Skip to main content
EFSA Journal logoLink to EFSA Journal
. 2022 Aug 6;20(8):e07415. doi: 10.2903/j.efsa.2022.7415

Avian influenza overview March – June 2022

European Food Safety Authority; European Centre for Disease Prevention and Control; European Union Reference Laboratory for Avian Influenza, Cornelia Adlhoch, Alice Fusaro, José L Gonzales, Thijs Kuiken, Stefano Marangon, Éric Niqueux, Christoph Staubach, Calogero Terregino, Inma Aznar, Irene Muñoz Guajardo, Francesca Baldinelli
PMCID: PMC9356771  PMID: 35949938

Abstract

The 2021–2022 highly pathogenic avian influenza (HPAI) epidemic season is the largest epidemic so far observed in Europe, with a total of 2,398 outbreaks in poultry, 46 million birds culled in the affected establishments, 168 detections in captive birds, and 2,733 HPAI events in wild birds in 36 European countries. Between 16 March and 10 June 2022, 1,182 HPAI virus detections were reported in 28 EU/EEA countries and United Kingdom in poultry (750), and in wild (410) and captive birds (22). During this reporting period, 86% of the poultry outbreaks were secondary due to between‐farm spread of HPAI virus. France accounted for 68% of the overall poultry outbreaks, Hungary for 24% and all other affected countries for less than 2% each. Most detections in wild birds were reported by Germany (158), followed by the Netherlands (98) and the United Kingdom (48). The observed persistence of HPAI (H5) virus in wild birds since the 2020–2021 epidemic wave indicates that it may have become endemic in wild bird populations in Europe, implying that the health risk from HPAI A(H5) for poultry, humans, and wildlife in Europe remains present year‐round, with the highest risk in the autumn and winter months. Response options to this new epidemiological situation include the definition and the rapid implementation of suitable and sustainable HPAI mitigation strategies such as appropriate biosecurity measures and surveillance strategies for early detection measures in the different poultry production systems. Medium to long‐term strategies for reducing poultry density in high‐risk areas should also be considered. The results of the genetic analysis indicate that the viruses currently circulating in Europe belong to clade 2.3.4.4b. HPAI A(H5) viruses were also detected in wild mammal species in Canada, USA and Japan, and showed genetic markers of adaptation to replication in mammals. Since the last report, four A(H5N6), two A(H9N2) and two A(H3N8) human infections were reported in China and one A(H5N1) in USA. The risk of infection is assessed as low for the general population in the EU/EEA, and low to medium for occupationally exposed people.

Keywords: avian influenza, captive birds, HPAI/LPAI, humans, monitoring, poultry, wild birds

Suggested citation: EFSA (European Food Safety Authority), ECDC (European Centre for Disease Prevention and Control), EURL (European Reference Laboratory for Avian Influenza) , Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Marangon S, Niqueux É, Staubach C, Terregino C, Aznar I, Muñoz Guajardo I and Baldinelli F, 2022. Scientific report: Avian influenza overview March–June 2022. EFSA Journal 2022;20(8):7415, 67 pp. 10.2903/j.efsa.2022.7415

Requestor: European Commission

Question number: EFSA‐Q‐2022‐00300

Acknowledgements: In addition to the listed authors, EFSA, ECDC and the EURL wish to thank the following: Member State representatives who provided epidemiological data on avian influenza outbreaks or shared sequence data: Lika Aldin and Tana Kika (Albania), Eveline Wodakand and Sandra Revilla‐Fernandez (Austria), Ingeborg Mertens and Mieke Steensels (Belgium), Aleksandra Miteva and Gabriela Goujgoulova (Bulgaria), Lucie Kalášková and Alexander Nagy (Czechia), Vladimir Savic (Croatia), Charlotte Kristiane Hjulsager (Denmark), Imbi Nurmoja (Estonia), Niina Tammiranta (Finland), Béatrice Grasland, Audrey Schmitz, Karen Bucher, François‐Xavier Briand, Anne Van de Wiele, Andrea Jimenez Pellicer, Séverine Rautureau Célia Locquet and (France), Franz Conraths, Christoph Staubach and Timm Harder (Germany), George Georgiades (Greece), Georgina Helyes, Bálint Ádám and Malik Péter (Hungary), Laura Garza Cuartero (Ireland), Auður Lilja Arnþórsdóttir and Brigitte Brugger (Iceland), Scolamacchia Francesca, Dorotea Tiziano, Fornasiero Diletta, Mulatti Paolo, Bianca Zecchin and Isabella Monne (Italy), Sadik Heta, Bafti Murati, Armend Cana, Kujtim Uka and Xhavit Merovci (Kosovo), Chantal Snoeck (Luxembourg), Oxana Groza and Vitalie Caraus (Moldova) Michael McMenamy (United kingdom (Northern Ireland)), Britt Gjerset and Silje Granstad (Norway), Magdalena Gawędzka, Aleksandra Podrażka, Krzysztof Śmietanka and Edyta Swieton (Poland), Margarida Duarte (Portugal), Marcel Spierenburg, Dennis Bol and Nancy Beerens (The Netherlands), Onita Iuliana, Ioana Neghirla and Flavius Prelipcean (Romania), Martin Chudy and Vilem Kopriva (Slovakia), Brigita Slavec (Slovenia), Elena García Villacieros, Luis José Romero Gonzalez, Germán Cáceres Garrido and Azucena Sánchez Sánchez (Spain), Siamak Zohari, (Sweden); Ian Brown from the Animal and Plant Health Agency (United Kingdom); Ilya Chvala from Federal Center for Animal Health (FGBI ‘ARRIAH’, Russia); Camille Delavenne from AUSVET Europe for conducting the data analysis under the contract OC/EFSA/ALPHA/2021/02; Paolo Tizzani from WOAH for the support provided with WAHIS data; Paolo Calistri and Karl Stahl from the EFSA AHAW Panel for reviewing the report; Grazina Mirinaviciute and Edoardo Colzani from ECDC, Linnea Lindgren Kero and Gina Cioacata from EFSA for the support provided to this scientific output; we gratefully acknowledge the authors, originating and submitting laboratories of the sequences from GISAID’s EpiFlu™ Database, which is used for this assessment.

