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

Virology Journal

Yuelong Shu⁴  Jianfei Huang⁵  Mingdong Yu¹  Zhiyong Bai¹  Hong Zhang²  Zhihong Deng³  Yiwei Huang³  Wenfei Zhu⁴  Xiang Zhao⁴  Lei Yang⁴  Tian Bai⁴  Shixiong Hu³  Yun Zhu⁴ 

[1] Yueyang Center for Disease Control and Prevention, Yueyang, China;Hunan East Dongting Lake National Nature Reserve, Yueyang, China;Hunan Provincial Center for Disease Control and Prevention, Changsha, China;Key Laboratory for Medical Virology, National Health and Family Planning Commission, National Institute for Viral Disease Control and Prevention, China CDC, Beijing 102206, China;Yueyang County Center for Disease Control and Prevention, Yueyang, China

关键词: Reassortant;    Dongting Lake;    H9N2 subtype;    Wild waterfowl;    Avian influenza virus;   

Others  :  805995
DOI  :  10.1186/1743-422X-11-77

 received in 2014-01-07, accepted in 2014-04-16,  发布年份 2014

【 摘 要 】

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.

【 授权许可】

   
2014 Zhu et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev 1992, 56:152-179.
• [2]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.
• [3]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.
• [4]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.
• [5]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.
• [6]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.
• [7]Alexander DJ: An overview of the epidemiology of avian influenza. Vaccine 2007, 25:5637-5644.
• [8]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.
• [9]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]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.
• [11]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.
• [12]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.
• [13]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.
• [14]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.
• [15]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.
• [16]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.
• [17]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.
• [18]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.
• [19]Horimoto T, Kawaoka Y: Pandemic threat posed by avian influenza A viruses. Clin Microbiol Rev 2001, 14:129-149.
• [20]Alexander PE, De P, Rave S: Is H9N2 avian influenza virus a pandemic potential? Can J Infect Dis Med Microbiol 2009, 20:e35-e36.
• [21]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. BioMed Central Full Text
• [22]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.
• [23]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.
• [24]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.
• [25]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.
• [26]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.
• [27]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.
• [28]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.
• [29]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.
• [30]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.
• [31]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.
• [32]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.
• [33]Stallknecht DE, Shane SM, Kearney MT, Zwank PJ: Persistence of avian influenza viruses in water. Avian Dis 1990, 34:406-411.
• [34]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.
• [35]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]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.
• [37]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.
• [38]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.
• [39]FAO: Wild Birds and Avian Influenza: an introduction to applied field research and disease sampling techniques. In FAO Animal Production and Health Manual, No. 5. Edited by Whitworth D, Newman SH, Mundkur T, Harris P. Rome; 2007:73-84. Available at: http://www.fao.org/avianflu webcite