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Evidence Project Final Report

EVID4 Evidence Project Final Report (Rev. 06/11) of 18

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NoteIn line with the Freedom of Information Act 2000, Defra aims to place the results of its completed research projects in the public domain wherever possible. The Evidence Project Final Report is designed to capture the information on the results and outputs of Defra-funded research in a format that is easily publishable through the Defra websiteAn Evidence Project Final Report must be completed for all projects.

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ACCESS TO INFORMATIONThe information collected on this form will be stored electronically and may be sent to any part of Defra, or to individual researchers or organisations outside Defra for the purposes of reviewing the project. Defra may also disclose the information to any outside organisation acting as an agent authorised by Defra to process final research reports on its behalf. Defra intends to publish this form on its website, unless there are strong reasons not to, which fully comply with exemptions under the Environmental Information Regulations or the Freedom of Information Act 2000.Defra may be required to release information, including personal data and commercial information, on request under the Environmental Information Regulations or the Freedom of Information Act 2000. However, Defra will not permit any unwarranted breach of confidentiality or act in contravention of its obligations under the Data Protection Act 1998. Defra or its appointed agents may use the name, address or other details on your form to contact you in connection with occasional customer research aimed at improving the processes through which Defra works with its contractors.

Project identification

1. Defra Project code SE4107

2. Project title

Arthropod-borne viral diseases of livestock: risk to the UK

3. Contractororganisation(s)

Institute for Animal Health

Pirbright Laboratory

Ash Road

Pirbright

Surrey

GU24 0NF

54. Total Defra project costs £ 90,653

(agreed fixed price)

5. Project: start date................ 28/06/2010

end date................. 27/12/2010


6. It is Defra’s intention to publish this form.

Please confirm your agreement to do so...................................................................................YES NO (a) When preparing Evidence Project Final Reports contractors should bear in mind that Defra intends that

they be made public. They should be written in a clear and concise manner and represent a full account of the research project which someone not closely associated with the project can follow.Defra recognises that in a small minority of cases there may be information, such as intellectual property or commercially confidential data, used in or generated by the research project, which should not be disclosed. In these cases, such information should be detailed in a separate annex (not to be published) so that the Evidence Project Final Report can be placed in the public domain. Where it is impossible to complete the Final Report without including references to any sensitive or confidential data, the information should be included and section (b) completed. NB: only in exceptional circumstances will Defra expect contractors to give a "No" answer.In all cases, reasons for withholding information must be fully in line with exemptions under the Environmental Information Regulations or the Freedom of Information Act 2000.

(b) If you have answered NO, please explain why the Final report should not be released into public domain

Executive Summary7. The executive summary must not exceed 2 sides in total of A4 and should be understandable to the

intelligent non-scientist. It should cover the main objectives, methods and findings of the research, together with any other significant events and options for new work.

This project examined the risk to UK livestock and horses from exotic arthropod-borne viruses and the national capability to study those viruses. The potential for virus introduction was explored based on known global distribution and capacity for introduction by various routes. The potential economic impact of a virus outbreak was then calculated from the number of registered livestock and equine hosts within the potential region of transmission, based on the known distribution of confirmed and suspected vector species, and using published estimates of mortality rates and the estimated economic cost of stock We then used a questionnaire to conduct a national inventory of expertise and facilities for researching, identifying and controlling arboviruses and their vectors, and used this and the results of our analyses to identify potentially important gaps in data availability and national capability. These include the scarcity of quantitative data on the risk of introduction by various routes, information on the competence of UK arthropods for the target viruses, and a lack of resources for studying the mechanical transmission of viruses by arthropods. We also proposed actions to improve communication within the UK arbovirus research and outbreak management community, and recommend methodological improvements for future studies in this area.

Our analysis suggests that the exotic arboviruses able to exploit the widest range of introduction routes (WNV, POWV, WEEV, RVFV, EEEV, VEEV, BTV, GETV, AKAV, and CEV) are those which have a broad current geographical distribution and a known or suspected capacity for transmission by multiple types of vector.

The arthropod-borne viruses with the greatest potential impact on the UK horse industry are likely to be African horse sickness virus, the equine encephalomyelitis viruses (Venezuelan, Western and Eastern), West Nile virus, Japanese encephalitis virus and equine infectious anaemia virus.

The arboviral viruses predicted to have the greatest potential impact on the UK cattle industry included Rift Valley fever virus, bluetongue virus, lumpy skin disease virus, epizootic haemorrhagic disease virus and bovine leukaemia virus. Although several severe outbreaks of RVFV have occurred in the last 50 years and some expansion of its range may be underway, it has not been associated with the rapid large-scale expansion seen with viruses such as WNV and BTV, and other as-yet unknown factors may be geographically limiting its expansion. As a result the overall risk to the UK is unlikely to be as high as its potential impact would suggest.

The most important threat to the UK pig industry was African swine fever virus, which is also currently circulating close to the eastern borders of the EU. The primary route of transmission of ASFV in the UK is likely to be direct or via fomites, although the mechanical transmission of the virus by biting flies present in the UK has been demonstrated under laboratory conditions. Other threats included Japanese encephalitis virus, swinepox virus and eastern equine encephalitis virus.

Key threats to the UK small ruminant industries (sheep, goat, deer) are likely to include bluetongue virus, Rift Valley fever virus and sheep pox virus. As discussed above, the slow rate at which RVFV has emerged in the last fifty years compared with that of WNV and BTV suggests that it may not present as


great a threat to the UK as its potential impact might suggest, and that other currently poorly understood factors may be limiting its expansion.

Highlands J virus and Israel-Turkey meningoencephalitis virus may have a minor impact on the UK poultry and game industries, but that overall risk to these industries was low.

Our study suggests that, based on current knowledge, a number of arboviruses (BEFV, DUGV, EEV, ITV, MIDV, MURV, PALV, PHV, POWV, THOV, WESSV, and YUOV) pose no threat to the UK as no known or suspected vectors occur here.

