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Lumpy skin disease: I. Data collection and analysis

2017; Wiley; Volume: 15; Issue: 4 Linguagem: Inglês

10.2903/j.efsa.2017.4773

1831-4732

Plant and Fungal Interactions Research

EFSA JournalVolume 15, Issue 4 e04773 Scientific ReportOpen Access Lumpy skin disease: I. Data collection and analysis European Food Safety Authority (EFSA), European Food Safety Authority (EFSA)Search for more papers by this author European Food Safety Authority (EFSA), European Food Safety Authority (EFSA)Search for more papers by this author First published: 20 April 2017 https://doi.org/10.2903/j.efsa.2017.4773Citations: 22 Correspondence: alpha@efsa.europa.eu Requestor: European Commission Question number: EFSA-Q-2016-00542 Acknowledgements: EFSA wishes to thank the members of the Working Group on lumpy skin disease: Jan Arend Stegeman, Simon Gubbins, Nick Lyons, Eyal Klement, Miguel Miranda, Yuval Gottlieb for the preparatory work on this scientific output and the hearing experts Ledi Pite, Džemil Hajrić, Aleksandra Miteva, Brigita Hengl, Sotiria-Eleni Antoniou, Bafti Murati, Tatjana Labus, Drago Maroejvic, Ioana Neghirla, Srgjan Meshterovikj, Esra Satir for the data collection; Dominique Bicout, Anette Bottner for reviewing the document, and EFSA staff members: Alessandro Broglia, Josè Cortiñas Abrahantes, Andrey Gogin, Lisa Kohnle, Mario Monguidi, Jane Richardson, Jelena Vracar for the support provided to this scientific output. A special thanks is to: Ledi Pite from Ministry of Agriculture, Rural Development and Water Administration, Albania; Aleksandra Miteva from Food Safety Agency, Bulgaria; Brigita Hengl from Croatian Food Agency and Ivica Sučec from Ministry of Agriculture, Croatia; Sotiria-Eleni Antoniou and Chrysoula Dile of the Animal Health Directorate of the Greek Ministry of Rural Development and Food and to the veterinary staff of the Greek NRL of Capripoxviruses and Regional Veterinary Authorities, Greece; Bafti Murati from the Food and Veterinary Agency, Kosovo; Drago Marojevic from the Ministry of Agriculture and Rural Development, Montenegro; Srgjan Meshterovikj, Food and Veterinary Agency, former Yugoslav Republic of Macedonia; Tatjana Labus from the Ministry of Agriculture and Environmental Protection, Republic of Serbia; Esra Satir from Pendik Veterinary Control Institute, Turkey for the timely provision of the epidemiological data for this report. A special thanks also to Stefan Niemeyer and Andrea Toreti from Joint Research Centre (EC) for the timely provision of meteorological data. Approved: 27 March 2017 Reproduction of the images listed below is prohibited and permission must be sought directly from the copyright holder: Figure C.4: © Elsevier BV; Figure C.9: © Australian Society for Parasitology Inc; Figure C.10: © Cambridge University Press AboutSectionsPDF ToolsExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Abstract An epidemiological analysis of the temporal and spatial patterns of LSD epidemics and of the risk factors for LSD spread in south-eastern Europe was performed, based on the data collected from affected and at risk countries. Since 2015, the extent of the LSD epidemics in south-eastern Europe was over 7,600 LSD outbreaks with 12,800 affected animals, with most outbreaks occurring between May and August. Most LSD spread occurs over a relatively small distance, approximately between 10 and 20 km, and the speed of propagation was estimated to be mostly up 2 km/day, in agreement with the vector-borne pattern of LSD. Proximity to affected farms, warm temperatures and related vector abundance were among the main risk factors for LSD spread. Within a few months' at least 90% of the animal population had been vaccinated with live homologous vaccine against LSD in south-eastern Europe. Where almost total vaccination coverage was achieved, no further outbreaks were reported. The vaccination effectiveness in Albania was estimated to be around 70% at farm level and 77% at animal level. Possible adverse effects to live homologous vaccine, including fever, decreased milk production and oedema at injection site were reported in Croatia (a LSD-free country) mostly within 2 weeks after vaccination, in 0.09% of the vaccinated animals. Unique farm identifiers should be always used across all databases, so to allow further analysis especially on improving the mathematical models for more robust estimates of transmission parameters applicable to the region, and for better estimation of vaccination effectiveness. All suspected clinical cases in vaccinated animals should be confirmed by differentiating field virus from vaccine strain. Trapping surveys for estimation of vector abundance can be carried out by targeting some sentinel farms, to be followed up during the whole LSD season, while long-term studies can give more accurate information about species composition and seasonality of potential