Note: Kosovo – this designation is without prejudice to positions on status and is in line with United Nations Security Council Resolution 1244 and the International Court of Justice Opinion on the Kosovo Declaration of Independence.

Figures 1–15, 17, 19 and Tables 1, 2 and 3 © EFSA; Figures 16, 18, 20–22 © ECDC.

Approved: 30 June 2022

This article was originally published on the EFSA website www.efsa.europa.eu on 30 June 2022 as part of EFSA's urgent publication procedures.

References

  1. Adlhoch C, Baldinelli F, Fusaro A and Terregino C, 2021. Avian influenza, a new threat to public health in Europe Clin Microbiol Infect. doi: 10.1016/j.cmi.2021.11.005 [DOI] [PubMed] [Google Scholar]
  2. AEWA (Agreement on the Conservation of African‐Eurasian Migratory Waterbirds) , online. Avian Influenza Continues to Impact Wild Migratory Birds: The Case of Prespa National Park. Available online: https://www.unep-aewa.org/en/news/avian-influenza-continues-impact-wild-migratory-birds-case-prespa-national-park [Accessed: 29 June 2022].
  3. Ärzteblatt D, online. Bird flu virus detected in dead seals. Available online: https://www.aerzteblatt.de/nachrichten/127460/Vogelgrippevirus-bei-toten-Seehunden-nachgewiesen [Accessed: 29 September 2021].
  4. Avian Flu Diary , online. Two Reports On HPAI H5N8 Infecting Marine Mammals (Denmark & Germany). Available online: https://afludiary.blogspot.com/2022/02/two-reports-on-hpai-h5n8-infecting.html [Accessed: 29 June 2022].
  5. Awuni JA, Bianco A, Dogbey OJ, Fusaro A, Yingar DT, Salviato A, Ababio PT, Milani A, Bonfante F and Monne I, 2019. Avian influenza H9N2 subtype in Ghana: virus characterization and evidence of co‐infection. Avian Pathology, 48, 470–476. 10.1080/03079457.2019.1624687 [DOI] [PubMed] [Google Scholar]
  6. BBC , online. Avian flu hits world's largest gannet colony on Bass Rock. Available online: https://www.bbc.com/news/uk-scotland-edinburgh-east-fife-61829551 [Accessed: 29 June 2022].
  7. Beerens N, Germeraad EA, Venema S, Verheij E, Pritz‐Verschuren SBE and Gonzales JL, 2021. Comparative pathogenicity and environmental transmission of recent highly pathogenic avian influenza H5 viruses. Emerg Microbes Infect, 10, 97–108. 10.1080/22221751.2020.1868274 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bevins SN, Shriner SA, Cumbee JC Jr, Dilione KE, Douglass KE, Ellis JW, Killian ML, Torchetti MK and Lenoch JB, 2022. Intercontinental Movement of Highly Pathogenic Avian Influenza A(H5N1) Clade 2.3.4.4 Virus to the United States, 2021. Emerg Infect Dis, 28, 1006–1011. 10.3201/eid2805.220318 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. BNO , online. China reports 2 new human cases of H5N6 bird flu. Available online: https://bnonews.com/index.php/2022/04/china-reports-2-new-human-cases-of-h5n6-bird-flu-2/ [Accessed: 29 June 2022].
  10. Bonfante F, Mazzetto E, Zanardello C, Fortin A, Gobbo F, Maniero S, Bigolaro M, Davidson I, Haddas R, Cattoli G and Terregino C, 2018. A G1‐lineage H9N2 virus with oviduct tropism causes chronic pathological changes in the infundibulum and a long‐lasting drop in egg production. Veterinary Research, 49, 83. 10.1186/s13567-018-0575-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Caliendo V, Mensink M, Begeman L, Embregts C, de Vrijer M, De Baerdemaeker A, Scheuer R, Vuong O, Fouchier RAM and Kuiken T, 2022. Highly Pathogenic Avian Influenza Virus (H5n8) Outbreak in a Wild Bird Rescue Center, the Netherlands: Consequences and Recommendations. J Zoo Wildl Med, 53, 41–49. 10.1638/2021-0083 [DOI] [PubMed] [Google Scholar]
  12. CBS 58 News , online. Avian flu detected in Utah foxes, marking 1st mammal cases in statee. Available online: https://www.cbs58.com/news/avian-flu-detected-in-utah-foxes-marking-1st-mammal-cases-in-state [Accessed: 29 June 2022].
  13. CDC (Centers for Disease Control and Prevention) , online‐a. Summary of Influenza Risk Assessment Tool (IRAT) Results. Available online: https://www.cdc.gov/flu/pandemic-resources/monitoring/irat-virus-summaries.htm?CDC_AA_refVal=https%3A%2F%2Fwww.cdc.gov%2Fflu%2Fpandemic-resources%2Ftools%2Firat-virus-summaries.htm#H5N8clade [Accessed: 29 June 2022a].
  14. CDC (Centers for Disease Control and Prevention) , online‐b. Update on A(H5N6) Bird Flu: How is the U.S. CDC Monitoring A(H5N6) Infections and Contributing to Global Pandemic Preparedness? Available online: https://www.cdc.gov/flu/spotlights/2021-2022/H5N6.htm [Accessed: 29 June 2022b].