Project Report to Defra8. As a guide this report should be no longer than 20 sides of A4. This report is to provide Defra with details of

the outputs of the research project for internal purposes; to meet the terms of the contract; and to allow Defra to publish details of the outputs to meet Environmental Information Regulation or Freedom of Information obligations. This short report to Defra does not preclude contractors from also seeking to publish a full, formal scientific report/paper in an appropriate scientific or other journal/publication. Indeed, Defra actively encourages such publications as part of the contract terms. The report to Defra should include: the objectives as set out in the contract; the extent to which the objectives set out in the contract have been met; details of methods used and the results obtained, including statistical analysis (if appropriate); a discussion of the results and their reliability; the main implications of the findings; possible future work; and any action resulting from the research (e.g. IP, Knowledge Exchange).

Arthropod-borne viral diseases of livestock: risk to the UK1. Context and ObjectivesDefra’s involvement in outbreaks of infectious livestock diseases is based on four considerations:

(i) to protect human health, in the case of zoonotic infections,(ii) to protect and promote the welfare of animals,(iii) to protect the interests of the wider economy, environment and society, and(iv) to maintain disease-free status to allow international trade.Arthropod-borne viruses (arboviruses) cause some of the most important emerging infectious diseases of humans and animals, and previously unseen arboviral diseases are likely to threaten UK livestock and horses in the future. Perceptions of arboviral disease threat, however, may be biased by recent events and media interest and are not normally based on a systematic review of available data.

Until recently, research into European arthropods as potential vectors of disease has been a relatively low priority, and as a result data gaps exist concerning their distribution, movement and capacity for transmission. The UK’s investment in bluetongue virus research, however, helped to prevent a major outbreak in 2007, saving an estimated £485m and approximately 10,000 jobs and illustrating the potential economic benefits of funding research into exotic arboviral diseases. Research on arboviruses and their vectors requires skills and resources which can take many years to develop and are expensive to maintain, and a high level of preparedness for all viruses that could potentially affect UK livestock and horses is not practical, so objective assessment of the risk to the UK from arboviruses is necessary to support cost-effective policy decisions on research funding and facility development. ‘Data gaps’ which prevent such assessment, and deficits in the facilities and/or expertise required for research and/or outbreak management, must also be identified and potential solutions investigated.

The objectives of this project, which were met in full, were to:

1. Produce a hazard list of exotic arboviruses able to cause significant disease in livestock and/or horses,2. Build an inventory of the UK’s national capacity to work with these viruses,3. Develop proposals for building a UK network of researchers working with livestock arboviruses,4. Indicate the relative risk to UK livestock posed by each virus identified in (1) above,5. Share information on these viruses with Defra for incorporation into the disease profiles database, and6. Make recommendations on strategic areas of research required to support UK risk assessments and/or

outbreak management.

2. Scope of the Project


This project had two overarching aims: to identify exotic arboviral threats to UK livestock and horses, and to document the UK’s capability to address those threats. We reviewed potential routes for each virus to be introduced to the UK based on its known and suspected vectors, published data on the ability of those vectors to be introduced via different routes, and the existence of links between the UK and the current known distribution of the virus. We then reviewed the potential impact of an outbreak of each virus in the UK based on published estimates of mortality in a range of hosts and the implications of an outbreak for human health, animal welfare, wider societal interests and international trade.

Our analysis included horses and livestock species that form a common part of UK agriculture: cattle, sheep, goats, pigs, farmed deer (red, roe and fallow), chickens, turkeys, ducks, geese, pheasant, partridge (red-legged) and grouse. We defined ‘arboviruses’ to include both viruses which replicate within an arthropod vector and those in which mechanical transmission by arthropods is a significant route of transmission. Virus species were defined according to the International Committee on Taxonomy of Viruses (ICTV) database. Abbreviations used within this report for virus species are those suggested by the ICTV. We did not explicitly consider potential future changes to the arthropods present in the UK, although we did consider the sensitivity of our results to our assumptions about the potential transmission range of each virus.

3. Risk AnalysisHazard IdentificationWe define a potential hazard as a virus not currently occurring in the UK, transmitted biologically or mechanically by arthropods and which causes clinical or subclinical disease in at least one of the species included in the study. A range of sources were reviewed to identify viruses meeting these criteria, including the electronic global reporting system ProMed Mail, catalogues of arboviral pathogens, texts on arthropod-borne pathogens, UK government texts, international intergovernmental organisations and European and UK legislation. Experts contacted during the inventory of national arbovirus expertise (see below) were also invited to recommend additional viruses for inclusion in the assessment if supported by published literature. At the same time, for each virus information was gathered on susceptible hosts and hosts exhibiting clinical signs. If a virus was identified as hazardous then information was also gathered on confirmed and suspected vectors.

Risk AssessmentRelease AssessmentSeven general pathways were considered as potential routes of introduction to the UK:

1. the introduction of infected biological vectors,

2. the introduction of infected hosts,

3. the introduction of infected migratory birds,

4. the introduction of infectious products of animal origin (POAO),

5. the introduction of infectious germplasm,

6. the introduction of viruses via human movements, and

7. the introduction of virus via the deliberate importation of wildlife.

Pathway 1 was divided into six sub-pathways, each relating to a potential route of introduction of infected vectors to the UK:

Pathway 1A, the introduction of infected vectors on imported livestock,

Pathway 1B, the introduction of infected vectors on migratory birds,

Pathway 1C, the introduction of infected vectors by movement on the wind,

Pathway 1D, the introduction of infected vectors in air cargo,

Pathway 1E, the introduction of infected vectors in containerised sea cargo,

Pathway 1F, the introduction of infected vectors in refrigerated plant material.

The potential for a virus to be introduced via each of the pathways above was estimated based on:

(i) the existence of the virus in regions linked to the UK by that pathway and

(ii) published evidence of the ability of the virus or vector to be introduced via that pathway.

