African swine fever eradication: The Spanish model Marisa Arias and José Manuel Sánchez-Vizcaíno $a$ Summary This chapter reviews the Spanish African

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1 African swine fever eradication: The Spanish model Marisa Arias and José Manuel Sánchez-Vizcaíno $a$ Summary This chapter reviews the Spanish African swine fever (ASF) eradication program (1985 to 1995). Since no vaccine was available, the program was primarily based on the detection of ASF positive and carrier animals by laboratory diagnosis and the enforcement of strict sanitary measures. The key components of the program included: 1) a network of mobile veterinary field teams responsible for the control and diagnosis of the disease; 2) serological testing of animals; 3) improvements in hygiene within production facilities; 4) elimination of all ASF outbreaks and identification and slaughter of carrier animals; and 5) veterinary control of all swine movement, with individual identification of every animal moved for fattening or breeding purposes. In 1995, Spain was declared free of ASF. At present, Spain is the second largest swine-producing country in the European Union with a total pig population of 22,435,000 animals and 2,478,000 breeding sows. $a$ Introduction African swine fever (ASF) is a highly contagious viral disease of swine and of such concern that it is included among the List A diseases by the Office International des Epizooties (OIE). The disease causes significant economic losses in affected countries due to the high mortality rates associated with the acute and peracute forms. In addition, it is recognized as possessing the potential for extensive and rapid spread at international levels. Such an occurrence would have important socio-economical consequences in the international trade of animals and swine products. Domestic pigs and European wild boars are very susceptible and infection produces a wide range of clinical forms: acute, subacute, chronic, and subclinical (Arias et al. 1986; Sánchez- Vizcaíno 1999). African wild boars, bushpigs (Potamochoerus porcus), and warthogs (Phacochoerus aethiopicus), are very resistant to the disease, present inapparent infections, and

2 serve as reservoir host in Africa (Heuschele and Coggins 1965). Soft ticks, especially Ornithodoros erraticus and Ornithodoros moubata, act as reservoirs and transmission vectors of ASF virus (Sánchez-Botija 1963; Plowright et al. 1970). African Swine Fever was confined to Africa until the end of the 1950 s when it appeared in Portugal in 1957 from Angola. It subsequently spread to other European countries: Spain in 1960, France in 1964, Italy in 1967, 1969, and 1993, Belgium in 1985, and the Netherlands in Between 1978 and 1980 ASF appeared in several American countries: Brazil, Cuba, the Dominican Republic and Haiti. In the latter two countries, ASF was successfully eradicated by stamping out all the pigs on the island of Hispaniola. In Europe, the disease remained endemic in Portugal and Spain for decades until 1994 and 1995 when both countries were declared ASF free. In November 1999, ASF appeared again in the Alentejo, Portugal but was successfully eradicated (OIE information). Currently, ASF is primarily present in sub-saharan countries of Africa. It has acquired a greater importance since 1997 because of increased outbreaks in Angola, Benin, Botswana, Cameroon, Cape Verde, Ghana, Madagascar, Malawi, Mozambique, Namibia, Nigeria, Senegal, Togo, Uganda, and Zambia. In these countries, ASF is maintained by a cycle of infection between wild boars (reservoir) and soft ticks (vector) with transmission to domestic pigs. This vector-borne cycle of transmission makes eradication difficult. Outside of Africa, ASF is only present in Sardinia (Italy), in which carrier wild boars and domestic pigs recovered from the ASF virus (ASFV) infection are believed to play a role in maintaining the disease. $a$ ASF eradication program in Spain Since there is no vaccine against ASF, the Spanish eradication program (1985 to 1995) was based on the detection of ASFV-infected animals by laboratory diagnosis and the enforcement of strict sanitary measures. In the final stages of the program, a new Coordinated Program was prepared jointly with Portugal in order to intensify the fight against ASF in the southwestern

