Antiviral Susceptibilities of Avian Influenza A(H5), A(H7), and A(H9) Viruses Isolated in Japan

The circulation of avian influenza A viruses in poultry is a public health concern due to the potential transmissibility and severity of these viral infections. Monitoring the susceptibility of these viruses to antivirals is important for developing measures to strengthen the level of preparedness a...

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Published in	Japanese Journal of Infectious Diseases Vol. 75; no. 4; pp. 398 - 402
Main Authors	Takashita, Emi, Morita, Hiroko, Nagata, Shiho, Shirakura, Masayuki, Fujisaki, Seiichiro, Miura, Hideka, Takayama, Ikuyo, Arita, Tomoko, Suzuki, Yasushi, Yamaoka, Masaoki, Tanikawa, Taichiro, Tsunekuni, Ryota, Mine, Junki, Sakuma, Saki, Uchida, Yuko, Shibata, Akihiro, Iwanaka, Mari, Kishida, Noriko, Nakamura, Kazuya, Kageyama, Tsutomu, Watanabe, Shinji, Hasegawa, Hideki, The Influenza Virus Surveillance Group of Japan
Format	Journal Article
Language	English
Published	Japan National Institute of Infectious Diseases, Japanese Journal of Infectious Diseases Editorial Committee 31.07.2022 Japan Science and Technology Agency
Subjects	Amino acids Antiviral agents antiviral susceptibility Avian flu avian influenza DNA-directed RNA polymerase Exo-a-sialidase Influenza Influenza A Inhibitors neuraminidase inhibitor Oseltamivir Pandemics Public health RNA polymerase RNA polymerase inhibitor Viral infections Viruses Zanamivir Japan Avian influenza neuraminidase inhibitor antiviral susceptibility RNA polymerase inhibitor
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Abstract	The circulation of avian influenza A viruses in poultry is a public health concern due to the potential transmissibility and severity of these viral infections. Monitoring the susceptibility of these viruses to antivirals is important for developing measures to strengthen the level of preparedness against influenza pandemics. However, drug susceptibility information on these viruses is limited. Here, we determined the susceptibilities of avian influenza A(H5N1), A(H5N2), A(H5N8), A(H7N7), A(H7N9), A(H9N1), and A(H9N2) viruses isolated in Japan to the antivirals approved for use there: an M2 inhibitor (amantadine), neuraminidase inhibitors (oseltamivir, peramivir, zanamivir, and laninamivir) and RNA polymerase inhibitors (baloxavir and favipiravir). Genotypic methods that detect amino acid substitutions associated with antiviral resistance and phenotypic methods that assess phenotypic viral susceptibility to drugs have revealed that these avian influenza A viruses are susceptible to neuraminidase and RNA polymerase inhibitors. These results suggest that neuraminidase and RNA polymerase inhibitors currently approved in Japan could be a treatment option against influenza A virus infections in humans.
