Seroprevalence of influenza viruses in Shandong, Northern China during the COVID-19 pandemic

doi:10.1007/s11684-022-0930-5

Front. Med.

2022, Vol. 16

Issue (6) : 984-990 https://doi.org/10.1007/s11684-022-0930-5

LETTER TO FRONTIERS OF MEDICINE

Seroprevalence of influenza viruses in Shandong, Northern China during the COVID-19 pandemic

Chuansong Quan¹, Zhenjie Zhang¹, Guoyong Ding², Fengwei Sun³, Hengxia Zhao⁴, Qinghua Liu⁵, Chuanmin Ma¹, Jing Wang¹, Liang Wang¹, Wenbo Zhao¹, Jinjie He⁴, Yu Wang⁶, Qian He², Michael J. Carr^7,⁸, Dayan Wang⁹, Qiang Xiao⁵(

), Weifeng Shi^1,²(

)

¹. Key Laboratory of Etiology and Epidemiology of Emerging Infectious Diseases in Universities of Shandong, Shandong First Medical University & Shandong Academy of Medical Sciences, Taian 271000, China
². School of Public Health, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan 250117, China
³. The Department of Infectious Disease, The Second Affiliated Hospital of Shandong First Medical University, Taian 271000, China
⁴. Clinical Laboratory, The Department of Clinical Laboratory, Boshan District Hospital, Zibo 255200, China
⁵. Clinical Laboratory, The Department of Clinical Laboratory, The Second Affiliated Hospital of Shandong First Medical University, Taian 271000, China
⁶. The Department of Cancer Center, Taian Tumor Prevention and Treatment Hospital, Taian 271000, China
⁷. National Virus Reference Laboratory, School of Medicine, University College Dublin, Dublin 4, Ireland
⁸. International Collaboration Unit, International Institute for Zoonosis Control, Hokkaido University, Sapporo, Hokkaido, 001-0020, Japan
⁹. Chinese National Influenza Center, National Institute for Viral Disease Control and Prevention, Collaboration Innovation Center for Diagnosis and Treatment of Infectious Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory for Medical Virology, National Health and Family Planning Commission, Beijing 102206, China

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Abstract

Nonpharmaceutical interventions (NPIs) have been commonly deployed to prevent and control the spread of the coronavirus disease 2019 (COVID-19), resulting in a worldwide decline in influenza prevalence. However, the influenza risk in China warrants cautious assessment. We conducted a cross-sectional, sero-epidemiological study in Shandong Province, Northern China in mid-2021. Hemagglutination inhibition was performed to test antibodies against four influenza vaccine strains. A combination of descriptive and meta-analyses was adopted to compare the seroprevalence of influenza antibodies before and during the COVID-19 pandemic. The overall seroprevalence values against A/H1N1pdm09, A/H3N2, B/Victoria, and B/Yamagata were 17.8% (95% CI 16.2%–19.5%), 23.5% (95% CI 21.7%–25.4%), 7.6% (95% CI 6.6%–8.7%), and 15.0 (95% CI 13.5%–16.5%), respectively, in the study period. The overall vaccination rate was extremely low (2.6%). Our results revealed that antibody titers in vaccinated participants were significantly higher than those in unvaccinated individuals (P < 0.001). Notably, the meta-analysis showed that antibodies against A/H1N1pdm09 and A/H3N2 were significantly low in adults after the COVID-19 pandemic ( P < 0.01). Increasing vaccination rates and maintaining NPIs are recommended to prevent an elevated influenza risk in China.

Keywords influenza virus seroprevalence antibody COVID-19 cross-sectional study

Corresponding Author(s): Qiang Xiao,Weifeng Shi

Just Accepted Date: 29 July 2022 Online First Date: 22 September 2022 Issue Date: 16 January 2023

Cite this article:

Chuansong Quan,Zhenjie Zhang,Guoyong Ding, et al. Seroprevalence of influenza viruses in Shandong, Northern China during the COVID-19 pandemic[J]. Front. Med., 2022, 16(6): 984-990.

URL:

https://academic.hep.com.cn/fmd/EN/10.1007/s11684-022-0930-5
https://academic.hep.com.cn/fmd/EN/Y2022/V16/I6/984

Fig.1 Inclusion criteria of participants and studies in the meta-analysis. (A) Participant selection. Light gold color represents urban communities, and light green color represents rural communities. (B) Study selection in the meta-analysis. *(1)–(5) represent the inclusion criteria for the literature screening in the meta-analysis, which have been described in the supplementary materials and methods.

Tab.1 Demographic characteristics of the study participants

Tab.2 Seroprevalence of antibodies against the four influenza strains in Shandong Province

Fig.2 Subgroup analysis of the seroprevalence of influenza antibodies between the relevant literature and our study: (A) A/H1N1pdm09, (B) A/H3N2, (C) B/Victoria, and (D) B/Yamagata.

