Research priorities to fill knowledge gaps in the control of African swine fever: possible transmission of African swine fever virus by vectors
2021; Wiley; Volume: 19; Issue: 6 Linguagem: Inglês
10.2903/j.efsa.2021.6676
ISSN1831-4732
AutoresSøren Saxmose Nielsen, Julio Álvarez, Dominique Bicout, Paolo Calistri, Klaus Depner, Julian Ashley Drewe, Bruno Garin‐Bastuji, José Luis Gonzales Rojas, Christian Gortázar, Mette Herskin, Virginie Michel, Paolo Pasquali, Helen Clare Roberts, Liisa Sihvonen, H.A.M. Spoolder, Karl Ståhl, Antonio Velarde, Christoph Winckler, Sandra Blome, Anette Boklund, Anette Bøtner, Sofie Dhollander, Cristina Rapagnà, Yves Van der Stede, Miguel Ángel Miranda Chueca,
Tópico(s)Viral Infections and Immunology Research
ResumoEFSA JournalVolume 19, Issue 6 e06676 Scientific OpinionOpen Access Research priorities to fill knowledge gaps in the control of African swine fever: possible transmission of African swine fever virus by vectors European Food Safety Authority (EFSA), Corresponding Author ahaw@efsa.europa.eu Correspondence:ahaw@efsa.europa.euSearch for more papers by this authorSøren Saxmose Nielsen, Search for more papers by this authorJulio Alvarez, Search for more papers by this authorDominique Joseph Bicout, Search for more papers by this authorPaolo Calistri, Search for more papers by this authorKlaus Depner, Search for more papers by this authorJulian Ashley Drewe, Search for more papers by this authorBruno Garin-Bastuji, Search for more papers by this authorJose Luis Gonzales Rojas, Search for more papers by this authorChristian Schmidt, Search for more papers by this authorMette Herskin, Search for more papers by this authorVirginie Michel, Search for more papers by this authorPaolo Pasquali, Search for more papers by this authorHelen Claire Roberts, Search for more papers by this authorLiisa Helena Sihvonen, Search for more papers by this authorHans Spoolder, Search for more papers by this authorKarl Stahl, Search for more papers by this authorAntonio Velarde, Search for more papers by this authorChristoph Winckler, Search for more papers by this authorSandra Blome, Search for more papers by this authorAnette Boklund, Search for more papers by this authorAnette Bøtner, Search for more papers by this authorSofie Dhollander, Search for more papers by this authorCristina Rapagnà, Search for more papers by this authorYves Van der Stede, Search for more papers by this authorMiguel Angel Miranda Chueca, Search for more papers by this author European Food Safety Authority (EFSA), Corresponding Author ahaw@efsa.europa.eu Correspondence:ahaw@efsa.europa.euSearch for more papers by this authorSøren Saxmose Nielsen, Search for more papers by this authorJulio Alvarez, Search for more papers by this authorDominique Joseph Bicout, Search for more papers by this authorPaolo Calistri, Search for more papers by this authorKlaus Depner, Search for more papers by this authorJulian Ashley Drewe, Search for more papers by this authorBruno Garin-Bastuji, Search for more papers by this authorJose Luis Gonzales Rojas, Search for more papers by this authorChristian Schmidt, Search for more papers by this authorMette Herskin, Search for more papers by this authorVirginie Michel, Search for more papers by this authorPaolo Pasquali, Search for more papers by this authorHelen Claire Roberts, Search for more papers by this authorLiisa Helena Sihvonen, Search for more papers by this authorHans Spoolder, Search for more papers by this authorKarl Stahl, Search for more papers by this authorAntonio Velarde, Search for more papers by this authorChristoph Winckler, Search for more papers by this authorSandra Blome, Search for more papers by this authorAnette Boklund, Search for more papers by this authorAnette Bøtner, Search for more papers by this authorSofie Dhollander, Search for more papers by this authorCristina Rapagnà, Search for more papers by this authorYves Van der Stede, Search for more papers by this authorMiguel Angel Miranda Chueca, Search for more papers by this author First published: 21 June 2021 https://doi.org/10.2903/j.efsa.2021.6676 Requestor: European Commission Question number: EFSA-Q-2020-00429 Panel members: Julio Alvarez, Dominique Joseph Bicout, Paolo Calistri, Klaus Depner, Julian Ashley Drewe, Bruno Garin-Bastuji, Jose Luis Gonzales Rojas, Christian Gortazar Schmidt, Mette Hersink, Virginie Michel, Miguel Angel Miranda Chueca, Paolo Pasquali, Søren Saxmose Nielsen, Helen Clare Roberts, Liisa Helena Sihvonen, Hans Spoolder, Karl Stahl, Antonio Velarde, Arvo Viltrop and Christoph Winckler. Declarations of interest: The declarations of interest of all scientific experts active in EFSA's work are available at https://ess.efsa.europa.eu/doi/doiweb/doisearch. Acknowledgments: AHAW Panel wishes to thank the Trainee Eleonora Chinchio for her work on the references (AHAW team, ALPHA unit, EFSA). Adopted: 5 May 2021 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 onEmailFacebookTwitterLinked