AbstractList	The circulation of avian influenza A viruses in poultry is a public health concern due to the potential transmissibility and severity of these viral infections. Monitoring the susceptibility of these viruses to antivirals is important for developing measures to strengthen the level of preparedness against influenza pandemics. However, drug susceptibility information on these viruses is limited. Here, we determined the susceptibilities of avian influenza A(H5N1), A(H5N2), A(H5N8), A(H7N7), A(H7N9), A(H9N1), and A(H9N2) viruses isolated in Japan to the antivirals approved for use there: an M2 inhibitor (amantadine), neuraminidase inhibitors (oseltamivir, peramivir, zanamivir, and laninamivir) and RNA polymerase inhibitors (baloxavir and favipiravir). Genotypic methods that detect amino acid substitutions associated with antiviral resistance and phenotypic methods that assess phenotypic viral susceptibility to drugs have revealed that these avian influenza A viruses are susceptible to neuraminidase and RNA polymerase inhibitors. These results suggest that neuraminidase and RNA polymerase inhibitors currently approved in Japan could be a treatment option against influenza A virus infections in humans. Circulation of avian influenza A viruses in poultry is a public health concern because these viruses may cause severe disease in humans and have the potential to become more transmissible among humans. Monitoring the susceptibility of these viruses to antivirals is important for influenza pandemic preparedness. However, information about their antiviral susceptibility is limited. Here, we determined the susceptibilities of avian influenza A(H5N1), A(H5N2), A(H5N8), A(H7N7), A(H7N9), A(H9N1), and A(H9N2) viruses isolated in Japan to the antivirals approved for use there: the M2 inhibitor amantadine; the neuraminidase inhibitors oseltamivir, peramivir, zanamivir, and laninamivir; and the RNA polymerase inhibitors baloxavir and favipiravir. Genotypic methods that detect amino acid substitutions associated with antiviral resistance and phenotypic methods that assess viral susceptibility to drugs revealed that these avian influenza A viruses are susceptible to neuraminidase inhibitors and RNA polymerase inhibitors. These results suggest that the neuraminidase inhibitors and the RNA polymerase inhibitors currently approved in Japan could be a treatment option against influenza A virus infections in humans. The circulation of avian influenza A viruses in poultry is a public health concern due to the potential transmissibility and severity of these viral infections. Monitoring the susceptibility of these viruses to antivirals is important for developing measures to strengthen the level of preparedness against influenza pandemics. However, drug susceptibility information on these viruses is limited. Here, we determined the susceptibilities of avian influenza A(H5N1), A(H5N2), A(H5N8), A(H7N7), A(H7N9), A(H9N1), and A(H9N2) viruses isolated in Japan to the antivirals approved for use there: an M2 inhibitor (amantadine), neuraminidase inhibitors (oseltamivir, peramivir, zanamivir, and laninamivir) and RNA polymerase inhibitors (baloxavir and favipiravir). Genotypic methods that detect amino acid substitutions associated with antiviral resistance and phenotypic methods that assess phenotypic viral susceptibility to drugs have revealed that these avian influenza A viruses are susceptible to neuraminidase and RNA polymerase inhibitors. These results suggest that neuraminidase and RNA polymerase inhibitors currently approved in Japan could be a treatment option against influenza A virus infections in humans.The circulation of avian influenza A viruses in poultry is a public health concern due to the potential transmissibility and severity of these viral infections. Monitoring the susceptibility of these viruses to antivirals is important for developing measures to strengthen the level of preparedness against influenza pandemics. However, drug susceptibility information on these viruses is limited. Here, we determined the susceptibilities of avian influenza A(H5N1), A(H5N2), A(H5N8), A(H7N7), A(H7N9), A(H9N1), and A(H9N2) viruses isolated in Japan to the antivirals approved for use there: an M2 inhibitor (amantadine), neuraminidase inhibitors (oseltamivir, peramivir, zanamivir, and laninamivir) and RNA polymerase inhibitors (baloxavir and favipiravir). Genotypic methods that detect amino acid substitutions associated with antiviral resistance and phenotypic methods that assess phenotypic viral susceptibility to drugs have revealed that these avian influenza A viruses are susceptible to neuraminidase and RNA polymerase inhibitors. These results suggest that neuraminidase and RNA polymerase inhibitors currently approved in Japan could be a treatment option against influenza A virus infections in humans.
