Rapid Evolution of H7N9 Highly Pathogenic Viruses that Emerged in China in 2017.

Jianzhong Shi¹ Guohua Deng¹ Shujie Ma¹ Xianying Zeng¹ Xin Yin¹ Mei Li¹ Bo Zhang¹ Pengfei Cui¹ Yan Chen¹ Huanliang Yang¹ Xiaopeng Wan¹ Liling Liu¹ Pucheng Chen¹ Yongping Jiang¹ Yuntao Guan¹ Jinxiong Liu¹ Wenli Gu¹ Shuyu Han¹ Yangming Song¹ Libin Liang¹ Zhiyuan Qu¹ Yujie Hou¹ Xiurong Wang¹ Hongmei Bao¹ Guobin Tian¹ Yanbing Li¹ Li Jiang¹ Chengjun Li¹ Hualan Chen²

Affiliations 2 institutions

State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, Heilongjiang 150069, People's Republic of China.
State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, Heilongjiang 150069, People's Republic of China. Electronic address: [email protected].

PMID30269969 DOI10.1016/j.chom.2018.08.006 Year2018 Journal Cell host & microbe Cell Host Microbe Languageeng Statusppublish

Abstract

H7N9 low pathogenic influenza viruses emerged in China in 2013 and mutated to highly pathogenic strains in 2017, resulting in human infections and disease in chickens. To control spread, a bivalent H5/H7 inactivated vaccine was introduced in poultry in September 2017. To monitor virus evolution and vaccine efficacy, we collected 53,884 poultry samples across China from February 2017 to January 2018. We isolated 252 H7N9 low pathogenic viruses, 69 H7N9 highly pathogenic viruses, and one H7N2 highly pathogenic virus, of which two low pathogenic and 14 highly pathogenic strains were collected after vaccine introduction. Genetic analysis of highly pathogenic strains revealed nine genotypes, one of which is predominant and widespread and contains strains exhibiting high virulence in mice. Additionally, some H7N9 and H7N2 viruses carrying duck virus genes are lethal in ducks. Thus, although vaccination reduced H7N9 infections, the increased virulence and expanded host range to ducks pose new challenges.

Supporting text Virus Host Location

chickens 146 ducks 81 evolution 62 H7N9 highly pathogenic influenza viruses 1 mice 254 vaccine 6 virulence 116 Evolution, Molecular 176 Animals 1948 Chickens 146 China 229 Communicable Diseases, Emerging 33 Ducks 81 Female 289 Humans 1440 Influenza A Virus, H7N9 Subtype 87 Influenza in Birds 341 Influenza Vaccines 20 Influenza, Human 286 Mice 253 Mice, Inbred BALB C 73 Specific Pathogen-Free Organisms 6 Vaccines, Inactivated 4 Virulence 108

Evidence records

5 total

Zoonotic Surveillance

3 records · 1 evidence types

Evidence type Virus Isolation

3 records

OVE3102 Virus Isolation

Key finding

Researchers successfully isolated 252 H7N9 low pathogenic influenza viruses from poultry samples collected across China.

Virus

Host

Location

Supporting text

We isolated 252 H7N9 low pathogenic viruses, 69 H7N9 highly pathogenic viruses, and one H7N2 highly pathogenic virus, of which two low pathogenic and 14 highly pathogenic strains were collected after vaccine introduction.

Sample type: poultry samples

OVE3103 Virus Isolation

Key finding

Researchers successfully isolated 69 H7N9 highly pathogenic influenza viruses from poultry samples collected across China.

Virus

Host

Location

Supporting text

Sample type: poultry samples

OVE3104 Virus Isolation

Key finding

Researchers successfully isolated one H7N2 highly pathogenic influenza virus from poultry samples collected across China.

Virus

Host

Location

Supporting text

Sample type: poultry samples

Experimental Infection

1 records · 1 evidence types

Evidence type Pathogenicity Experiment

1 records

OVE3105 Pathogenicity Experiment

Key finding

Highly pathogenic H7N9 influenza virus strains showed high virulence in experimentally infected mice.