InRedditWechat Abstract The European Commission requested that EFSA provide study designs for the investigation of four research domains according to major gaps in knowledge identified by EFSA in a report published in 2019: (i) the patterns of seasonality of African Swine Fever (ASF) in wild boar and domestic pigs in the EU; (ii) the epidemiology of ASF in wild boar; (iii) survival of ASF virus (ASFV) in the environment and (iv) transmission of ASFV by vectors. In this Scientific Opinion, the fourth research domain on ASFV transmission by vectors is addressed. Eleven research objectives were proposed by the EFSA working group and broader ASF expert networks, such as ASF stop, ENETWILD, VectorNet, AHAW network and the AHAW Panel Experts. Of the 11 research objectives, six were prioritised based on the following set of criteria: (1) the impact on ASF management; (2) the feasibility or practicality to carry out the study; (3) the potential implementation of study results in practice; (4) a possible short time-frame study (< 1 year); (5) the novelty of the study and (6) if it was a priority for risk managers. The prioritised research objectives were: (I) Studies on the potential vector fauna at the pig–wild boar interface and the feeding preference of blood-feeding potential vectors in ASF-affected areas; (II) Assessment of the efficacy of insect screens on indoor/outdoor pig holdings to prevent the entry of blood-sucking vectors (i.e. Stomoxys) in ASF endemic areas; (III) Assess the role of mechanical vectors in the virus transmission in ASF-affected areas; (IV) Distribution of the potential mechanical transmission vectors in ASF-affected areas of the EU; (V) ASFV transmission by synanthropic birds; and (VI) Assessment on the presence/absence of the soft tick Ornithodoros erraticus in ASF-affected areas in Europe. For each of the selected research objectives, a research protocol has been proposed considering the potential impact on ASF management and the period of 1 year for the research activities. Summary This Scientific Opinion follows up on a Scientific Report published in 2019 by EFSA titled 'Research gap analysis on African swine fever'. That Scientific Report provided a review of the most significant African swine fever (ASF) knowledge gaps as perceived by the EU Veterinary Services and other stakeholders involved in pig production and wild boar management. The aim of that Scientific Report was to identify gaps in knowledge that could improve short-term ASF risk management once addressed, and to facilitate evidence-informed decision-making on ASF prevention and spread. Based on this report, the European Commission requested EFSA to provide study designs to investigate four research domains according to major gaps in knowledge identified by EFSA in the report published in 2019: (i) the patterns of seasonality of ASF in wild boar and domestic pigs in the EU; (ii) the epidemiology of ASF in wild boar; (iii) survival of ASF virus (ASFV) in the environment and (iv) transmission of ASFV by vectors. In this Scientific Opinion, the fourth research domain is addressed, focussing on the potential of ASFV transmission by vectors. To address the fourth ASF research domain on ASFV transmission by vectors, 11 specific research objectives were proposed by the working group and broader ASF expert networks, such as ASF stop, ENETWILD, VectorNet, AHAW network and the AHAW Panel Experts. Of the 11 research objectives, six were prioritised and elaborated into a general protocol/study design research proposal, namely: (1) Studies on the potential vector fauna at the pig–wild boar interface and the feeding preference of blood-feeding potential vectors in ASF-affected areas; (2) Assessment of the efficacy of insect screens on indoor/outdoor pig holdings to prevent the entry of blood-sucking insects (i.e. Stomoxys) in ASF endemic areas; (3) Assessment of the role of mechanical vectors in the virus transmission in ASF-affected areas; (4) Distribution of the potential mechanical transmission vectors in ASF-affected areas of the EU; (5) ASFV transmission by synanthropic birds; and (6) Assessment on the presence/absence of the soft tick Ornithodoros erraticus and other potential vectors of the genus Ornithodoros in ASF-affected areas in Europe. For each of the selected research objectives, a research protocol has been proposed considering the potential impact on ASF management and the period of one year for the research activities. 