1887
  1. Home
  2. Eurosurveillance
  3. Volume 28, Issue 41, 12/Oct/2023
  4. Article
Surveillance Open Access
Like 0
Download

Abstract

Background

Two human cases of avian influenza A (H3N8) virus infection were reported in China in 2022.

Aim

To characterise H3N8 viruses circulating in China in September 2021−May 2022.

Methods

We sampled poultry and poultry-related environments in 25 Chinese provinces. After isolating H3N8 viruses, whole genome sequences were obtained for molecular and phylogenetic analyses. The specificity of H3N8 viruses towards human or avian receptors was assessed in vitro. Their ability to replicate in chicken and mice, and to transmit between guinea pigs was also investigated.

Results

In total, 98 H3N8 avian influenza virus isolates were retrieved from 38,639 samples; genetic analysis of 31 representative isolates revealed 17 genotypes. Viruses belonging to 10 of these genotypes had six internal genes originating from influenza A (H9N2) viruses. These reassorted viruses could be found in live poultry markets and comprised the strains responsible for the two human infections. A subset of nine H3N8 viruses (including six reassorted) that replicated efficiently in mice bound to both avian-type and human-type receptors in vitro. Three reassorted viruses were shed by chickens for up to 9 days, replicating efficiently in their upper respiratory tract. Five reassorted viruses tested on guinea pigs were transmissible among these by respiratory droplets.

Conclusion

Avian H3N8 viruses with H9N2 virus internal genes, causing two human infections, occurred in live poultry markets in China. The low pathogenicity of H3N8 viruses in poultry allows their continuous circulation with potential for reassortment. Careful monitoring of spill-over infections in humans is important to strengthen early-warning systems and maintain influenza pandemic preparedness.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2023.28.41.2200871
2023-10-12
2024-12-23
/content/10.2807/1560-7917.ES.2023.28.41.2200871
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/28/41/eurosurv-28-41-2.html?itemId=/content/10.2807/1560-7917.ES.2023.28.41.2200871&mimeType=html&fmt=ahah