Virus

Host

Location

Supporting text

Genetic analysis of highly pathogenic strains revealed nine genotypes, one of which is predominant and widespread and contains strains exhibiting high virulence in mice.

Method: experimental infection | genetic characterization of viral genotypes
Experimental system: mouse infection model

Genomic Evolution

1 records · 1 evidence types

Evidence type Phylogenetic Evolution

1 records

OVE3108 Phylogenetic Evolution

Key finding

Phylogenetic analysis of H7N9 highly pathogenic viruses collected from poultry in China identified nine genotypes, with one predominant and widely distributed lineage.

Virus

Host

Location

Supporting text

To monitor virus evolution and vaccine efficacy, we collected 53,884 poultry samples across China from February 2017 to January 2018. Genetic analysis of highly pathogenic strains revealed nine genotypes, one of which is predominant and widespread and contains strains exhibiting high virulence in mice.

Analysis methods: genetic analysis

References

52 references

Reference network

Force-directed citation graph. OmniVira-indexed references are prioritized and recursively expanded up to three steps.

260 nodes · 430 links · capped

Drag nodes to explore citation neighborhoods


PMID 19618616	History of highly pathogenic avian influenza	Alexander	2009
PMID 20300991	Detection of Influenza A Virus Neuraminidase and PB2 Gene Segments by One Step Reverse Transcription Polymerase Chain Reaction In RT-PCR Protocols: Second Edition, Series Title Methods in Molecular Biology, King N, ed. (Springer Science + Business Media, LLC; ), pp. 65–81	Alvarez	2010
PMID 23842497 In OmniVira	Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice.	Belser	2013
PMID 20181719	PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells	Bussey	2010
PMID 19471864	H5N1 avian influenza in China	Chen H (2009). H5N1 avian influenza in C	2009
PMID 19768404	Development and application of avian influenza vaccines in China	Chen	2009
PMID 23623390 In OmniVira	Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome.	Chen	2013
PMID 19117585	Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice	Fan	2009
PMID 26656683	Glycine at Position 622 in PB1 Contributes to the Virulence of H5N1 Avian Influenza Virus in Mice	Feng	2016
PMID 14745020	(2004). Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome	Fouchier	2004
PMID 10074171	Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong	Gao	1999
PMID 9815209	Characterization of influenza A/HongKong/156/97 (H5N1) virus in a mouse model and protective effect of zanamivir on H5N1 infection in mice	Gubareva	1998
PMID 11546875	Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses	Hatta	2001
PMID 23255810	(2013). The PA-gene-mediated lethal dissemination and excessive innate immune response contribute to the high virulence of H5N1 avian influenza virus in mice	Hu	2013
PMID 29056430 In OmniVira	A Highly Pathogenic Avian H7N9 Influenza Virus Isolated from A Human Is Lethal in Some Ferrets Infected via Respiratory Droplets.	Imai	2017
PMID 18032512	A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice	Jiao	2008
PMID 25411973 In OmniVira	Genetics, receptor binding property, and transmissibility in mammals of naturally isolated H9N2 Avian Influenza viruses.	Li	2014
PMID 20538856	(2010). Continued evolution of H5N1 influenza viruses in wild birds, domestic poultry, and humans in China from 2004 to 2009	Li	2010
PMID 16140781 In OmniVira	Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model.	Li	2005
PMID 16971424 In OmniVira	The NS1 gene contributes to the virulence of H5N1 avian influenza viruses.	Li	2006
PMID 28941628	Characteristics of the emerging chicken-origin highly pathogenic H7N9 viruses: A new threat to public health and poultry industry	Liu	2018