1	ML Anderson, C Dobkin, D Gorry. Effect of influenza vaccination for the elderly on hospitalization and mortality. Ann Intern Med 2020; 173( 4): 322– 323 https://doi.org/10.7326/L20-0829 pmid: 32805160
2	C Xu, L Liu, B Ren, L Dong, S Zou, W Huang, H Wei, Y Cheng, J Tang, R Gao, L Feng, R Zhang, C Yuan, D Wang, J Chen. Incidence of influenza virus infections confirmed by serology in children and adult in a suburb community, northern China, 2018–2019 influenza season. Influenza Other Respir Viruses 2021; 15( 2): 262– 269 https://doi.org/10.1111/irv.12805 pmid: 32978902
3	YH Tam, SA Valkenburg, RAPM Perera, JHF Wong, VJ Fang, TWY Ng, ASK Kwong, WWS Tsui, DKM Ip, LLM Poon, CKV Chau, IG Barr, JSM Peiris, BJ Cowling. Immune responses to twice-annual influenza vaccination in older adults in Hong Kong. Clin Infect Dis 2018; 66( 6): 904– 912 https://doi.org/10.1093/cid/cix900 pmid: 29069368
4	LM Shu, J Zhang, X Huo, C Chen, SS Fang, KX Zong, YY Guo, YZ Zhao, J Zhang, CJ Bao, JJ Xia, FC Zhu, DY Wang, GZ Wu, F Gao, J Liu. Preplanned studies: surveillance on the immune effectiveness of quadrivalent and trivalent split influenza vaccines — Shenzhen City and Changzhou City, China, 2018–2019. China CDC Wkly 2020; 2( 21): 370– 375 https://doi.org/10.46234/ccdcw2020.095 pmid: 34594663
5	H Zhu, ACY Lee, C Li, WWN Mak, YY Chen, KH Chan, AJX Zhang, WF Fung, RQ Zhang, YF Fung, RWS Poon, JY Lam, S Tam, IFN Hung, H Chen, KY Yuen, KKW To. Low population serum microneutralization antibody titer against the predominating influenza A(H3N2) N121K virus during the severe influenza summer peak of Hong Kong in 2017. Emerg Microbes Infect 2018; 7( 1): 23 https://doi.org/10.1038/s41426-018-0041-1 pmid: 29511175
6	Health Commission of the People’s Republic of China National. Overview of the national epidemic of statutory infectious diseases. 2019. Available at the website of National Health Commission of the People’s Republic of China (accessed December 28, 2021)
7	S Feng, C Shen, N Xia, W Song, M Fan, BJ Cowling. Rational use of face masks in the COVID-19 pandemic. Lancet Respir Med 2020; 8( 5): 434– 436 https://doi.org/10.1016/S2213-2600(20)30134-X pmid: 32203710
8	KA Prather, CC Wang, RT Schooley. Reducing transmission of SARS-CoV-2. Science 2020; 368( 6498): 1422– 1424 https://doi.org/10.1126/science.abc6197 pmid: 32461212
9	NHL Leung, DKW Chu, EYC Shiu, KH Chan, JJ McDevitt, BJP Hau, HL Yen, Y Li, DKM Ip, JSM Peiris, WH Seto, GM Leung, DK Milton, BJ Cowling. Respiratory virus shedding in exhaled breath and efficacy of face masks. Nat Med 2020; 26( 5): 676– 680 https://doi.org/10.1038/s41591-020-0843-2 pmid: 32371934
10	S Han, T Zhang, Y Lyu, S Lai, P Dai, J Zheng, W Yang, X Zhou, L Feng. The incoming influenza season — China, the United Kingdom, and the United States, 2021–2022. China CDC Wkly 2021; 3( 49): 1039– 1045 https://doi.org/10.46234/ccdcw2021.253 pmid: 34934512
11	Health Organization World. Review of global influenza circulation, late 2019 to 2020, and the impact of the COVID-19 pandemic on influenza circulation. 2021. Available at the website of World Health Organization (accessed December 28, 2021)
12	AJ Zhang, ACY Lee, JFW Chan, F Liu, C Li, Y Chen, H Chu, SY Lau, P Wang, CCS Chan, VKM Poon, S Yuan, KKW To, H Chen, KY Yuen. Coinfection by severe acute respiratory syndrome coronavirus 2 and influenza A(H1N1)pdm09 virus enhances the severity of pneumonia in golden syrian hamsters. Clin Infect Dis 2021; 72( 12): e978– e992 https://doi.org/10.1093/cid/ciaa1747 pmid: 33216851
13	L Bai, Y Zhao, J Dong, S Liang, M Guo, X Liu, X Wang, Z Huang, X Sun, Z Zhang, L Dong, Q Liu, Y Zheng, D Niu, M Xiang, K Song, J Ye, W Zheng, Z Tang, M Tang, Y Zhou, C Shen, M Dai, L Zhou, Y Chen, H Yan, K Lan, K Xu. Coinfection with influenza A virus enhances SARS-CoV-2 infectivity. Cell Res 2021; 31( 4): 395– 403 https://doi.org/10.1038/s41422-021-00473-1 pmid: 33603116
