BA.5.2.7, BA.2.3.20, BA.5.1.30, BA.2.5, BA.2.75.9, BA.2.2.1, CA.3, BQ.1.13, BA.5.2.12, BN.1.1, and BQ.1.1.17.

Abbreviations: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2; PLADs=provincial-level administrative divisions.

BA.5.2 and its descendant lineages, including BA.5.2, BA.5.2.1, BA.5.2.12, BA.5.2.16, BA.5.2.20, BA.5.2.21, BA.5.2.26, BA.5.2.27, BA.5.2.28, BA.5.2.34, BA.5.2.48, BA.5.2.49, BA.5.2.6, and BA.5.2.7 (Figure 1B), increased from 47.54% (September 26–October 2, 2022) to 82.66% (October 17–23, 2022), then decreased to 62.97% (October 31–November 6, 2022), increased again to 81.43% (November 14–20, 2022), and then decreased to 58.81% (December 5–11, 2022), finally reaching about 76%. BF.7 and its descendant lineages, including BF.7, BF.7.5, and BF.7.14 (Figure 1B), decreased from 21.92% (September 26–October 2, 2022) to 8.08% (October 17–23, 2022), then increased to 22.31% (October 31–November 6, 2022), decreased again to 15.37% (November 14–20, 2022), and then rose to 39.15% (December 5–11, 2022), finally reaching about 24%. When considering BA.5.2 and its descendant lineages and BF.7 and its descendant lineages together, their proportions increased from 69.46% (September 26–October 2, 2022) to about 100.00% (January 23–28, 2023).

Local BQ.1 and its descendent lineages (BQ.1.1, BQ.1.2, BQ.1.5, BQ.1.8, BQ.1.10, BQ.1.13, BQ.1.23, and BQ.1.1.17) were identified from October 10, 2022, with a total of 63 relative cases. Of these, BQ.1.10 and BQ.1.1 accounted for 50.79% (32/63) and 14.29% (9/63), respectively. Local XBB.1 and XBB.1.2 were identified from October 14, 2022, with a total of 16 relative cases.

From September 26, 2022 to January 29, 2023, a total of 1,978 valid genome sequences of COVID-19 imported cases were reported, with 169 evolutionary lineages. BA.5 and its descendant lineages were dominant in the imported mutant strains. Among them, BA.5.2, BF.7, BQ.1.1 (and BQ.1.2), and XBB.1 variants accounted for 18.17%, 8.63%, 11.26%, 7.57%, and 6.76% of imported cases, respectively (Figure 2).

Figure 2. 

Dynamic trends of SARS-CoV-2 lineages of imported cases from September 26, 2022 to January 21, 2023.

