Skip to main content
NCBI home page
EFSA Journal logoLink to EFSA Journal
. 2018 Dec 20;16(12):e05573. doi: 10.2903/j.efsa.2018.5573

Avian influenza overview August – November 2018

European Food Safety Authority; European Centre for Disease Prevention and Control; European Union Reference Laboratory for Avian Influenza, Cornelia Adlhoch, Adam Brouwer, Thijs Kuiken, Aleksandra Miteva, Paolo Mulatti, Krzysztof Smietanka, Christoph Staubach, Andrey Gogin, Irene Muñoz Guajardo, Francesca Baldinelli
PMCID: PMC7009621  PMID: 32625795

Abstract

Between 16 August and 15 November 2018, 14 highly pathogenic avian influenza (HPAI) A(H5N8) outbreaks in poultry establishments in Bulgaria and seven HPAI A(H5N6) outbreaks, one in captive birds in Germany and six in wild birds in Denmark and the Netherlands were reported in the European Union (EU). No human infection due to HPAI A(H5N8) and A(H5N6) viruses have been reported in Europe so far. Seroconversion of people exposed during outbreaks in Russia has been reported in one study. Although the risk of zoonotic transmission to the general public in Europe is considered to be very low, appropriate personal protection measures of people exposed will reduce any potential risk. Genetic clustering of the viruses isolated from poultry in Bulgaria suggests three separate introductions in 2016 and a continuing circulation and transmission of these viruses within domestic ducks. Recent data from Bulgaria provides further indication that the sensitivity of passive surveillance of HPAI A(H5N8) in domestic ducks may be significantly compromised. Increased vigilance is needed especially during the periods of cold spells in winter when aggregations of wild birds and their movements towards areas with more favourable weather conditions may be encouraged. Two HPAI outbreaks in poultry were reported during this period from western Russia. Low numbers of HPAI outbreaks were observed in Africa and Asia, no HPAI cases were detected in wild birds in the time period relevant for this report. Although a few HPAI outbreaks were reported in Africa and Asia during the reporting period, the probability of HPAI virus introductions from non‐EU countries via wild birds particularly via the north‐eastern route from Russia is increasing, as the fall migration of wild birds from breeding and moulting sites to the wintering sites continues. Furthermore, the lower temperatures and ultraviolet radiation in winter can facilitate the environmental survival of any potential AI viruses introduced to Europe.

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

Suggested citation: EFSA (European Food Safety Authority) , ECDC (European Centre for Disease Prevention and Control) , EURL (European Reference Laboratory for Avian Influenza) , Adlhoch C, Brouwer A, Kuiken T, Miteva A, Mulatti P, Smietanka K, Staubach C, Gogin A, Muñoz Guajardo I and Baldinelli F, 2018. Scientific report: Avian influenza overview August – November 2018. EFSA Journal 2018;16(12):5573, 40 pp. doi: 10.2903/j.efsa.2018.5573

Requestor: European Commission

Question number: EFSA‐Q‐2018‐00747

Acknowledgements: in addition to the listed authors, EFSA, ECDC and the EURL wish to thank the following: Member State representatives that provided data on avian influenza outbreaks, animal populations or wrote case reports for this scientific output: Bulgaria (Aleksandra Miteva), Denmark (Pernille Dahl Nielsen), the Netherlands (Marcel Spierenburg); Dominique Bicout, Jan Arend Stegeman and Preben Willeberg for reviewing the document; Laura Amato, Ian Brown, Timm Harder and Nicola Lewis for the support provided to this scientific output.

Amendment: An editorial correction was carried out that does not materially affect the contents or outcome of this scientific output. Figure 8 was amended: In the legend, ‘HPAI (H5N1) outbreaks in birds’ was changed to ‘HPAI outbreaks in birds’; ‘the figure title ‘Geographical distribution of HPAI outbreaks in Europe, Asia and Africa by virus subtype and affected subpopulation, 16 August – 15 November 2018 (n=36)’ was changed to ‘Geographical distribution of HPAI outbreaks in Europe, Asia and Africa by virus subtype and affected subpopulation, 16 August – 15 November 2018 (n=39)’. To avoid confusion, the older version has been removed from the EFSA Journal, but is available on request, as is a version showing all the changes made.

