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Pathogenesis and Immunity

Domestic Pigs Are Susceptible to Infection with Influenza B Viruses

Zhiguang Ran, Huigang Shen, Yuekun Lang, Elizabeth A. Kolb, Nuri Turan, Laihua Zhu, Jingjiao Ma, Bhupinder Bawa, Qinfang Liu, Haixia Liu, Megan Quast, Gabriel Sexton, Florian Krammer, Ben M. Hause, Jane Christopher-Hennings, Eric A. Nelson, Juergen Richt, Feng Li, Wenjun Ma
R. M. Sandri-Goldin, Editor
Zhiguang Ran
aDepartment of Biology and Microbiology, South Dakota State University, Brookings, South Dakota, USA
cDepartment of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, South Dakota, USA
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Huigang Shen
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Yuekun Lang
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Elizabeth A. Kolb
aDepartment of Biology and Microbiology, South Dakota State University, Brookings, South Dakota, USA
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Nuri Turan
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Laihua Zhu
aDepartment of Biology and Microbiology, South Dakota State University, Brookings, South Dakota, USA
cDepartment of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, South Dakota, USA
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Jingjiao Ma
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Bhupinder Bawa
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Qinfang Liu
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Haixia Liu
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Megan Quast
aDepartment of Biology and Microbiology, South Dakota State University, Brookings, South Dakota, USA
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Gabriel Sexton
aDepartment of Biology and Microbiology, South Dakota State University, Brookings, South Dakota, USA
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Florian Krammer
dDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, USA
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Ben M. Hause
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Jane Christopher-Hennings
cDepartment of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, South Dakota, USA
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Eric A. Nelson
cDepartment of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, South Dakota, USA
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Juergen Richt
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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Feng Li
aDepartment of Biology and Microbiology, South Dakota State University, Brookings, South Dakota, USA
cDepartment of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, South Dakota, USA
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Wenjun Ma
bDepartment of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, Kansas, USA
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R. M. Sandri-Goldin
Roles: Editor
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DOI: 10.1128/JVI.00059-15
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ABSTRACT

Influenza B virus (IBV) causes seasonal epidemics in humans. Although IBV has been isolated from seals, humans are considered the primary host and reservoir of this important pathogen. It is unclear whether other animal species can support the replication of IBV and serve as a reservoir. Swine are naturally infected with both influenza A and C viruses. To determine the susceptibility of pigs to IBV infection, we conducted a serological survey for U.S. Midwest domestic swine herds from 2010 to 2012. Results of this study showed that antibodies to IBVs were detected in 38.5% (20/52) of sampled farms, and 7.3% (41/560) of tested swine serum samples were positive for IBV antibodies. Furthermore, swine herds infected with porcine reproductive and respiratory syndrome virus (PRRSV) showed a higher prevalence of IBV antibodies in our 2014 survey. In addition, IBV was detected in 3 nasal swabs collected from PRRSV-seropositive pigs by real-time RT-PCR and sequencing. Finally, an experimental infection in pigs, via intranasal and intratracheal routes, was performed using one representative virus from each of the two genetically and antigenically distinct lineages of IBVs: B/Brisbane/60/2008 (Victoria lineage) and B/Yamagata/16/1988 (Yamagata lineage). Pigs developed influenza-like symptoms and lung lesions, and they seroconverted after virus inoculation. Pigs infected with B/Brisbane/60/2008 virus successfully transmitted the virus to sentinel animals. Taken together, our data demonstrate that pigs are susceptible to IBV infection; therefore, they warrant further surveillance and investigation of swine as a potential host for human IBV.

IMPORTANCE IBV is an important human pathogen, but its ability to infect other species, for example, pigs, is not well understood. We showed serological evidence that antibodies to two genetically and antigenically distinct lineages of IBVs were present among domestic pigs, especially in swine herds previously infected with PRRSV, an immunosuppressive virus. IBV was detected in 3 nasal swabs from PRRSV-seropositive pigs by real-time reverse transcription-PCR and sequencing. Moreover, both lineages of IBV were able to infect pigs under experimental conditions, with transmissibility of influenza B/Victoria lineage virus among pigs being observed. Our results demonstrate that pigs are susceptible to IBV infections, indicating that IBV is a swine pathogen, and swine may serve as a natural reservoir of IBVs. In addition, pigs may serve as a model to study the mechanisms of transmission and pathogenesis of IBVs.

FOOTNOTES

    • Received 9 January 2015.
    • Accepted 3 February 2015.
    • Accepted manuscript posted online 11 February 2015.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/JVI.00059-15.

  • Copyright © 2015, American Society for Microbiology. All Rights Reserved.
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Domestic Pigs Are Susceptible to Infection with Influenza B Viruses
Zhiguang Ran, Huigang Shen, Yuekun Lang, Elizabeth A. Kolb, Nuri Turan, Laihua Zhu, Jingjiao Ma, Bhupinder Bawa, Qinfang Liu, Haixia Liu, Megan Quast, Gabriel Sexton, Florian Krammer, Ben M. Hause, Jane Christopher-Hennings, Eric A. Nelson, Juergen Richt, Feng Li, Wenjun Ma
Journal of Virology Apr 2015, 89 (9) 4818-4826; DOI: 10.1128/JVI.00059-15

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Domestic Pigs Are Susceptible to Infection with Influenza B Viruses
Zhiguang Ran, Huigang Shen, Yuekun Lang, Elizabeth A. Kolb, Nuri Turan, Laihua Zhu, Jingjiao Ma, Bhupinder Bawa, Qinfang Liu, Haixia Liu, Megan Quast, Gabriel Sexton, Florian Krammer, Ben M. Hause, Jane Christopher-Hennings, Eric A. Nelson, Juergen Richt, Feng Li, Wenjun Ma
Journal of Virology Apr 2015, 89 (9) 4818-4826; DOI: 10.1128/JVI.00059-15
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