  15. CDC (Centers for Disease Control and Prevention) , online‐c. Recent Bird Flu Infections in U.S. Wild Birds and Poultry Pose a Low Risk to the Public. Available online: https://www.cdc.gov/flu/avianflu/spotlights/2021-2022/bird-flu-poses-low-risk-public.htm [Accessed: 29 June 2022c].
  16. CDC (Centers for Disease Control and Prevention) , online‐d. March 7, 2022d. Update: H5N1 Bird Flu Poses Low Risk to the Public. Available online: https://www.cdc.gov/flu/avianflu/spotlights/2021-2022/h5n1-low-risk-public.htm?web=1&wdLOR=c187C9BEB-C6F3-4E38-80C1-CDE7B987F389 [Accessed: 29 June 2022]. [Google Scholar]
  17. CDC (Centers for Disease Control and Prevention) , online‐e. Highly Pathogenic Avian Influenza A(H5N1) Virus: Recommendations for Human Health Investigations and Response. Available online: https://emergency.cdc.gov/han/2022/han00464.asp?ACSTrackingID=USCDC_511-DM81097&ACSTrackingLabel=HAN%20464%20-%20General%20Public&deliveryName=USCDC_511-DM81097 [Accessed: 29 June 2022e].
  18. CDC (Centers for Disease Control and Prevention) , online‐f. Past Reported Global Human Cases with Highly Pathogenic Avian Influenza A(H5N1) (HPAI H5N1) by Country, 1997‐2022. Available online: https://www.cdc.gov/flu/avianflu/chart-epi-curve-ah5n1.html [Accessed: 29 June 2022f].
  19. Chinese National Influenza Center, WHO Collaborating Center for Reference and Research on Influenza and National Institute for Viral Disease Control and Prevention China , 2018. Chinese Influenza Weekly Report week 44, 2018. 6 pp. Available online: http://www.chinaivdc.cn/cnic/en/Surveillance/WeeklyReport/201811/P020181109515197928770.pdf
  20. CHP (Center for Health Protection Hong Kong) , 2021a. Avian Influenza Report, Reporting period: Nov 14 – Nov 20, 2021 (Week 47). Hong Kong, CHP. 13 pp. Available online: https://www.chp.gov.hk/files/pdf/2021_avian_influenza_report_vol17_wk47.pdf
  21. CHP (Center for Health Protection Hong Kong) , 2021b. Avian Influenza Report, Reporting period: Apr 18, 2021 – Apr 24, 2021 (Week 17). Hong Kong, CHP. 12 pp. Available online: https://www.chp.gov.hk/files/pdf/2021_avian_influenza_report_vol17_wk17.pdf
  22. CHP (Center for Health Protection Hong Kong) , 2022. Avian Influenza Report, Reporting period: May 15 – May 21, 2022 (Week 21). Hong Kong, CHP. 13 pp. Available online: https://www.chp.gov.hk/files/pdf/2022_avian_influenza_report_vol18_wk21.pdf
  23. Chrzastek K, Lee DH, Gharaibeh S, Zsak A and Kapczynski DR, 2018. Characterization of H9N2 avian influenza viruses from the Middle East demonstrates heterogeneity at amino acid position 226 in the hemagglutinin and potential for transmission to mammals. Virology, 518, 195–201. 10.1016/j.virol.2018.02.016 [DOI] [PubMed] [Google Scholar]
  24. Connor RJ, Kawaoka Y, Webster RG and Paulson JC, 1994. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology, 205, 17–23. 10.1006/viro.1994.1615 [DOI] [PubMed] [Google Scholar]
  25. CTV News , online. Bird flu found in Alberta skunks for first time. Available online: https://edmonton.ctvnews.ca/bird-flu-found-in-alberta-skunks-for-first-time-experts-1.5913063 [Accessed: 29 June 2022].
  26. dwhc (Dutch Wildlife Health Centre) , online. Polecat and foxes infected with bird flu. Available online: https://dwhc.nl/bunzing-en-vossen-besmet-met-vogelgriep/ [Accessed: 30 March 2022].
  27. ECDC (European Centre for Disease Prevention and Control) , 2021a. Communicable Disease Threats Report ‐ Week 46, 14‐20 November 2021. ECDC: Stockholm. 14 pp. Available online: https://www.ecdc.europa.eu/sites/default/files/documents/Communicable-disease-threats-report-week%2046-2021.pdf
  28. ECDC (European Centre for Disease Prevention and Control) , 2021b. Threat Assessment Brief: First identification of human cases of avian influenza A(H5N8) infection. ECDC: Stockholm, 24 February 2021. 9 pp. Available online: https://www.ecdc.europa.eu/sites/default/files/documents/First-identification-human-cases-avian-influenza-A-H5N8-infection.pdf [Google Scholar]
