Abstract
Between 1 September and 15 November 2017, 48 A(H5N8) highly pathogenic avian influenza (HPAI) outbreaks in poultry holdings and 9 H5 HPAI wild bird events were reported within Europe. A second epidemic HPAI A(H5N8) wave started in Italy on the third week of July and is still ongoing on 15 November 2017. The Italian epidemiological investigations indicated that sharing of vehicles, sharing of personnel and close proximity to infected holdings are the more likely sources of secondary spread in a densely populated poultry area. Despite the ongoing human exposures to infected poultry during the outbreaks, no transmission to humans has been identified in the EU. The report includes an update of the list of wild bird target species for passive surveillance activities that is based on reported AI‐infected wild birds since 2006. The purpose of this list is to provide information on which bird species to focus in order to achieve the most effective testing of dead birds for detection of H5 HPAI viruses. Monitoring the avian influenza situation in other continents revealed the same risks as in the previous report (October 2016‐August 2017): the recent human case of HPAI A(H5N6) in China underlines the continuing threat of this avian influenza virus to human health and possible introduction via migratory wild birds into Europe. Close monitoring is required of the situation in Africa with regards to HPAI of the subtypes A(H5N1) and A(H5N8), given the rapidity of the evolution and the uncertainty on the geographical distribution of these viruses. Interactions between EFSA and member states have taken place to initiate discussions on improving the quality of data collections and to find a step‐wise approach to exchange relevant (denominator) data without causing an additional resource burden.
Keywords: avian influenza, HPAI/LPAI, monitoring, poultry, captive birds, wild birds, humans
Supporting information
Maximum likelihood phylogenetic tree of the HA gene.
Suggested citation: EFSA (European Food Safety Authority) , ECDC (European Centre for Disease Prevention and Control) , EURL (European Reference Laboratory on Avian Influenza) , Brown I, Kuiken T, Mulatti P, Smietanka K, Staubach C, Stroud D, Therkildsen OR, Willeberg P, Baldinelli F, Verdonck F and Adlhoch C, 2017. Scientific report: Avian influenza overview September – November 2017. EFSA Journal 2017;15(12):5141, 70 pp. doi: 10.2903/j.efsa.2017.5141
Requestor: European Commission
Question number: EFSA‐Q‐2017‐00649
Competing interests: In line with EFSA's policy on declarations of interest, the following working group (WG) experts: Ian Brown, Paolo Mulatti, Krzysztof Smietanka and Christoph Staubach, have declared that they have current involvement in risk assessment activities at national level related to avian influenza, which constitutes a conflict of interest (CoI) with the mandate of the EFSA WG in hand. The CoIs have been waived and the waivers were adopted in accordance with Article 16(5) of the Decision of the Executive Director on Declarations of Interest of 31 July 2017 EFSA/LRA/DEC/02/2014, available at http://www.efsa.europa.eu/sites/default/files/corporate_publications/files/independencerules2014.pdf. Pursuant to Article 16(7) of the above mentioned Decision, the concerned experts were allowed to take part in the discussions and in the drafting phase of the EFSA Scientific report on Avian influenza monitoring (Art. 31) ‐ overview October 2016 – August 2017, and have not been allowed to be, or act as, a chairman, a vice‐chairman or rapporteur of the WG.
Acknowledgements: in addition to the listed authors, EFSA, ECDC and the EURL wish to thank the following: Kaja Kaasik Aaslav, Epidemic Intelligence team at ECDC and Pasi Penttinen, Head of the Disease Programme Influenza and other Respiratory Viruses for the support provided to this scientific output; Members States representatives that provided the data on AI outbreaks, animal population and/or wrote case reports for this scientific output: Italy (Anna Sorgente, Alessandra Azzolini, Lebana Bonfanti, Giovanni Cunial, Diletta Fornasiero, Stefano Marangon); Dominique Bicout and Arjan Stegeman for reviewing the document.
Figures from 1 to 6 and Table 1 © EURL; Figures from 7 to 14 © EFSA; Figures 15, 17, 18, 20, 21, 22, 23, 24 © Friedrich‐Loeffler‐Institut (FLI); Figures 16, 19, 25, 26, 27, 28 and Table 3 © ECDC.
