Prevalence of Influenza B/Yamagata Viruses From Season 2012/2013 to 2021/2022 in Italy As an Indication of a Potential Lineage Extinction

Overview

Journal Influenza Other Respir Viruses

Publisher Wiley

Specialty Microbiology

Date 2024 Sep 11

PMID 39257041

Authors

Serena Marchi

Marco Bruttini

Giovanna Milano

Ilaria Manini

Maria Chironna

Elena Pariani

Alessandro Manenti

Otfried Kistner

Emanuele Montomoli

Nigel Temperton

Claudia Maria Trombetta

Affiliations

Soon will be listed here.

Abstract

Background: Influenza B/Yamagata viruses exhibited weak antigenic selection in recent years, reducing their prevalence over time and requiring no update of the vaccine component since 2015. To date, no B/Yamagata viruses have been isolated or sequenced since March 2020.

Methods: The antibody prevalence against the current B/Yamagata vaccine strain in Italy was investigated: For each influenza season from 2012/2013 to 2021/2022, 100 human serum samples were tested by haemagglutination inhibition (HAI) assay against the vaccine strain B/Phuket/3073/2013. In addition, the sequences of 156 B/Yamagata strains isolated during the influenza surveillance activities were selected for analysis of the haemagglutinin genome segment.

Results: About 61.9% of the human samples showed HAI antibodies, and 21.7% had protective antibody levels. The prevalence of antibodies at protective levels in the seasons between the isolation of the strain and its inclusion in the vaccine was between 11% and 25%, with no significant changes observed in subsequent years. A significant increase was observed in the 2020/2021 season, in line with the increase in influenza vaccine uptake during the pandemic. Sequence analysis showed that from 2014/2015 season onward, all B/Yamagata strains circulating in Italy were closely related to the B/Phuket/2013 vaccine strain, showing only limited amino acid variation.

Conclusions: A consistent prevalence of antibodies to the current B/Yamagata vaccine strain in the general population was observed. The prolonged use of a well-matched influenza vaccine and a low antigenic diversity of B/Yamagata viruses may have facilitated a strong reduction in B/Yamagata circulation, potentially contributing to the disappearance of this lineage.

Citing Articles

Post-disappearance scenarios: policy implications following the potential disappearance of B/Yamagata lineage influenza viruses.

Riccio M, Nunes M, Cowling B, Lina B, McCauley J, Meijer A Euro Surveill. 2024; 29(45).

PMID: 39512167 PMC: 11544721. DOI: 10.2807/1560-7917.ES.2024.29.45.2400196.

References

Young B, Sadarangani S, Jiang L, Wilder-Smith A, Chen M . Duration of Influenza Vaccine Effectiveness: A Systematic Review, Meta-analysis, and Meta-regression of Test-Negative Design Case-Control Studies. J Infect Dis. 2017; 217(5):731-741. DOI: 10.1093/infdis/jix632. View

Zheng L, Qi J, Wu J, Zheng M . Changes in Influenza Activity and Circulating Subtypes During the COVID-19 Outbreak in China. Front Med (Lausanne). 2022; 9:829799. PMC: 8980715. DOI: 10.3389/fmed.2022.829799. View

Puzelli S, Di Martino A, Facchini M, Fabiani C, Calzoletti L, Di Mario G . Co-circulation of the two influenza B lineages during 13 consecutive influenza surveillance seasons in Italy, 2004-2017. BMC Infect Dis. 2019; 19(1):990. PMC: 6873537. DOI: 10.1186/s12879-019-4621-z. View

Virk R, Jayakumar J, Mendenhall I, Moorthy M, Lam P, Linster M . Divergent evolutionary trajectories of influenza B viruses underlie their contemporaneous epidemic activity. Proc Natl Acad Sci U S A. 2019; 117(1):619-628. PMC: 6955377. DOI: 10.1073/pnas.1916585116. View

Dudas G, Bedford T, Lycett S, Rambaut A . Reassortment between influenza B lineages and the emergence of a coadapted PB1-PB2-HA gene complex. Mol Biol Evol. 2014; 32(1):162-72. PMC: 4271528. DOI: 10.1093/molbev/msu287. View

Adlhoch C, Snacken R, Melidou A, Ionescu S, Penttinen P . Dominant influenza A(H3N2) and B/Yamagata virus circulation in EU/EEA, 2016/17 and 2017/18 seasons, respectively. Euro Surveill. 2018; 23(13). PMC: 5883452. DOI: 10.2807/1560-7917.ES.2018.23.13.18-00146. View

