Primary assessment of the diversity of Omicron sublineages and the epidemiologic features of autumn/winter 2022 COVID-19 wave in Chinese mainland

doi:10.1007/s11684-022-0981-7

Front. Med.

2023, Vol. 17

Issue (4) : 758-767 https://doi.org/10.1007/s11684-022-0981-7

RESEARCH ARTICLE

Primary assessment of the diversity of Omicron sublineages and the epidemiologic features of autumn/winter 2022 COVID-19 wave in Chinese mainland

Gang Lu¹, Yun Ling², Minghao Jiang¹, Yun Tan¹, Dong Wei³, Lu Jiang¹, Shuting Yu¹, Fangying Jiang¹, Shuai Wang¹, Yao Dai¹, Jinzeng Wang¹, Geng Wu⁴, Xinxin Zhang³, Guoyu Meng¹(

), Shengyue Wang¹(

), Feng Liu¹(

), Xiaohong Fan²(

), Saijuan Chen¹(

)

¹. Shanghai Institute of Hematology, National Research Center for Translational Medicine, State Key Laboratory of Medical Genomics, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
². Shanghai Public Health Clinical Center, Fudan University, Shanghai 200083, China
³. Department of Infectious Diseases, Research Laboratory of Clinical Virology, National Research Center for Translational Medicine, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
⁴. State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, The Joint International Research Laboratory of Metabolic and Developmental Sciences, Shanghai Jiao Tong University, Shanghai 200240, China

Download: PDF(2213 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

With the recent ongoing autumn/winter 2022 COVID-19 wave and the adjustment of public health control measures, there have been widespread SARS-CoV-2 infections in Chinese mainland. Here we have analyzed 369 viral genomes from recently diagnosed COVID-19 patients in Shanghai, identifying a large number of sublineages of the SARS-CoV-2 Omicron family. Phylogenetic analysis, coupled with contact history tracing, revealed simultaneous community transmission of two Omicron sublineages dominating the infections in some areas of China (BA.5.2 mainly in Guangzhou and Shanghai, and BF.7 mainly in Beijing) and two highly infectious sublineages recently imported from abroad (XBB and BQ.1). Publicly available data from August 31 to November 29, 2022 indicated an overall severe/critical case rate of 0.035% nationwide, while analysis of 5706 symptomatic patients treated at the Shanghai Public Health Center between September 1 and December 26, 2022 showed that 20 cases (0.35%) without comorbidities progressed into severe/critical conditions and 153 cases (2.68%) with COVID-19-exacerbated comorbidities progressed into severe/critical conditions. These observations shall alert healthcare providers to place more resources for the treatment of severe/critical cases. Furthermore, mathematical modeling predicts this autumn/winter wave might pass through major cities in China by the end of the year, whereas some middle and western provinces and rural areas would be hit by the upcoming infection wave in mid-to-late January 2023, and the duration and magnitude of upcoming outbreak could be dramatically enhanced by the extensive travels during the Spring Festival (January 21, 2023). Altogether, these preliminary data highlight the needs to allocate resources to early diagnosis and effective treatment of severe cases and the protection of vulnerable population, especially in the rural areas, to ensure the country’s smooth exit from the ongoing pandemic and accelerate socio-economic recovery.

Keywords SARS-CoV-2 COVID-19 Omicron genomic epidemiology

Corresponding Author(s): Guoyu Meng,Shengyue Wang,Feng Liu,Xiaohong Fan,Saijuan Chen

Just Accepted Date: 30 December 2022 Online First Date: 29 March 2023 Issue Date: 12 October 2023

Cite this article:

Gang Lu,Yun Ling,Minghao Jiang, et al. Primary assessment of the diversity of Omicron sublineages and the epidemiologic features of autumn/winter 2022 COVID-19 wave in Chinese mainland[J]. Front. Med., 2023, 17(4): 758-767.