Note: Data were derived from valid SARS-CoV-2 genome sequences of domestic cases submitted by PLADs with a deadline of January 29, 2023. Numbers marked on the right of the figure represent the number of valid genome sequences per week for all lineages. “Other” refers to lineages with proportions of Omicron variants less than 0.5% of imported cases. The other 158 lineages included BA.5.2.47, XBB.3, CM.12, BN.1.4, BQ.1.12, XBB.1.1, BA.5.9, BF.7.4.1, BQ.1.8, BN.1.5, BQ.1.25, BF.7.5, BA.2.75.5, CK.1, BQ.1.1.4, BE.1, BA.4.6, BN.1.9, BQ.1.11, BF.11, BN.1.3.1, BF.21, XBB.1.4, BA.5.2.19, BA.5.2.43, BQ.1.1.31, CM.4, BA.5.2.16, BQ.1.13, BA.5.2.28, BA.5.6, BA.2, BQ.1.1.1, BF.7.4, CM.5, BA.5, BF.28, BL.1, BF.7.6, BQ.1.14, BQ.1.1.3, BA.5.2.9, BA.5.2.24, BA.5.2.7, CK.2.1, BA.5.1.30, BQ.1.1.8, BF.4, BA.2.3.7, BA.5.2.36, BF.14, CP.1, BA.4, XBB.1.3, CM.2, BA.2.10.1, BA.5.1.22, BY.1, BA.5.1.10, CH.1.1.1, BQ.1.3, DQ.1, CR.1.1, BN.3.1, XBF, XBB.1.9, BW.1.1, BQ.1.24, BA.5.1.25, BA.5.2.3, BA.5.6.4, BE.1.1.1, BA.5.2.26, BS.1, BA.5.1.24, BA.5.1.6, BA.5.1.5, BA.5.2.13, BL.1.4, BM.1.1.3, DA.1, BA.5.2.25, BN.6, BQ.1.13.1, CN.1, CR.1.3, BA.5.5, BA.5.2.23, BA.5.1.28, BQ.1.1.13, BR.2, CR.1, BE.8, CK.2.1.1, BN.1.1, BF.26, BE.4.2, CM.5.1, BN.1.1.1, BQ.1.1.10, BE.1.4.2, CK.1.2, BF.7.15, BQ.1.27, BA.5.2.18, CZ.1, BA.2.75, BA.4.7, BM.1.1.1, BA.5.1.31, XBB.3.1, BA.5.3.1, BA.5.2.44, BA.4.1.8, BA.5.1.9, BF.31.1, XBB.4, BA.2.75.8, BA.5.2.21, BA.2.2, BA.5.2.14, BS.1.1, BM.4.1.1, XBB.2.1, BQ.1.1.22, CM.8.1, BF.11.2, BM.1.1, XBB.3.2, BE.10, BM.1, BA.5.5.1, BJ.1, BL.2, DG.1, XBB.2.2, BU.1, BQ.1.22, CJ.1, BF.7.13.2, BE.7, BQ.1.7, BQ.1.26, BA.5.1.1, BR.3, BQ.1.1.27, BF.25, BA.5.2.32, DE.2, BQ.1.1.2, BL.6, BQ.1.10.1, BQ.1.1.5, CH.1.1.3, BQ.1.1.32, BA.5.1.3, BN.1.3.2, and BE.9.

Abbreviation: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2; PLADs=provincial-level administrative divisions.

From December 1, 2022 to January 29, 2023, the 31 PLADs and XPCC reported 11,311 valid SARS-CoV-2 genome sequences from domestic cases, with 26 evolutionary lineages in total. The most prevalent lineages were BA.5.2.48 (62.08%) and BF.7.14 (26.95%), followed by 6 other lineages, BA.5.2.49, BA.5.2, BF.7, BA.5.1, BA.2.76, and BA.5.2.20, with proportions ranging from 0.16% to 6.88%. The remaining 18 lineages accounted for 0.42%. No novel SARS-CoV-2 Omicron variants with altered biological properties or of public health significance were identified since December 1, 2022.

Table 1 shows that 54.55% of the cases were male, 37.03% were female, and 8.42% were unknown. The 19–60-year age group had the highest proportion (39.49%), followed by the 61–80-year age group (22.04%). The numbers of subjects in the <4 and 4–18-year age groups were similar, and 10.15% of the subjects had no information regarding their age. From December 1, 2022, the number of subjects gradually increased to 2,342 cases (January 5–11, 2023). The main lineages after December 2022 were BA.5.2.48 and BF.7.14, which together accounted for 89.03% of the total.

Overall, BF.7 and its descendant lineages were predominant in Beijing and Tianjin Municipalities. The prevalence rates of BF.7 and its descendant lineages and BA.5.2 and its descendant lineages in Jiangsu Province and Inner Mongolia Autonomous Region were approximately equal. BA.5.2 and its descendant lineages were predominant in other PLADs (Figure 3).

Figure 3. 

Surveillance of the epidemic variant of SARS-CoV-2 in all PLADs and XPCC in China.

Note: Collection date interval was from September 26, 2022 to January 28, 2023. The data were derived from the valid genome sequences of SARS-CoV-2 of indigenous cases submitted by PLADs with a deadline of January 29, 2023.

