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Archives of Virology

, Volume 164, Issue 2, pp 535–545 | Cite as

Pathogenicity of two novel human-origin H7N9 highly pathogenic avian influenza viruses in chickens and ducks

  • Taichiro Tanikawa
  • Yuko Uchida
  • Nobuhiro Takemae
  • Ryota Tsunekuni
  • Junki Mine
  • Ming-Tsan Liu
  • Ji-Rong Yang
  • Masayuki Shirakura
  • Shinji Watanabe
  • Takato Odagiri
  • Takehiko SaitoEmail author
Original Article

Abstract

Human infection by low-pathogenic avian influenza viruses of the H7N9 subtype was first reported in March 2013 in China. Subsequently, these viruses caused five outbreaks through September 2017. In the fifth outbreak, H7N9 virus possessing a multiple basic amino acid insertion in the cleavage site of hemagglutinin emerged and caused 4% of all human infections in that period. To date, H7N9 highly pathogenic avian influenza viruses (HPAIVs) have been isolated from poultry, mostly chickens, as well as the environment. To evaluate the relative infectivity of these viruses in poultry, chickens and ducks were subjected to experimental infection with two H7N9 HPAIVs isolated from humans, namely A/Guangdong/17SF003/2016 and A/Taiwan/1/2017. When chickens were inoculated with the HPAIVs at a dose of 106 50% egg infectious dose (EID50), all chickens died within 2–5 days after inoculation, and the viruses replicated in most of the internal organs examined. The 50% lethal doses of A/Guangdong/17SF003/2016 and A/Taiwan/1/2017 in chickens were calculated as 103.3 and 104.7 EID50, respectively. Conversely, none of the ducks inoculated with either virus displayed any clinical signs, and less-efficient virus replication and less shedding were observed in ducks compared to chickens. These findings indicate that chickens, but not ducks, are highly permissive hosts for emerging H7N9 HPAIVs.

Notes

Acknowledgements

The authors are grateful to the National Institute for Viral Disease Control and Prevention, CCDC, for kindly providing the A/Guangdong/17SF003/2016. The authors would also like to thank Enago (http://www.enago.jp) for the English language review.

Funding

This study was partially supported by the research project for improving food safety and animal health of the Ministry of Agriculture, Forestry and Fisheries of Japan.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Ethical standard statement

All experimental and animal procedures were approved by the ethics committee of the National Institute of Animal Health, Japan.