1 Introduction 1.1 Background and Terms of Reference as provided by the requestor African Swine Fever (ASF) is an infectious lethal disease affecting domestic pigs and wild boar. It can be transmitted via direct animal contact, dissemination of contaminated food or equipment and, in some regions, via biological vectors. This disease has serious economic implications for pig meat production and related sectors, including indirect costs related to trade restrictions. The persistence of the disease in wild boar and the limited number of control measures available represents a challenge for the pig-breeding sector in the EU, in particular for the pig farming industry. There is no licensed vaccine or cure despite active ongoing research. From the beginning of 2014 up to now, ASF has been notified in the following EU Member States: Belgium (officially free again since October 1, 2020), Bulgaria, the Czech Republic (free again since March 2019), Estonia, Germany, Greece, Hungary, Latvia, Lithuania, Poland, Romania and Slovakia. The disease has also been reported in Belarus, Moldova, Russia, Serbia and Ukraine, which creates a constant risk for all the Member States bordering with these third countries. The virus strains involved in this ongoing epidemic that started 2007 in Georgia, belong to genotype II. Apart from this, ASF virus strains of genotype I have been present in Italy (Sardinia only) since 1978. There is knowledge, legislation, scientific, technical, and financial tools in the EU to face properly ASF. In addition, Member States and the Commission are continuously updating the 'Strategic approach to the management of African Swine Fever for the EU' and the related legislation. On 27 August 2019, EFSA published a scientific report titled 'Research gap analysis on African swine fever.11 https://www.efsa.europa.eu/en/efsajournal/pub/5811 The Scientific Report provided a review of the most significant ASF knowledge gaps as perceived by the EU Veterinary Services and other stakeholders involved in pig production and wild boar management. The aim of this scientific report was to improve short-term ASF risk management and to facilitate evidence-informed decision making on ASF prevention and spread. Four major gaps were identified: 'wild boar', 'African swine fever virus (ASFV) survival and transmission', 'biosecurity', and 'surveillance'. The EU is in need to further address some of the major research gaps as identified by EFSA in the Scientific Report, in particular: 'wild boar' and 'ASFV survival and transmission' are crucial to practically implement risk management actions to prevent and control ASF. For this, it is necessary that EFSA complements its previous Scientific Report providing new scientific input and technical assistance to the Commission on those crucial topics identified by the stakeholders as perceived major research gaps and suggests additional studies to fill the knowledge gaps. 1.2 Terms of Reference (TOR) In accordance with Article 29 of Regulation (EC) No 178/2002, EFSA is requested to provide a Scientific Opinion addressing the following three TORs: Design studies needed to evaluate: (i) the impact of reducing the wild boar population densities in relation to transmission of African swine fever virus (ASFV); (ii) the natural behaviour of wild boar to improve effectiveness of wild boar population management. EFSA should assess feasibility and provide support to design studies, or pilot trials, to verify suitability of new methods for wild boar population control such as immunocontraception (as a tool for population and health control of wild boar) and any other methods, including diverse types of hunting. EFSA should base the Scientific Output or Scientific Technical report on previous EFSA works on this subject and review existing literature, data and information to identify effective methods to reduce and to manage effectively wild boar populations. Design studies needed to understand: (i) the role and impact of vectors, in particular arthropod vectors, in ASF transmission (biological and mechanical); (ii) ASF survival and transmission from contaminated environment and (iii) residual infectivity of buried wild boar carcasses, all this assessing its overall [relative] role in the epidemiology of ASF. EFSA should provide the state of the art of what is known and base the Scientific Output, or Scientific Technical report, on previous EFSA works on this subject. EFSA should review existing literature, data and information to investigate the role of vectors and of the environment to clarify the pathways that facilitate ASF persistence and transmission in affected areas over a number of years. Design studies to investigate the patterns of seasonality in wild boar and domestic pigs and identify main factors that determinate these patterns. Provide recommendations in particular in relation to risk mitigation options to address these factors, where relevant. EFSA should focus again its analysis on the European experience. EFSA should investigate if seasonal patterns differ across different areas (e.g. temporal spatial increase of already infected areas or seasonality of the so-called 'jumps'). 