PMID 27558424	(2016). Characterization of Clade 7.2 H5 Avian Influenza Viruses That Continue To Circulate in Chickens in China	Liu	2016
PMID 10364342	A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans	Lu	1999
PMID 19995968	Adaptive strategies of the influenza virus polymerase for replication in humans	Mehle	2009
-	No. 2541 of the notice of the ministry of agriculture of the People’s Republic of China. The ministry of agriculture;	MoA	2017
PMID 24403592	Amino Acid Substitutions in Polymerase Basic Protein 2 Gene Contribute to the Pathogenicity of the Novel A/H7N9 Influenza Virus in Mammalian Hosts	Mok	2014
PMID 16707041	Host range restriction and pathogenicity in the context of influenza pandemic	Neumann	2006
-	Manual of diagnostic tests and vaccines for terrestrial animals. OIE - World Organisation for Animal Health	OIE	2011
-	Weekly Disease Information. OIE - World Organisation for Animal Health;	OIE	2018
PMID 24574407	Role of poultry in the spread of novel H7N9 influenza virus in China	Pantin-Jackwood	2014
PMID 29070694	(2018). Emergence and Adaptation of a Novel Highly Pathogenic H7N9 Influenza Virus in Birds and Humans from a 2013 Human-Infecting Low-Pathogenic Ancestor	Qi	2018
PMID 23925116 In OmniVira	Limited airborne transmission of H7N9 influenza A virus between ferrets.	Richard	2013
PMID 8790895	Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: amino acid sequence at the HA cleavage site as a marker of pathogenicity potential	Senne	1996
PMID 29151586	(2017). H7N9 virulent mutants detected in chickens in China pose an increased threat to humans	Shi	2017
-	(2013). Isolation and characterization of H7N9 viruses from live poultry markets-Implication of the source of current H7N9 infection in humans	Shi	2013
PMID 21177821	(2011). The PA protein directly contributes to the virulence of H5N1 avian influenza viruses in domestic ducks	Song	2011
PMID 8445709	A single amino acid in the PB2 gene of influenza A virus is a determinant of host range	Subbarao	1993
PMID 23402099	Impact of vaccines and vaccination on global control of avian influenza	Swayne	2012
PMID 22435196	Assessment of national strategies for control of high-pathogenicity avian influenza and low-pathogenicity notifiable avian influenza in poultry, with emphasis on vaccines and vaccination	Swayne	2011
PMID 22371588	(2012). A distinct lineage of influenza A virus from bats. Proceedings of the National Academy of Sciences of the United States of America. 109(11), 4269–4274	Tong	2012
PMID 24130481	(2013). New world bats harbor diverse influenza A viruses	Tong	2013
PMID 16330777	Quantification of the effect of vaccination on transmission of avian influenza (H7N7) in chickens	van der Goot	2005
PMID 23842494	(2013). Characterization of H7N9 influenza A viruses isolated from humans	Watanabe	2013
-	Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003–2018	WHO/GIP (2018a)	2011
-	Monthly Risk Assessment Summary	WHO/GIP (2018b)	2011
PMID 16424427	Avian influenza virus infections in humans	Wong	2006
PMID 28956760	(2017). Genesis and Spread of Newly Emerged Highly Pathogenic H7N9 Avian Viruses in Mainland China	Yang	2017
PMID 24394699	The PB2 E627K mutation contributes to the high polymerase activity and enhanced replication of H7N9 influenza virus	Zhang	2014
PMID 23868922	(2013). H7N9 influenza viruses are transmissible in ferrets by respiratory droplet	Zhang	2013
PMID 28100622	(2017). Glycosylation of the Hemagglutinin Protein of H5N1 Influenza Virus Increases Its Virulence in Mice by Exacerbating the Host Immune Response	Zhao	2017
PMID 23823727	(2013). Biological features of novel avian influenza A (H7N9) virus	Zhou	2013
PMID 17942562	(2008). A naturally occurring deletion in its NS gene contributes to the attenuation of an H5N1 swine influenza virus in chickens	Zhu	2008