LSD vectors. Summary The European Commission requested the European Food Safety Authority (EFSA) to perform an epidemiological analysis based on the data collected from the Member States or non-EU countries affected by lumpy skin disease (LSD). In particular, an analysis of the temporal and spatial patterns of LSD and an analysis of the risk factors involved in the occurrence, spread and persistence of the LSD virus among the cattle population should be included. Two reports are foreseen for presenting the results of this analysis, the present report and a second report to be delivered in January 2018. In this first report, an analysis is presented with the available data received from the countries involved in this project so far, namely by Albania, Bulgaria, Croatia, Greece, the former Yugoslav Republic of Macedonia, Kosovo,1 Montenegro, Serbia and Turkey. The collection of data from the affected countries included data on the structure and distribution of cattle farms, on LSD outbreaks and on vaccination, up to end of 2016. Although a certain degree of heterogeneity was observed in timeliness, quantity and quality of data received from the different countries, given the current epidemiological situation in the affected and at-risk countries, there has been a very high level of commitment and collaboration by the veterinary services from the countries involved in this data collection project. The methodology was based on descriptive epidemiology, mapping tools and on a survival analysis for the estimation of the effectiveness of vaccination. This analysis included a description of temporal and spatial patterns of LSD epidemics in the south-eastern Europe compared to animal density, temperatures, progressive vaccination coverage and an analysis of vaccination effectiveness in the selected case study of Albania. This was chosen due to the characteristics of that situation, i.e. no culling of affected animals and mixed presence of vaccinated and unvaccinated farms, which fit the purpose of the analysis. An analysis of the possible adverse effects of vaccination in an unaffected country (Croatia) was also presented. Regarding the role of vectors as one of the main risk factors for LSD spread, opportunity maps for LSD vector survival were presented. Besides that, since the presence and abundance of LSD vectors is one of the main risk factors for the spread and since the knowledge on possible vectors of LSD virus is limited, in this first report, some indications are provided for survey and trapping protocols for vector insects of LSD. This is also linked to the importance of studying vectors during current outbreaks. Since the introduction into Turkey in 2013, LSD virus outbreaks have expanded northwards to the west through south-eastern Europe and to the east through the Caucasus, reaching Russia. In terms of extent of the epidemics, since the beginning over 7,600 LSD outbreaks with 12,800 affected animals were reported, with a clear seasonal pattern, with most outbreaks occurring between May and August, in south-eastern Europe in 2015, excluding Turkey. The seasonality of the outbreaks is in agreement with the opportunity maps for vector survival. These maps also show that vector survival would be possible throughout the entire year in many regions of Greece. For this reason, warm temperatures and related abundance of vectors could be considered one of the main risk factors for LSD spread and persistence. According to the analysis done for LSD in Turkey until October 2014 (no vaccination performed) and in line with what previously estimated by mathematical model in EFSA outputs, most LSD spread occurs over a relatively small distance, approximately between 10 and 20 km, and the speed of propagation was estimated to be mostly (75% percentile) up 2 km/day, with few values (95% CI) up to 15 km/day. This is in agreement with the vector-borne pattern of LSD, with mainly vector transmission over a short distance, and with some transmission over much longer distances, and faster spread rate, as would be expected for less frequent long distance movement of infected cattle. In relation to that, proximity to affected farms can be considered a further risk factor for LSD spread. Mass vaccination campaigns with live homologous vaccines against LSD were carried out at regional level in south-eastern Europe in all affected countries and Croatia. These campaigns resulted in at least 90% vaccination coverage of the animal population, within a period of a few months, indicating a high level of responsiveness and preparedness of the national authorities of those countries to control the epidemics. Where almost total vaccination coverage was achieved, no further outbreaks were reported after beginning of October 2016; only few sporadic outbreaks have been reported in Greece and the former Yugoslav Republic of Macedonia. In some cases, (e.g. Bulgaria) the epidemics did not reach