References
- 1. Adlhoch C, Brown IH, Angelova SG, Bálint Á, Bouwstra R, Buda S, Castrucci MR, Dabrera G, Dán Á, Grund C, Harder T, van der Hoek W, Krisztalovics K, Parry‐Ford F, Popescu R, Wallensten A, Zdravkova A, Zohari S, Tsolova S and Penttinen P, 2016. Highly pathogenic avian influenza A(H5N8) outbreaks: protection and management of exposed people in Europe, 2014/15 and 2016. Eurosurveillance, 21, 30419 10.2807/1560-7917.ES.2016.21.49.30419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Arafa AS, Naguib MM, Luttermann C, Selim AA, Kilany WH, Hagag N, Samy A, Abdelhalim A, Hassan MK, Abdelwhab EM, Makonnen Y, Dauphin G, Lubroth J, Mettenleiter TC, Beer M, Grund C and Harder TC, 2015. Emergence of a novel cluster of influenza A(H5N1) virus clade 2.2.1.2 with putative human health impact in Egypt, 2014/15. Eurosurveillance, 20, 2–8. [DOI] [PubMed] [Google Scholar]
- 3. Azab AA, Arafa A, Selim A, Hassan MK, Bazid AI, Sultan AH, Hussein HA and Abdelwhab EM, 2017 Sep. Pathogenicity of the Egyptian A/H5N1 avian influenza viruses in chickens. Microb Pathog., 110, 471–476. doi: 10.1016/j.micpath.2017.07.026. Epub 2017 Jul 21. [DOI] [PubMed] [Google Scholar]
- 4. Barman S, Marinova‐Petkova A, Hasan MK, Akhtar S, El‐Shesheny R, Turner JC, Franks J, Walker D, Seiler J, Friedman K, Kercher L, Jeevan T, Darnell D, Kayali G, Jones‐Engel L, McKenzie P, Krauss S, Webby RJ, Webster RG and Feeroz MM, 2017. Role of domestic ducks in the emergence of a new genotype of highly pathogenic H5N1 avian influenza A viruses in Bangladesh. Emerging Microbes & Infections, 6, e72. doi: 10.1038/emi.2017.60. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Beerens N, Heutink R, Bergervoet SA, Harders F, Bossers A and Koch G, 2017. Multiple Reassorted Viruses as Cause of Highly Pathogenic Avian Influenza A(H5N8) Virus Epidemic, the Netherlands, 2016. Emerging Infectious Diseases, 23, 1974–1981. doi: 10.3201/eid2312.171062. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Belser JA, Johnson A, Pulit‐Penaloza JA, Pappas C, Pearce MB, Tzeng W‐P, Hossain MJ, Ridenour C, Wang L, Chen L‐M, Wentworth DE, Katz JM, Maines TR and Tumpey TM, 2017. Pathogenicity testing of influenza candidate vaccine viruses in the ferret model. Virology, 511, 135–141. doi: 10.1016/j.virol.2017.08.024 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Bertran K, Swayne DE, Pantin‐Jackwood MJ, Kapczynski DR, Spackman E and Suarez DL, 2016. Lack of chicken adaptation of newly emergent Eurasian H5N8 and reassortant H5N2 high pathogenicity avian influenza viruses in the US is consistent with restricted poultry outbreaks in the Pacific flyway during 2014‐2015. Virology, 494, 190–197. [DOI] [PubMed] [Google Scholar]
- 8. Bertran K, Lee DH, Pantin‐Jackwood MJ, Spackman E, Balzli C, Suarez DL, Swayne DE, 2017. Pathobiology of Clade 2.3.4.4 H5Nx High‐Pathogenicity Avian Influenza Virus Infections in Minor Gallinaceous Poultry Supports Early Backyard Flock Introductions in the Western United States in 2014‐2015. Journal of Virology, 91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Bhat S, Nagarajan S, Kumar M, Murugkar HV, Kalaiyarasu S, Venkatesh G and Tosh C, 2017. Antigenic characterization of H5N1 highly pathogenic avian influenza viruses isolated from poultry in India, 2006‐2015. Archives of Virology, 162, 487–494. [DOI] [PubMed] [Google Scholar]
- 10. Bi YH, Liu HZ, Xiong CC, Liu D, Shi WF, Li MX, Liu SL, Chen J, Chen G, Li Y, Yang GX, Lei YS, Xiong YP, Lei FM, Wang HZ, Chen QJ, Chen JJ and Gao GF, 2016. Novel avian influenza A (H5N6) viruses isolated in migratory waterfowl before the first human case reported in China, 2014. Scientific Reports, 6, 10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Briand FX, Schmitz A, Ogor K, Le Prioux A, Guillou‐Cloarec C, Guillemoto C, Allee C, Le Bras M, Hirchaud E, Quenault H, Touzain F, Cherbonnel‐Pansart M, Lemaitre E, Courtillon C, Gares H, Daniel P, Fediaevsky A Massin P, Blanchard Y, Eterradossi N, Van Der Werf S, Jestin V and Niqueux E, 2017. Emerging highly pathogenic H5 avian influenza viruses in France during winter 2015/16: phylogenetic analyses and markers for zoonotic potential. Eurosurveillance, 22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. CDC (Centre for Disease Control) , online. Bird Infections with Highly‐Pathogenic Avian Influenza A (H5N2), (H5N8), and (H5N1) Viruses: Recommendations for Human Health Investigations and Response. Available online: https://emergency.cdc.gov/han/han00378.asp [Accessed: 18 December 2017]
