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Aerosol Transmission of Gull-Origin Iceland Subtype H10N7 Influenza A Virus in Ferrets.

Identifieur interne : 000181 ( PubMed/Checkpoint ); précédent : 000180; suivant : 000182

Aerosol Transmission of Gull-Origin Iceland Subtype H10N7 Influenza A Virus in Ferrets.

Auteurs : Minhui Guan [États-Unis] ; Jeffrey S. Hall [États-Unis] ; Xiaojian Zhang [États-Unis] ; Robert J. Dusek [États-Unis] ; Alicia K. Olivier [États-Unis] ; Liyuan Liu [États-Unis] ; Lei Li [États-Unis] ; Scott Krauss [États-Unis] ; Angela Danner [États-Unis] ; Tao Li [États-Unis] ; Wiriya Rutvisuttinunt [États-Unis] ; Xiaoxu Lin [États-Unis] ; Gunnar T. Hallgrimsson [Islande] ; Sunna B. Ragnarsdottir [Islande] ; Solvi R. Vignisson [Islande] ; Josh Teslaa [États-Unis] ; Sean W. Nashold [États-Unis] ; Richard Jarman [États-Unis] ; Xiu-Feng Wan [États-Unis]

Source :

RBID : pubmed:30996092

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English descriptors

Abstract

Subtype H10 influenza A viruses (IAVs) have been recovered from domestic poultry and various aquatic bird species, and sporadic transmission of these IAVs from avian species to mammals (i.e., human, seal, and mink) are well documented. In 2015, we isolated four H10N7 viruses from gulls in Iceland. Genomic analyses showed four gene segments in the viruses were genetically associated with H10 IAVs that caused influenza outbreaks and deaths among European seals in 2014. Antigenic characterization suggested minimal antigenic variation among these H10N7 isolates and other archived H10 viruses recovered from human, seal, mink, and various avian species in Asia, Europe, and North America. Glycan binding preference analyses suggested that, similar to other avian-origin H10 IAVs, these gull-origin H10N7 IAVs bound to both avian-like alpha 2,3-linked sialic acids and human-like alpha 2,6-linked sialic acids. However, when the gull-origin viruses were compared with another Eurasian avian-origin H10N8 IAV, which caused human infections, the gull-origin virus showed significantly higher binding affinity to human-like glycan receptors. Results from a ferret experiment demonstrated that a gull-origin H10N7 IAV replicated well in turbinate, trachea, and lung, but replication was most efficient in turbinate and trachea. This gull-origin H10N7 virus can be transmitted between ferrets through the direct contact and aerosol routes, without prior adaptation. Gulls share their habitat with other birds and mammals and have frequent contact with humans; therefore, gull-origin H10N7 IAVs could pose a risk to public health. Surveillance and monitoring of these IAVs at the wild bird-human interface should be continued.IMPORTANCE Subtype H10 avian influenza A viruses (IAVs) have caused sporadic human infections and enzootic outbreaks among seals. In the fall of 2015, H10N7 viruses were recovered from gulls in Iceland, and genomic analyses showed that the viruses were genetically related with IAVs that caused outbreaks among seals in Europe a year earlier. These gull-origin viruses showed high binding affinity to human-like glycan receptors. Transmission studies in ferrets demonstrated that the gull-origin IAV could infect ferrets, and that the virus could be transmitted between ferrets through direct contact and aerosol droplets. This study demonstrated that avian H10 IAV can infect mammals and be transmitted among them without adaptation. Thus, avian H10 IAV is a candidate for influenza pandemic preparedness and should be monitored in wildlife and at the animal-human interface.