the expected peak of outbreaks in August, rather it died off earlier. The protective effect of vaccination is confirmed by the results of the analysis of the vaccination effectiveness in the case study of Albania. The effectiveness is estimated to be around 70% at farm level and 77% at animal level. This evidence shows that mass vaccination with homologous vaccines is one of the factors that mainly influence LSD spread and supports the findings of previous EFSA outputs by analysing Greek data and of the studies from Israel. These highlighted that the vaccination with the live homologous vaccine, when applied as uniformly as possible across the population with high coverage is most effective in reducing LSD virus (LSDV) spread. Adverse effects to live homologous vaccines applied in situation of disease freedom (Croatia) were reported on 0.24% of the vaccinated farms, involving 0.09% of the total animals affected and 0.02% deaths. The majority of symptoms were reported within 2 weeks after vaccination and included fever, decrease in milk production and oedema at injection site. The presence and abundance of all potential LSD vectors was one of the major risk factors considered to contribute to LSD spread and persistence. Thus, in the absence of specific data, the most relevant indications for vector collection to study seasonal dynamics and abundance are provided in this report, so to encourage the affected countries to perform vector surveys. Concerning those indications, it can be concluded that potential vectors for LSD can be identified by epidemiological evidences using their abundances during outbreak season. Moreover, different sampling methods for potential vectors of LSD are available, according to the scenario and the aim of the survey (i.e. epidemics, surveillance, LSD detection on vectors). In any case, each targeted vector requires specific sampling methods and training/ expertise on taxonomy. To improve data quality and quantity, it is recommended that the data models as provided by EFSA are followed as much as possible. In particular, it is important to indicate the unique identifier of farms (farm ID) across all databases to allow connection between different databases. If possible, the unique identifier of farms should be also included as a variable in the Animal Disease Notification System (ADNS) system, so to be able to indicate which farm is involved in each outbreak reported. Improvement of data quantity, quality and time availability will enable further analysis on different epidemiological aspects to enhance the mathematical models used previously, as well as to determine other potential risk factors for LSD spread and persistence. This will provide more robust estimates for transmission parameters that are directly applicable to the region, as well as to better assess the effectiveness of vaccination, based on field data. Concerning the surveillance and any possible new LSD cases in 2017, given the current situation where most animals have been vaccinated with live LSDV homologous strain without DIVA possibilities, the most feasible option for surveillance seems to be the immediate notification of clinical suspected cases, the confirmation of LSDV in those animals by laboratory testing including the differentiation of field virus from vaccine strain. Concerning adverse effects of vaccination, these should be collected systematically, where possible, at animal level. In relation to field surveys on potential LSD vectors, it is recommended to carry out ad hoc trapping surveys to calculate relative abundance of potential LSD vectors by targeting a number of outbreak farms, to be followed up during the whole LSD season, from the first LSD cases in spring until the last one in autumn. Moreover, long-term studies (i.e. biannual, triennial) would give more accurate information about species compositions in farms and seasonality of potential vectors of LSD. 1 Introduction 1.1 Background and Terms of Reference as provided by the requestor Lumpy skin disease (LSD) is a viral infection affecting cattle which is transmitted primarily by blood feeding insects (vectors) and to a lesser extent through direct contact between animals. Mortality due to LSD is not very high (up to 10%); however, occurrence of the disease is associated with a drop in production and serious trade restrictions. LSD is endemic in most African countries. Since 2012, LSD has been spreading on an unusually large scale throughout the Middle East, including Egypt and Israel, into Turkey (reported steadily since 2013) where it is now considered endemic. By November 2014, shortly before the publication of EFSA's opinion on LSD (January 2015), the disease was confirmed in the island of Cyprus (in the areas not under the effective control of the Republic of Cyprus). In the months that followed, LSD also gradually progressed from Anatolia (Turkey) where it is endemic, into the East Thrace