URL:

https://academic.hep.com.cn/fmd/EN/10.1007/s11684-022-0981-7
https://academic.hep.com.cn/fmd/EN/Y2023/V17/I4/758

Fig.1 Genomic epidemiology analysis of the SARS-CoV-2 genomes sampled from patients diagnosed during the outbreak of autumn/winter 2022. (A) Phylogenetic tree of recently sequenced viral genomes in Shanghai cases. Major sublineages are indicated by squares. (B) Bar plot of the number of genomes for different Omicron sublineages. (C) Pie charts of inferred origin-of-infection for indicated sublineages. (D) Pie charts of the relative fractions of Omicron sublineages per inferred origin-of-infection. Asterisk indicates all known subvariants grouped under each sublineage. The BF.7 sublineage was not included in counting of the BA.5.2 sublineage in (D).

Fig.2 Symptomatic patients during autumn/winter COVID-19 outbreaks in Chinese mainland. (A) Count of all infected cases (upper panel) and severe/critical cases (bottom panel) in Chinese mainland. (B) Pie chart of symptomatic patients with different severities treated in Shanghai Public Health Center (SHPHC).

Tab.1 Clinical features of enrolled patients as of December 26, 2022

Fig.3 Mathematical modeling of the ongoing Omicron outbreak in representative areas in Chinese mainland. (A) Plot of accumulated total COVID-19 cases in the modeling of the autumn/winter Omicron infection waves in selected regions (cities or provinces). (B) Plot of predicted number of daily COVID-19 cases and accumulated total cases as in (A). Total cases in each region were used for simulation except for Chongqing, where the cases in urban or suburban areas were separated. For Chongqing suburban cases, two independent simulations were performed to estimate the influence of Spring Festival travel rush on the rural areas.