3 portion of the Iberian Peninsula, the last remaining infected area. In 1995 Spain was declared free of the disease. $a$ History and epidemiological situation In 1960, when ASF appeared in Spain, it spread within what was essentially an undeveloped sector. During the 1960s, as the Spanish economy began to take off, a marked change took place in pig production. In a few years Spain went from family-type holdings to an industrial organization characterised by intensive swine production systems, the incorporation of European breeds, and the use of new handling techniques. Pig production, which until then had been located mainly in the south and southwest and operated as outdoor production systems, began to be carried out in industrial farms that were found mainly in six regions. Galicia, Castilla, León, and Murcia specialised in the production of piglets, and Aragón, Cataluña, and Segovia in large feeding farms. This situation resulted in the extensive movement of livestock within the Spanish territory. In 1960, the virus spread widely in certain areas of the country. Initially, the usual picture of ASF was acute clinical signs and high mortality. This changed through the years to an endemic disease characterised by mild to subclinical forms and a mortality rate below 5% in infected herds. Thereafter, confirmation of the disease by laboratory diagnosis was required. In addition, the virus also could be transmitted by the soft tick vector, Ornithodoros erraticus, found in certain southwestern areas where the disease was endemic and where the outdoor production of Iberian pigs was located. In spite of ASF, the pork-producing sector experienced strong development and swine production increased from 6 million head in 1960 to 16.7 million in 1989 (1.9 million breeding animals), representing an increase of 178.3% from 1960 to 1989 (Bech-Nielsen et al. 1995). At this time, the sector employed 200,000 people, taking into account secondary industries, and produced nearly 1.2 million tons of meat. Of this, 50% was consumed as manufactured products, of which cured products constituted 45% - a very high percentage compared to the European

4 countries. On the whole, the contribution of the pig industry to the total annual agricultural production was million pesetas (1.4 million Euros). Only export restrictions restrained significant development of the Spanish pig sector. The ASF imposed economic hardships on pig producers and created barriers to intra-community trade in live pigs, fresh pig meat, and certain pork products. Furthermore, ASF control measures produced great economic costs to the Spanish administration. An analysis of the effort to control ASF in Spain in the year 1983 estimated costs at 1900 million pesetas (11.4 million Euros). The Spanish administration, aware of the situation, established a Coordinated Program to eradicate ASF in Spain (Royal Decree 425/1985) in March It was approved in its totality and provided an initial financial support of 7200 million pesetas (more than 43 million Euros) by the European community (Council decision 86/650/EEC). $a$ Key actions of the eradication program The new regulations introduced the following: 1) A network for the control and diagnosis of the disease implemented by mobile veterinary field teams (127) exclusively dedicated to the program. The field teams worked in the sanitary control of holdings, animal identification, epidemiological surveys, sample collection for the serological surveillance of breeders, serological control at slaughterhouses, epidemiological investigations, and they also promoted and encouraged pig producers to create Sanitary Associations. 2) Serological surveillance of 100% of the pig farms. To achieve this goal, it was necessary to put into place a simple, fast, accurate, and specific diagnosis test and a reference laboratory to harmonise the techniques to be used in regional and province laboratories. The indirect ELISA was selected as the best assay for obtaining a rapid and reliable diagnosis of the disease (Sánchez-Vizcaíno et al. 1982). The Department of Animal Health of the Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) became the National Reference Laboratory. At present this is known as CISA-INIA, the ASF

5 reference laboratory for the OIE and the European Union. At the beginning of the program, the regional laboratories used the indirect ELISA to screen samples and an indirect fluorescent antibody (IFA) assay to confirm results. In the final stages, the National Reference Laboratory of INIA developed an improved ELISA based on a new soluble antigen that contained all the ASFV proteins (Sánchez-Vizcaíno 1986). This allowed better recognition of carrier animals. In addition, an immunoblotting assay was developed as a serologic confirmatory test in place of the IFA (Pastor et al. 1989; Arias and Sánchez-Vizcaíno 1992). This assay allowed easier and more objective interpretation of results and a better recognition of weak-positive samples. The virological studies for the detection of new outbreaks were carried out at the National Reference Center. A total of 13 regional laboratories were involved in serologic surveillance during the eradication program (actually there are 39 laboratories located in the 17 Autonomous Communities). In order to assure the quality and reliability of results, these laboratories received the reagents required to perform the serological assays from the National Reference Center. 3) Improvements in animal holding facilities. The primary objective was to improve sanitary barriers to prevent the spread of the disease. This involved adoption of basic measures of hygiene including: fences, sanitary enclosures, safe disposal of manure, etc. For this purpose it was possible to obtain funds to cover part of the investment or loans at low interest rates. More than 2,175 holdings were improved between 1985 and ) Elimination of all ASF outbreaks, euthanasia of ASFV carriers, depopulation of infected herds. As soon as the National Reference Laboratory confirmed an outbreak of ASF, all pigs in the infected holdings had to be killed immediately. Sample collection for virological and epidemiological investigations was also performed (case report). The responsible authorities arranged immediate and adequate compensation to be paid to the pig producers of the infected holdings, in compliance with the