area of Turkey (May 2015) and from there to Greece (Evros, August 2015) where it continued to spread westwards, producing new outbreaks as far as the regional units of Thessaloniki and Chalkidiki. In 2016, the disease reappeared in Greece, close to the border with Bulgaria, in the region of Serres where vaccine coverage was relatively low. Thus, the decision was taken to expand the vaccination zone further to the west (procedure ongoing). Shortly, after the first outbreaks in Greece in 2015, in 2016, the disease occurred for the first time in Bulgaria, Albania, Serbia, the former Yugoslav Republic of Macedonia, Montenegro and Kosovo.1 The European Union (EU) legislation imposes culling and destruction of all cattle present in the affected holdings. This is followed by the establishment of a protection zone (3 km radius) and a surveillance zone (10 km radius) with special restrictions for cattle and products thereof. Additional Commission protection measures, namely regionalization, apply in the affected areas and the vaccinated areas (specific Commission Implementing Decision are in place for Greece and Bulgaria). Similar measures are envisaged for all areas where vaccination is applied to prevent the spread of the disease to previously unaffected areas through the movement of potentially infected cattle. The Standing Group of Experts on Lumpy skin disease for south-east Europe under the GF-TADs umbrella,2 in their first meeting (Brussels 4–5 July 2016) proposed, among other recommendations, that: 'The collection of surveillance data and scientific information that maybe relevant (e.g. incidence, weather conditions) be coordinated for purposes of better risk assessment and management' (Final recommendations, available at http://web.oie.int/RR-Europe/eng/Regprog/docs/docs/LSD1/LSD%20SGE1%20(Brussels%20%20July2016)%20-%20Conclusions%20and%20recommendations%20(Final).pdf) In the light of the above, the Commission needs an updated epidemiological analysis based on the data collected from the Member States affected by LSD. The use of the European Food Safety Authority (EFSA) Data Collection Framework is encouraged as it promotes the harmonisation of data collection. Any data that is available from neighbouring non-EU countries should be used as well. This analysis should consider and develop the findings of the EFSA scientific opinion on LSD adopted in January 2015. The data to be used should include all the available epidemiological data from 2014 onwards. Therefore, in the context of Article 31 of Regulation (EC) No. 178/2002, EFSA should provide technical and scientific assistance to the Commission based on the following Terms of Reference: To analyse the epidemiological data on LSD from Cyprus, Greece, Bulgaria and any other Member States or non-EU countries that might be affected by LSD. To include an analysis of the temporal and spatial patterns of LSD. To include an analysis of the risk factors involved in the occurrence, spread and persistence of the LSD virus among the cattle population. 1.2 Introduction and interpretation of the Terms of Reference In this first report produced in the framework of this mandate, an analysis is presented with the data received so far by the countries involved in this project, namely Greece, Bulgaria, Albania, Serbia, Bosnia and Herzegovina, the former Yugoslav Republic of Macedonia, Montenegro, Turkey, Romania, Croatia and Kosovo.1 The collection of data from the affected countries included data on the structure and distribution of cattle farms, on LSD outbreaks and on vaccination at farm level. To guarantee harmonisation, the EFSA Data Collection Framework was used as much as possible along the project. This analysis included a description of temporal and spatial patterns of LSD epidemics in the south-eastern Europe, a comparison between temporal trends of outbreak, temperatures and progressive vaccination coverage and an analysis of vaccination effectiveness in the selected case study of Albania, with respect to the characteristics of that situation, i.e. no culling of affected animals and mixed presence of vaccinated and unvaccinated farm which fit the purpose of the analysis. An analysis of the possible adverse effects of vaccination in an unaffected country (Croatia) was also presented. Regarding the role of vectors as one of the main risk factors for LSD spread, opportunity maps for LSD vector survival were presented. Besides that, since the presence and abundance of LSD vectors is one of the main risk factors for the spread and since the knowledge on possible vectors of LSD virus is limited, in this first report, some indications are provided for survey and trapping protocols vector insects of LSD. This is also linked to the importance of studying vectors during current outbreaks. Requesting and collecting epidemiological data from multiple countries currently affected by a livestock epidemic that causes huge losses