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Published in: Virology Journal 1/2017

Open Access 01-12-2017 | Case report

Isolation and genetic characterization of a novel 2.2.1.2a H5N1 virus from a vaccinated meat-turkeys flock in Egypt

Authors: Ahmed H. Salaheldin, Jutta Veits, Hatem S. Abd El-Hamid, Timm C. Harder, Davud Devrishov, Thomas C. Mettenleiter, Hafez M. Hafez, Elsayed M. Abdelwhab

Published in: Virology Journal | Issue 1/2017

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Abstract

Background

Vaccination of poultry to control highly pathogenic avian influenza virus (HPAIV) H5N1 is used in several countries. HPAIV H5N1 of clade 2.2.1 which is endemic in Egypt has diversified into two genetic clades. Clade 2.2.1.1 represents antigenic drift variants in vaccinated commercial poultry while clade 2.2.1.2 variants are detected in humans and backyard poultry. Little is known about H5N1 infection in vaccinated turkeys under field conditions.

Case presentation

Here, we describe an HPAI H5N1 outbreak in a vaccinated meat-turkey flock in Egypt. Birds were vaccinated with inactivated H5N2 and H5N1 vaccines at 8 and 34 days of age, respectively. At 72nd day of age (38 days post last vaccination), turkeys exhibited mild respiratory signs, cyanosis of snood and severe congestion of the internal organs. Survivors had a reduction in feed consumption and body gain. A mortality of ~29% cumulated within 10 days after the onset of clinical signs. Laboratory diagnosis using RT-qPCRs revealed presence of H5N1 but was negative for H7 and H9 subtypes. A substantial antigenic drift against different serum samples from clade 2.2.1.1 and clade 2.3.4.4 was observed. Based on full genome sequence analysis the virus belonged to clade 2.2.1.2 but clustered with recent H5N1 viruses from 2015 in poultry in Israel, Gaza and Egypt in a novel subclade designated here 2.2.1.2a which is distinct from 2014/2015 2.2.1.2 viruses. These viruses possess 2.2.1.2 clade-specific genetic signatures and also mutations in the HA similar to those in clade 2.2.1.1 that enabled evasion from humoral immune response. Taken together, this manuscript describes a recent HPAI H5N1 outbreak in vaccinated meat-turkeys in Egypt after infection with a virus representing novel distinct 2.2.1.2a subclade.

Conclusions

Infection with HPAIV H5N1 in commercial turkeys resulted in significant morbidity and mortality despite of vaccination using H5 vaccines. The isolated virus showed antigenic drift and clustered in a novel cluster designated here 2.2.1.2a related to viruses in poultry in Israel, Gaza and Egypt. Enforcement of biosecurity and constant update of vaccine virus strains may be helpful to protect vaccinated birds and prevent spillover infection to neighbouring countries.
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Literature
1.
go back to reference Yoon SW, Webby RJ, Webster RG. Evolution and ecology of influenza a viruses. Curr Top Microbiol Immunol. 2014;385:359–75.PubMed Yoon SW, Webby RJ, Webster RG. Evolution and ecology of influenza a viruses. Curr Top Microbiol Immunol. 2014;385:359–75.PubMed
2.
3.
go back to reference Guan Y, Peiris JS, Lipatov AS, Ellis TM, Dyrting KC, Krauss S, Zhang LJ, Webster RG, Shortridge KF. Emergence of multiple genotypes of H5N1 avian influenza viruses in hong Kong SAR. Proc Natl Acad Sci U S A. 2002;99:8950–5.CrossRefPubMedPubMedCentral Guan Y, Peiris JS, Lipatov AS, Ellis TM, Dyrting KC, Krauss S, Zhang LJ, Webster RG, Shortridge KF. Emergence of multiple genotypes of H5N1 avian influenza viruses in hong Kong SAR. Proc Natl Acad Sci U S A. 2002;99:8950–5.CrossRefPubMedPubMedCentral
4.
