Research and analysis

29 November 2023: updated outbreak assessment for bluetongue virus in Europe

Updated 23 December 2024

Updated outbreak assessment 8.

Disease report

Our last report on 18 October 2023, highlighted for the first time the presence of Bluetongue serotype 3 (BTV-3) in Belgium and Germany, as well as the vast spread of BTV-3 in the Netherlands. It also highlighted the expansion of a new strain of BTV-8 which has been circulating in southern France since August 2023. On 10 November 2023, it was confirmed that 1 cow on a farm in Canterbury located in Kent, England (Figure 1) tested positive for BTV-3 after samples were taken as part of annual Bluetongue surveillance. As of 29 November 2023, there have been 4 further cases of BTV-3 all located within a 10km Temporary Control Zone (TCZ) in Great Britain.

Regarding BTV-3, there have been a further 3,409 outbreaks in the Netherlands, bringing the total to 5,668 outbreaks (1,509 clinically positive and 4,159 PCR positive) reported by the Dutch Ministry of Agriculture, Nature and Food Quality (NVWA) (Figure 2). The clinically positive farms have not had testing performed due to clinical signs being clearly visible. In Germany, there have been 14 more outbreaks of BTV-3 reported by The Animal Disease Information System (TSIS) bringing the total to 15 (Figure 3). In Belgium, there have been 3 additional outbreaks of BTV-3 on sheep farms bringing the total to 4 outbreaks, according to The Federal Agency for Security of Food Chain (AFSCA) (Figure 4).

Additionally, in France the new strain of BTV serotype 8 (BTV-8) has continued to spread northeast as well as southeast to the island of Corsica (Figure 5). There have been a total of 1,350 outbreaks (1,018 in cattle and 332 in sheep) according to Plateforme ESA. Recently, there have also been reports published showing multiple serotypes of BTV are endemic in Sardinia (BTV-3,4,8) and mainland Italy (BTV-1,4). The Italian National Veterinary Epidemiological Bulletin (IZS) has confirmed that since September 2023 there have been 271 outbreaks, half of which occurred in November 2023 and for a number of these outbreaks the serotype has not yet been confirmed (Figure 6).

Finally, the Spanish Ministry of Agriculture has recently reported that BTV-4 has expanded further northeast. As of 20 November 2023, 5 outbreaks have occurred in regions previously unaffected by BTV-4. As a result, Galicia and Madrid regions are now under restrictions and surveillance (Figure 7).

Situation assessment

Great Britain

On 2 November 2023, a cattle holding in Kent was sampled as part of annual end of vector season BTV surveillance (designed to identify absence of infection in the area most at risk of airborne movement of infected vectors from the continent). Out of 15 cattle sampled in a herd of 75, a single homebred adult cow tested non-negative for BTV. On 10 November 2023, further sampling of the whole herd was conducted. The Pirbright Institute conducted both reverse transcription-polymerase chain reaction (RT-PCR) and enzyme-linked immunosorbent assay (ELISA) confirming only the animal which had tested initially non-negative for BTV, was positive for BTV-3. None of the cattle on this holding showed clinical signs of Bluetongue. Following this confirmation, a 10km TCZ was put in place around the farm. No person may move any animal, semen, ovum or embryos on to or off premises in the zone except in accordance with a license issued by a veterinary inspector. Further surveillance and testing for BTV is being conducted within the TCZ.

On 26 November 2023, the Chief Veterinary Officer confirmed 4 additional cases of BTV-3 in individual cattle, on two premises. None of these cases showed clinical signs of Bluetongue. This takes the total to 5 confirmed cases, all in cattle and all located within the 10km TCZ which has not been extended. At the time of writing this report, the source of infection for the BTV3 cases in England is still under investigation.

Figure 1: Map of the TCZ in Canterbury, Kent England where the 5 cases of BTV-3 have been reported by Department for Environment, Food and Rural Affairs (Defra).

Netherlands

Bluetongue was originally confirmed in the municipalities of Wijdemeren and Stichtse Vecht, following reports on clinical suspicion by private veterinarians, and was subsequently confirmed as BTV-3 (House of Representatives of the Netherlands 2023). Since our last update, the Netherlands have reported consistently high reports of disease across the country bringing the total to 5,668 outbreaks as of 22 November (3,409 outbreaks since our last report) (Figure 2). This peaked, between the 6 and 13 of November there were over 1,000 outbreaks reported (including both PCR and clinical) and has since rapidly declined each week with 75 outbreaks reported in the last 7 days (NVWA 2023). This decrease could be due to the recent lower temperatures as winter approaches and Culicoides numbers decrease, or a consequence of the limited number of unaffected premises in the Netherlands. BTV requires a minimum average temperature of 12°C to 15°C for replication and for the extrinsic incubation period (EIP) of the virus to complete (Carpenter et al., 2011). Studies have suggested that the strain of BTV-3 circulating the Netherlands is somewhat similar to the BTV-3 which circulated in Sardinia in 2018, but there are noticeable differences (Holwerda et al 2023). At this time the origin of this strain in the Netherlands is unknown.

Figure 2: Map showing 5,668 outbreaks (4,159 PCR positive in red, 1,509 clinically positive in blue) of BTV-3 in the Netherlands reported by The Dutch Ministry of Agriculture, Nature and Food Quality (NVWA) as of 28 November 2023 (Source: Bluetongue positive by place of residence, NVWA, accessed 29 November 2023).

Germany

On the 13 October 2023, BTV-3 was detected for the first time in Germany in the state of North Rhine-Westphalia which borders the Netherlands. Since then, there have been a further 14 outbreaks in Germany, bringing the total to 15 (Figure 3). These outbreaks show a movement of BTV-3 north towards Denmark. Intra community movement of live ruminants and germinal products remain restricted by the EU.

Figure 3: Map showing a total of 15 outbreaks of BTV-3 in Germany reported by The Animal Disease Information System (TSIS) as of 27 November 2023 (Source: TSIS, accessed on 29 November 2023).

Belgium

The first detection of BTV-3 in Belgium was in the province of Antwerp on a small sheep farm, 6.5km away from the Netherlands border on 29 September 2023. As of 28 November 2023, there have been 4 outbreaks of BTV-3 on sheep farms in Belgium along the border of the Netherlands according to AFSCA (Figure 4).

Figure 4: Map showing a total of 4 outbreaks of BTV-3 in Belgium reported The Federal Agency for Security of Food Chain (AFSCA) as of 28 November 2023 (Source: AFSCA, accessed on 29 November 2023).

France

Since our last update, the newly identified strain of BTV serotype 8 has spread from 600 to over 1,350 establishments. It 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 serotype 8 remain effective against this new strain (ESA 2023). The new strain of BTV-8 has continually spread primarily northeast but also in all other directions. Most notably in Ain which borders Switzerland, Corsica which is close to Sardinia and Pyrénées-Atlantiques which borders Spain and has a high livestock density (Figure 5).

Figure 5: Map showing the departments in France affected by the recently emergent strain of BTV-8, dark orange represents the department in which the new strain of BTV-8 was first reported, the lighter orange shows subsequent detections and the red line represents the 50km coastal area where windborne incursion would be likely (This map was created from data published by Platform ESA, sourced at BHVSI-SA, accessed 29 November 2023).

Italy

Recently, Italy published reports that indicated a significant number of outbreaks from multiple strains of BTV have occurred since September 2023 (IZS 2023). There has been a total of 273 outbreaks since September 2023 with 234 of these occurring in Sardinia compared to 39 outbreaks in mainland Italy. As BTV-1,4,3 and 8 are endemic in Italy, there is no obligation to report these to WOAH. In Sardinia there have been, 2 outbreaks of BTV-3, 83 outbreaks of BTV-4, 45 outbreaks of BTV-8 and a further 104 outbreaks which have not been serotyped. In mainland Italy there have been 38 outbreaks of BTV-4 and 1 outbreak of BTV-1 (IZS 2023) (Figure 6). At this time, the outbreaks of BTV-3 in Sardinia are not thought to be of the same strains as the BTV-3 which was recently detected in the Netherlands (IZS 2023). There have been reports of a new variant of BTV-8 in Sardinia, but it is not known if this is the same as the strain reported recently in France (ProMED 2023).

Figure 6: Map showing a total of 271 outbreaks of BTV in Sardinia (outbreaks include BTV-3,4,8 and untyped in grey) and mainland Italy (outbreaks include BTV-1,4 and untyped in grey) from 1 September 2023 to 22 November 2023 reported by The Italian National Veterinary Epidemiological Bulletin (IZS) (Source: IZS, accessed on 29 November 2023).

Spain

As of the 20 November 2023, the Spanish Ministry of Agriculture reported a total of 5 outbreaks of BTV-4 in new areas that were until recently free from BTV (Figure 7). These outbreaks were seen in Galicia and Madrid regions marking the expansion of BTV-4 to the north and east. Now the Spanish authorities have put into place restrictions in these areas to limit trade and improve surveillance (Spanish Ministry of Agriculture 22 November 2023).

Figure 7: Map showing 5 outbreaks of BTV-4 in Spain (red dots) reported 20 November 2023 by the Spanish Ministry of Agriculture and restriction zones for BTV-4, BTV-1 and unrestricted regions (green) (Source: Spanish Ministry of Agriculture accessed on 29 November 2023).

Conclusion

In Europe, Culicoides populations peak mid to late summer, during early autumn the conditions are optimal for BTV transmission by infected Culicoides (Plateforme 2023) (Wittman et al., 2002). As we approach the end of autumn and temperatures drop, we expect to see a decrease in transmission. Although, as of 24 November 2023 parous female midges (that is, those which are likely to have had a blood meal and are therefore potentially carrying the virus) were still being detected (at low levels) in vector surveillance traps located in Kent, indicating that vector season has not yet come to an end (The Pirbright Institute, personal communication). BTV requires a minimum average temperature of 12°C to 15°C for virus replication, therefore temperatures need to be higher than this for infected Culicoides to become infectious and transmit the virus (Carpenter et al., 2011). Despite this, as vectors themselves can remain active at lower temperatures, any previously infected vectors which had become infectious prior to the drop in temperature could continue to infect livestock throughout their life span (Brand et al., 2017). Typically, Culicoides live 2 to 3 weeks, but some have been documented to survive for longer (3.5 months) in favorable conditions (Mellor et al. 2000). Additionally, the incubation period in sheep is usually 4 to 8 days but, in some cases it can be as many as 20 days (Irish department of Agriculture, Food and the Marine 2023). For these reasons we may see a delay before the number of outbreaks in Europe decreases. Even if virus transmission is expected to have reduced in recent weeks, further cases could still be detected due to variability in the expression of clinical signs, especially in the presence of active surveillance efforts.

The presence of 5 cases of BTV-3 in Kent highlights the large geographic jumps that can be made by the virus. At this time, it is not known how BTV-3 was able to enter Great Britain but an investigation is ongoing. At this time there is no evidence that BTV-3 is circulating in Culicoides populations in Great Britain.

The whole territory of mainland France is a BTV-4 and BTV-8 restriction zone. This means that susceptible livestock cannot be moved to Great Britain without prior vaccination for the circulating BTV-4 and BTV-8 serotypes. The situation in France with the new strain of BTV-8 appears to be more clinically severe, however, the French authorities have suggested that the current BTV-8 vaccine in use is effective (ESA 2023). In the coming year it is likely that this new strain will continue spreading north. If it is able to reach the coast region of northern France, there could be potential for windborne incursion of infected Culicoides into Great Britain.

Unlike France, in Spain BTV is restricted to specific zones which are under restrictions. Recent data has shown an expansion of BTV-4 into Galicia and Madrid, meaning that these previously free areas have become restriction zones with increased surveillance and a ban on movement of unvaccinated livestock. In Italy, various BTV serotypes are endemic. What is of concern are the recent reports showing a potential new variant of BTV-8 (ProMED 2023) and a number of clinical signs of disease in recent BTV-4 outbreaks even with the susceptible being vaccinated (ProMED).

Considering all disease incursion routes from France, the Netherlands, Belgium and Germany, the overall risk of BTV entry into Great Britain has been assessed as medium.

Live ruminants from the Netherlands, Belgium and Germany are currently unable to be sent to Great Britain 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. Hence the risk to Great Britain is currently from the incursion of infected Culicoides (windborne and via transport), and the movement of infected livestock following undetected spread into other areas which export these animals to Great Britain.

The possibility for the windborne incursion of Culicoides from affected areas is monitored frequently, with a collaborative effort between APHA, The Pirbright institute (as vector and disease experts) and the Met Office (who can predict potential airborne movement of vectors into Great Britain using their Numerical Atmospheric-dispersion Modelling Environment (NAME) and provide estimates of climate suitability for spread in Great Britain and on the Continent). The NAME model predicts how many ‘plumes’ of Culicoides may have been able to reach the British coastline over the previous two-week period, and where in Great Britain these plumes may have entered. Outputs from the risk assessment are communicated to risk managers. As we head into winter and the temperature drops, Culicoides activity is expected to decrease, and onwards virus spread will further reduce.