Abbreviation: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2; PLADs=provincial-level administrative divisions; XPCC=Xinjiang Production and Construction Corps.

According to the latest data from the Pango nomenclature, the strain BF.7 was identified as containing four characteristic amino acid mutation sites (ORF7a:H47Y, ORF1b:L238F, S:C1243F, and ORF1a:V274L) and one characteristic nucleotide mutation site (C29632T), and was designated BF.7.14.

Among the domestic cases, the lineages of BF.7.14 accounted for 99.52%, suggesting that the main prevalence of BF.7 was BF.7.14. In the imported cases, BF.7.14 lineages accounted for 61.90%, indicating that BF.7.14 had been found in the imported cases from international sources to our country. The earliest reported BF.7.14 domestic cases were from the Inner Mongolia Autonomous Region on September 27, 2022. Subsequent cases were mainly distributed between November 21 and December 6, 2022, and from December 19, 2022 to January 19, 2023. The earliest reported BF.7.14 imported case was from Belarus on September 25, 2022. Subsequent BF.7.14 imported cases were mainly concentrated in December 2022 (Figure 4A).

Figure 4. 

Distribution of domestic and imported cases in (A) BF.7.14 lineage and (B) BA.5.2.48 lineage based on sampling time.

According to the latest data from Pango nomenclature, BA.5.2 containing four additional characteristic nucleotide acid mutation sites (C2710T, C8626T, C16887T, and T17208C) was named BA.5.2.48. The BA.5.2.48 subvariants accounted for 69.18% of BA.5.2 in domestic cases and 9.08% in imported cases in China. The earliest domestic case of BA.5.2.48 was reported in Guangdong Province on July 13, 2022. The earliest reported BA.5.2.48 imported case was a case who entered the country from Russia on August 15, 2022 (Figure 4B).

The chi-square test revealed statistically significant differences in the proportions of three clinical types of cases (asymptomatic, mild, and severe) between BA.5.2 and BF.7 (P<0.05) (Table 2). The proportions of asymptomatic and severe cases of BA.5.2 were higher than those of BF.7, while the proportion of mild cases was lower than that of BF.7. Additionally, there was no statistically significant difference in the proportions of the clinical type cases of ordinary and death between BA.5.2 and BF.7.

Data from September 26, 2022 showed that the predominant lineages circulating in China were domestic cases of BA.5.2 and BF.7, accounting for 93.95% of the total. The proportion of BA.5.2 fluctuated from rising to falling before entering a plateau period, while the proportion of BF.7 experienced two declines and rises before also entering a plateau period. This suggests a counter-balancing relationship between the two main epidemic strains, with the other lineages gradually decreasing.

According to the World Health Organization (WHO), from December 30, 2022 to January 30, 2023, the Omicron variant of concern (VOC) accounted for 99.9% of sequences reported in the GISAID database in the past 30 days globally (6). BA.5 and its descendent lineages remain dominant globally (6). Major subvariants BF.7, BQ.1 (and BQ.1.1), and XBB, which are currently being tracked by WHO, also accounted for an important proportion of imported cases in China, suggesting that the imported SARS-CoV-2 variants in China were consistent with the international epidemic variants.

Surveillance of domestic and imported cases revealed that, following the adjustment of China’s dynamic COVID-zero policy in December 2022, BA.5.2 and BF.7 quickly became the predominant circulating lineages and caused widespread epidemics in the country. No novel SARS-CoV-2 Omicron variants were identified that resulted in altered biological properties or were of public health significance. The COVID-19 epidemic Omicron variants in China were associated with imported cases, in line with the overall global situation.

China will continue to conduct comprehensive monitoring of the variation in the SARS-CoV-2 genomic sequences. If emerging lineages with mutations of interest are detected, closer attention will be paid, and the genome sequence will be shared globally via GISAID or other international genome databases.

No conflicts of interest.

