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      Disease Dynamics and Bird Migration—Linking Mallards Anas platyrhynchos and Subtype Diversity of the Influenza A Virus in Time and Space

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          Abstract

          The mallard Anas platyrhynchos is a reservoir species for influenza A virus in the northern hemisphere, with particularly high prevalence rates prior to as well as during its prolonged autumn migration. It has been proposed that the virus is brought from the breeding grounds and transmitted to conspecifics during subsequent staging during migration, and so a better understanding of the natal origin of staging ducks is vital to deciphering the dynamics of viral movement pathways. Ottenby is an important stopover site in southeast Sweden almost halfway downstream in the major Northwest European flyway, and is used by millions of waterfowl each year. Here, mallards were captured and sampled for influenza A virus infection, and positive samples were subtyped in order to study possible links to the natal area, which were determined by a novel approach combining banding recovery data and isotopic measurements (δ 2H) of feathers grown on breeding grounds. Geographic assignments showed that the core natal areas of studied mallards were in Estonia, southern and central Finland, and northwestern Russia. This study demonstrates a clear temporal succession of latitudes of natal origin during the course of autumn migration. We also demonstrate a corresponding and concomitant shift in virus subtypes. Acknowledging that these two different patterns were based in part upon different data, a likely interpretation worth further testing is that the early arriving birds with more proximate origins have different influenza A subtypes than the more distantly originating late autumn birds. If true, this knowledge would allow novel insight into the origins and transmission of the influenza A virus among migratory hosts previously unavailable through conventional approaches.

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          Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls.

          In wild aquatic birds and poultry around the world, influenza A viruses carrying 15 antigenic subtypes of hemagglutinin (HA) and 9 antigenic subtypes of neuraminidase (NA) have been described. Here we describe a previously unidentified antigenic subtype of HA (H16), detected in viruses circulating in black-headed gulls in Sweden. In agreement with established criteria for the definition of antigenic subtypes, hemagglutination inhibition assays and immunodiffusion assays failed to detect specific reactivity between H16 and the previously described subtypes H1 to H15. Genetically, H16 HA was found to be distantly related to H13 HA, a subtype also detected exclusively in shorebirds, and the amino acid composition of the putative receptor-binding site of H13 and H16 HAs was found to be distinct from that in HA subtypes circulating in ducks and geese. The H16 viruses contained NA genes that were similar to those of other Eurasian shorebirds but genetically distinct from N3 genes detected in other birds and geographical locations. The European gull viruses were further distinguishable from other influenza A viruses based on their PB2, NP, and NS genes. Gaining information on the full spectrum of avian influenza A viruses and creating reagents for their detection and identification will remain an important task for influenza surveillance, outbreak control, and animal and public health. We propose that sequence analyses of HA and NA genes of influenza A viruses be used for the rapid identification of existing and novel HA and NA subtypes.
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            Statistical Analysis of Circular Data

            N. FISHER (1993)
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              Predicting the global spread of H5N1 avian influenza.

              The spread of highly pathogenic H5N1 avian influenza into Asia, Europe, and Africa has resulted in enormous impacts on the poultry industry and presents an important threat to human health. The pathways by which the virus has and will spread between countries have been debated extensively, but have yet to be analyzed comprehensively and quantitatively. We integrated data on phylogenetic relationships of virus isolates, migratory bird movements, and trade in poultry and wild birds to determine the pathway for 52 individual introduction events into countries and predict future spread. We show that 9 of 21 of H5N1 introductions to countries in Asia were most likely through poultry, and 3 of 21 were most likely through migrating birds. In contrast, spread to most (20/23) countries in Europe was most likely through migratory birds. Spread in Africa was likely partly by poultry (2/8 introductions) and partly by migrating birds (3/8). Our analyses predict that H5N1 is more likely to be introduced into the Western Hemisphere through infected poultry and into the mainland United States by subsequent movement of migrating birds from neighboring countries, rather than from eastern Siberia. These results highlight the potential synergism between trade and wild animal movement in the emergence and pandemic spread of pathogens and demonstrate the value of predictive models for disease control.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                20 April 2012
                : 7
                : 4
                : e35679
                Affiliations
                [1 ]Division of Natural Sciences, Kristianstad University, Kristianstad, Sweden
                [2 ]Section for Zoonotic Ecology and Epidemiology, School of Natural Sciences, Linnaeus University, Kalmar, Sweden
                [3 ]Wildlife and Landscape Science, Environment Canada, Saskatoon, Canada
                [4 ]Section of Infectious Diseases, Department of Medical Sciences, Uppsala University Hospital, Uppsala, Sweden
                [5 ]Department of Virology, Erasmus Medical Center, Rotterdam, The Netherlands
                Centers for Disease Control and Prevention, United States of America
                Author notes

                Conceived and designed the experiments: GG NLM KAH SLVW JE BO JW. Performed the experiments: GG NLM KAH SLVW. Analyzed the data: GG NLM KAH SLVW JW. Contributed reagents/materials/analysis tools: GG NLM KAH SLVW BO RAMF JW. Wrote the paper: GG NLM KAH SLVW JE RAMF JW.

                Article
                PONE-D-11-21829
                10.1371/journal.pone.0035679
                3335010
                22536424
                fbda2059-cced-4390-b206-da5173083d74
                Gunnarsson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 3 November 2011
                : 22 March 2012
                Page count
                Pages: 9
                Categories
                Research Article
                Biology
                Microbiology
                Vector Biology
                Viral Vectors
                Virology
                Viral Transmission and Infection
                Viral Vectors
                Emerging Viral Diseases
                Emerging Infectious Diseases
                Medicine
                Infectious Diseases
                Viral Diseases
                Influenza
                Zoonoses
                Avian influenza A viruses
                Veterinary Science
                Animal Types
                Wildlife
                Veterinary Diseases
                Veterinary Virology

                Uncategorized
                Uncategorized

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