- 13. CHP (Centre for Health Protection of the Department of Health Hong Kong) , 2017. Reporting period: November 5, 2017 ‐ November 11, 2017 (Week 45). Avian Influenza Report, 13, 45, 7 pp. Available online: http://www.chp.gov.hk/files/pdf/2017avian_influenza_report_vol13_wk45.pdf [Google Scholar]
- 14. CHP (Centre for Health Protection of the Department of Health Hong Kong) , online. CHP notified of human case of avian influenza A(H5N6) in Guangxi. Available online: http://www.info.gov.hk/gia/general/201711/20/P2017112000784.htm [Accessed: 28/11/2017]
- 15. Chen LJ, Lin XD, Tian JH, Liao Y, Ying XH, Shao JW, Yu B, Guo JJ, Wang MR, Peng Y, Shi M, Holmes EC, Yang ZQ and Zhang YZ, 2017. Diversity, evolution and population dynamics of avian influenza viruses circulating in the live poultry markets in China. Virology, 505, 33–41. [DOI] [PubMed] [Google Scholar]
- 16. Chinese National Influenza Center 2017. Chinese Influenza Weekly Report, Week 34 2017. Available online: http://www.chinaivdc.cn/cnic/en/Surveillance/WeeklyReport/201709/t20170905_151981.htm [Accessed: 18 December 2017]
- 17. Chinese CDC (Chinese Center for Disease Control and Prevention) , online. Avian Influenza ‐ disease outbreaks. Available online: http://www.chinacdc.cn/en/http://www.chinaivdc.cn/cnic/en/Surveillance/WeeklyReport/201709/t20170905_151981.htm
- 18. CONSISE (Consortium for the Standardization of Influenza Seroepidemiology) , 2013. CONSISE and avian influenza H7N9. Available online: http://consise.tghn.org/articles/consise-and-avian-influenza-h7n9/ [Accessed: 18 December 2017]
- 19. Du Y, Chen M, Yang J, Jia Y, Han S, Holmes EC and Cui J, 2017. Molecular evolution and emergence of H5N6 avian influenza virus in central China. Journal of Virology, 91, e00143–00117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Ducatez M, Sonnberg S, Crumpton JC, Rubrum A, Phommachanh P, Douangngeun B, Peiris M, Guan Y, Webster R and Webby R, 2017. Highly pathogenic avian influenza H5N1 clade 2.3.2.1 and clade 2.3.4 viruses do not induce a clade‐specific phenotype in mallard ducks. Journal of General Virology, 98, 1232–1244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. El Romeh A, Zecchin B, Fusaro A, Ibrahim E, El Bazzal B, El Hage J, Milani A, Zamperin G and Monne I, 2017. Highly pathogenic avian influenza H5N1 Clade 2.3.2.1c Virus in Lebanon, 2016. Avian Diseases, 61, 271–273. [DOI] [PubMed] [Google Scholar]
- 22. EFSA AHAW Panel (EFSA Panel on Animal Health and Welfare) , More S, Bicout D, Bøtner A, Butterworth A, Calistri P, Depner K, Edwards S, Garin‐Bastuji B, Good M, GortazarSchmidt C, Michel V, Miranda MA, Nielsen SS, Raj M, Sihvonen L, Spoolder H, Thulke H‐H, Velarde A,Willeberg P, Winckler C, Breed A, Brouwer A, Guillemain M, Harder T, Monne I, Roberts H, Baldinelli F,Barrucci F, Fabris C, Martino L, Mosbach‐Schulz O, Verdonck F, Morgado J and Stegeman JA, 2017. Scientific opinion on avian influenza. EFSA Journal 2017;15(10):4991, 233 pp. [Google Scholar]
- 23. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control) , 2014. Highly pathogenic avian influenza A subtype A(H5N8). EFSA Journal, 12, 3941‐n/a. doi: 10.2903/j.efsa.2014.3941 [DOI] [Google Scholar]
- 24. EFSA (European Food Safety Authority) , ECDC (European Centre for Disease Prevention and Control) , EURL (European Union Reference Laboratory for Avian influenza) , 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. EFSA Journal 2017;15(10), 101 pp. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. ECDC (European Centre for Disease Prevention and Control) 2006. Technical Report on Avian Influenza Portfolio ‐ Collected risk assessments, technical guidance to public health authorities and advice to the general public. ECDC, Stockholm, 50 pp. Available online: http://ecdc.europa.eu/en/publications/Publications/0606_TER_Avian_Influenza_Portafolio.pdf
