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Published in: Virology Journal 1/2014

Open Access 01-12-2014 | Research

Phylogenetic and antigenic characterization of reassortant H9N2 avian influenza viruses isolated from wild waterfowl in the East Dongting Lake wetland in 2011–2012

Authors: Yun Zhu, Shixiong Hu, Tian Bai, Lei Yang, Xiang Zhao, Wenfei Zhu, Yiwei Huang, Zhihong Deng, Hong Zhang, Zhiyong Bai, Mingdong Yu, Jianfei Huang, Yuelong Shu

Published in: Virology Journal | Issue 1/2014

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Abstract

Background

Wild waterfowl are recognized as the natural reservoir for influenza A viruses. Two distinct lineages, the American and Eurasian lineages, have been identified in wild birds. Gene flow between the two lineages is limited. The H9N2 virus has become prevalent in poultry throughout Eurasia, and mainly circulates in wild ducks and shorebirds in North America.

Methods

In this study, 22 H9N2 avian influenza viruses were isolated from wild waterfowl feces in East Dongting Lake Nature Reserve in November 2011 and March 2012. The phylogenetic, molecular, and antigenic characteristics of these viruses were analyzed based on analyses of the whole genome sequence of each isolate.

Results

Phylogenetic analyses indicated that these H9N2 viruses were generated by reassortment events. The HA, NA, PA, and NS genes were derived from the American gene pool, and the other four genes were derived from the Eurasian gene pool. Antigenic analyses indicated that these viruses were significantly different from the Eurasian lineage viruses.