Rivas M, Alegretti M, Coppola L, Ramas V, Chiparelli H, Goni N . Epidemiology and Genetic Variability of Circulating Influenza B Viruses in Uruguay, 2012-2019. Microorganisms. 2020; 8(4). PMC: 7232498. DOI: 10.3390/microorganisms8040591. View

van de Sandt C, Bodewes R, Rimmelzwaan G, de Vries R . Influenza B viruses: not to be discounted. Future Microbiol. 2015; 10(9):1447-65. DOI: 10.2217/fmb.15.65. View

Skowronski D, Hottes T, De Serres G, Ward B, Janjua N, Sabaiduc S . Influenza Β/Victoria antigen induces strong recall of Β/Yamagata but lower Β/Victoria response in children primed with two doses of Β/Yamagata. Pediatr Infect Dis J. 2011; 30(10):833-9. DOI: 10.1097/INF.0b013e31822db4dc. View

10.

Kissling E, Nunes B, Robertson C, Valenciano M, Reuss A, Larrauri A . I-MOVE multicentre case-control study 2010/11 to 2014/15: Is there within-season waning of influenza type/subtype vaccine effectiveness with increasing time since vaccination?. Euro Surveill. 2016; 21(16). DOI: 10.2807/1560-7917.ES.2016.21.16.30201. View

11.

Trombetta C, Montomoli E . Influenza immunology evaluation and correlates of protection: a focus on vaccines. Expert Rev Vaccines. 2016; 15(8):967-76. DOI: 10.1586/14760584.2016.1164046. View

12.

Koutsakos M, Wheatley A, Laurie K, Kent S, Rockman S . Influenza lineage extinction during the COVID-19 pandemic?. Nat Rev Microbiol. 2021; 19(12):741-742. PMC: 8477979. DOI: 10.1038/s41579-021-00642-4. View

13.

Monto A, Zambon M, Weir J . The End of B/Yamagata Influenza Transmission - Transitioning from Quadrivalent Vaccines. N Engl J Med. 2024; 390(14):1256-1258. DOI: 10.1056/NEJMp2314801. View

14.

Tsuzuki S, Schwehm M, Eichner M . Simulation studies to assess the long-term effects of Japan's change from trivalent to quadrivalent influenza vaccination. Vaccine. 2018; 36(5):624-630. DOI: 10.1016/j.vaccine.2017.12.058. View

15.

Waldock J, Zheng L, Remarque E, Civet A, Hu B, Jalloh S . Assay Harmonization and Use of Biological Standards To Improve the Reproducibility of the Hemagglutination Inhibition Assay: a FLUCOP Collaborative Study. mSphere. 2021; 6(4):e0056721. PMC: 8530177. DOI: 10.1128/mSphere.00567-21. View

16.

Piralla A, Lunghi G, Ruggiero L, Girello A, Bianchini S, Rovida F . Molecular epidemiology of influenza B virus among hospitalized pediatric patients in Northern Italy during the 2015-16 season. PLoS One. 2017; 12(10):e0185893. PMC: 5648122. DOI: 10.1371/journal.pone.0185893. View

17.

Dhanasekaran V, Sullivan S, Edwards K, Xie R, Khvorov A, Valkenburg S . Human seasonal influenza under COVID-19 and the potential consequences of influenza lineage elimination. Nat Commun. 2022; 13(1):1721. PMC: 8971476. DOI: 10.1038/s41467-022-29402-5. View

18.

Skowronski D, Hamelin M, Janjua N, De Serres G, Gardy J, Rheaume C . Cross-lineage influenza B and heterologous influenza A antibody responses in vaccinated mice: immunologic interactions and B/Yamagata dominance. PLoS One. 2012; 7(6):e38929. PMC: 3382187. DOI: 10.1371/journal.pone.0038929. View

19.

Trucchi C, Alicino C, Orsi A, Paganino C, Barberis I, Grammatico F . Fifteen years of epidemiologic, virologic and syndromic influenza surveillance: A focus on type B virus and the effects of vaccine mismatch in Liguria region, Italy. Hum Vaccin Immunother. 2016; 13(2):456-463. PMC: 5328239. DOI: 10.1080/21645515.2017.1264779. View

20.

Skowronski D, Hottes T, Chong M, De Serres G, Scheifele D, Ward B . Randomized controlled trial of dose response to influenza vaccine in children aged 6 to 23 months. Pediatrics. 2011; 128(2):e276-89. DOI: 10.1542/peds.2010-2777. View