- 26. ECDC (European Centre for Disease Prevention and Control) , 2014. Technical Report on Risk assessment guidelines for infectious diseases transmitted on aircraft (RAGIDA) ‐ Influenza. ECDC, Stockholm, 18 pp. Available online: http://www.ecdc.europa.eu/en/publications/Publications/influenza-RAGIDA-2014.pdf
- 27. ECDC (European Centre for Disease prevention and Control) 2017. Expert opinion on neuraminidase inhibitors for the prevention and treatment of influenza ‐ Review of recent systematic reviews and meta‐analyses. ECDC, Stockholm, 43 pp. Available online: https://ecdc.europa.eu/sites/portal/files/documents/Scientific-advice-neuraminidase-inhibitors-2017.pdf
- 28. ECDC (European Centre for Disease Prevention and Control), online. Available online: https://ecdc.europa.eu/en/home [Accessed: 18 December 2017]
- 29. FAO (Food and Agriculture Organization of the United Nations) , online‐a. A(H5N8) HPAI situation update. Available online: http://www.fao.org/ag/againfo/programmes/en/empres/H5N8/situation_update.html [Accessed: 14 November 2016]
- 30. FAO (Food and Agriculture Organization of the United Nations) , online‐b. H7N9 situation update. Available online: http://www.fao.org/ag/againfo/programmes/en/empres/h7n9/ [Accessed: 25 October 2017]
- 31. 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. Emerg Infect Dis, 23, 1543–1547. doi: 10.3201/eid2309.170539 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32. Ghafouri SA, Langeroudi AG, Maghsoudloo H, Tehrani F, Khaltabadifarahani R, Abdollahi H and Fallah MH, 2017a. Phylogenetic study‐based hemagglutinin (HA) gene of highly pathogenic avian influenza virus (H5N1) detected from backyard chickens in Iran, 2015. Virus Genes, 53, 117–120. [DOI] [PubMed] [Google Scholar]
- 33. Ghafouri SA, GhalyanchiLangeroudi A, Maghsoudloo H, Kh Farahani R, Abdollahi H, Tehrani F and Fallah MH, 2017b. Clade 2.3.4.4 avian influenza A (H5N8) outbreak in commercial poultry, Iran, 2016: the first report and update data. Trop Anim Health Production, 49, 1089–1093. [DOI] [PubMed] [Google Scholar]
- 34. Globig A, Starick E, Homeier T, Pohlmann A, Grund C, Wolf P, Zimmermann A, Wolf C, Heim D, Schlosser H, Zander S, Beer M, Conraths FJ and Harder TC, 2017. Epidemiological and Molecular Analysis of an Outbreak of Highly Pathogenic Avian Influenza H5N8 clade 2.3.4.4 in a German Zoo: Effective Disease Control with Minimal Culling. Transboundary and Emerging Diseases, 64, 1813–1824. [DOI] [PubMed] [Google Scholar]
- 35. Guo HB, de Vries E, McBride R, Dekkers J, Peng WJ, Bouwman KM, Nycholat C, Verheije MH, Paulson JC, van Kuppeveld FJM and de Haan CAM, 2017. Highly pathogenic influenza A(H5Nx) viruses with altered H5 receptorbinding specificity. Emerging Infectious Diseases, 23, 220–231. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36. Hiono T, Okamatsu M, Matsuno K, Haga A, Iwata R, Nguyen LT, Suzuki M, Kikutani Y, Kida H, Onuma M and Sakoda Y, 2017. Characterization of H5N6 highly pathogenic avian influenza viruses isolated from wild and captive birds in the winter season of 2016‐2017 in northern Japan. Microbiology and Immunology, 61, 387–397. [DOI] [PubMed] [Google Scholar]
- 37. Imai M, Watanabe T, Kiso M, Nakajima N, Yamayoshi S, Iwatsuki‐Horimoto K, Hatta M, Yamada S, Ito M, Sakai‐Tagawa Y, Shirakura M, Takashita E, Fujisaki S, McBride R, Thompson AJ, Takahashi K, Maemura T, Mitake H, Chiba S, Zhong G, Fan S, Oishi K, Yasuhara A, Takada K, Nakao T, Fukuyama S, Yamashita M, Lopes TJS, Neumann G, Odagiri T, Watanabe S, Shu Y, Paulson JC, Hasegawa H and Kawaoka Y, 2017. A Highly Pathogenic Avian H7N9 Influenza Virus Isolated from A Human Is Lethal in Some Ferrets Infected via Respiratory Droplets. Cell Host Microbe, 22(615‐626), e618. doi: 10.1016/j.chom.2017.09.008 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38. International Severe Acute Respiratory and Emerging Infection Consortium , 2013. ISARIC and WHO SARI and Natural History Protocols. Accessed on 7 May. Available online: http://isaric.tghn.org/articles/isaric-and-who-sari-and-natural-history-protocols/