go back to reference Smith GJ, Donis RO. World health organization/world organisation for animal HF, agriculture organization HEWG: 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. 2015;9:271–6.CrossRefPubMedPubMedCentral Smith GJ, Donis RO. World health organization/world organisation for animal HF, agriculture organization HEWG: 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. 2015;9:271–6.CrossRefPubMedPubMedCentral
5.
go back to reference Yassine HM, Al-Natour MQ, Lee CW, Saif YM. Interspecies and intraspecies transmission of triple reassortant H3N2 influenza a viruses. Virol J. 2007;4:129.CrossRefPubMedPubMedCentral Yassine HM, Al-Natour MQ, Lee CW, Saif YM. Interspecies and intraspecies transmission of triple reassortant H3N2 influenza a viruses. Virol J. 2007;4:129.CrossRefPubMedPubMedCentral
6.
go back to reference Pillai SP, Pantin-Jackwood M, Yassine HM, Saif YM, Lee CW. The high susceptibility of turkeys to influenza viruses of different origins implies their importance as potential intermediate hosts. Avian Dis. 2010;54:522–6.CrossRefPubMed Pillai SP, Pantin-Jackwood M, Yassine HM, Saif YM, Lee CW. The high susceptibility of turkeys to influenza viruses of different origins implies their importance as potential intermediate hosts. Avian Dis. 2010;54:522–6.CrossRefPubMed
7.
go back to reference Ladman BS, Driscoll CP, Pope CR, Slemons RD, Gelb Jr J. Potential of low pathogenicity avian influenza viruses of wild bird origin to establish experimental infections in turkeys and chickens. Avian Dis. 2010;54:1091–4.CrossRefPubMed Ladman BS, Driscoll CP, Pope CR, Slemons RD, Gelb Jr J. Potential of low pathogenicity avian influenza viruses of wild bird origin to establish experimental infections in turkeys and chickens. Avian Dis. 2010;54:1091–4.CrossRefPubMed
8.
go back to reference Cilloni F, Toffan A, Giannecchini S, Clausi V, Azzi A, Capua I, Terregino C. Increased pathogenicity and shedding in chickens of a wild bird-origin low pathogenicity avian influenza virus of the H7N3 subtype following multiple in vivo passages in quail and turkey. Avian Dis. 2010;54:555–7.CrossRefPubMed Cilloni F, Toffan A, Giannecchini S, Clausi V, Azzi A, Capua I, Terregino C. Increased pathogenicity and shedding in chickens of a wild bird-origin low pathogenicity avian influenza virus of the H7N3 subtype following multiple in vivo passages in quail and turkey. Avian Dis. 2010;54:555–7.CrossRefPubMed
9.
go back to reference Capua I, Mutinelli F, Marangon S, Alexander DJ. H7N1 avian influenza in Italy (1999 to 2000) in intensively reared chickens and turkeys. Avian Pathol. 2000;29:537–43.CrossRefPubMed Capua I, Mutinelli F, Marangon S, Alexander DJ. H7N1 avian influenza in Italy (1999 to 2000) in intensively reared chickens and turkeys. Avian Pathol. 2000;29:537–43.CrossRefPubMed
10.
go back to reference Spackman E, Gelb Jr J, Preskenis LA, Ladman BS, Pope CR, Pantin-Jackwood MJ, McKinley ET. The pathogenesis of low pathogenicity H7 avian influenza viruses in chickens, ducks and turkeys. Virol J. 2010;7:331.CrossRefPubMedPubMedCentral Spackman E, Gelb Jr J, Preskenis LA, Ladman BS, Pope CR, Pantin-Jackwood MJ, McKinley ET. The pathogenesis of low pathogenicity H7 avian influenza viruses in chickens, ducks and turkeys. Virol J. 2010;7:331.CrossRefPubMedPubMedCentral
11.
