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Risks of Avian Influenza Transmission in Areas of Intensive Free-Ranging Duck Production with Wild Waterfowl

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Abstract

For decades, southern China has been considered to be an important source for emerging influenza viruses since key hosts live together in high densities in areas with intensive agriculture. However, the underlying conditions of emergence and spread of avian influenza viruses (AIV) have not been studied in detail, particularly the complex spatiotemporal interplay of viral transmission between wild and domestic ducks, two major actors of AIV epidemiology. In this synthesis, we examine the risks of avian influenza spread in Poyang Lake, an area of intensive free-ranging duck production and large numbers of wild waterfowl. Our synthesis shows that farming of free-grazing domestic ducks is intensive in this area and synchronized with wild duck migration. The presence of juvenile domestic ducks in harvested paddy fields prior to the arrival and departure of migrant ducks in the same fields may amplify the risk of AIV circulation and facilitate the transmission between wild and domestic populations. We provide evidence associating wild ducks migration with the spread of H5N1 in the spring of 2008 from southern China to South Korea, Russia, and Japan, supported by documented wild duck movements and phylogenetic analyses of highly pathogenic avian influenza H5N1 sequences. We suggest that prevention measures based on a modification of agricultural practices may be implemented in these areas to reduce the intensity of AIV transmission between wild and domestic ducks. This would require involving all local stakeholders to discuss feasible and acceptable solutions.

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References

  • Alexander DJ (2007). An overview of the epidemiology of avian influenza. Vaccine 25:5637-5644.

    Article  CAS  PubMed  Google Scholar 

  • Brown JD, Stallknecht DE, and Swaynet DE (2008). Experimental infection of swans and geese with highly pathogenic avian influenza virus (H5N1) of Asian lineage. Emerging Infectious Diseases 14:136-142.

    Article  PubMed Central  PubMed  Google Scholar 

  • Chen H, Deng G, Li Z, Tian G, Li Y, Jiao P, et al. (2004). The evolution of H5N1 influenza viruses in ducks in southern China. Proceedings of the National Academy of Sciences of the United States of America 101:10452-10457.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen H, Smith GJD, Li KS, Wang J, Fan XH, Rayner JM, et al. (2006). Establishment of multiple sublineages of H5N1 influenza virus in Asia: Implications for pandemic control. Proceedings of the National Academy of Sciences of the United States of America 103:2845-2850.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Desvaux S, Grobois V, Pham Thi Thanh H, Dao DT, Nguyen TD, Fenwick S, et al. (2013). Evaluation of the vaccination efficacy against H5N1 in domestic poultry in the Red River Delta in Vietnam. Epidemiology and Infection 141:776-788.

    Article  CAS  PubMed  Google Scholar 

  • Domanska-Blicharz K, Minta Z, Smietanka K, Marche S, and van den Berg T (2010). H5N1 high pathogenicity avian influenza virus survival in different types of water. Avian Diseases 54:734-737.

    Article  PubMed  Google Scholar 

  • Duan L, Zhu H, Wang J, Huang K, Cheung C-L, Peiris JSM, et al. (2011). Influenza virus surveillance in migratory ducks and sentinel ducks at Poyang Lake, China. Influenza and Other Respiratory Viruses 5:65-68.

    PubMed  Google Scholar 

  • Gaidet N, Cappelle J, Takekawa JY, Prosser DJ, Iverson SA, Douglas DC, et al. (2010). Potential spread of highly pathogenic avian influenza H5N1 by wildfowl: dispersal ranges and rates determined from large-scale satellite telemetry. Journal of Applied Ecology 47:1147-1157.

    Article  Google Scholar 

  • Gilbert M, Chaitaweesub P, Parakarnawongsa T, Premashthira S, Tiensin T, Kalpravidh W, et al. (2006). Free-grazing ducks and highly pathogenic avian influenza, Thailand. Emerging Infectious Diseases 12:227-234.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gilbert M, Xiao XM, Pfeiffer DU, Epprecht M, Boles S, Czarnecki C, et al. (2008). Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia. Proceedings of the National Academy of Sciences of the United States of America 105:4769-4774.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guan Y, Peiris JSM, Lipatov AS, Ellis TM, Dyrting KC, Krauss S, et al. (2002). Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proceedings of the National Academy of Sciences of the United States of America 99:8950-8955.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hill NJ, Takekawa JY, Ackerman JT, Hobson KA, Herring G, Cardona CJ, et al. (2012). Migration strategy affects avian influenza dynamics in mallards (Anas platyrhynchos). Molecular Ecology 21:5986-5999.