ArticleNumber	JJID.2021.751
Author	Takashita, Emi Yamaoka, Masaoki Shirakura, Masayuki Morita, Hiroko Mine, Junki Suzuki, Yasushi Watanabe, Shinji Miura, Hideka Uchida, Yuko Fujisaki, Seiichiro Tsunekuni, Ryota Kageyama, Tsutomu Iwanaka, Mari The Influenza Virus Surveillance Group of Japan Nakamura, Kazuya Shibata, Akihiro Takayama, Ikuyo Tanikawa, Taichiro Sakuma, Saki Nagata, Shiho Kishida, Noriko Hasegawa, Hideki Arita, Tomoko
AuthorAffiliation	The members of the group are listed in the Appendix
AuthorAffiliation_xml	– name: The members of the group are listed in the Appendix
Author_xml	– sequence: 1 fullname: Takashita, Emi organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 2 fullname: Morita, Hiroko organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 3 fullname: Nagata, Shiho organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 4 fullname: Shirakura, Masayuki organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 5 fullname: Fujisaki, Seiichiro organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 6 fullname: Miura, Hideka organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 7 fullname: Takayama, Ikuyo organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 8 fullname: Arita, Tomoko organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 9 fullname: Suzuki, Yasushi organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 10 fullname: Yamaoka, Masaoki organization: Hyogo Prefectural Institute of Public Health Science, Japan – sequence: 11 fullname: Tanikawa, Taichiro organization: Virus group, Division of Infectious Animal Disease Research, National Institute of Animal Health, National Agriculture and Food Research Organization, Japan – sequence: 12 fullname: Tsunekuni, Ryota organization: Emerging Virus Group, Division of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research Organization, Japan – sequence: 13 fullname: Mine, Junki organization: Emerging Virus Group, Division of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research Organization, Japan – sequence: 14 fullname: Sakuma, Saki organization: Emerging Virus Group, Division of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research Organization, Japan – sequence: 15 fullname: Uchida, Yuko organization: Emerging Virus Group, Division of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research Organization, Japan – sequence: 16 fullname: Shibata, Akihiro organization: Animal Quarantine Service, Ministry of Agriculture, Forestry and Fisheries, Japan – sequence: 17 fullname: Iwanaka, Mari organization: Animal Quarantine Service, Ministry of Agriculture, Forestry and Fisheries, Japan – sequence: 18 fullname: Kishida, Noriko organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 19 fullname: Nakamura, Kazuya organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 20 fullname: Kageyama, Tsutomu organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 21 fullname: Watanabe, Shinji organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 22 fullname: Hasegawa, Hideki organization: Research Center for Influenza and Respiratory Viruses, National Institute of Infectious Diseases, Japan – sequence: 23 fullname: The Influenza Virus Surveillance Group of Japan
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Cites_doi	10.1056/NEJMoa1304459 10.1016/j.virol.2018.08.001 10.1016/j.vetmic.2007.04.025 10.3389/fmicb.2018.03026 10.3390/v13030489 10.1038/nature12392 10.1016/j.antiviral.2020.104828 10.1016/j.antiviral.2020.104718 10.1128/JVI.01514-15 10.1006/viro.1998.9529 10.1016/j.chom.2017.09.008 10.1128/JVI.01580-17 10.1111/tbed.12726 10.1073/pnas.1811345115
