The Alarming Situation of Highly Pathogenic Avian Influenza Viruses in 2019-2023

Abstract

Avian influenza viruses (AIVs) have the potential to cause severe illness in wild birds, domestic poultry, and humans. The ongoing circulation of highly pathogenic avian influenza viruses (HPAIVs) has presented significant challenges to global poultry industry and public health in recent years. This study aimed to elucidate the circulation of HPAIVs during 2019 to 2023. Specifically, we assess the alarming global spread and continuous evolution of HPAIVs. Moreover, we discuss their transmission and prevention strategies to provide valuable references for future prevention and control measures against AIVs.

Keywords

highly pathogenic avian influenza viruses / epidemiology / transmission / prevention and control

Funding/Acknowledgments

This research was supported by the Youth Program of National Natural Science Foundation of China (NO. 82003517).

Conflict of Interest

None declared.

References

[1] Lefkowitz EJ, Dempsey DM, Hendrickson RC, Orton RJ, Siddell SG, Smith DB. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res 2018; 46(D1): D708-D717

[2] Behboudi S. Alphainfluenzavirus influenzae. CABI Compendium. 2023. ; at

[3] Kim JH, Cho CH, Shin JH, et al. Highly sensitive and label-free detection of influenza H5N1 viral proteins using affinity peptide and porous BSA/MXene nanocomposite electrode. Anal Chim Acta 2023; 1251: 341018

[4] Charostad J, Rezaei Zadeh Rukerd M, Mahmoudvand S, et al. A comprehensive review of highly pathogenic avian influenza (HPAI) H5N1: an imminent threat at doorstep. Travel Med Infect Dis 2023; 55: 102638

[5] Carnegie L, Raghwani J, Fournié G, Hill SC. Phylodynamic approaches to studying avian influenza virus. Avian Pathol 2023; 52[phone]

[6] Verhagen JH, van Dijk JG, Vuong O, et al. Migratory birds reinforce local circulation of avian influenza viruses. PLoS One 2014; 9(11) e112366

[7] Nuñez IA, Ross TM. A review of H5Nx avian influenza viruses. Ther Adv Vaccines Immunother 2019; 7: 2515135518821625

[8] Kleyheeg E, Slaterus R, Bodewes R, et al. Deaths among wild birds during highly pathogenic avian influenza A (H5N8) virus outbreak, the Netherlands. Emerg Infect Dis 2017; 23(12) 2050-2054

[9] Lean FZX, Vitores AG, Reid SM, et al. Gross pathology of high pathogenicity avian influenza virus H5N1 2021-2022 epizootic in naturally infected birds in the United Kingdom. One Health 2022; 14: 100392

[10] Lai S, Qin Y, Cowling BJ, et al. Global epidemiology of avian influenza A H5N1 virus infection in humans, 1997-2015: a systematic review of individual case data. Lancet Infect Dis 2016; 16(07) e108-e118

[11] Blagodatski A, Trutneva K, Glazova O, et al. Avian influenza in wild birds and poultry: dissemination pathways, monitoring methods, and virus ecology. Pathogens 2021; 10(05) 630

[12] Agüero M, Monne I, Sánchez A, et al. Highly pathogenic avian influenza A(H5N1) virus infection in farmed minks, Spain, October 2022. Euro Surveill 2023; 28[phone]

[13] Vreman S, Kik M, Germeraad E, et al. Zoonotic mutation of highly pathogenic avian influenza H5N1 virus identified in the brain of multiple wild carnivore species. Pathogens 2023; 12(02) 168

[14] Hampson AW, Mackenzie JS. The influenza viruses. Med J Aust 2006; 185(S10): S39-S43

[15] Rimi NA, Hassan MZ, Chowdhury S, et al. A decade of avian influenza in Bangladesh: where are we now?. Trop Med Infect Dis 2019; 4(03) 119

[16] Wille M, Holmes EC. The ecology and evolution of influenza viruses. Cold Spring Harb Perspect Med 2020; 10(07) a038489

[17] Ghedin E, Sengamalay NA, Shumway M, et al. Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 2005; 437(7062) 1162-1166

[18] Bouvier NM, Palese P. The biology of influenza viruses. Vaccine 2008; 26(Suppl 4, Suppl 4): D49-D53

[19] Kosik I, Yewdell JW. Influenza hemagglutinin and neuraminidase: Yin-Yang proteins coevolving to thwart immunity. Viruses 2019; 11(04) 346

[20] Kayal V, Brundha M, Sivaswamy V. New concepts of antigenic shift and antigenic drift in influenza and corona-a review of literature. Int J Pharmaceutical Res 2021; 13[phone]