1	Y Zhang, H Zhang, W Zhang. SARS-CoV-2 variants, immune escape, and countermeasures. Front Med 2022; 16(2): 196–207 https://doi.org/10.1007/s11684-021-0906-x pmid: 35253097
2	PV Markov, A Katzourakis, NI Stilianakis. Antigenic evolution will lead to new SARS-CoV-2 variants with unpredictable severity. Nat Rev Microbiol 2022; 20(5): 251–252 https://doi.org/10.1038/s41579-022-00722-z pmid: 35288685
3	N Jalali, HK Brustad, A Frigessi, EA MacDonald, H Meijerink, SL Feruglio, KM Nygård, G Rø, EH Madslien, Blasio BF de. Increased household transmission and immune escape of the SARS-CoV-2 Omicron compared to Delta variants. Nat Commun 2022; 13(1): 5706 https://doi.org/10.1038/s41467-022-33233-9 pmid: 36175424
4	Y Cao, J Wang, F Jian, T Xiao, W Song, A Yisimayi, W Huang, Q Li, P Wang, R An, J Wang, Y Wang, X Niu, S Yang, H Liang, H Sun, T Li, Y Yu, Q Cui, S Liu, X Yang, S Du, Z Zhang, X Hao, F Shao, R Jin, X Wang, J Xiao, Y Wang, XS Xie. Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies. Nature 2022; 602(7898): 657–663 https://doi.org/10.1038/s41586-021-04385-3 pmid: 35016194
5	LB Shrestha, C Foster, W Rawlinson, N Tedla, RA Bull. Evolution of the SARS-CoV-2 omicron variants BA.1 to BA.5: implications for immune escape and transmission. Rev Med Virol 2022; 32(5): e2381 https://doi.org/10.1002/rmv.2381 pmid: 35856385
6	Y CaoF Jian J WangY YuW SongA YisimayiJ Wang R AnX Chen N ZhangY WangP WangL ZhaoH Sun L YuS Yang X NiuT Xiao Q GuF Shao X HaoY Xu R JinZ Shen Y WangXS Xie. Imprinted SARS-CoV-2 humoral immunity induces convergent Omicron RBD evolution. Nature 2022; [Epub ahead of print] doi: 10.1038/s41586-022-05644-7 pmid: 36535326
7	G Bálint, B Vörös-Horváth, A Széchenyi. Omicron: increased transmissibility and decreased pathogenicity. Signal Transduct Target Ther 2022; 7(1): 151 https://doi.org/10.1038/s41392-022-01009-8 pmid: 35525870
8	National Health Commission of China. Transcription of the Press Conference of the State Council Joint Prevention and Control Mechanism on December 14th, 2022. 2022. Available at the website of the National Health Commission of China
9	PB McIntyre, R Aggarwal, I Jani, J Jawad, S Kochhar, N MacDonald, SA Madhi, E Mohsni, K Mulholland, KM Neuzil, H Nohynek, F Olayinka, P Pitisuttithum, AJ Pollard, A Cravioto. COVID-19 vaccine strategies must focus on severe disease and global equity. Lancet 2022; 399(10322): 406–410 https://doi.org/10.1016/S0140-6736(21)02835-X pmid: 34922639
10	SA Buchan, H Chung, KA Brown, PC Austin, DB Fell, JB Gubbay, S Nasreen, KL Schwartz, ME Sundaram, M Tadrous, K Wilson, SE Wilson, JC Kwong. Estimated effectiveness of COVID-19 vaccines against Omicron or Delta symptomatic infection and severe outcomes. JAMA Netw Open 2022; 5(9): e2232760 https://doi.org/10.1001/jamanetworkopen.2022.32760 pmid: 36136332
11	National Health Commission of China. Notice on Issuing the Overall Plan for Implementing Class B Management for COVID-19 Infection. 2022-12-16. Available at the website of the National Health Commission of China