Information on the distribution of suspected and confirmed outbreaks of the target viruses was obtained via a literature review to identify published outbreak reports. For routes 1A, 1D, 1E, 1F, 2, 4, 5 and 6, whether a region was considered to be ‘linked’ to the UK was determined using a range of sources. Data on countries from which the UK imported livestock and horses, POAO, germplasm and wildlife (routes 1A, 2, 4, 5, 7) in 2008 and 2009,


based on information submitted to the ‘Trade Control and Expert System’ (TRACES), were obtained from Defra. Because movement of horses and of POAO within the EU are not recorded, all EU member states were considered as importing countries. Data on countries from which the UK imported cargo by air or container ship (routes 1D, 1E) in 2008 and 2009 were obtained (from OAG Cargo (UBM Aviation, Dunstable, England) and Sea-web™ (IHS Fairplay, Redhill, England) respectively). Data on countries outside the EU from which the UK imported plant material (route 1F) between October 2009 and September 2010 were obtained from the UK Plant Health and Seeds Inspectorate. Because the movement of live plant material within the EU is not subject to inspection, all EU member states were considered as importing countries. Due to the extensive free global movement of human passengers, for pathway 6 all countries were considered as ‘linked’ to the UK. The number of captive wild animals imported to the UK in any given year is extremely low but the species imported and the countries of origin vary from year to year. It was therefore assumed that all countries were linked. For routes 1B and 3, relating to bird migration, regions were assumed to be ‘linked’ if they were part of the East Atlantic Flyway, by which most migratory birds are introduced into the UK.

The ability of a virus or vector to be introduced by a specific path was estimated by a review of the scientific literature. In the case of vectors, introduction was assumed to be possible if a verified example could be found in the scientific literature of the introduction of a potentially infectious life stage of a vector of the relevant group via the specified pathway.

Exposure AssessmentThe number of hosts potentially exposed to each virus in the event of an introduction was estimated from the distribution of susceptible hosts and the combined range of all known or suspected vector species implicated during the hazard identification step. Hosts within the range of known or suspected vectors of a virus were assumed to be at risk of exposure to that virus in the event of an outbreak.

Host distribution data was obtained by contacting the relevant government departments (Defra and the Northern Ireland Department of Agriculture and Rural Development). Data were obtained at county level where possible, and subdivided by age, sex and production type where possible. In the case of pigs and sheep, the population of Scotland and Wales were allocated to age and sex categories in the same proportions recorded in England, as indicated by the results of the English June Survey of Agriculture and Horticulture. Where data were available, hosts were classified by sex and age.

In the case of viruses which can only be transmitted biologically by arthropods, we inferred vector competence where one or more of the following three criteria was met:

(i) isolation of the disease-producing agent from field-caught specimens,(ii) demonstration of ability to become infected by feeding upon a viraemic vertebrate host,(iii) demonstration of ability to transmit by bite/infection of the salivary glands.

With the exception of BTV in Culicoides spp. and louping ill virus (LIV) in Ixodes ricinus, the competence of UK arthropod populations for arboviruses has not been studied. As a consequence of this data gap, for the purposes of this study we considered UK populations as potential vectors if evidence of competence existed at a population level. However, competence may vary between populations, and studies of the competence of UK populations of suspected vectors, particularly for viruses with a high potential economic impact, are required to confirm this assumption.

Data on the UK distribution of potential vector species was obtained from the Health Protection Agency (HPA) Mosquito Recording Scheme and the National Biodiversity Network (NBN) gateway for mosquitoes (Culicidae), from the National Culicoides Reference Laboratory at the Institute for Animal Health for biting midges (Culicoides), from the HPA Tick Recording Scheme and the NBN gateway for hard and soft tick species (Ixodidae and Argasidae) and from the Natural History Museum and the NBN gateway for blackflies (Simuliidae). No sandfly (Phlebotominae) species occur in the UK.

In the case of viruses known or suspected to be transmissible directly between hosts, all target hosts in the UK were assumed to be at risk. In addition, because some species likely to act as efficient mechanical vectors (e.g. Stomoxys calcitrans) occur throughout the UK, all target hosts in the UK were considered to be ‘at risk’ from viruses known or suspected to be mechanically transmitted by arthropods.

Consequence AssessmentThe consequences of exposure to each virus were considered with reference to the Defra priorities for intervention listed in section 1. Public health considerations were considered qualitatively based on whether a virus was able to cause zoonotic infection.

Animal welfare implications and the impact of an outbreak on the economy, the environment and society were considered based on the number of animals expected to die during a “worst-case” outbreak. Minimum and maximum mortality rates for each hazardous virus species identified were estimated based on a review of the scientific literature. For virus species where mortality has been observed but no quantitative estimates were available in the published literature, a mortality rate of 0.1% was assumed. Estimates of the impact of each virus in the event of introduction were obtained by multiplying together the estimated at-risk population of each host by


the mortality rates in each host type. Monte Carlo simulations were used to represent the effects of variability and uncertainty in mortality rates on our estimates of the economic impact. A uniform PDF was used to describe the distribution of the variability in mortality rates, with the assumption that there was an equal probability of occurrence of all values between the minimum and maximum mortality rates identified. In many cases, uncertainty exists regarding the potential for virus transmission in the UK due to uncertainty in vector distribution, the possibility that other UK species are able to act as vectors, and uncertainty in the potential for these viruses to be transmitted by other routes (such as mechanical transmission). Rather than introduce speculative assumptions about untested virus-vector combinations which would necessarily be biased by the expertise of the authors, we repeated our analysis under a ‘worst case’ assumption that all the hazardous viruses in our study could be transmitted across the UK to investigate the possible importance of this uncertainty.

The impact of an outbreak on international trade was considered based on the restrictions recommended by the Terrestrial Animal Health Code published by the OIE. At the same time, users of this report should be aware that countries are allowed to impose restrictions stricter than these recommendations, although OIE recommends that such restrictions be based on a formal risk assessment. The Sanitary International Standards (SIS) team of the United States’ Animal and Plant Health Inspection Service (APHIS) reported that countries have unilaterally taken trade-restrictive actions against vesicular stomatitis virus (VSV) and bluetongue virus (BTV) following the detection and reporting of these infectious agents in the past, despite provision within the OIE Code for mitigations to minimise the risk associated with trade.

