Understanding the ecology, epidemiology and evolution of the 2017 outbreak of highly-pathogenic H5N8 avian influenza virus in a wild mute swans

Highly pathogenic avian influenza (HPAI) viruses cause substantial economic losses to the poultry industry, and pose a significant threat to animal and human health. HPAI first came to prominence in the late 1990s with the emergence from Asia of the H5N1 lineage, which resulted in the culling of 100s of millions of birds and more than 500 human deaths. HPAI resurfaced as a global threat in 2013, with the emergence in China of a novel strain belonging to subtype H5N8.

The speed of global H5N8 spread since 2014 has surprised scientists. The strain spread rapidly through Asia, North America, Europe, and most recently, Africa. The spread to North America is unprecedented, at an estimated cost of ~$3.3 billion to businesses there. A report published last October concluded that H5N8 global spread was driven primarily by long-distance bird migration.

Reports of H5N8 outbreaks in both wild and farmed birds across Europe increased in autumn 2016, spreading westwards until they reached the UK in late December. Cases in wild birds have been reported in Wales, Scotland and England. The largest outbreak to date is ongoing within a large population (~750) of wild mute swans in Abbotsbury, on the Dorset coast in southern England. Although only 9 swans (so far) have laboratory confirmed H5N8 infections, more than 175 untested swans have died since the start of the outbreak, vastly in excess of normal mortality. The first H5N8 infection was detected in a dead swan found at the Swannery on 23rd December 2016. Although mortality appears to have decreased from the apparent peak in the second week of January 2017, an above-normal number of dead birds are still being recovered and the outbreak is still considered to be current and ongoing by the authorities (2nd February 2017).

This outbreak, whilst devastating for the bird population, could tell us much about how HPAI spreads in wild birds. The long-lived swans have been subjected to long-term ecological study by ornithologists at the University of Oxford and are individually ringed; for most birds we know age, sex, parentage and other variables. Crucially, exactly the same population suffered an outbreak of H5N1 HPAI in early 2008. However, in 2008 only 10 swans died, almost all of which were <3 years old. Our research after the 2008 outbreak showed that older birds were more likely to have antibody responses that might help give immunological protection against avian influenza. Specifically almost all birds >3 years old harbour influenza antibodies and older birds have antibodies to a broader range of different influenza strains. Thus we hypothesise that previous exposure to common, mild forms of influenza may have protected these wild birds against H5N1 infection.

The current outbreak offers the potential to directly compare H5N1 and H5N8 HPAI epidemiology in the same population of wild birds, an opportunity that we think is unique worldwide. High bird mortality during H5N8 outbreaks have been reported elsewhere in Europe, and by comparing the ecology and epidemiology of the H5N8 and H5N1 outbreaks at Abbotsbury we may be able to find out the cause of this.

We aim to find out how, and from where, the H5N8 virus entered the population, how long it was present locally before it was detected, and how the virus spread through the population. To do this we will sequence the genomes of the viruses recovered from affected birds, and analyse these genomes using established statistical methods. We will look at the antibodies that birds in the population carry, to see if some birds, particularly the older ones, are protected against severe disease as a result of previous exposure to harmless strains of avian influenza. This will help us understand if immunity to flu in humans and long-lived birds is similar or different, and extend our understanding of how this virus spreads in wild birds.

This project has particularly direct and well defined impacts for several non-academic institutions and entities.

(1) The proposed research will be of great relevance to those responsible for detecting and controlling avian influenza outbreak in wild birds and farmed poultry, specifically the APHA (Animal & Plant Health Agency). New H5N8 outbreaks are continuing to be detected in England. The UK government will therefore benefit substantially from a detailed understanding of how H5N8 spreads in wild bird populations.The APHA is directly represented here through project partner Prof Ian H Brown, who is Head of Virology at APHA-Weybridge and the Director of the EU/OIE/FAO International Reference Lab for Avian Influenza. Prof Brown sits on numerous national and international committees (listed below); Prof Brown will guide the dissemination of our results to these groups, either by providing evidence directly himself, or by inviting us to submit evidence.
- OFFLU avian influenza expert group
- WHO/OFFLU H5N1 Evolution Working Group
- EU disease emergency task force
- GOARN focal point for APHA, UK, and member institution in the European Virus Archive (EVA) Network
- Centres of Excellence on Influenza Research and Surveillance (CEIRS) (Scientific Committee)
- Global Initiative on Sharing Avian Influenza Data (GISAID) (Scientific Advisory Council)
- UK New and Emerging Respiratory Virus Threats Advisory Group (NERVTAG)
- UK NFU Health Committee
- UK Joint Board for Emerging Infections and Zoonosis
- UK Poultry Health and Welfare Group
- UK Poultry Disease Group
- UK Outbreak Readiness Board

(2) The Abbotsbury Swannery is a tourist destination owned and managed by the Ilchester Estates. Our research could lead to insights that will benefit the health of the birds at Abbotsbury or reduce the likelihood of future HPAI outbreak at the site. Our findings will be communicated directly to the lead swanherd, Dave Wheeler, with whom we are in frequent contact.

(3) The broader relevance of our results for food security can be communicated through the activities of the Oxford Martin Programme on the Future of Food (http://www.futureoffood.ox.ac.uk). Advice on dissemination to the wider food system will be sought from Prof Lord John Krebs, who is Chair of the advisory group of the Future of Food programme.

(4) Understanding the potential for spillover of H5N8 into farmed poultry is also of great scientific and economic interest to the UK poultry industry.