  29. EFSA (European Food Safety Authority) , ECDC (European Centre for Disease Prevention and Control) , EURL (European Reference Laboratory) , Adlhoch C, Brouwer A, Kuiken T, Miteva A, Mulatti P, Smietanka K, Staubach C, Gogin A, Munoz Guajardo I and Baldinelli F, 2019. Scientific Report: Avian influenza overview November 2018 – February 2019. EFSA Journal 2019;17(3):5664. 35 pp. doi: 10.2903/j.efsa.2019.5664 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. EFSA (European Food Safety Authority) , ECDC (European Centre for Disease Prevention and Control) , EURL (European Reference Laboratory) , Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Marangon S, Niqueux E, Staubach C, Terregino C, Azynar I, Munoz Guajardo I and Baldinelli F, 2021a. Scientific Report: Avian influenza overview May – September 2021. EFSA Journal 2021;20(1):7122. 76 pp. doi: 10.2903/j.efsa.2022.7122 [DOI] [Google Scholar]
  31. EFSA (European Food Safety Authority) , ECDC (European Centre for Disease Prevention and Control), EURL (EUropean Reference Laboratory) , Adlhoch C, Fusaro A, Gozales JL, Kuiken T, Marangon S, Niqueux E, Staubach C, Terregino C, Aznar I, Munoz Guajardo I and Baldinelli F, 2021b. Scientific Report: Avian influenza overview September – December 2021. EFSA Journal 2021;19(12):7108. 94 pp. doi: 10.2903/j.efsa.2021.7108. Available online: https://efsa.onlinelibrary.wiley.com/doi/epdf/ 10.2903/j.efsa.2021.7108 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. EFSA (European Food Safety Authority) , ECDC (European Centre for Disease Prevention and Control), EURL (European Reference Laboratory) , Adlhoch C, Fusaro A, Gozales JL, Kuiken T, Marangon S, Niqueux E, Staubach C, Terregino C, Aznar I, Munoz Guajardo I and Baldinelli F, 2022. Scientific Report: Avian influenza overview December 2021 – March 2022. EFSA Journal 2022;20(4):7289. 64 pp. doi: 10.2903/j.efsa.2022.7289. Available online: https://www.efsa.europa.eu/it/efsajournal/pub/7289 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. EFSA (European Food Safety Authority) , ECDC (European Centre for Disease Prevention and Control), EURL (European Reference Laboratory) , Brown I, Mulatti P, Smietanka K, Staubach C, Willeberg P, Adlhoch C, Candiani D, Fabris C, Zancanaro G, Morgado J and Verdonck F, 2017. Scientific report: Avian influenza overview October 2016 – August 2017. EFSA Journal 2017;15(10):5018. 101 pp. doi: 10.2903/j.efsa.2017.5018 [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. EFSA AHAW Panel (EFSA Panel on Animal Health and Welfare) , 2017. Scientific opinion on avian influenza. 4991. EFSA Journal 2017;15(10):4991. 233 pp. doi: 10.2903/j.efsa.2017.4991 [DOI] [Google Scholar]
  35. European Commission , online. Animal Disease Information System (ADIS). Available online: https://ec.europa.eu/food/animals/animal-diseases/animal-disease-information-system-adis_en [Accessed: 29 June 2022].
  36. European Commission , online. Animal Health ‐ Regulatory Committee presentations. Available online: https://ec.europa.eu/food/animals/health/regulatory_committee/presentations_en [Accessed: 26 June 2020].
  37. FAO (Preliminary FAO/OIE/WHO Joint Rapid Risk Assessment) , 2022. Human infection with Influenza A(H3N8), China. 5 pp. Available online: https://www.fao.org/3/cc0204en/cc0204en.pdf [Google Scholar]
  38. FAO (Food and Agriculture Organization) , online. H7N9 situation update. Available online: http://www.fao.org/ag/againfo/programmes/en/empres/h7n9/situation_update.html [Accessed: 29 June 2022].
  39. FFA (Finnish Food Authority) , online. Avian influenza cases in Finland. Available online: https://www.ruokavirasto.fi/en/farmers/animal-husbandry/animal-health-and-diseases/animal-diseases/poultry/avian-influenza/avian-influenza-in-finland/ [Accessed: 30 March 2022].
  40. Floyd T, Banyard AC, Lean FZX, Byrne AMP, Fullick E, Whittard E, Mollett BC, Bexton S, Swinson V, Macrelli M, Lewis NS, Reid SM, Núñez A, Duff JP, Hansen R and Brown IH, 2021. Systemic infection with highly pathogenic H5N8 of avian origin produces encephalitis and mortality in wild mammals at a UK rehabilitation centre. bioRxiv:2021.2005.2026.445666. doi: 10.1101/2021.05.26.445666 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD and Stech J, 2005. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A, 102, 18590–18595. 10.1073/pnas.0507415102 [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Gabriel G, Herwig A and Klenk HD, 2008. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog, 4, e11. 10.1371/journal.ppat.0040011 [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Gonzales JL and Elbers ARW, 2018. Effective thresholds for reporting suspicions and improve early detection of avian influenza outbreaks in layer chickens. Sci Rep, 8, 8533. 10.1038/s41598-018-26954-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. GovMO (The Government of Macao Special Administrative Region Press release) , online. One human case of H5N6 avian influenza confirmed in Sichuan. Available online: https://www.deepl.com/translator#zh/en/%E5%9B%9B%E5%B7%9D%E7%A1%AE%E8%AF%8A%E4%B8%80%E4%BE%8B%E4%BA%BA%E6%84%9F%E6%9F%93H5N6%E7%A6%BD%E6%B5%81%E6%84%9F%E7%97%85%E4%BE%8B [Accessed: 29 June 2022a].
