VETERINARY RISK ASSESSMENT - WHAT IS THE RISK OF CAUSING BLUETONGUE (BTV8) OUTBREAKS IN SCOTLAND BY ALLOWING MOVEMENTS OF ANIMALS (TO LIVE) FROM BLUETONGUE RESTRICTED ZONES DURING THE "VECTOR-FREE" PERIOD AND THEREAFTER
Hazard identification
1. Bluetongue virus ( BTV) naturally infects domestic and wild ruminants and camelids and is transmitted by several species of Culicoides (biting midges). Bluetongue is primarily a disease of sheep where cattle exist as reservoirs of virus. The basic pathological process is endothelial damage. The disease impacts on animal populations in four ways:
- Direct losses to the sheep farming industry through severe outbreaks - with potentially high levels of sheep mortality.
- Severe illness in infected sheep (and cattle) with significant levels of suffering, compromised animal welfare and production losses.
- Bans on exports of live ruminants and germ plasm can be long term and economically damaging.
- Movement restrictions severely stifle usual economic activity within restricted regions?
2. Outbreaks can be very difficult to control and eradicate because little can be done about the vector. Non-symptomatic cattle and goats can harbour high levels of undetected infection.
Pathogenesis
Sheep
3. Infected sheep have virus replicating in local lymph nodes from days one to three post infection. A true viraemia is usually detectable by day three, with a peak by day six to seven. Circulating systemic antibodies appear one to two weeks after infection, when circulating virus falls in parallel with the appearance of neutralising antibody and interferon. It is rare to be able to detect virus in sheep after day 14. The longest period of viraemia reported for sheep is 54 days, but this is described as exceptional. Clinical signs of disease typically appear within a week of infection; the peak clinical signs, including fever, often coincide with peak viraemia. BTV strains differ in severity and the timing of clinical signs. In sheep that recover, there is a typically long convalescence. Return to clinical normality may take several months, even if animals are seropositive as the viraemia subsides. Although seropositivity may not always be consistent with "clinically recovered", the vast majority of seropositive sheep and cattle from endemic regions are not infected with the virus and seropositivity caused by neutralising antibody can still be detected after three years or more.
Cattle
4. In cattle, most infections are clinically inapparent (although the recent BTV8 outbreak in Europe and on the Continent has caused disease in cattle). Without clinical signs the initial viraemia is harder to detect. The virus becomes closely associated with cattle red blood cells and is quite effective at protecting itself from the bovine immune system. BTV antigen has been detected in cattle (by PCR) at 140 days or so post infection; however, the PCR assay for BTV is considered to be a very conservative way to screen ruminants as "non-contagious", as it is also the case that animals can remain positive by PCR long after all infectious virus is cleared from their blood. The OIE report the "true" viraemia of cattle as less than four weeks, with fewer than one per cent exceeding 8 weeks. Some authorities now consider that the maximum affected duration of viraemia is about 50 days in cattle.
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Culicoides vectors
5. Vector species of Culicoides biting midges tend to breed in damp or wet soil, enriched with fresh or composted dung, and they blood-feed opportunistically on large vertebrate hosts. Culicoides midges tend to be most active from about an hour before sunset until an hour after sunrise. They are most active in the evening, until about midnight, when activity eases off, with another peak of activity around sunrise. However, on dull days or in shady areas vectors may be active during the day. Most Culicoides species are averse to entering confined spaces, such as buildings or vehicles, although recent and ongoing research work suggests that there may be more midge activity indoors in colder seasons than was originally thought to be the case. Female midges take a blood meal prior to egg laying ( Culicoides impunctatus, the Highland midge, being the exception). They feed at roughly four day intervals and live typically for two to three weeks. The eggs hatch in two to three days and depending on the temperature the larval stages lasts 12 to 16 days. The life cycle is egg, four larval instars, pupa and adult. In temperate cool regions midges "over winter" at the fourth level instar stage. Adults emerge two to three days after pupation and take a blood meal roughly one day later. They also mate during this time. Over the year, Culicoides populations in Britain fluctuate but there is generally a peak in May/June and a second peak in September/October. Adult midge populations in Britain tend to fall dramatically from mid to late October and from December adults are usually either not detectable at all, or only in very small numbers, depending on the prevailing temperature. In April to May populations rise again. In cooler conditions their metabolism slows and they survive for periods of more than a month. When infected with BTV midges remain infected for life.