12	National Health Commission of China. Notice on Further Optimizing Measures for the Prevention and Control of COVID-19 Epidemic and Scientifically and Precisely Carrying out Prevention and Control Work. 2022-11-01. Available at the website of the National Health Commission of China
13	OT Ng, K Marimuthu, N Lim, ZQ Lim, NM Thevasagayam, V Koh, CJ Chiew, S Ma, M Koh, PY Low, SB Tan, J Ho, S Maurer-Stroh, VJM Lee, YS Leo, KB Tan, AR Cook, CC Tan. Analysis of COVID-19 incidence and severity among adults vaccinated with 2-dose mRNA COVID-19 or inactivated SARS-CoV-2 vaccines with and without boosters in Singapore. JAMA Netw Open 2022; 5(8): e2228900 https://doi.org/10.1001/jamanetworkopen.2022.28900 pmid: 36018588
14	L Tang, Y Zhang, F Wang, D Wu, ZH Qian, R Zhang, AB Wang, C Huang, H Wang, Y Ye, M Lu, C Wang, YT Ma, J Pan, YF Li, XY Lv, Z An, L Rodewald, XY Wang, YM Shao, ZY Wu, Z Yin. Relative vaccine effectiveness against Delta and Omicron COVID-19 after homologous inactivated vaccine boosting: a retrospective cohort study. BMJ Open 2022; 12(11): e063919 https://doi.org/10.1136/bmjopen-2022-063919 pmid: 36368753
15	SL Kwok, SM Cheng, JN Leung, K Leung, CK Lee, JM Peiris, JT Wu. Waning antibody levels after COVID-19 vaccination with mRNA Comirnaty and inactivated CoronaVac vaccines in blood donors, Hong Kong, April 2020 to October 2021. Euro Surveill 2022; 27(2): 2101197 https://doi.org/10.2807/1560-7917.ES.2022.27.2.2101197 pmid: 35027105
16	Y Cao, A Yisimayi, F Jian, W Song, T Xiao, L Wang, S Du, J Wang, Q Li, X Chen, Y Yu, P Wang, Z Zhang, P Liu, R An, X Hao, Y Wang, J Wang, R Feng, H Sun, L Zhao, W Zhang, D Zhao, J Zheng, L Yu, C Li, N Zhang, R Wang, X Niu, S Yang, X Song, Y Chai, Y Hu, Y Shi, L Zheng, Z Li, Q Gu, F Shao, W Huang, R Jin, Z Shen, Y Wang, X Wang, J Xiao, XS Xie. BA.2.12.1, BA.4 and BA.5 escape antibodies elicited by Omicron infection. Nature 2022; 608(7923): 593–602 https://doi.org/10.1038/s41586-022-04980-y pmid: 35714668
17	X Zhang, Y Tan, Y Ling, G Lu, F Liu, Z Yi, X Jia, M Wu, B Shi, S Xu, J Chen, W Wang, B Chen, L Jiang, S Yu, J Lu, J Wang, M Xu, Z Yuan, Q Zhang, X Zhang, G Zhao, S Wang, S Chen, H Lu. Viral and host factors related to the clinical outcome of COVID-19. Nature 2020; 583(7816): 437–440 https://doi.org/10.1038/s41586-020-2355-0 pmid: 32434211
18	X Zhang, W Zhang, S Chen. Shanghai’s life-saving efforts against the current omicron wave of the COVID-19 pandemic. Lancet 2022; 399(10340): 2011–2012 https://doi.org/10.1016/S0140-6736(22)00838-8 pmid: 35533708
19	Y Ling, G Lu, F Liu, Y Tan, X Xu, D Wei, J Xu, S Wang, S Yu, F Jiang, X Zhang, S Chen, S Wang, X Fan, S Chen. The Omicron BA.2.2.1 subvariant drove the wave of SARS-CoV-2 outbreak in Shanghai during spring 2022. Cell Discov 2022; 8(1): 97 https://doi.org/10.1038/s41421-022-00468-1 pmid: 36167678
20	M Jiang, H Yin, S Zhang, G Meng, G Wu. Mathematical appraisal of SARS-CoV-2 Omicron epidemic outbreak in unprecedented Shanghai lockdown. Front Med (Lausanne) 2022; 9: 1021560 https://doi.org/10.3389/fmed.2022.1021560 pmid: 36425099
