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. 2020 Jun 30;18(6):e06194. doi: 10.2903/j.efsa.2020.6194

Avian influenza overview February – May 2020

European Food Safety Authority; European Centre for Disease Prevention and Control and European Union Reference Laboratory for Avian Influenza, Cornelia Adlhoch, Alice Fusaro, Thijs Kuiken, Eric Niqueux, Christoph Staubach, Calogero Terregino, Irene Muñoz Guajardo, Francesca Baldinelli
PMCID: PMC7448026  PMID: 32874346

Abstract

Between 16 February and 15 May 2020, 290highly pathogenic avian influenza (HPAI) A(H5) virus outbreakswere reported in Europe in poultry (n=287), captive birds (n=2) and wild birds (n=1)in Bulgaria, Czechia,Germany,Hungary andPolandand two low pathogenic avian influenza (LPAI) A(H7N1) virus outbreaks were reported in poultry in Italy. 258 of 287 poultry outbreaks detected in Europe were secondary outbreaks, suggesting that in the large majoryty of cases the spread of the virus was not due to wild birds.Allthe HPAI outbreaks were A(H5N8) apart from three,which were reported as A(H5N2) from Bulgaria. Genetic analysis of the HPAI A(H5N8) viruses isolated from the eastern and central European countries indicates that this is a reassortant between HPAI A(H5N8) viruses from Africa and LPAI viruses from Eurasia. Two distict subtypes were identified in Bulgaria, a novel reassortant A(H5N2) and A(H5N8) that is persisting in the country since 2016. There could be several reasons why only very few HPAI cases were detected in wild birds in this 2019‐2020 epidemic season and a better knowledge of wild bird movements and virus‐host interaction (e.g. susceptibility of the hosts to this virus) could help to understand the reasons for poor detection of HPAI infected wild birds. In comparison with the last reporting period, a decreasing number of HPAI A(H5)‐affected countries and outbreaks were reported from outside Europe. However, there is considerable uncertainty regarding the current epidemiological situation in many countries out of Europe. Four human cases due to A(H9N2) virus infection were reported during the reporting period from China.

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, Kuiken T, Niqueux E, Terregino C, Staubach C, Muñoz Guajardo I and Baldinelli F, 2020. Scientific report: Avian influenza overview February – May 2020. EFSA Journal 2020;18(6):6194, 47 pp. doi: 10.2903/j.efsa.2020.6194

Requestor:European Commission

Question number: EFSA‐Q‐2020‐00272

Acknowledgements:In addition to the listed authors, EFSA, ECDC and the EURL wish to thank the following:Member State representatives who provided data on avian influenza outbreaks,or wrote case reports for this scientific output: Aleksandra Miteva and Gabriela Goujgoulova (Bulgaria), Lucie Kalášková, MiladaDubská and Alexander Nagy (Czechia); Timm Harder and Franz Conraths (Germany); Georgina Helyes and Malik Peter (Hungary); Paolo Mulatti (Italy);Krzysztof Smietankaand the General Veterinary Inspectorate (Poland);Martin Tinak (Slovakia); Dominique Bicout,Jan Arend Stegeman and Preben Willeberg for reviewing the document; Bianca Zecchin from IZSVe for her support in the genetic analyses of European A(H5N8); Timm Harder from FriedrichLoefflerInstitut,Inmaculada Aznar and Elisabeth Dorbek‐Kolin from EFSA for the support provided to this scientific output.

Figures 1–13, 16–16, 18–19, 21–22 and Tables 1–5 © EFSA; Figures 14 © EURL; Figures 17, 20, 23–25 © ECDC