    Article  PubMed  Google Scholar 

  • Hulse-Post DJ, Sturm-Ramirez KM, Humberd J, Seiler P, Govorkova EA, Krauss S, et al. (2005). Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proceedings of the National Academy of Sciences of the United States of America 102:10682-10687.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. (2008). Global trends in emerging infectious diseases. Nature 451:990-U994.

    Article  Google Scholar 

  • Kang H-M, Batchuluun D, Kim M-C, Choi J-G, Erdene-Ochir T-O, Paek M-R, et al. (2011). Genetic analyses of H5N1 avian influenza virus in Mongolia, 2009 and its relationship with those of eastern Asia. Veterinary Microbiology 147:170-175.

    Article  CAS  PubMed  Google Scholar 

  • Keawcharoen J, van Riel D, van Amerongen G, Bestebroer T, Beyer WE, van Lavieren R, et al. (2008). Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5NI). Emerging Infectious Diseases 14:600-607.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kilpatrick AM, Chmura AA, Gibbons DW, Fleischer RC, Marra PP, and Daszak P (2006). Predicting the global spread of H5N1 avian influenza. Proceedings of the National Academy of Sciences of the United States of America 103:19368-19373.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim H-R, Lee Y-J, Park C-K, Oem J-K, Lee OS, Kang H-M, et al. (2012). Highly Pathogenic Avian Influenza (H5N1) Outbreaks in Wild Birds and Poultry, South Korea. Emerging Infectious Diseases 18:480-483.

    Article  PubMed Central  PubMed  Google Scholar 

  • Kim JK, Seiler P, Forrest HL, Khalenkov AM, Franks J, Kumar M, et al. (2008). Pathogenicity and Vaccine Efficacy of Different Clades of Asian H5N1 Avian Influenza A Viruses in Domestic Ducks. Journal of Virology 82:11374-11382.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, et al (2013) The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502(7470):241-4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li P, Feng Z, Jiang L, Liu Y, and Xiao X (2012). Changes in rice cropping systems in the Poyang Lake Region, China during 2004–2010. Journal of Geographical Sciences 22:653-668.

    Article  Google Scholar 

  • Li Y, Liu L, Zhang Y, Duan Z, Tian G, Zeng X, et al. (2011). New Avian Influenza Virus (H5N1) in Wild Birds, Qinghai, China. Emerging Infectious Diseases 17:265-267.

    Article  PubMed Central  PubMed  Google Scholar 

  • Manin TB, Chvala IA, Kolosov SN, Pchelkina IP, Irza VN, and Drygin VV (2010). H5N1 Avian Influenza Outbreak in the Far East of Russia in 2008: New Introduction. Avian Diseases 54:509-512.

    Article  PubMed  Google Scholar 

  • Martin V, Pfeiffer DU, Zhou X, Xiao X, Prosser DJ, Guo F, et al. (2011). Spatial Distribution and Risk Factors of Highly Pathogenic Avian Influenza (HPAI) H5N1 in China. PLoS Pathogens 7:e1001308.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Munster VJ, Baas C, Lexmond P, Waldenström J, Wallensten A, Fransson T, et al. (2007). Spatial, Temporal, and Species Variation in Prevalence of Influenza A Viruses in Wild Migratory Birds. PLoS Pathogens 3:e61.

    Article  PubMed Central  PubMed  Google Scholar 

  • Munster VJ, Wallensten A, Baas C, Rimmelzwaan GF, Schutten M, Olsen B, et al. (2005). Mallards and highly pathogenic avian influenza ancestral viruses, northern Europe. Emerging Infectious Diseases 11:1545-1551.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nemeth NM, Brown JD, Stallknecht DE, Howerth EW, Newman SH, and Swayne DE (2013) Experimental infection of Bar-Headed Geese (Anser indicus) and Ruddy Shelducks (Tadorna ferruginea) with a clade 2.3.2 H5N1 highly pathogenic avian influenza virus. Veterinary Pathology 50(6):961-70.

    Article  CAS  PubMed  Google Scholar 

  • Newman SH, Hill NJ, Spragens KA, Janies D, Voronkin IO, Prosser DJ, et al. (2012). Eco-virological approach for assessing the role of wild birds in the spread of avian Influenza H5N1 along the Central Asian Flyway. PLoS One 7(2):e30636.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus A, and Fouchier RAM (2006). Global patterns of influenza A virus in wild birds. Science 312:384-388.

    Article  CAS  PubMed  Google Scholar 

  • Posada D, and Crandall KA (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.

    Article  CAS  PubMed  Google Scholar 

  • Prosser D, Hungerford L, Erwin RM, Ottinger MA, Takekawa JY, and Ellis E (2013) Mapping avian influenza transmission risk at the interface of domestic poultry and wild birds. Frontiers in Public Health 1:28.

