AFRICAN SWINE FEVER
FRANCISCO RUIZ-FONS
Instituto de Investigacion en Recursos Cinegeticos IREC (CSIC-UCLM-JCCM), Ciudad Real, Spain
African swine fever is a haemorrhagic disease of pigs caused by the African swine fever virus (ASFV).
The disease causes devastating losses in the pig industry.AETIOLOGY
ASFV is the only member of the genus Asfivirus in the family Asfarviridae. Some 54 different viral structural proteins have been identified in ASFV. Twenty- two different genotypes have been identified based on the sequence of the C-terminal end of the p72 gene (reviewed in(28)). ASFV is highly resistant at low temperatures in an organic medium but is inactivated in 30 minutes at 60°C. The virus can be isolated from serum or blood kept at room temperature for 18 months and may persist and remain infective in pork-meat products for more than 100 days.
EPIDEMIOLOGY
ASFV is currently endemic in many sub- Saharan countries. The virus was first described outside Africa in 1957 when it reached Portugal and, after a second epizootic in Portugal, it was also identified in Andorra, Belgium, France, Italy, Malta, the Netherlands and Spain. Thereafter, ASFV was eradicated from these countries, except from parts of Italy. Nowadays, Sardinia is the only European territory where ASFV is still reported. In 2007, ASFV appeared in the Caucasus via a port in Georgia, and since then it has spread in Georgia, and to Armenia, Azerbaijan and Russia. A recent report from the European Food Safety Authority (EFSA) established a moderate risk of ASFV reaching countries in the EU and becoming endemic in European wild boar populations(28).
ASFV is maintained in Africa by wild suids, domestic swine and soft ticks of the genus Ornithodorosλ2'. Three African wild suids are infected by ASFV with no clinical manifestations: the warthog (Phacochoerus africanus), the bush pig (Potamochoerus larvatus) and the red river hog (Potamochoerusporcus).
The role of another wild suid, the giant forest hog (Hylochoerus meinertzhagenz) remains unclear. Eurasian wild boar and feral pigs (Sus scrofa) are also susceptible hosts for ASFV, although their role as an ASFV reservoir remains unresolved.Following the introduction of highly virulent ASFV strains to wild boar populations, massive mortality is observed in all age and sex classes.
Several Ornithodoros spp. of tick are recognized as reservoirs of ASFV in Europe, Africa and America. The only proven vector of the genus in Europe is the O. erraticus group, which is distributed in Italy, Portugal, Spain and Turkey(28). A wild cycle involving O. moubata/ porcinus and the warthog is of significant importance for the maintenance of ASFV in Africa. Nonetheless, stable populations of O. erraticus have only been found in European domestic pig premises, especially in older, more traditional pig farms in which environmental tick maintenance sites such as crevices and cracks were present. Ornithodoros erraticus has never been described in Eurasian wild boar and, in contrast to the warthog, the Eurasian wild boar does not habitually reside in burrows where ticks may be present. Thus, it seems unlikely that a wild cycle involving Eurasian wild boar and Ornithodoros spp. ticks would occur in Europe.
The warthog acts as a true ASFV reservoir in that the virus infects the animal without inducing any lesions and O. moubata/ porcinus are essential for its maintenance1-29). The bush pig is able to maintain the virus, although at low circulation rates, and the significance of this species as a wild reservoir of ASFV is lower(29). Other wild African suids are considered to be of less significance as ASFV reservoirs in addition to their more restricted habitats, behaviour, abundance and distribution.
Clinical signs occur in both domestic and wild Sus scrofa following infection by ASFV, and infection with a highly virulent virus strain is frequently fatal.
This occurred following the introduction of ASFV to the Iberian Peninsula, Sardinia and more recently the Russian Federation, where mortality of wild boar was reported. In domestic pigs, infection by low virulence isolates had a subclinical course. Wild boar infected by ASFV in Spain were found to be either subclinically infected, to have recovered from infection or to have been infected by a low viral dose(30). This together with the reported decrease in virulence of the ASFV isolates circulating in domestic pig herds in the same region (reviewed in(30)) suggests a possible circulation of low-virulence ASFV isolates in wild boar populations in the area at that time. According to reported observations, two different epidemiologic scenarios may occur in Eurasian wild boar populations: i) a scenario in which circulating ASFV maintains high virulence; and ii) a scenario in which circulating ASFV reduces its virulence. In the first scenario, it would be expected that the mortality of wild boar would cause a significant impact in viral transmission, leading to the natural eradication of the virus. However, if large and interconnected wild boar populations are present in a region, the virus may spread rapidly. This seems to have occurred in Russia, where dead wild boar with ASF have been found in areas where the disease has not been reported in domestic pigs(28). In the second epidemiologic scenario, the Eurasian wild boar would eventually become a reservoir for ASFV, dependent to some extent on the pathogenicity of the ASFV isolate and on the wild boar population characteristics. This epidemiological scenario seems to contradict the experience in Sardinia, where it has been suggested that in the absence of the virus in domestic pigs, the wild boar is unable to maintain the virus(31). But the Sardinian situation may be similar to the first epidemiological scenario in which ASFV isolates did not develop reduced virulence.Most transmission of ASFV is direct between individual animals.