anticipated a series of difficulties. The effort demonstrated by the veterinary services in collecting, compiling and providing the data to EFSA was recognised and appreciated, especially because this data collection was carried out while the disease had recently spread over the region and when veterinary services were overloaded with implementation of control measures. Thus, a certain degree of heterogeneity in timeliness, quantity and quality of data received from the different countries was expected and observed. For this reason, the present report should be considered as a starting point in this project, and it does not pretend to already present an exhaustive picture of all possible epidemiological characteristics and risk factors of the LSD epidemics in Europe. In fact, the databases could be refined throughout 2017 and the output of further analyses to be included in a second report which is foreseen by January 2018, together with an analysis of the data referring to 2017. Because of the limited knowledge about possible vectors of LSD virus and because of the importance of studying vectors during current outbreak, in this first report a section is dedicated to possible vector insects of LSD, some indications are provided for survey and trapping protocols. 2 Data and methodologies To discuss and agree which data were useful to collect and what would be feasible to provide within the timeline available for the present report, a workshop with the contact points from the countries involved in this project (see Section 1.2) was organised at EFSA in December 2016. Data models about cattle population, vaccination (including data on adverse effects of vaccination from non-affected countries), were presented, and agreed (see Appendix A). For the LSD outbreak data, the ADNS3 format was used. The importance of providing a unique identifier for the farms (farm ID) in each type of database, that would allow connecting the different databases, was stressed. It was agreed that data on cattle population up to 1 January 2016, data on LSD outbreaks and vaccination up to 31 December 2016 would be used. Most of these data were submitted to EFSA by 31 January 2017. It was agreed not to provide laboratory data because they are not systematically collected, and in some countries only few tests are performed to confirm the outbreaks (diagnosis based on clinical signs). For the second report (January 2018), the database for population, outbreak and vaccination from all the involved countries will be completed as far as possible, as well as the collection of the data from 2017. This would be important to compare the LSD spread in a season associated with susceptible animals and a starting vaccination campaign (2016) with spread in a season when almost the whole population has been vaccinated at least with one doses and immunity due to previous exposure is present. The application of the mathematical model for the between-farm spread of LSD virus (LSDV) developed as part of an earlier opinion (EFSA AHAW Panel, 2015, 2016) to outbreak data for the affected countries extracted from ADNS was explored. This was designed to provide updated estimates for transmission parameters for LSDV. However, the modelling approach, as currently implemented, only applies to spread in an unvaccinated population. For all countries, there were too few outbreaks over too short an interval prior to the implementation of vaccination to allow robust parameter estimates to be obtained. However, future work will explore the possibility of linking the demographic, vaccination and outbreak data sets for some or all the affected countries. An extended version of the model that includes vaccination will then be applied to these data. This will allow us to obtain more robust estimates for transmission parameters that are directly applicable to the region, as well as to assess the impact of vaccination on disease spread. Regarding the last section about surveys on vectors, the data and information used is collected from the published literature, ECDC,4 Vectornet consortium5 and expert knowledge. 2.1 Epidemiological data For the present, report data were provided by the competent authorities of Greece, Bulgaria, Albania, Serbia, Montenegro, Croatia, the former Yugoslav Republic of Macedonia, Kosovo and Turkey. 2.1.1 Cattle population data Data on cattle population and farm structure as indicated in Appendix A (Table A.1) were provided at farm level by Greece, Bulgaria, Albania, Montenegro, Croatia, Serbia and from Turkey (in the latter case, data were provided at NUTS3 level). 2.1.2 Outbreak data Concerning LSD outbreak data, an ADNS extraction as submitted to the European Commission was updated with the data on LSD outbreaks reported up to the end of 2016 received by Greece, Bulgaria, Albania, Montenegro and Kosovo (see data model in Appendix A, Table A.2). Greece, Kosovo, Bulgaria, the former Yugoslav Republic of Macedonia, Kosovo and Albania also provided the identifiers of farm IDs. In most cases, the outbreaks reported are confirmed by laboratory test of samples taken from on few clinically affected animals. In other cases, e.g. Albania, the reported outbreaks are confirmed by clinical diagnosis based on signs of lumpy skin disease. 