References

  1. Wille M, Holmes EC. The Ecology and Evolution of Influenza Viruses. Cold Spring Harb Perspect Med. 2020;10(7):a038489.  https://doi.org/10.1101/cshperspect.a038489  PMID: 31871237 
  2. Lee DH, Criado MF, Swayne DE. Pathobiological Origins and Evolutionary History of Highly Pathogenic Avian Influenza Viruses. Cold Spring Harb Perspect Med. 2021;11(2):a038679.  https://doi.org/10.1101/cshperspect.a038679  PMID: 31964650 
  3. Wang D, Zhu W, Yang L, Shu Y. The Epidemiology, Virology, and Pathogenicity of Human Infections with Avian Influenza Viruses. Cold Spring Harb Perspect Med. 2021;11(4):a038620.  https://doi.org/10.1101/cshperspect.a038620  PMID: 31964651 
  4. Cui P, Zeng X, Li X, Li Y, Shi J, Zhao C, et al. Genetic and biological characteristics of the globally circulating H5N8 avian influenza viruses and the protective efficacy offered by the poultry vaccine currently used in China. Sci China Life Sci. 2022;65(4):795-808.  https://doi.org/10.1007/s11427-021-2025-y  PMID: 34757542 
  5. Cui P, Shi J, Wang C, Zhang Y, Xing X, Kong H, et al. Global dissemination of H5N1 influenza viruses bearing the clade 2.3.4.4b HA gene and biologic analysis of the ones detected in China. Emerg Microbes Infect. 2022;11(1):1693-704.  https://doi.org/10.1080/22221751.2022.2088407  PMID: 35699072 
  6. Gu W, Shi J, Cui P, Yan C, Zhang Y, Wang C, et al. Novel H5N6 reassortants bearing the clade 2.3.4.4b HA gene of H5N8 virus have been detected in poultry and caused multiple human infections in China. Emerg Microbes Infect. 2022;11(1):1174-85.  https://doi.org/10.1080/22221751.2022.2063076  PMID: 35380505 
  7. Zeng X, Tian G, Shi J, Deng G, Li C, Chen H. Vaccination of poultry successfully eliminated human infection with H7N9 virus in China. Sci China Life Sci. 2018;61(12):1465-73.  https://doi.org/10.1007/s11427-018-9420-1  PMID: 30414008 
  8. Yuan J, Zhang L, Kan X, Jiang L, Yang J, Guo Z, et al. Origin and molecular characteristics of a novel 2013 avian influenza A(H6N1) virus causing human infection in Taiwan. Clin Infect Dis. 2013;57(9):1367-8.  https://doi.org/10.1093/cid/cit479  PMID: 23881153 
  9. Qi X, Qiu H, Hao S, Zhu F, Huang Y, Xu K, et al. Human Infection with an Avian-Origin Influenza A (H10N3) Virus. N Engl J Med. 2022;386(11):1087-8.  https://doi.org/10.1056/NEJMc2112416  PMID: 35294820 
  10. Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, et al. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet. 2014;383(9918):714-21.  https://doi.org/10.1016/S0140-6736(14)60111-2  PMID: 24507376 
  11. Cheng D, Dong Y, Wen S, Shi C. A child with acute respiratory distress syndrome caused by avian influenza H3N8 virus. J Infect. 2022;85(2):174-211.  https://doi.org/10.1016/j.jinf.2022.05.007  PMID: 35577072 
  12. Tan X, Yan X, Liu Y, Wu Y, Liu J, Mu M, et al. A case of human infection by H3N8 influenza virus. Emerg Microbes Infect. 2022;11(1):2214-7.  https://doi.org/10.1080/22221751.2022.2117097  PMID: 36000153 
  13. Zhang Y, Zhao C, Hou Y, Chen Y, Meng F, Zhuang Y, et al. Pandemic threat posed by H3N2 avian influenza virus. Sci China Life Sci. 2021;64(11):1984-7.  https://doi.org/10.1007/s11427-021-1916-4  PMID: 33765225 
  14. Ma S, Zhang B, Shi J, Yin X, Wang G, Cui P, et al. Amino Acid Mutations A286V and T437M in the Nucleoprotein Attenuate H7N9 Viruses in Mice. J Virol. 2020;94(2):e01530-19.  https://doi.org/10.1128/JVI.01530-19  PMID: 31666373 
  15. Kong X, Guan L, Shi J, Kong H, Zhang Y, Zeng X, et al. A single-amino-acid mutation at position 225 in hemagglutinin attenuates H5N6 influenza virus in mice. Emerg Microbes Infect. 2021;10(1):2052-61.  https://doi.org/10.1080/22221751.2021.1997340  PMID: 34686117 
  16. Li X, Shi J, Guo J, Deng G, Zhang Q, Wang J, et al. Genetics, receptor binding property, and transmissibility in mammals of naturally isolated H9N2 Avian Influenza viruses. PLoS Pathog. 2014;10(11):e1004508.  https://doi.org/10.1371/journal.ppat.1004508  PMID: 25411973 
  17. Feng X, Wang Z, Shi J, Deng G, Kong H, Tao S, et al. Glycine at Position 622 in PB1 Contributes to the Virulence of H5N1 Avian Influenza Virus in Mice. J Virol. 2016;90(4):1872-9.  https://doi.org/10.1128/JVI.02387-15  PMID: 26656683 
  18. Fan S, Deng G, Song J, Tian G, Suo Y, Jiang Y, et al. Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. Virology. 2009;384(1):28-32.  https://doi.org/10.1016/j.virol.2008.11.044  PMID: 19117585 
  19. Yang R, Sun H, Gao F, Luo K, Huang Z, Tong Q, et al. Human infection of avian influenza A H3N8 virus and the viral origins: a descriptive study. Lancet Microbe. 2022;3(11):e824-34.  https://doi.org/10.1016/S2666-5247(22)00192-6  PMID: 36115379 
  20. Wan Z, Jiang W, Gong J, Zhao Z, Tang T, Li Y, et al. Emergence of chicken infection with novel reassortant H3N8 avian influenza viruses genetically close to human H3N8 isolate, China. Emerg Microbes Infect. 2022;11(1):2553-5.  https://doi.org/10.1080/22221751.2022.2128437  PMID: 36150006 
