Literature detail

H9N2 influenza virus spillover into wild birds from poultry in China bind to human-type receptors and transmit in mammals via respiratory droplets.

Xinghai Zhang^1,2 Yuanguo Li^1,2 Song Jin³ Tiecheng Wang^2,4 Weiyang Sun^2,4 Yiming Zhang³ Fangxu Li³ Menglin Zhao^2,4 Leiyun Sun^2,4 Xinyu Hu^2,4 Na Feng^2,4 Ying Xie⁵ Yongkun Zhao^2,4 Songtao Yang^2,4 Xianzhu Xia^1,2,4,6 Yuwei Gao^2,4,6

Affiliations 6 institutions

Department of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Changchun, China.
Changchun Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Changchun, China.
Ruminant Diseases Research Center, College of Life Sciences, Shandong Normal University, Jinan, China.
Key Laboratory of Jilin Province for Zoonosis Prevention and Control, Military Veterinary Research Institute, Academy of Military Sciences, Changchun, China.
Hebei Key Lab of Laboratory Animal Science, Department of Laboratory Animal Science, Hebei Medical University, Shijiazhuang, China.
Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, China.

PMID 33566453 2022 Transbound Emerg Dis eng ppublish

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Article

Publication summary

H9N2 influenza virus has been reported worldwide for several decades, and it has evolved into multiple genotypes among domestic poultry. However, the study involving ecology and evolution of low pathogenic avian influenza virus H9N2 in wild birds in China is limited. Here, we carried out surveillance of avian influenza virus H9N2 in wild birds along with the East Asian-Australian migratory flyway in China in 2017. To estimate the prevalence of H9N2 avian virus in wild birds, information on exposure of wild bird populations to H9N2 viruses using serology, in addition to virology, would greatly improve monitoring capabilities. In this study, we also present serological data of H9N2 among wild birds in China during 2013-2016. We report the identification of poultry-derived H9N2 isolates from asymptomatic infected multispecies wild birds such as Common kestrel (Falco tinnunculus), Northern goshawk (Accipiter gentilis), Little owl (Athene noctua) and Ring-necked Pheasant (Phasianus colchicus) in North China in June 2017. Phylogenetic analysis demonstrated that Tianjin H9N2 isolates belong to the G81 and carry internal genes highly homologous to human H10N8 and H7N9. The isolates could directly infect mice without adaptation but were restricted to replicate in the respiratory system. Glycan-binding preference analyses suggested that the H9N2 isolates have acquired a binding affinity for the human-like receptor. Notably, results from transmission experiment in guinea pigs and ferrets demonstrated the wild birds-derived H9N2 influenza virus exhibits efficient transmission phenotypes in mammalian models via respiratory droplets. Our results indicate that the H9N2 AIVs continued to circulate extensively in wild bird populations and migratory birds play an important role in the spread and genetic diversification of H9N2 AIVs. The pandemic potential of H9N2 viruses demonstrated by aerosol transmission in mammalian models via respiratory droplets highlights the importance of monitoring influenza viruses in these hosts.

H9N2 influenza virus human-type receptors mammals pathogenesis respiratory droplets transmission wild birds Influenza A Virus, H7N9 Subtype Influenza A Virus, H9N2 Subtype Influenza in Birds Animals Australia Birds China Ferrets Guinea Pigs Humans Mammals

Structured evidence records

Evidence records

9 total

Host Range Experiment 3 records

Host Range Experiment Extraction confidence 0.90

Key finding

Wild bird–derived H9N2 influenza virus isolates infected mice and transmitted among guinea pigs and ferrets via respiratory droplets, demonstrating host susceptibility and airborne transmission in mammalian models.

Virus

Host

Location

Supporting text

The isolates could directly infect mice without adaptation but were restricted to replicate in the respiratory system. Notably, results from transmission experiment in guinea pigs and ferrets demonstrated the wild birds-derived H9N2 influenza virus exhibits efficient transmission phenotypes in mammalian models via respiratory droplets.

Method: experimental infection; replication assay
Sample type: respiratory system
Experimental system: in vivo animal experiment

Host Range Experiment Extraction confidence 0.90

Key finding

Wild bird–derived H9N2 influenza virus transmitted efficiently among guinea pigs and ferrets by respiratory droplets, showing mammalian host range and airborne transmission potential.

Virus

Host

Location

Supporting text

Results from transmission experiment in guinea pigs and ferrets demonstrated the wild birds-derived H9N2 influenza virus exhibits efficient transmission phenotypes in mammalian models via respiratory droplets.