go back to reference Pasick J, Berhane Y, Joseph T, Bowes V, Hisanaga T, Handel K, Alexandersen S. Reassortant highly pathogenic influenza a H5N2 virus containing gene segments related to Eurasian H5N8 in British Columbia, Canada, 2014. Sci Rep. 2015;5:9484.CrossRefPubMedPubMedCentral Pasick J, Berhane Y, Joseph T, Bowes V, Hisanaga T, Handel K, Alexandersen S. Reassortant highly pathogenic influenza a H5N2 virus containing gene segments related to Eurasian H5N8 in British Columbia, Canada, 2014. Sci Rep. 2015;5:9484.CrossRefPubMedPubMedCentral
12.
go back to reference Lee DH, Bahl J, Torchetti MK, Killian ML, Ip HS, DeLiberto TJ, Swayne DE. Highly pathogenic avian influenza viruses and generation of novel reassortants, united states, 2014–2015. Emerg Infect Dis. 2016;22:1283–5.CrossRefPubMedPubMedCentral Lee DH, Bahl J, Torchetti MK, Killian ML, Ip HS, DeLiberto TJ, Swayne DE. Highly pathogenic avian influenza viruses and generation of novel reassortants, united states, 2014–2015. Emerg Infect Dis. 2016;22:1283–5.CrossRefPubMedPubMedCentral
13.
go back to reference Harder T, Maurer-Stroh S, Pohlmann A, Starick E, Horeth-Bontgen D, Albrecht K, Pannwitz G, Teifke J, Gunalan V, Lee RT, et al. Influenza a(H5N8) virus similar to strain in Korea causing highly pathogenic avian influenza in Germany. Emerg Infect Dis. 2015;21:860–3.CrossRefPubMedPubMedCentral Harder T, Maurer-Stroh S, Pohlmann A, Starick E, Horeth-Bontgen D, Albrecht K, Pannwitz G, Teifke J, Gunalan V, Lee RT, et al. Influenza a(H5N8) virus similar to strain in Korea causing highly pathogenic avian influenza in Germany. Emerg Infect Dis. 2015;21:860–3.CrossRefPubMedPubMedCentral
14.
go back to reference Bos ME, Nielen M, Koch G, Stegeman A, De Jong MC. Effect of H7N1 vaccination on highly pathogenic avian influenza H7N7 virus transmission in turkeys. Vaccine. 2008;26:6322–8.CrossRefPubMed Bos ME, Nielen M, Koch G, Stegeman A, De Jong MC. Effect of H7N1 vaccination on highly pathogenic avian influenza H7N7 virus transmission in turkeys. Vaccine. 2008;26:6322–8.CrossRefPubMed
15.
go back to reference Poetri ON, Van Boven M, Claassen I, Koch G, Wibawan IW, Stegeman A, Van den Broek J, Bouma A. Silent spread of highly pathogenic avian influenza H5N1 virus amongst vaccinated commercial layers. Res Vet Sci. 2014;97:637–41.CrossRefPubMed Poetri ON, Van Boven M, Claassen I, Koch G, Wibawan IW, Stegeman A, Van den Broek J, Bouma A. Silent spread of highly pathogenic avian influenza H5N1 virus amongst vaccinated commercial layers. Res Vet Sci. 2014;97:637–41.CrossRefPubMed
16.
go back to reference El-Zoghby EF, Arafa AS, Kilany WH, Aly MM, Abdelwhab EM, Hafez HM. Isolation of avian influenza H5N1 virus from vaccinated commercial layer flock in Egypt. Virol J. 2012;9:294.CrossRefPubMedPubMedCentral El-Zoghby EF, Arafa AS, Kilany WH, Aly MM, Abdelwhab EM, Hafez HM. Isolation of avian influenza H5N1 virus from vaccinated commercial layer flock in Egypt. Virol J. 2012;9:294.CrossRefPubMedPubMedCentral
17.