Finally, we estimated the potential impact of each virus across all industries from the perspective of national food security and sustainable food production. Based on the results of the literature review, we assumed that animals dying of disease would not be considered fit for consumption, but that recovering animals would be considered safe to eat, and that the food value of an animal is proportional to the financial cost of replacing a dead animal at market rates. We therefore multiplied the median number of animals dying during an outbreak (as calculated above) by the average cost of replacing an animal in the same sex and age group, as suggested by industry texts. This allowed comparison across livestock species (for obvious reasons, we excluded horses from this part of the assessment). This approach was chosen due to the short duration of this study but oversimplifies several aspects, particularly the cost of clinical signs such as reduced weight gain during disease and the possibility of animal slaughter on welfare grounds, which would increase the amount of material unsuitable for consumption. We therefore recommend the development of more accurate methods to quantify the economic impact of an outbreak if these estimates are considered valuable for policy decisions.

Risk ManagementAvailability of diagnostics and vaccinesThe availability of commercially-available vaccines for the target viruses was researched using scientific literature databases, manufacturer information and internet searches. The availability of diagnostic tests for the target viruses was researched using scientific literature databases (PubMed) and the OIE website.

Inventory of UK national capabilityAn inventory of expertise, services, and facilities available in the UK to research and diagnose the viruses identified during this study was created, based on responses received to an electronic questionnaire. The questionnaire was distributed via email to UK-based organisations with potentially relevant research themes (except for the Institute for Animal Health (IAH) and the Animal Health and Veterinary Laboratories Agency (AHVLA), at which questionnaires were circulated by the authors). Ninety-three universities were contacted based on submissions to the 2008 Research Assessment Exercise in areas of potential relevance, including “Infection and Immunology”, “Epidemiology and Public Health”, “Biological Sciences”, “Agricultural, Veterinary and Food Sciences”, “Earth Systems and Environmental Sciences”, “Statistics and Operational Research” and “Geography and Environmental Sciences”. Universities whose research programs were excluded by these criteria were investigated and were predominantly arts-, media- and business-focused institutions. The questionnaire was also distributed to six university-associated agricultural colleges operating relevant research programs, eight UK-based research institutes funded by Research Councils UK, three Scottish Agricultural and Biological Research Institutes (SABRIs) which receive funding via the Scottish Executive Environment and Rural Affairs Department (SEERAD), and four government-funded agencies with relevant research themes: Biomathematics and Statistics Scotland (BioSS), the AHVLA, the Food and Environment Research Agency (FERA) and the Health Protection Agency (HPA). Three other research organisations (the Natural History museum, Zoological Society of London and the Animal Heath Trust) were also included. The questionnaire was also distributed to six commercial organisations based in the UK with potentially relevant areas of expertise and/or facilities. Contact details for organisations with licences issued under the Specified Animal Pathogens Order were sought from the Pathogens Licensing team at Defra but were stated to be unavailable for commercial sensitivity reasons. It is therefore possible that some commercial organisations with expertise in the relevant areas were not identified.

4. Results


Hazard IdentificationThe literature review identified 71 exotic ICTV-recognised virus species which are known or suspected to be transmitted by arthropods and to be capable of infecting at least one of the species in the study. Four further species were added to this list based on feedback accompanying questionnaire responses.

Thirty-nine of the 71 exotic arboviruses were found to be hazardous, i.e. to cause morbidity or mortality in at least one of the species in the study, based on published scientific literature. The remaining viruses were excluded from further study as they do not cause significant clinical disease in any host species within the scope of this study.

Risk AssessmentReleaseThe results of the literature review of potential introduction routes are shown in Table I. As might be predicted, the viruses which are able to exploit the widest range of introduction routes are those which have a broad current geographical distribution and a known or suspected capacity for transmission by several vector groups.

The flow diagram developed for the release assessment is shown in Appendix A.

Table I: release assessment results. Red: high risk, blue: low risk, blank: negligible risk (see Appendix B).

Pathway 1A 1B 1C 1D 1E 1F 2 3 4 5 6 7Other UK risk assessments

Virus AHSV Defra 2009AKAV -ASFV RVC, 2011*BEFV -BHV-2 -BLV -BTV Defra 2004CEV -DUGV -EEEVEEVEHDVEIAV Defra 2010GETVGTPVHJVITVJEVLSDVMDVMIDVMURVPALVPHVPOWVRRVRVFVSHUVSPPVSWPVTHOVVEEVVSAVVSIVVSNJVWEEVWESSVWNV Defra 2009YUOV

*ASF risk assessment not yet available.


http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/monitoring/documents/qra-wnv-090210.pdf

http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/monitoring/documents/eia-qrau-update100308.pdf

http://webarchive.nationalarchives.gov.uk/20080108002802/http:/defra.gov.uk/animalh/diseases/monitoring/pdf/bt-spainandportugal.pdf

http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/monitoring/documents/ahs_uk081106.pdf

It should be noted that the number of routes via which introduction may be able to occur does not necessarily reflect the frequency with which introduction is likely to occur or the degree to which introductions can be controlled. This is best exemplified by EIAV, for which only one high-risk route of introduction is believed to exist (‘via infected hosts’), but which is introduced into the UK on a regular basis due to the difficulty of detecting infection in hosts, the broad distribution of this virus and the high frequency of international horse movements. Although qualitative risk assessments have been performed by Defra International Animal Health for a number of the viruses included in this study (see Table I), quantitative assessment of the likely frequency of introduction of each of these viruses would require considerable effort and was beyond the scope of the current study. However, in general terms introductions via vectors on the wind (1C) and via infectious migratory birds (3) are both proven and uncontrollable, introduction via livestock imports (2) and via products of animal origin (4) are also proven but their risk may be managed to a greater or lesser degree depending on the virus, and the remaining routes are either not proven, are well controlled, are dependent on very rare events, or some combination of these factors.

ExposureThe hazard identification step indicated that chickens, ducks and grouse were not clinically affected by any of the viruses in the study, and these species were therefore removed from further stages of the analysis. Information on the distribution of the remaining species by geographic region was provided for England, Scotland and Wales by the Veterinary Science Evidence Base (VSEB) at Defra. Livestock and horse distribution data for Northern Ireland (NI) were provided by Northern Ireland Department of Agriculture and Rural Development (DARDNI). In the case of NI, data on geese was not available and other data were only available at a whole-country level. Estimates of the split of ‘other poultry’ data for NI (provided by DARDNI) were used to estimate the number of turkey and partridges in NI.

