Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
권호 표지
DOI QR코드

DOI QR Code

Current situation and control strategies of H9N2 avian influenza in South Korea

  • Mingeun Sagong (Avian Influenza Research & Diagnostic Division, Animal and Plant Quarantine Agency) ;
  • Kwang-Nyeong Lee (Avian Influenza Research & Diagnostic Division, Animal and Plant Quarantine Agency) ;
  • Eun-Kyoung Lee (Avian Influenza Research & Diagnostic Division, Animal and Plant Quarantine Agency) ;
  • Hyunmi Kang (Avian Influenza Research & Diagnostic Division, Animal and Plant Quarantine Agency) ;
  • Young Ki Choi (Department of Microbiology, College of Medicine and Medical Research Institute, Chungbuk National University) ;
  • Youn-Jeong Lee (Avian Influenza Research & Diagnostic Division, Animal and Plant Quarantine Agency)
  • Received : 2022.08.24
  • Accepted : 2022.10.20
  • Published : 2023.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

The H9N2 avian influenza (AI) has become endemic in poultry in many countries since the 1990s, which has caused considerable economic losses in the poultry industry. Considering the long history of the low pathogenicity H9N2 AI in many countries, once H9N2 AI is introduced, it is more difficult to eradicate than high pathogenicity AI. Various preventive measures and strategies, including vaccination and active national surveillance, have been used to control the Y439 lineage of H9N2 AI in South Korea, but it took a long time for the H9N2 virus to disappear from the fields. By contrast, the novel Y280 lineage of H9N2 AI was introduced in June 2020 and has spread nationwide. This study reviews the history, genetic and pathogenic characteristics, and control strategies for Korean H9N2 AI. This review may provide some clues for establishing control strategies for endemic AIV and a newly introduced Y280 lineage of H9N2 AI in South Korea.

Keywords

References

  1. Guan Y, Shortridge KF, Krauss S, Webster RG. Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci U S A. 1999;96(16):9363-9367. https://doi.org/10.1073/pnas.96.16.9363
  2. Guo YJ, Krauss S, Senne DA, Mo IP, Lo KS, Xiong XP, et al. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology. 2000;267(2):279-288. https://doi.org/10.1006/viro.1999.0115
  3. Dong G, Luo J, Zhang H, Wang C, Duan M, Deliberto TJ, et al. Phylogenetic diversity and genotypical complexity of H9N2 influenza A viruses revealed by genomic sequence analysis. PLoS One. 2011;6(2):e17212.
  4. Peacock TH, James J, Sealy JE, Iqbal M. A global perspective on H9N2 avian influenza virus. Viruses. 2019;11(7):620.
  5. Lee YJ, Shin JY, Song MS, Lee YM, Choi JG, Lee EK, et al. Continuing evolution of H9 influenza viruses in Korean poultry. Virology. 2007;359(2):313-323. https://doi.org/10.1016/j.virol.2006.09.025
  6. Lee DH, Song CS. H9N2 avian influenza virus in Korea: evolution and vaccination. Clin Exp Vaccine Res. 2013;2(1):26-33. https://doi.org/10.7774/cevr.2013.2.1.26
  7. Mo IP, Bae YJ, Lee SB, Mo JS, Oh KH, Shin JH, et al. Review of avian influenza outbreaks in South Korea from 1996 to 2014. Avian Dis. 2016;60(1 Suppl):172-177. https://doi.org/10.1637/11095-041715-Review
  8. Lee DH, Fusaro A, Song CS, Suarez DL, Swayne DE. Poultry vaccination directed evolution of H9N2 low pathogenicity avian influenza viruses in Korea. Virology. 2016;488:225-231. https://doi.org/10.1016/j.virol.2015.11.023
  9. Heo GB, Kye SJ, Sagong M, Lee EK, Lee KN, Lee YN, et al. Genetic characterization of H9N2 avian influenza virus previously unrecognized in Korea. J Vet Sci. 2021;22(2):e21.
