Scientific Opinion on sheep and goat pox


Panel on Animal Health and Welfare
EFSA Journal
EFSA Journal 2014;12(11):3885 [122 pp.].
Panel members at the time of adoption
Edith Authie, Charlotte Berg, Anette Bøtner, Howard Browman, Aline De Koeijer, Klaus Depner, Mariano Domingo, Christian Ducrot, Sandra Edwards, Christine Fourichon, Frank Koenen, Simon More, Mohan Raj, Liisa Sihvonen, Hans Spoolder, Jan Arend Stegeman, Hans-Hermann Thulke, Ivar Vågsholm, Antonio Velarde, Preben Willeberg and Stéphan Zientara.

The Panel wishes to thank the members of the Working Group on sheep and goat pox: Tsviatko Alexandrov, Aline De Koeijer, Dimitrios Dilaveris, Mariano Domingo, Simon Gubbins, Arjan Stegeman, Eeva Tuppurainen for the preparatory work on this scientific opinion and EFSA staff: Alessandro Broglia, Josè Cortinhas, Anna Zuliani, Olaf Mosbach-Schulz, Andrey Gogin, Justyna Jaskiewicz, Matthew Watts and Andrea Gervelmeyer for the support provided to this scientific opinion.

Opinion of the Scientific Committee/Scientific Panel
On request from
European Commission
Question Number
22 October 2014
13 November 2014
European Food Safety Authority (EFSA), Parma, Italy
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Sheep pox (SPP) and goat pox (GTP) are viral diseases of sheep and goats characterised by severe losses, especially in naive animals. SPP and GTP are endemic in many African, Middle Eastern and Asian countries, with recurrent epidemics in Greece and Bulgaria, as in 2013–2014. The main mode of SPP/GTP transmission is direct contact between animals, but, since the virus can survive in the environment, indirect transmission may also occur through fomites such as human movement, vehicles, wildlife and trade of hides when insufficiently treated. According to a model developed to evaluate the spread of SPP, the probability of spread of the infection in south-eastern Europe is <1 %, while, if introduced in the Iberian Peninsula, the probability that SPP would spread is more than 50 %. The long-term survival of the SPP virus in the environment enhances the likelihood of SPP endemicity; however, this can be reduced by extensive cleaning and disinfection, and with a waiting period before re-stocking culled herds. Early detection and notification, prompt movement restriction of animals, an extension of duration and size of the protection zone and culling affected herds, based on clinical signs, are effective and time-saving control measures recommended by the AHAW Panel. Only live attenuated vaccines are available for SPP/GTP, which are not licensed within the EU and without principle for differentiating infected from vaccinated animals. The AHAW Panel recommends further investigation of potential SPP/GTP transmission through arthropods and wildlife, the survival of SPP/GTP viruses in grazing sites and in animal feed and hides and the development of inactivated vaccines. Sentinel animals could be used prior to re-stocking culled herds. Awareness-raising campaigns for farmers and veterinary staff to promote recognition of the disease should be considered. The cooperation of EU with neighbouring countries should be encouraged to prevent transboundary disease spread.


Following a request from the European Commission, the EFSA Panel on Animal Health and Welfare (AHAW Panel) was asked to deliver a scientific opinion on sheep pox (SPP) and goat pox (GTP), in order to provide an update on the characterisation of the diseases, to assess the risk of spread and to determine if further measures are justified. This is linked to recent outbreaks of SPP in the European Union (EU) and the fact that it is already endemic in some EU neighbouring countries.

In particular, EFSA was asked to (i) characterise the disease and provide an update on the global occurrence of SPP and GTP and changes in the distribution during the last 15 years; (ii) map the regions of concern, and other countries of the Mediterranean Basin and Black Sea, displaying identified or likely major live animal trade routes; (iii) evaluate all possible pathways of SPP and GTP introduction into the EU, ranking them on the basis of their level of risk, with the view of enhancing preparedness and prevention; (iv) assess the risk and speed of propagation of SPP and GTP into the EU and neighbouring countries; (v) assess the risk of SPP and GTP becoming endemic in EU animal populations and neighbouring countries; (vi) assess the impact and consequences of SPP and GTP entering the EU by considering different scenarios with regard to the effectiveness of surveillance and control measures; and (vii) review the feasibility, availability and effectiveness of the main disease prevention and control measures (diagnostic tools, biosecurity measures, restrictions on the movement, culling, vaccination).