  45. GovMO (The Government of Macao Special Administrative Region Press release) , online. Two human H9N2 avian influenza cases confirmed in Hunan and Guizhou provinces. Available online: https://www.deepl.com/translator#zh/en/%E5%9B%9B%E5%B7%9D%E7%A1%AE%E8%AF%8A%E4%B8%80%E4%BE%8B%E4%BA%BA%E6%84%9F%E6%9F%93H5N6%E7%A6%BD%E6%B5%81%E6%84%9F%E7%97%85%E4%BE%8B%0A%0A%E6%B9%96%E5%8D%97%E7%9C%81%E5%8F%8A%E8%B4%B5%E5%B7%9E%E7%9C%81%E5%85%B1%E7%A1%AE%E8%AF%8A2%E4%BE%8B%E4%BA%BA%E6%84%9F%E6%9F%93H9N2%E7%A6%BD%E6%B5%81%E6%84%9F%E4%B8%AA%E6%A1%88 [Accessed: 29 June 2022b].
  46. GovUK (UK Health Security Agency) , online. Human case of avian flu detected in UK. Available online: https://www.gov.uk/government/news/human-case-of-avian-flu-detected-in-uk [Accessed: 30 March 2022].
  47. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD and Fouchier RA, 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science, 336, 1534–1541. 10.1126/science.1213362 [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Herve S, Schmitz A, Briand FX, Gorin S, Queguiner S, Niqueux E, Paboeuf F, Scoizec A, Le Bouquin‐Leneveu S, Eterradossi N and Simon G, 2021. Serological Evidence of Backyard Pig Exposure to Highly Pathogenic Avian Influenza H5N8 Virus during 2016‐2017 Epizootic in France. Pathogens, 10. 10.3390/pathogens10050621 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Jiang H, Wu P, Uyeki TM, He J, Deng Z, Xu W, Lv Q, Zhang J, Wu Y, Tsang TK, Kang M, Zheng J, Wang L, Yang B, Qin Y, Feng L, Fang VJ, Gao GF, Leung GM, Yu H and Cowling BJ, 2017. Preliminary Epidemiologic Assessment of Human Infections With Highly Pathogenic Avian Influenza A(H5N6) Virus, China. Clinical Infectious Diseases, 65, 383–388. 10.1093/cid/cix334 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Kariithi HM, Welch CN, Ferreira HL, Pusch EA, Ateya LO, Binepal YS, Apopo AA, Dulu TD, Afonso CL and Suarez DL, 2019. Genetic characterization and pathogenesis of the first H9N2 low pathogenic avian influenza viruses isolated from chickens in Kenyan live bird markets. Infection, Genetics and Evolution:104074. 10.1016/j.meegid.2019.104074 [DOI] [PubMed] [Google Scholar]
  51. Kim JH, Hatta M, Watanabe S, Neumann G, Watanabe T and Kawaoka Y, 2010. Role of host‐specific amino acids in the pathogenicity of avian H5N1 influenza viruses in mice. J Gen Virol, 91, 1284–1289. 10.1099/vir.0.018143-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. King J, Schulze C, Engelhardt A, Hlinak A, Lennermann SL, Rigbers K, Skuballa J, Staubach C, Mettenleiter TC, Harder T, Beer M and Pohlmann A, 2020. Novel HPAIV H5N8 Reassortant (Clade 2.3.4.4b) Detected in Germany. Viruses, 12. 10.3390/v12030281, [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Lee EK, Lee YN, Kye SJ, Lewis NS, Brown IH, Sagong M, Heo GB, Kang YM, Cho HK, Kang HM, Cheon SH, Lee M, Park BK, Kim YJ and Lee YJ, 2018. Characterization of a novel reassortant H5N6 highly pathogenic avian influenza virus clade 2.3.4.4 in Korea, 2017. Emerging Microbes & Infections, 7:103. doi: 10.1038/s41426-018-0104-3 [DOI] [PMC free article] [PubMed]
  54. Li YT, Chen CC, Chang AM, Chao DY and Smith GJD, 2020. Co‐circulation of both low and highly pathogenic avian influenza H5 viruses in current poultry epidemics in Taiwan. Virus Evol, 6(veaa037). 10.1093/ve/veaa037 [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Lo FT, Zecchin B, Diallo AA, Racky O, Tassoni L, Diop A, Diouf M, Diouf M, Samb YN, Pastori A, Gobbo F, Ellero F, Diop M, Lo MM, Diouf MN, Fall M, Ndiaye AA, Gaye AM, Badiane M, Lo M, Youm BN, Ndao I, Niaga M, Terregino C, Diop B, Ndiaye Y, Angot A, Seck I, Niang M, Soumare B, Fusaro A and Monne I, 2022. Intercontinental Spread of Eurasian Highly Pathogenic Avian Influenza A(H5N1) to Senegal. Emerg Infect Dis, 28, 234–237. 10.3201/eid2801.211401 [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Manzoor R, Sakoda Y, Nomura N, Tsuda Y, Ozaki H, Okamatsu M and Kida H, 2009. PB2 protein of a highly pathogenic avian influenza virus strain A/chicken/Yamaguchi/7/2004 (H5N1) determines its replication potential in pigs. J Virol, 83, 1572–1578. 10.1128/JVI.01879-08 [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. offlu (WOAH FAO network on animal influenza) , 2022. Avian H3N8 human case. 8 pp. Available online: https://www.offlu.org/wp-content/uploads/2022/04/Human-H3N8-Genome-Analysis.pdf