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References	7. Imai M, Watanabe T, Kiso M, et al. A highly pathogenic avian H7N9 influenza virus isolated from a human is lethal in some ferrets infected via respiratory droplets. Cell Host Microbe. 2017;22:615-626. e8. 9. Goldhill DH, Te Velthuis AJW, Fletcher RA, et al. The mechanism of resistance to favipiravir in influenza. Proc Natl Acad Sci U S A. 2018;115:11613-11618. 11. Takashita E, Abe T, Morita H, et al. Influenza A(H1N1)pdm09 virus exhibiting reduced susceptibility to baloxavir due to a PA E23K substitution detected from a child without baloxavir treatment. Antiviral Res. 2020;180:104828. 14. Sakuma S, Uchida Y, Kajita M, et al. First outbreak of an H5N8 highly pathogenic avian influenza virus on a chicken farm in Japan in 2020. Viruses. 2021;13:489. 8. Okamatsu M, Saito T, Yamamoto Y, et al. Low pathogenicity H5N2 avian influenza outbreak in Japan during the 2005–2006. Vet Microbiol. 2007;124:35-46. 15. Takashita E, Daniels RS, Fujisaki S, et al. Global update on the susceptibilities of human influenza viruses to neuraminidase inhibitors and the cap-dependent endonuclease inhibitor baloxavir, 2017–2018. Antiviral Res. 2020;175:104718. 3. World Health Organization (WHO). Antigenic and genetic characteristics of zoonotic influenza A viruses and development of candidate vaccine viruses for pandemic preparedness. Available at <https://cdn.who.int/media/docs/default-source/influenza/who-influenza-recommendations/vcm-northern-hemisphere-recommendation-2021-2022/202103_zoonotic_vaccinevirusupdate.pdf?sfvrsn=97ae1340_13>. Accessed July 1, 2022. 10. Takashita E, Morita H, Ogawa R, et al. Susceptibility of influenza viruses to the novel cap-dependent endonuclease inhibitor baloxavir marboxil. Front Microbiol. 2018;9:3026. 2. Gao R, Cao B, Hu Y, et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013;368:1888-1897. 12. Choi WS, Jeong JH, Kwon JJ, et al. Screening for neuraminidase inhibitor resistance markers among avian influenza viruses of the N4, N5, N6, and N8 neuraminidase subtypes. J Virol. 2018;92:e01580-17. 5. Shibata A, Hiono T, Fukuhara H, et al. Isolation and characterization of avian influenza viruses from raw poultry products illegally imported to Japan by international flight passengers. Transbound Emerg Dis. 2018;65:465-475. 1. Bender C, Hall H, Huang J, et al. Characterization of the surface proteins of influenza A(H5N1) viruses isolated from humans in 1997–1998. Virology. 1999;254:115-123. 4. Shibata A, Okamatsu M, Sumiyoshi R, et al. Repeated detection of H7N9 avian influenza viruses in raw poultry meat illegally brought to Japan by international flight passengers. Virology. 2018;524:10-17. 6. Watanabe T, Kiso M, Fukuyama S, et al. Characterization of H7N9 influenza A viruses isolated from humans. Nature. 2013;501:551-555. 13. Song MS, Marathe BM, Kumar G, et al. Unique determinants of neuraminidase inhibitor resistance among N3, N7, and N9 avian influenza viruses. J Virol. 2015;89:10891-10900. 16. Global Initiation on Sharing All Influenza Data (GISAID). Epi Ful database. Available at <https://www.gisaid.org>. Accessed July 1, 2022. 11 12 13 14 15 16 1 2 3 4 5 6 7 8 9 10
References_xml	– reference: 8. Okamatsu M, Saito T, Yamamoto Y, et al. Low pathogenicity H5N2 avian influenza outbreak in Japan during the 2005–2006. Vet Microbiol. 2007;124:35-46. – reference: 10. Takashita E, Morita H, Ogawa R, et al. Susceptibility of influenza viruses to the novel cap-dependent endonuclease inhibitor baloxavir marboxil. Front Microbiol. 2018;9:3026. – reference: 13. Song MS, Marathe BM, Kumar G, et al. Unique determinants of neuraminidase inhibitor resistance among N3, N7, and N9 avian influenza viruses. J Virol. 2015;89:10891-10900. – reference: 7. Imai M, Watanabe T, Kiso M, et al. A highly pathogenic avian H7N9 influenza virus isolated from a human is lethal in some ferrets infected via respiratory droplets. Cell Host Microbe. 2017;22:615-626. e8. – reference: 2. Gao R, Cao B, Hu Y, et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013;368:1888-1897. – reference: 6. Watanabe T, Kiso M, Fukuyama S, et al. Characterization of H7N9 influenza A viruses isolated from humans. Nature. 