Vector-borne diseases (VBDs) are diseases that are transmitted between animals (including people) by an intermediate host or “vector”, usually invertebrates (such as mosquitoes, midges or, ticks). Climate, landscape and vegetation affect the risk of vector-borne disease introduction and spread. This means the risks posed to Scotland differ from the remainder of the UK, whilst changing as the climate changes. This is important because VBDs have the potential to negatively affect the health of humans and livestock, create economic losses for farmers through trade restrictions, diminished productivity, abortions, malformed births, illness and/or death. EPIC’s scientists are working in collaboration with international experts, using multi-disciplinary approaches to assess the risk of introduction and spread of VBD for Scotland’s livestock and horse populations in order to identify optimal control strategies and inform policy on disease mitigation and management.
‘Vector-borne’ disease (VBD) describes those diseases that utilise an intermediary species (vector) to spread infection in a population. Many important VBDs are carried by arthropods (a group of invertebrates that includes insects and spiders) such as midges, mosquitos and ticks. VBDs have a global impact on human and animal health. Diseases such as Bluetongue Virus (BTV), Schmallenberg Virus (SBV), Fasciolosis (liver fluke), and African Horse Sickness (AHS) present a risk of significant economic impact on livestock, through losses in productivity, trade bans and movement restrictions, whilst diseases such as Lyme Disease or West Nile Virus (WNV) are zoonoses, also posing a threat to human health (see panel right for diseases studied by EPIC scientists).
Understanding and managing VBD presents additional challenges compared to other diseases. Vector reproduction, behaviour and competence (the efficacy of a vector to transmit disease), are strongly influenced by environmental factors such as temperature, humidity, habitat and presence of the host species that the vector feeds on, leading to strong seasonal patterns. Climate change is also changing many of these factors. In Scotland, Culicoides (midge) and Ixodes (tick) vectors are most active between April and October; the rest of the year described as the ‘vector-free period’. This is because sustained low temperatures affect some vectors’ ability to survive and reproduce. Nevertheless, some vectors which carry disease-causing agents (pathogens) can survive in cold temperatures a process known as “over-wintering”. For example midges can survive in livestock winter housing, while others, such as ticks, remain dormant in the soil or leaf litter.
The spread of VBDs is influenced by the ecology and behaviour of the vector, the pathogen and the hosts. For example, the time interval between a midge biting an infected animal and being infectious to another animal ranges from one to three weeks depending on temperature. During this time, midge vectors can move, typically causing local spread of distances up to 10km/week. Furthermore, midges and mosquitoes are able to disperse over large distances blown by the wind. A distance of 700km in a single movement can occur over water.
Global spread of VBD is exacerbated by international trade and travel. Pathogens can be transported via infected animals, wildlife, people or vectors to new geographical areas where vectors may already exist, or become established. BTV-8 emerged in the Netherlands in 2006, and is believed to have originated in sub-Saharan Africa. After a number of years ‘absence’ from North-West Europe, it re-emerged in France in 2015. It is most likely that it remained undetected at a low level in between outbreaks, illustrating the challenges of implementing effective VBD surveillance and the limitations of traditional disease control measures (such as biosecurity measures and movement restrictions) for control of VBD. The importance of these challenges has been underscored again in 2017, when BTV was detected as part of routine post-import testing in a batch of 10 cattle imported into Scotland from the same assembly centre in France. Analysis of weather data from the area of introduction in Scotland demonstrated that there was no risk of onward transmission from these animals.
The following examples illustrate the multidisciplinary approaches used by EPIC scientists to improve VBD preparedness and control strategies for important livestock diseases.
Understanding the risk to Scotland’s livestock and horses posed by the incursion of vector borne disease is part of EPIC’s preparedness remit. EPIC scientists’ work focuses on the particular influences Scotland’s landscape and climate plays in potential disease spread compared to the rest of Great Britain (GB).
EPIC’s scientists work closely with Defra and Scottish Government to produce regular livestock disease horizon scanning reports. Through tracking over 40 diseases across the globe EPIC’s scientists are able to analyse the risk of incursion and impact of the most economically import livestock diseases into Scotland.
