Phylodynamics of high pathogenicity avian influenza virus in Bangladesh identifying domestic ducks as the amplifying host reservoir.

Ariful Islam1,2,3 Michelle Wille4 Mohammed Ziaur Rahman5 Ashleigh F Porter6 Mohammed Enayet Hosaain5 Mohammad Mahmudul Hassan7,8 Tahmina Shirin9 Jonathan H Epstein2 Marcel Klaassen1
Affiliations 9 institutions
  1. Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, Victoria, Australia.
  2. EcoHealth Alliance, New York, NY, USA.
  3. Training Hub Promoting Regional Industry and Innovation in Virology and Epidemiology,Gulbali Institute, Charles Sturt University, Wagga Wagga, NSW, Australia.
  4. Centre for Pathogen Genomics, Department of Microbiology and Immunology, The University of Melbourne, at the Peter Doherty Institute for Infection and Immunity, Melbourne, Australia.
  5. One Health Laboratory, International Centre for Diarrheal Diseases Research, Bangladesh, Bangladesh.
  6. Department of Microbiology and Immunology, The University of Melbourne, at the Peter Doherty Institute for Infection and Immunity, Melbourne, Australia.
  7. Queensland Alliance for One Health Sciences, School of Veterinary Science, University of Queensland, Brisbane, QLD, Australia.
  8. Faculty of Veterinary Medicine, Chattogram Veterinary and Animal Sciences University, Chattogram, Bangladesh.
  9. Institute of Epidemiology, Disease Control and Research (IEDCR), Dhaka Bangladesh.

Abstract

High pathogenicity avian influenza (HPAI) virus H5N1 first emerged in Bangladesh in 2007. Despite the use of vaccines in chickens since 2012 to control HPAI, HPAI H5Nx viruses have continued to infect poultry, and wild birds, resulting in notable mass mortalities in house crows (Corvus splendens). The first HPAI H5Nx viruses in Bangladesh belonged to clade 2.2.2, followed by clade 2.3.4.2 and 2.3.2.1 viruses in 2011. After the implementation of chicken vaccination in 2012, these viruses were mostly replaced by clade 2.3.2.1a viruses and more recently clade 2.3.4.4b and h viruses. In this study, we reconstruct the phylogenetic history of HPAI H5Nx viruses in Bangladesh to evaluate the role of major host species in the maintenance and evolution of HPAI H5Nx virus in Bangladesh and reveal the role of heavily impacted crows in virus epidemiology. Epizootic waves caused by HPAI H5N1 and H5N6 viruses amongst house crows occurred annually in winter. Bayesian phylodynamic analysis of clade 2.3.2.1a revealed frequent bidirectional viral transitions between domestic ducks, chickens, and house crows that was markedly skewed towards ducks; domestic ducks might be the source, or reservoir, of HPAI H5Nx in Bangladesh, as the number of viral transitions from ducks to chickens and house crows was by far more numerous than the other transitions. Our results suggest viral circulation in domestic birds despite vaccination, with crow epizootics acting as a sentinel. The vaccination strategy needs to be updated to use more effective vaccinations, assess vaccine efficacy, and extension of vaccination to domestic ducks, the key reservoir.

Supporting text Virus Host Location
AIV 5 highly pathogenic avian influenza 15 poultry 130 spill-over 5 surveillance 60 wildlife 48 Chickens 146 Disease Reservoirs 149 Ducks 81 Influenza in Birds 341 Phylogeny 805 Animals 1948 Animals, Wild 187 Bangladesh 25 Crows 4 Influenza A virus 186 Influenza A Virus, H5N1 Subtype 300 Poultry Diseases 74

Evidence records

3 total
Zoonotic Surveillance
2 records · 2 evidence types
Evidence type
1 records
OVE8341
Key finding

High pathogenicity avian influenza H5Nx viruses, including H5N1 and H5N6, were detected infecting poultry, wild birds, and causing mass mortality among house crows in Bangladesh.

Virus
Host
Location
Supporting text

High pathogenicity avian influenza (HPAI) virus H5N1 first emerged in Bangladesh in 2007. Despite the use of vaccines in chickens since 2012 to control HPAI, HPAI H5Nx viruses have continued to infect poultry, and wild birds, resulting in notable mass mortalities in house crows (Corvus splendens).

Method
viral detection in birds | surveillance observation of mass mortality
Geographic raw
Bangladesh
Country inferred
BGD
Evidence type
1 records
OVE8344
Key finding

Crow epizootics were interpreted as sentinel events indicating continued circulation of HPAI H5Nx viruses among domestic birds in Bangladesh.

Virus
Host
Location
Supporting text

Our results suggest viral circulation in domestic birds despite vaccination, with crow epizootics acting as a sentinel.

Method
phylodynamic and epidemiological analysis
Geographic raw
Bangladesh
Country inferred
BGD
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE8342
Key finding

Phylogenetic reconstruction showed temporal lineage replacement of HPAI H5Nx clades in Bangladesh, with early clade 2.2.2 and 2.3.4.2 viruses supplanted by clade 2.3.2.1a and later 2.3.4.4b/h viruses after 2012.

Virus
Host
Not specified
Location
Not specified
Supporting text

The first HPAI H5Nx viruses in Bangladesh belonged to clade 2.2.2, followed by clade 2.3.4.2 and 2.3.2.1 viruses in 2011. After the implementation of chicken vaccination in 2012, these viruses were mostly replaced by clade 2.3.2.1a viruses and more recently clade 2.3.4.4b and h viruses.

Analysis methods
phylogenetic reconstruction | phylodynamic analysis