[21] Yoon SW, Webby RJ, Webster RG. Evolution and ecology of influenza A viruses. Curr Top Microbiol Immunol 2014; 385: 359-375

[22] Blaurock C, Scheibner D, Landmann M, et al. Non-basic amino acids in the hemagglutinin proteolytic cleavage site of a European H9N2 avian influenza virus modulate virulence in turkeys. Sci Rep 2020; 10(01) 21226

[23] Verhagen JH, Eriksson P, Leijten L, et al. Host range of influenza A virus H1 to H16 in Eurasian ducks based on tissue and receptor binding studies. J Virol 2021; 95(06) 01873-20

[24] World Health Organization. Antigenic and genetic characteristics of zoonotic influenza A viruses and development of candidate vaccine viruses for pandemic preparedness. Wkly Epidemiol Rec 2020; 95(44) 525-539

[25] WHO/OIE/FAO H5N1 Evolution Working Group. Continued evolution of highly pathogenic avian influenza A (H5N1): updated nomenclature. Influenza Other Respir Viruses 2012; 6(01) 1-5

[26] Neumann G, Chen H, Gao GF, Shu Y, Kawaoka Y. H5N1 influenza viruses: outbreaks and biological properties. Cell Res 2010; 20(01) 51-61

[27] Bi Y, Chen Q, Wang Q, et al. Genesis, evolution and prevalence of H5N6 avian influenza viruses in China. Cell Host Microbe 2016; 20[phone]

[28] Du Y, Chen M, Yang J, et al. Molecular evolution and emergence of H5N6 avian influenza virus in central China. J Virol 2017; 91(12) 00143-17

[29] Cui Y, Li Y, Li M, et al. Evolution and extensive reassortment of H5 influenza viruses isolated from wild birds in China over the past decade. Emerg Microbes Infect 2020; 9[phone]

[30] Gu W, Shi J, Cui P, 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[phone]

[31] Hesterberg U, Harris K, Stroud D, et al. Avian influenza surveillance in wild birds in the European Union in 2006. Influenza Other Respir Viruses 2009; 3(01) 1-14

[32] Adlhoch C, Gossner C, Koch G, et al. Comparing introduction to Europe of highly pathogenic avian influenza viruses A(H5N8) in 2014 and A(H5N1) in 2005. Euro Surveill 2014; 19(50) 20996

[33] Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus AD, Fouchier RA. Global patterns of influenza a virus in wild birds. Science 2006; 312(5772) 384-388

[34] European Food Safety Authority, European Centre for Disease Prevention and Control. Highly pathogenic avian influenza A subtype H5N8. EFSA J 2014; 12(12) 3941

[35] Jeong J, Kang HM, Lee EK, 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

[36] Lee DH, Torchetti MK, Winker K, Ip HS, Song CS, Swayne DE. Intercontinental spread of Asian-origin H5N8 to North America through Beringia by migratory birds. J Virol 2015; 89(12) 6521-6524

[37] Li Y, Li M, Li Y, et al. Outbreaks of highly pathogenic avian influenza (H5N6) virus subclade 2.3.4.4 h in swans, Xinjiang, Western China, 2020. Emerg Infect Dis 2020; 26(12) 2956-2960

[38] Youk S, Torchetti MK, Lantz K, et al. H5N1 highly pathogenic avian influenza clade 2.3.4.4b in wild and domestic birds: Introductions into the United States and reassortments, December 2021-April 2022. Virology 2023; 587: 109860

[39] Howley PM, Knipe DM. Fields Virology: Emerging Viruses. Philadelphia, PA: Lippincott Williams & Wilkins; 2020

[40] Centers for Disease Control and Prevention. Reported human infections with avian influenza A viruses. 2023. Accessed 1 March 2024 at:

[41] Liu Q, Liu DY, Yang ZQ. Characteristics of human infection with avian influenza viruses and development of new antiviral agents. Acta Pharmacol Sin 2013; 34(10) 1257-1269

[42] Government of Canada. Biosafety directive for new and emerging influenza A viruses. Accessed 1 March 2024 at:

[43] Mostafa A, Abdelwhab EM, Mettenleiter TC, Pleschka S. Zoonotic potential of influenza A viruses: a comprehensive overview. Viruses 2018; 10(09) 497

[44] Lycett SJ, Duchatel F, Digard P. A brief history of bird flu. Philos Trans R Soc Lond B Biol Sci 2019; 374(1775) 20180257

[45] Centers for Disease Control and Prevention. Highlights in the History of Avian Influenza (Bird Flu). Accessed 1 March 2024 at:

[46] Hu T, Zhao H, Zhang Y, et al. Fatal influenza A (H5N1) virus infection in zoo-housed Tigers in Yunnan Province, China. Sci Rep 2016; 6(01) 25845

