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Published in: Archives of Virology 2/2019

01-02-2019 | Original Article

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

Authors: Taichiro Tanikawa, Yuko Uchida, Nobuhiro Takemae, Ryota Tsunekuni, Junki Mine, Ming-Tsan Liu, Ji-Rong Yang, Masayuki Shirakura, Shinji Watanabe, Takato Odagiri, Takehiko Saito

Published in: Archives of Virology | Issue 2/2019

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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.
Literature
2.
go back to reference 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 CrossRef 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 CrossRef
11.
go back to reference 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 CrossRefPubMedPubMedCentral 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 CrossRefPubMedPubMedCentral
12.
go back to reference 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 CrossRefPubMedPubMedCentral 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 CrossRefPubMedPubMedCentral
14.
go back to reference 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 CrossRefPubMedPubMedCentral 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 CrossRefPubMedPubMedCentral
17.
go back to reference 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 CrossRefPubMedPubMedCentral 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 CrossRefPubMedPubMedCentral
19.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
22.
go back to reference Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493–497CrossRef Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493–497CrossRef
23.
go back to reference Organization WHO (2002) WHO manual on animal influenza diagnosis and surveillance. WHO/CDS/CSR/ NCS/2002.5. Organization WHO (2002) WHO manual on animal influenza diagnosis and surveillance. WHO/CDS/CSR/ NCS/2002.5.
24.
go back to reference 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 49:4075–4084CrossRefPubMedPubMedCentral 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 49:4075–4084CrossRefPubMedPubMedCentral
25.
go back to reference Ohuchi M, Ohuchi R, Feldmann A, Klenk HD (1997) Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J Virol 71:8377–8384PubMedPubMedCentral Ohuchi M, Ohuchi R, Feldmann A, Klenk HD (1997) Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J Virol 71:8377–8384PubMedPubMedCentral
26.
go back to reference 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 96:259–268CrossRefPubMed 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 96:259–268CrossRefPubMed
27.
go back to reference 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 43:28CrossRefPubMedPubMedCentral 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 43:28CrossRefPubMedPubMedCentral
28.
go back to reference 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 86:584–588CrossRefPubMedPubMedCentral 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 86:584–588CrossRefPubMedPubMedCentral
29.
go back to reference Li J, Cardona CJ (2010) Adaptation and transmission of a wild duck avian influenza isolate in chickens. Avian Dis 54:586–590CrossRefPubMed Li J, Cardona CJ (2010) Adaptation and transmission of a wild duck avian influenza isolate in chickens. Avian Dis 54:586–590CrossRefPubMed
30.
go back to reference 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 41:377–388CrossRefPubMed 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 41:377–388CrossRefPubMed
31.
go back to reference Barber MR, Aldridge JR, Webster RG, Magor KE (2010) Association of RIG-I with innate immunity of ducks to influenza. Proc Natl Acad Sci 107:5913–5918CrossRefPubMed Barber MR, Aldridge JR, Webster RG, Magor KE (2010) Association of RIG-I with innate immunity of ducks to influenza. Proc Natl Acad Sci 107:5913–5918CrossRefPubMed
33.
go back to reference 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 182:108–115CrossRefPubMed 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 182:108–115CrossRefPubMed
34.
go back to reference 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 4:17–25CrossRefPubMed 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 4:17–25CrossRefPubMed
35.
go back to reference 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 261:15–19CrossRefPubMed 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 261:15–19CrossRefPubMed
36.
go back to reference 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 21:886CrossRefPubMedPubMedCentral 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 21:886CrossRefPubMedPubMedCentral
40.
go back to reference 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 90:9967–9982CrossRefPubMedPubMedCentral 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 90:9967–9982CrossRefPubMedPubMedCentral
Metadata
Title
Pathogenicity of two novel human-origin H7N9 highly pathogenic avian influenza viruses in chickens and ducks
Authors
Taichiro Tanikawa
Yuko Uchida
Nobuhiro Takemae
Ryota Tsunekuni
Junki Mine
Ming-Tsan Liu
Ji-Rong Yang
Masayuki Shirakura
Shinji Watanabe
Takato Odagiri
Takehiko Saito
Publication date
01-02-2019
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 2/2019
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-018-4102-5

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