DOI: 10.1128/JVI.00282-19
PubMed: 30996092


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pubmed:30996092

Le document en format XML

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<name sortKey="Guan, Minhui" sort="Guan, Minhui" uniqKey="Guan M" first="Minhui" last="Guan">Minhui Guan</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Basic Science, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA.</nlm:affiliation>
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<region type="state">État du Mississippi</region>
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<name sortKey="Hall, Jeffrey S" sort="Hall, Jeffrey S" uniqKey="Hall J" first="Jeffrey S" last="Hall">Jeffrey S. Hall</name>
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<nlm:affiliation>United States Geological Survey National Wildlife Health Center, Madison, Wisconsin, USA.</nlm:affiliation>
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<placeName>
<region type="state">Wisconsin</region>
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<name sortKey="Zhang, Xiaojian" sort="Zhang, Xiaojian" uniqKey="Zhang X" first="Xiaojian" last="Zhang">Xiaojian Zhang</name>
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<nlm:affiliation>Department of Basic Science, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Basic Science, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi</wicri:regionArea>
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<region type="state">État du Mississippi</region>
</placeName>
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<name sortKey="Dusek, Robert J" sort="Dusek, Robert J" uniqKey="Dusek R" first="Robert J" last="Dusek">Robert J. Dusek</name>
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<nlm:affiliation>United States Geological Survey National Wildlife Health Center, Madison, Wisconsin, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>United States Geological Survey National Wildlife Health Center, Madison, Wisconsin</wicri:regionArea>
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<region type="state">Wisconsin</region>
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<name sortKey="Olivier, Alicia K" sort="Olivier, Alicia K" uniqKey="Olivier A" first="Alicia K" last="Olivier">Alicia K. Olivier</name>
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<nlm:affiliation>Department of Population and Pathobiology Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA.</nlm:affiliation>
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<name sortKey="Liu, Liyuan" sort="Liu, Liyuan" uniqKey="Liu L" first="Liyuan" last="Liu">Liyuan Liu</name>
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<nlm:affiliation>Department of Basic Science, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA.</nlm:affiliation>
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<name sortKey="Li, Lei" sort="Li, Lei" uniqKey="Li L" first="Lei" last="Li">Lei Li</name>
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<name sortKey="Krauss, Scott" sort="Krauss, Scott" uniqKey="Krauss S" first="Scott" last="Krauss">Scott Krauss</name>
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<nlm:affiliation>Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, USA.</nlm:affiliation>
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<wicri:regionArea>Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee</wicri:regionArea>
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<region type="state">Tennessee</region>
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<name sortKey="Danner, Angela" sort="Danner, Angela" uniqKey="Danner A" first="Angela" last="Danner">Angela Danner</name>
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<nlm:affiliation>Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, USA.</nlm:affiliation>
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<region type="state">Tennessee</region>
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<name sortKey="Li, Tao" sort="Li, Tao" uniqKey="Li T" first="Tao" last="Li">Tao Li</name>
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<nlm:affiliation>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA.</nlm:affiliation>
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<name sortKey="Rutvisuttinunt, Wiriya" sort="Rutvisuttinunt, Wiriya" uniqKey="Rutvisuttinunt W" first="Wiriya" last="Rutvisuttinunt">Wiriya Rutvisuttinunt</name>
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<name sortKey="Lin, Xiaoxu" sort="Lin, Xiaoxu" uniqKey="Lin X" first="Xiaoxu" last="Lin">Xiaoxu Lin</name>
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<nlm:affiliation>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA.</nlm:affiliation>
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<region type="state">Maryland</region>
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<name sortKey="Hallgrimsson, Gunnar T" sort="Hallgrimsson, Gunnar T" uniqKey="Hallgrimsson G" first="Gunnar T" last="Hallgrimsson">Gunnar T. Hallgrimsson</name>
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<nlm:affiliation>University of Iceland, Reykjavik, Iceland.</nlm:affiliation>
<country xml:lang="fr">Islande</country>
<wicri:regionArea>University of Iceland, Reykjavik</wicri:regionArea>
<wicri:noRegion>Reykjavik</wicri:noRegion>
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<name sortKey="Ragnarsdottir, Sunna B" sort="Ragnarsdottir, Sunna B" uniqKey="Ragnarsdottir S" first="Sunna B" last="Ragnarsdottir">Sunna B. Ragnarsdottir</name>
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<nlm:affiliation>Southwest Iceland Nature Research Centre, Sandgerdi, Iceland.</nlm:affiliation>
<country xml:lang="fr">Islande</country>
<wicri:regionArea>Southwest Iceland Nature Research Centre, Sandgerdi</wicri:regionArea>
<wicri:noRegion>Sandgerdi</wicri:noRegion>
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<author>
<name sortKey="Vignisson, Solvi R" sort="Vignisson, Solvi R" uniqKey="Vignisson S" first="Solvi R" last="Vignisson">Solvi R. Vignisson</name>
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<nlm:affiliation>Sudurnes Science and Learning Center, Sandgerdi, Iceland.</nlm:affiliation>
<country xml:lang="fr">Islande</country>
<wicri:regionArea>Sudurnes Science and Learning Center, Sandgerdi</wicri:regionArea>
<wicri:noRegion>Sandgerdi</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Teslaa, Josh" sort="Teslaa, Josh" uniqKey="Teslaa J" first="Josh" last="Teslaa">Josh Teslaa</name>
<affiliation wicri:level="2">
<nlm:affiliation>United States Geological Survey National Wildlife Health Center, Madison, Wisconsin, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>United States Geological Survey National Wildlife Health Center, Madison, Wisconsin</wicri:regionArea>
<placeName>
