Research and analysis

15 March 2024: updated outbreak assessment for Bluetongue virus in Europe

Updated 25 March 2024

Our last report on 29 November 2023, highlighted for the first time the presence of Bluetongue serotype 3 (BTV-3) in England. At that time, there were a total of 5 cases, all located in Kent, within a 10km Temporary Control Zone (TCZ).

On 4 December the Kent TCZ was extended after the detection of another case. On 8 December, BTV-3 was identified in a second location (Norfolk) and another TCZ was established. On 27 January 2024 the Norfolk TCZ was also extended. The strain of BTV-3 responsible was first reported in the Netherlands in September 2023 and subsequently spread to Belgium, Germany and Great Britain, but the origin is unknown. Genetic sequencing has suggested some differences between BTV-3 in Northern Europe when compared to BTV-3 in Sardinia and Tunisia (Holwerda et al 2023).

On 27 January, in Great Britain the Seasonal Vector Low Period (SVLP) was confirmed, and the start of this period was determined to be 8 January 2024. On 11 February a case of BTV-3 was detected in Suffolk outside of the Norfolk TCZ. On 19 February all temporary control zones were lifted in response to the SVLP. On 21 February, one case of BTV-3 was confirmed in Surrey. Currently, the total number of reported cases of BTV-3 in England is 126 across 73 locations in 4 counties (Kent, Norfolk, Suffolk and Surrey). Of these 126 identified cases, 119 were in cattle and 7 were in sheep. None of these animals were detected through clinical signs and all cases were identified through active surveillance. At this time there is no evidence to suggest that BTV-3 is currently circulating in Culicoides in Great Britain due to the SVLP, but there has been a case of transplacental transmission in cattle.

On the European continent, there has been a decrease in the number of reported outbreaks for BTV-3 since the beginning of winter.  As of 15 March, there have been an additional 266 reported outbreaks since 29 November 2023. This brings the total to 5934 since the disease was first detected in September 2023 (NVWA., 2024).

In Belgium, there have been a further 3 reported outbreaks bringing the total for this country to 7 since 29 September 2023 (Plateforme ESA., 2024).

In Germany, there have been a further 32 reported outbreaks of BTV-3 bringing the total to 47 since the 13 October 2023 (TSIS., 2024).

At the time of writing this report, there have been no reported cases of BTV-3 in France. However, the French authorities have confirmed the presence of two strains of BTV serotype 8 (BTV-8). It is unclear on the extent of the spread of the ‘new strain’ of BTV-8 or the number of outbreaks that have occurred (Plateforme ESA., 2024).

In Italy, there have been 84 more reported outbreaks of BTV located across Sardinia, Sicily and on the mainland (IZS., 2024). These outbreaks were caused by multiple serotypes (3, 4 and 8) of bluetongue virus. The strain of BTV-3 in Italy was first reported in 2017, it is not thought to be the same as the strain which was first reported in the Netherlands. On the other hand, the outbreaks caused by BTV-8 in Italy were recently genetically sequenced and it was confirmed to be the ‘new strain’ which has been spreading across France and Corsica in recent months (Plateforme ESA., 2024).

In December, Spain confirmed that the strain of BTV-4 responsible for outbreaks in Murcia was different to that circulating in the north of Spain. Additionally, BTV-1 was detected on 2 farms in Andalucía which were of North African origin (PAFF Spain 2023).

On 7 February 2024, the Spanish Ministry of Agriculture reported 1 outbreak of BTV-4 in the province of Alicante which was previously free from BTV (Spanish Ministry of Agriculture., 2023)..

Situation assessment

Great Britain

On 4 December 2023, the Temporary Control Zone (TCZ) in Kent was extended after an individual cow was confirmed to be positive for BTV-3 on a holding outside of the original TCZ.

On 8 December 2023, two samples tested positive for BTV-3 on a holding in Norfolk and a 10km TCZ was established to minimize the spread of the disease. These farms were identified as part of the annual Bluetongue survey (designed to identify absence of infection in the area most at risk of airborne movement of infected vectors from the continent).

