{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T18:20:06Z","timestamp":1792174806786,"version":"4.4.0"},"reference-count":125,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T00:00:00Z","timestamp":1621468800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Bio &amp; Medical Technology Development Program of the National Research Foundation (NRF) and Korean govern-ment (MSIT)","award":["NRF-2018M3A9H4055193"],"award-info":[{"award-number":["NRF-2018M3A9H4055193"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Avian influenza is one of the largest known threats to domestic poultry. Influenza outbreaks on poultry farms typically lead to the complete slaughter of the entire domestic bird population, causing severe economic losses worldwide. Moreover, there are highly pathogenic avian influenza (HPAI) strains that are able to infect the swine or human population in addition to their primary avian host and, as such, have the potential of being a global zoonotic and pandemic threat. Migratory birds, especially waterfowl, are a natural reservoir of the avian influenza virus; they carry and exchange different virus strains along their migration routes, leading to antigenic drift and antigenic shift, which results in the emergence of novel HPAI viruses. This requires monitoring over time and in different locations to allow for the upkeep of relevant knowledge on avian influenza virus evolution and the prevention of novel epizootic and epidemic outbreaks. In this review, we assess the role of migratory birds in the spread and introduction of influenza strains on a global level, based on recent data. Our analysis sheds light on the details of viral dissemination linked to avian migration, the viral exchange between migratory waterfowl and domestic poultry, virus ecology in general, and viral evolution as a process tightly linked to bird migration. We also provide insight into methods used to detect and quantify avian influenza in the wild. This review may be beneficial for the influenza research community and may pave the way to novel strategies of avian influenza and HPAI zoonosis outbreak monitoring and prevention.<\/jats:p>","DOI":"10.3390\/pathogens10050630","type":"journal-article","created":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T06:13:45Z","timestamp":1621491225000},"page":"630","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":211,"title":["Avian Influenza in Wild Birds and Poultry: Dissemination Pathways, Monitoring Methods, and Virus Ecology"],"prefix":"10.3390","volume":"10","author":[{"given":"Artem","family":"Blagodatski","sequence":"first","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"},{"name":"Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences Pushchino, 142290 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4748-6362","authenticated-orcid":false,"given":"Kseniya","family":"Trutneva","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"},{"name":"Research Institute of Personalized Medicine, National Center for Personalized Medicine of Endocrine Diseases, The National Medical Research Center for Endocrinology, 117036 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga","family":"Glazova","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga","family":"Mityaeva","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liudmila","family":"Shevkova","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2638-0454","authenticated-orcid":false,"given":"Evgenii","family":"Kegeles","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nikita","family":"Onyanov","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kseniia","family":"Fede","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5780-1330","authenticated-orcid":false,"given":"Anna","family":"Maznina","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena","family":"Khavina","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seon-Ju","family":"Yeo","sequence":"additional","affiliation":[{"name":"Department of Tropical Medicine and Parasitology, College of Medicine, Seoul National University, Seoul 03080, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hyun","family":"Park","sequence":"additional","affiliation":[{"name":"Zoonosis Research Center, Department of Infection Biology, School of Medicine, Wonkwang University, Iksan 570-749, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pavel","family":"Volchkov","sequence":"additional","affiliation":[{"name":"Life Sciences Research Center, Moscow Institute of Physics and Technology, 141700 Dolgoprudniy, Russia"},{"name":"Research Institute of Personalized Medicine, National Center for Personalized Medicine of Endocrine Diseases, The National Medical Research Center for Endocrinology, 117036 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,5,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Liu, W.J., Wu, Y., Bi, Y., Shi, W., Wang, D., Shi, Y., and Gao, G.F. (2020). Emerging HxNy Influenza