1.3 Interpretation of the Terms of Reference To facilitate the assessment, the three TORs were interpreted and divided into four general research domains (RD) according to their aim: Wild boar management measures with the objective to reduce or stop the spread of ASFV; TOR 1 i) and ii). Potential of ASFV transmission by vectors (including arthropod vectors and scavengers; TOR 2 i). Potential survival of ASFV in the environment; TOR 2 ii) and iii). Possible factors that determine seasonality of ASF in wild boar and/or domestic pig populations; TOR 3. Each of the four research domains is assessed in a separate Scientific Opinion sharing the same methodology. This Scientific Opinion answers to research domain 2 (TOR 2), in particular the assessment identifies and prioritises research that could address the knowledge gaps pertaining the potential of ASFV transmission by vectors. These vectors may be biological or mechanical vectors. The latter could be arthropods, synanthropic birds and/or other scavengers. 2 Methodologies To identify, prioritise and develop the guidelines for the studies needed to address the knowledge gaps about the role of vectors (biological and mechanical) in ASF transmission (TOR 2; RD 2), a methodology including four steps was applied. Step 1 consisted in the identification of the research objectives by the experts of the EFSA working group (WG), followed by Step 2, where the list of research objectives produced by the WG was circulated among different expert networks that were also able to provide inputs to the list of research objectives. Step 3 consisted in the review of all provided information and prioritisation of the collected research objective by the criteria established by the WG. Finally, Step 4 consisted in the development of the guidelines for each of the research objectives, either by the WG or by external contractors. 2.1 Step 1: Identification of research objectives by working group Brainstorm session during a web conference of the working group to identify possible research objectives for each research domain (see Section 1.3). According to the interpretation of TORs, the following research domains (RD) were identified: Wild boar management measures with the objective to reduce or stop the spread of ASF. Potential of ASFV transmission by vectors. Potential survival of ASFV in the environment and in buried carcasses. Possible factors that determine seasonality of ASF in wild boar and/or domestic pig populations. For each RD, specific research objectives were identified and discussed. For each research objective, a brief description was provided, focusing on the main aim of the research regarding ASF management. In addition, keywords were defined by the WG to facilitate identification of research objectives. Contributions by each individual working group member to the results generated during the brainstorm session A table for each of the four RD was circulated among the WG members. Each WG member worked separately on-line on the table and proposed all research objectives considered to be of interest for the particular research domains that could be achieved in a relatively short timeframe (i.e. less than a year). Thereafter, proposals for each research objective were discussed during a web conference among all WG members. Overlapping research objectives were identified and amended in agreement with the WG. The final version of the table with research objectives was agreed among WG members and prepared to be circulated among networks. 2.2 Step 2: Identification of research objectives by broader networks An online survey (Annex A) based on the table produced by the WG was distributed to the following networks of experts: ASF stop, ENETWILD, VectorNet, AHAW network and the AHAW Panel Experts. The experts in the networks had 2 weeks to complete the survey online, using the same tables of the RD and their research objectives developed by the WG. The WG conducted an analysis of the survey results, identifying new potential objectives and merging overlapping ones. The research objectives selected for the final list, which combined the research objectives suggested by the WG and networks were then prioritised according to procedure explained in Section 2.3. 2.3 Step 3: Prioritisation of research objectives Inclusion criterion: The research objectives proposed by the working group and the different networks were included if they were related to the particular domain of research. In the case of this Scientific Opinion, the inclusion criterion was: Is the research objective related to the possible ASFV transmission by vectors (including arthropod vectors and scavenger birds) (Research Domain 2)? If the answer to this question was 'YES', the research objective was included; if it was 'NO', the research objective was excluded. Apply scoring criteria for each research objective according to the criteria listed in Table 1. The working group scored the research objectives proposed by the working group and the different networks using the scoring criteria provided in Table 1. Each member of the WG scored independently from each other the different research objectives. The different criteria for ranking the priority of the research objectives and their definitions were discussed and agreed with the requestor