go back to reference Long NT, Thanh TT, van Doorn HR, Vu PP, Dung PT, Dung TT, Tien TN, Thao DT, Hung P, Quang NV, et al. Recent avian influenza virus a/H5N1 evolution in vaccinated and unvaccinated poultry from farms in southern Vietnam, january-march 2010. Transbound Emerg Dis. 2011;58:537–43.CrossRefPubMedPubMedCentral Long NT, Thanh TT, van Doorn HR, Vu PP, Dung PT, Dung TT, Tien TN, Thao DT, Hung P, Quang NV, et al. Recent avian influenza virus a/H5N1 evolution in vaccinated and unvaccinated poultry from farms in southern Vietnam, january-march 2010. Transbound Emerg Dis. 2011;58:537–43.CrossRefPubMedPubMedCentral
18.
go back to reference Hafez MH, Arafa A, Abdelwhab EM, Selim A, Khoulosy SG, Hassan MK, Aly MM. Avian influenza H5N1 virus infections in vaccinated commercial and backyard poultry in Egypt. Poult Sci. 2010;89:1609–13.CrossRefPubMed Hafez MH, Arafa A, Abdelwhab EM, Selim A, Khoulosy SG, Hassan MK, Aly MM. Avian influenza H5N1 virus infections in vaccinated commercial and backyard poultry in Egypt. Poult Sci. 2010;89:1609–13.CrossRefPubMed
19.
go back to reference Savill NJ, St Rose SG, Keeling MJ, Woolhouse ME. Silent spread of H5N1 in vaccinated poultry. Nature. 2006;442:757.CrossRefPubMed Savill NJ, St Rose SG, Keeling MJ, Woolhouse ME. Silent spread of H5N1 in vaccinated poultry. Nature. 2006;442:757.CrossRefPubMed
20.
go back to reference Parker CD, Irvine RM, Slomka MJ, Pavlidis T, Hesterberg U, Essen S, Cox B, Ceeraz V, Alexander DJ, Manvell R, et al. Outbreak of Eurasian lineage H5N1 highly pathogenic avian influenza in turkeys in great Britain in november 2007. Vet Rec. 2014;175:282.CrossRefPubMed Parker CD, Irvine RM, Slomka MJ, Pavlidis T, Hesterberg U, Essen S, Cox B, Ceeraz V, Alexander DJ, Manvell R, et al. Outbreak of Eurasian lineage H5N1 highly pathogenic avian influenza in turkeys in great Britain in november 2007. Vet Rec. 2014;175:282.CrossRefPubMed
21.
go back to reference Abdelwhab EM, Hassan MK, Abdel-Moneim AS, Naguib MM, Mostafa A, Hussein IT, Arafa A, Erfan AM, Kilany WH, Agour MG, et al. Introduction and enzootic of a/H5N1 in Egypt: virus evolution, pathogenicity and vaccine efficacy ten years on. Infect Genet Evol. 2016;40:80–90.CrossRefPubMed Abdelwhab EM, Hassan MK, Abdel-Moneim AS, Naguib MM, Mostafa A, Hussein IT, Arafa A, Erfan AM, Kilany WH, Agour MG, et al. Introduction and enzootic of a/H5N1 in Egypt: virus evolution, pathogenicity and vaccine efficacy ten years on. Infect Genet Evol. 2016;40:80–90.CrossRefPubMed
22.
go back to reference Aly MM, Arafa A, Hassan MK. Epidemiological findings of outbreaks of disease caused by highly pathogenic H5N1 avian influenza virus in poultry in Egypt during 2006. Avian Dis. 2008;52:269–77.CrossRefPubMed Aly MM, Arafa A, Hassan MK. Epidemiological findings of outbreaks of disease caused by highly pathogenic H5N1 avian influenza virus in poultry in Egypt during 2006. Avian Dis. 2008;52:269–77.CrossRefPubMed
23.
go back to reference Abdel-Moneim AS, Shany SA, Fereidouni SR, Eid BT, El-Kady MF, Starick E, Harder T, Keil GM. Sequence diversity of the haemagglutinin open reading frame of recent highly pathogenic avian influenza H5N1 isolates from Egypt. Arch Virol. 2009;154:1559–62.CrossRefPubMed Abdel-Moneim AS, Shany SA, Fereidouni SR, Eid BT, El-Kady MF, Starick E, Harder T, Keil GM. Sequence diversity of the haemagglutinin open reading frame of recent highly pathogenic avian influenza H5N1 isolates from Egypt. Arch Virol. 2009;154:1559–62.CrossRefPubMed
24.