A Viruses. Cold Spring Harb. Perspect. Med.","DOI":"10.1101\/cshperspect.a038406"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1328","DOI":"10.3389\/fmicb.2019.01328","article-title":"Adaptive Evolution of Human-Isolated H5Nx Avian Influenza A Viruses","volume":"10","author":"Guo","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Kargarfard, F., Sami, A., Mohammadi-Dehcheshmeh, M., and Ebrahimie, E. (2016). Novel approach for identification of influenza virus host range and zoonotic transmissible sequences by determination of host-related associative positions in viral genome segments. BMC Genom., 17.","DOI":"10.1186\/s12864-016-3250-9"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/1297-9716-42-10","article-title":"Highly pathogenic or low pathogenic avian influenza virus subtype H7N1 infection in chicken lungs: Small differences in general acute responses","volume":"42","author":"Rebel","year":"2011","journal-title":"Vet. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1128\/CMR.14.1.129-149.2001","article-title":"Pandemic threat posed by avian influenza A viruses","volume":"14","author":"Horimoto","year":"2001","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1016\/S0140-6736(98)01182-9","article-title":"Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus","volume":"351","author":"Yuen","year":"1998","journal-title":"Lancet"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"E8","DOI":"10.1038\/nature04823","article-title":"Molecular virology: Was the 1918 pandemic caused by a bird flu?","volume":"440","author":"Gibbs","year":"2006","journal-title":"Nature"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1038\/nature04230","article-title":"Characterization of the 1918 influenza virus polymerase genes","volume":"437","author":"Taubenberger","year":"2005","journal-title":"Nature"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/j.antiviral.2013.02.013","article-title":"Antiviral resistance among highly pathogenic influenza A (H5N1) viruses isolated worldwide in 2002-2012 shows need for continued monitoring","volume":"98","author":"Govorkova","year":"2013","journal-title":"Antiviral. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"D65","DOI":"10.1016\/j.vaccine.2009.08.038","article-title":"Influenza vaccines","volume":"27","author":"Ellebedy","year":"2009","journal-title":"Vaccine"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1038\/39218","article-title":"A pandemic warning?","volume":"389","author":"Claas","year":"1997","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"S58","DOI":"10.1086\/338820","article-title":"Outbreak of avian influenza A(H5N1) virus infection in Hong Kong in 1997","volume":"34","author":"Chan","year":"2002","journal-title":"Clin. Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"70S","DOI":"10.1046\/j.1365-2672.94.s1.8.x","article-title":"The next influenza pandemic: Lessons from Hong Kong","volume":"94","author":"Shortridge","year":"2003","journal-title":"J. Appl. Microbiol."},{"key":"ref_14","unstructured":"Pavade, G., Weber-Vintze, L., Hamilton, K., Dehove, A., and Zepeda, C. (2021, April 29). OFFLU Review of Avian Influenza Surveillance and Epidemiological Projects in Some European, African, and Asian Countries. Available online: https:\/\/rr-africa.oie.int\/wp-content\/uploads\/2020\/02\/offlu_ai.pdf."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1016\/S1473-3099(17)30323-7","article-title":"Epidemiology of avian influenza A H7N9 virus in human beings across five epidemics in mainland China, 2013\u20132017: An epidemiological study of laboratory-confirmed case series","volume":"17","author":"Wang","year":"2017","journal-title":"Lancet Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1111\/irv.12412","article-title":"The ecology and adaptive evolution of influenza A interspecies transmission","volume":"11","author":"Joseph","year":"2017","journal-title":"Influenza Other Respir. Viruses"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1637\/7088","article-title":"Molecular characterization of low pathogenicity H7N3 avian influenza viruses isolated in Italy","volume":"48","author":"Bedini","year":"2004","journal-title":"Avian Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"693","DOI":"10.3201\/eid1004.030396","article-title":"Recombination resulting in virulence shift in avian influenza outbreak, Chile","volume":"10","author":"Suarez","year":"2004","journal-title":"Emerg. Infect. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2192","DOI":"10.3201\/eid1012.040743","article-title":"Novel avian influenza H7N3 strain outbreak, British Columbia","volume":"10","author":"Hirst","year":"2004","journal-title":"Emerg. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1126\/science.7063847","article-title":"Mass mortality of harbor seals: Pneumonia associated with influenza A virus","volume":"215","author":"Geraci","year":"1982","journal-title":"Science"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"9363","DOI":"10.1073\/pnas.96.16.9363","article-title":"Molecular characterization of H9N2 influenza viruses: Were they the donors of the \u201cinternal\u201d genes of H5N1 viruses in Hong Kong?","volume":"96","author":"Guan","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1016\/S0140-6736(99)03311-5","article-title":"Human infection with influenza H9N2","volume":"354","author":"Peiris","year":"1999","journal-title":"Lancet"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1093\/infdis\/jiv109","article-title":"A Systematic Review and Meta-Analysis of the Seroprevalence of Influenza A(H9N2) Infection Among Humans","volume":"212","author":"Khan","year":"2015","journal-title":"J. Infect. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4603","DOI":"10.1128\/jvi.63.11.4603-4608.1989","article-title":"Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics","volume":"63","author":"Kawaoka","year":"1989","journal-title":"J. Virol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"9436","DOI":"10.1038\/s41598-020-66343-9","article-title":"Protection of layers and breeders against homologous or heterologous HPAIv by vaccines from Korean national antigen bank","volume":"10","author":"Kang","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"European Food Safety Authority, European Centre for Disease Prevention and Control and European Union Reference Laboratory for Avian Influenza, Adlhoch, C., Fusaro, A., Kuiken, T., Niqueux, E., Staubach, C., Terregino, C., Guajardo, I.M., and Baldinelli, F. (2020). Avian influenza overview November 2019- February2020. EFSA J., 18, e06096.","DOI":"10.2903\/j.efsa.2020.6096"},{"key":"ref_27","unstructured":"Reuters (2021, May 19). South African Commercial Poultry Farm Hit by Avian Flu Outbreak. Available online: https:\/\/www.reuters.com\/article\/us-safrica-avian-flu\/south-african-commercial-poultry-farm-hit-by-avian-flu-outbreak-idUSKBN2C019V."},{"key":"ref_28","unstructured":"WHO (2021, April 29). Human Infection with Avian Influenza A(H5) Viruses. Available online: https:\/\/www.who.int\/docs\/default-source\/wpro---documents\/emergency\/surveillance\/avian-influenza\/ai-20210507.pdf?sfvrsn=30d65594_125#:~:text=To%20date%2C%20there%20is%20no,have%20serious%20public%20health%20impacts."},{"key":"ref_29","unstructured":"(2021, May 19). Human Infection with Avian Influenza A (H5N8)\u2014The Russian Federation. Available online: https:\/\/www.who.int\/csr\/don\/26-feb-2021-influenza-a-russian-federation\/en\/."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1128\/mr.56.1.152-179.1992","article-title":"Evolution and ecology of influenza A viruses","volume":"56","author":"Webster","year":"1992","journal-title":"Microbiol. Rev."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1128\/iai.30.2.547-553.1980","article-title":"Duck influenza lacking evidence of disease signs and immune response","volume":"30","author":"Kida","year":"1980","journal-title":"Infect. Immun."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1016\/0042-6822(78)90247-7","article-title":"Intestinal influenza: Replication and characterization of influenza viruses in ducks","volume":"84","author":"Webster","year":"1978","journal-title":"Virology"},{"key":"ref_33","first-page":"20201680","article-title":"Influenza A viruses remain infectious for more than seven months in northern wetlands of North America","volume":"287","author":"Ramey","year":"2020","journal-title":"Proc. Biol. Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2986","DOI":"10.1038\/s41596-019-0210-2","article-title":"SHERLOCK: Nucleic acid detection with CRISPR nucleases","volume":"14","author":"Kellner","year":"2019","journal-title":"Nat. Protoc."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1159\/000334691","article-title":"Role of water fleas (Daphnia magna) in the accumulation of avian influenza viruses from the surrounding water","volume":"55","author":"Abbas","year":"2012","journal-title":"Intervirology"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7249","DOI":"10.1128\/AEM.02439-13","article-title":"Accumulation and inactivation of avian influenza virus by the filter-feeding invertebrate Daphnia magna","volume":"79","author":"Meixell","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"911","DOI":"10.7589\/2012-04-111","article-title":"Failure of transmission of low-pathogenic avian influenza virus between Mallards and freshwater snails: An experimental evaluation","volume":"49","author":"Oesterle","year":"2013","journal-title":"J. Wildl. Dis."},{"key":"ref_38","first-page":"3727","article-title":"Filter-feeding bivalves can remove avian influenza viruses from water and reduce infectivity","volume":"276","author":"Faust","year":"2009","journal-title":"Proc. Biol. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1637\/9162-111709-Reg.1","article-title":"Accumulation of a low pathogenic avian influenza virus in zebra mussels (Dreissena polymorpha)","volume":"54","author":"Stumpf","year":"2010","journal-title":"Avian Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1111\/zph.12688","article-title":"Effects of freshwater crayfish on influenza A virus persistence in water","volume":"67","author":"Root","year":"2020","journal-title":"Zoonoses Public Health"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e124","DOI":"10.1111\/zph.12420","article-title":"Survivability of low pathogenic (H9N2) avian influenza virus in water in the presence of Atyopsis moluccensis (Bamboo shrimp)","volume":"65","author":"Pathak","year":"2018","journal-title":"Zoonoses Public Health"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"17744","DOI":"10.1016\/S0021-9258(18)45442-7","article-title":"Effects of low pH on influenza virus. Activation and inactivation of the membrane fusion capacity of the hemagglutinin","volume":"262","author":"Stegmann","year":"1987","journal-title":"J. Biol. Chem."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Dalziel, A.E., Delean, S., Heinrich, S., and Cassey, P. (2016). Persistence of Low Pathogenic Influenza A Virus in Water: A Systematic Review and Quantitative Meta-Analysis. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0168789"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1007\/s12560-017-9323-3","article-title":"Morphological and Biochemical Characteristics of Avian Faecal Droppings and Their Impact on Survival of Avian Influenza Virus","volume":"10","author":"Pawar","year":"2018","journal-title":"Food Environ. Virol."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Schmitz, A., Pertusa, M., Le Bouquin, S., Rousset, N., Ogor, K., LeBras, M.O., Martenot, C., Daniel, P., Belen Cepeda Hontecillas, A., and Scoizec, A. (2020). Natural and Experimental Persistence of Highly Pathogenic H5 Influenza Viruses in Slurry of Domestic Ducks, with or without Lime Treatment. Appl. Environ. Microbiol., 86.","DOI":"10.1128\/AEM.02288-20"},{"key":"ref_46","unstructured":"Sendor, A.B., Weerasuriya, D., and Sapra, A. (2021). Avian Influenza, StatPearls. NBK553072."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0378-1135(00)00161-9","article-title":"Evolution of avian influenza viruses","volume":"74","author":"Suarez","year":"2000","journal-title":"Vet. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"512","DOI":"10.7589\/0090-3558-45.2.512","article-title":"Active surveillance for avian influenza virus infection in wild birds by analysis of avian fecal samples from the environment","volume":"45","author":"Pannwitz","year":"2009","journal-title":"J. Wildl. Dis."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Ruiz, S., Jimenez-Bluhm, P., Di Pillo, F., Baumberger, C., Galdames, P., Marambio, V., Salazar, C., Mattar, C., Sanhueza, J., and Schultz-Cherry, S. (2020). Temporal dynamics and the influence of environmental variables on the prevalence of avian influenza virus in main wetlands in central Chile. Transbound. Emerg. Dis.","DOI":"10.1111\/tbed.13831"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s13567-019-0623-5","article-title":"Long-term avian influenza virus epidemiology in a small Spanish wetland ecosystem is driven by the breeding Anseriformes community","volume":"50","author":"Torrontegi","year":"2019","journal-title":"Vet. Res."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"P\u00e9rez-Ram\u00edrez, E., Acevedo, P., Allepuz, A., Gerrikagoitia, X., Alba, A., Busquets, N., D\u00edaz-S\u00e1nchez, S., \u00c1lvarez, V., Abad, F.X., and Barral, M. (2012). Ecological factors driving avian influenza virus dynamics in Spanish wetland ecosystems. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0046418"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1186\/s13567-016-0308-2","article-title":"Avian influenza infection dynamics under variable climatic conditions, viral prevalence is rainfall driven in waterfowl from temperate, south-east Australia","volume":"47","author":"Ferenczi","year":"2016","journal-title":"Vet. Res."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Reeves, A.B., Hall, J.S., Poulson, R.L., Donnelly, T., Stallknecht, D.E., and Ramey, A.M. (2018). Influenza A virus recovery, diversity, and intercontinental exchange: A multi-year assessment of wild bird sampling at Izembek National Wildlife Refuge, Alaska. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0195327"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1007\/s11262-020-01764-2","article-title":"Genetic and antigenic characterization of H5 and H7 avian influenza viruses isolated from migratory waterfowl in Mongolia from 2017 to 2019","volume":"56","author":"Ulaankhuu","year":"2020","journal-title":"Virus Genes"},{"key":"ref_55","unstructured":"(2021, May 19). Avian Influenza (Infection with Avian Influenza Viruses). Available online: https:\/\/www.oie.int\/fileadmin\/Home\/eng\/Health_standards\/tahm\/3.03.04_AI.pdf."