Top

Published in:

01-07-2015 | Original Article

Characterization of an H5N8 influenza A virus isolated from chickens during an outbreak of severe avian influenza in Japan in April 2014

Authors: Katsushi Kanehira, Yuko Uchida, Nobuhiro Takemae, Hirokazu Hikono, Ryota Tsunekuni, Takehiko Saito

Published in: Archives of Virology | Issue 7/2015

Abstract

A highly pathogenic avian influenza virus (HPAIV) of subtype H5N8, A/chicken/Kumamoto/1-7/2014, was isolated from a Japanese chicken farm during an outbreak in April 2014. Phylogenetic analysis revealed that this virus belonged to HA clade 2.3.4.4. All eight genomic segments showed high sequence similarity to those of the H5N8 subtype HPAIVs A/broiler duck/Korea/Buan2/2014 and A/baikal teal/Korea/Donglim3/2014, which were isolated in Korea in January 2014. Intranasal experimental infection of chickens and ducks with A/chicken/Kumamoto/1-7/2014 was performed to assess the pathogenicity of the virus in chickens and the potential for waterfowl to act as a virus reservoir and carrier. A high-titer virus challenge (10⁶ EID₅₀ per animal) was lethal in chickens, but they were unaffected by lower virus doses (10² EID₅₀ or 10⁴ EID₅₀ per animal). Virus challenge at all doses examined was found to result in asymptomatic infection of ducks. An HI assay revealed that A/chicken/Kumamoto/1-7/2014 possessed relatively low cross-reactivity with H5 viruses belonging to clades other than clade 2.3.4.4. These results suggest that waterfowl may be able to spread the virus even if they possess antibodies resulting from a previous infection with H5 HPAIV that was antigenically distinguishable from viruses belonging to clade 2.3.4.4.

Bridges CB, Lim W, Hu-Primmer J, Sims L, Fukuda K, Mak KH, Rowe T, Thompson WW, Conn L, Lu X, Cox NJ, Katz JM (2002) Risk of influenza A (H5N1) infection among poultry workers, Hong Kong, 1997–1998. J Infect Dis 185(8):1005–1010. doi:10.1086/340044 PubMedCrossRef

de Vries RP, Zhu X, McBride R, Rigter A, Hanson A, Zhong G, Hatta M, Xu R, Yu W, Kawaoka Y, de Haan CA, Wilson IA, Paulson JC (2014) Hemagglutinin receptor specificity and structural analyses of respiratory droplet-transmissible H5N1 viruses. J Virol 88(1):768–773. doi:10.1128/JVI.02690-13 PubMedCentralPubMedCrossRef

Fan S, Deng G, Song J, Tian G, Suo Y, Jiang Y, Guan Y, Bu Z, Kawaoka Y, Chen H (2009) Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. Virology 384(1):28–32. doi:10.1016/j.virol.2008.11.044 PubMedCrossRef

Gu M, Zhao G, Zhao K, Zhong L, Huang J, Wan H, Wang X, Liu W, Liu H, Peng D, Liu X (2013) Novel variants of clade 2.3.4 highly pathogenic avian influenza A(H5N1) viruses, China. Emerg Infect Dis 19(12):2021–2024. doi:10.3201/eid1912.130340 PubMedCentralPubMedCrossRef

Hatta M, Gao P, Halfmann P, Kawaoka Y (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293(5536):1840–1842. doi:10.1126/science.1062882 PubMedCrossRef

Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, Zhong G, Hanson A, Katsura H, Watanabe S, Li C, Kawakami E, Yamada S, Kiso M, Suzuki Y, Maher EA, Neumann G, Kawaoka Y (2012) Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486(7403):420–428. doi:10.1038/nature10831 PubMedCentralPubMed

Jiao P, Tian G, Li Y, Deng G, Jiang Y, Liu C, Liu W, Bu Z, Kawaoka Y, Chen H (2008) A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J Virol 82(3):1146–1154. doi:10.1128/JVI.01698-07 PubMedCentralPubMedCrossRef

Kanehira K, Takemae N, Uchida Y, Hikono H, Saito T (2014) Reassortant swine influenza viruses isolated in Japan contain genes from pandemic A(H1N1) 2009. Microbiol Immunol 58(6):327–341. doi:10.1111/1348-0421.12152 PubMedCrossRef

Kida H, Yanagawa R, Matsuoka Y (1980) Duck influenza lacking evidence of disease signs and immune response. Infect Immun 30(2):547–553PubMedCentralPubMed

10.