    Article  PubMed Central  PubMed  Google Scholar 

  • Reid SM, Shell WM, Barboi G, Onita I, Turcitu M, Cioranu R, et al. (2011). First Reported Incursion of Highly Pathogenic Notifiable Avian Influenza A H5N1 Viruses from Clade 2.3.2 into European Poultry. Transboundary and Emerging Diseases 58:76-78.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shortridge KF (1982). Avian influenza A viruses of southern China and Hong Kong: ecological aspects and implications for man. Bulletin of the World Health Organization 60:129- 135.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smith GJD, Vijaykrishna D, Ellis TM, Dyrting KC, Leung YHC, Bahl J, et al. (2009). Characterization of Avian Influenza Viruses A (H5N1) from Wild Birds, Hong Kong, 2004-2008. Emerging Infectious Diseases 15:402-407.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Songserm T, Jam-on R, Sae-Heng N, Meemak N, Hulse-Post DJ, Sturm-Ramirez KM, et al. (2006). Domestic ducks and H5N1 influenza epidemic, Thailand. Emerging Infectious Diseases 12:575-581.

    Article  PubMed Central  PubMed  Google Scholar 

  • Sturm-Ramirez KM, Hulse-Post DJ, Govorkova EA, Humberd J, Seiler P, Puthavathana P, et al. (2005). Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? Journal of Virology 79:11269-11279.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Swofford DL (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods) version 4.0 (Computer program). Sunderland, Massachusetts: Sinauer Associates.

  • Takekawa JY, Newman SH, Xiao X, Prosser DJ, Spragens KA, Palm EC, et al. (2010). Migration of Waterfowl in the East Asian Flyway and Spatial Relationship to HPAI H5N1 Outbreaks. Avian Diseases 54:466-476.

    Article  PubMed  Google Scholar 

  • Torbick N, Salas W, Xiao X, Ingraham P, Fearon MG, Biradar C, et al. (2011). Integrating SAR and optical imagery for regional mapping of paddy rice attributes in the Poyang Lake watershed, China. Canadian Journal of Remote Sensing 37:17-26.

    Article  Google Scholar 

  • Usui T, Yamaguchi T, Ito H, Ozaki H, Murase T, and Ito T (2009). Evolutionary genetics of highly pathogenic H5N1 avian influenza viruses isolated from whooper swans in northern Japan in 2008. Virus Genes 39:319-323.

    Article  CAS  PubMed  Google Scholar 

  • van Dijk JGB, Hoye BJ, Verhagen JH, Nolet BA, Fouchier RAM, and Klaassen M (2013). Juveniles and migrants as drivers for seasonal epizootics of avian influenza virus. Journal of Animal Ecology, 83(1):266-75.

    Article  PubMed  Google Scholar 

  • Webster RG, Bean WJ, Gorman OT, Chambers TM, and Kawaoka Y (1992). Evolution and Ecology of Influenza-A Viruses. Microbiological Reviews 56:152-179.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Webster RG, Peiris M, Chen HL, and Guan Y (2006). H5N1 outbreaks and enzootic influenza. Emerging Infectious Diseases 12:3-8.

    Article  PubMed Central  PubMed  Google Scholar 

  • Yamamoto Y, Nakamura K, Yamada M, and Mase M (2010). Persistence of Avian Influenza Virus (H5N1) in Feathers Detached from Bodies of Infected Domestic Ducks. Applied and Environmental Microbiology 76:5496-5499.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao G, Zhong L, Lu X, Hu J, Gu X, Kai Y, et al. (2012). Characterisation of a highly pathogenic H5N1 clade 2.3.2 influenza virus isolated from swans in Shanghai, China. Virus Genes 44:55-62.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by a grant from the National Institutes of Health (NIH 1R01AI101028-01A1), a grant from the NIH Fogarty International Center (R01-TW007869) through the NSF/NIH Ecology of Infectious Diseases program, the Food and Agriculture Organization of the United Nations, the U.S. Geological Survey, and a grant from National Aeronautics and Space Administration (NASA) Public Health Program (NNX11AF66G). Julien Cappelle was supported by the Gripavi project funded by the French Ministry of Foreign Affairs. We thank Martine Duportal for her help in designing the figures and Isa Woo with editorial assistance. The use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Correspondence to Julien Cappelle.

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Cappelle, J., Zhao, D., Gilbert, M. et al. Risks of Avian Influenza Transmission in Areas of Intensive Free-Ranging Duck Production with Wild Waterfowl. EcoHealth 11, 109–119 (2014). https://doi.org/10.1007/s10393-014-0914-2

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