Modelling transmission of Hendra virus from flying foxes to horses

Martín Muñoz de Cote, Gerardo Antonio (2017) Modelling transmission of Hendra virus from flying foxes to horses. PhD thesis, James Cook University.

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Abstract

Diseases that originate in wildlife and spillover to humans and domestic animals are of increasing public health concern. Of the wildlife groups in which emergent diseases originate, bats (Mammalia: Chyroptera) are a common source of some of the most virulent organisms: Ebola and Marburgh viruses, SARS Coronavirus and Nipah and Hendra viruses. Of these, Hendra virus (HeV, Paramyxoviridae: Henipavirus) is the only one that has not caused an epidemic outbreak a.er it spills over to horses and thence to humans. However, its geographic location in Australia represents an unparalleled opportunity to study spillover dynamics of emerging viruses, given the research capacity and human resources immediately available. .e importance of understanding spillover dynamics lies in the potential ability of reducing the risk of epidemics by decreasing the frequency of spillover. Since emergence HeV has spilled over to horses on 55 occasions along a 1500 km coastal stripe in eastern Australia, from northern Queensland to central New South Wales, with mortality rates in infected horses and humans close to 50-75%.

In this study I used a series of modelling techniques to address basic questions of HeV epidemiology and ecology: What are the essential components of the spillover system? How is HeV transmitted from bats to horses? Which reservoir host species are more likely involved in spillover? What are the potential avenues to predict spillover occurrence? How does the spillover host affect spillover risk? How can we mitigate risk of HeV spillover?

To identify the components of the HeV spillover system I participated in a workshop with the National HeV Research Program investigators. We discussed the available evidence and theory regarding spillover and published a conceptual model that is included here as Chapter 2. .e conceptual model consists of an explicit representation of the factors that have to be present for spillover to occur.

Then, to find out how HeV is transmitted, I used unpublished experimental data on HeV survival at different temperatures in the laboratory (Australian Animal Health Laboratory, Paul Selleck), to generate a HeV survival model in the form of an ordinary differential equation. I used the model to test if survival could predict spillover in space (Chapter 3). .e poor predictive capacity of the HeV survival model suggested that transmission to horses could be direct. However, given that I could not completely rule out indirect transmission I quantified HeV decay in the microclimates it experiences once excreted in paddocks. With the simulations and analyses I found that HeV survival is lower on the ground than at ambient air temperatures, and that ground vegetation and tree shade increase survival. In addition, given that desiccation occurs in most circumstances and further decreases survival, HeV can seldom be indirectly transmitted (Chapter 4).

At the time this project began in late 2012 it was not clear which of the four flying fox species were more important for spillover. To identify the most likely reservoir hosts I used the concept of ecological niche to see if spillover occurred where prevailing climatic conditions are preferred by a specific flying fox species. Using these methods I identified P. alecto and P. conspicillatus as the most important reservoir hosts explaining spillover, and therefore most likely to transmit HeV to horses (Chapter 5). Using similar methods I identified climatic correlates of the spatio-temporal pattern of spillover, and produced spillover risk maps in response to climate change. In Chapter 6 I modelled the spatio-temporal risk pattern and found that the most likely climatic factors involved are the seasonal amplitudes of minimum temperature and rainfall. Finally, I modelled HeV risk in response to the climatic suitability for P. alecto and P. conspicillatus (Chapter 7). With these models I found that the horse population at risk will increase by up to 165,000 by 2050, given the number of horses in 2007. In addition I predicted a reservoir host replacement in the northern limits of the HeV spillover distribution.

In my last results Chapter (8) I studied how horses affect spillover risk by modelling the effects of paddock structure on horse behaviour. To do this I deployed GPS trackers in horses and found that when horses are kept in small areas such as paddocks their movements tend to be random. This indicates that beyond the tree coverage of the paddock the effect of its structure on risk of contact with HeV is minimal.

The last Chapter of this thesis is a general discussion and conclusions, in which I present a series of mitigation strategies and recommendations and guidelines for future research. Among research recommendations and guidelines I included a simulation framework that can be extended to improve HeV risk prediction (Chapter 9).

Item ID: 51045
Item Type: Thesis (PhD)
Keywords: climate change, density, flying foxes, Hendra virus, Henipavirus, HeV, horse behaviour, horses, niche centroid, paramyxoviruses, spillover, transmission, veterinary virology, virus diseases
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Plowright, Raina K., Eby, Peggy, Hudson, Peter J., Smith, Ina L., Westcott, David, Bryden, Wayne L., Middleton, Deborah, Reid, Peter A., McFarlane, Rosemary A., Martin, Gerardo, Tabor, Gary M., Skerratt, Lee F., Anderson, Dale L., Crameri, Gary, Quammen, David, Jordan, David, Freeman, Paul, Wang, Lin-Fa, Epstein, Jonathan H., Marsh, Glenn A., Kung, Nina Y., and McCallum, Hamish (2014) Ecological dynamics of emerging bat virus spillover. Proceedings of the Royal Society of London Series B: biological sciences, 282 (1798). pp. 1-9.

Chapter 3: Martin, Gerardo, Plowright, Raina, Chen, Carla, Kault, David, Selleck, Paul, and Skerratt, Lee F. (2015) Hendra virus survival does not explain spillover patterns and implicates relatively direct transmission routes from flying foxes to horses. Journal of General Virology, 96. pp. 1229-1237.

Chapter 5: Martin, Gerardo A., Yanez-Arenas, Carlos, Roberts, Billie J., Chen, Carla, Plowright, Raina K., Webb, Rebecca J., and Skerratt, Lee F. (2016) Climatic suitability influences species specific abundance patterns of Australian flying foxes and risk of Hendra virus spillover. One Health, 2. pp. 115-121.

Date Deposited: 06 Oct 2017 01:52
FoR Codes: 07 AGRICULTURAL AND VETERINARY SCIENCES > 0707 Veterinary Sciences > 070712 Veterinary Virology @ 40%
05 ENVIRONMENTAL SCIENCES > 0501 Ecological Applications > 050101 Ecological Impacts of Climate Change @ 30%
11 MEDICAL AND HEALTH SCIENCES > 1117 Public Health and Health Services > 111799 Public Health and Health Services not elsewhere classified @ 30%
SEO Codes: 92 HEALTH > 9204 Public Health (excl. Specific Population Health) > 920405 Environmental Health @ 50%
96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960804 Farmland, Arable Cropland and Permanent Cropland Flora, Fauna and Biodiversity @ 30%
97 EXPANDING KNOWLEDGE > 970107 Expanding Knowledge in the Agricultural and Veterinary Sciences @ 20%
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