Approved: 17 December 2018

Amended: 29 January 2019

References

  1. Adlhoch C, Dabrera G, Penttinen P, Pebody R and Country E, 2018. Protective Measures for Humans against Avian Influenza A(H5N8) Outbreaks in 22 European Union/European Economic Area Countries and Israel, 2016‐17. Emerging Infectious Disease, 24. doi: 10.3201/eid2410.180269 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Chinese National Influenza Center 2018. Chinese Influenza Weekly Report week 44 2018. Weekly Report, pp. Available online: http://www.chinaivdc.cn/cnic/en/Surveillance/WeeklyReport/201811/t20181109_197046.htm
  4. 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]
  5. Dharmayanti N, Thor SW, Zanders N, Hartawan R, Ratnawati A, Jang Y, Rodriguez M, Suarez DL, Samaan G, and Davis CT, 2018. Attenuation of highly pathogenic avian influenza A(H5N1) viruses in Indonesia following the reassortment and acquisition of genes from low pathogenicity avian influenza A virus progenitors. Emerging Microbes & Infection, 7, 147. doi: 10.1038/s41426-018-0147-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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. a. Scientific Report: Avian influenza overview May – August 2018. EFSA Journal 16(9):5230, 1831–4732. 43 pp. Available online: 10.2903/j.efsa.2018.5430. [DOI] [Google Scholar]
  7. 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. b. Scientific Report: Avian influenza overview February – May 2018. EFSA Journal 16(6):5358, 1831–4732. 50 pp. Available online: 10.2903/j.efsa.2018.5358. [DOI] [Google Scholar]
  8. 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. 55 pp. Available online: doi: 10.2903/j.efsa.2018.5240 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. EFSA , ECDC , EURL , 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 on the avian influenza overview October 2016 – August 2017. 15(10):5018, EFSA Journal 2017. 101 pp. Available online: doi: 10.2903/j.efsa.2017.5018 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. European Commission , online‐a. Animal Health ‐ Regulatory Committee presentations. Available online: https://ec.europa.eu/food/animals/health/regulatory_committee/presentations_en
  11. European Commission , online‐b. Animal Disease Notification System (ADNS). Available online: https://ec.europa.eu/food/animals/animal-diseases/not-system_en
  12. FAO (Food and Agriculture Organization) , online‐a. H7N9 situation update ‐ 24 November 2017. Available online: http://www.fao.org/ag/againfo/programmes/en/empres/h7n9/wave_6/Situation_update_2017_11_24.html
  13. FAO (Food and Agriculture Organization) , online‐b. EMPRES‐i ‐ Global Animal Disease Information System. Available online: http://empres-i.fao.org/eipws3g/
  14. GISAID , online. GISAID ‐ Homepage. Available online: https://www.gisaid.org/
  15. He J, Liu BY, Gong L, Chen Z, Chen XL, Hou S, Yu JL, Wu JB, Xia ZC, Latif A, Gao R, Su B and Liu Y, 2018a. Genetic characterization of the first detected human case of avian influenza A (H5N6) in Anhui Province. East China. Scientific Report, 8, 15282 10.1038/s41598-018-33356-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ilyicheva TN, Durymanov AG, Svyatchenko SV, Marchenko VY, Sobolev IA, Bakulina AY, Goncharova NI, Kolosova NP, Susloparov IM, Pyankova OG, Ryzhikov AB and Maksyutov RA, 2018. Humoral immunity to influenza in an at‐risk population and severe influenza cases in Russia in 2016‐2017. Archives of Virology. doi: 10.1007/s00705-018-3904-9 [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Jonas M, Sahesti A, Murwijati T, Lestariningsih CL, Irine I, Ayesda CS, Prihartini W and Mahardika GN, 2018. Identification of avian influenza virus subtype H9N2 in chicken farms in Indonesia. Preventive Veterinary Medicine, 159, 99–105. 10.1016/j.prevetmed.2018.09.003. [DOI] [PubMed] [Google Scholar]