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Le, T.B., Kim, H.K., Na, W., Le, V.P., Song, M.S., Song, D., Jeong, D.G., and Yoon, S.W. (2020). Development of a Multiplex RT-qPCR for the Detection of Different Clades of Avian Influenza in Poultry. Viruses, 12.","DOI":"10.3390\/v12010100"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"3256","DOI":"10.1128\/JCM.40.9.3256-3260.2002","article-title":"Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes","volume":"40","author":"Spackman","year":"2002","journal-title":"J. Clin. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1769","DOI":"10.1128\/JCM.02204-07","article-title":"Development and validation of a one-step real-time PCR assay for simultaneous detection of subtype H5, H7, and H9 avian influenza viruses","volume":"46","author":"Monne","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1637\/7674-063006R1.1","article-title":"Identification of sensitive and specific avian influenza polymerase chain reaction methods through blind ring trials organized in the European Union","volume":"51","author":"Slomka","year":"2007","journal-title":"Avian Dis."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1177\/104063870802000512","article-title":"Analytical validation of a real-time reverse transcription polymerase chain reaction test for Pan-American lineage H7 subtype Avian influenza viruses","volume":"20","author":"Spackman","year":"2008","journal-title":"J. Vet. Diagn. Invest."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"8441","DOI":"10.1038\/s41598-020-64003-6","article-title":"Detection of avian influenza virus: A comparative study of the in silico and in vitro performances of current RT-qPCR assays","volume":"10","author":"Laconi","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s12985-015-0250-3","article-title":"Detection of highly pathogenic zoonotic influenza virus H5N6 by reverse-transcriptase quantitative polymerase chain reaction","volume":"12","author":"Heine","year":"2015","journal-title":"Virol. J."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"27211","DOI":"10.1038\/srep27211","article-title":"Riems influenza a typing array (RITA): An RT-qPCR-based low density array for subtyping avian and mammalian influenza a viruses","volume":"6","author":"Hoffmann","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Hassan, M.M., El Zowalaty, M.E., Islam, A., Khan, S.A., Rahman, M.K., J\u00e4rhult, J.D., and Hoque, M.A. (2020). Prevalence and Diversity of Avian Influenza Virus Hemagglutinin Sero-Subtypes in Poultry and Wild Birds in Bangladesh. Vet. Sci., 7.","DOI":"10.3390\/vetsci7020073"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"425051","DOI":"10.1155\/2014\/425051","article-title":"Comparison of a new gold immunochromatographic assay for the rapid diagnosis of the novel influenza A (H7N9) virus with cell culture and a real-time reverse-transcription PCR assay","volume":"2014","author":"Jin","year":"2014","journal-title":"Biomed. Res. Int."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.7150\/thno.10255","article-title":"Rapid and quantitative detection of zoonotic influenza A virus infection utilizing coumarin-derived dendrimer-based fluorescent immunochromatographic strip test (FICT)","volume":"4","author":"Yeo","year":"2014","journal-title":"Theranostics"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"7933","DOI":"10.1038\/s41598-017-08328-9","article-title":"Improvement of a rapid diagnostic application of monoclonal antibodies against avian influenza H7 subtype virus using Europium nanoparticles","volume":"7","author":"Yeo","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1835","DOI":"10.7150\/thno.18857","article-title":"Rapid Detection of Avian Influenza Virus by Fluorescent Diagnostic Assay using an Epitope-Derived Peptide","volume":"7","author":"Bao","year":"2017","journal-title":"Theranostics"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1016\/j.bios.2017.03.068","article-title":"Rapid detection of avian influenza A virus by immunochromatographic test using a novel fluorescent dye","volume":"94","author":"Yeo","year":"2017","journal-title":"Biosens Bioelectron"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"231","DOI":"10.7150\/thno.14023","article-title":"Smartphone-Based Fluorescent Diagnostic System for Highly Pathogenic H5N1 Viruses","volume":"6","author":"Yeo","year":"2016","journal-title":"Theranostics"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2249","DOI":"10.1007\/s00705-016-2922-8","article-title":"Evaluation of a smartphone-based rapid fluorescent diagnostic system for H9N2 virus in specific-pathogen-free chickens","volume":"161","author":"Yeo","year":"2016","journal-title":"Arch. Virol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"6132","DOI":"10.7150\/thno.28027","article-title":"Development of a smartphone-based rapid dual fluorescent diagnostic system for the simultaneous detection of influenza A and H5 subtype in avian influenza A-infected patients","volume":"8","author":"Yeo","year":"2018","journal-title":"Theranostics"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1021\/acs.analchem.0c03153","article-title":"A Size-Selectively Biomolecule-Immobilized Nanoprobe-Based Chemiluminescent Lateral Flow Immunoassay for Detection of Avian-Origin Viruses","volume":"93","author":"Jung","year":"2021","journal-title":"Anal. Chem."