Kilpatrick AM, Chmura AA, Gibbons DW, Fleischer RC, Marra PP, Daszak P (2006) Predicting the global spread of H5N1 avian influenza. Proc Natl Acad Sci USA 103(51):19368–19373. doi:10.1073/pnas.0609227103 PubMedCentralPubMedCrossRef

11.

Kim Y-I, Pascua PNQ, Kwon H-I, Lim G-J, Kim E-H, Yoon S-W, Park S-J, Kim SM, Choi E-J, Si Y-J, Lee O-J, Shim W-S, Kim S-W, Mo I-P, Bae Y, Lim YT, Sung MH, Kim C-J, Webby RJ, Webster RG, Choi YK (2014) Pathobiological features of a novel, highly pathogenic avian influenza A(H5N8) virus. Emerg Microbes Infect 3:e75. doi:10.1038/emi.2014.75 PubMedCentralPubMedCrossRef

12.

Lee YJ, Kang HM, Lee EK, Song BM, Jeong J, Kwon YK, Kim HR, Lee KJ, Hong MS, Jang I, Choi KS, Kim JY, Lee HJ, Kang MS, Jeong OM, Baek JH, Joo YS, Park YH (2014) Lee HS (2014) Novel reassortant influenza A(H5N8) viruses, South Korea. Emerg Infect Dis 20(6):1087–1089. doi:10.3201/eid2006.140233 PubMedCentralPubMedCrossRef

13.

Li Q, Wang X, Gu M, Zhu J, Hao X, Gao Z, Sun Z, Hu J, Hu S, Wang X, Liu X, Liu X (2014) Novel H5 clade 2.3.4.6 viruses with both alpha-2,3 and alpha-2,6 receptor binding properties may pose a pandemic threat. Vet Res 45:127. doi:10.1186/s13567-014-0127-2 PubMedCentralPubMedCrossRef

14.

Linster M, van Boheemen S, de Graaf M, Schrauwen EJ, Lexmond P, Manz B, Bestebroer TM, Baumann J, van Riel D, Rimmelzwaan GF, Osterhaus AD, Matrosovich M, Fouchier RA, Herfst S (2014) Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus. Cell 157(2):329–339. doi:10.1016/j.cell.2014.02.04 PubMedCentralPubMedCrossRef

15.

Liu Q, Qiao C, Marjuki H, Bawa B, Ma J, Guillossou S, Webby RJ, Richt JA, Ma W (2012) Combination of PB2 271A and SR polymorphism at positions 590/591 is critical for viral replication and virulence of swine influenza virus in cultured cells and in vivo. J Virol 86(2):1233–1237. doi:10.1128/JVI.05699-11 PubMedCentralPubMedCrossRef

16.

Mase M, Tsukamoto K, Imada T, Imai K, Tanimura N, Nakamura K, Yamamoto Y, Hitomi T, Kira T, Nakai T, Kiso M, Horimoto T, Kawaoka Y, Yamaguchi S (2005) Characterization of H5N1 influenza A viruses isolated during the 2003–2004 influenza outbreaks in Japan. Virology 332(1):167–176. doi:10.1016/j.virol.2004.11.016 PubMedCrossRef

17.

Nakamura K, Imada T, Imai K, Yamamoto Y, Tanimura N, Yamada M, Mase M, Tsukamoto K, Yamaguchi S (2008) Pathology of specific-pathogen-free chickens inoculated with H5N1 avian influenza viruses isolated in Japan in 2004. Avian Dis 52(1):8–13PubMedCrossRef

18.