Approved: 25 June 2020

References

  1. Abdollahi H, Maken Ali AS, Monne I, Milani A, Habibi M, Zamperin G, Ghafouri SA, Maghsoudloo H, Mohammadpoor B, Esmaeilzadeh S, Farahani RK, Ghasemi Y, Afzalkhani AA, Nabipoor J, Javanmardi B, Fusaro A and Zecchin B, 2020. Spatial spread and emergence of reassortant H5 highly pathogenic avian influenza viruses in Iran reassortant H5 highly pathogenic avian influenza virus in Iran. Infection, Genetics and Evolution, 83, 104342 10.1016/j.meegid.2020.104342. [DOI] [PubMed] [Google Scholar]
  2. Abolnik C and 2019. Outbreaks of Clade 2.3.4.4 H5N8 highly pathogenic avian influenza in, , 2018. in the northern regions of South Africa were unrelated to those of 2017. Transbound Emerg Dis, 10.1111/tbed.13448. [DOI] [PubMed] [Google Scholar]
  3. Adlhoch C, Miteva A, Zdravkova A, Miskic T, Knezevic D, Perdikaris S, Smietanka K, Swieton E, Kopriva V, Chudy M, Romero Gonzalez LJ, Moreno Gil I, Wallen Norell A and Verdonck F, 2019. Estimation of the number of exposed people during highly pathogenic avian influenza virus outbreaks in EU/EEA countries, October 2016‐September 2018. Zoonoses Public Health, 66, 874–878. 10.1111/zph.12629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Alyas K, Wajid A, Dundon WG, Ather S, Batool T and Babar ME, 2019. Isolation and Characterization of Avian Influenza H9N2 Viruses from Different Avian Species in Pakistan 2016‐17. Avian Dis, 63, 721–726. 10.1637/aviandiseases-D-19-00070. [DOI] [PubMed] [Google Scholar]
  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. 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]
  7. Chen Z, Huang Q, Yang S, Su S, Li B, Cui N and Xu C, 2020. A Well‐Defined H9N2 Avian Influenza Virus Genotype with High Adaption in Mammals was Prevalent in Chinese Poultry Between 2016 to 2019. Viruses, 12, 10.3390/v12040432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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. 6pp. Available online: http://www.chinaivdc.cn/cnic/en/Surveillance/WeeklyReport/201811/P020181109515197928770.pdf
  9. 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]
  10. EFSA, ECDC, EURL , Adlhoch C, Brouwer A, Kuiken T, Miteva A, Mulatti P, Smietanka K, Staubach C, Gogin A, Munoz Guajardo I and Baldinelli F, 2018. a. Scientific Report: Avian influenza overview August ‐ November 2018. Efsa Journal, 16(12):5573, 40pp., 10.2903/j.efsa.2018.5573 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. EFSA, ECDC, EURL , Adlhoch C, Brouwer A, Kuiken T, Miteva A, Mulatti P, Smietanka K, Staubach C, Gogin A, Munoz Guajardo I and Baldinelli F, 2019. a. Scientific Report: Avian influenza overview November 2018 ‐ February 2019. Efsa Journal, 17(3):5664, 35pp.,doi: 10.2903/j.efsa.2019.5664 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. EFSA, ECDC, EURL , Adlhoch C, Brouwer A, Kuiken T, Mulatti P, Smietanka K, Staubach C, Munoz Guajardo I, Amato L and Baldinelli F, 2018. b. Scientific Report: Avian influenza overview May ‐ August 2018. Efsa Journal, 16(9):5430, 43pp., 10.2903/j.efsa.2018.5430 [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. EFSA, ECDC, EURL , Adlhoch C, Brouwer A, Kuiken T, Mulatti P, Smietanka K, Staubach C, Willeberg P, Barrucci F, Verdonck F, Amato L and Baldinelli F, 2018. c. Scientific Report: Avian influenza overview November 2017 ‐ February 2018. 16(3):5240, EFSA Journal 2018. 55pp., 10.2903/j.efsa.2018.5240 [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. EFSA, ECDC, EURL , Adlhoch C, Fusaro A, Kuiken T, Monne I, Smietanka K, Staubach C, Munoz Guajardo I and Baldinelli F, 2019. b. Scientific Report: Avian influenza overview February ‐ August 2019. Efsa Journal, 17(9):5843, 38pp., 10.2903/j.efsa.2019.5843 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. EFSA, ECDC, EURL , Adlhoch C, Fusaro A, Kuiken T, Niqueux E, Staubach C, Terregino C, Munoz Guajardo I and Baldinelli F, 2020. Scientific Report: Avian influenza overview November 2019 ‐ February 2020. Efsa Journal, 18(3):6069, 54pp.,doi: 10.2903/j.efsa.2020.6069 Available [DOI] [Google Scholar]
  16. EFSA AHAW Panel (EFSA Panel on Animal Health and Welfare) , 2017. Scientific opinion on avian influenza. Efsa Journal, 15, 4991, 233pp., 10.2903/j.efsa.2017.4991 [DOI] [Google Scholar]