Other potential pathways for BTV into Great Britain include imports and illegal movement of infected animals or germplasm. There is a potential risk of virus entry associated with the movement of infected Culicoides in other traded or transported commodities. 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.

Assurances should be sought from traders to ensure BTV susceptible animals are fully protected with the appropriate serotype vaccination prior to travel. 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.

We will continue to monitor the current situation.

Authors

Adem Yusuf

Dr Lauren Perrin

Dr Alexander Mastin

Tony Pacey

Dr Melanie Nicholls

References

All disease reports are available from the OIE WAHIS database.

ADIS (2023) Animal Disease Information System Available from: Animal Disease Information System (ADIS) (Accessed on 29 November)

Brand, S.P. and Keeling, M.J., 2017. The impact of temperature changes on vector-borne disease transmission: Culicoides midges and bluetongue virus. Journal of the Royal Society Interface, 14(128), p.20160481.

BENV National Veterinary Epidemiological Bulletin (IZS) Bluetongue (Accessed 28 November 2023)

Cappai, S., Rolesu, S., Loi, F., Liciardi, M., Leone, A., Marcacci, M., Teodori, L., Mangone, I., Sghaier, S., Portanti, O. and Savini, G., 2019. Western Bluetongue virus serotype 3 in Sardinia, diagnosis and characterization. Transboundary and emerging diseases, 66(3), pp.1426-1431.

Carpenter, S., Wilson, A., Barber, J., Veronesi, E., Mellor, P., Venter, G. and Gubbins, S., 2011. Temperature dependence of the extrinsic incubation period of orbiviruses in Culicoides biting midges. PloS one, 6(11), p.e27987.

European Commission (2023) About Bluetongue (europa.eu) (Accessed on 29 September)

Holwerda, M., Santman-Berends, I., Harders, F., Engelsma, M.Y., Vloet, R., Dijkstra, E., van Gennip, R., Mars, J., Spierenburg, M., Roos, L. and van den Brom, R., 2023. Emergence of bluetongue virus serotype 3 in the Netherlands in September 2023. bioRxiv, pp.2023-09.

Irish Department of Agriculture, Food and the Marine 2023 Bluetongue virus update (Accessed on 29 November)

House of Representatives of the Netherlands (2023) Animal disease bluetongue, House of Representatives of the States-General (tweedekamer.nl) (Accessed on 29 November)

Melkvee (2023) (Accessed on 29 November)

Ministerio de Agricultura, Pesca y Alimentación (Ministry of Agriculture, Fisheries and Food) (2023) Disease Situation Update 8 August 2023 (Accessed on 29 November)

Mellor, P. S., J. Boorman, and M. Baylis. “Culicoides biting midges: their role as arbovirus vectors.” Annual review of entomology 45, no. 1 (2000): 307-340.

Plateforme ESA (2023) Weekly Bulletin of International Animal Health Surveillance (BHVSI-SA) 21 September 2023 (Accessed 29 November 2023)

ProMED 2023 (Accessed on 29 November)

Sanidad (2020) Bluetongue virus, Sanidad (Accessed on 29 November)

Wittmann (2002) Effect of temperature on the transmission of orbiviruses by the biting midge, Culicoides sonorensis - Wittmann - 2002 - Medical and Veterinary Entomology - Wiley Online Library

WVBR (2023) European Reference Laboratory confirms bluetongue virus serotype 3 - WUR (Accessed on 29 November)

Plateforme ESA (2023) Weekly Bulletin of International Animal Health Surveillance (BHVSI-SA) 17 October 2023 (Accessed on 29 November)

TSIS (2023) TSIS - Animal Disease Information System (fli.de) (Accessed on 29 November)

Netherlands Ministry of Agriculture, Nature and Food Quality (NVWA) (2023) Bluetongue positive by place of residence, NVWA Map (Accessed on 29 November)

Ministry of Agriculture and Consumer Protection of the State of North Rhine-Westphalia, First detection of bluetongue in the district of Kleve - Ministry of Agriculture (nrw.de) (Accessed on 29 November)

FASFC - Bluetongue: Confirmed bluetongue serotype 3 infection in a sheep farmer in Merksplas (favv-afsca.be)

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