Epidemiology and evolutionary dynamics of H9N2 avian influenza virus in Bangladesh.

Ariful Islam1,2 Emama Amin3 Md Arif Khan3 Monjurul Islam3 Suman Das Gupta1,4 Josefina Abedin5 Mohammed Ziaur Rahman6 Jade K Forwood1,2,7 Mohammed Enayet Hosaain6 Tahmina Shirin3
Affiliations 7 institutions
  1. Biosecurity Research Program and Training Centre, Gulbali Institute, Charles Sturt University, Wagga Wagga, Australia.
  2. Training Hub Promoting Regional Industry and Innovation in Virology and Epidemiology, Gulbali Institute, Charles Sturt University, Wagga Wagga, Australia.
  3. Institute of Epidemiology, Disease Control and Research (IEDCR), Dhaka Bangladesh.
  4. School of Agricultural, Environmental and Veterinary Sciences, Faculty of Science and Health, Charles Sturt University, Wagga Wagga, Australia.
  5. Queensland Alliance for One Health Sciences, School of Veterinary Science, University of Queensland, Brisbane, Australia.
  6. One Health Laboratory, International Centre for Diarrheal Diseases Research, Bangladesh (icddr,b), Dhaka, Bangladesh.
  7. School of Dentistry and Medical Sciences, Charles Sturt University, Wagga Wagga, Australia.

Abstract

Low pathogenicity avian influenza (LPAI) H9N2 has been enzootic in Bangladeshi poultry since 2006. H9N2 outbreaks can decrease egg production and growth and pose a risk to human health. The role of avian hosts in the persistence, evolution, and dispersion of H9N2 is poorly understood in Bangladesh. Hence, this study unveils the intricate role of major host species in virus maintenance and evolution and the temporal and seasonal patterns of H9N2 in Bangladesh from 2006 to 2023. Multinomial logistic regression analysis indicated that the circulation of H9N2 in different species and interfaces is significantly influenced by the seasons. Bayesian phylogenetic analysis of H9N2 sequences in Bangladesh revealed two distinct lineages: G1 and Eurasian. The G1 lineage split into two clusters, coexisting until 2019, at which point only one cluster persisted. Bayesian phylodynamic analysis of G1 lineage unveiled frequent bidirectional viral transitions among ducks, chickens, and quails. Chickens might be a pivotal source of H9N2 in Bangladesh, with a higher number of viral transitions from chickens to ducks and quails. Quails appear to acquire most of their viral transitions from chickens rather than ducks, suggesting that quail epizootics are primarily triggered by spillover events from chickens. Our results suggest viral circulation in commercial chickens despite vaccination. The vaccination approach should be revised, assess vaccine efficacy, and extension of vaccination to backyard chickens and quails.

Supporting text Virus Host Location
AIV 5 LPAI 2 Phylodynamics 7 poultry 130 surveillance 60 vaccination 14 zoonotic 23 Influenza A Virus, H9N2 Subtype 71 Influenza in Birds 341 Poultry Diseases 74 Animals 1948 Bangladesh 25 Bayes Theorem 32 Chickens 146 Ducks 81 Evolution, Molecular 176 Humans 1440 Phylogeny 805 Quail 7 Seasons 47

Evidence records

6 total
Zoonotic Surveillance
2 records · 2 evidence types
Evidence type
1 records
OVE9078
Key finding

H9N2 avian influenza virus was detected circulating among multiple avian species and poultry interfaces in Bangladesh, with circulation patterns varying by season.

Virus
Host
Location
Supporting text

Multinomial logistic regression analysis indicated that the circulation of H9N2 in different species and interfaces is significantly influenced by the seasons.

Method
multinomial logistic regression analysis | surveillance viral detection
Sample type
surveillance samples
Geographic raw
Bangladesh
Country inferred
BGD
Evidence type
1 records
OVE9073
Key finding

Chickens are identified as the pivotal host maintaining circulation of H9N2 avian influenza virus in Bangladesh.

Virus
Host
Location
Supporting text

Chickens might be a pivotal source of H9N2 in Bangladesh, with a higher number of viral transitions from chickens to ducks and quails.

Method
Bayesian phylodynamic analysis
Geographic raw
Bangladesh
Country inferred
BGD
Transmission Evidence
3 records · 1 evidence types
Evidence type
3 records
OVE9075
Key finding

Phylogenetic evidence supports H9N2 transmission from chickens to ducks and quails, indicating chickens as a major source host in Bangladesh.

Virus
Host
Location
Supporting text

Chickens might be a pivotal source of H9N2 in Bangladesh, with a higher number of viral transitions from chickens to ducks and quails.

Method
Bayesian phylogenetic analysis | phylogenetic transition analysis
Study design
Bayesian phylodynamic analysis
Transmission direction
animal-to-animal
Geographic raw
Bangladesh
OVE9076
Key finding

Quails predominantly acquired H9N2 from chickens rather than ducks, suggesting quail epizootics were driven by spillover from chickens.

Virus
Host
Location
Supporting text

Quails appear to acquire most of their viral transitions from chickens rather than ducks, suggesting that quail epizootics are primarily triggered by spillover events from chickens.

Method
phylogenetic transition analysis
Study design
Bayesian phylogenetic analysis
Transmission direction
animal-to-animal
Geographic raw
Bangladesh
OVE9074
Key finding

Bayesian phylodynamic analysis indicated frequent bidirectional H9N2 transmission among ducks, chickens, and quails in Bangladesh.

Virus
Host
Location
Supporting text

Bayesian phylodynamic analysis of H9N2 G1 lineage unveiled frequent bidirectional viral transitions among ducks, chickens, and quails.

Method
Bayesian phylogenetic analysis | phylodynamic modeling
Study design
Bayesian phylodynamic analysis
Transmission direction
cross-species transmission
Geographic raw
Bangladesh
Country inferred
BGD
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE9077
Key finding

Bayesian phylogenetic analysis showed that H9N2 viruses circulating in Bangladesh formed two distinct lineages, G1 and Eurasian, with the G1 lineage further splitting into two clusters that coexisted until 2019 before one cluster persisted.

Virus
Host
Not specified
Location
Not specified
Supporting text

Bayesian phylogenetic analysis of H9N2 sequences in Bangladesh revealed two distinct lineages: G1 and Eurasian. The G1 lineage split into two clusters, coexisting until 2019, at which point only one cluster persisted.

Analysis methods
Bayesian phylogenetic analysis