  17. European Commission, online‐a. Animal Disease Notification System (ADNS) . Available online: https://ec.europa.eu/food/animals/animal-diseases/not-system_en [Accessed: 17 December 2019]
  18. European Commission, online‐b. Animal Health ‐ Regulatory Committee presentations . Available online: https://ec.europa.eu/food/animals/health/regulatory_committee/presentations_en [Accessed: 26 June 2020]
  19. FAO (Food and Agriculture Organization), online‐a. H7N9 situation update . Available online: http://www.fao.org/ag/againfo/programmes/en/empres/h7n9/wave_6/Situation_update_2017_11_24.html [Accessed: 26 June 2020]
  20. FAO (Food and Agriculture Organization) , online‐b. EMPRES‐i ‐ Global Animal Disease Information System. Available online: http://empres-i.fao.org/eipws3g/ [Accessed: 26 June 2020]
  21. Fusaro A, Monne I, Mulatti P, Zecchin B, Bonfanti L, Ormelli S, Milani A, Cecchettin K, Lemey P, Moreno A, Massi P, Dorotea T, Marangon S and Terregino C, 2017. Genetic Diversity of Highly Pathogenic Avian Influenza A(H5N8/H5N5) Viruses in Italy, 2016‐17. Emerging Infectious Diseases, 23, 1543–1547. 10.3201/eid2309.170539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Jiang W, Hou G, Li J, Peng C, Wang S, Liu S, Zhuang Q, Yuan L, Yu X, Li Y, Wang J and Liu H, 2020. Antigenic Variant of Highly Pathogenic Avian Influenza A(H7N9) Virus, China, 2019. Emerging Infectious Diseases, 26, 10.3201/eid2502.191105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Lee DH, Bertran K, Kwon JH and Swayne DE, 2017. Evolution, global spread, and pathogenicity of highly pathogenic avian influenza H5Nx clade 2.3.4.4. Journal of Veterinary Science, 18, 269–280. 10.4142/jvs.2017.18.S1.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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. 10.1038/s41426-018-0104-3 [DOI] [PMC free article] [PubMed]
  28. Li T, Ma Y, Li K, Tang X, Wang M and Yang Z, 2016. Death of a very young child infected with influenza A (H5N6). Journal of Infection, 73, 626–627. 10.1016/j.jinf.2016.07.015. [DOI] [PubMed] [Google Scholar]
  29. Li X, Sun J, Lv X, Wang Y, Li Y, Li M, Liu W, Zhi M, Yang X, Fu T, Ma P, Li Y, Zhou X, Li Y, Yang G, Chen G, Zhang J, Zheng H, Zhang G, Hua Y, Yang S, Li Y, Richt JA and Chai H, 2020. Novel Reassortant Avian Influenza A(H9N2) Virus Isolate in Migratory Waterfowl in Hubei Province. China. Frontiers in Microbiology, 11, 220 10.3389/fmicb.2020.00220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. OIE (World Organisation for Animal Health), online. World Animal Health Information Database (WAHIS) Interface . Available online: https://www.oie.int/wahis_2/public/wahid.php/Wahidhome/Home/indexcontent/newlang/en [Accessed: 26 June 2020]
  31. Parvin R, Kabiraj CK, Mumu TT, Chowdhury EH, Islam MR, Beer M and Harder T, 2020. Active virological surveillance in backyard ducks in Bangladesh: Detection of avian influenza and gamma‐coronaviruses. Avian Pathology, 1‐29, 10.1080/03079457.2020.1753654. [DOI] [PubMed] [Google Scholar]
  32. Peacock THP, James J, Sealy JE and Iqbal M, 2019. A Global Perspective on H9N2 Avian Influenza Virus. Viruses, 11, 620 10.3390/v11070620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Potdar V, Hinge D, Satav A, Simões EF, Yadav PD and Chadha MS, 2019. Laboratory‐confirmed avian influenza A(H9N2) virus infection, India, 2019. Emerging Infectious Diseases, 25, 10.3201/eid2512.190636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Qu B, Li X, Cardona CJ and Xing Z, 2020. Reassortment and adaptive mutations of an emerging avian influenza virus H7N4 subtype in China. PLoS One, 15, e0227597 10.1371/journal.pone.0227597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Shittu I, Bianco A, Gado D, Mkpuma N, Sulaiman L, Laleye A, Gobbo F, Bortolami A, Bonfante F, Vakuru C, Meseko C, Fusaro A, Shamaki D, Alabi O, Terregino C and Joannis T, 2020. First detection of highly pathogenic H5N6 avian influenza virus on the African continent. Emerging Microbes & Infections, 9, 886–888. 10.1080/22221751.2020.1757999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Smith GJ, Donis RO, 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]
  38. Swieton E, Fusaro A, Shittu I, Niemczuk K, Zecchin B, Joannis T, Bonfante F, Smietanka K and Terregino C, 2020. Sub‐Saharan Africa and Eurasia Ancestry of Reassortant Highly Pathogenic Avian Influenza A(H5N8) Virus, Europe, December 2019. Emerging Infectious Disease journal, 26, 1557 10.3201/eid2607.200165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Taiwan Centers for Disease Control Press Releases, online. China's Shandong Province new type A influenza travel epidemic recommended to be upgraded to the second level alert (Alert) . Available online: https://www.cdc.gov.tw/Bulletin/Detail/q4Cy5WfdLLN0MFjjwRtTvw?typeid=9 [Accessed: 26 June 2020]
  40. The Government of Hong Kong Special Administrative Region Press Release, online . CHP investigating a case of influenza A (H9) infection. Available online: https://www.info.gov.hk/gia/general/202002/07/P2020020700608.htm [Accessed: 26 June 2020]
  41. Thurain K, Mon PP, Nasamran C, Charoenkul K, Boonyapisitsopa S, Tun TN, San YY, Aye AM and Amonsin A, 2020. Surveillance of influenza A virus subtype H5N1 in a live bird market in Yangon, Myanmar: 2017‐2018. Transboundary and Emerging Diseases. 10.1111/tbed.13618 [DOI] [PubMed] [Google Scholar]
  42. WHO (World Health Organization) , 2019. a. Influenza at the human‐animal interface ‐ Summary and assessment, from 25 June 2019 to 27 September 2019.WHO, Geneva. 3pp. Available online: https://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_27_09_2019.pdf?ua=1 [Google Scholar]
  43. WHO (World Health Organization) , 2019. b. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003‐2019. WHO, Geneva. 3pp. Available online: https://www.who.int/influenza/human_animal_interface/2019_06_24_tableH5N1.pdf?ua=1 [Google Scholar]
  44. WHO (World Health Organization) , 2019. c. Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness, February 2019. WHO, Geneva. 10pp. Available online: https://www.who.int/influenza/vaccines/virus/201902_zoonotic_vaccinevirusupdate.pdf?ua=1 [Google Scholar]
  45. WHO (World Health Organization) , 2019. d. Avian Influenza Weekly Update Number 713. WHO, Geneva. 3pp. Available online: https://iris.wpro.who.int/bitstream/handle/10665.1/14328/AI-20191101.pdf [Google Scholar]
  46. WHO (World Health Organization) , 2020. a. Influenza at the human‐animal interface; Summary and assessment, from 28 February to 8 May 2020. Geneva. 3pp. Available online: https://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_08_05_2020.pdf?ua=1 [Google Scholar]
  47. WHO (World Health Organization) , 2020. b. Recommended composition of influenza virus vaccines for use in the 2020‐2021 northern hemisphere influenza season. WHO, Geneva. 12pp. Available online: https://www.who.int/influenza/vaccines/virus/recommendations/202002_recommendation.pdf?ua=1 [Google Scholar]
  48. WHO (World Health Organization) , 2020. c. Influenza at the human‐animal interface ‐ Summary and assessment, from 21 January to 28 February 2020. Geneva. 4pp. Available online: https://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_28_02_2020.pdf?ua=1 [Google Scholar]
  49. WHO (World Health Organization) , 2020. d. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003‐2020. Geneva. 4pp. Available online: https://www.who.int/influenza/human_animal_interface/2020_MAY_tableH5N1.pdf?ua=1 [Google Scholar]
  50. WHO (World Health Organization) , 2020. e. Antigenic and genetic characteristics of zoonotic influenza A viruses and development of candidate vaccine viruses for pandemic preparedness. Geneva. 8pp. Available online: https://www.who.int/influenza/vaccines/virus/202002_zoonotic_vaccinevirusupdate.pdf?ua=1 [Google Scholar]
  51. WHO (World Health Organization) , online. Assessment of risk associated with influenza A(H5N8) virus, 17 November 2016. Available online: https://www.who.int/influenza/human_animal_interface/avian_influenza/riskassessment_AH5N8_201611/en/ [Accessed: 26 June 2020]
  52. 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]
  53. 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]
  54. 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]

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