Epidemiology and management of high pathogenicity avian influenza in South African coastal seabirds, 2018-2022

Abstract

High pathogenicity avian influenza (HPAI) is a viral disease of birds that has caused increasing harm to global poultry production and food security and, more recently, to the conservation of wild bird and marine mammal populations. Avian influenza viruses are also closely monitored because of their inherent human pandemic potential. Since 2016, Clade 2.3.4.4b viruses of the Goose-Guangdong HPAI lineage have spread from Asia to all continents, except Oceania, in an unprecedented manner. Two different clade 2.3.4.4b viruses reached South Africa in 2018 and 2021 respectively and at least thirty thousand South African coastal seabirds died, mostly Endangered Cape Cormorants and African Penguins. This was followed by severe seabird outbreaks elsewhere around the globe and increasing discussion around suitable response measures, which have remained limited.

This dissertation aimed to document lessons learnt during the South African seabird HPAI outbreaks, address epidemiological knowledge gaps and examine options for future outbreak response. It begins with a description of the 2018 and 2021/2022 outbreaks of HPAI in coastal birds and the lessons learnt from the outbreak responses.

To improve understanding of the epidemiology of HPAI in African Penguins, and inform future outbreak response, a cross-sectional survey was conducted across their breeding range in 2021 and 2022. This involved sampling of 530 adult penguins in breeding colonies and 382 penguins of varying ages, admitted to a rehabilitation centre. Possible risk factors, such as colony density, were linked with the detection of virus in penguins admitted for rehabilitation.

Vaccination is a potential option for managing HPAI in seabirds, though fully effective vaccines are not yet available and suitable formulations and vaccination protocols have not been explored. A randomised trial was conducted in captive African Penguins. It compared the magnitude and duration of antibody response to a conventional inactivated clade 2.3.4.4b H5N8 HPAI whole virus vaccine, with the response to a tobacco leaf-produced H5 hemagglutinin based virus-like particle (VLP) vaccine. The VLP vaccine induced significantly higher antibody titres by day 14 and one dose induced similar titres to two doses of the inactivated vaccine. VLP vaccines therefore provide an example of a vaccine technology that may help vaccination to become more feasible for wild birds.

The results of this research were used to compile preparedness plans for disease outbreaks generally, and HPAI specifically in South African coastal birds. Stakeholders were consulted and international workshops attended to identify information required by those involved in responding to an outbreak. It was challenging to obtain input during writing of the plans, but they contain the necessary background information, responsibilities of different stakeholder groups and activities to prepare for outbreaks and they discuss the options for response.

There is currently very little that can be done to stop or slow an HPAI outbreak in wild birds, so preparation for outbreaks, efficient use of resources and consolidation of accumulated knowledge is vital. This dissertation documents lessons learnt from responding to and planning for unprecedented seabird outbreaks in South Africa, which can be built on and refined for other scenarios. The mortality rate, attributed to HPAI, varied across African Penguin colonies, most likely due to high environmental viral load and proximity of breeding birds in some colonies. This information can be used to estimate risk, compile surveillance plans and prioritise potential mitigation measures. Adult African penguins appear more susceptible to the virus than juveniles, which has a relatively more serious population implications, and vaccination is one of the few potential tools to protect these valuable birds. This dissertation illustrates that avian influenza vaccines should be safe and effective in African Penguins and that technology is available that could make vaccination programs feasible, especially if less invasive application methods can be developed.