[47] Keawcharoen J, Oraveerakul K, Kuiken T, et al. Avian influenza H5N1 in tigers and leopards. Emerg Infect Dis 2004; 10(12) 2189-2191

[48] World Organisation for Animal Health. Immediate notification highly pathogenic influenza A viruses (Inf. with) (non-poultry including wild birds). 2017 -), Estonia. Accessed 1 March 2024 at:

[49] World Health Organization.Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO,. 2003-2023. Accessed 1 March 2024 at:

[50] Dalli J. Commission Decision 2010/367/EU of 25 June 2010 on the implementation by Member States of surveillance programmes for avian influenza in poultry and wild birds. Official Journal of the European Union 2010; 166: 22-32

[51] Li C, Chen H. H7N9 influenza virus in China. Cold Spring Harb Perspect Med 2021; 11(08) a038349

[52] Huang P, Sun L, Li J, et al. Potential cross-species transmission of highly pathogenic avian influenza H5 subtype (HPAI H5) viruses to humans calls for the development of H5-specific and universal influenza vaccines. Cell Discov 2023; 9(01) 58

[53] Tian H, Zhou S, Dong L, et al. Avian influenza H5N1 viral and bird migration networks in Asia. Proc Natl Acad Sci U S A 2015; 112[phone]

[54] Bragstad K, Jørgensen PH, Handberg K, Hammer AS, Kabell S, Fomsgaard A. First introduction of highly pathogenic H5N1 avian influenza A viruses in wild and domestic birds in Denmark, Northern Europe. Virol J 2007; 4: 43

[55] Lewis NS, Banyard AC, Whittard E, et al. Emergence and spread of novel H5N8, H5N5 and H5N1 clade 2.3.4.4 highly pathogenic avian influenza in 2020. Emerg Microbes Infect 2021; 10[phone]

[56] Adlhoch C, Fusaro A, Gonzales JL, et al; European Food Safety Authority, European Centre for Disease Prevention, Control, European Union Reference Laboratory for Avian Influenza. Avian influenza overview September - December 2021. EFSA J 2021; 19(12) e07108

[57] Caliendo V, Lewis NS, Pohlmann A, et al. Transatlantic spread of highly pathogenic avian influenza H5N1 by wild birds from Europe to North America in 2021. Sci Rep 2022; 12(01) 11729

[58] Günther A, Krone O, Svansson V, et al. Iceland as stepping stone for spread of highly pathogenic avian influenza virus between Europe and North America. Emerg Infect Dis 2022; 28(12) 2383-2388

[59] USDA APHIS. Confirmations of highly pathogenic avian influenza in commercial and backyard flocks. Accessed 1 March 2024 at:

[60] Elsmo E, Wünschmann A, Beckmen K, et al. Pathology of natural infection with highly pathogenic avian influenza virus (H5N1) clade 2.3.4.4 b in wild terrestrial mammals in the United States in 2022. BioRxiv 2023; 2023.03

[61] USDA APHIS. Detections of highly pathogenic avian influenza in mammals. Accessed 1 March 2024 at:

[62] Rijks JM, Hesselink H, Lollinga P, et al. Highly pathogenic avian influenza A (H5N1) virus in wild red foxes, the Netherlands, 2021. Emerg Infect Dis 2021; 27(11) 2960-2962

[63] Adlhoch C, Fusaro A, Gonzales JL, et al; European Food Safety Authority, European Centre for Disease Prevention and Control, European Union Reference Laboratory for Avian Influenza. Avian influenza overview June-September 2023. EFSA J 2023; 21(10) e08328

[64] Fisheries N. Recent increase in seal deaths in maine linked to avian flu. Accessed 1 March 2024 at:

[65] Adlhoch C, Fusaro A, Gonzales JL, et al; European Food Safety Authority, European Centre for Disease Prevention and Control, European Union Reference Laboratory for Avian Influenza. Avian influenza overview December 2021 - March 2022. EFSA J 2022; 20(04) e07289

[66] Oliver I, Roberts J, Brown CS, et al. A case of avian influenza A(H5N1) in England, January 2022. Euro Surveill 2022; 27[phone]

[67] Qu N, Zhao B, Chen Z, et al. Genetic characteristics, pathogenicity and transmission of H5N6 highly pathogenic avian influenza viruses in Southern China. Transbound Emerg Dis 2019; 66[phone]

[68] Li H, Li Q, Li B, et al. Continuous reassortment of clade 2.3. 4.4 H5N6 highly pathogenetic avian influenza viruses demonstrating high risk to public health. Pathogens 2020; 9(08) 670