  10. Youk S, Cho AY, Lee DH, Jeong S, Kim YJ, Lee S, et al. Detection of newly introduced Y280-lineage H9N2 avian influenza viruses in live bird markets in Korea. Transbound Emerg Dis. 2022;69(2):881-885. https://doi.org/10.1111/tbed.14014
  11. Davidson I, Fusaro A, Heidari A, Monne I, Cattoli G. Molecular evolution of H9N2 avian influenza viruses in Israel. Virus Genes. 2014;48(3):457-463. https://doi.org/10.1007/s11262-014-1037-0
  12. El Houadfi M, Fellahi S, Nassik S, Guerin JL, Ducatez MF. First outbreaks and phylogenetic analyses of avian influenza H9N2 viruses isolated from poultry flocks in Morocco. Virol J. 2016;13(1):140.
  13. Nagy A, Mettenleiter TC, Abdelwhab EM. A brief summary of the epidemiology and genetic relatedness of avian influenza H9N2 virus in birds and mammals in the Middle East and North Africa. Epidemiol Infect. 2017;145(16):3320-3333. https://doi.org/10.1017/S0950268817002576
  14. Carnaccini S, Perez DR. H9 influenza viruses: an emerging challenge. Cold Spring Harb Perspect Med. 2020;10(6):a038588.
  15. Gu M, Xu L, Wang X, Liu X. Current situation of H9N2 subtype avian influenza in China. Vet Res. 2017;48(1):49.
  16. Choi YK, Ozaki H, Webby RJ, Webster RG, Peiris JS, Poon L, et al. Continuing evolution of H9N2 influenza viruses in Southeastern China. J Virol. 2004;78(16):8609-8614. https://doi.org/10.1128/JVI.78.16.8609-8614.2004
  17. Li C, Yu K, Tian G, Yu D, Liu L, Jing B, et al. Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology. 2005;340(1):70-83. https://doi.org/10.1016/j.virol.2005.06.025
  18. Sealy JE, Fournie G, Trang PH, Dang NH, Sadeyen JR, Thanh TL, et al. Poultry trading behaviours in Vietnamese live bird markets as risk factors for avian influenza infection in chickens. Transbound Emerg Dis. 2019;66(6):2507-2516.  https://doi.org/10.1111/tbed.13308
  19. Shibata A, Hiono T, Fukuhara H, Sumiyoshi R, Ohkawara A, Matsuno K, et al. Isolation and characterization of avian influenza viruses from raw poultry products illegally imported to Japan by international flight passengers. Transbound Emerg Dis. 2018;65(2):465-475. https://doi.org/10.1111/tbed.12726
  20. Zinyakov NG, Sosipatorova VY, Andriyasov AV, Ovchinnikova EV, Nikonova ZB, Kozlov AA, et al. Genetic analysis of genotype G57 H9N2 avian influenza virus isolate A/chicken/Tajikistan/2379/2018 recovered in Central Asia. Arch Virol. 2021;166(6):1591-1597. https://doi.org/10.1007/s00705-021-05011-3
  21. World Health Organization. Avian Influenza Weekly Update Number 853 -15 July 2022. Geneva: World Health Organization; 2022. 
  22. Guan Y, Shortridge KF, Krauss S, Chin PS, Dyrting KC, Ellis TM, et al. H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China. J Virol. 2000;74(20):9372-9380. https://doi.org/10.1128/JVI.74.20.9372-9380.2000
  23. Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, et al. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature. 2013;502(7470):241-244. https://doi.org/10.1038/nature12515
  24. 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):714-721. https://doi.org/10.1016/S0140-6736(14)60111-2
  25. Shen YY, Ke CW, Li Q, Yuan RY, Xiang D, Jia WX, et al. Novel Reassortant Avian Influenza A(H5N6) Viruses in Humans, Guangdong, China, 2015. Emerg Infect Dis. 2016;22(8):1507-1509. https://doi.org/10.3201/eid2208.160146
  26. Zhang M, Zhang X, Xu K, Teng Q, Liu Q, Li X, et al. Characterization of the pathogenesis of H10N3, H10N7, and H10N8 subtype avian influenza viruses circulating in ducks. Sci Rep. 2016;6(1):34489.
  27. Gu M, Xu L, Wang X, Liu X. Current situation of H9N2 subtype avian influenza in China. Vet Res. 2017;48(1):49.
  28. Xu KM, Smith GJ, Bahl J, Duan L, Tai H, Vijaykrishna D, et al. The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol. 2007;81(19):10389-10401. https://doi.org/10.1128/JVI.00979-07
  29. Sun Y, Pu J, Jiang Z, Guan T, Xia Y, Xu Q, et al. Genotypic evolution and antigenic drift of H9N2 influenza viruses in China from 1994 to 2008. Vet Microbiol. 2010;146(3-4):215-225. https://doi.org/10.1016/j.vetmic.2010.05.010
  30. Chen LJ, Lin XD, Guo WP, Tian JH, Wang W, Ying XH, et al. Diversity and evolution of avian influenza viruses in live poultry markets, free-range poultry and wild wetland birds in China. J Gen Virol. 2016;97(4):844-854. https://doi.org/10.1099/jgv.0.000399
  31. Chen LJ, Lin XD, Tian JH, Liao Y, Ying XH, Shao JW, et al. Diversity, evolution and population dynamics of avian influenza viruses circulating in the live poultry markets in China. Virology. 2017;505:33-41. https://doi.org/10.1016/j.virol.2017.02.009
  32. Gu M, Chen H, Li Q, Huang J, Zhao M, Gu X, et al. Enzootic genotype S of H9N2 avian influenza viruses donates internal genes to emerging zoonotic influenza viruses in China. Vet Microbiol. 2014;174(3-4):309-315. https://doi.org/10.1016/j.vetmic.2014.09.029
  33. Jonas M, Sahesti A, Murwijati T, Lestariningsih CL, Irine I, Ayesda CS, et al. Identification of avian influenza virus subtype H9N2 in chicken farms in Indonesia. Prev Vet Med. 2018;159:99-105. https://doi.org/10.1016/j.prevetmed.2018.09.003
  34. Karlsson EA, Horm SV, Tok S, Tum S, Kalpravidh W, Claes F, et al. Avian influenza virus detection, temporality and co-infection in poultry in Cambodian border provinces, 2017-2018. Emerg Microbes Infect. 2019;8(1):637-639. https://doi.org/10.1080/22221751.2019.1604085
  35. Saito T, Lim W, Suzuki T, Suzuki Y, Kida H, Nishimura SI, et al. Characterization of a human H9N2 influenza virus isolated in Hong Kong. Vaccine. 2001;20(1-2):125-133. https://doi.org/10.1016/S0264-410X(01)00279-1
  36. Choi YK, Ozaki H, Webby RJ, Webster RG, Peiris JS, Poon L, et al. Continuing evolution of H9N2 influenza viruses in Southeastern China. J Virol. 2004;78(16):8609-8614.   https://doi.org/10.1128/JVI.78.16.8609-8614.2004
  37. Mase M, Eto M, Imai K, Tsukamoto K, Yamaguchi S. Characterization of H9N2 influenza A viruses isolated from chicken products imported into Japan from China. Epidemiol Infect. 2007;135(3):386-391. https://doi.org/10.1017/S0950268806006728
  38. Nomura N, Sakoda Y, Endo M, Yoshida H, Yamamoto N, Okamatsu M, et al. Characterization of avian influenza viruses isolated from domestic ducks in Vietnam in 2009 and 2010. Arch Virol. 2012;157(2):247-257. https://doi.org/10.1007/s00705-011-1152-3
  39. Thuy DM, Peacock TP, Bich VT, Fabrizio T, Hoang DN, Tho ND, et al. Prevalence and diversity of H9N2 avian influenza in chickens of Northern Vietnam, 2014. Infect Genet Evol. 2016;44:530-540. https://doi.org/10.1016/j.meegid.2016.06.038
  40. Suttie A, Tok S, Yann S, Keo P, Horm SV, Roe M, et al. The evolution and genetic diversity of avian influenza A(H9N2) viruses in Cambodia, 2015 - 2016. PLoS One. 2019;14(12):e0225428.