2013;501:551-555. – reference: 15. Takashita E, Daniels RS, Fujisaki S, et al. Global update on the susceptibilities of human influenza viruses to neuraminidase inhibitors and the cap-dependent endonuclease inhibitor baloxavir, 2017–2018. Antiviral Res. 2020;175:104718. – reference: 4. Shibata A, Okamatsu M, Sumiyoshi R, et al. Repeated detection of H7N9 avian influenza viruses in raw poultry meat illegally brought to Japan by international flight passengers. Virology. 2018;524:10-17. – reference: 3. World Health Organization (WHO). Antigenic and genetic characteristics of zoonotic influenza A viruses and development of candidate vaccine viruses for pandemic preparedness. Available at <https://cdn.who.int/media/docs/default-source/influenza/who-influenza-recommendations/vcm-northern-hemisphere-recommendation-2021-2022/202103_zoonotic_vaccinevirusupdate.pdf?sfvrsn=97ae1340_13>. Accessed July 1, 2022. – reference: 9. Goldhill DH, Te Velthuis AJW, Fletcher RA, et al. The mechanism of resistance to favipiravir in influenza. Proc Natl Acad Sci U S A. 2018;115:11613-11618. – reference: 11. Takashita E, Abe T, Morita H, et al. Influenza A(H1N1)pdm09 virus exhibiting reduced susceptibility to baloxavir due to a PA E23K substitution detected from a child without baloxavir treatment. Antiviral Res. 2020;180:104828. – reference: 1. Bender C, Hall H, Huang J, et al. Characterization of the surface proteins of influenza A(H5N1) viruses isolated from humans in 1997–1998. Virology. 1999;254:115-123. – reference: 5. Shibata A, Hiono T, Fukuhara H, et al. Isolation and characterization of avian influenza viruses from raw poultry products illegally imported to Japan by international flight passengers. Transbound Emerg Dis. 2018;65:465-475. – reference: 16. Global Initiation on Sharing All Influenza Data (GISAID). Epi Ful database. Available at <https://www.gisaid.org>. Accessed July 1, 2022. – reference: 14. Sakuma S, Uchida Y, Kajita M, et al. First outbreak of an H5N8 highly pathogenic avian influenza virus on a chicken farm in Japan in 2020. Viruses. 2021;13:489. – reference: 12. Choi WS, Jeong JH, Kwon JJ, et al. Screening for neuraminidase inhibitor resistance markers among avian influenza viruses of the N4, N5, N6, and N8 neuraminidase subtypes. J Virol. 2018;92:e01580-17. – ident: 2 doi: 10.1056/NEJMoa1304459 – ident: 3 – ident: 4 doi: 10.1016/j.virol.2018.08.001 – ident: 8 doi: 10.1016/j.vetmic.2007.04.025 – ident: 10 doi: 10.3389/fmicb.2018.03026 – ident: 14 doi: 10.3390/v13030489 – ident: 6 doi: 10.1038/nature12392 – ident: 11 doi: 10.1016/j.antiviral.2020.104828 – ident: 16 – ident: 15 doi: 10.1016/j.antiviral.2020.104718 – ident: 13 doi: 10.1128/JVI.01514-15 – ident: 1 doi: 10.1006/viro.1998.9529 – ident: 7 doi: 10.1016/j.chom.2017.09.008 – ident: 12 doi: 10.1128/JVI.01580-17 – ident: 5 doi: 10.1111/tbed.12726 – ident: 9 doi: 10.1073/pnas.1811345115
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Snippet	The circulation of avian influenza A viruses in poultry is a public health concern due to the potential transmissibility and severity of these viral... Circulation of avian influenza A viruses in poultry is a public health concern because these viruses may cause severe disease in humans and have the potential...
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SubjectTerms	Amino acids Antiviral agents antiviral susceptibility Avian flu avian influenza DNA-directed RNA polymerase Exo-a-sialidase Influenza Influenza A Inhibitors neuraminidase inhibitor Oseltamivir Pandemics Public health RNA polymerase RNA polymerase inhibitor Viral infections Viruses Zanamivir
Title	Antiviral Susceptibilities of Avian Influenza A(H5), A(H7), and A(H9) Viruses Isolated in Japan
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