[69] Zhang J, Ye H, Liu Y, Liao M, Qi W. Resurgence of H5N6 avian influenza virus in 2021 poses new threat to public health. Lancet Microbe 2022; 3(08) e558

[70] Shittu I, Bianco A, Gado D, et al. First detection of highly pathogenic H5N6 avian influenza virus on the African continent. Emerg Microbes Infect 2020; 9[phone]

[71] Yang L, Zhu W, Li X, et al. Genesis and dissemination of highly pathogenic H5N6 avian influenza viruses. J Virol 2017; 91(05) 02199-16

[72] Zhang Y, Chen M, Huang Y, et al. Human infections with novel reassortant H5N6 avian influenza viruses in China. Emerg Microbes Infect 2017; 6(06) e50

[73] Sun W, Li J, Hu J, et al. Genetic analysis and biological characteristics of different internal gene origin H5N6 reassortment avian influenza virus in China in 2016. Vet Microbiol 2018; 219: 200-211

[74] Zhang R, Lei Z, Liu C, et al. Live poultry feeding and trading network and the transmission of avian influenza A(H5N6) virus in a large city in China, 2014-2015. Int J Infect Dis 2021; 108: 72-80

[75] Zhu W, Li X, Dong J, et al. Epidemiologic, clinical, and genetic characteristics of human infections with influenza A (H5N6) viruses, China. Emerg Infect Dis 2022; 28[phone]

[76] Sun H, Pu J, Wei Y, et al. Highly pathogenic avian influenza H5N6 viruses exhibit enhanced affinity for human type sialic acid receptor and in-contact transmission in model ferrets. J Virol 2016; 90(14) 6235-6243

[77] Pan M, Gao R, Lv Q, et al. Human infection with a novel, highly pathogenic avian influenza A (H5N6) virus: virological and clinical findings. J Infect 2016; 72(01) 52-59

[78] Yang L, Zhao X, Li X, et al. Case report for human infection with a highly pathogenic avian influenza A (H5N6) virus in Beijing, China 2019. Biosafety Health 2020; 2(01) 49-52

[79] Lee YJ, Kang HM, Lee EK, et al. Novel reassortant influenza A(H5N8) viruses, South Korea, 2014. Emerg Infect Dis 2014; 20[phone]

[80] Adlhoch C, Fusaro A, Kuiken T, et al; European Food Safety Authority, European Centre for Disease Prevention and Control and European Union Reference Laboratory for Avian Influenza. Avian influenza overview February - May 2020. EFSA J 2020; 18(06) e06194

[81] Xiong J, Zhou H, Fan L, et al. Emerging highly pathogenic avian influenza (H5N8) virus in migratory birds in Central China, 2020. Emerg Microbes Infect 2021; 10[phone]

[82] Floyd T, Banyard AC, Lean FZX, et al. Encephalitis and death in wild mammals at a rehabilitation center after infection with highly pathogenic avian influenza A(H5N8) virus, United Kingdom. Emerg Infect Dis 2021; 27(11) 2856-2863

[83] King J, Harder T, Globig A, et al. Highly pathogenic avian influenza virus incursions of subtype H5N8, H5N5, H5N1, H5N4, and H5N3 in Germany during 2020-21. Virus Evol 2022; 8(01) veac035

[84] Liang Y, Nissen JN, Krog JS, et al. Novel clade 2.3.4.4 b highly pathogenic avian influenza A H5N8 and H5N5 viruses in Denmark, 2020. Viruses 2021; 13(05) 886

[85] Pyankova OG, Susloparov IM, Moiseeva AA, et al. Isolation of clade 2.3.4.4b A(H5N8), a highly pathogenic avian influenza virus, from a worker during an outbreak on a poultry farm, Russia, December 2020. Euro Surveill 2021; 26(24) 2100439

[86] Hall JS, Dusek RJ, Spackman E. Rapidly expanding range of highly pathogenic avian influenza viruses. Emerg Infect Dis 2015; 21[phone]

[87] Lycett SJ, Pohlmann A, Staubach C, et al; Global Consortium for H5N8 and Related Influenza Viruses. Genesis and spread of multiple reassortants during the 2016/2017 H5 avian influenza epidemic in Eurasia. Proc Natl Acad Sci U S A 2020; 117(34) 20814-20825

[88] Fusaro A, Zecchin B, Vrancken B, et al. Disentangling the role of Africa in the global spread of H5 highly pathogenic avian influenza. Nat Commun 2019; 10(01) 5310

[89] Świętoń E, Fusaro A, Shittu I, et al. Sub-Saharan Africa and Eurasia ancestry of reassortant highly pathogenic avian influenza A(H5N8) virus, Europe, December 2019. Emerg Infect Dis 2020; 26[phone]