  19. Krone O, Globig A, Ulrich R, Harder T, Schinkothe J, Herrmann C, Gerst S, Conraths FJ and Beer M, 2018. White‐Tailed Sea Eagle (Haliaeetus albicilla) Die‐Off Due to Infection with Highly Pathogenic Avian Influenza Virus, Subtype H5N8, in Germany. Viruses, 10. doi: 10.3390/v10090478 [DOI] [PMC free article] [PubMed]
  20. Kwon HI, Kim EH, Kim YI, Park SJ, Si YJ, Lee IW, Nguyen HD, Yu KM, Yu MA, Jung JH, Choi WS, Kwon JJ, Ahn SJ, Baek YH, Van Lai D, Lee OJ, Kim SW, Song MS, Yoon SW, Kim CJ, Webby RJ, Mo IP and Choi YK, 2018. Comparison of the pathogenic potential of highly pathogenic avian influenza (HPAI) H5N6, and H5N8 viruses isolated in South Korea during the 2016‐2017 winter season. Emerging Microbes & Infection, 7, 29 10.1038/s41426-018-0029-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kwon JH, Jeong S, Lee DH, Swayne DE, Kim YJ, Lee SH, Noh JY, Erdene‐Ochir TO, Jeong JH and Song CS, 2018. New Reassortant Clade 2.3.4.4b Avian Influenza A(H5N6) Virus in Wild Birds, South Korea, 2017‐18. Emerging Infection Disease, 24, 1953–1955. 10.3201/eid2410.180461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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. a. Characterization of a novel reassortant H5N6 highly pathogenic avian influenza virus clade 2.3.4.4 in Korea, 2017. Emerging Microbes & Infection, 7. doi: 10.1038/s41426-018-0104-3 [DOI] [PMC free article] [PubMed]
  23. Lee K, Lee EK, Lee H, Heo GB, Lee YN, Jung JY, Bae YC, So B, Lee YJ and Choi EJ, 2018b. Highly Pathogenic Avian Influenza A(H5N6) in Domestic Cats, South Korea. Emerging Infectious Diseases, 24, 2343–2347. 10.3201/eid2412.180290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lee YN, Cheon SH, Kye SJ, Lee EK, Sagong M, Heo GB, Kang YM, Cho HK, Kim YJ, Kang HM, Lee MH and Lee YJ, 2018. c. Novel reassortants of clade 2.3.4.4 H5N6 highly pathogenic avian influenza viruses possessing genetic heterogeneity in Republic of Korea in late 2017. Journal of Veterinary Science. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. MoA, (Ministry of Agriculture of the People's Republic of China) , online. H7N9 situation update. Available online: http://english.agri.gov.cn/
  27. Ndumu D, Zecchin B, Fusaro A, Arinaitwe E, Erechu R, Kidega E, Kayiwa J, Muwanga E, Kirumira M, Kirembe G, Lutwama J and Monne I, 2018. Highly pathogenic avian influenza H5N8 Clade 2.3.4.4B virus in Uganda, 2017. Infect Genet Evol, 66, 269–271. 10.1016/j.meegid.2018.10.010. [DOI] [PubMed] [Google Scholar]
  28. Nooruzzaman M, Haque ME, Chowdhury EH and Islam MR, 2018. Pathology of clade 2.3.2.1 avian influenza virus (H5N1) infection in quails and ducks in Bangladesh. Avian Pathology, 1–7. doi: 10.1080/03079457.2018.1535165 [DOI] [PubMed] [Google Scholar]
  29. OIE (World Organisation for Animal Health) , online. WAHIS Interface disease information. Available online: http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/Diseasehome