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1038\/s41586-020-2279-8","article-title":"Massively multiplexed nucleic acid detection with Cas13","volume":"582","author":"Ackerman","year":"2020","journal-title":"Nature"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1126\/science.aas8836","article-title":"Field-deployable viral diagnostics using CRISPR-Cas13","volume":"360","author":"Myhrvold","year":"2018","journal-title":"Science"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1896","DOI":"10.3201\/eid1612.100776","article-title":"Surveillance and analysis of avian influenza viruses, Australia","volume":"16","author":"Hansbro","year":"2010","journal-title":"Emerg. Infect. Dis."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Verhagen, J.H., van der Jeugd, H.P., Nolet, B.A., Slaterus, R., Kharitonov, S.P., de Vries, P.P., Vuong, O., Majoor, F., Kuiken, T., and Fouchier, R.A. (2015). Wild bird surveillance around outbreaks of highly pathogenic avian influenza A(H5N8) virus in the Netherlands, 2014, within the context of global flyways. Euro. Surveill., 20.","DOI":"10.2807\/1560-7917.ES2015.20.12.21069"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"412","DOI":"10.2307\/1591429","article-title":"Effects of pH, temperature, and salinity on persistence of avian influenza viruses in water","volume":"34","author":"Stallknecht","year":"1990","journal-title":"Avian Dis."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1089\/vbz.2009.0240","article-title":"Bird migration and risk for H5N1 transmission into Qinghai Lake, China","volume":"11","author":"Cui","year":"2011","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.virol.2017.02.009","article-title":"Diversity, evolution and population dynamics of avian influenza viruses circulating in the live poultry markets in China","volume":"505","author":"Chen","year":"2017","journal-title":"Virology"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Fourment, M., Darling, A.E., and Holmes, E.C. (2017). The impact of migratory flyways on the spread of avian influenza virus in North America. BMC Evol. Biol., 17.","DOI":"10.1186\/s12862-017-0965-4"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1080\/01652176.2019.1697013","article-title":"Role for migratory domestic poultry and\/or wild birds in the global spread of avian influenza?","volume":"39","year":"2019","journal-title":"Vet. Q."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1007\/s11262-008-0248-7","article-title":"Phylogenic analysis of the M genes of influenza viruses isolated from free-flying water birds from their Northern Territory to Hokkaido, Japan","volume":"37","author":"Manzoor","year":"2008","journal-title":"Virus Genes"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/s11262-015-1214-9","article-title":"Genetic and antigenic characterization of H5 and H7 influenza viruses isolated from migratory water birds in Hokkaido, Japan and Mongolia from 2010 to 2014","volume":"51","author":"Hiono","year":"2015","journal-title":"Virus Genes"},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Diskin, E.R., Friedman, K., Krauss, S., Nolting, J.M., Poulson, R.L., Slemons, R.D., Stallknecht, D.E., Webster, R.G., and Bowman, A.S. (2020). Subtype Diversity of Influenza A Virus in North American Waterfowl: A Multidecade Study. J. Virol., 94.","DOI":"10.1128\/JVI.02022-19"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1637\/8914-043009-Reg.1","article-title":"Migration of waterfowl in the East Asian flyway and spatial relationship to HPAI H5N1 outbreaks","volume":"54","author":"Takekawa","year":"2010","journal-title":"Avian Dis."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"5986","DOI":"10.1111\/j.1365-294X.2012.05735.x","article-title":"Migration strategy affects avian influenza dynamics in mallards (Anas platyrhynchos)","volume":"21","author":"Hill","year":"2012","journal-title":"Mol. Ecol."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Sullivan, J., Takekawa, J., Spragens, K., Newman, S., Xiao, X., Leader, P., Smith, B., and Prosser, D. (2018). Waterfowl Spring Migratory Behavior and Avian Influenza Transmission Risk in the Changing Landscape of the East Asian-Australasian Flyway. Front. Ecol. Evol., 6.","DOI":"10.3389\/fevo.2018.00206"},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Global Consortium for H5N8 and Related Influenza Viruses (2016). Role for migratory wild birds in the global spread of avian influenza H5N8. Science, 354, 213\u2013217.","DOI":"10.1126\/science.aaf8852"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.tvjl.2010.12.022","article-title":"Implications of global and regional patterns of highly pathogenic avian influenza virus H5N1 clades for risk management","volume":"190","author":"Pfeiffer","year":"2011","journal-title":"Vet. J."