- 39. Jeong J, Woo C, Ip HS, An I, Kim Y, Lee K, Jo S‐D, Son K, Lee S, Oem J‐K, Wang S‐J, Kim Y, Shin J, Sleeman J and Jheong W, 2017. Identification of two novel reassortant avian influenza a (H5N6) viruses in whooper swans in Korea, 2016. Virology Journal, 14, 60. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40. 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. doi: 10.1093/cid/cix334 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41. Jiao PR, Cui J, Song YF, Song H, Zhao ZS, Wu SY, Qu NN, Wang NC, Ouyang GW and Liao M, 2016. New reassortant H5N6 highly pathogenic avian influenza viruses in Southern China, 2014. Frontiers in Microbiology, 7, 12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42. Kandeil A, Kayed A, Moatasim Y, Webby RJ, McKenzie PP, Kayali G and Ali MA, 2017a. Genetic characterization of highly pathogenic avian influenza A H5N8 viruses isolated from wild birds in Egypt. Journal of General Virology, 98, 1573–1586. 10.1099/jgv.0.000847 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43. Kang HM, Lee EK, Song BM, Heo GB, Jung J, Jang I, Bae YC, Jung SC and Lee YJ, 2017. Experimental infection of mandarin duck with highly pathogenic avian influenza A (H5N8 and H5N1) viruses. Veterinary Microbiology, 198, 59–63. [DOI] [PubMed] [Google Scholar]
- 44. Kaplan BS, Torchetti MK, Lager KM, Webby RJ and Vincent AL, 2017. Absence of clinical disease and contact transmission of HPAI H5NX clade 2.3.4.4 from North America in experimentally infected pigs. Influenza Other Respir Viruses, 11, 464–470. doi: 10.1111/irv.12463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45. Kleyheeg E, Slaterus R, Bodewes R, Rijks JM, Spierenburg MAH, Beerens N, Kelder L, Poen MJ, Stegeman JA, Fouchier RAM, Kuiken T and van der Jeugd HP, 2017. Deaths among Wild Birds during Highly Pathogenic Avian Influenza A(H5N8) Virus Outbreak, the Netherlands. Emerging Infectious Diseases, 23, 2050–2054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46. Kim YI, Park SJ, Kwon HI, Kim EH, Si YJ, Jeong JH, Lee IW, Nguyen HD, Kwon JJ, Choi WS, Song MS, Kim CJ and Choi YK, 2017. Genetic and phylogenetic characterizations of a novel genotype of highly pathogenic avian influenza (HPAI) H5N8 viruses in 2016/2017 in South Korea. Infection Genetics and Evolution, 53, 56–67. [DOI] [PubMed] [Google Scholar]
- 47. Kwon JH, Noh YK, Lee DH, Yuk SS, Erdene‐Ochir TO, Noh JY, Hong WT, Jeong JH, Jeong S, Gwon GB, Song CS and Nahm SS, 2017a. Experimental infection with highly pathogenic H5N8 avian influenza viruses in the Mandarin duck (Aix galericulata) and domestic pigeon (Columba livia domestica). Veterinary Microbiology, 203, 95–102. [DOI] [PubMed] [Google Scholar]
- 48. Kwon JH, Lee DH, Jeong JH, Yuk SS, Erdene‐Ochir TO, Noh JY, Hong WT, Jeong S, Gwon GB, Lee SW, Choi IS, Song CS, 2017b. Isolation of an H5N8 Highly Pathogenic Avian Influenza Virus Strain from Wild Birds in Seoul, a Highly Urbanized Area in South Korea Journal of Wildlife Diseases 53(3):630–635. [DOI] [PubMed] [Google Scholar]
- 49. Laurie KL, Huston P, Riley S, Katz JM, Willison DJ, Tam JS, Mounts AW, Hoschler K, Miller E, Vandemaele K, Broberg E, Van Kerkhove MD and Nicoll A, 2013. Influenza serological studies to inform public health action: best practices to optimise timing, quality and reporting. Influenza Other Respi Viruses, 7, 211–224. doi: 10.1111/j.1750-2659.2012.0370a.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50. Laleye A, Joannis T, Shittu I, Meseko C, Zamperin G, Milani A, Zecchin B, Fusaro A, Monne I and Abolnik C, 2017. A two‐year monitoring period of the genetic properties of clade 2.3.2.1c H5N1 viruses in Nigeria reveals the emergence and co‐circulation of distinct genotypes. Infection, Genetics and Evolution, 57, 98–105. doi: 10.1016/j.meegid.2017.10.027. [DOI] [PubMed] [Google Scholar]
- 51. Lee DH, Kwon JH, Noh JY, Park JK, Yuk SS, Erdene‐Ochir TO, Lee JB, Park SY, Choi IS, Lee SW and Song CS, 2016. Pathogenicity of the Korean A(H5N8) highly pathogenic avian influenza virus in commercial domestic poultry species. Avian Pathology, 45, 208–211. doi: 10.1080/03079457.2016.1142502. [DOI] [PubMed] [Google Scholar]
- 52. Lee EK, Song BM, Kang HM, Woo SH, Heo GB, Jung SC, Park YH, Lee YJ and Kim JH, 2016b. Experimental infection of SPF and Korean native chickens with highly pathogenic avian influenza virus (H5N8). Poultry Science, 95, 1015–1019. 10.3382/ps/pew028 [DOI] [PubMed] [Google Scholar]