Nidom CA, Takano R, Yamada S, Sakai-Tagawa Y, Daulay S, Aswadi D, Suzuki T, Suzuki Y, Shinya K, Iwatsuki-Horimoto K, Muramoto Y, Kawaoka Y (2010) Influenza A (H5N1) viruses from pigs, Indonesia. Emerg Infect Dis 16(10):1515–1523. doi:10.3201/eid1610.100508 PubMedCentralPubMedCrossRef

19.

Pinto LH, Holsinger LJ, Lamb RA (1992) Influenza virus M2 protein has ion channel activity. Cell 69(3):517–528PubMedCrossRef

20.

Ramey AM, Spackman E, Yeh JY, Fujita G, Konishi K, Uchida K, Reed JA, Wilcox BR, Brown JD, Stallknecht DE (2013) Antibodies to H5 subtype avian influenza virus and Japanese encephalitis virus in northern pintails (Anas acuta) sampled in Japan. Jpn J Vet Res 61:117–123PubMed

21.

Reed LJ, Muench HA (1938) A simple method for estimating fifty percent endpoints. Am J Hyg 27(3):493–497

22.

Sakoda Y, Ito H, Uchida Y, Okamatsu M, Yamamoto N, Soda K, Nomura N, Kuribayashi S, Shichinohe S, Sunden Y, Umemura T, Usui T, Ozaki H, Yamaguchi T, Murase T, Ito T, Saito T, Takada A, Kida H (2012) Reintroduction of H5N1 highly pathogenic avian influenza virus by migratory water birds, causing poultry outbreaks in the 2010–2011 winter season in Japan. J Gen Virol 93(3):541–550. doi:10.1099/vir.0.037572-0 PubMedCrossRef

23.

Samson M, Pizzorno A, Abed Y, Boivin G (2013) Influenza virus resistance to neuraminidase inhibitors. Antiviral Res 98(2):174–185. doi:10.1016/j.antiviral.2013.03.014 PubMedCrossRef

24.

Schmolke M, Manicassamy B, Pena L, Sutton T, Hai R, Varga ZT, Hale BG, Steel J, Perez DR, Garcia-Sastre A (2011) Differential contribution of PB1-F2 to the virulence of highly pathogenic H5N1 influenza A virus in mammalian and avian species. PLoS Pathog 7(8):e1002186. doi:10.1371/journal.ppat.1002186 PubMedCentralPubMedCrossRef

25.

Srinivasan K, Raman R, Jayaraman A, Viswanathan K, Sasisekharan R (2013) Quantitative description of glycan-receptor binding of influenza A virus H7 hemagglutinin. PloS One 8(2):e49597. doi:10.1371/journal.pone.0049597 PubMedCentralPubMedCrossRef

26.

Steel J, Lowen AC, Mubareka S, Palese P (2009) Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5(1):e1000252. doi:10.1371/journal.ppat.1000252 PubMedCentralPubMedCrossRef

27.

Uchida Y, Chaichoune K, Wiriyarat W, Watanabe C, Hayashi T, Patchimasiri T, Nuansrichay B, Parchariyanon S, Okamatsu M, Tsukamoto K, Takemae N, Ratanakorn P, Yamaguchi S, Saito T (2008) Molecular epidemiological analysis of highly pathogenic avian influenza H5N1 subtype isolated from poultry and wild bird in Thailand. Virus Res 138(1–2):70–80. doi:10.1016/j.virusres.2008.08.007 PubMedCrossRef

28.

Uchida Y, Suzuki Y, Shirakura M, Kawaguchi A, Nobusawa E, Tanikawa T, Hikono H, Takemae N, Mase M, Kanehira K, Hayashi T, Tagawa Y, Tashiro M, Saito T (2012) Genetics and infectivity of H5N1 highly pathogenic avian influenza viruses isolated from chickens and wild birds in Japan during 2010-11. Virus Res 170(1–2):109–117. doi:10.1016/j.virusres.2012.09.004 PubMedCrossRef

29.