Regarding disease characterisation, the AHAW Panel reported that SPP and GTP are characterised by severe clinical signs and losses, especially in naive and young animals, with morbidity up to 90 % and case fatality up to 100 %. There is no evidence to date that these viruses can infect wildlife. Capripoxviruses are not considered to be zoonotic agents. SPP and GTP are endemic in many African, Middle Eastern and Asian countries, with recurrent incursions of SPP into Greece and Bulgaria, the most recent of which caused 91 outbreaks in Greece and 4 in Bulgaria from August 2013 until April 2014. SPP virus (SPPV) and GTP virus (GTPV) can be detected in animal secretions (e.g. ocular, nasal discharge) up to two months after infection. If protected from sunlight, the virus can survive in scabs and, therefore, also in the environment for up to six months, and in the wool, hair or skin of infected animal for up to three months. The virus is susceptible to high temperatures and common disinfectants. The main mode of transmission of SPPV/GTPV is direct contact between infectious and susceptible animals. Indirect transmission may also occur through dissemination of the virus from animal secretions and products (e.g. scabs, skin, wool) from infected animals or through human movements or fomites such as birds or insects acting as mechanical carriers of the virus.

Considering the identified or likely animal movements in the regions of concern and other countries of the Mediterranean Basin and Black Sea, the AHAW Panel remarked that movement of live animals from third countries in the Mediterranean Basin and Black Sea areas to the EU is currently forbidden, according to EU animal health legislation on the import of live animals from countries where SPP/GTP is endemic, although illegal movements of animals cannot be quantified.

By analysing the animal movements within Greece, Bulgaria and Turkey, it has been shown that a large number of live small ruminants is usually shipped from the provinces that have been affected by SPP/GTP to other parts of each country; therefore, the prompt introduction of movement restriction when SPP cases are detected is considered an important measure for limiting the spread of the disease. There is also a large amount of trade of skin, wool and hides from countries where SPP/GTP is present to the EU, although, in order to perform a risk assessment, detailed information is needed to clarify whether the commodity has undergone appropriate treatment for sufficient inactivation of SPPV/GTPV. Skins and hides processed only by drying or salting treatments may pose a risk for introduction of SPPV/GTPV into the EU if imported from affected areas.

The identified possible pathways of SPP and GTP introduction into the EU are related to movement/proximity of animals, humans and fomites. The pathways of introduction linked to animal movements include the legal or illegal trade of live animals and animal products (e.g. skin, hides, wool) and the movement or proximity of animals to contaminated areas/pastures shared by flocks from infected countries. The pathways of introduction linked to human movements are identified as the movement of visitors, tourists, animal workers and immigrants. The pathways of introduction linked to fomites or mechanical carriers are supposed to be the movement of vehicles, birds and insects.

Based on expert knowledge elicitation conducted with the veterinary service from Greece and Bulgaria, the most likely pathways of SPP introduction, into the EU, are the movement of people having contact with animals (e.g. immigrants, traders, visitors, animal workers), vehicles and illegal movement of animals. The potential introduction of SPP/GTP into the EU through flying arthropods and wildlife, including the movement of wild birds across the river Evros at the border with Turkey, was reported as a likely source, although the role of these vectors has yet to be confirmed. Ranking of the pathways based on the expert knowledge elicitation should be used with caution given the small number of SPP/GTP introductions into the EU and the small number of experts involved in the expert knowledge elicitation. Nevertheless, the value of the expert knowledge elicitation lies in the fact that it reflects the views of the field staff involved in outbreak management.

In order to assess the risk and speed of propagation of SPP and GTP into the EU and neighbouring countries, a model has been developed to evaluate the spread of SPPV over space, using data from the 2013–2014 outbreaks in the EU and European Turkey (East Thrace). Several different models and assumptions on regional sheep demography were tested. The best-fit model was based on the assumption that the transmission between regions is proportional to the total number of sheep per NUTS3 region (Nomenclature of Territorial Units for Statistics). Given the very limited availability of data, the analysis is restricted to an evaluation of the probability of SPPV transmission over a given distance (fitted to data of transmission between regions in Greece/Bulgaria), for each scenario, and its dependence on the number of herds or sheep in a region. This model does not distinguish between possible transmission routes or mechanisms. Three scenarios for the spread of SPP in the EU after 1, 6 and 12 months and after 5 years were simulated for (i) incursion in the regions of Bulgaria and Greece; (ii) incursion in Croatia and Hungary, over the Balkans; and (iii) incursion in southern Spain, from northern Africa. In the first two scenarios, the infection does not spread far and fast over space. The epidemic may spread further north into Romania and Hungary but with a very low probability (<1 %). In the scenario of SPP spread throughout Spain, and given the control measures applied in Greece and Bulgaria, SPP quickly spreads throughout Portugal and Spain with a high probability (>50 %), while the spread slows down in France (probability of spread <30 %). This increased speed of spread is because of a greater number of animals in NUTS3 regions in Spain and Portugal. Under the assumptions of the model, the current epidemic in Greece and Bulgaria is likely to be controlled by the current measures applied and is unlikely to spread further. However, SPPV spread throughout Spain may be more difficult to control because of the greater number of animals per NUTS3. The results of the model simulations are heavily based on the assumption that the contact patterns within Europe are similar to those which occur in Bulgaria and Greece. Owing to a limited data set, the uncertainty in quantifying the level of transmission is large. Consequently, the model predictions should be considered as examples of the options that have to be taken into account when assessing the risk of SPP epidemics in SPPV-free parts of the EU and should not be taken as fact.

Regarding the risk of SPP and GTP becoming endemic in animal population in the EU, the long-term survival of the SPPV/GTPV in the environment enhances the likelihood of SPP/GTP endemicity. The likelihood of SPP endemicity can be reduced by extensive cleaning and disinfection measures of premises and risk materials, combined with a waiting period before re-stocking of culled herds is allowed. Under the control measures applied in affected Member States (MSs), SPP has not become endemic.

When assessing the impact and consequences of SPP and GTP entering the EU, the AHAW Panel concluded that the major impact of SPP in Greece and Bulgaria was the culling of animals, around 19,300 animals in Greece and 687 in Bulgaria up until April 2014, and the decrease in animal movements from the affected provinces due to the restriction policy (34 % decrease in Greece and 80 % decrease in Bulgaria). Based on the output from the spread modelling study and assuming the application of current control measures as applied in Greece and Bulgaria, it is predicted that there will be limited disease impact after its introduction in Greece and Bulgaria, even 12 weeks after the first outbreak. In contrast, it is predicted that, by simulating the introduction of SPP/GTP infection in the Iberian Peninsula, the impact of the disease will be much higher, based on the output from a spread modelling study and assuming that the control measures currently applied in Greece and Bulgaria are used. This is attributed to the higher concentration of farms per NUTS3 in this region. Each of the modelling outputs has underlying uncertainty and need to be interpreted with care.

The main prevention and control measures for SPP/GTP have been assessed. Culling of the affected herds on the basis of the clinical signs and lesions is an effective and time-saving measure to reduce the risk of spread. Nevertheless, the diagnosis at herd level should be confirmed by laboratory testing in order to increase knowledge of the epidemiology and transmission of SPP.

Considering the diagnostic tools, under field conditions the clinical diagnosis performed by trained veterinary staff is effective for the early detection of outbreaks and the consequent prompt implementation of measures. Polymerase chain reaction (PCR) assays and enzyme-linked immunosorbent assays (ELISAs) are considered the most sensitive and specific diagnostic tests, for the detection the nucleic acid of the virus and antibodies against it, respectively.

As far as immunisation against SPP/GTP is concerned, the AHAW Panel reported that all the commercially available vaccines for SPP and GTP are live attenuated vaccines, prepared from a limited number of strains. None of these are licensed within the EU or support the principle of differentiating infected from vaccinated animals (DIVA). The use of these vaccines would inflict immediate restrictions on the international trade of live sheep and goats. Where applied, live attenuated SPP/GTP vaccines provide good protection and are able to control the outbreaks where a minimal coverage of 75 % is created and maintained. Although capripoxviruses are considered to be cross-protective, the use of homologous vaccine is more effective. Sufficiently attenuated and tested vaccines are safe and can be used in pregnant animals, providing lambs with three months’ immunity. However, some vaccines may have unacceptably high levels of residual pathogenicity. Inactivated vaccines are not commercially available and the immunity provided by them is not long-lasting (up to six months). The use of inactivated vaccines could be considered only in the event of an imminent outbreak, as an emergency vaccine and as a safer option than the use of live attenuated vaccine in non-endemic countries.

If a proper disease surveillance and reporting system is in place, allowing early detection and notification, movement restriction of animals appears to be an effective measure. It prevents direct contact between animals, which is the main mode of SPP transmission.

The AHAW Panel recommends further investigation of the potential transmission of SPP/GTP through arthropods and wildlife, and on the survival and infectivity of SPPV and GTPV in grazing sites as well as in animal feed (e.g. fodder or silage). In addition, further research and real-scale trials are needed on SPPV/GTPV inactivation through drying or salting treatments on sheep and goats hides, and a quantitative import risk assessment of skin and hides from affected regions should be performed. Furthermore, molecular typing of SPPV/GTPV strains, isolated during an outbreak, should be considered to better understand epidemiological links between outbreaks. In order to reduce the uncertainty regarding SPP/GTP epidemiology, harmonised data collection of outbreaks from MSs and neighbouring countries is recommended. In order to provide maximal safety, the development of inactivated vaccines, preferably along with application of the DIVA principle, is recommended. The safety of live attenuated vaccines should be further investigated, especially with regard to, for example, the reversion to virulence, the residual virulence, the spread of the vaccine strain and recombination in the field.

In term of preparedness, the AHAW Panel suggests that enforced biosecurity measures should be applied in risk areas, i.e. (i) introduction of new animals into the herds (quarantine), (ii) farm workers, visitors and veterinarians (e.g. cleaning and disinfection of hands, use of clean protective clothing and footwear) and (iii) cleaning and disinfection of the wheels of vehicles entering/exiting farms. Adequate veterinary care and improved surveillance should be in place for transhumant flocks along the migratory routes in risk areas, in particular for long-distance migration.

Awareness-raising campaigns and training for farmers and veterinary staff in recognising the disease under field conditions should be considered, especially for regions at higher risk of introduction of SPP (i.e. those bordering affected regions). Finally, if non-biological drivers of transmission of transboundary animal diseases change (e.g. breakdown of veterinary infrastructures, human migration, political unrest) the risk of SPP/GTP introduction should be accordingly reassessed. Under this perspective, the cooperation of the EU with neighbouring countries should be encouraged for prevention of transboundary animal diseases (TADs) and enhance preparedness.

In terms of disease control, the AHAW Panel recommends that after culling infected and in-contact sheep/goats and disinfection of affected farms, fully susceptible young sheep could be used as sentinel animals prior to re-stocking. The health of such animals should be monitored for three months (clinical inspection). It is recommended that active surveillance be in place for the first months after repopulating previously infected premises, to enable early detection of recurring epidemics. Extending the duration of setting the surveillance and protection zone beyond 21 and 42 days, as prescribed by the EC Directive 92/119, could be considered in order to reduce the risk of secondary outbreaks. Owing to extensive animal movement from affected provinces, it is recommended that restriction of animal movements is initiated promptly and efficiently when SPP cases are detected, in order to limit the spread of the disease. More stringent control measures, including prompt culling after clinical diagnosis and/or extension of the duration and/or size of the surveillance and protection zone, should be considered for SPP control after introduction into areas with greater numbers of sheep.

Sheep pox, goat pox, spread, prevention, impact, culling, vaccine
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