go back to reference Watanabe Y, Ibrahim MS, Ellakany HF, Kawashita N, Mizuike R, Hiramatsu H, Sriwilaijaroen N, Takagi T, Suzuki Y, Ikuta K. Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. PLoS Pathog. 2011;7:e1002068.CrossRefPubMedPubMedCentral Watanabe Y, Ibrahim MS, Ellakany HF, Kawashita N, Mizuike R, Hiramatsu H, Sriwilaijaroen N, Takagi T, Suzuki Y, Ikuta K. Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. PLoS Pathog. 2011;7:e1002068.CrossRefPubMedPubMedCentral
25.
go back to reference Arafa AS, Naguib MM, Luttermann C, Selim AA, Kilany WH, Hagag N, Samy A, Abdelhalim A, Hassan MK, Abdelwhab EM, et al. Emergence of a novel cluster of influenza a(H5N1) virus clade 2.2.1.2 with putative human health impact in Egypt, 2014/15. Euro Surveill. 2015;20:2–8.CrossRefPubMed Arafa AS, Naguib MM, Luttermann C, Selim AA, Kilany WH, Hagag N, Samy A, Abdelhalim A, Hassan MK, Abdelwhab EM, et al. Emergence of a novel cluster of influenza a(H5N1) virus clade 2.2.1.2 with putative human health impact in Egypt, 2014/15. Euro Surveill. 2015;20:2–8.CrossRefPubMed
26.
go back to reference Naguib MM, Abdelwhab EM, Harder TC. Evolutionary features of influenza a/H5N1 virus populations in Egypt: poultry and human health implications. Arch Virol. 2016;161:1963–7.CrossRefPubMed Naguib MM, Abdelwhab EM, Harder TC. Evolutionary features of influenza a/H5N1 virus populations in Egypt: poultry and human health implications. Arch Virol. 2016;161:1963–7.CrossRefPubMed
27.
go back to reference El-Shesheny R, Kandeil A, Bagato O, Maatouq AM, Moatasim Y, Rubrum A, Song MS, Webby RJ, Ali MA, Kayali G. Molecular characterization of avian influenza H5N1 virus in Egypt and the emergence of a novel endemic subclade. J Gen Virol. 2014;95:1444–63.CrossRefPubMedPubMedCentral El-Shesheny R, Kandeil A, Bagato O, Maatouq AM, Moatasim Y, Rubrum A, Song MS, Webby RJ, Ali MA, Kayali G. Molecular characterization of avian influenza H5N1 virus in Egypt and the emergence of a novel endemic subclade. J Gen Virol. 2014;95:1444–63.CrossRefPubMedPubMedCentral
28.
go back to reference Li C, Bu Z, Chen H. Avian influenza vaccines against H5N1 ‘bird flu’. Trends Biotechnol. 2014;32:147–56.CrossRefPubMed Li C, Bu Z, Chen H. Avian influenza vaccines against H5N1 ‘bird flu’. Trends Biotechnol. 2014;32:147–56.CrossRefPubMed
29.
go back to reference Kapczynski DR, Dorsey K, Chrzastek K, Moraes M, Jackwood M, Hilt D, Gardin Y. Vaccine protection of turkeys against H5N1 highly pathogenic avian influenza virus with a recombinant turkey herpesvirus expressing the hemagglutinin gene of avian influenza. Avian Dis. 2016;60:413–7.CrossRefPubMed Kapczynski DR, Dorsey K, Chrzastek K, Moraes M, Jackwood M, Hilt D, Gardin Y. Vaccine protection of turkeys against H5N1 highly pathogenic avian influenza virus with a recombinant turkey herpesvirus expressing the hemagglutinin gene of avian influenza. Avian Dis. 2016;60:413–7.CrossRefPubMed
30.