Subsequently, on the 27 January the Norfolk TCZ was extended after cases of BTV-3 were discovered near Norwich. The seasonal vector low period (SVLP) has now been confirmed, and the start of this period was back dated to 8 January 2024. The SVLP is defined by Culicoides traps on farms, where the number of pigmented Culicoides found each week must be less than 5 in all traps for 2 consecutive weeks (Communication from The Pirbright Institute, 2024). On 11 February a case of BTV-3 was detected in Suffolk outside of the Norfolk TCZ. After the confirmation of SVLP, on Monday 19 February the temporary control zones (TCZs) in Kent, Norfolk and Suffolk were lifted Bluetongue: how to spot and report it - GOV.UK (www.gov.uk). On 21 February, one case of BTV-3 was confirmed in a cow in Surrey.

As of the 15 March 2024, there have been a total of 126 confirmed cases of BTV-3 across 73 locations, all located in England (Kent, Norfolk, Suffolk and Surrey). These cases have been predominately in cattle (119 cases) with a limited number of cases in sheep (7 cases).

No positive cases were detected through the manifestation of clinical signs. Due to the SVLP these infections were likely historical. All recent positive cases across England were detected through active surveillance and in each case, the animal was confirmed BTV-3 positive through RT-PCR and ELISA tests. PCR is able to detect BTV RNA up to RNA up to 6 months post infection and ELISA can detect BTV antibodies for years post infection (Hike et al., 2019, Biteau-Coroller., 2006). There is no evidence to suggest that BTV-3 is currently circulating in Culicoides in Great Britain, due to the SVLP. In one case of BTV-3, a day-old calf was found to be positive after being born from a cow which was positive for BTV-3. This suggests that transplacental transmission had occurred. Transplacental transmission is well documented for BTV-8, but evidence for this in BTV-3 has previously been scarce.

Transplacental transmission could be one potential mechanism of virus surviving through the winter months. Overwintering is a characteristic of Bluetongue virus where the virus is able to resurface after the seasonal low vector period and is currently considered to be quite rare.

Figure 1: Map showing the locations of BTV-3 cases (red dots) in Great Britain, Belgium, Germany and the Netherlands (whole country affected) (Source: Plateforme ESA, accessed on 11 March 2024).

Netherlands

Since our last report, the Netherlands has reported an additional 266 outbreaks of BTV-3 (54 clinically positive and 212 PCR positive) across the country, bringing the total to 5,934 outbreaks as of 4 March 2024.

There has been a continued decline in the number of reported cases throughout winter. This is likely due to low winter temperatures and the low levels of vector activity. However, it could also be a consequence of the large number of premises already affected in the Netherlands and the completion of surveillance sampling. There have been no additional cases confirmed based on clinical signs since 2 January 2024 indicating that new subclinical infections may be occurring at very low levels, or new infections may not be occurring at all.

In December 2023, the NVWA highlighted that a variety of ruminants were found to be infected with BTV-3 which included sheep, goats, cows, alpacas, lamas, mouflon, water buffalo, wisent and yak (PAFF Netherlands 2023).

Belgium

In Belgium, BTV-3 was first identified in the province of Antwerp on a small sheep farm, 6.5km away from the border with the Netherlands on 29 September 2023. The Federal Agency for the Safety of the Food Chain (FASFC) started testing cattle farms for BTV-3 in December 2023 (PAFF Belgium 2023). On 29 January 2024, 2 outbreaks in cattle was reported bringing the total to 7 outbreaks of BTV-3 in Belgium (Plateforme ESA., 2024).

Germany

In Germany, since our last report, there have been an additional 32 outbreaks confirmed through PCR testing. This brings the total to 47 as of 7 February 2024. Of these outbreaks, 43 were detected in cattle, and the remaining 4 were detected in sheep.

France

As of 15 March 2024, there have been no reported cases of BTV-3 in France. However, the French authorities have confirmed the presence of two strains of BTV serotype 8 (BTV-8). BTV-8 has been endemic in France since 2015, but a ‘new strain’ of BTV-8 was first reported in Aveyron in August 2023 (Plateforme ESA., 2023).

Our last update indicated that over 1,350 establishments were affected with BTV-8 in the south of France. The ‘new strain’ of BTV-8 was first identified when severe clinical symptoms uncharacteristic of the enzootic BTV-8 were observed (pyrexia, mouth ulcers and coughing). However, the French authorities did report that existing vaccines against BTV serotype 8 remain effective against this new strain (Plateforme ESA., 2023).

At this time, it is unclear on the extent of the spread of the ‘new strain’ of BTV-8 or the number of outbreaks (Plateforme ESA., 2024).

