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
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.
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)
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)