  58. News Outbreak, online. Denmark reports 1st highly pathogenic avian influenza case in harbor seal. Available online: http://outbreaknewstoday.com/denmark-reports-1st-highly-pathogenic-avian-influenza-case-in-harbor-seal-89870/ [Accessed: 29 June 2022].
  59. Peters M, King J, Wohlsein P, Grund C and Harder T, 2022. Genuine lethal infection of a wood pigeon (Columba palumbus) with high pathogenicity avian influenza H5N1, clade 2.3.4.4b, in Germany, 2022. Vet Microbiol, 270:109461. doi: 10.1016/j.vetmic.2022.109461 [DOI] [PubMed] [Google Scholar]
  60. Pyankova OG, Susloparov IM, Moiseeva AA, Kolosova NP, Onkhonova GS, Danilenko AV, Vakalova EV, Shendo GL, Nekeshina NN, Noskova LN, Demina JV, Frolova NV, Gavrilova EV, Maksyutov RA and Ryzhikov AB, 2021. 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. Eurosurveillance, 26:2100439. doi: doi: 10.2807/1560-7917.ES.2021.26.24.2100439 [DOI] [PMC free article] [PubMed]
  61. Resource WUR (Resources Wageninge University Research) , online. We are concerned about mutations of the bird flu virus. Available online: https://www.resource-online.nl/index.php/2022/02/04/we-zijn-beducht-op-mutaties-van-het-virus/ [Accessed: 30 March 2022].
  62. Rijks JM, Hesselink H, Lollinga P, Wesselman R, Prins P, Weesendorp E, Engelsma M, Heutink R, Harders F, Kik M, Rozendaal H, van den Kerkhof H and Beerens N, 2021. Highly Pathogenic Avian Influenza A(H5N1) Virus in Wild Red Foxes, the Netherlands, 2021. Emerg Infect Dis, 27, 2960–2962. 10.3201/eid2711.211281 [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Schülein A, Ritzmann M, Christian J, Schneider K and Neubauer‐Juric A, 2021. Exposure of wild boar to Influenza A viruses in Bavaria: Analysis of seroprevalences and antibody subtype specificity before and after the panzootic of highly pathogenic avian influenza viruses A (H5N8). Zoonoses and Public Health, n/a. doi: https://doi.org/ 10.1111/zph.12841 [DOI] [PubMed]
  64. Shin J, Kang S, Byeon H, Cho SM, Kim SY, Chung YJ and Jung SH, 2020. Highly pathogenic H5N6 avian influenza virus subtype clade 2.3.4.4 indigenous in South Korea. Scientific Reports, 10(7241). 10.1038/s41598-020-64125-x [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Smietanka K, Swieton E, Wyrostek K, Kozak E, Tarasiuk K, Stys‐Fijol N, Dziadek K and Niemczuk K, 2022. Highly Pathogenic Avian Influenza H5Nx in Poland in 2020/2021: a Descriptive Epidemiological Study of a Large‐scale Epidemic. J Vet Res, 66, 1–7. 10.2478/jvetres-2022-0017 [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Smith GJ, Donis RO and World Health Organization/World Organisation for Animal HF and Agriculture Organization HEWG , 2015. Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013‐2014. Influenza Other Respir Viruses, 9, 271–276. 10.1111/irv.12324 [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. SSI (Staten Serum Insitut) , online. Bird flu in Danish seals. Available online: https://www.ssi.dk/aktuelt/nyheder/2022/fugleinfluenza-i-dansk-sael [Accessed: 29 June 2022].
  68. Su Y, Yang HY, Zhang BJ, Jia HL and Tien P, 2008. Analysis of a point mutation in H5N1 avian influenza virus hemagglutinin in relation to virus entry into live mammalian cells. Arch Virol, 153, 2253–2261. 10.1007/s00705-008-0255-y [DOI] [PubMed] [Google Scholar]
  69. Suttie A, Deng YM, Greenhill AR, Dussart P, Horwood PF and Karlsson EA, 2019. Inventory of molecular markers affecting biological characteristics of avian influenza A viruses. Virus Genes, 55, 739–768. 10.1007/s11262-019-01700-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. SVA (National Veterinary Institute Sweden) , online. Highly pathogenic bird flu ‐ the past season and the infection situation for the coming season. Available online: https://www.sva.se/statsepizootologen-kommenterar/hogpatogen-fagelinfluensa-den-gangna-sasongen-och-smittlaget-infor-kommande-sasong/ [Accessed: 21 December 2021].
  71. The Government of the Hong Kong Special Administrative Region Press Releases , onlinea. CHP notified of human case of avian influenza A(H3N8) in Mainland. Available online: https://www.info.gov.hk/gia/general/202205/30/P2022053000587.htm [Accessed: 29 June 2022].