EPIC scientists co-authored a qualitative risk assessment on the threat of an incursion of BTV-8 from France in 2016. These documents describe in detail the risks of an incursion and risk of spread within the UK. Both the risk of BTV incursion and the risk of onward spread are strongly seasonal, predominantly due to the effect of temperature on vector reproduction, activity and competence. Only in a hot year the possible incursion of disease could occur as early as May, but more likely June. Movement controls alone in a hotter than average year would not be sufficient to control disease spread. The analysis highlights the importance of timing and location of BTV incursion on disease spread.
Although WNV has never occurred in UK, infected migrating passerine birds can carry WNV over long distances and could present a route of incursion to Scotland. EPIC scientists have studied the migratory patterns of key wild bird species to assess the risk of the introduction of WNV into Scotland from disease ‘hot spots’ in the Camargue region of France. The map below shows the areas that migrating birds most frequently stop, as well as locations of recovered ringed birds (black crosses), key wetland areas - the Camargue, Grande Briere and La Brenne (solid red polygons) and other wetland areas in France (red outlines).
Analyses by EPIC has demonstrated that given the current locations of outbreaks in the south of France, there is a small risk that the disease would be carried to England by migrating birds. If WNV was to expand further into the north of France, the threat to England and to Scotland would increase. This work has contributed to the horizon scanning assessment of the risk of WNV introduction ino Scotland.
In order to assist in monitoring and understanding the global spread of disease, EPIC scientists have curated a database of publicly available genetic sequences of diseases threatening the UK. Whole genome, individual genes or variable genomic regions of a virus can be used to infer a set of phylogenetic trees. Utilizing knowledge of the natural mutation rate of the virus genome for each replication cycle (molecular clock signal) provides a time scale of incursion. These analysis help inform control strategies by identifying routes of infection.
The map below shows transmission routes of BTV determined by analysis of segment 10 of the virus genome. The colour coded transmission routes show related viruses (clades). The long range transmissions highlighted occur due to international trade. Shorter range transmissions occur through local animal movements and vector spread. The mapping of transmission routes highlights the importance of post import testing regimes, such as those which identified BTV in a batch of 10 cattle imported into Scotland from France in 2017.
Spatial-Temporal analysis of BTV related sequences
EPIC scientists (alongside the Scottish Government- funded Strategic Research Programme) are building a picture of VBD such as Lyme disease, Louping Ill Virus, and Fasciolosis (liver fluke) in relation to environmental factors (climate, land use, hosts and landscape).
The farmed landscape has a direct impact on vector abundance. For example tick numbers are influenced by livestock grazing patterns, local climate, and numbers of deer and other tick hosts, as well as habitat. Conservation management schemes can play a role in the risk of Lyme disease and Louping Ill Virus; particularly those impacting numbers of deer which, are the most important hosts to ticks. Through understanding the impact of changes in land management and climate on VBD EPIC scientists are improving assessments of disease risk, predicting future risk, and identifying potential tick and tick-borne disease mitigation strategies.
Liver fluke infection causes serious disease (fasciolosis) in cattle and sheep, resulting in production losses and additional economic consequences due to condemnation of the liver at slaughter. Liver fluke depends on mud snail vectors infecting livestock when ingested through grazing. Utilizing surveillance monitoring of slaughterhouse liver condemnations combined with animal movement and environmental data, researchers identified an increased risk of liver fluke with increased animal age, rainfall, and temperature and for farms located further to the West, in excess of the risk associated with a warmer, wetter climate.
EPIC scientists, in collaboration with the Centre for Ecology and Hydrology, are developing mathematical models to predict the potential number of new cases of BTV generated if an infected vector (i.e. a Culicoides midge) was introduced at different locations in the UK and Europe. The challenge for scientists is that the abundances of BTV-susceptible midge species in Scotland vary widely in different locations, even between farms separated only by a few miles, meaning that transmission is also very variable and difficult to predict. To solve this problem, Culicoides surveillance data are being incorporated into a modelling framework to predict the maximum annual abundance of these vectors. This model takes into consideration the effect of environmental factors such as precipitation, land cover type, host density and amount of vegetation at each surveillance site. The results of this work will improve the accuracy of current models which predict BTV spread. This is important for Scotland, because BTV has continued to spread north through Europe since the 1990s as a result of changes in regional climates.
