Classical swine fever: the global situation - UFRGS

Veterinary Microbiology 73 (2000) 103±119

Classical swine fever: the global situation Steven Edwardsa,*, Akio Fukushob, Pierre-Charles LefeÁvrec, Andrzej Lipowskid, Zygmunt Pejsakd, Paulo Roehee, Jùrgen Westergaardf a

Veterinary Laboratories Agency, Weybridge, New Haw, Addlestone, Surrey KT15 3NB, UK b National Veterinary Assay Laboratory, Tokyo, Japan c Ministere de l'Agriculture et de la Peche, Paris, France d National Veterinary Research Institute, Pulawy, Poland e Center for Veterinary Research `Desiderio Finamor', Porto Alegre, Brazil f Department of Veterinary and Zootechnical Legislation, European Commission, Brussels, Belgium

Abstract A historical and current perspective is given of classical swine fever and its impact on pig production in different regions of the world. Data were obtained from a variety of sources including returns to the Of®ce International des Epizooties, of®cial government reports, other published material and local information through personal contacts. The disease has been recognized for about 170 years and efforts to control it by of®cial intervention began in the nineteenth century. Despite this it remains a lingering problem in many parts of the world where it has both, an economic impact on swine production and a constraining effect on trade due to the measures necessary to prevent spread. # 2000 Elsevier Science B.V. All rights reserved. Keywords: Swine fever; Bovine viral

1. Introduction The supposed ®rst record of a disease in pigs corresponding to what we now know as classical swine fever (CSF) or hog cholera, was in 1833 in Ohio, USA. Hanson (1957) made it clear that this claim is not sustainable from the original evidence, and that the Ohio outbreak was only one among many in the USA in the early 19th century. Indeed, an epizootic resembling CSF was reported in France in 1822 (Birch, 1992; cited by Cole et al., 1962), which lends weight to the possibility that the disease may have been introduced *

Corresponding author. E-mail address: [email protected] (S. Edwards) 0378-1135/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 3 5 ( 0 0 ) 0 0 1 3 8 - 3

104

S. Edwards et al. / Veterinary Microbiology 73 (2000) 103±119

to America with pigs from Europe. Whatever the origin, the disease was widespread in Europe and America by the 1860s. The spread of the infection may have been facilitated by the development of railways during the mid-19th century (Birch, 1922). Transmission of the disease was demonstrated by bacteria-free ®ltrates (de Schweinitz and Dorset, 1903), while milestones in control of the disease were: the use of immunization by simultaneous antiserum and virulent virus in 1907 (Niles, 1910); the application of crystal violet inactivated vaccine in 1934 (McBryde and Cole, 1936); the use of attenuated live virus vaccines from 1951 (Cole et al., 1962); and, most recently, the development of subunit `marker' vaccines (van Rijn et al., 1996). Meanwhile, signi®cant advances in the laboratory diagnosis of CSF infection have been made with the recognition of its relationship to bovine viral diarrhoea virus (Darbyshire, 1960), the application of ¯uorescent antibody techniques to antigen detection (Mengeling et al., 1963), the use of ELISA for serology (Have, 1984), the development and application of monoclonal antibodies to the virus (Wensvoort et al., 1986) and the use of molecular technology for epidemiological investigation (Lowings et al., 1994) and diagnosis (McGoldrick et al., 1998). CSF is a serious, economically damaging disease of swine which can spread in an epizootic form as well as establish enzootic infections in domestic and wild pig populations. It is on the Of®ce International des Epizooties (OIE) List A. Most countries with signi®cant pig production have statutory control measures for the disease, although the ef®cacy of these measures varies in accordance with the national economy, and the state of development of veterinary and laboratory infrastructure. Although effective vaccines exist, they do not on their own bring about disease eradication. Any use of vaccine has to be done in the light of the consequences for the disease status of the country or region. The OIE de®nes the requirements for CSF-free status as follows (OIE, 1998): Absence of CSF for at least two years One year after slaughter of the last affected animal following a stamping out campaign with vaccination. Six months after slaughter of the last affected animal following a stamping out campaign without vaccination. At the end of the 20th century, CSF remains widespread in many parts of the globe (Fig. 1). Successful eradication has been achieved in many countries, including North America, Australasia, and parts of Northern Europe, and many such countries have successfully maintained freedom in the absence of vaccination, i.e. with a totally susceptible swine population. Despite this, complete eradication has proved elusive in parts of Europe and new approaches to control may be needed in the remaining infected regions. The situation in most of Africa is uncertain, but the disease is not reported as a problem there except in Madagascar. 2. America and the Caribbean 2.1. North and Central America Canada has been free of CSF since 1963. The of®cial eradication scheme in the USA started in 1961, the last case being recorded in 1976 (Wise, 1986). No further outbreaks