of the mandate (the European Commission). For each criterion, a simplified 5 point Likert scale of either 1 (low), 3 (medium) or 5 (high) was given per research objective according to Table 1. Likert scales are commonly used method to rate people's opinions or perceptions on importance or priorities (Joshi et al., 2015). For each scoring criterion provided, each of the WG members provided a rationale that was discussed afterwards, collectively, during another on-line meeting. Only criterion 6 (priority for the risk managers) was scored by one person, the liaison of the European Commission, who attended the working group. A few criteria were not scored by all working group members, but the group scoring was provided by calculating the average of the group, as shown in Annex A and discussed and agreed upon by the whole working group. The overall average score for each RO, estimated including all scores for all criteria, was selected to estimate central tendency (of the perception of priority of the working group) as a measure for the general opinion of the WG. This ensured that the overall score reduced extreme values in each criterion scoring that may have arisen due to different expertise and/or experience of the WG members. To ensure that proposed ROs (fulfilled the prioritisation requirements mentioned in Table 1, a minimum average score of 3.5 (70% of the maximum score) was agreed a priori by the working group as the cut-off for a research objective to be further developed into a protocol. A limitation of this approach is that the average score for each RO is very sensitive to small variations in scoring: this is due to the small number of scores, and the limited range of possible scores (only scores of either 1, 3 or 5 could be chosen). However, a consensus was reached in all cases on the average values of the scores and the WG discussed and agreed with the omission of those proposals that did not reach the score of 3.5. The standard deviation and the coefficient of variation were given to show the uncertainty in the initial judgements by the experts on the criteria for each of the objectives (Annex A). Table 1. Criteria for prioritising research objectives No. Criterion High = 5 points Medium = 3 points Low = 1 point 1 Impact on ASF management The results can have a high impact on the practical management of the disease spread. The topic is part of or is included in one or more of the main strategies for ASF control. The results can have a medium impact on the practical management of the disease spread.The topic is part of, or includes, one or more of the secondary strategies for ASF control. The results can have a low impact on the practical management of the disease spread. The topic is not included in any of the main or secondary strategies for ASF control. 2 Feasibility or practicality to carry out the study Low complexity, methodology fully available Medium complexity, methodology available but needs further development High complexity methodology needs to be fully developed 3 Potential implementation of study results in practice Results can be easily implemented in a short time in the current management of ASF Results could somehow be implemented in a short time in the current management of ASF Results are not easily implemented in a short time in the current management of ASF 4 Short time frame study possible (1 year) The study can be completely carried out in 1 year Part of the study could be done in 1 year (i.e. 50% or more) The study cannot be completely carried out in 1 year (i.e. less than 50%) 5 Novelty: other studies carried out on the same topic? No previous studies available Few previous studies available High number of previous studies available 6 Priority for risk managers The research gap was perceived as important by the stakeholders (experts and risk managers) in the previous Gap analysis; experts and funding are available for the research objective and results will be useful in short term to manage the disease The research gap was less perceived as important by the stakeholders (experts and risk managers) in the previous Gap analysis; experts and funding are less available for the research objective and results will be less useful in short term to manage the disease The research gap was not perceived as important by the stakeholders (experts and risk managers) in the previous Gap analysis; experts and funding are not available for the research objective and results will not be useful in short term to manage the disease No.: number. 