  72. Trouw , online. Terns and spoonbills succumb to bird flu in bushes. Available online: https://www.trouw.nl/duurzaamheid-natuur/sterns-en-lepelaars-bezwijken-bij-bosjes-aan-de-vogelgriep~bf284859/ [Accessed: 29 June 2022].
  73. Vizi A, 2022. Outcome of the avian flu outbreak in Dalmatian pelican population at Skadar lake, Montenegro. Natura Montenegrina, Podgorica, 14, 125–127. [Google Scholar]
  74. Vogelbescherming (Netherlands) , online. Massive deaths among sandwich terns due to bird flu are major concerns. Available online: https://www.vogelbescherming.nl/actueel/bericht/grote-zorgen-door-massale-sterfte-onder-grote-sterns-door-vogelgriep [Accessed: 29 June 2022].
  75. Wang W, Lu B, Zhou H, Suguitan AL Jr, Cheng X, Subbarao K, Kemble G and Jin H, 2010. Glycosylation at 158N of the hemagglutinin protein and receptor binding specificity synergistically affect the antigenicity and immunogenicity of a live attenuated H5N1 A/Vietnam/1203/2004 vaccine virus in ferrets. J Virol, 84, 6570–6577. 10.1128/JVI.00221-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. WHO (World Health Organization) , 2016. International Health Regulations (2005) ‐ Third edition. 84 pp. Available online: http://www.who.int/ihr/publications/9789241580496/en/
  77. WHO (World Health Organization) , 2017. Operational Guidance on Sharing Influenza Viruses with Human Pandemic Potential (IVPP) under the Pandemic Influenza Preparedness (PIP) Framework. Geneva, WHO. 20 pp. Available online: http://apps.who.int/iris/bitstream/handle/10665/259402/WHO-WHE-IHM-GIP-2017.3-eng.pdf;jsessionid=FF66316FB599ADA38D34499AA56765FA?sequence=1 [Google Scholar]
  78. WHO (World Health Organization) , 2018. Protocol to investigate non‐seasonal influenza and other emerging acute respiratory diseases. Geneva WHO. 73 pp. Available online: https://apps.who.int/iris/bitstream/handle/10665/275657/WHO-WHE-IHM-GIP-2018.2-eng.pdf?ua=1 [Google Scholar]
  79. WHO (World Health Organization) , 2019a. Influenza at the human‐animal interface ‐ Summary and assessment, from 25 June 2019 to 27 September 2019. Geneva, WHO. 3 pp. Available online: https://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_27_09_2019.pdf?ua=1
  80. WHO (World Health Organization) , 2019b. Avian Influenza Weekly Update Number 713. WHO, Geneva. 3 p. Available online: https://iris.wpro.who.int/bitstream/handle/10665.1/14328/AI-20191101.pdf [Google Scholar]
  81. WHO (World Health Organization) , 2020a. Antigenic and genetic characteristics of zoonotic influenza A viruses and development of candidate vaccine viruses for pandemic preparedness. Geneva. 8 pp. Available online: https://www.who.int/influenza/vaccines/virus/202002_zoonotic_vaccinevirusupdate.pdf?ua=1 [Google Scholar]
  82. WHO (World Health Organization) , 2020b. Influenza at the human‐animal interface ‐ Summary and assessment, from 21 January to 28 February 2020. Geneva. 4 pp. Available online: https://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_28_02_2020.pdf?ua=1 [Google Scholar]
  83. WHO (World Health Organization) , 2020c. Influenza at the human‐animal interface; Summary and assessment, from 28 February to 8 May 2020. Geneva. 3 pp. Available online: https://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_08_05_2020.pdf?ua=1 [Google Scholar]
  84. WHO (World Health Organization) , 2020d. Influenza at the human‐animal interface; Summary and assessment, from 9 August to 1 October 2021. Geneva. 7 pp. Available online: https://cdn.who.int/media/docs/default-source/influenza/human-animal-interface-risk-assessments/influenza_summary_ira_ha_interface_oct_2021.pdf?sfvrsn=5da1328d_9&download=true [Google Scholar]
  85. WHO (World Health Organization) , 2021c. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003‐2021 (22 June 2021). Geneva, WHO. 4 pp. Available online: https://cdn.who.int/media/docs/default-source/influenza/h5n1-human-case-cumulative-table/2021_june_tableh5n1.pdf?sfvrsn=839e65a9_10&download=true [Google Scholar]
  86. WHO (World Health Organization) , 2021d. Antigenic and genetic characteristics of zoonotic influenza A viruses and development of candidate vaccine viruses for pandemic preparedness September 2021. Geneva. 13 pp. Available online: https://cdn.who.int/media/docs/default-source/influenza/who-influenza-recommendations/vcm-southern-hemisphere-recommendation-2022/202110_zoonotic_vaccinevirusupdate.pdf?sfvrsn=8f87a5f1_11 [Google Scholar]