[90] Tian J, Bai X, Li M, et al. Highly pathogenic avian influenza virus (H5N1) clade 2.3.4.4 b introduced by wild birds, China, 2021. Emerg Infect Dis 2023; 29[phone]

[91] Śmietanka K, Świętoń E, Kozak E, et al. Highly pathogenic avian influenza H5N8 in Poland in 2019-2020. J Vet Res (Pulawy) 2020; 64[phone]

[92] Sobolev I, Sharshov K, Dubovitskiy N, et al. Highly pathogenic avian influenza A(H5N8) virus clade 2.3.4.4 b, Western Siberia, Russia, 2020. Emerg Infect Dis 2021; 27[phone]

[93] Beerens N, Heutink R, Harders F, et al. Incursion of novel highly pathogenic avian influenza A(H5N8) virus, the Netherlands, October 2020. Emerg Infect Dis 2021; 27[phone]

[94] Isoda N, Twabela AT, Bazarragchaa E, et al. Re-invasion of H5N8 high pathogenicity avian influenza virus clade 2.3. 4.4 b in Hokkaido, Japan, 2020. Viruses 2020; 12(12) 1439

[95] Jeong S, Lee D-H, Kwon J-H, et al. Highly pathogenic avian influenza clade 2.3.4.4 b subtype H5N8 virus isolated from Mandarin duck in South Korea, 2020. Viruses 2020; 12(12) 1389

[96] Baek YG, Lee YN, Lee DH, et al. Multiple reassortants of H5N8 clade 2.3.4.4 b highly pathogenic avian influenza viruses detected in South Korea during the Winter of 2020-2021. Viruses 2021; 13(03) 490

[97] Beerens N, Germeraad EA, Venema S, Verheij E, Pritz-Verschuren SBE, Gonzales JL. Comparative pathogenicity and environmental transmission of recent highly pathogenic avian influenza H5 viruses. Emerg Microbes Infect 2021; 10(01) 97-108

[98] Khalil AM, Fujimoto Y, Kojima I, et al. Genetic characterization of H5N8 highly pathogenic avian influenza viruses isolated from falcated ducks and environmental water in Japan in November 2020. Pathogens 2021; 10(02) 171

[99] Lopez-Martinez I, Balish A, Barrera-Badillo G, et al. Highly pathogenic avian influenza A(H7N3) virus in poultry workers, Mexico, 2012. Emerg Infect Dis 2013; 19[phone]

[100] Shu Y, McCauley J. GISAID: Global initiative on sharing all influenza data - from vision to reality. Euro Surveill 2017; 22(13) 30494

[101] Navarro-Lopez R, Xu W, Gomez-Romero N, Velazquez-Salinas L, Berhane Y. Phylogenetic inference of the 2022 highly pathogenic H7N3 avian influenza outbreak in Northern Mexico. Pathogens 2022; 11(11) 1284

[102] Youk S, Lee D-H, Killian ML, Pantin-Jackwood MJ, Swayne DE, Torchetti MK. Highly pathogenic avian influenza A (H7N3) virus in poultry, United States, 2020. Emerg Infect Dis 2020; 26(12) 2966-2969

[103] Lu L, Lycett SJ, Leigh Brown AJ. Determining the phylogenetic and phylogeographic origin of highly pathogenic avian influenza (H7N3) in Mexico. PLoS One 2014; 9(09) e107330

[104] Youk S, Lee DH, Ferreira HL, et al. Rapid evolution of Mexican H7N3 highly pathogenic avian influenza viruses in poultry. PLoS One 2019; 14(09) e0222457

[105] Trovão NS, Talavera GA, Nelson MI, Perez de la Rosa JD. Evolution of highly pathogenic H7N3 avian influenza viruses in Mexico. Zoonoses Public Health 2020; 67[phone]

[106] Youk SS, Lee DH, Leyson CM, et al. Loss of fitness of Mexican H7N3 highly pathogenic avian influenza virus in mallards after circulating in chickens. J Virol 2019; 93(14) 00543-19

[107] Beerens N, Heutink R, Harders F, Bossers A, Koch G, Peeters B. Emergence and selection of a highly pathogenic avian influenza H7N3 virus. J Virol 2020; 94(08) 01818-01819

[108] Banks J, Speidel ES, Moore E, et al. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch Virol 2001; 146[phone]

[109] Röhm C, Horimoto T, Kawaoka Y, Süss J, Webster RG. Do hemagglutinin genes of highly pathogenic avian influenza viruses constitute unique phylogenetic lineages?. Virology 1995; 209[phone]