go back to reference Tian G, Zeng X, Li Y, Shi J, Chen H. Protective efficacy of the H5 inactivated vaccine against different highly pathogenic H5N1 avian influenza viruses isolated in china and Vietnam. Avian Dis. 2010;54:287–9.CrossRefPubMed Tian G, Zeng X, Li Y, Shi J, Chen H. Protective efficacy of the H5 inactivated vaccine against different highly pathogenic H5N1 avian influenza viruses isolated in china and Vietnam. Avian Dis. 2010;54:287–9.CrossRefPubMed
31.
go back to reference Zeng X, Chen P, Liu L, Deng G, Li Y, Shi J, Kong H, Feng H, Bai J, Li X, et al. Protective efficacy of an H5N1 inactivated vaccine against challenge with lethal H5N1, H5N2, H5N6, and H5N8 influenza viruses in chickens. Avian Dis. 2016;60:253–5.CrossRefPubMed Zeng X, Chen P, Liu L, Deng G, Li Y, Shi J, Kong H, Feng H, Bai J, Li X, et al. Protective efficacy of an H5N1 inactivated vaccine against challenge with lethal H5N1, H5N2, H5N6, and H5N8 influenza viruses in chickens. Avian Dis. 2016;60:253–5.CrossRefPubMed
32.
go back to reference Zeng X, Deng G, Liu L, Li Y, Shi J, Chen P, Feng H, Liu J, Guo X, Mao S, et al. Protective efficacy of the inactivated H5N1 influenza vaccine Re-6 against different clades of H5N1 viruses isolated in china and the democratic People’s republic of Korea. Avian Dis. 2016;60:238–40.CrossRefPubMed Zeng X, Deng G, Liu L, Li Y, Shi J, Chen P, Feng H, Liu J, Guo X, Mao S, et al. Protective efficacy of the inactivated H5N1 influenza vaccine Re-6 against different clades of H5N1 viruses isolated in china and the democratic People’s republic of Korea. Avian Dis. 2016;60:238–40.CrossRefPubMed
33.
go back to reference Liu LL, Zeng XY, Chen PC, Deng GH, Li YB, Shi JZ, Gu CY, Kong HH, Suzuki Y, Jiang YP, et al. Characterization of clade 7.2 H5 avian influenza viruses that continue to circulate in chickens in china. J Virol. 2016;90:9797–805.CrossRefPubMedPubMedCentral Liu LL, Zeng XY, Chen PC, Deng GH, Li YB, Shi JZ, Gu CY, Kong HH, Suzuki Y, Jiang YP, et al. Characterization of clade 7.2 H5 avian influenza viruses that continue to circulate in chickens in china. J Virol. 2016;90:9797–805.CrossRefPubMedPubMedCentral
34.
go back to reference Grund C, el SM A, Arafa AS, Ziller M, Hassan MK, Aly MM, Hafez HM, Harder TC, Beer M. Highly pathogenic avian influenza virus H5N1 from Egypt escapes vaccine-induced immunity but confers clinical protection against a heterologous clade 2.2.1 Egyptian isolate. Vaccine. 2011;29:5567–73.CrossRefPubMed Grund C, el SM A, Arafa AS, Ziller M, Hassan MK, Aly MM, Hafez HM, Harder TC, Beer M. Highly pathogenic avian influenza virus H5N1 from Egypt escapes vaccine-induced immunity but confers clinical protection against a heterologous clade 2.2.1 Egyptian isolate. Vaccine. 2011;29:5567–73.CrossRefPubMed
35.
go back to reference Kilany WH, Abdelwhab EM, Arafa AS, Selim A, Safwat M, Nawar AA, Erfan AM, Hassan MK, Aly MM, Hafez HM. Protective efficacy of H5 inactivated vaccines in meat turkey poults after challenge with Egyptian variant highly pathogenic avian influenza H5N1 virus. Vet Microbiol. 2011;150:28–34.CrossRefPubMed Kilany WH, Abdelwhab EM, Arafa AS, Selim A, Safwat M, Nawar AA, Erfan AM, Hassan MK, Aly MM, Hafez HM. Protective efficacy of H5 inactivated vaccines in meat turkey poults after challenge with Egyptian variant highly pathogenic avian influenza H5N1 virus. Vet Microbiol. 2011;150:28–34.CrossRefPubMed
36.
go back to reference Abdelwhab EM, Grund C, Aly MM, Beer M, Harder TC, Hafez HM. Multiple dose vaccination with heterologous H5N2 vaccine: immune response and protection against variant clade 2.2.1 highly pathogenic avian influenza H5N1 in broiler breeder chickens. Vaccine. 2011;29:6219–25.CrossRefPubMed Abdelwhab EM, Grund C, Aly MM, Beer M, Harder TC, Hafez HM. Multiple dose vaccination with heterologous H5N2 vaccine: immune response and protection against variant clade 2.2.1 highly pathogenic avian influenza H5N1 in broiler breeder chickens. Vaccine. 2011;29:6219–25.CrossRefPubMed
37.
go back to reference Watanabe Y, Arai Y, Daidoji T, Kawashita N, Ibrahim MS, El-Gendy Eel D, Hiramatsu H, Kubota-Koketsu R, Takagi T, Murata T, et al. Characterization of H5N1 influenza virus variants with hemagglutinin mutations isolated from patients. MBio. 2015;6(2). Watanabe Y, Arai Y, Daidoji T, Kawashita N, Ibrahim MS, El-Gendy Eel D, Hiramatsu H, Kubota-Koketsu R, Takagi T, Murata T, et al. Characterization of H5N1 influenza virus variants with hemagglutinin mutations isolated from patients. MBio. 2015;6(2).
38.
go back to reference Schmier S, Mostafa A, Haarmann T, Bannert N, Ziebuhr J, Veljkovic V, Dietrich U, Pleschka S. In silico prediction and experimental confirmation of HA residues conferring enhanced human receptor specificity of H5N1 influenza a viruses. Sci Rep. 2015;5:11434.CrossRefPubMedPubMedCentral Schmier S, Mostafa A, Haarmann T, Bannert N, Ziebuhr J, Veljkovic V, Dietrich U, Pleschka S. In silico prediction and experimental confirmation of HA residues conferring enhanced human receptor specificity of H5N1 influenza a viruses. Sci Rep. 2015;5:11434.CrossRefPubMedPubMedCentral
39.
go back to reference Duvvuri VR, Duvvuri B, Cuff WR, Wu GE, Wu J. Role of positive selection pressure on the evolution of H5N1 hemagglutinin. Genomics Proteomics Bioinformatics. 2009;7:47–56.CrossRefPubMedPubMedCentral Duvvuri VR, Duvvuri B, Cuff WR, Wu GE, Wu J. Role of positive selection pressure on the evolution of H5N1 hemagglutinin. Genomics Proteomics Bioinformatics. 2009;7:47–56.CrossRefPubMedPubMedCentral
40.
go back to reference Cattoli G, Milani A, Temperton N, Zecchin B, Buratin A, Molesti E, Aly MM, Arafa A, Capua I. Antigenic drift in H5N1 avian influenza virus in poultry is driven by mutations in major antigenic sites of the hemagglutinin molecule analogous to those for human influenza virus. J Virol. 2011;85:8718–24.CrossRefPubMedPubMedCentral Cattoli G, Milani A, Temperton N, Zecchin B, Buratin A, Molesti E, Aly MM, Arafa A, Capua I. Antigenic drift in H5N1 avian influenza virus in poultry is driven by mutations in major antigenic sites of the hemagglutinin molecule analogous to those for human influenza virus. J Virol. 2011;85:8718–24.CrossRefPubMedPubMedCentral
41.