105

Fig. 1. Countries (shaded grey) reporting the occurrence of classical swine fever to OIE during the period 1995± 1998 (Source: OIE, 1999).

have occurred in Canada or the USA which must be attributable, at least in part, to a highly rigorous control policy for import of pigs and pig products to this region. Mexico can be divided into three areas in respect of CSF status: the northern states bordering the USA, together with the Yucatan Peninsula, are free of the disease, with no vaccination and a high degree of vigilance for any suspected outbreaks; the southern states are designated as a control area, i.e. with endemic infection and continued use of vaccination for control. There are particular dif®culties in the control area due to the high proportion of `backyard' pigs, a highly mobile pig population, and an inadequate level of vaccination. The central part of Mexico is the eradication area, where vaccination has been prohibited, stamping out is practised, and outbreaks have ceased. The aim is to extend the CSF-free area to include these states, once the appropriate period of freedom from disease has been achieved. In Central America, only Belize and Panama are free of the disease, and the rest of the area is endemically infected with control by vaccination. 2.2. Brazil Brazil has a vast territorial area (8,500,000 km2). The swine population is around 36 million head, much of it (about 12 million) concentrated in the more industrialized swine producing region, comprising the southern states of the country. The country is the sixth largest world producer of pork (ca.1.4 million tons per year). However, exports of Brazilian pork have been limited so far to about 40,000 tons per year. Large-scale vaccination against CSF with the lapinised chinese strain of CSF virus achieved control of the disease in the most intensive pig farming areas. This was supported by constant ®eld surveillance and laboratory monitoring of suspect cases. As a

106


consequence, no outbreaks of CSF have been observed in the three southern Brazilian states (Rio Grande do Sul, Santa Catarina and ParanaÂ) since 1988, apart from an isolated incident in 1997. This made national eradication an achievable goal and, in 1992, the National Programme for Control and Eradication of CSF was implemented (MAARA, 1992). As the country has such a vast territory, eradication of the disease in the whole federation in one step was neither technically nor economically viable. Therefore, the programme was designed ``to achieve eradication in a progressive way, starting from areas selected according to the importance of swine farming , and according to the epidemiological status of the disease within the area'' (MAARA, 1992). Thus, the country was subdivided into three areas. Area I comprised the three southern states which were free of the disease, and where vaccination was prohibited. Area II comprised states where CSF was still endemic and with a relatively large swine population, where vaccination was made compulsory. Area III comprised the rest of the country where swine farming was not industrially signi®cant, and where vaccination was not made compulsory. Apart from these measures, a private contingency fund, (sponsored by the swine industry and farmers) was created in each of the states within Area I to cover the costs of slaughter and other control measures in the event of an outbreak. CSF was absent from Area I until 1997, when an outbreak occurred in the state of ParanaÂ. However, the two other states in Area I were not affected. As the outbreak occurred in only one large pig-producing company, no vaccination was used. Immediate assistance to the focus, control of transit, disinfection and destruction of sick and suspect and in-contact animals, excreta and offals were carried out. Stringent movement restrictions and a slaughter policy within, and around, the outbreak were adopted. Since then, no other episodes of CSF have been detected within Area I. The favourable control situation led to the of®cial prohibition of CSF vaccination in the whole country, from 15 May 1998 (Ministry of Food and Agriculture, 1998). Only of®cially authorized limited emergency vaccination is now permitted, around foci of con®rmed infection. At present, the states of Rio Grande do Sul, Santa Catarina, ParanaÂ, Minas Gerais and Mato Grosso do Sul have been declared free of the disease. Periodic serological monitoring and surveillance of suspect cases are carried out, together with of®cial control measures, including obligatory noti®cation of outbreaks, slaughter of infected and incontact pigs, destruction of carcasses and contaminated materials, disinfection of vehicles, control of transit, and establishment of 3-km protection zones, and 10-km surveillance zones around disease foci. 2.3. Other countries in South America CSF is still enzootic in most of South America (Table 1), the exceptions being Uruguay and Chile. No CSF has been recorded in Uruguay since 1991 and the country is of®cially free of the disease. Chile declared itself free of CSF (without vaccination) from April 1998. The last case in Chile was in August 1996. Vaccination was prohibited throughout the country from October 1997. Interestingly many pig farmers took out insurance cover of their production before stopping vaccination. This was a crucial step towards


107

Table 1 Countries where classical swine fever (CSF) has been recently reported in South America (OIE, 1999) Argentina Brazil Bolivia Colombia Ecuador Paraguay Peru Venezuela