  41. Lin TN, Nonthabenjawan N, Chaiyawong S, Bunpapong N, Boonyapisitsopa S, Janetanakit T, et al. Influenza A(H9N2) virus, Myanmar, 2014-2015. Emerg Infect Dis. 2017;23(6):1041-1043. https://doi.org/10.3201/eid2306.161902
  42. Novianti AN, Rahardjo K, Prasetya RR, Nastri AM, Dewantari JR, Rahardjo AP, et al. Whole-genome sequence of an avian influenza A/H9N2 virus isolated from an apparently healthy chicken at a live-poultry market in Indonesia. Microbiol Resour Announc. 2019;8(17):e01671-18.
  43. Nugroho CM, Silaen OS, Kurnia RS, Soejoedono RD, Poetri ON, Soebandrio A. Isolation and molecular characterization of the hemagglutinin gene of H9N2 avian influenza viruses from poultry in Java, Indonesia. J Adv Vet Anim Res. 2021;8(3):423-434. https://doi.org/10.5455/javar.2021.h530
  44. Capua I, Alexander DJ. Avian influenza infections in birds--a moving target. Influenza Other Respi Viruses. 2007;1(1):11-18. https://doi.org/10.1111/j.1750-2659.2006.00004.x
  45. Capua I, Alexander DJ. Avian influenza infection in birds: a challenge and opportunity for the poultry veterinarian. Poult Sci. 2009;88(4):842-846. https://doi.org/10.3382/ps.2008-00289
  46. Sakoda Y, Sugar S, Batchluun D, Erdene-Ochir TO, Okamatsu M, Isoda N, et al. Characterization of H5N1 highly pathogenic avian influenza virus strains isolated from migratory waterfowl in Mongolia on the way back from the southern Asia to their northern territory. Virology. 2010;406(1):88-94. https://doi.org/10.1016/j.virol.2010.07.007
  47. Jeong J, Kang HM, Lee EK, Song BM, Kwon YK, Kim HR, et al. Highly pathogenic avian influenza virus (H5N8) in domestic poultry and its relationship with migratory birds in South Korea during 2014. Vet Microbiol. 2014;173(3-4):249-257. https://doi.org/10.1016/j.vetmic.2014.08.002
  48. Wang B, Chen Q, Chen Z. Complete genome sequence of an H9N2 avian influenza virus isolated from egret in Lake Dongting wetland. J Virol. 2012;86(21):11939.
  49. Zhu G, Wang R, Xuan F, Daszak P, Anthony SJ, Zhang S, et al. Characterization of recombinant H9N2 influenza viruses isolated from wild ducks in China. Vet Microbiol. 2013;166(3-4):327-336. https://doi.org/10.1016/j.vetmic.2013.05.013
  50. Wang H, Zhang Z, Chen Z, Zhang Y, Lv Q, An X, et al. High genetic diversity and frequent genetic reassortment of avian influenza A(H9N2) viruses along the East Asian-Australian migratory flyway. Infect Genet Evol. 2016;39:325-329. https://doi.org/10.1016/j.meegid.2016.02.013
  51. Li X, Sun J, Lv X, Wang Y, Li Y, Li M, et al. Novel reassortant avian influenza A(H9N2) virus isolate in migratory waterfowl in Hubei Province, China. Front Microbiol. 2020;11:220.