<region type="state">Wisconsin</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Nashold, Sean W" sort="Nashold, Sean W" uniqKey="Nashold S" first="Sean W" last="Nashold">Sean W. Nashold</name>
<affiliation wicri:level="2">
<nlm:affiliation>United States Geological Survey National Wildlife Health Center, Madison, Wisconsin, USA.</nlm:affiliation>
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<term>Respiratory System (virology)</term>
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<div type="abstract" xml:lang="en">Subtype H10 influenza A viruses (IAVs) have been recovered from domestic poultry and various aquatic bird species, and sporadic transmission of these IAVs from avian species to mammals (i.e., human, seal, and mink) are well documented. In 2015, we isolated four H10N7 viruses from gulls in Iceland. Genomic analyses showed four gene segments in the viruses were genetically associated with H10 IAVs that caused influenza outbreaks and deaths among European seals in 2014. Antigenic characterization suggested minimal antigenic variation among these H10N7 isolates and other archived H10 viruses recovered from human, seal, mink, and various avian species in Asia, Europe, and North America. Glycan binding preference analyses suggested that, similar to other avian-origin H10 IAVs, these gull-origin H10N7 IAVs bound to both avian-like alpha 2,3-linked sialic acids and human-like alpha 2,6-linked sialic acids. However, when the gull-origin viruses were compared with another Eurasian avian-origin H10N8 IAV, which caused human infections, the gull-origin virus showed significantly higher binding affinity to human-like glycan receptors. Results from a ferret experiment demonstrated that a gull-origin H10N7 IAV replicated well in turbinate, trachea, and lung, but replication was most efficient in turbinate and trachea. This gull-origin H10N7 virus can be transmitted between ferrets through the direct contact and aerosol routes, without prior adaptation. Gulls share their habitat with other birds and mammals and have frequent contact with humans; therefore, gull-origin H10N7 IAVs could pose a risk to public health. Surveillance and monitoring of these IAVs at the wild bird-human interface should be continued.
<b>IMPORTANCE</b>
Subtype H10 avian influenza A viruses (IAVs) have caused sporadic human infections and enzootic outbreaks among seals. In the fall of 2015, H10N7 viruses were recovered from gulls in Iceland, and genomic analyses showed that the viruses were genetically related with IAVs that caused outbreaks among seals in Europe a year earlier. These gull-origin viruses showed high binding affinity to human-like glycan receptors. Transmission studies in ferrets demonstrated that the gull-origin IAV could infect ferrets, and that the virus could be transmitted between ferrets through direct contact and aerosol droplets. This study demonstrated that avian H10 IAV can infect mammals and be transmitted among them without adaptation. Thus, avian H10 IAV is a candidate for influenza pandemic preparedness and should be monitored in wildlife and at the animal-human interface.</div>
</front>
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<DateCompleted>
<Year>2020</Year>
<Month>05</Month>
<Day>28</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>05</Month>
<Day>28</Day>
</DateRevised>
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<ISSN IssnType="Electronic">1098-5514</ISSN>
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<Volume>93</Volume>
<Issue>13</Issue>
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<Year>2019</Year>
<Month>07</Month>
<Day>01</Day>
</PubDate>
</JournalIssue>
<Title>Journal of virology</Title>
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<ArticleTitle>Aerosol Transmission of Gull-Origin Iceland Subtype H10N7 Influenza A Virus in Ferrets.</ArticleTitle>
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<AbstractText>Subtype H10 influenza A viruses (IAVs) have been recovered from domestic poultry and various aquatic bird species, and sporadic transmission of these IAVs from avian species to mammals (i.e., human, seal, and mink) are well documented. In 2015, we isolated four H10N7 viruses from gulls in Iceland. Genomic analyses showed four gene segments in the viruses were genetically associated with H10 IAVs that caused influenza outbreaks and deaths among European seals in 2014. Antigenic characterization suggested minimal antigenic variation among these H10N7 isolates and other archived H10 viruses recovered from human, seal, mink, and various avian species in Asia, Europe, and North America. Glycan binding preference analyses suggested that, similar to other avian-origin H10 IAVs, these gull-origin H10N7 IAVs bound to both avian-like alpha 2,3-linked sialic acids and human-like alpha 2,6-linked sialic acids. However, when the gull-origin viruses were compared with another Eurasian avian-origin H10N8 IAV, which caused human infections, the gull-origin virus showed significantly higher binding affinity to human-like glycan receptors. Results from a ferret experiment demonstrated that a gull-origin H10N7 IAV replicated well in turbinate, trachea, and lung, but replication was most efficient in turbinate and trachea. This gull-origin H10N7 virus can be transmitted between ferrets through the direct contact and aerosol routes, without prior adaptation. Gulls share their habitat with other birds and mammals and have frequent contact with humans; therefore, gull-origin H10N7 IAVs could pose a risk to public health. Surveillance and monitoring of these IAVs at the wild bird-human interface should be continued.
<b>IMPORTANCE</b>
Subtype H10 avian influenza A viruses (IAVs) have caused sporadic human infections and enzootic outbreaks among seals. In the fall of 2015, H10N7 viruses were recovered from gulls in Iceland, and genomic analyses showed that the viruses were genetically related with IAVs that caused outbreaks among seals in Europe a year earlier. These gull-origin viruses showed high binding affinity to human-like glycan receptors. Transmission studies in ferrets demonstrated that the gull-origin IAV could infect ferrets, and that the virus could be transmitted between ferrets through direct contact and aerosol droplets. This study demonstrated that avian H10 IAV can infect mammals and be transmitted among them without adaptation. Thus, avian H10 IAV is a candidate for influenza pandemic preparedness and should be monitored in wildlife and at the animal-human interface.</AbstractText>
<CopyrightInformation>Copyright © 2019 American Society for Microbiology.</CopyrightInformation>
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<LastName>Guan</LastName>
<ForeName>Minhui</ForeName>
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