6 relevant legislation. Once the outbreak was identified, depopulation by killing all the pigs in the affected herd was initiated and additional measures were also adopted. The buildings underwent complete cleaning and disinfection about one month after depopulation. This included insect and rodent extermination and the removal and destruction of all animal feed, animal products, and thorough cleansing of manure pits using 2% sodium hydroxide, as well as the incineration of straw bedding at the pig holding facility. A sanitary zone of a few hundred meters radius was designated in and movement of animals, animal products, animal feed, and waste into or out of the sanitary zone and the movement of people to and from the area was restricted. The restrictions in the sanitary zone were gradually eased although some specific biosafety measures were maintained for at least 3 months. After complete cleaning and disinfection ASF seronegative sentinel animals were introduced in the holding and taken through all the facilities. The number of sentinel pigs was usually equivalent to 10 to 20% of the population at the time when re-stocking was completed. If after a month they did not become sick, they were re-tested serologically. If the results were negative, the authorities allowed the repopulation of the farm, with identified animals from a health status-controlled farm. Re-stocking procedures were usually completed within 3 months following the entry of sentinel pigs. On holdings known to be infested with Ornithodoros erraticus, no re-stocking could take place unless special arrangements were made after consultation with the Central Veterinary Administration. Biosafety and sanitary measures developed to avoid transmission of the virus between herds played an important role in the eradication of the disease. Reports on sources of ASF outbreaks collected through epidemiological investigations indicated that 84% and 93% outbreaks in 1989 and 1990 respectively, listed neighbour contact as the most likely source of the outbreak (Bech-Nielsen et al. 1995).

7 $a$ Restricted Areas A protection and a surveillance zones were established upon confirmation of an outbreak. The radius of the zones depended on the initial findings of the epidemiological investigation, but the protection zone had a radius of at least 3 km and the surveillance zone a radius of 10 km. Pigs kept on all holdings situated within the protection zone were serologically screened immediately after an outbreak was confirmed. Further screenings in the 3-km and 10-km zones were done not sooner than 30 days after the preliminary cleaning and disinfection of the infected holding was completed. Movement of live pigs within the zones were prohibited for 30 days, but this limitation could be lifted after completion of serological tests proved that the area was negative. Live pigs could not be move out of the zones. The traffic police and other competent authorities carried out the control of movement of animals. $a$ Livestock movement and animal identification Livestock movement was strictly controlled. Vehicles were required to be properly washed and disinfected. Animals in transit, which had been previously identified, required an official veterinary certificate stating their origin and sanitary situation. At all times, program administrators retained authority over transportation of animals and their destination (abattoir or breeding farm). When pigs arrived at an abattoir, the official veterinarian checked the sanitary certificate prior to slaughter. In addition, live animals were inspected ante mortem and tissues post mortem. The abattoir retained the sanitary certificate for at least one year following slaughter. Throughout the process, manufacturers retained identification of the origin of the meat from the moment of the arrival of the animal to the final manufactured product. All of these direct measures worked together with others, such as an improved producer registry, a census of pig holdings, a list of infected farms, and an annual report of the program development. However, all of these measures would have been useless without the direct involvement and the active

8 participation of the farmers. Thanks to a wide publicity campaign in the mass media and on the radio, primarily directed to the rural environment, the pig producers became aware of the need to fight against the ASF. The pig producers created associations for sanitary defence (Health Protection Group) and took a leadership role in the eradication program. The associations were originally started by a group of farmers who voluntarily adopted, at the municipal level, a common approach against ASF. These farmers maintained serological surveillance of breeders and the correct sanitary infrastructures. They maintained sanitary programs suitable for ASF and other pig diseases and received important aid from the administration. In 1990, more than 979 associations had been created in Spain that included over 41,321 farmers and 922,996 breeding animals. A registry was created with the aim of classifying holdings in accordance with the health status of the pig herd, the facilities for on the holding, and the different type of farms: holdings with confirmed health status, holdings with special health protection, and holdings free of African swine fever located in the free area. $a$ The eradication program evolves into regionalization As a result of the progress of the eradication program, in December 1989 the European Community Council (EEC) adopted a new rule. This Decision (89/21/EEC) divided Spain into two regions: an ASF-free region and an ASF-infected region. Regionalization lifted the prohibitions on trade in certain areas in Spain and allowed the trade in live pigs, fresh pig meat, and certain meat products from the free areas to other European countries. The free region, in which the last outbreak was recorded in 1987, covered the largest part of the country and included about 70% of the pig population of Spain. The infected region covered complete or partial areas of the provinces of Salamanca, Cáceres, Badajoz, Huelva, Córdoba, Sevilla, Cádiz, and Málaga (Figure 1, Decision 89/21/ECC). Figure here African swine fever in Spain to 1993