  21. Deng G, Tan D, Shi J, Cui P, Jiang Y, Liu L, et al. Complex reassortment of multiple subtypes of avian influenza viruses in domestic ducks at the Dongting Lake Region of China. J Virol. 2013;87(17):9452-62.  https://doi.org/10.1128/JVI.00776-13  PMID: 23804642 
  22. Yang H, Xiao Y, Meng F, Sun F, Chen M, Cheng Z, et al. Emergence of H3N8 equine influenza virus in donkeys in China in 2017. Vet Microbiol. 2018;214:1-6.  https://doi.org/10.1016/j.vetmic.2017.11.033  PMID: 29408020 
  23. Anthony SJ, St Leger JA, Pugliares K, Ip HS, Chan JM, Carpenter ZW, et al. Emergence of fatal avian influenza in New England harbor seals. mBio. 2012;3(4):e00166-12.  https://doi.org/10.1128/mBio.00166-12  PMID: 22851656 
  24. Li Y, Li P, Xi J, Yang J, Wu H, Zhang Y, et al. Wild bird-origin H3N8 avian influenza virus exhibit well adaptation in mammalian host. J Infect. 2022;84(4):579-613.  https://doi.org/10.1016/j.jinf.2021.12.014  PMID: 34953909 
  25. Crawford PC, Dubovi EJ, Castleman WL, Stephenson I, Gibbs EP, Chen L, et al. Transmission of equine influenza virus to dogs. Science. 2005;310(5747):482-5.  https://doi.org/10.1126/science.1117950  PMID: 16186182 
  26. Li M, Yin X, Guan L, Zhang X, Deng G, Li T, et al. Insights from avian influenza surveillance of chickens and ducks before and after exposure to live poultry markets. Sci China Life Sci. 2019;62(6):854-7.  https://doi.org/10.1007/s11427-019-9522-7  PMID: 30977013 
  27. Zhang Q, Shi J, Deng G, Guo J, Zeng X, He X, et al. H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science. 2013;341(6144):410-4.  https://doi.org/10.1126/science.1240532  PMID: 23868922 
  28. Shi J, Deng G, Kong H, Gu C, Ma S, Yin X, et al. H7N9 virulent mutants detected in chickens in China pose an increased threat to humans. Cell Res. 2017;27(12):1409-21.  https://doi.org/10.1038/cr.2017.129  PMID: 29151586 
  29. Liang L, Jiang L, Li J, Zhao Q, Wang J, He X, et al. Low Polymerase Activity Attributed to PA Drives the Acquisition of the PB2 E627K Mutation of H7N9 Avian Influenza Virus in Mammals. mBio. 2019;10(3):e01162-19.  https://doi.org/10.1128/mBio.01162-19  PMID: 31213560 
  30. Liu K, Ding P, Pei Y, Gao R, Han W, Zheng H, et al. Emergence of a novel reassortant avian influenza virus (H10N3) in Eastern China with high pathogenicity and respiratory droplet transmissibility to mammals. Sci China Life Sci. 2022;65(5):1024-35.  https://doi.org/10.1007/s11427-020-1981-5  PMID: 34542812 
  31. Taft AS, Ozawa M, Fitch A, Depasse JV, Halfmann PJ, Hill-Batorski L, et al. Identification of mammalian-adapting mutations in the polymerase complex of an avian H5N1 influenza virus. Nat Commun. 2015;6(1):7491.  https://doi.org/10.1038/ncomms8491  PMID: 26082035 
Analysis of avian influenza A (H3N8) viruses in poultry and their zoonotic potential, China, September 2021 to May 2022
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Pengfei+Cui&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cui Pengfei</a>, <a href="/search?value1=Jianzhong+Shi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Shi Jianzhong</a>, <a href="/search?value1=Cheng+Yan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Yan Cheng</a>, <a href="/search?value1=Congcong+Wang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wang Congcong</a>, <a href="/search?value1=Yuancheng+Zhang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zhang Yuancheng</a>, <a href="/search?value1=Yaping+Zhang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zhang Yaping</a>, <a href="/search?value1=Xin+Xing&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Xing Xin</a>, <a href="/search?value1=Yuan+Chen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chen Yuan</a>, <a href="/search?value1=Jie+Zhang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zhang Jie</a>, <a href="/search?value1=Liling+Liu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Liu Liling</a>, <a href="/search?value1=Xianying+Zeng&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zeng Xianying</a>, <a href="/search?value1=Guobin+Tian&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tian Guobin</a>, <a href="/search?value1=Chengjun+Li&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Li Chengjun</a>, <a href="/search?value1=Yasuo+Suzuki&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Suzuki Yasuo</a>, <a href="/search?value1=Guohua+Deng&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Deng Guohua</a>, <a href="/search?value1=Hualan+Chen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chen Hualan</a></span>. Analysis of avian influenza A (H3N8) viruses in poultry and their zoonotic potential, China, September 2021 to May 2022. <a href="/content/ecdc">Euro Surveill.</a> 2023;28(41):pii=2200871. <a href="https://doi.org/10.2807/1560-7917.ES.2023.28.41.2200871" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2023.28.41.2200871</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 09 Nov 2022;&nbsp;&nbsp; <span class="generated">Accepted</span>: 14 Apr 2023 </span> </p>
/content/10.2807/1560-7917.ES.2023.28.41.2200871
/content/10.2807/1560-7917.ES.2023.28.41.2200871
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error