Owing to the long persistence ofASFV in organic material, indirect transmission via cannibalism or consumption of infected pork or meat products may occur. Indirect transmission through Ornithodoros spp. ticks is also important. Transmission over long distances occurs by movement of infectious meat and meat waste products that are fed to pigs(28). Wild boar may acquire ASFV infection by: i) direct contact with infected individuals or fomites contaminated by faeces, urine or saliva containing virus; ii) wounds caused during fighting with infected individuals; iii) consumption of infected products (waste meat products, carcasses); iv) rooting in pastures to which manure from infected pig herds has been applied; and v) being bitten by infected Ornithodoros spp. ticks. Transmission may also occur between wild boar and domestic pigs in areas where the virus is endemic in the domestic pig and where extensive farming systems with free- r oaming pig production is traditional (e.g. areas in Italy, Portugal, Romania and Spain). Wild boar are suspected to have been the source of ASFV in Armenia, Azerbaijan and Chech- nya(28,32) as well as the source for a small number of ASFV outbreaks in Spanish pig herds(30).PATHOGENESIS, PATHOLOGY AND IMMUNITY
ASFV is present in blood, tissues, secretions and excretions. The establishment of infections may depend on the virulence of the viral strain involved, which may also determine the level of excretion, persistence or viral replication.
The first sites of replication of ASFV vary depending on the site of initial infection. In domestic pigs, ASFV is commonly observed to replicate first in mononuclear phagocytic cells of tonsils and mandibular, or retropharyngeal, lymph nodes. Other primary replication sites following infection via aerosols are bronchial, gastrohepatic and mesenteric lymph nodes. From these initial replication sites the virus spreads to the target organs through the lymphatic drainage system and blood.
ASFV has also been found infecting megakaryocytes, endothelial cells, glomerulus mesangial cells, hepatocytes, renal tubular epithelial cells, thymus reticulum-epithelial cells, fibroblasts, muscle cells of venules and arterioles and neutrophils(33).Peracute, acute, subacute, chronic and subclinical manifestations of ASFV infection may take place in both domestic swine and wild boar, for which disease development is highly dependent on the strain of the virus. The clinical manifestation of ASFV infection shows marked variation between individual animals.
Persistent infection has been described in domestic swine and has relevance for control and eradication of the disease, but it is not known if it occurs in wild boar.
Naturally infected Spanish wild boar showed lesions consistent with acute ASF(30). Gross lesions consisted of severe, diffuse haemorrhages in lymph nodes (mesenteric, gastrohepatic and mediastinal lymph nodes) and the spleen. Similar gross lesions were observed in experimentally infected feral pigs(34). Microscopic findings consisted of severe necrosis and depletion of lymphocytes in para- cortical areas of the lymph nodes and similar but more moderate changes in lymphoid follicles of the lymph nodes and spleen. Macrophages and monocytes appeared with a cytopathic effect.
ASFV produces a strong humoral immune response and high levels of specific antibodies are produced, lasting for a long time after initial infection(33). However, there is currently little available information on the humoral and cellular immune responses to ASFV in Eurasian wild boar.
CLINICAL SIGNS
Wild boar develop similar clinical signs to those of domestic swine. Experimental infection of feral pigs with high and moderate virulent ASFV isolates resulted in fatal disease(34), in which pyrexia (temperatures >41°C) was the first clinical sign reported, accompanied by lethargy and inappetance. Animals died between 2 and 13 days postinfection depending on the virulence of the ASFV isolate.
Clinical signs of ASF in wild boar, which die quickly when infected with moderate and high virulence strains, have not been reported. Chronic manifestations of ASF in wild boar also have not been reported, probably because in these cases, assumed to be caused by low virulence isolates, the clinical signs are mild.DIAGNOSIS
Clinical diagnosis of ASF is difficult because of low specificity of the clinical signs. Laboratory diagnostic tests employed to test domestic swine are also recommended to test wild boar(29,35). Direct isolation/detection of ASFV or indirect detection of specific anti-ASFV antibodies are the two recommended approaches. Virus detection is usually carried out by the haemadsorption test. Some isolates are not haemadsorbent, and in these cases, the immunofluorescence test can be used to detect viral particles in tissues. PCR targeted against highly conserved genetic sequences in the different ASFV isolates offers a quick, sensitive and specific detection method in animal tissue samples. Serological tests for the presence of specific anti-ASFV antibodies can be performed by ELISA, indirect immunofluorescence test, immunoblotting and counter immunoelectrophoresis(35).
MANAGEMENT, CONTROL AND REGULATIONS
No effective vaccine is currently available for the prevention and control of ASF. Control and eradication in domestic swine has been performed by strict biosecurity measures, early detection and removal of positive swine(28). Control of the wild cycle involving the warthog and soft ticks in Africa is considered impractical at present(29). Only biosecurity measures preventing the contact of domestic swine with warthogs and ticks have been proposed to avoid transmission from the wild reservoir.
In the case of the Eurasian wild boar there is concern that ASFV could become endemic in large interconnected wild boar populations. Control of ASFV spread in these instances may be difficult, but reducing population densities could reduce viral transmission.
REGULATIONS AND REPORTING
ASF is a notifiable disease to the World Organisation for Animal Health (OIE). Regulation and reporting protocols for ASF in the EU are detailed in the Council Directive 2002∕60∕EC(36).The suspicion of ASF in pigs or wild boar must be immediately notified to the regional and national animal health authorities and confirmed by regional and national reference laboratories. If ASF is confirmed, the outbreak must be notified to the OIE and to every EU member state.
PUBLIC HEALTH CONCERN
ASF is a disease strictly affecting suids, and as a consequence there are no current known public health concerns.
SIGNIFICANCE AND IMPLICATIONS FOR ANIMAL HEALTH
Highly virulent ASF isolates cause severe losses in domestic swine populations. The effect on wild boar population dynamics seems also to be potentially significant. Recent information from Russia suggests that the virus could have a significant impact on the population dynamics of wild boar. The introduction of ASFV in the dense, continuous wild boar populations of Central and Eastern Europe may be devastating if high virulence is maintained.