References

  1. 1.
    World Health Organization. Influenza at the human-animal interface. Monthly risk assessment summary as of 28 May 2018. https://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_28_05_2018.pdf?ua=1. Accessed 16 Sept 2018.
  2. 2.
    EFSA (European Food Safety Authority), EFSA ECDC (European Centre for Disease Prevention and Control), EURL (European Reference Laboratory for Avian Influenza), Adlhoch C, Brouwer A, Kuiken T, Mulatti P, Smietanka K, Staubach C, Willeberg P, Barrucci F, Verdonck F (2018) Amato L and Baldinelli F (2018) Scientific report: avian influenza overview November 2017–February 2018. EFSA J 16(3):5240.  https://doi.org/10.2903/j.efsa.2018.5240 Google Scholar
  3. 3.
    World Health Organization. Human infection with avian influenza A(H7N9) virus—update. Disease outbreak news of 17 February 2014. http://www.who.int/csr/don/2014_02_17/en/. Accessed 9 May 2018.
  4. 4.
    World Health Organization. Human infection with avian influenza A(H7N9) virus—Canada. Disease outbreak news of 1 February 2015. http://www.who.int/csr/don/01-february-2015-avian-influenza/en/. Accessed 9 May 2018.
  5. 5.
    Chinese National Influenza Center. Chinese influenza weekly report. http://www.chinaivdc.cn/cnic/en/Surveillance/WeeklyReport/201807/t20180706_183192.htm. Accessed 16 Sept 2018
  6. 6.
    World Health Organization. Human infection with avian influenza A(H7N9) virus—China. Disease outbreak news of 22 February 2017. http://www.who.int/csr/don/22-february-2017-ah7n9-china/en/. Accessed 9 May 2018.
  7. 7.
    Wang D, Yang L, Zhu W, Zhang Y, Zou S, Bo H, Gao R, Dong J, Huang W, Guo J, Li Z, Zhao X, Li X, Xin L, Zhou J, Chen T, Dong L, Wei H, Li X, Liu L, Tang J, Lan Y, Yang J, Shu Y (2016) Two outbreak sources of influenza A (H7N9) viruses have been established in China. J Virol 90:5561–5573.  https://doi.org/10.1128/JVI.03173-15 CrossRefGoogle Scholar
  8. 8.
    Yang L, Zhu W, Li X, Chen M, Wu J, Yu P, Qi S, Huang Y, Shi W, Dong J, Zhao X, Huang W, Li Z, Zeng X, Bo H, Chen T, Chen W, Liu J, Zhang Y, Liang Z, Shi W, Shu Y, Wang D (2017) Genesis and spread of newly emerged highly pathogenic H7N9 avian viruses in mainland China. J Virol 91:e01277-17.  https://doi.org/10.1128/jvi.01277-17 CrossRefGoogle Scholar
  9. 9.
    World Organisation for Animal Health. Update on highly pathogenic avian influenza in animals (Type H5 and H7). http://www.oie.int/en/animal-health-in-the-world/update-on-avian-influenza/. Accessed 16 Sept 2018
  10. 10.
    Chen J, Zhang J, Zhu W, Zhang Y, Tan H, Liu M, Cai M, Shen J, Ly H, Chen J (2017) First genome report and analysis of chicken H7N9 influenza viruses with poly-basic amino acids insertion in the hemagglutinin cleavage site. Sci Rep 7:9972.  https://doi.org/10.1038/s41598-017-10605-6 CrossRefGoogle Scholar
  11. 11.
    Qi W, Jia W, Liu D, Li J, Bi Y, Xie S, Li B, Hu T, Du Y, Xing L, Zhang J, Zhang F, Wei X, Eden JS, Li H, Tian H, Li W, Su G, Lao G, Xu C, Xu B, Liu W, Zhang G, Ren T, Holmes EC, Cui J, Shi W, Gao GF, Liao M (2018) Emergence and adaptation of a novel highly pathogenic H7N9 Influenza virus in birds and humans from a 2013 human-infecting low-pathogenic ancestor. J Virol 92:e00921-17.  https://doi.org/10.1128/jvi.00921-17 CrossRefGoogle Scholar
  12. 12.
    Quan C, Shi W, Yang Y, Yang Y, Liu X, Xu W, Li H, Li J, Wang Q, Tong Z, Wong G, Zhang C, Ma S, Ma Z, Fu G, Zhang Z, Huang Y, Song H, Yang L, Liu WJ, Liu Y, Liu W, Gao GF, Bi Y (2018) New threats of H7N9 influenza virus: the spread and evolution of highly and low pathogenic variants with high genomic diversity in Wave Five. J Virol.  https://doi.org/10.1128/jvi.00301-18 Google Scholar
  13. 13.
    Belser JA, Gustin KM, Pearce MB, Maines TR, Zeng H, Pappas C, Sun X, Carney PJ, Villanueva JM, Stevens J, Katz JM, Tumpey TM (2013) Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice. Nature 501:556–559.  https://doi.org/10.1038/nature12391 CrossRefGoogle Scholar
  14. 14.