Conclusions

This study presents the isolation of novel intercontinental recombinant H9N2 viruses from wild waterfowl in the East Dongting Lake wetland. The novel genotype H9N2 virus has not been detected in poultry in the region yet, and may be transmitted to naïve birds in poultry farms. Therefore, our results highlight the need for ongoing surveillance of wild birds and poultry in this region.
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Literature
1.
go back to reference Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev. 1992, 56: 152-179.PubMedPubMedCentral Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev. 1992, 56: 152-179.PubMedPubMedCentral
2.
go back to reference Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD: Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol. 2005, 79: 2814-2822. 10.1128/JVI.79.5.2814-2822.2005.PubMedPubMedCentralCrossRef Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD: Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol. 2005, 79: 2814-2822. 10.1128/JVI.79.5.2814-2822.2005.PubMedPubMedCentralCrossRef
3.
go back to reference Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA: Global patterns of influenza a virus in wild birds. Science. 2006, 312: 384-388. 10.1126/science.1122438.PubMedCrossRef Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA: Global patterns of influenza a virus in wild birds. Science. 2006, 312: 384-388. 10.1126/science.1122438.PubMedCrossRef
4.
go back to reference Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Camey PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO: New World Bats Harbor Diverse Influenza A Viruses. PLoS Pathog. 2013, 9: e1003657-10.1371/journal.ppat.1003657.PubMedPubMedCentralCrossRef Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Camey PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO: New World Bats Harbor Diverse Influenza A Viruses. PLoS Pathog. 2013, 9: e1003657-10.1371/journal.ppat.1003657.PubMedPubMedCentralCrossRef
5.
go back to reference Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, XU C, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO: A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A. 2012, 109: 4269-4274. 10.1073/pnas.1116200109.PubMedPubMedCentralCrossRef Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, XU C, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO: A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A. 2012, 109: 4269-4274. 10.1073/pnas.1116200109.PubMedPubMedCentralCrossRef
6.
go back to reference Saito T, Horimoto T, Kawaoka Y, Senne DA, Webster RG: Emergence of a potentially pathogenic H5N2 influenza virus in chickens. Virology. 1994, 201: 277-284. 10.1006/viro.1994.1292.PubMedCrossRef Saito T, Horimoto T, Kawaoka Y, Senne DA, Webster RG: Emergence of a potentially pathogenic H5N2 influenza virus in chickens. Virology. 1994, 201: 277-284. 10.1006/viro.1994.1292.PubMedCrossRef
7.
go back to reference Alexander DJ: An overview of the epidemiology of avian influenza. Vaccine. 2007, 25: 5637-5644. 10.1016/j.vaccine.2006.10.051.PubMedCrossRef Alexander DJ: An overview of the epidemiology of avian influenza. Vaccine. 2007, 25: 5637-5644. 10.1016/j.vaccine.2006.10.051.PubMedCrossRef
8.
go back to reference Munster VJ, Wallensten A, Baas C, Rimmelzwaan GF, Schutten M, Olsen B, Osterhaus AD, Fouchier RA: Mallards and highly pathogenic avian influenza ancestral viruses, northern Europe. Emerg Infect Dis. 2005, 11: 1545-1551. 10.3201/eid1110.050546.PubMedPubMedCentralCrossRef Munster VJ, Wallensten A, Baas C, Rimmelzwaan GF, Schutten M, Olsen B, Osterhaus AD, Fouchier RA: Mallards and highly pathogenic avian influenza ancestral viruses, northern Europe. Emerg Infect Dis. 2005, 11: 1545-1551. 10.3201/eid1110.050546.PubMedPubMedCentralCrossRef
9.
go back to reference Hossain MJ, Hickman D, Perez DR: Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. PLoS One. 2008, 3: e3170-10.1371/journal.pone.0003170.PubMedPubMedCentralCrossRef Hossain MJ, Hickman D, Perez DR: Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. PLoS One. 2008, 3: e3170-10.1371/journal.pone.0003170.PubMedPubMedCentralCrossRef
10.
go back to reference Xu KM, Smith GJ, Bahl J, Duan L, Tai H, Vijaykrishna D, Wang J, Zhang JX, Li KS, Fan XH, Webster RG, Chen H, Peiris JS, Guan Y: The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol. 2007, 81: 10389-10401. 10.1128/JVI.00979-07.PubMedPubMedCentralCrossRef Xu KM, Smith GJ, Bahl J, Duan L, Tai H, Vijaykrishna D, Wang J, Zhang JX, Li KS, Fan XH, Webster RG, Chen H, Peiris JS, Guan Y: The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol. 2007, 81: 10389-10401. 10.1128/JVI.00979-07.PubMedPubMedCentralCrossRef
11.
go back to reference Dong G, Luo J, Zhang H, Wang C, Duan M, Deliberto TJ, Nolte DL, Ji G, He H: Phylogenetic diversity and genotypical complexity of H9N2 influenza A viruses revealed by genomic sequence analysis. PLoS One. 2011, 6: e17212-10.1371/journal.pone.0017212.PubMedPubMedCentralCrossRef Dong G, Luo J, Zhang H, Wang C, Duan M, Deliberto TJ, Nolte DL, Ji G, He H: Phylogenetic diversity and genotypical complexity of H9N2 influenza A viruses revealed by genomic sequence analysis. PLoS One. 2011, 6: e17212-10.1371/journal.pone.0017212.PubMedPubMedCentralCrossRef
12.
go back to reference Sun Y, Pu J, Jiang Z, Guan T, Xia Y, Xu Q, Liu L, Ma B, Tian F, Brown EG, Liu J: Genotypic evolution and antigenic drift of H9N2 influenza viruses in China from 1994 to 2008. Vet Microbiol. 2010, 146 (3–4): 215-225.PubMedCrossRef Sun Y, Pu J, Jiang Z, Guan T, Xia Y, Xu Q, Liu L, Ma B, Tian F, Brown EG, Liu J: Genotypic evolution and antigenic drift of H9N2 influenza viruses in China from 1994 to 2008. Vet Microbiol. 2010, 146 (3–4): 215-225.PubMedCrossRef
13.
go back to reference Zhang H, Xu B, Chen Q, Chen Z: Characterization of H9N2 influenza viruses isolated from Dongting Lake wetland in 2007. Arch Virol. 2011, 156: 95-105. 10.1007/s00705-010-0836-4.PubMedCrossRef Zhang H, Xu B, Chen Q, Chen Z: Characterization of H9N2 influenza viruses isolated from Dongting Lake wetland in 2007. Arch Virol. 2011, 156: 95-105. 10.1007/s00705-010-0836-4.PubMedCrossRef
14.
go back to reference Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL, Lai RW, Orr WK, Shortridge KF: Human infection with influenza H9N2. Lancet. 1999, 354: 916-917. 10.1016/S0140-6736(99)03311-5.PubMedCrossRef Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL, Lai RW, Orr WK, Shortridge KF: Human infection with influenza H9N2. Lancet. 1999, 354: 916-917. 10.1016/S0140-6736(99)03311-5.PubMedCrossRef
15.
go back to reference Guo Y, Xie J, Wu K, Dong J, Wang M, Zhang Y, Guo J, Chen J, Chen Z, Li Z: Characterization of genome of A/Guangzhou/333/99(H9N2) virus. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi. 2002, 16: 142-145.PubMed Guo Y, Xie J, Wu K, Dong J, Wang M, Zhang Y, Guo J, Chen J, Chen Z, Li Z: Characterization of genome of A/Guangzhou/333/99(H9N2) virus. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi. 2002, 16: 142-145.PubMed
16.
go back to reference Matrosovich MN, Krauss S, Webster RG: H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology. 2001, 281: 156-162. 10.1006/viro.2000.0799.PubMedCrossRef Matrosovich MN, Krauss S, Webster RG: H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology. 2001, 281: 156-162. 10.1006/viro.2000.0799.PubMedCrossRef
17.
go back to reference Guan Y, Shortridge KF, Krauss S, Webster RG: Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong?. Proc Natl Acad Sci U S A. 1999, 96: 9363-9367. 10.1073/pnas.96.16.9363.PubMedPubMedCentralCrossRef Guan Y, Shortridge KF, Krauss S, Webster RG: Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong?. Proc Natl Acad Sci U S A. 1999, 96: 9363-9367. 10.1073/pnas.96.16.9363.PubMedPubMedCentralCrossRef
18.
go back to reference Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q: Human Infection with a Novel Avian-Origin Influenza A (H7N9) Virus. N Engl J Med. 2013, 368 (20): 1888-1897. 10.1056/NEJMoa1304459.PubMedCrossRef Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q: Human Infection with a Novel Avian-Origin Influenza A (H7N9) Virus. N Engl J Med. 2013, 368 (20): 1888-1897. 10.1056/NEJMoa1304459.PubMedCrossRef
19.
20.
go back to reference Alexander PE, De P, Rave S: Is H9N2 avian influenza virus a pandemic potential?. Can J Infect Dis Med Microbiol. 2009, 20: e35-e36.PubMedPubMedCentral Alexander PE, De P, Rave S: Is H9N2 avian influenza virus a pandemic potential?. Can J Infect Dis Med Microbiol. 2009, 20: e35-e36.PubMedPubMedCentral
21.
go back to reference Zhang H, Xu B, Chen Q, Chen J, Chen Z: Characterization of an H10N8 influenza virus isolated from Dongting lake wetland. Virol J. 2011, 8: 42-10.1186/1743-422X-8-42.PubMedPubMedCentralCrossRef Zhang H, Xu B, Chen Q, Chen J, Chen Z: Characterization of an H10N8 influenza virus isolated from Dongting lake wetland. Virol J. 2011, 8: 42-10.1186/1743-422X-8-42.PubMedPubMedCentralCrossRef
22.
go back to reference Deng G, Tan D, Shi J, Cui P, Jiang Y, Liu L, Tian G, Kawaoka Y, Li C, Chen H: Complex reassortment of multiple subtypes of avian influenza viruses in domestic ducks at the dongting lake region of china. J Virol. 2013, 87: 9452-9462. 10.1128/JVI.00776-13.PubMedPubMedCentralCrossRef Deng G, Tan D, Shi J, Cui P, Jiang Y, Liu L, Tian G, Kawaoka Y, Li C, Chen H: Complex reassortment of multiple subtypes of avian influenza viruses in domestic ducks at the dongting lake region of china. J Virol. 2013, 87: 9452-9462. 10.1128/JVI.00776-13.PubMedPubMedCentralCrossRef
23.
go back to reference Zhang H, Chen Q, Chen Z: Characterization of an H4N2 avian influenza virus isolated from domestic duck in Dongting Lake wetland in 2009. Virus Genes. 2011, 44 (1): 24-31.PubMedCrossRef Zhang H, Chen Q, Chen Z: Characterization of an H4N2 avian influenza virus isolated from domestic duck in Dongting Lake wetland in 2009. Virus Genes. 2011, 44 (1): 24-31.PubMedCrossRef
24.
go back to reference Wang B, Chen Q, Chen Z: Complete genome sequence of an H9N2 avian influenza virus Isolated from Egret in Lake Dongting Wetland. J Virol. 2012, 86: 11939-10.1128/JVI.02042-12.PubMedPubMedCentralCrossRef Wang B, Chen Q, Chen Z: Complete genome sequence of an H9N2 avian influenza virus Isolated from Egret in Lake Dongting Wetland. J Virol. 2012, 86: 11939-10.1128/JVI.02042-12.PubMedPubMedCentralCrossRef
25.
go back to reference Huang Y, Hu B, Wen X, Cao S, Gavrilov BK, Du Q, Khan MI, Zhang X: Diversified reassortant H9N2 avian influenza viruses in chicken flocks in northern and eastern China. Virus Res. 2010, 151 (1): 26-32. 10.1016/j.virusres.2010.03.010.PubMedCrossRef Huang Y, Hu B, Wen X, Cao S, Gavrilov BK, Du Q, Khan MI, Zhang X: Diversified reassortant H9N2 avian influenza viruses in chicken flocks in northern and eastern China. Virus Res. 2010, 151 (1): 26-32. 10.1016/j.virusres.2010.03.010.PubMedCrossRef
26.
go back to reference Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM, Lim W, Webster RG, Yuen KY, Peiris JS, Guan Y: Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol. 2005, 43: 5760-5767. 10.1128/JCM.43.11.5760-5767.2005.PubMedPubMedCentralCrossRef Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM, Lim W, Webster RG, Yuen KY, Peiris JS, Guan Y: Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol. 2005, 43: 5760-5767. 10.1128/JCM.43.11.5760-5767.2005.PubMedPubMedCentralCrossRef
27.
go back to reference Hurt AC, Holien JK, Parker MW, Barr IG: Oseltamivir resistance and the H274Y neuraminidase mutation in seasonal, pandemic and highly pathogenic influenza viruses. Drugs. 2009, 69: 2523-2531. 10.2165/11531450-000000000-00000.PubMedCrossRef Hurt AC, Holien JK, Parker MW, Barr IG: Oseltamivir resistance and the H274Y neuraminidase mutation in seasonal, pandemic and highly pathogenic influenza viruses. Drugs. 2009, 69: 2523-2531. 10.2165/11531450-000000000-00000.PubMedCrossRef
28.
go back to reference Orozovic G, Orozovic K, Lennerstrand J, Olsen B: Detection of resistance mutations to antivirals oseltamivir and zanamivir in avian influenza a viruses isolated from wild birds. PLoS One. 2011, 6: e16028-10.1371/journal.pone.0016028.PubMedPubMedCentralCrossRef Orozovic G, Orozovic K, Lennerstrand J, Olsen B: Detection of resistance mutations to antivirals oseltamivir and zanamivir in avian influenza a viruses isolated from wild birds. PLoS One. 2011, 6: e16028-10.1371/journal.pone.0016028.PubMedPubMedCentralCrossRef
29.
go back to reference Massin P, van der Werf S, Naffakh N: Residue 627 of PB2 is a determinant of cold sensitivity in RNA replication of avian influenza viruses. J Virol. 2001, 75: 5398-5404. 10.1128/JVI.75.11.5398-5404.2001.PubMedPubMedCentralCrossRef Massin P, van der Werf S, Naffakh N: Residue 627 of PB2 is a determinant of cold sensitivity in RNA replication of avian influenza viruses. J Virol. 2001, 75: 5398-5404. 10.1128/JVI.75.11.5398-5404.2001.PubMedPubMedCentralCrossRef
30.
go back to reference Mehle A, Doudna JA: Adaptive strategies of the influenza virus polymerase for replication in humans. Proc Natl Acad Sci U S A. 2009, 106: 21312-21316. 10.1073/pnas.0911915106.PubMedPubMedCentralCrossRef Mehle A, Doudna JA: Adaptive strategies of the influenza virus polymerase for replication in humans. Proc Natl Acad Sci U S A. 2009, 106: 21312-21316. 10.1073/pnas.0911915106.PubMedPubMedCentralCrossRef
31.
go back to reference Ping J, Dankar SK, Forbes NE, Keleta L, Zhou Y, Tyler S, Brown EG: PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus. J Virol. 2010, 84: 10606-10618. 10.1128/JVI.01187-10.PubMedPubMedCentralCrossRef Ping J, Dankar SK, Forbes NE, Keleta L, Zhou Y, Tyler S, Brown EG: PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus. J Virol. 2010, 84: 10606-10618. 10.1128/JVI.01187-10.PubMedPubMedCentralCrossRef
32.
go back to reference Munster VJ, Baas C, Lexmond P, Waldenstrom J, Wallensten A, Fransson T, Rimmelzwaan GF, Beyer WE, Schutten M, Olsen B, Osterhaus AD, Fouchier RA: Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog. 2007, 3: e61-10.1371/journal.ppat.0030061.PubMedPubMedCentralCrossRef Munster VJ, Baas C, Lexmond P, Waldenstrom J, Wallensten A, Fransson T, Rimmelzwaan GF, Beyer WE, Schutten M, Olsen B, Osterhaus AD, Fouchier RA: Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog. 2007, 3: e61-10.1371/journal.ppat.0030061.PubMedPubMedCentralCrossRef
33.
go back to reference Stallknecht DE, Shane SM, Kearney MT, Zwank PJ: Persistence of avian influenza viruses in water. Avian Dis. 1990, 34: 406-411. 10.2307/1591428.PubMedCrossRef Stallknecht DE, Shane SM, Kearney MT, Zwank PJ: Persistence of avian influenza viruses in water. Avian Dis. 1990, 34: 406-411. 10.2307/1591428.PubMedCrossRef
34.
go back to reference Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG: Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology. 1978, 84: 268-278. 10.1016/0042-6822(78)90247-7.PubMedCrossRef Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG: Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology. 1978, 84: 268-278. 10.1016/0042-6822(78)90247-7.PubMedCrossRef
35.
go back to reference Duan L, Zhu H, Wang J, Huang K, Cheung CL, Peiris JS, Chen H, Guan Y: Influenza virus surveillance in migratory ducks and sentinel ducks at Poyang Lake, China. Influenza Other Respi Viruses. 2011, 5 (Suppl 1): 65-68. Duan L, Zhu H, Wang J, Huang K, Cheung CL, Peiris JS, Chen H, Guan Y: Influenza virus surveillance in migratory ducks and sentinel ducks at Poyang Lake, China. Influenza Other Respi Viruses. 2011, 5 (Suppl 1): 65-68.
36.
go back to reference Krauss S, Obert CA, Franks J, Walker D, Jones K, Seiler P, Niles L, Pryor SP, Obenauer JC, Naeve CW, Widjaja L, Webby RJ, Webster RG: Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog. 2007, 3: e167-10.1371/journal.ppat.0030167.PubMedPubMedCentralCrossRef Krauss S, Obert CA, Franks J, Walker D, Jones K, Seiler P, Niles L, Pryor SP, Obenauer JC, Naeve CW, Widjaja L, Webby RJ, Webster RG: Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog. 2007, 3: e167-10.1371/journal.ppat.0030167.PubMedPubMedCentralCrossRef
37.
go back to reference Wan H, Sorrell EM, Song H, Hossain MJ, Ramirez-Nieto G, Monne I, Stevens J, Cattoli G, Capua I, Chen LM, Donis RO, Busch J, Paulson JC, Brockwell C, Webby R, Blanco J, Al-Natour MQ, Perez DR: Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One. 2008, 3: e2923-10.1371/journal.pone.0002923.PubMedPubMedCentralCrossRef Wan H, Sorrell EM, Song H, Hossain MJ, Ramirez-Nieto G, Monne I, Stevens J, Cattoli G, Capua I, Chen LM, Donis RO, Busch J, Paulson JC, Brockwell C, Webby R, Blanco J, Al-Natour MQ, Perez DR: Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One. 2008, 3: e2923-10.1371/journal.pone.0002923.PubMedPubMedCentralCrossRef
38.
go back to reference Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, Ma C, Lycett SJ, Leung CY, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Farooqui A, Kelvin DJ, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y: The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature. 2013, 502 (7470): 241-244. 10.1038/nature12515.PubMedPubMedCentralCrossRef Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, Ma C, Lycett SJ, Leung CY, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Farooqui A, Kelvin DJ, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y: The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature. 2013, 502 (7470): 241-244. 10.1038/nature12515.PubMedPubMedCentralCrossRef
39.
go back to reference FAO: Wild Birds and Avian Influenza: an introduction to applied field research and disease sampling techniques. FAO Animal Production and Health Manual, No. 5. Edited by: Whitworth D, Newman SH, Mundkur T, Harris P. 2007, Rome, 73-84. Available at: http://www.fao.org/avianflu FAO: Wild Birds and Avian Influenza: an introduction to applied field research and disease sampling techniques. FAO Animal Production and Health Manual, No. 5. Edited by: Whitworth D, Newman SH, Mundkur T, Harris P. 2007, Rome, 73-84. Available at: http://​www.​fao.​org/​avianflu
Metadata
Title
Phylogenetic and antigenic characterization of reassortant H9N2 avian influenza viruses isolated from wild waterfowl in the East Dongting Lake wetland in 2011–2012
Authors
Yun Zhu
Shixiong Hu
Tian Bai
Lei Yang
Xiang Zhao
Wenfei Zhu
Yiwei Huang
Zhihong Deng
Hong Zhang
Zhiyong Bai
Mingdong Yu
Jianfei Huang
Yuelong Shu
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2014
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-11-77

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