Analyses by EPIC have demonstrated that under certain circumstances that are unusual but not impossible (temperatures around 1°C warmer than average and a virus strain such as BTV-8 that is well adapted to spread at low temperatures), Scotland may be at risk of a Bluetongue outbreak. A large epidemic could infect up to 300,000 sheep.
The maps of Scotland below show the distribution of cattle (A) and sheep ( B), alongside the potential for BTV spread in an average year (C), compared to ‘worst case scenario’ involving warmer than average temperatures, an incursion in the middle of the vector season and a virus strain that can spread easily (D). The scale (C and D) illustrates the number of days per year when the disease R° is over 1 - a measure of potential spread.
Incursion locations (C & D shown by black points) were chosen to represent the different potential routes of introduction into Scotland:
A represents long range windborne introduction from North West Europe.
B represents short range windborne introduction from the north east of England;
D represents short range windborne introduction or local spread from the north west of England;
L represents an introduction by animal movements to a high risk area;
The maps illustrate the geographical variability in disease spread. Disease spread occurs for a significant proportion of the year in the ‘worst case scenario’ of higher than average temperatures, an incursion in the middle of vector season and a virus strain that can spread easily (map D). Under average conditions (map C) spread is limited to a small number of days per year. Longer term, as climate change is associated with increased extremes in weather conditions it is anticipated these will have considerable implications for VBD given their sensitivity to climactic conditions.
Movement restrictions and enhanced biosecurity are typically deployed as effective responses by farmers and government to non-VBD outbreaks. Although still important these responses are less effective for VBD, since vector movements are not constrained. Whilst a Protection Zone of 3km radius and Surveillance Zone of 10km are typically deployed for non-VBD, control zones for VBD are often much larger. As an example, during the BTV outbreak in 2016-17 in France, very large control zones (150km) were introduced- large enough to potentially include a small number of farms in Sussex and Kent. These restrictions ban movements out of control zones other than to an abattoir.
Vaccination is a potentially effective prevention/ control strategy for a VBD where a licenced vaccine is available. EPIC scientists’ models of BTV virus introduction into Scotland under optimal conditions (1⁰C above average temperature and incursion between mid-May to mid-June) estimate up to 105,000 sheep deaths if vaccination is not used. Optimal vaccine deployment strategies prior to disease introduction could prevent the deaths of most of these sheep through vaccination. However models suggest the most effective strategy involves vaccination not of sheep, but of cattle, with around 500,000 cattle required to be vaccinated to prevent the deaths of 96,000 sheep. The inclusion of host biting preference of the vector within the epidemiological model is a key factor in determining this strategy as the Culicoides vector has a higher biting preference for cattle.
EPIC scientists are developing economic forecasts (ex-ante) to appraise the impact of potential future BTV incursions and disease control options in Scotland. The costs of surveillance (early detection i.e. before it spreads) and pre-emptive vaccination activities are taken into account compared to the potential losses of a disease outbreak. Costs associated with the avoidance of disease include development of effective surveillance mechanisms, prevention (pre-emptive vaccination strategies) and mitigation (post-import testing regimes). The costs resulting from a disease outbreak include loss of productivity (e.g. mortality, weight loss, infertility, veterinary treatment and abortion), export trade bans, domestic consumer demand, and control/ eradication (movement restrictions, vaccination and surveillance).
Paul Bessell conducted the BTV & SBV epidemiological modelling and risk assessment of WNV incursion into Scotland. Paul is a post-doctoral researcher at the Roslin Institute.
Sam Lycett conducted the BTV global transmission route studies using phylodynamic modelling. Sam is a Chancellor’s Fellow at the Roslin Institute.
