Analysis of avian influenza A (H3N8) viruses in poultry and their zoonotic potential, China, September 2021 to May 2022.

Pengfei Cui1,2,3 Jianzhong Shi1,2,3,4 Cheng Yan1,3 Congcong Wang1 Yuancheng Zhang1 Yaping Zhang1 Xin Xing1 Yuan Chen1 Jie Zhang1 Liling Liu1 Xianying Zeng1 Guobin Tian1 Chengjun Li1 Yasuo Suzuki5 Guohua Deng1 Hualan Chen1,2
Affiliations 5 institutions
  1. State Key Laboratory for Animal Disease Control and Prevention, Harbin Veterinary Research Institute, CAAS, Harbin, China.
  2. National Poultry Laboratory Animal Resource Center, Harbin Veterinary Research Institute, CAAS, Harbin, China.
  3. These authors contributed equally to this manuscript.
  4. Western Research Institute, CAAS, Changji, China.
  5. Department of Medical Biochemistry, University of Shizuoka School of Pharmaceutical Sciences, Shizuoka, Japan.

Abstract

BackgroundTwo human cases of avian influenza A (H3N8) virus infection were reported in China in 2022.AimTo characterise H3N8 viruses circulating in China in September 2021-May 2022.MethodsWe sampled poultry and poultry-related environments in 25 Chinese provinces. After isolating H3N8 viruses, whole genome sequences were obtained for molecular and phylogenetic analyses. The specificity of H3N8 viruses towards human or avian receptors was assessed in vitro. Their ability to replicate in chicken and mice, and to transmit between guinea pigs was also investigated.ResultsIn total, 98 H3N8 avian influenza virus isolates were retrieved from 38,639 samples; genetic analysis of 31 representative isolates revealed 17 genotypes. Viruses belonging to 10 of these genotypes had six internal genes originating from influenza A (H9N2) viruses. These reassorted viruses could be found in live poultry markets and comprised the strains responsible for the two human infections. A subset of nine H3N8 viruses (including six reassorted) that replicated efficiently in mice bound to both avian-type and human-type receptors in vitro. Three reassorted viruses were shed by chickens for up to 9 days, replicating efficiently in their upper respiratory tract. Five reassorted viruses tested on guinea pigs were transmissible among these by respiratory droplets.ConclusionAvian H3N8 viruses with H9N2 virus internal genes, causing two human infections, occurred in live poultry markets in China. The low pathogenicity of H3N8 viruses in poultry allows their continuous circulation with potential for reassortment. Careful monitoring of spill-over infections in humans is important to strengthen early-warning systems and maintain influenza pandemic preparedness.

Supporting text Virus Host Location
Avian influenza virus 59 Guinea pig 1 H3N8, evolution 1 transmission 55 Influenza A Virus, H3N8 Subtype 13 Influenza A Virus, H9N2 Subtype 71 Influenza in Birds 341 Influenza, Human 286 Poultry Diseases 74 Animals 1948 Chickens 146 China 229 Guinea Pigs 21 Humans 1440 Mice 253 Phylogeny 805 Poultry 112

Evidence records

5 total
Zoonotic Surveillance
1 records · 1 evidence types
Evidence type
1 records
OVE7443
Key finding

Influenza A(H3N8) viruses were successfully isolated from poultry and poultry-related environmental samples collected across 25 provinces in China.

Virus
Host
Location
Not specified
Supporting text

We sampled poultry and poultry-related environments in 25 Chinese provinces. After isolating H3N8 viruses, whole genome sequences were obtained for molecular and phylogenetic analyses. In total, 98 H3N8 avian influenza virus isolates were retrieved from 38,639 samples.

Sample type
surveillance samples | environmental samples
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE7445
Key finding

Avian influenza A (H3N8) viruses found in live poultry markets were responsible for two human infections in China in 2022, indicating an animal-to-human spillover event.

Virus
Host
Location
Supporting text

ConclusionAvian H3N8 viruses with H9N2 virus internal genes, causing two human infections, occurred in live poultry markets in China.

Method
virus isolation | whole genome sequencing | phylogenetic analysis
Study design
epidemiological and genomic investigation of avian influenza viruses in poultry and associated human infections
Transmission direction
animal-to-human
Geographic raw
China
Country inferred
CHN
Experimental Infection
1 records · 1 evidence types
Evidence type
1 records
OVE7448
Key finding

Five reassorted H3N8 viruses infected guinea pigs and were transmissible among them by respiratory droplets, demonstrating susceptibility and replication in guinea pigs.

Virus
Host
Location
Not specified
Supporting text

Five reassorted H3N8 viruses tested on guinea pigs were transmissible among these by respiratory droplets.

Method
experimental infection | respiratory droplet transmission assay
Experimental system
animal infection and respiratory droplet exposure model in guinea pigs
Genomic Evolution
2 records · 2 evidence types
Evidence type
1 records
OVE7444
Key finding

Ten H3N8 influenza A genotypes were reassortants containing six internal genes derived from influenza A (H9N2) viruses.

Virus
Host
Not specified
Location
Not specified
Supporting text

Viruses belonging to 10 of these genotypes had six internal genes originating from influenza A (H9N2) viruses.

Event type
reassortment
Genes or segments
six internal genes
Evidence type
1 records
OVE7449
Key finding

Genetic analysis of avian influenza A (H3N8) viruses sampled across China revealed 17 distinct genotypes, demonstrating high genomic diversity among circulating strains.

Virus
Host
Not specified
Location
Not specified
Supporting text

In total, 98 H3N8 avian influenza virus isolates were retrieved from 38,639 samples; genetic analysis of 31 representative isolates revealed 17 genotypes.

Analysis methods
genetic analysis | phylogenetic analysis