Sporadic Area-related Sporadic Sporadic Enzootic Sporadic (last outbreak 1995) Enzootic (in small farms) Sporadic (last outbreak 1996)

eradication in that it gave farmers the con®dence to support the disease control programme (S Urcelay, personal communication). According to information provided to FAO, programmes for control of CSF are being implemented in Argentina, Brazil, Chile, Colombia, Costa Rica, Ecuador and Paraguay (FAO, 1997). The measures adopted include vaccination, laboratory testing, stamping out, quarantine, control of transit and import restrictions. The Mercosur trade alliance, where Brazil, Uruguay, Argentina and Paraguay are in the process of lifting commercial barriers, has also generated the motivation for improved animal disease control in the region. As a result, efforts towards eradication of CSF are expected to be enhanced, particularly among Mercosur participants. As regards wild pigs, a limited number of European wild boar have been imported for hunting purposes into Uruguay. Some of these have crossed the border and reached southern Brazil. However, although only a small number of samples has been examined so far, no signs of CSF infection have been detected in either Uruguay or southern Brazil. 2.4. Islands of the Caribbean CSF is present in three Caribbean countries: Cuba, Haiti and the Dominican Republic. It was ®rst introduced to Cuba in 1930 (probably from the USA) and since then was kept under control until 1993, through vaccination campaigns. Initially these used a crystal violet vaccine; then, from 1962, a locally produced modi®ed live vaccine using the lapinized Chinese strain of CSF virus was employed. In 1993, a new epizootic of CSF started as a consequence of the worsening economic situation in Cuba (insuf®cient implementation of sanitary measures, low level of vaccination, poor nutritional status of the pigs, etc.). From 1993 to 1997, 455 outbreaks were reported, causing the death or slaughter of >70,000 head from a population of 414,000 pigs (17%). Although Cuba is potentially well equipped for animal disease control, with comprehensive legislation, ®eld and laboratory facilities, highly skilled veterinarians, scientists and technicians, unfortunately the country lacks funds to support the running cost of a major eradication project. The introduction of CSF to Haiti is more recent. The ®rst case was reported in August 1996 in the suburbs of Port-au-Prince, but its origin is not known. It may have been introduced by plane from Cuba, but its presence in the country for several months prior to the ®rst report cannot be excluded. Under the auspices of FAO, massive vaccination

108


campaigns were organized with the ®nancial support of several donors (European Union, IDB, USAID, French Cooperation, IICA, etc.): 436,000 pigs were vaccinated during the ®rst campaigns, i.e. 70% of the population, and 400,000 during the second round. One of the objectives was to control CSF so that it would not cross the border with the Dominican Republic. Unfortunately, this goal was not successful and CSF was con®rmed in the Dominican Republic in June 1997, when an outbreak was reported in the Elias PinÄa province. In this country, the control strategy was based on (1) the stamping out of all the animals present in the outbreaks and the surrounding areas and (2) the depopulation of all the pigs in a 40-km wide corridor along the border with Haiti. This strategy was not successful, and in December 1997, 24 outbreaks were reported across the whole country, even in the eastern part. To protect the industrial pig sector, vaccination is now allowed. The three countries are very different: the pig sectors vary from traditional (Haiti) to industrial (Dominican Republic) and the veterinary services vary from well organized with skilled technicians (Cuba) to rather poor with no diagnostic capacity (Haiti). But all these countries have a common problem: the lack of funds to cover the rehabilitation of equipment and running costs. Therefore, a regional eradication project should be implemented as soon as possible. For such a project to succeed in eradicating the disease, it should include help for the countries with fundamental changes and improvements to the infrastructure according to their individual needs, by strengthening the veterinary services, training veterinarians, scientists and ®eld technicians, supporting farmer associations, etc. In addition, the project should: 1. facilitate the exchange of information between the countries; 2. standardize vaccination procedures (especially between Haiti and the Dominican Republic.); 3. harmonize diagnostic techniques; 4. promote regional co-operation between the countries and regional or international organizations (OIE, FAO, IICA, COFIPOC, USDA); 5. provide as necessary, institutional support for the organization and/or privatization of the veterinary services; 6. develop national epidemiological surveillance systems in accordance with the OIE International Animal Health Code (OIE, 1998).

3. Japan and south east Asia 3.1. Japan In Japan, the ®rst outbreak of CSF was recognized in 1888. Since then, many cases of the disease have been reported. Inactivated vaccines, such as phenol/glycerol, formalin or crystal violet, have been used in the ®eld for many years, but before 1968 it was dif®cult to control the disease because of the lack of potency of these inactivated vaccines. In 1969, a CSF attenuated live vaccine (GP vaccine) was developed in Japan. Although there are no published trials comparing GP and C strain vaccines, ®eld evidence would suggest that the safety and ef®cacy of both products is similar.