    Watanabe T, Kiso M, Fukuyama S, Nakajima N, Imai M, Yamada S, Murakami S, Yamayoshi S, Iwatsuki-Horimoto K, Sakoda Y, Takashita E, McBride R, Noda T, Hatta M, Imai H, Zhao D, Kishida N, Shirakura M, de Vries RP, Shichinohe S, Okamatsu M, Tamura T, Tomita Y, Fujimoto N, Goto K, Katsura H, Kawakami E, Ishikawa I, Watanabe S, Ito M, Sakai-Tagawa Y, Sugita Y, Uraki R, Yamaji R, Eisfeld AJ, Zhong G, Fan S, Ping J, Maher EA, Hanson A, Uchida Y, Saito T, Ozawa M, Neumann G, Kida H, Odagiri T, Paulson JC, Hasegawa H, Tashiro M, Kawaoka Y (2013) Characterization of H7N9 influenza A viruses isolated from humans. Nature 501:551–555.  https://doi.org/10.1038/nature12392 CrossRefGoogle Scholar
  15. 15.
    Kalthoff D, Bogs J, Grund C, Tauscher K, Teifke JP, Starick E, Harder T, Beer M (2014) Avian influenza H7N9/13 and H7N7/13: a comparative virulence study in chickens, pigeons, and ferrets. J Virol 88:9153–9165.  https://doi.org/10.1128/jvi.01241-14 CrossRefGoogle Scholar
  16. 16.
    Uchida Y, Kanehira K, Takemae N, Hikono H, Saito T (2017) Susceptibility of chickens, quail, and pigeons to an H7N9 human influenza virus and subsequent egg-passaged strains. Arch Virol 162:103–116.  https://doi.org/10.1007/s00705-016-3090-6 CrossRefGoogle Scholar
  17. 17.
    Shi J, Deng G, Kong H, Gu C, Ma S, Yin X, Zeng X, Cui P, Chen Y, Yang H, Wan X, Wang X, Liu L, Chen P, Jiang Y, Liu J, Guan Y, Suzuki Y, Li M, Qu Z, Guan L, Zang J, Gu W, Han S, Song Y, Hu Y, Wang Z, Gu L, Yang W, Liang L, Bao H, Tian G, Li Y, Qiao C, Jiang L, Li C, Bu Z, Chen H (2017) H7N9 virulent mutants detected in chickens in China pose an increased threat to humans. Cell Res 27:1409–1421.  https://doi.org/10.1038/cr.2017 CrossRefGoogle Scholar
  18. 18.
    Food and Agriculture Organization of the United Nations. H7N9 situation update. http://www.fao.org/ag/againfo/programmes/en/empres/H7N9/Situation_update.html. Accessed 16 Sept 2018
  19. 19.
    Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Zhang Y, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y (2013) Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368:1888–1897.  https://doi.org/10.1056/NEJMoa1304459 CrossRefGoogle Scholar
  20. 20.
    Zhang F, Bi Y, Wang J, Wong G, Shi W, Hu F, Yang Y, Yang L, Deng X, Jiang S, He X, Liu Y, Yin C, Zhong N, Gao GF (2017) Human infections with recently-emerging highly pathogenic H7N9 avian influenza virus in China. J Infect 75:71–75.  https://doi.org/10.1016/j.jinf.2017.04.001 CrossRefGoogle Scholar
  21. 21.
    Yang JR, Liu MT (2017) Human infection caused by an avian influenza A (H7N9) virus with a polybasic cleavage site in Taiwan, 2017. JFMA 116:210–212.  https://doi.org/10.1016/j.jfma.2017.02.011 Google Scholar
  22. 22.
    Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493–497CrossRefGoogle Scholar
  23. 23.
    Organization WHO (2002) WHO manual on animal influenza diagnosis and surveillance. WHO/CDS/CSR/ NCS/2002.5.Google Scholar
  24. 24.
    Yen H-L, Herlocher LM, Hoffmann E, Matrosovich MN, Monto AS, Webster RG, Govorkova EA (2005) Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob Agents Chemother 49:4075–4084CrossRefGoogle Scholar
  25. 25.
    Ohuchi M, Ohuchi R, Feldmann A, Klenk HD (1997) Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J Virol 71:8377–8384Google Scholar
  26. 26.
    Kong W, Liu L, Wang Y, He Q, Wu S, Qin Z, Wang J, Sun H, Sun Y, Zhang R (2015) C-terminal elongation of NS1 of H9N2 influenza virus induces a high level of inflammatory cytokines and increases transmission. J Gen Virol 96:259–268CrossRefGoogle Scholar
  27. 27.
    Costa T, Chaves AJ, Valle R, Darji A, van Riel D, Kuiken T, Majó N, Ramis A (2012) Distribution patterns of influenza virus receptors and viral attachment patterns in the respiratory and intestinal tracts of seven avian species. Vet Res 43:28CrossRefGoogle Scholar
  28. 28.
    Hoffmann T, Munier S, Larcher T, Soubieux D, Ledevin M, Esnault E, Tourdes A, Croville G, Guérin J-L, Quéré P (2012) Length variations in the NA stalk of an H7N1 influenza virus have opposite effects on viral excretion in chickens and ducks. J Virol 86:584–588CrossRefGoogle Scholar