Method: transmission experiment
Experimental system: in vivo animal experiment

Host Range Experiment Extraction confidence 0.90

Key finding

Wild bird–derived H9N2 influenza virus transmitted efficiently among ferrets via respiratory droplets, indicating susceptibility and airborne transmission capacity in a mammalian model.

Virus

Host

Location

Supporting text

Method: transmission experiment
Experimental system: in vivo animal experiment

Cross Species Transmission 1 records

Cross Species Transmission Extraction confidence 0.85

Key finding

H9N2 influenza virus was found to have spilled over from poultry into multiple wild bird species in China, evidencing cross-species transmission among birds.

Virus

Host

Location

Supporting text

We report the identification of poultry-derived H9N2 isolates from asymptomatic infected multispecies wild birds such as Common kestrel (Falco tinnunculus), Northern goshawk (Accipiter gentilis), Little owl (Athene noctua) and Ring-necked Pheasant (Phasianus colchicus) in North China in June 2017.

Method: phylogenetic analysis; serological survey
Study design: field surveillance
Transmission direction: animal-to-animal
Geographic raw: China
Country inferred: China

Genomic Evolution 1 records

Genomic Evolution Extraction confidence 0.90

Key finding

Phylogenetic analysis revealed that Tianjin H9N2 isolates belong to genotype G81 and have internal genes closely related to human H10N8 and H7N9 viruses.

Virus

Host

Location

Supporting text

Phylogenetic analysis demonstrated that Tianjin H9N2 isolates belong to the G81 and carry internal genes highly homologous to human H10N8 and H7N9.

Genes or proteins: internal genes
Analysis methods: phylogenetic analysis

Receptor Usage 1 records

Receptor Usage Extraction confidence 0.95

Key finding

H9N2 influenza virus isolates from wild birds showed binding affinity to human-like receptors, indicating receptor adaptation toward human-type sialic acid linkages.

Virus

Host

Location

Supporting text

Glycan-binding preference analyses suggested that the H9N2 isolates have acquired a binding affinity for the human-like receptor.

Method: glycan-binding preference analysis
Receptors: human-like receptor

Serological Evidence 1 records

Serological Evidence Extraction confidence 0.90

Key finding

Serological data demonstrated exposure of wild birds in China to H9N2 avian influenza virus between 2013 and 2016.

Virus

Host

Location

Supporting text

In this study, we also present serological data of H9N2 among wild birds in China during 2013-2016.

Method: serology
Sample type: serum

Spillover Event 1 records

Spillover Event Extraction confidence 0.95

Key finding

Poultry-derived H9N2 influenza virus was found infecting wild birds in China, demonstrating spillover from poultry to wild birds.

Virus

Host

Location

Supporting text

We report the identification of poultry-derived H9N2 isolates from asymptomatic infected multispecies wild birds such as Common kestrel, Northern goshawk, Little owl and Ring-necked Pheasant in North China in June 2017.

Method: phylogenetic analysis; serology; virology
Study design: field surveillance
Transmission direction: animal-to-human
Geographic raw: North China
Country inferred: China

Zoonotic Surveillance 1 records

Zoonotic Surveillance Extraction confidence 0.95

Key finding

Surveillance identified H9N2 avian influenza virus in multiple asymptomatic wild bird species sampled along the East Asian–Australasian flyway in China.

Virus

Host

Location

Supporting text

Here, we carried out surveillance of avian influenza virus H9N2 in wild birds along with the East Asian-Australian migratory flyway in China in 2017. We report the identification of poultry-derived H9N2 isolates from asymptomatic infected multispecies wild birds such as Common kestrel (Falco tinnunculus), Northern goshawk (Accipiter gentilis), Little owl (Athene noctua) and Ring-necked Pheasant (Phasianus colchicus) in North China in June 2017.

Method: surveillance; serology; virology
Geographic raw: China
Country inferred: China

Citation context

References

39 references

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Evidence overview

Evidence 9

Types 7

Virus 1

Host 4

Evidence types

Host Range Experiment 3 Cross Species Transmission 1 Genomic Evolution 1 Receptor Usage 1 Serological Evidence 1 Spillover Event 1 Zoonotic Surveillance 1

Linked entities

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Publication metadata

Journal: Transboundary and emerging diseases
Volume / Issue / Pages: 69 / 2 / 669-684
ISSN: 1865-1682
Journal country: Germany
DOI: 10.1111/tbed.14033