Italy

In Italy, there have been 84 more reported outbreaks of Bluetongue Virus located across Sardinia, Sicily and on the mainland since our last report.  50 of these outbreaks occurred before January and since then the number of outbreaks reported has decreased. These outbreaks were caused by multiple serotypes (3, 4 and 8) of bluetongue virus. In Sicily there were outbreaks of BTV-4. In Sardinia there were outbreaks of multiple serotypes of BTV (2 outbreaks of BTV-3, 5 outbreaks of BTV-4, 41 outbreaks of BTV-8 and 13 outbreaks which have not been serotyped). In mainland Italy, there have been multiple reported outbreaks of BTV-4 and, for the first time, 1 outbreak of BTV-8 was discovered in December 2023 (IZS., 2024).

Samples from the outbreaks of BTV-8 in both Sardinia and mainland Italy were recently genetically sequenced and were confirmed to be the ‘new strain’ which has spread across France and Corsica in recent months (Plateforme ESA., 2024).

Spain

Our previous report highlighted BTV-4 in the province of Murcia. In December 2023 it was confirmed that the strain of BTV-4 responsible for outbreaks in Murcia was different to the BTV-4 circulating in the north of the country. Genetic sequencing determined the strain to be of North African origin. Moreover, BTV-1 was detected on 2 farms in Andalucía was also determined to be of North African origin (PAFF Spain 2023). BTV-1 and BTV-4 are endemic in both Morocco and Algeria.

The proximity of southern Spain to the north coast of these countries would be consistent with vector blow-over as Culicoides are capable of being carried by wind hundreds of kilometers over water (Mellor et al., 2000). More recently, on 7 February 2024, the Spanish Ministry of Agriculture reported 1 outbreak of BTV-4 (north African origin) in the province of Alicante which was previously free from BTV.

The Spanish authorities have put into place movement restrictions in these areas to limit trade and improve surveillance (Spanish Ministry of Agriculture., 2024).

Implications for Great Britain

The Seasonal Vector Low Period (SVLP) is defined as less than 5 parous female Culicoides, which are capable of transmitting the virus, detected in vector surveillance traps over a period of 3 weeks. In Great Britain, the SVLP was declared to have started on 8 January 2024, following a period of uncharacteristic mild winter weather. At lower temperatures typically observed over winter months, midge activity decreases leading to the SVLP. Furthermore, the drop in temperature over winter months is generally unsuitable for BTV transmission as the virus requires a minimum average temperature of 12°C for virus replication and for the extrinsic incubation period (the time taken for the virus to travel from the midge gut to the mouth parts) of the virus to complete (Carpenter et al., 2011).

Current test results for the recent cases indicate historical infection with negligible risk for onwards transmission. These cases have been detected as part of continual active surveillance, and none of the infected animals were reported to have displayed clinical signs. All of these reported cases were tested using both RT-PCR and ELISA. RT-PCR is highly sensitive and is capable of detecting BTV RNA months after infection when the animal is no longer viraemic. Therefore, it is also important to conduct serological testing (ELISA) to measure BTV specific antibodies. A positive ELISA result shows that there has been an immune response to BTV infection, the combination of these test results enables a rough estimation of time since infection.

There is no evidence to suggest that BTV-3 is circulating in Culicoides in Great Britain at this time, and all recent cases appear to be historical because we are in the SVLP. But there is a possibility of more historical BTV-3 cases being detected though active surveillance. Also, there is a potential risk of BTV-3 overwintering through various mechanisms including, transplacental transmission and through the use of contaminated germplasm. However, there is a paucity of evidence surrounding these mechanisms.

At this time, the risk of incursion of new cases of BTV to Great Britain, has been assessed as LOW – rare but can occur, due to unsuitable environmental conditions, trade control measures on live animals and germplasm, and overwintering mechanisms considered to be rare events. It should be noted that if disease continues to circulate on the continent, the risk of windborne incursion will likely increase once Spring arrives as weather conditions will become more suitable for virus replication and Culicoides activity. This will be monitored via the collaborative reports between APHA, The Pirbright Institute and the Met office regarding windborne incursions of midges from affected areas as mentioned in our previous reports.

Conclusion

There are now a total of 126 reported cases of BTV-3 in England across 73 locations and 4 counties. Due to the seasonal vector low period, all of these cases appear to be historical and there is no evidence that BTV-3 is currently circulating in midges in Great Britain. In response to the SVLP the temporary control zones were lifted.