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"30262","DOI":"10.1038\/srep30262","article-title":"Southward autumn migration of waterfowl facilitates cross-continental transmission of the highly pathogenic avian influenza H5N1 virus","volume":"6","author":"Xu","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"e1060","DOI":"10.1002\/mbo3.1060","article-title":"Isolation of two novel reassortant H3N6 avian influenza viruses from long-distance migratory birds in Jiangxi Province, China","volume":"9","author":"Li","year":"2020","journal-title":"Microbiologyopen"},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Yeo, S.J., Than, D.D., Park, H.S., Sung, H.W., and Park, H. (2019). Molecular Characterization of a Novel Avian Influenza A (H2N9) Strain Isolated from Wild Duck in Korea in 2018. Viruses, 11.","DOI":"10.3390\/v11111046"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.ecolind.2014.04.027","article-title":"Bird Migration and Avian Influenza: A Comparison of Hydrogen Stable Isotopes and Satellite Tracking Methods","volume":"45","author":"Bridge","year":"2014","journal-title":"Ecol. Indic."},{"key":"ref_95","unstructured":"(2021, May 19). Influenza Research Databaise (IRD). Available online: https:\/\/www.fludb.org."},{"key":"ref_96","unstructured":"(2021, May 19). OpenFlu. Available online: http:\/\/openflu.vital-it.ch."},{"key":"ref_97","unstructured":"(2021, May 19). EMPRES-i. Available online: https:\/\/empres-i.review.fao.org."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1186\/s40249-018-0480-x","article-title":"Identifying key bird species and geographical hotspots of avian influenza A (H7N9) virus in China","volume":"7","author":"Shi","year":"2018","journal-title":"Infect. Dis. Poverty"},{"key":"ref_99","unstructured":"(2021, May 19). Human Infection with Avian Influenza A(H7N9) Virus. Available online: https:\/\/www.who.int\/csr\/don\/17-january-2017-ah7n9-china\/en\/."},{"key":"ref_100","doi-asserted-by":"crossref","unstructured":"Venkatesh, D., Poen, M.J., Bestebroer, T.M., Scheuer, R.D., Vuong, O., Chkhaidze, M., Machablishvili, A., Mamuchadze, J., Ninua, L., and Fedorova, N.B. (2018). Avian Influenza Viruses in Wild Birds: Virus Evolution in a Multihost Ecosystem. J. Virol., 92.","DOI":"10.1128\/JVI.00433-18"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.3201\/eid1308.070319","article-title":"Ecologic immunology of avian influenza (H5N1) in migratory birds","volume":"13","author":"Weber","year":"2007","journal-title":"Emerg. Infect. Dis."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1637\/0005-2086-64.2.135","article-title":"High Prevalence of Avian Influenza Virus Among Wild Waterbirds and Land Birds of Mexico","volume":"64","year":"2020","journal-title":"Avian Dis."},{"key":"ref_103","unstructured":"(2021, May 19). GISAID. Available online: https:\/\/www.gisaid.org."},{"key":"ref_104","unstructured":"(2021, May 19). H5N8 Highly Pathogenic Avian Influenza (HPAI) of Clade 2.3.4.4 Detected through Surveillance of Wild Migratory Birds in the Tyva Republic, the Russian Federation\u2014Potential for International Spread. Available online: http:\/\/www.fao.org\/3\/i6113e\/i6113e.pdf."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"20814","DOI":"10.1073\/pnas.2001813117","article-title":"Genesis and spread of multiple reassortants during the 2016\/2017 H5 avian influenza epidemic in Eurasia","volume":"117","author":"Lycett","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1186\/s13567-020-00841-6","article-title":"Enterotropism of highly pathogenic avian influenza virus H5N8 from the 2016\/2017 epidemic in some wild bird species","volume":"51","author":"Caliendo","year":"2020","journal-title":"Vet. Res."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"5310","DOI":"10.1038\/s41467-019-13287-y","article-title":"Disentangling the role of Africa in the global spread of H5 highly pathogenic avian influenza","volume":"10","author":"Fusaro","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"2592","DOI":"10.1038\/s41598-020-59077-1","article-title":"Waterfowl occurrence and residence time as indicators of H5 and H7 avian influenza in North American Poultry","volume":"10","author":"Humphreys","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1111\/tbed.13595","article-title":"Association of wild bird densities around poultry farms with the risk of highly pathogenic avian influenza virus subtype H5N8 outbreaks in the Netherlands, 2016","volume":"68","author":"Velkers","year":"2021","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"2175","DOI":"10.1038\/srep02175","article-title":"Modeling highly pathogenic avian influenza transmission in wild birds and poultry in West Bengal, India","volume":"3","author":"Pandit","year":"2013","journal-title":"Sci. Rep."