Pig and sheep sex and age data from the 2008 and 2009 English June Survey of Agriculture and Horticulture were used to estimate the number of pig and sheep in each class for Scotland and Wales. Data on cattle populations in England, Wales and Scotland by geographic region, production type (Dairy/Beef/Other) and age (<6 months old; >6 month old) during 2008 and 2009 were also obtained from the VSEB at Defra. Goat, deer, turkey and partridge populations were not spit into age and sex categories due to insufficient data.

Twenty-three of the 39 hazardous viruses in the study can only be transmitted biologically. For these viruses, the population at risk was calculated from the distribution of known and suspected arthropod vector species. Of the more than 250 vector species linked to these 23 viruses, only seven Culicoides species and 19 mosquito species have been recorded in the UK. Of the 16 virus species remaining in the study for which evidence exists in the scientific literature of other transmission routes, six are believed to be transmissible mechanically (some in addition to biological transmission) and 10 are believed to be transmissible directly (in addition to biological and/or mechanical transmission).

Consequence

Implications for human healthApproximately half of the hazardous livestock arboviruses identified during this study are believed to be zoonotic to some extent. These are marked in Table II. Furthermore, although this project was specifically commissioned to examine the threat to UK livestock posed by exotic arthropod-borne viral diseases, a number of zoonotic viruses exist which are able to infect livestock but which are not associated with significant levels of morbidity or mortality in livestock (and were therefore excluded from this study at the hazard identification stage). In several cases these may have substantial human health impact, such as Crimean-Congo Haemorrhagic Fever virus (CCHFV), which is currently emerging in Turkey, and tick-borne encephalitis virus (TBEV) which is endemic in large parts of Europe and which is closely related to the UK-endemic louping ill virus. Further quantitative prioritisation of the viruses in this study according to their human health impact was beyond the scope of this study but is feasible.

Implications for animal welfareSeveral of the viruses included in this study are associated with high levels of morbidity or mortality. These include ASFV, AHSV, LSDV and capripox (SPPV/GTPV). An outbreak of any of these diseases would have substantially higher implications for animal welfare than the direct mortality projections in the next section might indicate. Further quantitative prioritisation of the viruses in this study according to their animal welfare impact was beyond the scope of this study but is feasible.

Economic, environmental and societal implicationsThis is the broadest of the four criteria for intervention. Due to the short duration of this project, we chose to estimate the number of livestock and horse deaths which might occur during an outbreak affecting all animals potentially exposed to infection.

Our findings suggest that the arthropod-borne viruses with the greatest potential impact on the UK horse industry are likely to be African horse sickness virus, the equine encephalomyelitis viruses (Venezuelan,


Western and Eastern), West Nile virus, Japanese encephalitis virus and equine infectious anaemia virus. Although some references suggested that certain Asian strains of EIAV are associated with mortality of over 90%, this does not reflect the experience of the UK during multiple recent introductions of this virus, so that maximum mortality occurring during an outbreak of EIAV was assumed to be 10%. It should however be noted that novel strains posing higher potential threats are a risk with all of the viruses considered in this study.

The arboviral viruses predicted to have the greatest potential impact on the UK cattle industry included Rift Valley fever virus, bluetongue virus, lumpy skin disease virus, epizootic haemorrhagic disease virus and bovine leukaemia virus. Although several severe outbreaks of RVFV have occurred in the last 50 years and some expansion of its range may be underway (e.g. the first reported outbreak in Yemen in 2000), it has not been associated with the rapid large-scale expansion seen with viruses such as WNV and BTV, and other as-yet unknown factors may be geographically limiting its expansion. As a result the overall risk to the UK is unlikely to be as high as its potential impact would suggest.

The most important threat to the UK pig industry, by a considerable margin, was African swine fever virus. Other threats included Japanese encephalitis virus, swinepox virus and eastern equine encephalitis virus. The primary route of transmission of ASFV in the UK is likely to be direct or via fomites, although the mechanical transmission of the virus by biting flies present in the UK has been demonstrated under laboratory conditions. No effective commercial vaccine against ASFV currently exists, and it is also currently circulating close to the eastern borders of the EU.

Based on our analyses, key threats to the UK small ruminant industries (sheep, goat, deer) are likely to include bluetongue virus, Rift Valley fever virus and sheep pox virus. As discussed above, the slow rate at which RVFV has emerged in the last fifty years compared with that of WNV and BTV suggests that it may not present as great a threat to the UK as its potential impact might suggest, and that other currently poorly understood factors may be limiting its expansion.

Highlands J virus and Israel-Turkey meningoencephalitis virus may have a minor impact on the UK poultry and game industries, but that overall risk to these industries was low.

Our study suggests that, based on current knowledge, a number of arboviruses (BEFV, DUGV, EEV, ITV, MIDV, MURV, PALV, PHV, POWV, THOV, WESSV, and YUOV) pose no threat to the UK as no known or suspected vectors occur here. As described above, uncertainty may exist regarding the potential for transmission of these viruses in the UK, and rather than introduce speculative assumptions which would be biased by the expertise of the authors, we repeated our analysis under the “worst case” assumption that all the hazardous viruses in our study could be transmitted across the whole territory of the UK. Under this “worst case” assumption, EEEV increased in importance, DUGV became a major threat to the small ruminant industries and the threat to the UK from WESSV and BEFV increases but remains low. Nevertheless, the results demonstrate that our assumptions do not alter the relative ranking of most viruses.

More generally, the ability of UK populations to transmit most of the viruses in this study has not been confirmed.

Finally, the methods used in this study may overestimate the cost of outbreaks, as 100% of at-risk hosts are assumed to become infected. At the same time, our method does not address the consequences of morbidity, which will also contribute to the impact of an outbreak. Although it is probably reasonable to assume that the impact of a disease via mortality and the overall impact are approximately in proportion in most cases, the impact of viruses predominantly causing non-lethal conditions may be relatively underestimated. This issue becomes considerably more important when considering non-viral pathogens such as bacteria and parasites, which often cause chronic conditions.