  87. WHO (World Health Organization) , 2021e. Influenza at the human‐animal interface; Summary and assessment, from 22 May to 22 June 2021. Geneva. 7 pp. Available online: https://cdn.who.int/media/docs/default-source/influenza/human-animal-interface-risk-assessments/influenza_summary_ira_ha_interface_june_2021.pdf?sfvrsn=bf6f707e_6&download=true [Google Scholar]
  88. WHO (World Health Organization) , 2021f. Influenza at the human‐animal interface; Summary and assessment, from 23 June to 8 August 2021. Geneva. 13 pp. Available online: https://cdn.who.int/media/docs/default-source/influenza/human-animal-interface-risk-assessments/influenza_summary_ira_ha_interface_08_08_2021.pdf?sfvrsn=5aa110_5&download=true [Google Scholar]
  89. WHO (World Health Organization) , 2022. Influenza at the human‐animal interface; Summary and assessment, from 8 April to 13 May 2022. Geneva. 6 pp. Available online: https://cdn.who.int/media/docs/default-source/influenza/human-animal-interface-risk-assessments/influenza_summary_ira_ha_interface_may_2022.pdf?sfvrsn=6b4b3e20_1&download=true [Google Scholar]
  90. WHO (World Health Organization) , online‐a. Human infection with avian influenza A(H5N1) – India. Available online: https://www.who.int/emergencies/disease-outbreak-news/item/human-infection-with-avian-influenza-a(h5n1)‐%EF%BD%B0‐india [Accessed: 29 September 2021a].
  91. WHO (World Health Organization) , online‐b. Global Influenza Surveillance and Response System (GISRS). Available online: https://www.who.int/influenza/gisrs_laboratory/en/ [Accessed: 26 February 2021b].
  92. WOAH (World Organisation for Animal Health) , online‐a. Canada, Follow‐up report 1, REPORT ID FUR_155418 Available online: https://wahis.woah.org/#/report-info?reportId=54823 [Accessed: 29 June 2022a].
  93. WOAH (World Organisation for Animal Health) , online‐b. United States of America, Follow‐up report 1, REPORT ID FUR_155419 Available online: https://wahis.woah.org/#/report-info?reportId=54201 [Accessed: 29 June 2022b].
  94. WOAH (World Organisation for Animal Health), online‐c. World Animal Health Information Database (WAHIS) Interface. Available online: https://wahis.woah.org/#/home [Accessed: 29 June 2022].
  95. WOAH (World Organisation for Animal Health) , online‐d. Japan, Follow‐up report 1, REPORT ID FUR_155032 Available online: https://wahis.woah.org/#/report-info?reportId=52538 [Accessed: 29 June 2022c].
  96. WUR (Wageningen University Research) , online. Bird flu (H5N1) detected in a fox with neurological symptoms. Available online: https://www.wur.nl/en/research-results/research-institutes/bioveterinary-research/show-bvr/bird-flu-h5n1-detected-in-a-fox-with-neurological-symptoms.htm [Accessed: 30 March 2022].
  97. Xu C, Ye H, Qiu W, Lin H, Chen Y, Zhang H and Liao M, 2018. Phylogenetic classification of hemagglutinin gene of H9N2 avian influenza viruses isolated in China during 2012–2016 and evaluation of selected candidate vaccine strains. Poultry Science, 97, 3023–3030. 10.3382/ps/pey154 [DOI] [PubMed] [Google Scholar]
  98. Yamayoshi S, Kiso M, Yasuhara A, Ito M, Shu Y and Kawaoka Y, 2018. Enhanced Replication of Highly Pathogenic Influenza A(H7N9) Virus in Humans. Emerg Infect Dis, 24, 746–750. 10.3201/eid2404.171509 [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Yamayoshi S, Yamada S, Fukuyama S, Murakami S, Zhao D, Uraki R, Watanabe T, Tomita Y, Macken C, Neumann G and Kawaoka Y, 2014. Virulence‐affecting amino acid changes in the PA protein of H7N9 influenza A viruses. J Virol, 88, 3127–3134. 10.1128/JVI.03155-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Yang ZY, Wei CJ, Kong WP, Wu L, Xu L, Smith DF and Nabel GJ, 2007. Immunization by avian H5 influenza hemagglutinin mutants with altered receptor binding specificity. Science, 317, 825–828. 10.1126/science.1135165 [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Zecchin B, Minoungou G, Fusaro A, Moctar S, Ouedraogo‐Kabore A, Schivo A, Salviato A, Marciano S and Monne I, 2017. Influenza A(H9N2) Virus, Burkina Faso. Emerging Infectious Diseases, 23, 2118–2119. 10.3201/eid2312.171294 [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Zhu C, Hu C, Gui B, Chen Q, Zhang S and He G, 2018. Genetic characteristics of H9N2 avian influenza viruses isolated from free‐range poultry in Eastern China, in 2014‐2015. Poultry Science, 97, 3793–3800. 10.3382/ps/pey187 [DOI] [PubMed] [Google Scholar]

Articles from EFSA Journal are provided here courtesy of Wiley

RESOURCES