Vector competence
6. Critical in the understanding of the epidemiology of Bluetongue is knowledge of the viral competence of the Culicoides species in different ecosystems. Competent midges may become infected when biting viraemic vertebrates and the probability of infection is dependent on (a) the genotype of the midge, (b) the strain of the virus, (c) the level of viraemia, and (d) other environmental factors, including climate. The extrinsic incubation period ( EIP-the period between feeding on infected blood and the appearance of virus in the saliva of the midge) is one to two weeks. The proportion of adult Culicoides capable of transmitting virus is dependent on (a) the vector competence (the capacity for the virus to develop in, and be transmitted by, the vector - temperature dependent); (b) adult midge survival; (c) the blood feeding interval and (d) the EIP. In order to transmit virus Culicoides midges must not only be viral competent, but also survive long enough to blood feed after the completion of the viral EIP. They are most likely to satisfy these criteria at high temperatures (e.g. 27 to 300C) because, although adult survival is reduced at high temperatures, this is more than compensated for by the accompanying decrease in the duration of the EIP and blood-feeding interval. Consequently, it is likely that warmer temperatures will increase probability that Culicoides will survive long enough to transmit virus.
7. Vector competence studies on British midges ( Culicoides obsoletus) have recorded oral susceptibility rates of less than two percent, in comparison with a known major vector ( Culicoides sonorensis) which has an oral susceptibility incidence of 19.5%. However, it should be noted that Culicoides brevitarsis, the major vector of BTV in Australia, has an experimental competency of only 0.3% when feeding on sheep, although it is an effective vector in the field under warm conditions.
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BTV8 restricted zones - international/domestic situation
8. As of 3 December 2007, there have been 66 confirmed outbreaks of Bluetongue BTV8 since 28 September, in East Anglia and the South East of England, with a further case identified at post import testing in a German cow on a farm near Middlesbrough. Epidemiological reports conclude that the infection was likely to have been initially introduced into Norfolk, Suffolk and Essex on the night of 4/5 August by windborne transmission of infected midges from continental Europe. Disease in those areas has presented with generally low morbidity, low mortality, and low prevalence rates with the majority of infected premises having had only one infected animal.
International situation
9. In the autumn of 2006 Bluetongue was first found in the Netherlands, Belgium, Luxembourg, Western Germany and in parts of North Eastern France. The outbreak was identified as a new incursion in the EU. Bluetongue subsequently overwintered and re-emerged in these countries over the summer of 2007 in a more virulent form, spreading more widely than in the previous season. The existing restricted zones have now been expanded across the whole of Belgium, the Netherlands, Luxembourg, a large proportion of Germany and a large area covering the Northern half of France. First cases have recently been found in Denmark and Switzerland and restriction zones from affected countries now extend into parts of Poland and Sweden.
Mechanisms for BTV8 introduction to Scotland
- Windborne transmission of infected midges over long distances either from restricted zones on the continent or in England.
- Infected midges flying naturally in extended ranges from the restricted zone in England to Scotland.
- Infected midges transported mechanically to Scotland in livestock/other vehicles
- Infection enters Scotland in a legally imported viraemic animal.
- Infection enters Scotland in an illegally imported animal.
Risk analysis
10. This assessment determines the risk of movements of cattle or sheep (to live) from currently restricted zones, to Scotland, during the "vector free period" (as defined in EU Regulation 1266/2007) and thereafter - when midge activity resumes in spring 2008.
11. Commission Regulation 1266/2007 prohibits the movements of animals from restricted zones to the free area, except where the requirements described in Annex 3 are met or if livestock "comply with any other appropriate animal health guarantees based on positive outcomes of a risk assessment of measures against the spread of Bluetongue and approved by the competent authorities".
12. Movements of cattle and sheep (to live) could introduce BTV8 into Scotland by two mechanisms:-
A - Transport of infected competent midges by mechanical means, from the RZ to Scotland in livestock/other vehicles, and their subsequent release into the environment where they bite and infect susceptible Scottish livestock.
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13. The flight range of Culicoides is generally short (one to two kilometres per day range) and the Protection Zone is likely to be large enough to limit the movement of infected vectors by flight. The risk from wind dissemination of infected midges is considered to be negligible from England and very low from continental Europe. However, depending on climatic temperature in a Restricted Zone, infected midges could be transported in livestock vehicles to Scotland and may (a) bite and transmit disease to Scottish ruminants or (b) over winter in Scotland and emerge in spring 2008 to infect Scottish ruminants.
Risk mitigation
14. Moves of unvaccinated cattle and sheep (to live) from Restricted Zones are only currently allowed in the "vector free period". IAH Pirbright will advise when this period starts and ends for the UK, on the basis of midge trapping data that are being compiled from seven traps in the Restricted Zone, 16 traps outside the Restricted Zone in England and 34 traps in Scotland. Within the "vector free period" there will be a "transmission free period" when, even if a few midges are able to fly, all infected midges from 2007 will have died naturally. The risk of mechanical transportation of infected midges to Scotland during the vector free period, with subsequent disease transmission to native livestock, is considered to be generally very low (very rare but cannot be excluded). The same risk during the "transmission-free" period, when all midges that had been exposed to viraemic livestock in the RZ have died a natural death, is considered to be negligible (so rare that it does not merit to be considered). However, midge activity could resume temporarily in transiently warmer conditions. There is also evidence for an effective over wintering mechanism, that allows the virus to survive through the winter in either the midge vector or the mammalian host. Several possible mechanisms for the over wintering phenomenon have been suggested including vertical transmission in a vector, persistent infection of host gamma delta -T cells, midge survival over winter, and the possibility of a carrier status in a bovine/ovine host.