109

The GPEÿ strain adapted in guinea-pig kidney cell cultures was used as the seed virus for GP vaccine. It has the following unique characteristics: 1. It does not show the phenomenon of exaltation of Newcastle disease virus (END) (Kumagai et al., 1958, 1961), but shows unique, intrinsic interference (Shimizu et al., 1970; Fukusho et al., 1976) with heterologous viruses, such as Newcastle disease virus, western equine encephalitis virus, vesicular stomatitis virus, etc. (E marker). 2. The strain grows readily in guinea-pig kidney cell culture, unlike wild-type viruses which do not (G marker). 3. The strain propagates better at 308C than 408C, while wild-type and virulent viruses propagate well at both temperatures (T marker). 4. Swine inoculated with GPEÿ strain show no anorexia, pyrexia, or other clinical signs of CSF, and leukopenia, if present, is very mild. 5. GPEÿ strain rarely produces viraemia in inoculated swine. When it does occur, it is transient. 6. As the strain is not shed in excreta, in-contact pigs do not become infected. 7. Protection occurs from 3 days after vaccination with GP vaccine. When the GP vaccine was applied nation-wide in the ®eld since 1969, when outbreaks of CSF have decreased markedly. No outbreak of CSF was reported in the 4 years between 1975 and 1978. An unexpected local epidemic occurred in 1979 and was controlled by increasing the vaccination rate (to more than 80%). At the time of writing, no CSF epidemic has been reported in Japan since the last outbreak in 1992. The eradication programme was started in 1996. The programme consists of three phases; the ®rst 2-year phase is to immunize the pig population by vaccination (as close to 100% as possible); the second phase (next 2 years) is to establish a CSF-free local area without vaccination, to con®rm that the area is free of ®eld CSF viruses; the third phase (1 year ) is to suspend vaccination completely and to con®rm that the pig population is free of CSF. Before starting the eradication programme, two national committees (a general and a technical) were organized, together with a regional committee in each prefecture, for the investigation and control of CSF. The principles for the three phases of the national eradication policy are as follows:

Increase vaccination at the first phase Suspend vaccination partially at the second phase Suspend vaccination completely at the third phase Control feeding of unheated swill Control boars used for the artificial insemination Survey for antibody in wild boar population Surveillance for CSF clinically suspect pigs, and serological surveys for CSF antibody Control movement of pigs (e.g. movement of pigs into non-vaccination areas) Training of staff in regional diagnostic laboratories in 47 prefectures Promote education on CSF amongst veterinary clinicians, farmers, and pig industry organizations Establishment of a guarantee fund for pigs killed under the stamping out policy Emergency vaccination using GP vaccine, under control of the authorities

110


During the ®rst phase, many CSF suspected pigs were subject to laboratory tests, but all were negative. Sera from wild boar from various areas were negative for CSF antibody. Molecular typing of ®eld viruses isolated in previous years has also been carried out in order to improve epidemiological understanding (Sakoda et al., 1999). For diagnosis, the following unique methods were developed in Japan: 1. END method (based on exaltation of Newcastle disease virus) to assay most ®eld viruses 2. END neutralization test (Shimizu et al., 1964) 3. Interference method for GPEÿ strain (Shimizu et al., 1970; Fukusho et al., 1976) 4. Establishment of cell lines (FS-L3 and CPK-NS cells, which grow in serum free medium) for assay and neutralization test of CSF virus (Sakoda and Fukusho, 1998; Sakoda et al., 1998a, b); 5. monoclonal antibodies to distinguish ®eld strains from GPEÿ strain of GP vaccine; and 6. ELISA for antibody screening. 3.2. Other countries in SE Asia In South-East Asia, outbreaks of CSF still occur regularly in most countries except for Japan. Table 2 shows recent outbreaks of CSF in South-East Asian countries. Table 3 shows the control measures in use in each country. These data were reported from each country to the OIE Regional Laboratory for CSF in Japan. The situation in mainland China and North Korea is not known. For diagnosis, ¯uorescent antibody tests and virus isolation are used for detection of antigen or virus, and neutralization test, ELISA or NPLA are used for monitoring antibodies in most countries. However, control of CSF remains dif®cult in most of the region, and the prospect for the future is of continuing endemic CSF infection in South-East Asia. Factors underlying the lack of success in disease control are the lack of funds for vaccination, and in some countries limited expertise and diagnostic facilities. Table 2 Outbreaks of CSF in South-East Asian countries (1996 or 1997) Country

Pig population

No. of cases

Indonesia Japan Korea Malaysia Myanmar Mongolia Philippines Singapore Thailand Taiwan Vietnam

7,875,000 9,900,000 7,458,300 2,448,000 3,357,000 unknown 7,500,000 0 8,707,000 8,570,000 17,600,000

15,313 0 3