go back to reference Abdelwhab EM, Arafa A-S, Stech J, Grund C, Stech O, Graeber-Gerberding M, Beer M, Hassan MK, Aly MM, Harder TC, Hafez HM. Diversifying evolution of highly pathogenic H5N1 avian influenza virus in Egypt from 2006 to 2011. Virus Genes. 2012;45(23):14.CrossRefPubMed Abdelwhab EM, Arafa A-S, Stech J, Grund C, Stech O, Graeber-Gerberding M, Beer M, Hassan MK, Aly MM, Harder TC, Hafez HM. Diversifying evolution of highly pathogenic H5N1 avian influenza virus in Egypt from 2006 to 2011. Virus Genes. 2012;45(23):14.CrossRefPubMed
42.
go back to reference Munier S, Larcher T, Cormier-Aline F, Soubieux D, Su B, Guigand L, Labrosse B, Cherel Y, Quere P, Marc D, Naffakh N. A genetically engineered waterfowl influenza virus with a deletion in the stalk of the neuraminidase has increased virulence for chickens. J Virol. 2010;84:940–52.CrossRefPubMed Munier S, Larcher T, Cormier-Aline F, Soubieux D, Su B, Guigand L, Labrosse B, Cherel Y, Quere P, Marc D, Naffakh N. A genetically engineered waterfowl influenza virus with a deletion in the stalk of the neuraminidase has increased virulence for chickens. J Virol. 2010;84:940–52.CrossRefPubMed
45.
go back to reference Hoffmann B, Hoffmann D, Henritzi D, Beer M, Harder TC. Riems influenza a typing array (RITA): an RT-qPCR-based low density array for subtyping avian and mammalian influenza a viruses. Sci Rep. 2016;6:27211.CrossRefPubMedPubMedCentral Hoffmann B, Hoffmann D, Henritzi D, Beer M, Harder TC. Riems influenza a typing array (RITA): an RT-qPCR-based low density array for subtyping avian and mammalian influenza a viruses. Sci Rep. 2016;6:27211.CrossRefPubMedPubMedCentral
46.
go back to reference Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza a viruses. Arch Virol. 2001;146:2275–89.CrossRefPubMed Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza a viruses. Arch Virol. 2001;146:2275–89.CrossRefPubMed
47.
go back to reference Kreibich A, Stech J, Mettenleiter TC, Stech O. Simultaneous one-tube full-length amplification of the NA, NP, M, and NS genes of influenza a viruses for reverse genetics. J Virol Methods. 2009;159:308–10.CrossRefPubMed Kreibich A, Stech J, Mettenleiter TC, Stech O. Simultaneous one-tube full-length amplification of the NA, NP, M, and NS genes of influenza a viruses for reverse genetics. J Virol Methods. 2009;159:308–10.CrossRefPubMed
48.
go back to reference Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.CrossRefPubMed Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.CrossRefPubMed
49.
go back to reference Katoh K, Standley DM. MAFFT: iterative refinement and additional methods. Methods Mol Biol. 2014;1079:131–46.CrossRefPubMed Katoh K, Standley DM. MAFFT: iterative refinement and additional methods. Methods Mol Biol. 2014;1079:131–46.CrossRefPubMed
50.
go back to reference Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8.
51.
go back to reference Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.CrossRefPubMed Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.CrossRefPubMed
52.
go back to reference Santorum JM, Darriba D, Taboada GL, Posada D. Jmodeltest.org: selection of nucleotide substitution models on the cloud. Bioinformatics. 2014;30:1310–1.CrossRefPubMedPubMedCentral Santorum JM, Darriba D, Taboada GL, Posada D. Jmodeltest.org: selection of nucleotide substitution models on the cloud. Bioinformatics. 2014;30:1310–1.CrossRefPubMedPubMedCentral
Metadata
Title
Isolation and genetic characterization of a novel 2.2.1.2a H5N1 virus from a vaccinated meat-turkeys flock in Egypt
Authors
Ahmed H. Salaheldin
Jutta Veits
Hatem S. Abd El-Hamid
Timm C. Harder
Davud Devrishov
Thomas C. Mettenleiter
Hafez M. Hafez
Elsayed M. Abdelwhab
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2017
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-017-0697-5

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