The individual industry figures could be collated into a single measure of impact in several different ways, one of which is demonstrated in the next section. However, the economic, environmental and societal implications of these losses are considerably more complex than a simple comparison of the estimated economic value of each industry might indicate. The use of simplistic methods to reduce these data into a single metric was therefore not felt to be appropriate, and we recommend that the development of more advanced methods to integrate the economic, environmental and societal impact of these viruses is considered.

As described in the methods section, the analysis was repeated under the assumption that all viruses could in fact be transmitted across the whole territory of the UK, to investigate the sensitivity of our estimates to uncertainties in vector competence or the potential of some viruses for direct or mechanical transmission.

Implications for international tradeThe Terrestrial Animal Health Code indicates trade restrictions recommended by the OIE. These are summarised in Table II.

Table II: OIE recommended trade restrictions. IZ = infected zone; Q = quarantine (protection from vectors and/or hosts); C = no clinical signs; D = diagnostic test with -ve result; V = vaccination; Ab = demonstration of naturally-acquired


antibodies; PM = post-mortem inspection with -ve result. Pr = processing to inactivate virus; SF = “seasonally-free” designation possible, with reduced restrictions.

Viru

s Export typeLive animals Germplasm Meat

productsOther Declaring freedom

AHSV Q+D Donor: Q+D - - No cases for 2 years or surveillance for 1 year (less with vector surveillance). SF.

ASFV Q+C Donor: Q+C No trade with IZ. Adjacent zones: D.

Meat products not for human consumption, POAO, bristles, litter, manure: Pr.

Surveillance for 1 year (& 3 years without a case if tick vectors present)

BLV No trade with infected premises.

Oocytes/embryos: No restrictions. Semen: no trade with infected herds.

- - Surveillance for 3 years. UK surveillance already required to confirm freedom.

BTV Q, or (Q+D), or V, or Ab.

Oocytes & bovine embryos produced in vivo: no restrictions (except BTV-8). Semen: Q or D. Other embryos: Q or (Q+D).

No restrictions.

No restrictions on milk/milk products, hides, skins, wool and fibre.

Surveillance for 2 years. SF.

EEEV, WEEV

C; also Q or V if confirmed on premises.

- - -

EIAV C+D. No trade with infected premises.

- - -

GTPV, SPPV

Prohibition permitted. Otherwise, C+Q.

Oocytes/embryos: no restrictions.Semen: C+Q.

- Skins, fur, wool and hair: Pr.

Country: No cases for 3 years (6 months if stamped-out). Zone: 6 months, or 21 days if stamped out.

JEV C+Q or C+V. - - -LSDV Prohibition

permitted. Otherwise, C+Q or C+V.

Oocytes/embryos: C+Q+(V or D).Semen: prohibition permitted, otherwise C+Q.

- POAO: Pr. No cases for 3 years.

RVFV C+(Q or V) C+(V or D). Q+PM. Milk/milk products: Pasteurization or equivalent.No restrictions on hides, skins, wool and fibre.

Infection freedom: surveillance for 4 years; Disease freedom: no cases for six months.

VEEV Prohibition permitted. Otherwise, Q+C+(V or D).

Prohibition permitted.

- - No cases for 2 years.

VSV C+Q. Q+D. - - No cases for 2 years.WNV Horses: no

restrictions. Ducks, geese: Q or D or V. Non-poultry birds: C+Q+D.

Horse/poultry semen: no restrictions.

No restrictions.

No restrictions on eggs or egg products, feathers, down.

No cases for 2 years OR surveillance for 2 years. SF.

Outbreaks of some of the viruses in the study with high potential impact in other areas such as JEV, EEV and WEEV are associated with relatively minor restrictions, while others such as LSDV and VEEV are associated with substantial long-term restrictions. Further quantitative prioritisation of the viruses in this study according to their impact in international trade was beyond the scope of this study but is feasible.


http://www.oie.int/index.php?id=169&L=0&htmfile=chapitre_1.8.16.htm















Implications for food security

0

1000000

2000000

3000000

4000000

5000000

6000000

BTV

RV

FVE

HD

VLS

DV

AS

FVS

PP

VB

LVH

JVJE

VA

KA

VIT

VS

WP

VV

SN

JVV

SIV

VS

AV

BH

VE

EE

VG

TPV

WN

VG

ETV

BE

FVD

UG

VM

IDV

WE

SS

VY

UO

V

Virus

Rel

ativ

e fo

od s

ecur

ity im

pact

Figure 1 - Overall virus impact on livestock, rescaled in beef-calf-equivalent units.

0

1000000

2000000

3000000

4000000

5000000

6000000

BTV

RV

FVE

HD

VLS

DV

AS

FVS

PP

VB

LVH

JVJE

VA

KA

VIT

VS

WP

VV

SN

JVV

SIV

VS

AV

BH

VE

EE

VG

TPV

WN

VG

ETV

BE

FVD

UG

VM

IDV

WE

SS

VY

UO

V

Virus

Rel

ativ

e fo

od s

ecur

ity im

pact

Figure 2 - Overall impact under the assumption that transmission is possible throughout the UK (same order as Fig 1 for ease of comparison).


Risk Management

Availability of diagnostics and vaccinesReal-time RT-PCR, RT-PCR or PCR were available for the majority of the exotic hazardous viruses identified in the study, with the exception of DUGV, GETV, MDV, MIDV, SHUV, SWPV, THOV and YUOV. Due to the nature of the technologies, sequencing and virus isolation were available for all viruses. Commercial vaccine products are currently available for AHSV (horse), AKAV (horse), BTV (cattle, sheep, goat), BEFV (cattle), CEV (cattle), EEEV (horse), EIAV (horse), GETV (horse), LSDV (cattle), RVFV (cattle, sheep), SPPV (sheep), VEEV (horse), WNV (horse) and WEEV (horse). Apart from BTV and WNV, these vaccines are not yet licensed for UK use.

Inventory of UK national capabilityOf the 122 organisations contacted, completed questionnaires were received from 31 groups at 20 organisations. The responses are summarised in Appendix B. No organisations recorded research experience with BEFV, ITV, MURV, SHUV, or THOV, although diagnostic services do exist for BEFV.