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"2229","DOI":"10.3382\/ps.2011-01524","article-title":"Genetic analyses of avian influenza viruses in Mongolia, 2007 to 2009, and their relationships with Korean isolates from domestic poultry and wild birds","volume":"90","author":"Kang","year":"2011","journal-title":"Poult. Sci."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"5949","DOI":"10.1073\/pnas.1906954117","article-title":"Assessing the role of live poultry trade in community-structured transmission of avian influenza in China","volume":"117","author":"Yang","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"11755","DOI":"10.1038\/s41598-019-47788-z","article-title":"Airborne transmission may have played a role in the spread of 2015 highly pathogenic avian influenza outbreaks in the United States","volume":"9","author":"Zhao","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1080\/22221751.2020.1764396","article-title":"Mammalian pathogenicity and transmissibility of low pathogenic avian influenza H7N1 and H7N3 viruses isolated from North America in 2018","volume":"9","author":"Belser","year":"2020","journal-title":"Emerg. Microbes Infect."},{"key":"ref_115","doi-asserted-by":"crossref","unstructured":"Staller, E., Sheppard, C.M., Neasham, P.J., Mistry, B., Peacock, T.P., Goldhill, D.H., Long, J.S., and Barclay, W.S. (2019). ANP32 Proteins Are Essential for Influenza Virus Replication in Human Cells. J. Virol., 93.","DOI":"10.1128\/JVI.00217-19"},{"key":"ref_116","doi-asserted-by":"crossref","unstructured":"Long, J.S., Idoko-Akoh, A., Mistry, B., Goldhill, D., Staller, E., Schreyer, J., Ross, C., Goodbourn, S., Shelton, H., and Skinner, M.A. (2019). Species specific differences in use of ANP32 proteins by influenza A virus. Elife, 8.","DOI":"10.7554\/eLife.45066"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1093\/infdis\/jiz506","article-title":"Host-Specific Restriction of Avian Influenza Virus Caused by Differential Dynamics of ANP32 Family Members","volume":"221","author":"Park","year":"2020","journal-title":"J. Infect. Dis."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"17204","DOI":"10.1073\/pnas.1921186117","article-title":"Prevalent Eurasian avian-like H1N1 swine influenza virus with 2009 pandemic viral genes facilitating human infection","volume":"117","author":"Sun","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_119","doi-asserted-by":"crossref","unstructured":"Eng, C.L., Tong, J.C., and Tan, T.W. (2016). Distinct Host Tropism Protein Signatures to Identify Possible Zoonotic Influenza A Viruses. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0150173"},{"key":"ref_120","doi-asserted-by":"crossref","unstructured":"Eng, C.L.P., Tong, J.C., and Tan, T.W. (2017). Predicting Zoonotic Risk of Influenza A Viruses from Host Tropism Protein Signature Using Random Forest. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18061135"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1089\/hs.2019.0055","article-title":"Predicting Influenza A Tropism with End-to-End Learning of Deep Networks","volume":"17","author":"Scarafoni","year":"2019","journal-title":"Health Secur."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"1224","DOI":"10.1093\/molbev\/msz276","article-title":"Machine Learning Methods for Predicting Human-Adaptive Influenza A Viruses Based on Viral Nucleotide Compositions","volume":"37","author":"Li","year":"2020","journal-title":"Mol. Biol. Evol."},{"key":"ref_123","doi-asserted-by":"crossref","unstructured":"Yin, R., Zhou, X., Rashid, S., and Kwoh, C.K. (2020). HopPER: An adaptive model for probability estimation of influenza reassortment through host prediction. BMC Med. Genom., 13.","DOI":"10.1186\/s12920-019-0656-7"},{"key":"ref_124","unstructured":"World Health Organization (2017). Regional Office for Africa, Health Emergencies Programme. Influenza Virological Surveillance in the WHO African Region: Epidemiological Week 43, October 23 to 29. Influenza Virological Surveillance in the WHO African Region, World Health Organization."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1111\/irv.12724","article-title":"Human surveillance and phylogeny of highly pathogenic avian influenza A(H5N8) during an outbreak in poultry in South Africa, 2017","volume":"14","author":"Cloete","year":"2020","journal-title":"Influenza Other Respir. Viruses"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/5\/630\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:04:32Z","timestamp":1760162672000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/5\/630"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,20]]},"references-count":125,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["pathogens10050630"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10050630","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,20]]}}}