Lucy Gilbert conducted the predictive mapping of ticks and quantification of environmental risk of liver fluke in cattle. Lucy is a research leader in the Ecological Sciences group at the James Hutton Institute.
Giles Innocent conducted the quantification of environmental risk of liver fluke in cattle. Giles is a senior statistician at Biomathematics and statistics Scotland.
Luiza Toma conducted the economic modelling of BTV incursion and control strategies. Luiza is senior economist in the Land Economy, Environment & Society group at Scotland's Rural College.
Effects of conservation management of landscapes and vertebrate communities on Lyme borreliosis risk in the United Kingdom: Caroline Millins, Lucy Gilbert, Jolyon Medlock, Kayleigh Hansford, Des BA Thompson, Roman Biek Philosophical Transactions of the Royal Society Biological Sciences 2017
Quantifying the roles of host movement and vector dispersal in the transmission of vector-borne diseases of livestock: Tom Sumner, Richard J. Orton, Darren M. Green, Rowland R. Kao, Simon Gubbins PLOS Computational Biology 2017
Assessing the potential for Bluetongue virus 8 to spread and vaccination strategies in Scotland: Bessell PR, Searle KR, Auty HK, Handel IG, Purse BV, Bronsvoort BM Science Reports 2016
Challenges and priorities for modelling livestock health and pathogens in the context of climate change: Seyda Özkan, Andrea Vitali, Nicola Lacetera, Barbara Amon, André Bannink, Dave J. Bartley, et al., Environmental Research2016
Risk assessment for Bluetongue Virus (BTV-8): risk assessment of entry into the United Kingdom. APHA Feb. 2016: Helen Roberts, Ruth Moir , Clemens Matt, Marcus Spray, Lisa Boden and Paul Bessell. APHA Risk Assessment 2016
Using national movement databases to help inform responses to swine disease outbreaks in Scotland: the impact of uncertainty around incursion time: Thibaud Porphyre, Lisa A. Boden, Carla Correia-Gomes, Harriet K. Auty, George J. Gunn & Mark E. J. Woolhouse. Scientific Reports 2016
An ex-ante economic appraisal of Bluetongue virus incursions and control strategies: A. Fofana, L. Toma, D. Moran, G. J. Gunn, S. Gubbins, C. Szmaragd and A. W. Stott Journal of Agriculture 2016
Small-scale pig farmers’ behavior, silent release of African swine fever virus and consequences for disease spread: Solenne Costard, Francisco J. Zagmutt, Thibaud Porphyre & Dirk Udo Pfeiffer. Scientific Reports 2015
Quantifying the Risk of Introduction of West Nile Virus into Great Britain by Migrating Passerine Birds: P.R. Bessell, R.A. Robinson, N. Golding, K.R. Searle, I.G. Handel, L.A. Boden, B.V. Purse and B.M.de C. Bronsvoort. Transboundary and Emerging Diseases 2016
Impact of temperature, feeding preference and vaccination on Schmallenberg virus transmission in Scotland: Paul R. Bessell, Harriet K. Auty, Kate R. Searle, Ian G. Handel, Bethan V. Purse & B. Mark de C. Bronsvoort. Scientific Reports 2014
Supersize me: how whole-genome sequencing and big data are transforming epidemiology: Rowland R. Kao, Daniel T. Haydon, Samantha J. Lycett, Pablo R. Murcia. Trends in Microbiology 2014
Epidemic potential of an emerging vector borne disease in a marginal environment: Schmallenberg in Scotland: Paul R. Bessell, Kate R. Searle, Harriet K. Auty, Ian G. Handel, Bethan V. Purse & B. Mark deC Bronsvoort. Scientific Reports 2013
Combining Slaughterhouse Surveillance Data with Cattle Tracing Scheme and Environmental Data to Quantify Environmental Risk Factors for Liver Fluke in Cattle: Giles T. Innocent, Lucy Gilbert, Edward O. Jones, James E. McLeod, George Gunn, Iain J. McKendrick and Steve D. Albon. Frontiers in Veterinary Science 2017
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