There is some evidence to suggest that BTV-3 may overwinter due to transplacental transmission or from the use of germplasm. 

The situation in France surrounding the ‘new strain’ of BTV-8 is unclear, making it difficult to assess how far the new strain of BTV-8 has spread in France. This is due to a lack of consolidated data (Plateforme ESA., 2024). However, the French authorities have suggested that the current BTV-8 vaccine in use is effective for this ‘new strain’ (Plateforme ESA., 2023). Since our previous report the ‘new strain’ BTV-8 has been detected in Sardinia and mainland Italy. In Spain, BTV is limited to specific zones which are under restrictions. In these areas surveillance is increased and a ban on movement of unvaccinated livestock is enforced. Currently, there is no evidence to suggest that vaccination would not be effective in the newly identified strains of BTV-1 and BTV-4 of north African origin. In the Netherlands, Germany, and Belgium there has been a decrease in the number of outbreaks reported over winter, but there has been a continued reports of disease in previously unaffected areas. In almost all historical BTV epidemics in Europe, there was a similar trend of continued migration throughout winter, and the rate of spread was estimated to be as low as 10 km per week (40 km per week at the peak) (Nicolas et la., 2018). This continued migration may be the result of delays in outbreak detection, delays in movement restrictions or BTV circulation in low levels of Culicoides populations. Despite this, the unfavorable weather conditions make it unlikely for BTV-3 to spread to Great Britain. As a result, the risk of new incursions of BTV to Great Britain has been assessed as LOW. However, it should also be emphasized that in the coming months, the risk of incursions will likely increase due to warmer conditions and increased Culicoides populations.

It should also be noted that, the number of cases reported in Great Britain is expected to increase as more historical cases are identified as part of active surveillance efforts. Therefore, the overall risk of BTV in Great Britain has remained as MEDIUM at this time. Live ruminants from the Netherlands, Belgium and Germany are currently unable to be sent to GB due to them being unable to meet the certification requirements in the absence of a BTV-3 vaccine. However, geographic jumps of the virus into different countries show that spread can go undetected in a traded population and highlight the importance of continued post import testing.

Livestock owners are strongly advised to source replacement stock responsibly and consult with their private veterinarians to put in place controls preventing the introduction of Bluetongue virus. It is also strongly advisable to request pre-movement testing of animals prior to departure as a further check to ensure that animals are clear of infection before they travel. Currently, susceptible livestock cannot be moved to Great Britain without prior vaccination for countries affected with BTV. As there is no approved vaccine for BTV-3, countries affected with BTV-3 are unable to comply with the health certificate requirements. Assurances should be sought from traders to ensure BTV susceptible animals are fully protected with the appropriate serotype vaccination, where possible, prior to travel (BTV-1, BTV-3, BTV-4, and BTV-8 are circulating in Europe), however there is currently no BTV-3 vaccine.

If you keep livestock, you must continue to keep a close watch for, and report, any suspicion of bluetongue disease in your animals.

Sheep are more likely to show obvious clinical signs of bluetongue than cattle if they become infected. Signs of bluetongue in sheep include ulcers or sores in the mouth and nose. discharge from the eyes or nose, drooling from mouth swelling of the lips, tongue, head and neck and the coronary band, red skin as a result of blood collecting beneath the surface, fever, lameness, breathing problems, abortion, foetal deformities and stillbirths, death.

Lambs can become infected with bluetongue before birth if the dam is infected while pregnant. Signs of infection include born small, weak, deformed or blind, death of lambs within a few days of birth, stillbirths.

Cattle clinical signs include lethargy crusty erosions around the nostrils and muzzle, redness of the mouth, eyes, nose reddening of the skin above the hoof, nasal discharge, reddening and erosions on the teats, fever, milk drop, not eating, abortion, foetal deformities, and stillbirths.  Adult cattle may serve as a source of virus for several weeks while displaying little or no clinical signs of disease and are often the preferred host for insect vectors.

Calves can become infected with bluetongue before birth if the mother is infected while pregnant. Signs of infection include born small, weak, deformed or blind, death of calves within a few days of birth, stillbirths.

For more information and photos of clinical signs of Bluetongue virus visit Bluetongue: how to spot and report it. If livestock keepers or vets, consider bluetongue as a possibility they must report the suspicion to APHA immediately.

We will continue to monitor the current situation.

Authors

• Adem Yusuf
• Dr Lauren Perrin
• Dr Sonny Bacigalupo

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