Bluetongue is a haemorrhagic disease of ruminants caused by the bluetongue virus (BTV) and spread by biting midges. It is a notifiable disease and suspicion of disease must be reported to veterinary authorities.
Although bluetongue is mainly a disease of sheep, some strains have been shown to cause clinical disease in cattle. Symptoms include fever, haemorrhage, respiratory distress, lameness, in some instances a cyanotic tongue (from which the disease derives the name bluetongue; Figure 1) and even death. Animals that survive infection may show reduced milk yield, reduced weight gain and wool break.
Bluetongue was considered an exotic disease prior to the massive outbreak during 2006 to 2009, which represented the first incursion of the virus in northern latitudes. The unprecedented spread of BTV serotype 8 (BTV-8) through the naïve ruminant population placed considerable strain on veterinary services and financial losses on farmers within the EU. A widespread vaccination strategy brought the outbreak under control and since 2009, the UK has been BTV-free. Estimates of costs to affected countries during the 2006 outbreak are around £800 million, so it is unsurprising that BTV remains high on the agenda of veterinary authorities throughout Europe.
Challenges to disease control
The enormous diversity of BTV (29 serotypes) means that a vaccine for one serotype will not protect against another. This is a problem since a number of different serotypes are currently circulating in Europe. Inactivated vaccines (containing killed virus) are only readily available for two serotypes (BTV-4 and BTV-8) so considering the current situation, demand is high. The recent emergence of additional BTV serotypes, for which the BTV-4 and BTV-8 vaccine will not offer protection, further complicates the situation.
The nature by which BTV is transmitted poses a major difficulty in the control of disease. The primary vector for spread of BTV is Culicoides biting midges, which breed in semi-aquatic environments with farms providing an excellent breeding ground. The midges are most active during the warmer months, with May to October considered the main vector period and offering the highest chance of transmission and spread of disease. Apart from midges transmitting BTV over great distances, animal trade in the absence of control measures is a significant driver of disease spread.
Over the past two years, The Pirbright Institute, along with colleagues from the APHA and Defra, has detected BTV in a number of imported animals through its testing programmes. In all instances, each importation has occurred in periods of low-vector activity and so no onward transmission occurred. For an outbreak of bluetongue to be confirmed, there must be evidence of virus transmission; thus, no trade implications have been incurred by the UK due to these cases. However, the importation of animals without sufficient proof of successful vaccination poses a major risk, particularly as we are now in the vector-active period.
Monitoring the risk
Vaccination provides the only robust defence against BTV since midges can only be controlled to a very limited extent and animal trade is economically vital. An inactivated BTV-8 vaccine brought the 2006 to 2009 outbreak under control. Rather inexplicably, the same BTV serotype (BTV-8) re-emerged in France in 2015 and has recently spread into parts of Germany and Switzerland. However, the pathogenicity of this BTV-8 has, until recently, caused few clinical cases – unlike the previous BTV-8 strain from 2006. The lack of clinical signs reported has led to a reduced appetite for vaccination and has allowed the virus to spread, albeit slowly, since that time. Experimentally, we have observed a similar pathogenicity to what has been seen in the field.
The reasons behind the re-emergence of the virus in central France are unclear, as are the reasons behind the reduced pathogenicity, both of which warrant further study. However, since December 2018, a number of calves with congenital deformities have been born in France and Germany. These have been attributed to transplacental transmission, which was a unique feature of the 2006 to 2009 BTV-8 outbreak. Over the coming months, we may revisit familiar scenes of BTV-induced congenitally malformed foetuses should this BTV-8 strain continue its spread throughout Europe and possibly to the UK.
The risk of BTV is monitored and involves both passive and active surveillance, in addition to meteorological assessments. From a testing perspective, the situation in Europe is different now to what it was in 2006. Since that time, proficiency tests (where a mix of known-positive and negative samples are tested by different laboratories) have highlighted the most sensitive tests for BTV. The BTV ELISA detects BTV antibodies, which can be detected from five to seven days post-infection and can persist for many years.
For animals imported to the UK from areas within the EU restriction zones, testing blood samples using molecular assays (such as real-time RT-PCR) provides the most appropriate means to detect BTV and gives excellent assurance of the results. The assays used at Pirbright are accredited to the highest standard for testing laboratories (ISO/IEC 17025) by the United Kingdom Accreditation Service. Two different molecular tests (detecting different parts of the BTV genome) are used to negate or confirm infection. It is now possible to detect BTV in blood samples taken one day post-infection and, in some instances, for a number of months post-infection. Serotyping and additional molecular characterisation can also be performed, which is crucial for vaccine selection. Given the high sensitivity of the tests coupled with the prolonged viraemia, this testing regime gives us confidence to detect BTV either in imported animals or in the UK herd should natural infection occur.
The Pirbright Institute hosts the World Organisation for Animal Health (OIE) Reference Laboratory for bluetongue and has the expertise to inform policy teams within Defra. Being part of an international network of testing laboratories gives advanced warning of the situation in the field. Going forward, in spite of the uncertainties surrounding the UK EU exit, there will remain a commitment to advancing understanding of BTV for the protection of animal health. Building on expertise and working closely with international colleagues will underpin the response to the seemingly inevitable incursion of BTV to the UK.