15. At low temperatures the longevity of midges may be increased, although the rate of BTV replication is greatly retarded or even stopped by cold weather. Small numbers of adult Culicoides species were caught throughout the winter of 2006/07 in Belgium within the region of the outbreak, although it was not clear whether these were over wintering or newly emerged adults. Below 150C there is virtually no replication of the virus in a midge, although at low temperatures the virus remains dormant in midges and the midges themselves can potentially re-emerge in spring. There is a further risk mitigation measure required under EU law i.e. action to reduce the risk of mechanical transfer of competent vectors during transportation - insecticide treatment of livestock/vehicles.
16. The last case of confirmed disease in the English RZ was on 3 December. The last case detected in England was on 14 December, on premises near Middlesbrough, in an imported German cow from Lower Saxony, outwith the English RZ.
B - Transport of infected animals into Scotland (where they can be bitten by competent vectors which then become infected and infect non-infected animals)
17. For this to occur, animals on the premises of origin in the restricted zone would have to be infected with Bluetongue but not showing clinical signs, or have gone undetected.
There are four mechanisms by which an infected animal could be transported into Scotland:-
- The susceptible animal is incubating the disease and is not yet showing clinical signs. The incubation period following infection from a biting midge is three to twenty days in sheep and cattle ( OIE reference).
- The susceptible animal is viraemic but not demonstrating clinical signs. Viraemia has been detected in infected sheep for up to 54 days (although it has been recovered from sheep skin for up to 63 days post infection), in goats up to 38 days, and in cattle for up to approximately 100 days (by PCR which may not reflect a true infectious state).
- Clinical signs of disease in susceptible animals are not recognised by the animal keeper. Almost half of the confirmed cases in England have been detected by surveillance testing rather than by report case investigations.
- Clinical signs are recognised but the animals are transported illegally.
18. In the Restricted Zones the absence of infection in animals is determined by two methods:-
- The investigation and negation of report cases. Report cases are dependent on the animal keeper recognising signs of BTV and reporting it to Animal Health.
- The tracing and investigation of movements from premises known to have been infected.
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Risk Mitigation
19. Annex 3 of Regulation 1266/2007 provides further precautions to implement in risk mitigation:
- Treatment of fomites and animals with appropriate insecticides prior to movement.
- Maintenance of animals in vector proof accommodation for an appropriate period prior to transport.
- Testing of animals for Bluetongue virus using appropriate diagnostic tests ( PCR or ELISA).
- Serological testing of animals prior to movement.
- Vaccination of animals prior to movement.
20. The recent incident where an imported German cow was found to be BTVPCR positive, at post-import testing, in the north of England on 14 December, demonstrates our dependence on other member states complying with the detailed requirements of the Regulation. The risk of transporting infected livestock to Scotland from RZs, in the "vector-free period", under current rules with negative pre-movement testing, is considered to be very low (very rare but cannot be excluded).
Conclusion
21. The risk of infected competent midges being mechanically transported to Scotland in livestock vehicles is considered to be very low (very rare but cannot be excluded). The possibility cannot be excluded, during the "vector free period," that an infected midge could be transported to Scotland in a livestock vehicle because:
(a) Midge activity could resume in temporarily warmer periods,
(b) the criteria used by IAH Pirbright to determine the "vector free" and "transmission free" periods are dependent on incomplete midge trapping and climatic data
(c) There is the possibility that some infected midges may survive over winter, either inside buildings, or by some other, as yet uncharacterised mechanism,
(d) There will be some midge activity, even during the "vector-free period" as defined in the Regulation (fewer than 5 parous females caught by trapping weekly)
22. The controls provided for in Annex 3 of Regulation 1266/2007 provide significant risk mitigation, but provide no guarantees (as witnessed with the German cow described above) - given that insecticides, laboratory testing, midge protection and vaccination cannot eliminate risk completely. It is also important to consider recent evidence that a carrier state might exist whereby recovered animals, that are PCR negative at the time of movement, might become PCR positive after moving to Scotland. There are additional uncertainties about unusually long periods of viraemia that may exist in some cattle.
23. Overall, the risk of spreading Bluetongue virus to Scotland by allowing movements of cattle and/or sheep (to live) from Restricted Zones, during the vector-free period, under current rules with negative pre-movement testing, is considered to be very low (very rare but cannot be excluded). Thereafter, from roughly April onwards, the risk will increase markedly in line with midge activity to high (occurs very often), and these movements are then not advisable.
Veterinary Division
Rural Directorate
Scottish Executive
Room 336, Pentland House
47 Robb's Loan, Edinburgh , EH14 1TY
18 December 2007
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