5. Recommendations

Epidemiological data gaps

The ability of UK arthropods to transmit livestock viruses

The largest uncertainty encountered during this study is the competence of UK arthropods. As stated already, although competence may vary at a population level, due to a lack of data on UK arthropod populations we had to interpret evidence for competence at the species level. The impact of many of the viruses in this study could be reduced to zero if this assumption is invalid (although not for those where mechanical or direct transmission also occur). The potential for transmission of any of these viruses in the UK cannot be entirely disproved by laboratory studies of competence, but where transmission is likely to depend largely on a single species (for example, the transmission of West Nile virus by Culex pipiens), where competence studies have been conducted elsewhere in the world, and where our studies suggest that the virus is of potentially high impact, we recommend that the competence of UK arthropod populations should be confirmed.

Secondly, improved information on the vectors involved in transmission in the UK would allow better advice on the potential for protecting animals from vector attack or for removal or management of larval breeding habitats. Considering the number of potential virus-vector interactions involved, rapid and high-throughput techniques for identifying vectors or potential vectors of a virus should be investigated. These could include screening viruses using arthropod cell cultures, research into the molecular basis of competence, or studies to identify genetic markers for competence in both viruses and vectors.

A substantial number of the viruses considered in this study are known or suspected to be mechanically transmissible by arthropods. With the exception of EIAV (for which considerable evidence exists), the degree to which mechanical transmission of all of these viruses is possible under UK field conditions remains uncertain. As a result, further studies to clarify the degree to which these viruses are mechanically transmissible and the extent to which this is likely to occur in the field are also recommended.

Finally, the impact of some viruses is highly variable as a consequence of variation in strain pathogenicity. Research that improves our ability to predict the pathogenicity of novel strains, or the factors involved in the evolution of high-pathogenicity strains, would be highly valuable in the long run, although this field is not yet mature enough to promise short-term policy benefits.

Quantitative measures of risk: likelihood of introduction and measurements of impact

We encountered a number of data gaps during the preparation of the introduction and impact assessments above. These include a lack of quantitative data on the introduction of arthropods by different routes, and the collection of such data would facilitate quantitative or semi-quantitative assessments of the likelihood of introduction and thus allow overall risk (combining the likelihood of introduction and the probable consequences) to be compared across pathogens.

Defra has several specific criteria for intervening in outbreaks of animal disease, as discussed in section 1. Although they were beyond the scope of this project, data sources are available that would permit quantitative assessments within each of these areas and we recommend such research to improve the evidence basis for future policy decisions. Two related improvements to future studies in this area would also help to accurately understand the potential impact of an outbreak: (1) probable outbreak duration (including the potential for outbreaks to be controlled) and (2) the inclusion of morbidity, particularly for studies including non-viral pathogens as these are more likely to result in chronic non-lethal conditions. Future work to address this deficiency should


complement existing related Defra disease profiling projects and decision support tools such as D2R2.

Finally, the risk of these diseases from a UK perspective is likely to change in the future in response to their shifting global distribution and changes to the relative sizes of the UK livestock industries. We recommend that efforts are made to anticipate future changes in risk.

Basic entomological data

A substantial body of data exists on the distribution and seasonality of Culicoides on UK farms as a result of Defra-funded research at IAH. The frequency with which mosquito species occur on UK farms, and the times of the year at which adult activity begins and ceases, are less well understood. We recommend that baseline data on seasonal mosquito activity are collected on UK farms to provide insights into the diversity of species present and their seasonal activity. In a related area, we recommend studies to identify the climatic conditions which trigger mosquito and Culicoides emergence and activity, and the survival of adult mosquitoes under conditions typical for autumn and winter in the UK. This data will support the implementation of ‘seasonally vector-free periods’ under OIE recommendations, and will permit existing tools such as transmission models to be extended to mosquito-borne diseases.

National capacity and capability

Virus expertise

No organisations recorded research experience with five hazardous viruses identified in our study: BEFV, ITV, MURV, SHUV, or THOV. Three of these viruses (ITV, MURV, THOV) are zoonotic, but none are predicted to have a high UK veterinary impact even if introduced and even if transmission was possible (four – BEFV, ITV, MURV, THOV – are not expected to be transmissible in the UK), so we do not consider this a serious gap from the veterinary perspective.

Vector expertise

Colonies are crucial for most aspects of research into arthropod vectors, such as competence, incubation and bionomics studies, but require long-term investment and dedicated staff and facilities. The same is true of arthropod cell cultures. These requirements are poorly addressed by the current research funding model used by most funding bodies including Defra, RCUK and the Wellcome Trust, as a result of which a number of resources which were available ten or twenty years ago have now disappeared. The authors recommend that steps are taken to raise the profile of existing funded facilities to allow such facilities to become financially self-supporting to a greater extent.

As discussed in the previous section, there is evidence to suggest that a number of high-impact viruses in this study can be transmitted mechanically by arthropods. However, the responses we received to our questionnaire indicate a shortage of UK facilities or expertise to support the research into mechanical vectors such as large biting flies (Tabanidae, Stomoxys etc).

National diagnostic capability

Finally, no national reference laboratory has currently been designated for some of the arboviruses with high potential impact, such as WNV and RVFV, and some organisations which reported diagnostic expertise did not participate in ring trials or similar QA activities. It is the opinion of the authors that this could increase UK outbreak preparedness.

Other areasNo single UK organisation has the ability to research and manage outbreaks of all arboviral threats to UK livestock and horses. In addition, several respondents to the questionnaire expressed an interest in developing facilities or collaborative projects to research these viruses in the future. As a consequence, improved communication between organisations engaged in research on the viruses identified in this study is recommended to avoid duplication and add value to existing resources.

6. AcknowledgementsThe authors would like to thank the Veterinary Science Evidence Base (VSEB) at Defra for providing information on the distribution of livestock in GB and the importation of livestock, wildlife and POAO, the UK Plant Health and Seeds Inspectorate at FERA for providing information on the importation of plant material, the Northern Ireland Department of Agriculture and Rural Development for providing information on the distribution of livestock in NI, and NFU Mutual for providing data on the average insurance value of UK horses. The authors would also like to thank all organisations who responded to the questionnaire.


