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      Molecular Characterization of Subtype H11N9 Avian Influenza Virus Isolated from Shorebirds in Brazil

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          Abstract

          Migratory aquatic birds play an important role in the maintenance and spread of avian influenza viruses (AIV). Many species of aquatic migratory birds tend to use similar migration routes, also known as flyways, which serve as important circuits for the dissemination of AIV. In recent years there has been extensive surveillance of the virus in aquatic birds in the Northern Hemisphere; however in contrast only a few studies have been attempted to detect AIV in wild birds in South America. There are major flyways connecting South America to Central and North America, whereas avian migration routes between South America and the remaining continents are uncommon. As a result, it has been hypothesized that South American AIV strains would be most closely related to the strains from North America than to those from other regions in the world. We characterized the full genome of three AIV subtype H11N9 isolates obtained from ruddy turnstones ( Arenaria interpres) on the Amazon coast of Brazil. For all gene segments, all three strains consistently clustered together within evolutionary lineages of AIV that had been previously described from aquatic birds in North America. In particular, the H11N9 isolates were remarkably closely related to AIV strains from shorebirds sampled at the Delaware Bay region, on the Northeastern coast of the USA, more than 5000 km away from where the isolates were retrieved. Additionally, there was also evidence of genetic similarity to AIV strains from ducks and teals from interior USA and Canada. These findings corroborate that migratory flyways of aquatic birds play an important role in determining the genetic structure of AIV in the Western hemisphere, with a strong epidemiological connectivity between North and South America.

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          Most cited references22

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          Bat-derived influenza-like viruses H17N10 and H18N11

          Highlights • Bat-derived influenza-like virus hemagglutinin and neuraminidase lack canonical functions and structures. • Putative functional modules/domains in other bat-derived influenza-like proteins are conserved. • Potential genomic reassortments with canonical influenza virus cannot be ruled out and should be assessed.
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            Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002.

            Outbreaks of highly pathogenic H5N1 avian influenza have occurred in Hong Kong in chickens and other gallinaceous poultry in 1997, 2001, twice in 2002 and 2003. High mortality rates were seen in gallinaceous birds but not in domestic or wild waterfowl or other wild birds until late 2002 when highly pathogenic H5N1 avian influenza occurred in waterfowl (geese, ducks and swans), captive Greater Flamingo (Phoenicopterus ruber) and other wild birds (Little Egret Egretta garzetta) at two waterfowl parks and from two dead wild Grey Heron (Ardea cinerea) and a Black-headed Gull (Larus ridibundus) in Hong Kong. H5N1 avian influenza virus was also isolated from a dead feral pigeon (Columba livia) and a dead tree sparrow (Passer montanus) during the second outbreak. The first waterfowl outbreak was controlled by immediate strict quarantine and depopulation 1 week before the second outbreak commenced. Control measures implemented for the second outbreak included strict isolation, culling, increased sanitation and vaccination. Outbreaks in gallinaceous birds occurred in some live poultry markets concurrently with the second waterfowl outbreak, and infection on a chicken farm was detected 1 week after the second waterfowl park outbreak was detected, on the same day the second grey heron case was detected. Subsequent virus surveillance showed the outbreaks had been contained.
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              Influenza A viruses of migrating wild aquatic birds in North America.

              Surveillance of North America's wild ducks and shorebirds for 26 and 16 years, respectively, revealed differences in the prevalence of orthomyxoviruses between these hosts. Shorebirds had a high frequency of influenza A virus isolation during their northern migration, while wild ducks had high virus isolation frequencies during their southern migration. Some subtypes of influenza occurred regularly in both hosts with a 2-year periodicity, whereas others rarely occurred. Hemagglutinin subtypes H1 through H12 occurred in both hosts; H13 occurred only in shorebirds; and H14, H15, and influenza B and C never were detected. Shorebirds manifested a broader range of subtypes suggesting that shorebirds are the leading source of some viruses (such as H5) which are isolated less frequently from wild ducks. The viruses reported in this study are available for genomic study to determine whether prediction of host range or pandemic potential is possible.
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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, CA USA )
                1932-6203
                21 December 2015
                2015
                : 10
                : 12
                : e0145627
                Affiliations
                [1 ]Department of Preventive Veterinary Medicine and Animal Health, School of Veterinary Medicine, University of São Paulo, São Paulo, Brazil
                [2 ]Division of Virology, Department of Infectious Diseases, St. Jude Children’s Research Hospital, Memphis, Tennessee, United States of America
                [3 ]Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine, University of São Paulo, São Paulo, Brazil
                [4 ]Laboratory Biosafety Level 3+, Department of Microbiology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil
                Linneaus University, SWEDEN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: RH TF RETV SK RW RGW ELD. Performed the experiments: RH TF RETV. Analyzed the data: RH TF RETV SK. Contributed reagents/materials/analysis tools: RH TF SK RW RGW ELD. Wrote the paper: RH TF RETV SK RW RGW.

                Article
                PONE-D-15-46137
                10.1371/journal.pone.0145627
                4687026
                26689791
                9a4a56c2-c623-4139-9697-3a15bb4529ac
                © 2015 Hurtado 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
                : 20 October 2015
                : 7 December 2015
                Page count
                Figures: 3, Tables: 1, Pages: 11
                Funding
                This research was funded by São Paulo Research Foundation, National Counsel of Technological and Scientific Development, and Coordination for the Improvement of Higher Education Personnel. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                The gene sequences produced in this study are available on Genbank (accession number(s) KF824501-KF824506, KT932362-KT932379).

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                Uncategorized

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