  29. 29.
    Li J, Cardona CJ (2010) Adaptation and transmission of a wild duck avian influenza isolate in chickens. Avian Dis 54:586–590CrossRefGoogle Scholar
  30. 30.
    Magor KE, Navarro DM, Barber MR, Petkau K, Fleming-Canepa X, Blyth GA, Blaine AH (2013) Defense genes missing from the flight division. Dev Comp Immunol 41:377–388CrossRefGoogle Scholar
  31. 31.
    Barber MR, Aldridge JR, Webster RG, Magor KE (2010) Association of RIG-I with innate immunity of ducks to influenza. Proc Natl Acad Sci 107:5913–5918CrossRefGoogle Scholar
  32. 32.
    Pantin-Jackwood MJ, Miller PJ, Spackman E, Swayne DE, Susta L, Costa-Hurtado M, Suarez DL (2014) Role of poultry in the spread of novel H7N9 influenza virus in China. J Virol 88:5381–5390.  https://doi.org/10.1128/jvi.03689-13 CrossRefGoogle Scholar
  33. 33.
    Hiono T, Okamatsu M, Yamamoto N, Ogasawara K, Endo M, Kuribayashi S, Shichinohe S, Motohashi Y, Chu D-H, Suzuki M (2016) Experimental infection of highly and low pathogenic avian influenza viruses to chickens, ducks, tree sparrows, jungle crows, and black rats for the evaluation of their roles in virus transmission. Vet Microbiol 182:108–115CrossRefGoogle Scholar
  34. 34.
    Löndt BZ, Núñez A, Banks J, Alexander DJ, Russell C, Richard-Löndt AC, Brown IH (2010) The effect of age on the pathogenesis of a highly pathogenic avian influenza (HPAI) H5N1 virus in Pekin ducks (Anas platyrhynchos) infected experimentally. Influenza Other Respir Viruses 4:17–25CrossRefGoogle Scholar
  35. 35.
    Xu X, Subbarao K, Cox NJ, Guo Y (1999) Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 261:15–19CrossRefGoogle Scholar
  36. 36.
    Ip HS, Torchetti MK, Crespo R, Kohrs P, DeBruyn P, Mansfield KG, Baszler T, Badcoe L, Bodenstein B, Shearn-Bochsler V (2015) Novel Eurasian highly pathogenic avian influenza A H5 viruses in wild birds, Washington, USA, 2014. Emerg Infect Dis 21:886CrossRefGoogle Scholar
  37. 37.
    U.S. Department of Agriculture, Animal and Plant Health Inspection Service. HPAI 2014/15 confirmed detections. https://www.aphis.usda.gov/aphis/ourfocus/animalhealth/animal-disease-information/avian-influenza-disease/sa_detections_by_states/hpai-2014-2015-confirmed-detections. Accessed 10 May 2018.
  38. 38.
    Lycett SJ, Bodewes R, Pohlmann A, Banks J, Bányai K, Boni MF, Bouwstra R, Breed AC, Brown IH, Chen H, Dan A (2016) Role for migratory wild birds in the global spread of avian influenza H5N8. Science (New York, NY) 354:213–217.  https://doi.org/10.1126/science.aaf8852 CrossRefGoogle Scholar
  39. 39.
    Ministry of Environment, Government of Japan. Information on highly pathogenic influenza. https://www.env.go.jp/nature/dobutsu/bird_flu/index.html. Accessed 16 Sept 2018.
  40. 40.
    Pantin-Jackwood MJ, Costa-Hurtado M, Shepherd E, DeJesus E, Smith D, Spackman E, Kapczynski DR, Suarez DL, Stallknecht DE, Swayne DE (2016) Pathogenicity and transmission of H5 and H7 highly pathogenic avian influenza viruses in mallards. J Virol 90:9967–9982CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Taichiro Tanikawa
    • 1
  • Yuko Uchida
    • 1
  • Nobuhiro Takemae
    • 1
  • Ryota Tsunekuni
    • 1
  • Junki Mine
    • 1
  • Ming-Tsan Liu
    • 2
  • Ji-Rong Yang
    • 2
  • Masayuki Shirakura
    • 3
  • Shinji Watanabe
    • 3
  • Takato Odagiri
    • 3
  • Takehiko Saito
    • 1
    • 4
    Email author
  1. 1.Division of Transboundary Animal Disease, National Institute of Animal HealthNational Agriculture and Food Research Organization (NARO)TsukubaJapan
  2. 2.Center for Research, Diagnostics and Vaccine Development, Centers for Disease ControlMinistry of Health and WelfareTaipeiTaiwan
  3. 3.Influenza Virus Research CenterNational Institute of Infectious DiseasesMusashimurayamaJapan
  4. 4.United Graduate School of Veterinary SciencesGifu UniversityGifuJapan

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