SARS-CoV-2 Genome Working Group includes Yang Pan, Hui Xu, Zhaomin Feng, Fu Li, Shujuan Cui, Bing Lyu, Zhichao Liang, Daitao Zhang (Beijing Municipality); Xiaoyan Li, Zhichao Zhuang, Yue Lei, Ming Zou, Zhaolin Tan, Xin Gao, Baolu Zheng, Xiaochang Liu, Aiping Yu, Xiaohui Lu, Yuan Wang, Yanzhen Han, Ying Wang (Tianjin Municipality); Hui Jiang, Chaonan Wang, Lingyue Yuan, Xiaoxian Cui, Fanghao Fang, Run Li, Jing Zhou, Yuyang Wang, Jiajing Liu, Yong Chen, Xiaoqing Cui, Hongwei Di, Hongyou Chen, Min Chen (Shanghai Municipality); Sheng Ye, Shuang Chen, Yun Tang, Zhen Yu, Zhangping Tan, Mingyue Wang (Chongqing Municipality); Xu Han, Guangyue Han, Shiyou Liu, Zhaoyi Jia, Hongbin Zhang, Minghao Geng, Tong Su, Yanan Cai, Baohua He, Shaoxuan Song, Junli Zhang (Hebei Province); Junyu Zhao, Ruijuan Zhang, Binzhi Ren (Shanxi Province); Lingling Mao, Haibo Sun, Lulu Wang, Shuang Liu, Xuesheng Liu, Xiaoting Xu, Bo Wang, Lu Lei, Ge Song, Sinong Sun, Hanyi Guo, Na Liu, Zhijian Bo (Liaoning Province); Donglin Wu, Xianda Yang, Yao Yang, Jing Li, Hongmin Liu, Leilei Wei, Wei Zhao, Weiyu Zhang, Ben Shi, Hui Wang, Xihui Zang (Jilin Province); Jun Xu, Qi Liang, Chang Shu, Ming Yang, Fengju Ouyang, Lu Tang, Xin Shi, Hua Hua, Yan Leng, Fengying Xia (Heilongjiang Province); Changjun Bao, Liguo Zhu, Shenjiao Wang, Jianguang Fu, Huan Fan, Fei Deng, Huiyan Yu, Zhifeng Li, Lunbiao Cui, Kangcheng Zhao, Xiaojuan Zhu, Yiyue Ge (Jiangsu Province); Yi Sun, Hao Yan, Lingxuan Su, Honghu Chen, Baofeng Zhou, Wenwu Yao (Zhejiang Province); Yong Sun, Weiwei Li, Jun He, Peng Wang, Wenchang Li, Wanrong Luo, Wanxing Lu, Ruan Wu, Xinxin Wang, Tai Ma, Xiaomin Wu, Lingkang Yang, Weixi Fang, Xue Zhou, Juanjuan Liu (Anhui Province); Qi Lin, Zhimiao Huang, Wei Chen, Zhiwei Zeng, Yingxiang Zheng, Quwen Li (Fujian Province); Jianxiong Li, Yong Shi, Bowen Wuyang, Gang Xu, Jun Zhou, Yanni Zhang, Xiaoqing Liu, Qian Wang, Shiwen Liu, Dajin Xiao, Xin Ran, Shuting Wei, Jiabo Du (Jiangxi Province); Zengqiang Kou, Ti Liu, Yan Li, Ming Fang, Mingxiao Yao, Yuwei Zhang, Xiaolin Liu, Hui Lyu, Gaoxiang Sun, Zhongyan Fu, Bo Pang, Shuang Wang, Lu Liu, Julong Wu, Yujie He, Jianxing Wang, Shu Zhang, Ziqing Liu, Zhen Dong (Shandong Province); Hongxia Ma, Baifan Zhang, Yi Li, Sheng Zhao, Haiyan Wei, Dongxiao Li, Shidong Lu, Yun Song, Xiao Hu, Lin Zhu (Henan Province); Bin Fang, Linlin