  52. Zhang X, Li Y, Jin S, Wang T, Sun W, Zhang Y, et al. H9N2 influenza virus spillover into wild birds from poultry in China bind to human-type receptors and transmit in mammals via respiratory droplets. Transbound Emerg Dis. 2022;69(2):669-684. https://doi.org/10.1111/tbed.14033
  53. Liu JH, Okazaki K, Shi WM, Kida H. Phylogenetic analysis of hemagglutinin and neuraminidase genes of H9N2 viruses isolated from migratory ducks. Virus Genes. 2003;27(3):291-296. https://doi.org/10.1023/A:1026304117797
  54. Jackwood MW, Stallknecht DE. Molecular epidemiologic studies on North American H9 avian influenza virus isolates from waterfowl and shorebirds. Avian Dis. 2007;51(1 Suppl):448-450.   https://doi.org/10.1637/7536-032706R.1
  55. Lee DH, Park JK, Yuk SS, Erdene-Ochir TO, Kwon JH, Lee JB, et al. Complete genome sequence of a natural reassortant H9N2 avian influenza virus found in bean goose (Anser fabalis): direct evidence for virus exchange between Korea and China via wild birds. Infect Genet Evol. 2014;26:250-254. https://doi.org/10.1016/j.meegid.2014.06.007
  56. Hu M, Jin Y, Zhou J, Huang Z, Li B, Zhou W, et al. Genetic characteristic and global transmission of influenza a H9N2 virus. Front Microbiol. 2017;8:2611.
  57. Yang J, Xie D, Nie Z, Xu B, Drummond AJ. Inferring host roles in bayesian phylodynamics of global avian influenza A virus H9N2. Virology. 2019;538:86-96. https://doi.org/10.1016/j.virol.2019.09.011
  58. Ge FF, Zhou JP, Liu J, Wang J, Zhang WY, Sheng LP, et al. Genetic evolution of H9 subtype influenza viruses from live poultry markets in Shanghai, China. J Clin Microbiol. 2009;47(10):3294-3300. https://doi.org/10.1128/JCM.00355-09
  59. Youk SS, Lee DH, Jeong JH, Pantin-Jackwood MJ, Song CS, Swayne DE. Live bird markets as evolutionary epicentres of H9N2 low pathogenicity avian influenza viruses in Korea. Emerg Microbes Infect. 2020;9(1):616-627. https://doi.org/10.1080/22221751.2020.1738903
  60. Lee HJ, Kwon JS, Lee DH, Lee YN, Youn HN, Lee YJ, et al. Continuing evolution and interspecies transmission of influenza viruses in live bird markets in Korea. Avian Dis. 2010;54(1 Suppl):738-748. https://doi.org/10.1637/8785-040109-ResNote.1
  61. Mo IP, Song CS, Kim KS, Rhee JC. An occurrence of non-highly pathogenic avian influenza in Korea. Avian Dis. 2003;47(Special Issue):379-383. 
  62. Lai VD, Kim JW, Choi YY, Kim JJ, So HH, Mo J. First report of field cases of Y280-like LPAI H9N2 strains in South Korean poultry farms: pathological findings and genetic characterization. Avian Pathol. 2021;50(4):327-338. https://doi.org/10.1080/03079457.2021.1929833
  63. Lee CW, Song CS, Lee YJ, Mo IP, Garcia M, Suarez DL, et al. Sequence analysis of the hemagglutinin gene of H9N2 Korean avian influenza viruses and assessment of the pathogenic potential of isolate MS96. Avian Dis. 2000;44(3):527-535. https://doi.org/10.2307/1593091
  64. Kishida N, Sakoda Y, Eto M, Sunaga Y, Kida H. Co-infection of Staphylococcus aureus or Haemophilus paragallinarum exacerbates H9N2 influenza A virus infection in chickens. Arch Virol. 2004;149(11):2095-2104. https://doi.org/10.1007/s00705-004-0372-1
  65. Kim HR, Park CK, Oem JK, Bae YC, Choi JG, Lee OS, et al. Characterization of H5N2 influenza viruses isolated in South Korea and their influence on the emergence of a novel H9N2 influenza virus. J Gen Virol. 2010;91(Pt 8):1978-1983. https://doi.org/10.1099/vir.0.021238-0
  66. Kye SJ, Park MJ, Kim NY, Lee YN, Heo GB, Baek YK, et al. Pathogenicity of H9N2 low pathogenic avian influenza viruses of different lineages isolated from live bird markets tested in three animal models: SPF chickens, Korean native chickens, and ducks. Poult Sci. 2021;100(9):101318.