2.1.3 Vaccination data Data on vaccination against LSD were provided at farm level by Greece, Bulgaria, Albania, Montenegro, Croatia, Kosovo, Serbia, Kosovo, the former Yugoslav Republic of Macedonia and Turkey (in the latter case, data were provided at NUTS3 level for 2016). Croatia and Albania provided also information about post-vaccination adverse effects. 2.1.4 Climatic data Meteorological data from weather stations interpolated on a 25 x 25 km grid for min, max and average temperatures and rainfall were provided by the Joint Research Centre (JRC) of the European Commission6 through the Coordination Group for Meteorological Satellites (CGMS) database7 for the time window 2014–2016 for the countries involved. 2.2 Methodologies Descriptive epidemiological characteristics were derived from the data and GIS software was applied to map their spatial distribution. The vaccination effectiveness and opportunity map for vector survival were estimated as explained below. Information on vector trapping were derived from scientific literature and expert knowledge. 2.2.1 Estimation of the vaccination effectiveness In order to estimate the vaccination effectiveness, the case study of Albania was chosen because in this country the vaccination coverage at animal level was around 50%. Therefore, both vaccinated and unvaccinated farms were present during the epidemic. As said above, three databases were provided, namely: the registry of all the cattle farms in Albania, a list of all vaccinated farm and list of all the outbreaks which occurred in Albania until 31/12/2016. After merging the three databases according to farm ID, approximately 3,600 outbreak farms and a database of approximately 200,000 farms scattered in 36 districts were available for analysis. This allowed a comparison between vaccinated and not vaccinated herds towards the onset of an outbreak. In five districts, no outbreak occurred during 2016. Therefore, only data on farms from the other 31 districts were analysed. For each district, the date of occurrence of the first outbreak was defined as the date of the beginning of the follow-up period. A farm was defined as not vaccinated (vaccinated and protective immunity established) during the follow-up period if it had not been vaccinated or if the vaccination date plus 28 days (the time lag for immunity to be established) was later than the end of the year (31/12/2016) or if vaccination plus 28 days was later than the occurrence of an outbreak. Otherwise it was considered as vaccinated. In vaccinated farms, all animals are assumed to be vaccinated. Assuming the district as the most homogeneous geographical unit available from the spatiotemporal point of view for this analysis, the follow-up period for each farm was generated according to one of the following possible situations: In non-vaccinated farms with no outbreak event, the follow-up period is from the occurrence of the first outbreak in the district until 31/12/2016. In outbreak farms, which were not vaccinated, the follow-up period is from the occurrence of the first outbreak in the district until the date of the outbreak event in the farm. In vaccinated farms with no outbreak, the follow-up period is from the date of vaccination plus 28 days until 31/12/2016. In vaccinated outbreak farms, the follow-up period is from the date of vaccination + 28 days until the date of the outbreak event (first suspicion) in the herd. For vaccinated herds, a follow-up period as not vaccinated was included as well if the date of vaccination plus 28 days was later than the date of first outbreak in the district. In this case, the follow-up period for this herd considered as not vaccinated is from the occurrence of the first event in the district until the date of vaccination plus 28 days. A survival analysis was performed comparing LSD incidence in vaccinated vs unvaccinated farms, as previously described in other EFSA statement (EFSA, 2016). Kaplan–Meier survival curves were created using survival module in R and graphs were generated by using the GGplot package, with the purpose of studying the protective effectiveness of vaccination of animal population in the EU, on a farm level (i.e. the farm was the unit of interest, and the outcome was 'a herd becoming infected that is, at least one infected animals was identified). Hazard ratio (HR) for an outbreak in vaccinated vs non-vaccinated farms was calculated, using Cox proportional hazards ratio regression model. Vaccine effectiveness was calculated as 1-HR. The same analysis was performed at herd level (the smallest epidemiological unit availab