9 Since 1990, no outbreaks of clinical disease were recorded in certain parts of the infected region, although serological evidence of ASFV was observed in certain herds (in a very few animals). Progressively, new divisions of the Spanish territory were established: a free area, a surveillance area adjacent to the Portuguese border that included parts of the provinces of Salamanca, Cáceres, Badajoz, Cádiz, and Málaga, and an infected area that covered a small part of the southwest of the country and included the province of Huelva and parts of Córdoba and Sevilla. Outbreaks continued in the infected area until 1993 (Figure 1, Decisions: 91/112/ECC and 93/443/ECC). In the infected area, virus persistence was primarily due to the following factors: production facilities lacking basic sanitation and biosafety features; the presence of soft ticks, Ornithodoros erraticus, that acted as ASFV vectors; and the presence of an uncontrolled wild boar population. Figure here African swine fever in Spain - final stages of the eradication program At that juncture, new measures were put into place. This included a specific serological screening program as follows: In the free area, serological sampling of 5% of the national sow herd and wild boar population was required each year. Samples were collected mainly from areas adjacent to surveillance and infected areas and from herds in the vicinity of abattoirs authorised to kill pigs originating from the surveillance area. Wild boars killed during hunting in areas at risk were also screened. In the surveillance area: a) in each breeding herd, 30% of the breeding animals were tested each year; b) in farms using open or mixed production systems, 50% of the breeding animals in all herds were tested each year; c) pigs greater than 40 kg in weight had to be tested once. The sampling could be increased by a factor of two in the case of herds where carrier animals had been identified during the previous six months, or in areas where

10 evidence of ASF in the wild boar population had been found. In the infected area: a) 30% of breeding animals from breeding farms had to be serologically screened twice each year; b) in farms using open or mixed production systems, 50% of the breeding animals in all herds were tested every six months with sampling performed in such a way that every breeding animal was tested at least once per year; c) Pigs greater than 40 kg in weight had to be tested once each year; d) wild boars killed by hunting had to be examined for ASFV by virological and serological techniques. In addition, special measures were implemented in the surveillance and infected areas. These included the destruction of the unsanitary animal production facilities, serological surveillance by ELISA of pigs at risk of being bitten by ticks (Canals et al. 1990), and construction of metal fences of about 100 meter radius around the animal facilities with historic value or good sanitary conditions to avoid the contact with feral animals. $a$ Finale the coordinated program on the Iberian Peninsula In 1994, the epidemiological situation presented the need to join efforts with Portuguese authorities to eradicate ASF from the remaining infected areas located on the Spanish side of the border between the two countries. The last outbreaks in Portugal, in 1993, had been located in the Alentejo area (Portuguese border) in which mixed production systems were common. In June 1994, a coordinated program to eradicate ASF from the remaining infected areas of the Iberian Peninsula was arranged with the approval of the European Community (EC). Between July 1994 and December 1996, the EC funded 50% of the cost of serological testing, slaughter, and destruction of pigs, cleaning and disinfection, and epidemiological investigations of ticks and wild boars, up to a maximum of 7,210,000 Euros. This program involved the member states of the EC and the Commission, and pig producers, the pig meat industry, and the authorities of Spain and Portugal. Furthermore, the program established different National Committees and Monitoring Centers, as well as an

11 Advisory board that was responsible for supervising the eradication program. The program consisted of a number of health status areas: free area, surveillance area, and an infected area in Spain and a monitoring area in Portugal. The evolution of this coordinated eradication program is showed in Figure 2 (Decision 94/476/EC; 94/788/EC; 94/887/EC; 95/300/EC). $a$ ASF eradication - final remarks The methods used to eradicate ASF in Spain involved a great effort on the part of the Agriculture Ministry, primarily due to the need to create the necessary infrastructure and because of the need for highly qualified personnel. Coordination with the Spanish Regional Communities was also an important factor in the successful outcome of the program. Since 1987, no new outbreaks of ASF appeared in the areas that used confined production systems (about 96% of Spanish territory). In these regions, ASF eradication was easier and faster because of the absence of vectors or wild boars, compared to those using open swine production systems, in which ASF eradication was particularly difficult. Beginning in 1987, ASF outbreaks only appeared in specific southwestern areas of the country, i.e., in the regions of Salamanca, Sevilla, Córdoba, Huelva, Cádiz, and Málaga. As a consequence of the increased control and intensification of the effort in the provinces that were still affected, together with the Spanish-Portuguese Coordinated Program, since 1994 no new outbreaks have appeared anywhere in Spain. It should be noted that vaccine was not essential for ASF eradication, even in endemic areas. In December 1995, Spain was declared officially free of the disease. At present Spain is ranked as the second largest pig producing country in the European Union with a total pig population of 22,435,000 animals and 2,478,000 breeding sows. Acknowledgments We would like to thank the Dirección General de Ganadería from the Ministerio de Agricultura, Pesca y Alimentación of Spain for its help and support in preparing this review. $a$ References

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