14	E Cuadrado-Payán, E Montagud-Marrahi, M Torres-Elorza, M Bodro, M Blasco, E Poch, A Soriano, GJ Piñeiro. SARS-CoV-2 and influenza virus co-infection. Lancet 2020; 395( 10236): e84 https://doi.org/10.1016/S0140-6736(20)31052-7 pmid: 32423586
15	J Yang, KE Atkins, L Feng, M Pang, Y Zheng, X Liu, BJ Cowling, H Yu. Seasonal influenza vaccination in China: landscape of diverse regional reimbursement policy, and budget impact analysis. Vaccine 2016; 34( 47): 5724– 5735 https://doi.org/10.1016/j.vaccine.2016.10.013 pmid: 27745951
16	AC Hayward, EB Fragaszy, A Bermingham, L Wang, A Copas, WJ Edmunds, N Ferguson, N Goonetilleke, G Harvey, J Kovar, MSC Lim, A McMichael, ERC Millett, JS Nguyen-Van-Tam, I Nazareth, R Pebody, F Tabassum, JM Watson, FB Wurie, AM Johnson, M; Flu Watch Group Zambon. Comparative community burden and severity of seasonal and pandemic influenza: results of the Flu Watch cohort study. Lancet Respir Med 2014; 2( 6): 445– 454 https://doi.org/10.1016/S2213-2600(14)70034-7 pmid: 24717637
17	M Ma, BD Anderson, T Wang, Y Chen, D Zhang, GC Gray, J Lu. Serological evidence and risk factors for swine influenza infections among Chinese swine workers in Guangdong Province. PLoS One 2015; 10( 5): e0128479 https://doi.org/10.1371/journal.pone.0128479 pmid: 26016740
18	TWY Ng, RAPM Perera, VJ Fang, EM Yau, JSM Peiris, YH Tam, BJ Cowling. The effect of influenza vaccination history on changes in hemagglutination inhibition titers after receipt of the 2015–2016 influenza vaccine in older adults in Hong Kong. J Infect Dis 2020; 221( 1): 33– 41 https://doi.org/10.1093/infdis/jiz327 pmid: 31282541
19	D Gao, H Yang, B Deng, G Yin, W Song, H Zhang, Y Li. Safety and immunogenicity of 3 seasonal trivalent influenza vaccines in the Chinese military. Hum Vaccin Immunother 2016; 12( 10): 2634– 2639 https://doi.org/10.1080/21645515.2016.1194147 pmid: 27348250
20	SY Wang, SZ Liu, K Chu, Y Zhao, FC Zhu, YM Hu, FY Meng, JX Li, L Luo, JY Yang, P Liu, J Yu. Immunogenicity and safety of an inactivated quadrivalent influenza vaccine candidate versus inactivated trivalent influenza vaccines in participants >/=3 years of age: a double-blind, randomized, parallel-controlled phase III clinical trial in China. Expert Rev Vaccines 2017; 16( 11): 1155– 1169 https://doi.org/10.1080/14760584.2017.1374181 pmid: 28870140
21	J Chen, J Ma, SK White, Z Cao, Y Zhen, S He, W Zhu, C Ke, Y Zhang, S Su, G Zhang. Live poultry market workers are susceptible to both avian and swine influenza viruses, Guangdong Province, China. Vet Microbiol 2015; 181( 3–4): 230– 235 https://doi.org/10.1016/j.vetmic.2015.09.016 pmid: 26476563
22	JR Wang, WD Guan, LF Yau, WN Gao, YQ Zhan, L Liu, ZF Yang, ZH Jiang. Glycomic signatures on serum IgGs for prediction of postvaccination response. Sci Rep 2015; 5( 1): 7648 https://doi.org/10.1038/srep07648 pmid: 25612906
23	C Quan, Q Wang, J Zhang, M Zhao, Q Dai, T Huang, Z Zhang, S Mao, Y Nie, J Liu, Y Xie, B Zhang, Y Bi, W Shi, P Liu, D Wang, L Feng, H Yu, WJ Liu, GF Gao. Avian influenza A viruses among occupationally exposed populations, China, 2014–2016. Emerg Infect Dis 2019; 25( 12): 2215– 2225 https://doi.org/10.3201/eid2512.190261 pmid: 31742536
24	J Wu, L Yi, H Ni, L Zou, H Zhang, X Zeng, L Liang, L Li, H Zhong, X Zhang, JY Lin, C Ke. Anti-human H1N1pdm09 and swine H1N1 virus antibodies among swine workers in Guangdong Province, China. Sci Rep 2015; 5( 1): 12507 https://doi.org/10.1038/srep12507 pmid: 26205221
25	National Influenza Center Chinese. Chinese influenza weekly report. 2021. Available at the website of Chinese National Influenza Center (accessed December 28, 2021)
26	of Oxford University. Coronavirus (COVID-19) vaccinations. 2021. Available at the ourworldindata website (accessed December 28, 2021)
27	Health Organization World. Global circulation of influenza viruses. 2021. Available at the website of World Health Organization (accessed December 28, 2021)

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