2.4 Step 4: Development of calls for research protocols for research priorities A short research protocol was developed for each of the ROs that at least scored 3.5/5 points on average (and was therefore considered as a research priority). These protocols could be used by research agencies or funding agencies as a call for research proposals. The development of the research protocol has been outsourced to experts of the Vectornet Consortium and further discussed and elaborated by the WG. Thereafter, it was reviewed by the Panel on Animal Health and Welfare of EFSA. They can be found in Sections 3.4–3.10. These protocols should have the following minimum components: Outline of the research protocol for the prioritised research objectives (3–5 pages per protocol) Introduction o Summary of what is known on topic up to date, and identification of the research gap(s) o Potential impact on ASF control if the gaps of knowledge were to be filled Objectives o Research hypotheses Methodology o Study design o Suggestions for statistical analysis Deliverables and milestones 3 Assessment 3.1 Step 1: Identification of research objectives by working group During the web meeting/brainstorming exercise and further consultation by email from the WG, six ROs were identified based on their experience (Table 2). Table 2. Identification of research objectives by the WG for Research Domain 2: studies focusing on potential ASFV transmission by vectors No. Research objective Short description Keyword 1 Assess the role of mechanical vectors in the virus transmission in ASF-affected areas Screening by molecular diagnostic tools of blood feeders (i.e. Stomoxydae, Tabanidae, Culicidae, Ceratopogonidae, Ixodidae) and non-blood feeders (i.e. Muscidae, Calliphoridae) as potential mechanical vectors in ASF-affected areas. Apart of virus genome detection, virus persistence and transmission test in laboratory are also recommended considering both vector biting activity and vector ingestion by pigs (e.g. adult flies or ASFV-infected diptera larvae from carcasses). Recent study showed that infected O. erraticus after 2 months frozen is able to infect pigs when ingested with food. Range of action should be taken into consideration (pen/barn/region). Role of mechanical vectors 2 Assess the vector competence of potential biological vectors present in the EU Assessing the vector competence of potential vectors in the EU. The role as biological vector has been assessed in laboratory for Ornithodoros erraticus (from Portugal) and O. verrucosus (from Ukraine) for the strains (Georgia2007/1 and Ukr12/Zapo) showing that both species failed to transmit the virus. On the other hand, vector competence of O. erraticus group for local ASFV strains was demonstrated in Portugal (Boinas, 1994). The relation between ASFV strains and vector transmission, as well as the role of other species of mammal soft ticks present in Europe and Ornithodoros spp. populations found in ASF-affected areas in Europe are still not well characterised. Role of biological vectors 3 Assessment of the efficacy of insect screens on indoor/outdoor pig holdings to prevent the entry of blood-sucking insects (i.e. Stomoxys) in ASF endemic areas Integrated pest management should include the use of physical barriers, insecticide impregnated nets, traps, insecticide treated, ground spraying as well other biosecurity measures in endemic areas. Assess the impact on non-target arthropods. Including impregnated targets and traps (similar as used for tse-tse flies), live baits (insecticide treated pigs and boars), etc. Barriers could be used between treated and untreated areas. Vector control 4 Assessment on the presence/absence of O. erraticus and other potential vectors of genus Ornithodoros in ASF-affected areas in Europe Transmission and persistence of ASFV in Europe can be related to the presence of the major vector species O. erraticus. Showing the presence/absence of proven vectors such as O. erraticus as well as other potential species within the genus Ornithodoros has important implication for the declaration of ASF free areas. Vector presence/absence and distribution 5 Assessment of ASFV vertical transmission in European Ornithodoros spp. Vertical transmission of ASFV has been described in Ornithodoros African species. It is still unknown if vertical transmission in European species can lead to the persistence of the virus in endemic/epidemic ASFV areas. Virus persistence, Vectors 6 Studies on the potential vector fauna in the pig–wild boar interface and the feeding preference of blood-feeding potential vectors in ASF-affected areas. Pig holdings and areas where wild boar habit may share same potential vector species. It is important to know if there are bridge species that can transmit the virus from one habitat to another. In addition, the feeding preference of blood-feeding potential mechanical vectors will also provide information about the possible link between wild boar and pig holding interface areas. Role of vectors, Pig wild boar interface 3.2 Step 2: Identification of research objectives by broader networks In addition to the research objectives proposed by the WG (Table 2), two research objectives (7 and 8) were proposed by broader expert networks (Table 3). In addition to them, three research objectives (9, 10 and 11), originally proposed under RD 3 dealing with ASF survival (ASFV tra
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