Epidemiology of avian influenza in wild aquatic birds in a biosecurity hotspot, North Queensland, Australia
Introduction
Wild aquatic birds are considered a natural reservoir of avian influenza viruses (AIV) and harbour all known subtypes of the influenza A viruses including the highly pathogenic avian influenza (HPAI) strains (Brown et al., 2007, Munster et al., 2007). Australia has recorded five outbreaks of HPAI caused by H7 subtypes in commercial chickens (Selleck et al., 2003: Westbury, 2003). In at least two of the five Australian HPAI outbreaks, surface drinking water contaminated with Australian nomadic wild aquatic bird faeces was suspected to be the source of the spill-over infection. Therefore, understanding the epidemiology of endemic viruses in reservoir hosts such as the Australian nomadic wild aquatic birds is important in order to better evaluate and mitigate the risk of spill over.
Unlike all other human-inhabited continents, Australia has remained free of HPAI H5N1, but there are increased concerns that the virus could be introduced via migratory birds which travel between Australia and Southeast Asia where HPAI H5N1 is endemic (East et al., 2008). An H5N1 outbreak in wild migratory birds at Lake Qinghai, China in May 2005 (Lei et al., 2007, Wang et al., 2008) posed serious concerns because the lake is a major breeding site for migratory birds whose flyways extend to Southeast Asia, India, Siberia, Australia and New Zealand. Moreover, the HPAI H5N1 strain has been confirmed in Australia's close neighbour Indonesia (Capua and Alexander, 2004) and notably in West Papua on the island of New Guinea (McCallum et al., 2008). Migratory birds could introduce HPAI into Australia via North Queensland, the first point of entry into Australia for many migratory birds. Australia could provide another substantial reservoir for the virus resulting in impacts globally on trade and biosecurity. Therefore, conducting surveillance for these exotic viruses and understanding their risk of introduction into Australia is important. This can be achieved through avian influenza (AI) surveillance in high risk biosecurity areas like North Queensland and the genetic characterisation and subsequent molecular epidemiological understanding of AI subtypes in Australian nomadic wild aquatic birds.
Although cross sectional studies have been conducted on the epidemiology of AI in Australian nomadic wild aquatic birds (Downie et al., 1977, Senne, 2003, Haynes et al., 2009), systematic repeated studies with the aim of estimating seroprevalence and determining risk factors for increased AIV antibody prevalence and hence the risk of spill over have not been done. The determination of the full set of hemagglutinin (H) serotypes and patterns of occurrence over time and their influence on risk of spill over have also rarely been investigated in nomadic wild aquatic birds in Australia. Systematic long-term studies with the aim of estimating AIV ribonucleic acid (RNA) prevalence and the distribution and reassortment (gene evolution) of AIV subtypes, including exotic viruses, in Australian nomadic wild aquatic birds and how these may contribute to biosecurity risks are limited. Therefore, we performed a 3-year repeated cross sectional study in North Queensland from April 2007 up to March 2010 to understand the molecular- and sero-epidemiology of AI in Australian nomadic wild aquatic birds given it is a biosecurity hotspot with perhaps the greatest risk of introduction of HPAI into Australia by migratory birds (Murray et al., 2012). Specific objectives of the study were to estimate the prevalence of AIV RNA and AIV antibodies, establish the distribution of AIV subtypes (based on molecular and serological testing), identify risk factors associated with the prevalence of AIV antibodies and determine the molecular epidemiology of AIVs in nomadic wild aquatic birds in North Queensland. This knowledge will improve our understanding of the biosecurity risks posed by AIV in Australian nomadic wild aquatic birds.
Section snippets
Sites, sample size and sampling
The epidemiological study of AI was performed on nomadic wild aquatic birds in North Queensland. Birds which roosted at different wetlands located within the selected sites were considered as the sampling frame. Birds were sampled from the wetlands of four different sites in North Queensland (Fig. 1) using the most convenient sampling technique. Sites were selected based on their proximity to migratory routes, ease of access, the presence of nomadic wild aquatic birds and generally a large bird
Avian influenza virus RNA and antibody prevalence
A total of 1555 live birds from 19 species were captured from four sites in North Queensland between April 2007 and March 2010. The results of AIV RNA and antibody prevalence are presented in Table 1, Table 2.
Risk factor analysis with cELISA results
No interaction was detected regardless of the classes of data subsets and types of statistical models constructed except linear model B where a significant interaction was detected between year and sex (p = 0.03). Interaction factors were then adjusted in the model. No collinear variables
Ingress of Asiatic forms of H6 and H9 subtypes into Australia
A globally significant finding is our phylogenetic analysis of the H6 and H9 isolates providing further evidence for the transmission of AI viruses from Asia and Europe to Australia.
The phylogenetic analysis suggested that the H6 isolate (2009) was similar to the isolates from Sharp-Tailed Sandpipers (Calidris acuminata) for the M gene (CY025198) and Eurasian ducks for the H gene (GQ414861, HQ244430) and the H9 (2009) was a close relative of Asian duck isolates for both genes (EF597281, AB455035
Ethical approval
Birds were sampled per season (every 4 months) at Billabong Sanctuary and Cromarty, and Atherton Tableland (sporadically). Funnel traps were mostly used to capture birds at the above study sites (Ethics approval no. A1175, JCU, Townsville, QLD and Eco-access permit no. WISp04374507, Queensland Parks and Wildlife Service, Northern Region, Australia). Birds on Cape York were opportunistically captured for sampling using mist nets and a net launcher (licence no. WISP04524607, Queensland Parks and
Acknowledgments
We extend our thanks to scientific and ethics permit authorities for providing the following project approvals, Eco-access permit no. WISp04374507, Queensland Parks and Wildlife Service, Northern Region and ethics permit no. A1175, JCU. Finally, we extend our heartfelt thanks to the other contributors (Stephen Garland who helped in reviewing the script; David Roshier who helped in catching birds and providing samples of wild birds from Cape York. Ravi Dissanayake who helped in producing Fig. 1)
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