  30. Pohlmann A, Starick E, Grund C, Hoper D, Strebelow G, Globig A, Staubach C, Conraths FJ, Mettenleiter TC, Harder T and Beer M, 2018. Swarm incursions of reassortants of highly pathogenic avian influenza virus strains H5N8 and H5N5, clade 2.3.4.4b, Germany, winter 2016/17. Scientific Report, Jan 8, 15. doi: 10.1038/s41598-017-16936-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. The Government of the Hong Kong Special Administrative Region , 2018. CHP notified of human case of avian influenza A(H5N6) in Jiangsu. Available online: https://www.info.gov.hk/gia/general/201811/23/P2018112300411.htm
  32. WHO (World Health Organization) , 2016. International Health Regulations (2005) ‐ Third edition. Available online: http://www.who.int/ihr/publications/9789241580496/en/
  33. WHO (World Health Organization) , 2017. Operational Guidance on Sharing Influenza Viruses with Human Pandemic Potential (IVPP) under the Pandemic Influenza Preparedness (PIP) Framework. Available online: http://apps.who.int/iris/bitstream/handle/10665/259402/WHO-WHE-IHM-GIP-2017.3-eng.pdf;jsessionid=FF66316FB599ADA38D34499AA56765FA?sequence=1
  34. WHO (World Health Organization) , 2018. a. Influenza at the human‐animal interface ‐ Summary and assessment, 26 January to 2 March 2018. Available online: http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_02_03_2018.pdf?ua=1
  35. WHO (World Health Organization) , 2018. b. Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness ‐ September 2018. Available online: http://www.who.int/influenza/vaccines/virus/201809_zoonotic_vaccinevirusupdate.pdf?ua=1
  36. WHO (World Health Organization) , 2018. c. Influenza at the human‐animal interface; Summary and assessment, 22 September to 1 November 2018. Available online: http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_01_11_2018.pdf?ua=1
  37. WHO (World Health Organization) , 2018. d. Influenza at the human‐animal interface; Summary and assessment, 8 December 2017 to 25 January 2018., 5 pp. Available online: http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_25_01_2018_FINAL.pdf?ua=1
  38. WHO (World Health Organization) , 2018. e. Human infection with avian influenza A(H7N9) virus – China: Update 5 September 2018. Available online: http://www.who.int/csr/don/05-september-2018-ah7n9-china/en/
  39. WHO (World Health Organization) , online‐a. Human infection with avian influenza A(H7N4) virus – China: Update. Available online: http://www.who.int/csr/don/05-september-2018-ah7n9-china/en/ [Accessed on 18 September 2018]
  40. WHO (World Health Organization) , online‐b. Influenza ‐ Virus Sharing. Available online: http://www.who.int/influenza/pip/virus_sharing/en/ [Accessed on 4 September 2018]
  41. WUR (Wageningen University and Research) , online. Vogelgriep in Eemmeer. Available online: https://www.wur.nl/nl/Onderzoek-Resultaten/Onderzoeksinstituten/Bioveterinary-Research/show-bvr/Vogelgriep-in-Eemmeer.htm [Accessed on 3 December 2018]
  42. 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]
  43. Yegani S, Shoushtari AH, Eshratabadi F and Molouki A, 2018. Full sequence analysis of hemagglutinin and neuraminidase genes and proteins of highly pathogenic avian influenza H5N1 virus detected in Iran, 2015. Tropical Animal Health and Production. doi: 10.1007/s11250-018-1731-3 [DOI] [PubMed] [Google Scholar]
  44. Zeng X, Tian G, Shi J, Deng G, Li C and Chen H, 2018. Vaccination of poultry successfully eliminated human infection with H7N9 virus in China. Science China Life Sciences. doi: 10.1007/s11427-018-9420-1 [DOI] [PubMed] [Google Scholar]
  45. 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. Poulty Science, 97, 3793–3800. 10.3382/ps/pey187. [DOI] [PubMed] [Google Scholar]

Articles from EFSA Journal are provided here courtesy of Wiley

RESOURCES