  67. Bano S, Naeem K, Malik SA. Evaluation of pathogenic potential of avian influenza virus serotype H9N2 in chickens. Avian Dis. 2003;47(3 Suppl):817-822. https://doi.org/10.1637/0005-2086-47.s3.817
  68. Kwon JS, Lee HJ, Lee DH, Lee YJ, Mo IP, Nahm SS, et al. Immune responses and pathogenesis in immunocompromised chickens in response to infection with the H9N2 low pathogenic avian influenza virus. Virus Res. 2008;133(2):187-194. https://doi.org/10.1016/j.virusres.2007.12.019
  69. Xing Z, Cardona CJ, Li J, Dao N, Tran T, Andrada J. Modulation of the immune responses in chickens by low-pathogenicity avian influenza virus H9N2. J Gen Virol. 2008;89(Pt 5):1288-1299. https://doi.org/10.1099/vir.0.83362-0
  70. Shi H, Ashraf S, Gao S, Lu J, Liu X. Evaluation of transmission route and replication efficiency of H9N2 avian influenza virus. Avian Dis. 2010;54(1):22-27. https://doi.org/10.1637/8937-052809-Reg.1
  71. Yao M, Lv J, Huang R, Yang Y, Chai T. Determination of infective dose of H9N2 Avian Influenza virus in different routes: aerosol, intranasal, and gastrointestinal. Intervirology. 2014;57(6):369-374. https://doi.org/10.1159/000365925
  72. Chen H, Deng G, Li Z, Tian G, Li Y, Jiao P, et al. The evolution of H5N1 influenza viruses in ducks in southern China. Proc Natl Acad Sci U S A. 2004;101(28):10452-10457.   https://doi.org/10.1073/pnas.0403212101
  73. Sturm-Ramirez KM, Hulse-Post DJ, Govorkova EA, Humberd J, Seiler P, Puthavathana P, et al. Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? J Virol. 2005;79(17):11269-11279. https://doi.org/10.1128/JVI.79.17.11269-11279.2005
  74. Bi Y, Chen J, Zhang Z, Li M, Cai T, Sharshov K, et al. Highly pathogenic avian influenza H5N1 Clade 2.3.2.1c virus in migratory birds, 2014-2015. Virol Sin. 2016;31(4):300-305. https://doi.org/10.1007/s12250-016-3750-4
  75. Teng Q, Shen W, Liu Q, Rong G, Chen L, Li X, et al. Protective efficacy of an inactivated vaccine against H9N2 avian influenza virus in ducks. Virol J. 2015;12(1):143.
  76. Wang C, Wang Z, Ren X, Wang L, Li C, Sun Y, et al. Infection of chicken H9N2 influenza viruses in different species of domestic ducks. Vet Microbiol. 2019;233:1-4. https://doi.org/10.1016/j.vetmic.2019.04.018
  77. Huang R, Wang AR, Liu ZH, Liang W, Li XX, Tang YJ, et al. Seroprevalence of avian influenza H9N2 among poultry workers in Shandong Province, China. Eur J Clin Microbiol Infect Dis. 2013;32(10):1347-1351. https://doi.org/10.1007/s10096-013-1888-7
  78. Ma MJ, Zhao T, Chen SH, Xia X, Yang XX, Wang GL, et al. Avian influenza A virus infection among workers at live poultry markets, China, 2013-2016. Emerg Infect Dis. 2018;24(7):1246-1256. https://doi.org/10.3201/eid2407.172059
  79. European Food Safety AuthorityEuropean Centre for Disease Prevention and ControlEuropean Union Reference Laboratory for Avian InfluenzaAdlhoch C, Fusaro A, Gonzales JL, et al. Avian influenza overview March - June 2022. EFSA J. 2022;20(8):e07415.