[110] Navarro-López R, Solís-Hernández M, Márquez-Ruiz MA, et al. Epizootic of highly pathogenic H7N3 Avian Influenza in an ecologic reserve in Mexico. bioRxiv 2020; 2020.03.05.978502

[111] Lee DH, Criado MF, Swayne DE. Pathobiological origins and evolutionary history of highly pathogenic avian influenza viruses. Cold Spring Harb Perspect Med 2021; 11(02) a038679

[112] Kayed AE, Kutkat O, Kandeil A, et al. Comparative pathogenic potential of avian influenza H7N3 viruses isolated from wild birds in Egypt and their sensitivity to commercial antiviral drugs. Arch Virol 2023; 168(03) 82

[113] Skowronski DM, Li Y, Tweed SA, et al. Protective measures and human antibody response during an avian influenza H7N3 outbreak in poultry in British Columbia, Canada. CMAJ 2007; 176(01) 47-53

[114] Trinh TTT, Tiwari I, Durairaj K, et al. Genetic characterization and pathogenesis of avian influenza virus H7N3 isolated from spot-billed ducks in South Korea, early 2019. Viruses 2021; 13(05) 856

[115] Süss J, Schäfer J, Sinnecker H, Webster RG. Influenza virus subtypes in aquatic birds of eastern Germany. Arch Virol 1994; 135(1-2): 101-114

[116] Scheibner D, Blaurock C, Mettenleiter TC, Abdelwhab EM. Virulence of three European highly pathogenic H7N1 and H7N7 avian influenza viruses in Pekin and Muscovy ducks. BMC Vet Res 2019; 15(01) 142

[117] Spruit CM, Zhu X, Tomris I, et al. N-glycolylneuraminic acid binding of avian and equine H7 influenza A viruses. J Virol 2022; 96(05) e0212021

[118] van der Goot JA, Koch G, de Jong MC, van Boven M. Quantification of the effect of vaccination on transmission of avian influenza (H7N7) in chickens. Proc Natl Acad Sci U S A 2005; 102(50) 18141-18146

[119] Park MS, Steel J, García-Sastre A, Swayne D, Palese P. Engineered viral vaccine constructs with dual specificity: avian influenza and Newcastle disease. Proc Natl Acad Sci U S A 2006; 103(21) 8203-8208

[120] DeLay PD, Casey HL, Tubiash HS. Comparative study of fowl plague virus and a virus isolated from man. Public Health Rep 1967; 82[phone]

[121] Kurtz J, Manvell RJ, Banks J. Avian influenza virus isolated from a woman with conjunctivitis. Lancet 1996; 348(9031) 901-902

[122] Fouchier RA, Schneeberger PM, Rozendaal FW, et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 2004; 101[phone]

[123] Puzelli S, Rossini G, Facchini M, et al; Influenza Task Force. Human infection with highly pathogenic A(H7N7) avian influenza virus, Italy, 2013. Emerg Infect Dis 2014; 20(10) 1745-1749

[124] Munster VJ, de Wit E, van Riel D, et al. The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J Infect Dis 2007; 196[phone]

[125] Belser JA, Blixt O, Chen LM, et al. Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proc Natl Acad Sci U S A 2008; 105(21) 7558-7563

[126] Chan MC, Chan RW, Chan LL, et al. Tropism and innate host responses of a novel avian influenza A H7N9 virus: an analysis of ex-vivo and in-vitro cultures of the human respiratory tract. Lancet Respir Med 2013; 1[phone]

[127] Song C, Liu Y, Jiang X, et al. Ultrasensitive SERS determination of avian influenza A H7N9 virus via exonuclease III-assisted cycling amplification. Talanta 2019; 205: 120137

[128] Chen Y, Liang W, Yang S, et al. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 2013; 381(9881) 1916-1925

[129] Gao R, Cao B, Hu Y, et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 2013; 368(20) 1888-1897

[130] Ma MJ, Yang Y, Fang LQ. Highly pathogenic avian H7N9 influenza viruses: recent challenges. Trends Microbiol 2019; 27(02) 93-95

[131] Li G, Wang X, Li Q, et al. Development of an immunochromatographic strip for rapid detection of H7 subtype avian influenza viruses. Virol J 2021; 18(01) 68

[132] Zhang X, Li Y, Jin S, 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[phone]

[133] Qi W, Jia W, Liu D, et al. Emergence and adaptation of a novel highly pathogenic H7N9 influenza virus in birds and humans from a 2013 human-infecting low-pathogenic ancestor. J Virol 2018; 92(02) 00921-17

[134] Yang H, Winkler W, Wu X. Interferon Inducer IFI35 regulates RIG-I-mediated innate antiviral response through mutual antagonism with Influenza protein NS1. J Virol 2021; 95(11) 00283-21