Appendix A. Release assessment decision trees


Appendix B. National expertise and facilitiesTable III: national expertise with the hazardous arboviruses identified in the study.

Virus Species

SAPO

Rat

ing

ACDP

Rat

ing

ATC

SA 2

001

Sche

dule

5

Gene

ral E

xper

ienc

e

Areas of Expertise

Viro

logy

Imm

unol

ogy

Epidemiology

Risk

Ass

essm

ents

Vacc

ine

Deve

lopm

ent

Diag

nost

ic S

ervi

ces

Refe

renc

e Co

llect

ions

On-g

oing

UK

sero

surv

eilla

nce

Labo

rato

ry-b

ased

Fiel

dwor

k-ba

sed

Com

pute

r-bas

ed

AHSV 3 2 Y F, H, N, P F, H, N

F F, P F, P F H F F

ASFV 4 - Y F F F F F F F F F AKAV - 3 - F F F F F F F F BTV 3 2 Y F, H, J, N,

P, Q, TF, H, J F F F F, R F, R F, H,

NB, F, O, T

F

BEFV - - - T BHV-2 - - - T T T BLV - - - T T T T T T CEV - 2 - S S S DUGV - 2 - F, L, S F, L, S L S EEEV 3 3 Y E, T E E E E, T EHDV - 2 - F F F F F EEV - 2 - F, T F, T F F F, T EIAV 3 - - T T B, T T GETV - 3 Y T, F T, F F F GTPV 3 - Y F F F F F F HJV - 2 - F, T F F F ITV - 3 - JEV 3 3 Y E, P, Q, T E, P,

Q, TP, Q

P E E, P, T

LSDV 3 - Y F, T F F F F F MDV - - - S S S MIDV - 3 Y F, T F F F MURV - 3 Y T PALV - 2 - F F F PHV - 2 - F F POWV - 3 Y F F T RVFV 3 3 Y E, F, L, R,

S, TE, L, T E R E, R S E E

RRV - 2 - T SPPV 3 - Y F F F F F SHUV - - - SWPV - - - T T T T THOV - 2 - VEEV 3 3 Y E, T E E E E, T VSAV 3 2 Y T F VSIV 3 2 Y T T F T VSNJV 3 2 Y T F T WESSV - 3 - F F F WNV 3 3 - E, F, G,

O, P, R, TE, F, T F E, F,

OE, G R E, G,

R, T E, O,

TE, T T

WEEV 3 3 Y E, T E E E E, T E YUOV - 2 - F F F

Table IV: national expertise and facilities for research into arthropod vector groups


Vector Group

Bas

ic Id

entif

icat

ion

Taxo

nom

y

Imm

unol

ogy

Labo

rato

ry-B

ased

E

pide

mio

logy

Fiel

dwor

k-B

ased

E

pide

mio

logy

Com

pute

r-B

ased

E

pide

mio

logy

Ris

k A

sses

smen

ts

Ong

oing

UK

S

urve

illan

ce

Ong

oing

Oth

er

Sur

veill

ance

Col

onie

s(*

UK

-der

ived

)

Cel

l Lin

es

Oth

er L

abor

ator

y-B

ased

Exp

ertis

e

Biting Midges (Ceratopogonidae)

A, D, F, M, P, Q

A, F F A, F A, D, F, P

D, F, P, R

A, D, F, R

A, D, F, M, O

F F* F F, H

Blackflies (Simuliidae) D D - - - - - - - - - -Mosquitoes (Culicidae) A,

C, D, E, F, G, H, K, M, Q

D, E, F, H, K

L A, E, H, K, P

A, D, E, F, G, H, K

E, P, R

D, E, G, R

E, M E, G, H, K

A, C, H, P

C, F C, H

Sandflies (Phlebotominae)

F F - - F, R R R - - - - -

Ticks, Hard (Ixodidae) D, E, R, T

E D, L E, F, R

D, E, F

E, R E E, R, T

E, R, T

L E, F, L

-

Ticks, Soft (Argasidae) D, E, F, T

E D F F, R F, R F, R - - F E, L -

Large biting flies (Stomoxys, Tabanidae)

- - - - - - - - - - - -

Table V: key to organisations responding to the national capability assessmentLetter Organisation

A Advanced Pest Solutions Ltd.

B BioBest Laboratories Ltd.

C Cardiff University

D Centre for Ecology and Hydrology (NERC)

E Health Protection Agency

F Institute for Animal Health (BBSRC)

G Institute of Zoology (Zoological Society of London)

H London School of Hygiene and Tropical Medicine

I Moredun Research Institute

J MRC - University of Glasgow Centre for Virus Research

K Natural History Museum

L Roslin Institute (BBSRC)

M Rothamsted Research (BBSRC)

N Royal Veterinary College

O Scottish Agricultural College

P University of Liverpool

Q University of Nottingham

R University of Oxford

S University of St Andrews

T Animal Health and Veterinary Laboratories Agency


References to published material9. This section should be used to record links (hypertext links where possible) or references to other

published material generated by, or relating to this project.Oral Presentation:

“Arthropod-Borne Viral Diseases of Livestock: Risk to the UK”, 17th European Society of Vector Ecology

Annual Conference (ESOVE 2010), 14th September 2010, Wroclaw (Poland) [http://www.iah.ac.uk/research/Defra/SE4107/ESOVE_Lara_Harrup_IAH.pdf]

Publications:

Harrup, L.E., Mellor, P.S., Wilson, A.J., Johnson, N. and Fooks, A.R. (2010) “Study of the risk from

arthropod-borne viral diseases of livestock in the UK” [Letter], Veterinary Record, 167 (7), 264, doi:10.1136/vr.c4362 [http://veterinaryrecord.bmj.com/content/167/7/264.full.pdf]

Harrup LE, Johnson N, Fooks AR, Wilson AJ (in prep) “Objective prioritisation of arthropod-borne viral livestock diseases based on potential impact on UK livestock industries”.


http://veterinaryrecord.bmj.com/content/167/7/264.full.pdf

http://www.iah.ac.uk/research/Defra/SE4107/ESOVE_Lara_Harrup_IAH.pdf

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