21	Z FuD Liang W ZhangD ShiY MaD WeiJ Xi S YangX XuD TianZ ZhuM Guo L JiangS YuS WangF JiangY Ling S WangS ChenF LiuY TanX Fan. Host protection against Omicron BA.2.2 sublineages by prior vaccination in spring 2022 COVID-19 outbreak in Shanghai. Front Med 2022; [Epub ahead of print] doi:10.1007/s11684-022-0977-3
22	Y Tan, F Liu, X Xu, Y Ling, W Huang, Z Zhu, M Guo, Y Lin, Z Fu, D Liang, T Zhang, J Fan, M Xu, H Lu, S Chen. Durability of neutralizing antibodies and T-cell response post SARS-CoV-2 infection. Front Med 2020; 14(6): 746–751 https://doi.org/10.1007/s11684-020-0822-5 pmid: 33017040
23	National Health Commission of China. Diagnosis and Treatment Protocol for COVID-19 (Ninth Edition). 2022. Available at the website of the National Health Commission of China
24	S Chen, Y Zhou, Y Chen, J Gu. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34(17): i884–i890 https://doi.org/10.1093/bioinformatics/bty560 pmid: 30423086
25	DE Wood, J Lu, B Langmead. Improved metagenomic analysis with Kraken 2. Genome Biol 2019; 20(1): 257 https://doi.org/10.1186/s13059-019-1891-0 pmid: 31779668
26	Á O’Toole, E Scher, A Underwood, B Jackson, V Hill, JT McCrone, R Colquhoun, C Ruis, K Abu-Dahab, B Taylor, C Yeats, Plessis L du, D Maloney, N Medd, SW Attwood, DM Aanensen, EC Holmes, OG Pybus, A Rambaut. Assignment of epidemiological lineages in an emerging pandemic using the pangolin tool. Virus Evol 2021; 7(2): veab064 https://doi.org/10.1093/ve/veab064 pmid: 34527285
27	J Hadfield, C Megill, SM Bell, J Huddleston, B Potter, C Callender, P Sagulenko, T Bedford, RA Neher. Nextstrain: real-time tracking of pathogen evolution. Bioinformatics 2018; 34(23): 4121–4123 https://doi.org/10.1093/bioinformatics/bty407 pmid: 29790939
28	P Di Tommaso, M Chatzou, EW Floden, PP Barja, E Palumbo, C Notredame. Nextflow enables reproducible computational workflows. Nat Biotechnol 2017; 35(4): 316–319 https://doi.org/10.1038/nbt.3820 pmid: 28398311
29	Chuan Guan News. BA.5.2 and BF.7 showed no significant difference on host response. 2022-12-25. Available at the website of the People’s Government of Sichuan Province
30	Y Ling, G Lu, F Liu, Y Tan, X Xu, D Wei, J Xu, S Wang, S Yu, F Jiang, X Zhang, S Chen, S Wang, X Fan, S Chen. The Omicron BA.2.2.1 subvariant drove the wave of SARS-CoV-2 outbreak in Shanghai during spring 2022. Cell Discov 2022; 8(1): 97 https://doi.org/10.1038/s41421-022-00468-1 pmid: 36167678
31	Z CaoW Gao H BaoH Feng S MeiP Chen Y GaoZ Cui Q ZhangX MengH GuiW WangY Jiang Z SongY ShiJ SunY ZhangQ Xie Y XuG Ning Y GaoR Zhao. VV116 versus nirmatrelvir-ritonavir for oral treatment of Covid-19. N Engl J Med 2022; NEJMoa2208822 doi:10.1056/NEJMoa2208822 pmid: 36577095
32	J Hammond, H Leister-Tebbe, A Gardner, P Abreu, W Bao, W Wisemandle, M Baniecki, VM Hendrick, B Damle, A Simón-Campos, R Pypstra, JM; EPIC-HR Investigators Rusnak. Oral nirmatrelvir for high-risk, nonhospitalized adults with Covid-19. N Engl J Med 2022; 386(15): 1397–1408 https://doi.org/10.1056/NEJMoa2118542 pmid: 35172054