  80. Suarez DL, Perdue ML, Cox N, Rowe T, Bender C, Huang J, et al. Comparisons of highly virulent H5N1 influenza A viruses isolated from humans and chickens from Hong Kong. J Virol. 1998;72(8):6678-6688. https://doi.org/10.1128/jvi.72.8.6678-6688.1998
  81. Jegede A, Fu Q, Berhane Y, Lin M, Kumar A, Guan J. H9N2 avian influenza virus retained low pathogenicity after serial passage in chickens. Can J Vet Res. 2018;82(2):131-138.
  82. Ren W, Zhang CH, Li G, Liu G, Shan H, Li J. Two genetically similar H9N2 influenza viruses isolated from different species show similar virulence in minks but different virulence in mice. Acta Virol. 2020;64(1):67-77. https://doi.org/10.4149/av_2020_109
  83. Niu X, Wang H, Zhao L, Lian P, Bai Y, Li J, et al. All-trans retinoic acid increases the pathogenicity of the H9N2 influenza virus in mice. Virol J. 2022;19(1):113.
  84. Butt AM, Siddique S, Idrees M, Tong Y. Avian influenza A (H9N2): computational molecular analysis and phylogenetic characterization of viral surface proteins isolated between 1997 and 2009 from the human population. Virol J. 2010;7(1):319.
  85. Kimble B, Nieto GR, Perez DR. Characterization of influenza virus sialic acid receptors in minor poultry species. Virol J. 2010;7(1):365.
  86. Pusch EA, Suarez DL. The multifaceted zoonotic risk of H9N2 avian influenza. Vet Sci. 2018;5(4):82.
  87. Sun X, Belser JA, Maines TR. Adaptation of H9N2 influenza viruses to mammalian hosts: a review of molecular markers. Viruses. 2020;12(5):541.
  88. Huang Y, Li X, Zhang H, Chen B, Jiang Y, Yang L, et al. Human infection with an avian influenza A (H9N2) virus in the middle region of China. J Med Virol. 2015;87(10):1641-1648. https://doi.org/10.1002/jmv.24231
  89. Song Y, Zhang Y, Chen L, Zhang B, Zhang M, Wang J, et al. Genetic characteristics and pathogenicity analysis in chickens and mice of three H9N2 avian influenza viruses. Viruses. 2019;11(12):1127.
  90. Zhang RR, Yang X, Shi CW, Yu LJ, Lian YB, Huang HB, et al. Improved pathogenicity of H9N2 subtype of avian influenza virus induced by mutations occurred after serial adaptations in mice. Microb Pathog. 2021;160:105204.
  91. Murakami J, Shibata A, Neumann G, Imai M, Watanabe T, Kawaoka Y. Characterization of H9N2 avian influenza viruses isolated from poultry products in a mouse model. Viruses. 2022;14(4):728. 
  92. Park SJ, Kang YM, Cho HK, Kim DY, Kim S, Bae Y, et al. Cross-protective efficacy of inactivated whole influenza vaccines against Korean Y280 and Y439 lineage H9N2 viruses in mice. Vaccine. 2021;39(42):6213-6220. https://doi.org/10.1016/j.vaccine.2021.09.028
  93. Lin Z, Xu C, Liu B, Ji Y, Fu Y, Guo J, et al. Analysis of the phylogeny of Chinese H9N2 avian influenza viruses and their pathogenicity in mice. Arch Virol. 2014;159(10):2575-2586. https://doi.org/10.1007/s00705-014-2110-7
  94. Baek YG, Lee YN, Lee DH, Shin JI, Lee JH, Chung DH, et al. Multiple reassortants of H5N8 clade 2.3.4.4b highly pathogenic avian influenza viruses detected in South Korea during the winter of 2020-2021. Viruses. 2021;13(3):490.