Liu, Xiao Yu, Qiangling Yin, Xiaolu Zhang, Mingwei Peng, Yating Zhang, Cong Liu, Shi Han (Hubei Province); Xingyu Xiang, Zhifei Zhan, Yiwei Huang, Juan Wang, Shuai Chen, Zixiang He, Ran Liu (Hunan Province); Chang Zhang, Zhencui Li, Lijun Liang, Yao Hu, Fangzhu Ouyang, Shen Huang, Jiajun Liu, Zhonghua Zheng, Hanri Zeng, Jing Xu, Qianfang Guo, Jianxiang Yu, Qiqi Tan, Juan Su, Pengfai Jia (Guangdong Province); Lei Cui, Chuyang Sun, Yinggui Cai, Shizhuang Kuang, Xiaoting Gan, Yunting Zeng, Dandan Li, Su Wang, Xin Wei (Hainan Province); Jianan Xu, Li Liu, Zhongping Huang, Mingfeng Jiang, Chenxia Liu, Wenxia Zhao, Qiuhua Yu, Qinghua Huang, Xiaozhen Ma, Ranran Cao, Chaohua Xu, Ying Ding, Hongyu Liao, Rongmei Yuan, Na Li, Ximei Fu, Huiping Yang, Wei Li, Yuliang Feng, Hongrong Zhong, Cheng Wang, Wenbo Li, Lili Liu, Gaopeng Lei, Lin Zhang, Li Liu, Hong Lyu, Na Chen, Yi Zhang, Linzi Zeng (Sichuan Province); Lin Fu, Yonghu Wan, Ping Wu, Li Zhuang, Qian Ke, Ju Zheng, Weifang Shi, Dan Wang, Danya She, Qing Ma, Ying Liu, Chunting Liu, Xinggui Yang, Jingshu Xiang, Qian Zhou, Yuhui Wu, Xiaoyu Wei, Weijia Jiang (Guizhou Province); Meiling Zhang, Ruize Ni, Jienan Zhou, Xiaonan Zhao, Yanhong Sun, Zhaosheng Liu (Yunnan Province); Yao Meng, Shen Li, Bin Chen (Shaanxi Province); Baodi Li, Jianhua Chen, Congshan Xu, Miao Wang, Biao Wang, Zhe Zhao, Xueying Wang, Haizhuo Wu, Hui Zhang, Yingjie Zhao, Guina Zhu, Yu Zhen (Gansu Province); Youju Lei, Meiying Zhong, Qianlan Li, Mengqi Yin, Lifang He, Chonghai Li, Xiaotong Wang (Qinghai Province); Xiaoling Tian, Hai Yan, Wu Yihan, Tana, Lu Yang, Dongyan Zhang, Xinxin Yu, Xueyao Zhang, Ying Chen (Inner Mongolia Autonomous Region); Yu Ju, Fuyin Bi, Huafeng Chen, Ning Kang, Jing Wang, Zhenli Liang, Hang Huang, Bao Lu, Meirong Tang, Chizhen Liao (Guangxi Zhuang Autonomous Region); Hongmei, Qin Wang, Guolong Dai, Suolangdeji, Luoyangcuo, Wentao Zhao, Cidanzhuoga, Suoyang [Xizang (Tibet) Autonomous Region]; Zhonglan Wu, Jianxin Pei, Xiang Liu (Ningxia Hui Autonomous Region); Xin Ma, Jun Zhao, Jia Huang, Zhenguo Gao, Xuan Zhang, Yuan Chen, NIGEDELI·Alitengsaier, Hundezi·Awuxi, Quanxi Li, Rong Wang, Muhtar·Amir (Xinjiang Uygur Autonomous Region); Yuxia Liu, Yao He, Jingxia Guo, Chi Du (Xinjiang Production and Construction Corps). All teams were involved in high-throughput sequencing of the SARS-CoV-2 genome.