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

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

References

[1] AndersonML, DobkinC, GorryD. Effect of influenza vaccination for the elderly on hospitalization and mortality. Ann Intern Med 2020; 173( 4): 322– 323

[2] XuC, Liu L, RenB, DongL, ZouS, Huang W, WeiH, ChengY, TangJ, GaoR, Feng L, ZhangR, YuanC, WangD, ChenJ. 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

[3] TamYH, ValkenburgSA, PereraRAPM, WongJHF, FangVJ, NgTWY, KwongASK, TsuiWWS, IpDKM, PoonLLM, ChauCKV, BarrIG, PeirisJSM, CowlingBJ. Immune responses to twice-annual influenza vaccination in older adults in Hong Kong. Clin Infect Dis 2018; 66( 6): 904– 912

[4] ShuLM, ZhangJ, HuoX, Chen C, FangSS, ZongKX, GuoYY, ZhaoYZ, ZhangJ, BaoCJ, XiaJJ, ZhuFC, WangDY, WuGZ, Gao F, LiuJ. 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

[5] ZhuH, Lee ACY, LiC, MakWWN, ChenYY, ChanKH, ZhangAJX, FungWF, ZhangRQ, FungYF, PoonRWS, LamJY, TamS, Hung IFN, ChenH, YuenKY, ToKKW. 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

[6] NationalHealth Commission of the People’s Republic of China. 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] FengS, ShenC, XiaN, Song W, FanM, CowlingBJ. Rational use of face masks in the COVID-19 pandemic. Lancet Respir Med 2020; 8( 5): 434– 436

[8] PratherKA, WangCC, SchooleyRT. Reducing transmission of SARS-CoV-2. Science 2020; 368( 6498): 1422– 1424

[9] LeungNHL, ChuDKW, ShiuEYC, ChanKH, McDevittJJ, HauBJP, YenHL, LiY, Ip DKM, PeirisJSM, SetoWH, LeungGM, MiltonDK, CowlingBJ. Respiratory virus shedding in exhaled breath and efficacy of face masks. Nat Med 2020; 26( 5): 676– 680

[10] HanS, Zhang T, LyuY, LaiS, Dai P, ZhengJ, YangW, ZhouX, FengL. The incoming influenza season — China, the United Kingdom, and the United States, 2021–2022. China CDC Wkly 2021; 3( 49): 1039– 1045

[11] WorldHealth Organization. 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] ZhangAJ, LeeACY, ChanJFW, LiuF, Li C, ChenY, ChuH, Lau SY, WangP, ChanCCS, PoonVKM, YuanS, ToKKW, ChenH, YuenKY. 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

[13] BaiL, Zhao Y, DongJ, LiangS, GuoM, Liu X, WangX, HuangZ, SunX, Zhang Z, DongL, LiuQ, Zheng Y, NiuD, XiangM, SongK, YeJ, Zheng W, TangZ, TangM, ZhouY, ShenC, DaiM, Zhou L, ChenY, YanH, Lan K, XuK. Coinfection with influenza A virus enhances SARS-CoV-2 infectivity. Cell Res 2021; 31( 4): 395– 403

[14] Cuadrado-PayánE, Montagud-MarrahiE, Torres-ElorzaM, BodroM, BlascoM, PochE, SorianoA, PiñeiroGJ. SARS-CoV-2 and influenza virus co-infection. Lancet 2020; 395( 10236): e84

[15] YangJ, AtkinsKE, FengL, PangM, ZhengY, LiuX, Cowling BJ, YuH. Seasonal influenza vaccination in China: landscape of diverse regional reimbursement policy, and budget impact analysis. Vaccine 2016; 34( 47): 5724– 5735

[16] HaywardAC, FragaszyEB, BerminghamA, WangL, CopasA, EdmundsWJ, FergusonN, GoonetillekeN, HarveyG, KovarJ, LimMSC, McMichaelA, MillettERC, Nguyen-Van-TamJS, NazarethI, PebodyR, TabassumF, WatsonJM, WurieFB, JohnsonAM, ZambonM; Flu Watch Group. 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

[17] MaM, Anderson BD, WangT, ChenY, ZhangD, GrayGC, LuJ. Serological evidence and risk factors for swine influenza infections among Chinese swine workers in Guangdong Province. PLoS One 2015; 10( 5): e0128479

[18] NgTWY, PereraRAPM, FangVJ, YauEM, PeirisJSM, TamYH, CowlingBJ. 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

[19] GaoD, Yang H, DengB, YinG, Song W, ZhangH, LiY. Safety and immunogenicity of 3 seasonal trivalent influenza vaccines in the Chinese military. Hum Vaccin Immunother 2016; 12( 10): 2634– 2639

[20] WangSY, LiuSZ, ChuK, Zhao Y, ZhuFC, HuYM, Meng FY, LiJX, LuoL, Yang JY, LiuP, YuJ. 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

[21] ChenJ, MaJ, White SK, CaoZ, ZhenY, HeS, Zhu W, KeC, ZhangY, SuS, Zhang G. Live poultry market workers are susceptible to both avian and swine influenza viruses, Guangdong Province, China. Vet Microbiol 2015; 181( 3–4): 230– 235

[22] WangJR, GuanWD, YauLF, GaoWN, ZhanYQ, LiuL, Yang ZF, JiangZH. Glycomic signatures on serum IgGs for prediction of postvaccination response. Sci Rep 2015; 5( 1): 7648

[23] QuanC, WangQ, ZhangJ, ZhaoM, DaiQ, Huang T, ZhangZ, MaoS, Nie Y, LiuJ, XieY, Zhang B, BiY, ShiW, Liu P, WangD, FengL, YuH, Liu WJ, GaoGF. Avian influenza A viruses among occupationally exposed populations, China, 2014–2016. Emerg Infect Dis 2019; 25( 12): 2215– 2225

[24] WuJ, Yi L, NiH, ZouL, Zhang H, ZengX, LiangL, LiL, Zhong H, ZhangX, LinJY, KeC. Anti-human H1N1pdm09 and swine H1N1 virus antibodies among swine workers in Guangdong Province, China. Sci Rep 2015; 5( 1): 12507

[25] ChineseNational Influenza Center. Chinese influenza weekly report. 2021. Available at the website of Chinese National Influenza Center (accessed December 28, 2021)

[26] Universityof Oxford. Coronavirus (COVID-19) vaccinations. 2021. Available at the ourworldindata website (accessed December 28, 2021)

[27] WorldHealth Organization. Global circulation of influenza viruses. 2021. Available at the website of World Health Organization (accessed December 28, 2021)

Acknowledgements

We thank the participants of this study, as well as the staff of the Second Affiliated Hospital of Shandong First Medical University and Boshan District Hospital who made the survey possible. We thank the help from Ti Liu and Julong Wu in Shandong Center for Disease Control and Prevention. This work was supported by the Academic Promotion Programme of Shandong First Medical University (No. 2019QL006) and the Natural Science Foundation of Shandong Province (Nos. ZR2020QH133, ZR2020MH339, and ZR2021MC001).

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11684-022-0930-5 and is accessible for authorized users.

Compliance with ethics guidelines

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, and Weifeng Shi declare that they have no actual or potential competing financial interests. This study was approved by the Ethics Committee of Shandong First Medical University & Shandong Academy of Medical Sciences (approved No. R202105170154). The study conformed to the principles of the Declaration of Helsinki, and the standards of Good Clinical Practice defined by the International Conference on Harmonization. Written informed consent was obtained from all adult participants, and from legal guardians for participants ≤ 15 years old.

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