[1]	Hao Wang, Yu Yuan, Bihao Wu, Mingzhong Xiao, Zhen Wang, Tingyue Diao, Rui Zeng, Li Chen, Yanshou Lei, Pinpin Long, Yi Guo, Xuefeng Lai, Yuying Wen, Wenhui Li, Hao Cai, Lulu Song, Wei Ni, Youyun Zhao, Kani Ouyang, Jingzhi Wang, Qi Wang, Li Liu, Chaolong Wang, An Pan, Xiaodong Li, Rui Gong, Tangchun Wu. Neutralization against SARS-CoV-2 Delta/Omicron variants and B cell response after inactivated vaccination among COVID-19 convalescents[J]. Front. Med., 2023, 17(4): 747-757.
[2]	Ziyu Fu, Dongguo Liang, Wei Zhang, Dongling Shi, Yuhua Ma, Dong Wei, Junxiang Xi, Sizhe Yang, Xiaoguang Xu, Di Tian, Zhaoqing Zhu, Mingquan Guo, Lu Jiang, Shuting Yu, Shuai Wang, Fangyin Jiang, Yun Ling, Shengyue Wang, Saijuan Chen, Feng Liu, Yun Tan, Xiaohong Fan. Host protection against Omicron BA.2.2 sublineages by prior vaccination in spring 2022 COVID-19 outbreak in Shanghai[J]. Front. Med., 2023, 17(3): 562-575.
[3]	Chuansong Quan, Zhenjie Zhang, Guoyong Ding, Fengwei Sun, Hengxia Zhao, Qinghua Liu, Chuanmin Ma, Jing Wang, Liang Wang, Wenbo Zhao, Jinjie He, Yu Wang, Qian He, Michael J. Carr, Dayan Wang, Qiang Xiao, Weifeng Shi. Seroprevalence of influenza viruses in Shandong, Northern China during the COVID-19 pandemic[J]. Front. Med., 2022, 16(6): 984-990.
[4]	Suning Chen, Weili Zhao, Jianyong Li, Depei Wu, on behalf of Lymphoid Disease Group, Chinese Society of Hematology, Chinese Medical Association. Chinese expert consensus on oral drugs for the treatment of mature B-cell lymphomas (2020 edition)[J]. Front. Med., 2022, 16(5): 815-826.
[5]	Xiaoguang Xu, Wei Zhang, Mingquan Guo, Chenlu Xiao, Ziyu Fu, Shuting Yu, Lu Jiang, Shengyue Wang, Yun Ling, Feng Liu, Yun Tan, Saijuan Chen. Integrated analysis of gut microbiome and host immune responses in COVID-19[J]. Front. Med., 2022, 16(2): 263-275.
[6]	Yi Zhang, Haocheng Zhang, Wenhong Zhang. SARS-CoV-2 variants, immune escape, and countermeasures[J]. Front. Med., 2022, 16(2): 196-207.
[7]	Yiming Shao, Yingqi Wu, Yi Feng, Wenxin Xu, Feng Xiong, Xinxin Zhang. SARS-CoV-2 vaccine research and immunization strategies for improved control of the COVID-19 pandemic[J]. Front. Med., 2022, 16(2): 185-195.
[8]	Wei Zhang, Xiaoguang Xu, Ziyu Fu, Jian Chen, Saijuan Chen, Yun Tan. PathogenTrack and Yeskit: tools for identifying intracellular pathogens from single-cell RNA-sequencing datasets as illustrated by application to COVID-19[J]. Front. Med., 2022, 16(2): 251-262.
[9]	Zehong Huang, Yingying Su, Tianying Zhang, Ningshao Xia. A review of the safety and efficacy of current COVID-19 vaccines[J]. Front. Med., 2022, 16(1): 39-55.
[10]	Yuntao Zhang, Yunkai Yang, Niu Qiao, Xuewei Wang, Ling Ding, Xiujuan Zhu, Yu Liang, Zibo Han, Feng Liu, Xinxin Zhang, Xiaoming Yang. Early assessment of the safety and immunogenicity of a third dose (booster) of COVID-19 immunization in Chinese adults[J]. Front. Med., 2022, 16(1): 93-101.
[11]	Qiaoli Shi, Fei Xia, Qixin Wang, Fulong Liao, Qiuyan Guo, Chengchao Xu, Jigang Wang. Discovery and repurposing of artemisinin[J]. Front. Med., 2022, 16(1): 1-9.
[12]	Huai-yu Wang, Suyuan Peng, Zhanghui Ye, Pengfei Li, Qing Li, Xuanyu Shi, Rui Zeng, Ying Yao, Fan He, Junhua Li, Liu Liu, Shuwang Ge, Xianjun Ke, Zhibin Zhou, Gang Xu, Ming-hui Zhao, Haibo Wang, Luxia Zhang, Erdan Dong. Renin--angiotensin system inhibitor is associated with the reduced risk of all-cause mortality in COVID-19 among patients with/without hypertension[J]. Front. Med., 2022, 16(1): 102-110.
[13]	Jing Wang, Zequn Lu, Meng Jin, Ying Wang, Kunming Tian, Jun Xiao, Yimin Cai, Yanan Wang, Xu Zhang, Tao Chen, Zhi Yao, Chunguang Yang, Renli Deng, Qiang Zhong, Xiongbo Deng, Xin Chen, Xiang-ping Yang, Gonghong Wei, Zhihua Wang, Jianbo Tian, Xiao-ping Chen. Clinical characteristics and risk factors of COVID-19 patients with chronic hepatitis B: a multi-center retrospective cohort study[J]. Front. Med., 2022, 16(1): 111-125.
[14]	Li Ni, Zheng Wen, Xiaowen Hu, Wei Tang, Haisheng Wang, Ling Zhou, Lujin Wu, Hong Wang, Chang Xu, Xizhen Xu, Zhichao Xiao, Zongzhe Li, Chene Li, Yujian Liu, Jialin Duan, Chen Chen, Dan Li, Runhua Zhang, Jinliang Li, Yongxiang Yi, Wei Huang, Yanyan Chen, Jianping Zhao, Jianping Zuo, Jianping Weng, Hualiang Jiang, Dao Wen Wang. Effects of Shuanghuanglian oral liquids on patients with COVID-19: a randomized, open-label, parallel-controlled, multicenter clinical trial[J]. Front. Med., 2021, 15(5): 704-717.
[15]	Weijian Hang, Chen Chen, Xin A. Zhang, Dao Wen Wang. Endothelial dysfunction in COVID-19 calls for immediate attention: the emerging roles of the endothelium in inflammation caused by SARS-CoV-2[J]. Front. Med., 2021, 15(4): 638-643.

Viewed

Full text

Abstract

Cited

Shared

Discussed