[135] Wu Y, Hu J, Jin X, et al. Accelerated evolution of H7N9 subtype influenza virus under vaccination pressure. Virol Sin 2021; 36[phone]

[136] Zhu H, Lam TTY, Smith DK, Guan Y. Emergence and development of H7N9 influenza viruses in China. Curr Opin Virol 2016; 16: 106-113

[137] Li Q, Zhou L, Zhou M, et al. Epidemiology of human infections with avian influenza A(H7N9) virus in China. N Engl J Med 2014; 370[phone]

[138] Shi J, Deng G, Kong H, et al. H7N9 virulent mutants detected in chickens in China pose an increased threat to humans. Cell Res 2017; 27(12) 1409-1421

[139] Keawcharoen J, van den Broek J, Bouma A, Tiensin T, Osterhaus AD, Heesterbeek H. Wild birds and increased transmission of highly pathogenic avian influenza (H5N1) among poultry, Thailand. Emerg Infect Dis 2011; 17[phone]

[140] Harvey JA, Mullinax JM, Runge MC, Prosser DJ. The changing dynamics of highly pathogenic avian influenza H5N1: Next steps for management & science in North America. Biol Conserv 2023; 282: 110041

[141] Tsiodras S, Kelesidis T, Kelesidis I, Bauchinger U, Falagas ME. Human infections associated with wild birds. J Infect 2008; 56(02) 83-98

[142] Chowdhury S, Hossain ME, Ghosh PK, et al. The pattern of highly pathogenic avian influenza H5N1 outbreaks in South Asia. Trop Med Infect Dis 2019; 4(04) 138

[143] Wu T, Perrings C. The live poultry trade and the spread of highly pathogenic avian influenza: regional differences between Europe, West Africa, and Southeast Asia. PLoS One 2018; 13(12) e0208197

[144] Puranik A, Slomka MJ, Warren CJ, et al. Transmission dynamics between infected waterfowl and terrestrial poultry: Differences between the transmission and tropism of H5N8 highly pathogenic avian influenza virus (clade 2.3.4.4a) among ducks, chickens and turkeys. Virology 2020; 541: 113-123

[145] Islam SS, Akwar H, Hossain MM, et al. Qualitative risk assessment of transmission pathways of highly pathogenic avian influenza (HPAI) virus at live poultry markets in Dhaka city, Bangladesh. Zoonoses Public Health 2020; 67[phone]

[146] Dong G, Luo J, Zhang H, et al. Phylogenetic diversity and genotypical complexity of H9N2 influenza A viruses revealed by genomic sequence analysis. PLoS One 2011; 6(02) e17212

[147] Yamaji R, Saad MD, Davis CT, et al. Pandemic potential of highly pathogenic avian influenza clade 2.3.4.4 A(H5) viruses. Rev Med Virol 2020; 30(03) e2099

[148] Pulit-Penaloza JA, Brock N, Pappas C, et al. Characterization of highly pathogenic avian influenza H5Nx viruses in the ferret model. Sci Rep 2020; 10(01) 12700

[149] Gass Jr JD, Dusek RJ, Hall JS, et al. Global dissemination of influenza A virus is driven by wild bird migration through arctic and subarctic zones. Mol Ecol 2023; 32[phone]

[150] Feare CJ. Role of wild birds in the spread of highly pathogenic avian influenza virus H5N1 and implications for global surveillance. Avian Dis 2010; 54[phone]

[151] Bertran K, Balzli C, Kwon Y-K, Tumpey TM, Clark A, Swayne DE. Airborne transmission of highly pathogenic influenza virus during processing of infected poultry. Emerg Infect Dis 2017; 23(11) 1806-1814

[152] Zeng H, Goldsmith CS, Kumar A, et al. Tropism and infectivity of a seasonal A (H1N1) and a highly pathogenic avian A (H5N1) influenza virus in primary differentiated ferret nasal epithelial cell cultures. J Virol 2019; 93(10) 00080-19

[153] Ortiz JR, Katz MA, Mahmoud MN, et al. Lack of evidence of avian-to-human transmission of avian influenza A (H5N1) virus among poultry workers, Kano, Nigeria, 2006. J Infect Dis 2007; 196(11) 1685-1691

[154] Lei F, Shi W. Prospective of genomics in revealing transmission, reassortment and evolution of wildlife-borne avian influenza A (H5N1) viruses. Curr Genomics 2011; 12[phone]

[155] Sutton TC, Finch C, Shao H, et al. Airborne transmission of highly pathogenic H7N1 influenza virus in ferrets. J Virol 2014; 88(12) 6623-6635