  95. Sagong M, Lee YN, Song S, Cha RM, Lee EK, Kang YM, et al. Emergence of clade 2.3.4.4b novel reassortant H5N1 high pathogenicity avian influenza virus in South Korea during late 2021. Transbound Emerg Dis. 2022;69(5):e3255-e3260. https://doi.org/10.1111/tbed.14551
  96. Sun Y, Liu J. H9N2 influenza virus in China: a cause of concern. Protein Cell. 2015;6(1):18-25. https://doi.org/10.1007/s13238-014-0111-7
  97. Zhang P, Tang Y, Liu X, Peng D, Liu W, Liu H, et al. Characterization of H9N2 influenza viruses isolated from vaccinated flocks in an integrated broiler chicken operation in eastern China during a 5 year period (1998-2002). J Gen Virol. 2008;89(Pt 12):3102-3112. https://doi.org/10.1099/vir.0.2008/005652-0
  98. Sun Y, Pu J, Fan L, Sun H, Wang J, Zhang Y, et al. Evaluation of the protective efficacy of a commercial vaccine against different antigenic groups of H9N2 influenza viruses in chickens. Vet Microbiol. 2012;156(1-2):193-199. https://doi.org/10.1016/j.vetmic.2011.10.003
  99. Liu Y, Li S, Sun H, Pan L, Cui X, Zhu X, et al. Variation and molecular basis for enhancement of receptor binding of H9N2 avian influenza viruses in China isolates. Front Microbiol. 2020;11:602124.
  100. Cui H, de Jong MC, Beerens N, van Oers MM, Teng Q, Li L, et al. Vaccination with inactivated virus against low pathogenic avian influenza subtype H9N2 does not prevent virus transmission in chickens. J Virus Erad. 2021;7(3):100055.
  101. Zhang Y, Yin Y, Bi Y, Wang S, Xu S, Wang J, et al. Molecular and antigenic characterization of H9N2 avian influenza virus isolates from chicken flocks between 1998 and 2007 in China. Vet Microbiol. 2012;156(3-4): 285-293. https://doi.org/10.1016/j.vetmic.2011.11.014
  102. Bi J, Deng G, Dong J, Kong F, Li X, Xu Q, et al. Phylogenetic and molecular characterization of H9N2 influenza isolates from chickens in Northern China from 2007-2009. PLoS One. 2010;5(9):e13063.
  103. Liu S, Zhuang Q, Wang S, Jiang W, Jin J, Peng C, et al. Control of avian influenza in China: strategies and lessons. Transbound Emerg Dis. 2020;67(4):1463-1471. https://doi.org/10.1111/tbed.13515
  104. Choi JG, Lee YJ, Kim YJ, Lee EK, Jeong OM, Sung HW, et al. An inactivated vaccine to control the current H9N2 low pathogenic avian influenza in Korea. J Vet Sci. 2008;9(1):67-74. https://doi.org/10.4142/jvs.2008.9.1.67
  105. Cho HK, Kang YM, Kim HM, Lee CH, Kim DY, Choi SH, et al. Sales and immunogenicity of commercial vaccines to H9N2 low pathogenic avian influenza virus in Korea from 2007 to 2017. Vaccine. 2020;38(16):3191-3195. https://doi.org/10.1016/j.vaccine.2020.02.083
  106. Su H, Zhao Y, Zheng L, Wang S, Shi H, Liu X. Effect of the selection pressure of vaccine antibodies on evolution of H9N2 avian influenza virus in chickens. AMB Express. 2020;10(1):98.
  107. Park KJ, Song MS, Kim EH, Kwon HI, Baek YH, Choi EH, et al. Molecular characterization of mammalian-adapted Korean-type avian H9N2 virus and evaluation of its virulence in mice. J Microbiol. 2015;53(8):570-577. https://doi.org/10.1007/s12275-015-5329-4
  108. Kim DY, Kang YM, Cho HK, Park SJ, Lee MH, Lee YJ, et al. Development of a recombinant H9N2 influenza vaccine candidate against the Y280 lineage field virus and its protective efficacy. Vaccine. 2021;39(42):6201-6205. https://doi.org/10.1016/j.vaccine.2021.08.089