- 53. Lee DH, Sharshov K, Swayne DE, Kurskaya O, Sobolev I, Kabilov M, Alekseev A, Irza V and Shestopalov A, 2017. Novel reassortant clade 2.3.4.4 avian influenza A(H5N8) virus in wild aquatic birds, Russia, 2016. Emerging Infectious Diseases, 23, 359–360. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54. Li M, Liu H, Bi Y, Sun J, Wong G, Liu D, Li L, Liu J, Chen Q, Wang H, He Y, Shi W, Gao GF and Chen J, 2017. Highly pathogenic avian influenza A(H5N8) virus in wild migratory birds, qinghai lake, China. Emerging Infectious Diseases, 23, 637–641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55. Li XY, Fu YG, Yang JY, Guo J, He JJ, Guo JH, Weng ST, Jia YN, Liu B, Li XY, Zhu QY and Chen HL, 2015. Genetic and biological characterization of two novel reassortant H5N6 swine influenza viruses in mice and chickens. Infection Genetics and Evolution, 36, 462–466. [DOI] [PubMed] [Google Scholar]
- 56. Liu L, Zeng X, Chen P, Deng G, Li Y, Shi J, Gu C, Kong H, Suzuki Y, Jiang Y, Tian G and Chen H, 2016. Characterization of clade 7.2 H5 avian influenza viruses that continue to circulate in chickens in China. Journal of Virology, 90, 9797–9805. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57. Marchenko VY, Susloparov IM, Komissarov AB, Fadeev A, Goncharova NI, Shipovalov AV, Svyatchenko SV, Durymanov AG, Ilyicheva TN, Salchak LK, Svintitskaya EP, Mikheev VN and Ryzhikov AB, 2017. Reintroduction of highly pathogenic avian influenza A/H5N8 virus of clade 2.3.4.4. in Russia. Archives of Virology, 162, 1381–1385. [DOI] [PubMed] [Google Scholar]
- 58. Marinova‐Petkova A, Shanmuganatham K, Feeroz MM, Jones‐Engel L, Hasan MK, Akhtar S, Turner J, Walker D, Seiler P, Franks J, McKenzie P, Krauss S, Webby RJ and Webster RG, 2016a. The continuing evolution of H5N1 and H9N2 influenza viruses in Bangladesh between 2013 and 2014. Avian Diseases, 60, 108–117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59. Marinova‐Petkova A, Franks J, Tenzin S, Dahal N, Dukpa K, Dorjee J, Feeroz MM, Rehg JE, Barman S, Krauss S, McKenzie P, Webby RJ and Webster RG, 2016b. Highly pathogenic reassortant avian influenza A(H5N1) virus clade 2.3.2.1a in Poultry. Bhutan. Emerging Infectious Diseases, 22, 2137–2141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60. MoA (Ministry of Agriculture of the People's republic of China) , online. H7N9 situation update. Available online: http://www.moa.gov.cn/govpublic/ [Accessed: 18 December 2017]
- 61. Nagarajan S, Kumar M, Murugkar HV, Tripathi S, Shukla S, Agarwal S, Dubey G, Nagi RS, Singh VP and Tosh C, 2017. Novel reassortant highly pathogenic avian influenza (H5N8) virus in zoos, India. Emerging Infectious Diseases, 23, 717–719. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62. Naguib MM, Arafa AS, Parvin R, Beer M, Vahlenkamp T and Harder TC, 2017. Insights into genetic diversity and biological propensities of potentially zoonotic avian influenza H9N2 viruses circulating in Egypt. Virology, 511, 165–174. doi: 10.1016/j.virol.2017.08.028. [DOI] [PubMed] [Google Scholar]
- 63. Okamatsu M, Ozawa M, Soda K, Takakuwa H, Haga A, Hiono T, Matsuu A, Uchida Y, Iwata R, Matsuno K, Kuwahara M, Yabuta T, Usui T, Ito H, Onuma M, Sakoda Y, Saito T, Otsuki K, Ito T and Kida H, 2017. Characterization of highly pathogenic avian influenza virus A(H5N6), Japan, november 2016. Emerging Infectious Diseases, 23, 691–695. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64. Pantin‐Jackwood MJ, Costa‐Hurtado M, Bertran K, DeJesus E, Smith D and Swayne DE, 2017. Infectivity, transmission and pathogenicity of H5 highly pathogenic avian influenza clade 2.3.4.4 (H5N8 and H5N2) United States index viruses in Pekin ducks and Chinese geese. Veterinary Research, 48, 33 10.1186/s13567-017-0435-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65. Park S‐J, Kim E‐H, Kwon H‐I, Song M‐S, Kim SM, Kim Y‐I, Si Y‐J, Lee I‐W, Nguyen HD, Shin OS, Kim C‐J and Choi YK, 2017. Altered virulence of Highly Pathogenic Avian Influenza (HPAI) A(H5N8) reassortant viruses in mammalian models. Virulence, 5, 1–17. doi: 10.1080/21505594.2017.1366408. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66. Pearce MB, Pappas C, Gustin KM, Davis CT, Pantin‐Jackwood MJ, Swayne DE, Maines TR, Belser JA and Tumpey TM, 2017. Enhanced virulence of clade 2.3.2.1 highly pathogenic avian influenza A H5N1 viruses in ferrets. Virology, 502, 114–122. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 67. Pohlmann A, Starick E, Harder T, Grund C, Hoper D, Globig A, Staubach C, Dietze K, Strebelow G, Ulrich RG, Schinkothe J, Teifke JP, Conraths FJ, Mettenleiter TC and Beer M, 2017. Outbreaks among Wild Birds and Domestic Poultry Caused by Reassorted Influenza A(H5N8) Clade 2.3.4.4 Viruses, Germany, 2016. Emerging Infectious Diseases, 23, 633–636. doi: 10.3201/eid2304.161949. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68. Qi X, Cui L, Yu H, Ge Y and Tang F, 2014. Whole‐genome sequence of a reassortant H5N6 avian influenza virus isolated from a live poultry market in China, 2013. Genome Announcements, 2, e00706–e00714. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69. Rashid PMA, Saeed NM and Dyary HO, 2017. Genetic characterization and phylogenic analysis of H5N1 avian influenza virus detected in peafowl in Kirkuk province, Iraq. Journal of Medical Virology, 89, 1179–1185. [DOI] [PubMed] [Google Scholar]
- 70. Salaheldin AH, Veits J, El‐Hamid HSA, Harder TC, Devrishov D, Mettenleiter TC, Hafez HM and Abdelwhab EM, 2017. Isolation and genetic characterization of a novel 2.2.1.2a H5N1 virus from a vaccinated meat‐turkeys flock in Egypt. Virology Journal, 14, 11. doi: 10.1186/s12985-017-0697-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 71. Shittu I, Meseko CA, Gado DA, Olawuyi AK, Chinyere CN, Anefu E, Solomon P, Okewole PA, Shamaki D and Joannis TM, 2017. Highly pathogenic avian influenza (H5N1) in Nigeria in 2015: evidence of widespread circulation of WA2 clade 2.3.2.1c. Archives of Virology, 162, 841–847. [DOI] [PubMed] [Google Scholar]
- 72. Si Y, Lee I, Kim E, Kim Y, Kwon H, Park S, Nguyen HD, Kim SM, Kwon J, Choi W, Beak YH, Song M, Kim C, Webby RJ and Choi Y, 2017. Genetic characterisation of novel, highly pathogenic avian influenza (HPAI) H5N6 viruses isolated in birds, South Korea, November 2016. Eurosurveillance, 22, 2–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 73. Spackman E, Pantin‐Jackwood MJ, Kapczynski DR, Swayne DE and Suarez DL, 2016. H5N2 Highly Pathogenic Avian Influenza Viruses from the US 2014‐2015 outbreak have an unusually long pre‐clinical period in turkeys. BMC Veterinary Research, 12, 260. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74. Smith GJD and Donis RO and World Health Organization W , 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 and Other Respiratory Viruses, 9, 271–276. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 75. Sun HL, Pu J, Wei YD, Sun YP, Hu J, Liu LT, Xu GL, Gao WH, Li C, Zhang XX, Huang YH, Chang KC, Liu XF and Liu JH, 2016. Highly pathogenic avian influenza H5N6 viruses exhibit enhanced affinity for human type sialic acid receptor and in‐contact transmission in model ferrets. Journal of Virology, 90, 6235–6243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76. Taiwan CDC (Centers for Disease Control ROC, ‐Taiwan) , online. Available online: http://www.cdc.gov.tw/rwd/english [Accessed: 18 December 2017]
- 77. Tanikawa T, Kanehira K, Tsunekuni R, Uchida Y, Takemae N and Saito T, 2016. Pathogenicity of H5N8 highly pathogenic avian influenza viruses isolated from a wild bird fecal specimen and a chicken in Japan in 2014. Microbiol Immunology, 60, 243–252. [DOI] [PubMed] [Google Scholar]
- 78. Torchetti MK, Killian ML, Dusek RJ, Pedersen JC, Hines N, Bodenstein B, White CL and Ip HS, 2015. Novel H5 clade 2.3.4.4 reassortant (H5N1) virus from a green‐winged teal in Washington. USA. Genome Announcements, 3, e00195–00115. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 79. Van Kerkhove MD, Broberg E, Engelhardt OG, Wood J, Nicoll A and committee Cs, 2013. The consortium for the standardization of influenza seroepidemiology (CONSISE): a global partnership to standardize influenza seroepidemiology and develop influenza investigation protocols to inform public health policy. Influenza Other Respi Viruses, 7, 231–234. doi: 10.1111/irv.12068 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80. Woo C, Kwon JH, Lee DH, Kim Y, Lee K, Jo SD, Son KD, Oem JK, Wang SJ, Kim Y, Shin J, Song CS, Jheong W and Jeong J, 2017. Novel reassortant clade 2.3.4.4 avian influenza A (H5N8) virus in a grey heron in South Korea in 2017. Archives of Virology, 162, 3887–3891. doi: 10.1007/s00705-017-3547-2 Epub 2017 Sep 12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81. WHO (World Health Organization) , 2013. Laboratory Procedures Serological detection of avian influenza A(H7N9) virus infections by modified horse red blood cells haemagglutination‐inhibition assay. WHO, Geneva, 12 pp. Available online at: http://www.who.int/influenza/gisrs_laboratory/cnic_serological_diagnosis_hai_a_h7n9_20131220.pdf?ua=1
- 82. WHO (World Health Organization) , 2016a. Influenza at the human‐animal interface; Summary and assessment, 22 November to 19 December 2016. WHO, Geneva, 7 pp. Available online: http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_12_19_2016.pdf?ua=1
- 83. WHO (World Health Organization) , 2016b. International Health Regulations (2005) ‐ Third edition. WHO, Geneva, 84 pp. Available online: http://www.who.int/ihr/publications/9789241580496/en/
- 84. WHO (World Health Organization) , 2017a. Influenza at the human‐animal interface; Summary and assessment, 28 September to 30 October 2017. WHO, Geneva, 4 pp. Available online: http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_10_30_2017.pdf?ua=1
- 85. WHO (World Health Organization) , 2017b. Influenza at the human‐animal interface; Summary and assessment, 25 July 2017 to 27 September 2017. WHO, Geneva, 8 pp. Available online: http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_09_27_2017.pdf?ua=1
- 86. WHO (World Health Organization) , 2017c. Executive summary of the 9th meeting of the WHO working group RT‐PCR for the detection and subtyping of influenza viruses. Weekly Epidemiological Record, 92, 609–610. [PubMed] [Google Scholar]
- 87. WHO (World Health Organization) , 2017d. Zoonotic influenza viruses: antigenic and genetic characteristics and development of candidate vaccine viruses for pandemic preparedness. Weekly Epidemiological Record, 92, 633–647.29052410 [Google Scholar]
- 88. WHO (World Health Organization) , 2017e. Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness, September 2017. WHO, Geneva, 14 pp. Available online: http://www.who.int/influenza/vaccines/virus/201709_zoonotic_vaccinevirusupdate.pdf?ua=1
- 89. Wu HB, Lu RF, Peng XM, Peng XR, Chen B, Cheng LF and Wu NP, 2017. Molecular characterization of a novel reassortant H7N6 subtype avian influenza virus from poultry in Eastern China, in 2016. Archives of Virology, 162, 1341–1347. [DOI] [PubMed] [Google Scholar]
- 90. Xu W, Dai Y, Hua C, Wang Q, Zou P, Deng Q, Jiang S and Lu L, 2017. Genomic signature analysis of the recently emerged highly pathogenic A(H5N8) avian influenza virus: implying an evolutionary trend for bird‐to‐human transmission. Microbes and Infection. doi: 10.1016/j.micinf.2017.08.006 [DOI] [PubMed] [Google Scholar]
- 91. Yang L, Zhu WF, Li XD, Bo H, Zhang Y, Zou SM, Gao RB, Dong J, Zhao X, Chen WB, Dong LB, Zou XH, Xing YC, Wang DY and Shu YL, 2017. Genesis and dissemination of highly pathogenic H5N6 avian influenza viruses. Journal of Virology, 91, 13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 92. Yuk SS, Lee DH, Park JK, Tseren‐Ochir EO, Kwon JH, Noh JY and Song CS, 2017. Experimental infection of dogs with highly pathogenic avian influenza virus (H5N8). J Vet Sci, 18, 381–384. doi: 10.4142/jvs.2017.18.S1.381 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 93. Zhou L, Chen E, Bao C, Xiang N, Wu J, Wu S, Shi J, Wang X, Zheng Y, Zhang Y, Ren R, Greene CM, Havers F, Iuliano AD, Song Y, Li C, Chen T, Wang Y, Li D, Ni D, Zhang Y, Feng Z, Uyeki TM and Li Q, 2018. Clusters of human infection and human‐to‐human transmission of avian influenza A(H7N9) virus, China, 2013–2017. Emerging Infectious Diseases, 24. doi: 10.3201/eid2402.171565 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
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Supplementary Materials
Maximum likelihood phylogenetic tree of the HA gene.