[156] Pulit-Penaloza JA, Brock N, Belser JA, et al. Highly pathogenic avian influenza A(H5N1) virus of clade 2.3.4.4b isolated from a human case in Chile causes fatal disease and transmits between co-housed ferrets. Emerg Microbes Infect 2024; 13(12) 2332667

[157] Xu W, Dai Y, Hua C, et al. Genomic signature analysis of the recently emerged highly pathogenic A(H5N8) avian influenza virus: implying an evolutionary trend for bird-to-human transmission. Microbes Infect 2017; 19(12) 597-604

[158] Adlhoch C, Fusaro A, Kuiken T, et al; European Food Safety Authority, European Centre for Disease Prevention and Control and European Union Reference Laboratory for Avian Influenza. Avian influenza overview November 2019- February2020. EFSA J 2020; 18(03) e06096

[159] Zhou L, Liao Q, Dong L, et al. Risk factors for human illness with avian influenza A (H5N1) virus infection in China. J Infect Dis 2009; 199(12) 1726-1734

[160] Ly S, Vong S, Cavailler P, et al. Environmental contamination and risk factors for transmission of highly pathogenic avian influenza A(H5N1) to humans, Cambodia, 2006-2010. BMC Infect Dis 2016; 16(01) 631

[161] Shi J, Zeng X, Cui P, Yan C, Chen H. Alarming situation of emerging H5 and H7 avian influenza and effective control strategies. Emerg Microbes Infect 2023; 12[phone]

[162] Sun Z, Li Y, An Q, Gao X, Wang H. Risk factors contributing to highly pathogenic avian influenza H5N6 in China, 2014 Based on a MaxEnt model. Transbound Emerg Dis 2021; 2023: 2023

[163] Yamaji R, Yamada S, Le MQ, et al. Identification of PB2 mutations responsible for the efficient replication of H5N1 influenza viruses in human lung epithelial cells. J Virol 2015; 89[phone]

[164] Ungchusak K, Auewarakul P, Dowell SF, et al. Probable person-to-person transmission of avian influenza A (H5N1). N Engl J Med 2005; 352[phone]

[165] Wang H, Feng Z, Shu Y, et al. Probable limited person-to-person transmission of highly pathogenic avian influenza A (H5N1) virus in China. Lancet 2008; 371(9622) 1427-1434

[166] Lemon SM, Mahmoud AA. The threat of pandemic influenza: are we ready?. Biosecur Bioterror 2005; 3(01) 70-73

[167] Duan C, Li C, Ren R, Bai W, Zhou L. An overview of avian influenza surveillance strategies and modes. Science in One Health 2023; 2: 100043

[168] Simancas-Racines A, Cadena-Ullauri S, Guevara-Ramírez P, Zambrano AK, Simancas-Racines D. Avian influenza: strategies to manage an outbreak. Pathogens 2023; 12(04) 610

[169] Martin V, Forman A, Lubroth J. Preparing for Highly Pathogenic Avian Influenza. Québec City: Food and Agriculture Organization of the United Nations; 2006

[170] Jonas O, Warford L. Global program for Avian Influenza control and human pandemic preparedness and response: project accomplishments. Health, Nutrition and Population (HNP) Discussion Paper Series;. Washington, DC: The International Bank for Reconstruction and Development/The World Bank; 2014 (94043)

[171] Hay AJ, McCauley JW. The WHO global influenza surveillance and response system (GISRS)-a future perspective. Influenza Other Respir Viruses 2018; 12[phone]

[172] Hill EM, House T, Dhingra MS, et al. The impact of surveillance and control on highly pathogenic avian influenza outbreaks in poultry in Dhaka division, Bangladesh. PLOS Comput Biol 2018; 14(09) e1006439

[173] Kingstad-Bakke BA, Chandrasekar SS, Phanse Y, et al. Effective mosaic-based nanovaccines against avian influenza in poultry. Vaccine 2019; 37(35) 5051-5058

[174] Zhang F, Wang Y, Shang X, et al. Production of high-titer infectious influenza pseudotyped particles with envelope glycoproteins from highly pathogenic h5n1 and avian h7n9 viruses. J Vis Exp 2020; (155) e60663

[175] Wu X, Xiao L, Li L. Research progress on human infection with avian influenza H7N9. Front Med 2020; 14(01) 8-20

[176] Huang SW, Tai CH, Hsu YM, et al. Assessing the application of a pseudovirus system for emerging SARS-CoV-2 and re-emerging avian influenza virus H5 subtypes in vaccine development. Biomed J 2020; 43[phone]

RIGHTS & PERMISSIONS

Global Medical Genetics