Watanabe Y, Ibrahim MS, Ellakany HF, Kawashita N, Mizuike R, Hiramatsu H, Sriwilaijaroen N, Takagi T, Suzuki Y, Ikuta K (2011) Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. PLoS Pathog 7(5):e1002068. doi:10.1371/journal.ppat.1002068 PubMedCentralPubMedCrossRef

30.

World Health Organization/World Organisation for Animal, Health Food Agriculture Organization, H. N. Evolution Working Group (2014) Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza Other Respir Viruses 8(3):384–388. doi:10.1111/irv.12230 CrossRef

31.

World Health Organization/World Organisation for Animal, Health Food Agriculture Organization, H. N. Evolution Working Group (2015) WHO/OIE/FAO H5 Working Group reports a new clade designated 2.3.4.4. Promed Archive Number: 20150114.3090250

32.

World Health Organization (2014). http://www.who.int/influenza/human_animal_interface/en/. Accessed 13 April 2015

33.

World Organisation for Animal Health (2014) Chapter 2.3.4 Avian influenza. Manual of diagnostic tests and vaccines for terrestrial animals 2014. http://www.oie.int/international-standard-setting/terrestrial-manual/access-online/. Accessed 13 April 2015

34.

World Organisation for Animal Health (2014) 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/2014/. Accessed 13 April 2015

35.

World Organisation for Animal Health (2015) 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/2015/. Accessed 13 April 2015

36.

Wu H, Peng X, Xu L, Jin C, Cheng L, Lu X, Xie T, Yao H, Wu N (2014) Novel reassortant influenza A(H5N8) viruses in domestic ducks, Eastern China. Emerg Infect Dis 20(8):1315–1318. doi:10.3201/eid2008.140339 PubMedCentralPubMedCrossRef

37.

Xu X, Subbarao 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(1):15–19PubMedCrossRef

38.

Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, Sakai-Tagawa Y, Muramoto Y, Ito M, Kiso M, Horimoto T, Shinya K, Sawada T, Kiso M, Usui T, Murata T, Lin Y, Hay A, Haire LF, Stevens DJ, Russell RJ, Gamblin SJ, Skehel JJ, Kawaoka Y (2006) Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444(7117):378–382. doi:10.1038/nature05264 PubMedCrossRef

39.

Yamamoto Y, Nakamura K, Yamada M, Mase M (2010) Comparative pathology of chickens and domestic ducks experimentally infected with highly pathogenic avian influenza viruses (H5N1) isolated in Japan in 2007 and 2008. Jpn Agric Res Q 44(1):73–80CrossRef

40.

Yang H, Chen LM, Carney PJ, Donis RO, Stevens J (2010) Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site. PLoS Pathog 6(9):e1001081. doi:10.1371/journal.ppat.1001081 PubMedCentralPubMedCrossRef

Title: Characterization of an H5N8 influenza A virus isolated from chickens during an outbreak of severe avian influenza in Japan in April 2014
Authors: Katsushi Kanehira
Yuko Uchida
Nobuhiro Takemae
Hirokazu Hikono
Ryota Tsunekuni
Takehiko Saito
Publication date: 01-07-2015
Publisher: Springer Vienna
Published in: Archives of Virology / Issue 7/2015
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-015-2428-9

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

Illustration of figure on mountain summit/© Orapun / Stock.adobe.com, STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2015

Occurrence and genetic diversity of human cosavirus in influent and effluent of wastewater treatment plants in Arizona, United States

Prevalence and genetic diversity of noroviruses in adults with acute gastroenteritis in Huzhou, China, 2013–2014

Analysis of complete genome sequences and a V239A substitution in the helicase domain of swine hepatitis E virus strains isolated in Canada

Experimental infection of inbred BALB/c and A/J mice with Massachusetts and Brazilian strains of infectious bronchitis virus (IBV)

Comparison of three magnetic-bead-based RNA extraction methods for detection of cucumber green mottle mosaic virus by real-time RT-PCR

First complete genomic characterization and phylogeny of a new recombinant of tomato yellow leaf curl virus (genus Begomovirus, family Geminiviridae) from Kuwait

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage