African Swine Fever: An Epidemiological Update
Summary
African swine fever (ASF) is one of the most important swine diseases, mainly because of its significant sanitary and socioeconomic consequences. This review gives an update on the epidemiology of the disease and reviews key issues and strategies to improve control of the disease and promote its eradication. Several characteristics of ASF virus (ASFV) make its control and eradication difficult, including the absence of available vaccines, marked virus resistance in infected material and contaminated animal products, and a complex epidemiology and transmission involving tick reservoir virus interactions. The incidence of ASF has not only increased on the African continent over the last 15 years, so that it now affects West African countries, Mauritius and Madagascar, but it has also reached new areas, such as the Caucasus region in 2007. In fact, the rapid spread of the disease on the European continent and the uncontrolled situation in the Russian Federation places all countries at great risk as a result of intense global trade. The proximity of some affected areas to the European Union (EU) borders (<150 km) has increased concerns about the potential economic consequences of an ASF incursion into the EU pig sector. Establishing effective surveillance, control and eradication programmes that implicate all actors (veterinarians, farmers, and policy makers) is essential for controlling ASF. African swine fever ‐free countries should be aware of the potential risk of ASF incursion and implement risk reduction measures such as trade controls and other sanitary measures. This review will discuss lessons learnt so far about ASF control, current challenges to its control and future studies needed to support global efforts at prevention and control.
Introduction
African swine fever (ASF) was first described by Montgomery in Kenya in 1921. Since then, many African, European and American countries have been affected by the disease. African swine fever is one of the most complex and economically devastating viral diseases in swine herds, producing great socioeconomic impact in affected countries. For that reason, it is listed as a notifiable disease by the World Organization for Animal Health (OIE). African swine fever has several properties that make it difficult to control and eradicate, which are outlined below.
African swine fever virus (ASFV) is a very complex and large enveloped DNA virus with a genome of 170–190 kbp, and it is classified as a unique member of the Asfarviridae family, genus Asfivirus (Dixon et al., 2005). The virus presents high genetic and antigenic variability, with 22 different genotypes described based on the p72 sequences, all of which currently circulate on the African continent (Boshoff et al., 2007).
The natural hosts of ASFV are African wild pigs; however, wild boars and domestic pigs of all breeds and ages are also susceptible to the infection by ASFV. The virus also infects different species of soft ticks of the genus Ornithodoros, in which it can persist more than 5 years (Oleaga‐Pérez et al., 1990). In its natural hosts, ASFV targets primarily monocytes and macrophages of the mononuclear phagocytic system (Malmquist and Hay, 1960).
Protection against ASFV is not fully understood. Although ASFV infection induces small proportion of neutralizing antibodies against some virion proteins (Ruiz‐Gonzalvo et al., 1986; Zsak et al., 1993; Gomez‐Puertas et al., 1996), this protection is not enough for viral challenge (Neilan et al., 2004). Despite that, role of antibodies is important, as they confer some protection that does reduce viraemia, delay the onset of clinical signs and reduce the adverse effects of infection, as it was demonstrated by passive transferred of anti‐ASFV immunoglobulins by Onisk et al., 1994. Cellular immunity also plays an important role in immune protection against ASFV infection, specifically, cell activity of CD8 lymphocytes (Oura et al., 2005) and natural killer cells (NK) (Leitão et al., 2001). Cross‐protection has been also demonstrated by challenging infected animals with homologous isolates, (Mebus and Dardiri, 1980; Ruiz‐Gonzalvo et al., 1986), some of them field low virulent strains (Leitão et al., 2001; Boinas et al., 2004; King et al., 2011).
Nevertheless, all the previous attempts to develop a vaccine have failed and no effective vaccine is available against ASF. Live attenuated vaccines were previously used in Spain and Portugal, but their use implies unacceptable safety problems (Manso Ribeiro et al., 1963). Indeed, the vaccination applied in Iberian Peninsula with these live attenuated vaccines during 1960s might have been the origin of some low virulence strains that induced the onset of chronic forms of the disease during ASF infection in the Iberian Peninsula (1960–1995).
Other strategies such as the use of deleted replicating viruses with one or more, naturally or experimentally, deleted genes (Alfonso et al., 1998; Lewis et al., 2000; Salguero et al., 2008), subunit vaccines based on recombinant proteins (Ruiz‐Gonzalvo et al., 1996; Gomez‐Puertas et al., 1998; Neilan et al., 2004; Ivanov et al., 2011) or DNA vaccines (Perez‐Martin et al., 2006; Argilaguet et al., 2011; Lacasta et al., 2011), did no confer a complete real protection.
In summary, all the studies on ASF protection until now only proved the delay of the onset of clinical signs and death and partial protection against homologous viruses; but none of them has the adequate and required properties to be an effective and safe vaccine against ASF.
African swine fever virus is highly resistant to inactivation in the environment in the presence of organic material. The virus persists for long periods of time in infected material (blood, faeces, serum, slurry) and tissues, where it can survive for more than 15 weeks in putrefied blood, 11 days in faeces kept at room temperature or 1000 days in frozen meat (European Food Safety Authority (EFSA), 2009). This great persistence must be considered when developing ASF contingency and eradication plans, so that appropriate disinfectants and procedures should be used to achieve complete disinfection of contaminated areas and materials.
African swine fever is considered a haemorrhagic disease due to the typical haemorrhagic symptoms of the hyperacute and acute forms of the diseases, although other presentations (chronic and asymptomatic forms) of the disease are shown without these characteristic symptoms. African swine fever progresses with different clinical signs depending on isolate virulence, host, dose and route of exposure. Hyperacute and acute clinical signs in pigs and wild boars are very similar to those of other haemorrhagic diseases, such as classical swine fever, salmonellosis or erysipelas. Thus, laboratory diagnosis is required for differentiating among them. African swine fever clinical signs may vary from a hyperacute form, with 100% mortality from days 4–7 post‐infection and typical haemorrhagic symptoms, to a less common asymptomatic and chronic form that can turn animals into carriers. This last form, observed in wild and domestic animals, plays an important role in the persistence and dissemination of the disease in endemic areas, even more if infected ticks are present (Arias and Sánchez‐Vizcaíno, 2002a).
European wild boars are usually more resistant than domestic pigs to ASFV infection, although they present a similar pathological and epidemiological pattern (Sánchez‐Vizcaíno, 2006). African wild suids such as warthogs (genus Phacochoerus), bush pigs (Potamochoerus porcus and P. larvatus) and giant forest hogs (Hylochoerus meinertzhageni) may also be infected by ASFV, but they usually do not exhibit clinical signs, allowing them to act as reservoir hosts in Africa (De Tray, 1957). In these wild suids, ASF infection is characterized by low levels of virus in tissues and low or undetectable viraemia (Plowright, 1981). These levels of virus in adult suids are insufficient for transmission through direct contact between animals and/or indirect contact by ticks (Jori and Bastos, 2009). However, ASF transmission occurs repeatedly in warthog burrows, between infected soft ticks and neonatal warthogs that develop high levels of viraemia, sufficient to infect naive ticks that feed on them (Thomson, 1985). The role of these wild suids, especially warthogs, in the sylvatic cycle of ASF in Africa, is essential for the persistence of the disease in the continent, creating serious difficulties for the eradication of the disease in eastern and southern Africa. However, in West African countries, the role of wild suids and ticks seems to be less important for ASF spreading and endemicity (Penrith and Vosloo, 2009). In these countries, the disease is maintained and spread mainly by movements and illegal trade of infected pigs and pork products.
Depending on the existence of wild reservoirs and ticks, and their interactions with domestic suids, five ASF epidemiological scenarios can occur. The most ancient scenario describes transmission from eastern and southern African countries; this involves a sylvatic cycle explained before, where wild suids and soft ticks from the O. moubata species act as ASFV reservoirs. African swine fever transmission to domestic pigs is mainly caused by the bites of infected ticks or by the ingestion of tissues from acute‐infected warthogs (Wilkinson, 1986).
The second scenario describes the situation in West African countries, which have been more recently affected by ASF. Here, transmission occurs mainly through direct contact between domestic pigs or indirect contact between pigs and pork products, but no soft ticks are apparently involved. Socioeconomic factors such as lack of veterinary services, lack of compensation to farmers for culled animals and the consequent hiding of the diseased animals in its first stages, facilitate the spread of the disease within the country and to neighbouring countries. This situation is also occurring in some areas of the Caucasus and the Russian Federation (Beltrán‐Alcrudo et al., 2009).
A third scenario occurred when the disease was present on the Iberian Peninsula (1960–1995). Domestic pigs and wild boars suffered the disease, which was mainly transmitted by direct contact between animals and infected meat. O. erraticus soft ticks also contribute to disease transmission in outdoor pig production systems (Arias and Sánchez‐Vizcaíno, 2002b), as well as reservoir of ASFV in previous infected areas, in which, these ticks are able to transmit the disease 1 year after the removal of the infectious host, and allow the persistence of ASFV for 5 years (Boinas et al., 2011). However, in contrast to O. moubata, O. erraticus ticks participate only in transtadial ASFV transmission, so no transovarial transmission has been observed (Plowright, 1981). In this scenario, the presence of infected wild boars and these soft ticks made ASFV eradication difficult, particularly in outdoor swine production areas, where O. erraticus was the cause of re‐emergences of the disease, even after disease eradication, as it was the case of the single outbreak in Portugal in 1999 (Boinas et al., 2011). Nevertheless, after tremendous efforts, eradication was achieved through programmes that included the detection of anti‐tick antibodies in domestic and wild boars, as well as the destruction or isolation of the pigpens where ticks were present (Arias and Sánchez‐Vizcaíno, 2002b). Another model of this scenario occurs in certain areas of Central Africa (demonstrated in Malawi (Haresnape et al., 1988), and probably neighbouring Mozambique and Zambia), where ASF is maintained within the domestic pig population, that could also get infected by soft ticks present in the pig pens.
A similar situation occurred in the fourth scenario, when the disease was introduced into Central and South American countries (1968–1980), but this time the disease affected only domestic pigs, as wild animals (feral pigs) and soft ticks did not play an important role in the epidemiology and transmission of the disease. The absence of wild reservoirs or ticks facilitated early eradication of the disease after costly eradication campaigns in the area (Simeón‐Negrín and Frías‐Lepoureau, 2002; Lyra, 2006).
The last scenario occurs in currently affect areas of the Russian Federation and trans‐Caucasian countries. The epidemiological cycle of ASF is affecting domestic pigs and wild boars, but so far, ticks are not involved. Most of the outbreaks (79.8%) affect domestic pigs and have been caused by movements of infected or carrier animals and their products. Only 20.2% of outbreaks affect wild boars; these have been mainly caused by contact between wild boars and domestic pigs, whilst transmission within wild boar population also occurs (World Organization for Animal Health, 2011a; European Food Safety Authority (EFSA), 2010a). Although no soft ticks implicated in the cycle have presently been found in the area, some Ornithodoros species inhabit the region (European Food Safety Authority (EFSA), 2010a) and all Ornithodoros species tested to date are susceptible to ASFV infection (European Food Safety Authority (EFSA), 2010b). For this reason, further studies should be carried out to understand the transmission role of soft ticks in this area.
Understanding the different epidemiological scenarios and the characteristics of the disease is critical for developing successful contingency and eradication plans in affected areas.
ASF Distribution
Since the first description of the disease in Kenya in 1921, many sub‐Saharan countries have been affected by ASF. The disease was restricted to this region until 1957, when an outbreak occurred in Portugal, the first outbreak outside the African continent. This outbreak was effectively controlled and eradicated, but new ones occurred in 1960 near Lisbon (Manso Ribeiro and Azevedo, 1961). Recent genetic studies (Gallardo et al., 2009a,b) discriminate between these isolates, and suggest the possibility of two different introductions in the area. From this initial outbreaks, ASFV spread to many areas of the Iberian Peninsula (Spain and Portugal), where it remained endemic until 1995. During the 1970s and 1980s, ASFV travelled around the world, affecting more countries in Europe, such as the Netherlands, Italy, France and Belgium, as well as some countries in the Americas, notably the Dominican Republic and Brazil (Costard et al., 2009). The historical way of ASFV introduction into these disease‐free areas was mainly by feeding domestic animals with contaminated pork products that entered the territory via international airports and seaports. Once established in domestic herds, infected pigs and pork products become the primary sources of virus dissemination. Based on epidemiological data from Spanish scenario, role of carriers in virus dissemination seems to be not so important when appropriate control measures are put in place (Bech‐Nielsen et al., 1995). As a result of significant control efforts, the disease was eradicated from all these territories, but it persisted on the Italian island of Sardinia and on the African continent, especially in southeast Africa.
During the 1990s and 2000s, the epidemiology and distribution of the disease changed (Fig. 1): ASFV spread to other regions not typically affected by ASF. These included West African countries, where the virus was first reported in Côte d′Ivoire (1996), Nigeria (1997), Togo (1997), Ghana (1999), Burkina Faso (2003) and recently, Chad (2010). It also spread to some islands, such as Madagascar (1998) and Mauritius (2007). Importantly, the disease re‐entered the European continent in 2007, this time via Georgia (World Organization for Animal Health, 2011a).
Countries affected by African swine fever. Light grey indicates countries where disease is limited to a few areas; medium grey, countries where infections occurred before 1995; and black, countries where infections occurred after 1995.
This considerable epidemiological change may have been caused by a combination of several factors, the most important of which may be the increasing presence of ASFV on the African continent over the last 15 years, as the incidence of ASF has increased in endemic countries and entered previously disease‐free territories. This suggests that the amount of virus circulating in the world has increased, together with the number of infected animals and the amount of contaminated pig products. A second important factor is globalization. Nowadays, people, animals and products travel long distances around the world in very short periods of time. This movement increases the potential for introducing pathogens into new territories. The third important factor is the global financial crisis, which has forced small farmers to meet their needs in new ways, such as by using swill or garbage to feed their animals. These three factors, together with the high resistance of ASFV in the environment and meat products, the presence of asymptomatic carrier animals and the lack of vaccine may explain how the disease has not only increased in endemic areas but also spread to new territories.
ASF Situation in the Caucasus Region and the Russian Federation
In April 2007, a new outbreak of ASF p72 genotype II, compatible with the virus circulating in Mozambique, Madagascar and Zambia, reached the European continent via Georgia (Rowlands et al., 2008). Since then, all the ASFV isolates found in the Caucasus region and Russian Federation show identical p72, p54 and CVR sequences, suggesting that only one virus arrived in the area in 2007 and subsequently spread from this initial outbreak (Gallardo et al., 2009a,b). This ASFV is thought to have been introduced by international ships containing infected swill that were used to feed pigs near the port of Poti (Beltran‐Alcrudo et al., 2008). After this introduction, the disease spread very quickly, affecting four different countries: Georgia, Armenia, Azerbaijan and the Russian Federation. Since the introduction of the virus in the Caucasus region, the OIE has been notified of more than 273 outbreaks, in which more of 76 000 animals have died (World Organization for Animal Health, 2011a). The economic losses of these outbreaks in the Russian Federation have been estimated at 25–30 billion RuR (0.8–1 billion USD) (United States Department of Agriculture (USDA), 2010). The likelihood that ASF will become endemic and spread to nearby unaffected areas of the Russian Federation has been estimated as very high (European Food Safety Authority (EFSA), 2010a) due to the presence of some adverse factors in the area: demonstrated ASFV infection in wild boar populations, an extremely high volume of illegal trade of pigs and pork products within the country, a tradition of swill feeding, the absence of adequate veterinary services and lack of pig production infrastructure and traceability (Beltrán‐Alcrudo et al., 2009).
However, in some of the affected areas of Russian Federation, like Krasnodar region, important control measures are being applied. These measures are based on early detection and notification of the disease, promoted by education and importantly, compensation to the farmers (Shevkoplyas, 2011). Since the first introduction of the disease in the territory, ASF has been present in a hyperacute–acute form of the disease, without chronic forms of the disease, and an average incubation period of 4.3 days. No changes in the pathological and epidemiological pattern of the disease have been observed by Russian veterinaries that support the absence of recovered or undetected infected animals in their country (Blagodarsnosti, 2011). However, no active surveillance and serological diagnosis are being carried out by official veterinaries in Russian Federation until now.
All the factors mentioned before and the lack of a coordinated national control programme make control and eradication of the disease from this area very difficult, and increase the risk of spread to neighbouring countries, especially those with commercial and sociocultural relationships with the Russian Federation. These observations are supported by recent comments of the Russian Chief Veterinary Officer, who predicted a spread of the disease towards the northern and northwestern regions (Vlasov, 2011). Recent ASF outbreaks in October 2009, December 2010 and April 2011 occurred very near EU borders, less than 150 km away from Estonia, Finland and Norway (Fig. 2) (World Organization for Animal Health, 2009a; World Organization for Animal Health, 2010a; World Organization for Animal Health, 2011b). These outbreaks increase the risk of introduction into the EU.
Outbreaks of African swine fever in domestic pigs (•) and wild boar (★) in the Russian Federation and Trans‐Caucasian countries. European Union countries are shown in grey.
The EU is aware of the potential risk of ASFV introduction within its borders. A recent risk assessment (European Food Safety Authority (EFSA), 2010a,b; Wieland et al., 2011) estimates the risk of ASFV introduction into the EU as moderate. However, given the spread and uncontrolled situation of the disease in Russia and the recent outbreaks near the EU border, this estimation should be reconsidered. The same risk assessment highlights the risk of introduction through contaminated products used for swill feeding. Historically, this was the most frequent route of ASFV introduction into disease‐free countries, e.g. Spain, Netherlands, Belgium, Cuba and more recently, Georgia. At the same time, the risk assessment predicts that once the disease enters the EU, it is unlikely to persist there, given the relatively high biosecurity of the pork production industry.
Although imports of pigs and pig products from ASF‐affected areas into the EU have been completely banned since the first notification of the disease (World Organization for Animal Health, 2009b), the EU is aware of the continuing risk, and recently approved a new decision regulating livestock vehicles coming from Russia (Decision 2011/78/EU). As a result, vehicles used for pig transport that enter the EU from Russian territory must certify that they were adequately disinfected after the last uploading of pigs.
More detailed and complete analyses are being developed within the European project ASFRISK (EC, FP7‐KBBE‐2007‐1, Project #211691) to estimate the most likely pathways, countries and months of ASFV introduction into the EU. Preliminary results of this analysis consider the likelihood that ASFV will be introduced into the EU by import of live pigs as low (Mur et al., 2011). Methods and results obtained by this risk assessment may help allocate financial and human resources to areas and periods at higher risk, helping to reduce the risk of ASFV introduction into the EU.
Prevention and Control
Preventing the virus from entering disease‐free areas is crucial and must focus on avoiding the introduction of potentially infected pigs or pork products and properly disposing of fomites, particularly pork waste from aircrafts and ships. Once the disease has entered a territory, control measures should aim for early detection in the field following by a rapid laboratory diagnosis, as well as enforcement of strict sanitary measures (Sánchez‐Vizcaíno, 2006). Laboratory diagnosis is essential for correct diagnosis of the disease, due to the strong similarity of ASF clinical signs and macroscopic lesions with those of other haemorrhagic diseases of pigs. Several effective tests are available to detect infectious virus, viral antigens, viral DNA or specific antibodies induced by the 22 p72 different ASF genotypes (World Organization for Animal Health, 2010b). The parallel detection of antigen and antibodies is crucial for establishing correct diagnosis and evaluating the progress of the disease control programme (Sánchez‐Vizcaíno, 2006). This parallel diagnosis is not being currently developed in the affected area of Russian Federation and Trans Caucasian Countries, but should be soon implemented to delimit the ASF affected areas, control the progress of the disease, evaluate the successful of control programmes and definitively confirm the absence of carrier and recovered animals. African swine fever eradication without vaccination is possible, but difficult. Indeed, the eradication of ASF from Portugal and Spain proved that vaccination is not required for eradication even from countries where the disease has long been endemic (Arias and Sánchez‐Vizcaíno, 2002b). However, success depends on implementing a good eradication programme approved by all the role players (farmers, veterinarians and policy makers), adapted to each specific scenario and adequately financially supported. For example, ASF eradication programme (1985–1995) was internationally funded with $72 million from the European Community over five years (Bech‐Nielsen et al., 1995). Such a programme should provide accurate and timely information to farmers about the main sources of infection; monitor the movement of pigs and pork products; completely prohibit swill feeding practices; detect and eliminate positive animals, reservoir animals and carriers; increase biosecurity measures on farms; and provide reasonable economic compensation to farmers (Arias and Sánchez‐Vizcaíno, 2002b). In the case of Sub‐Saharan countries, although control and eradication programmes are cost and difficult, nowadays, there are unique solutions available against ASF, due to the absence of an effective vaccine. In such countries, where funds and resources are limited and insufficient for disease eradication, the perspective of the programme should not be the prompt eradication of the disease, but the improvement in pig husbandry systems and biosecurity measures, to achieve disease control and establishment of free disease areas in certain territories.
Acknowledgments
This study was funded by the EU ASFRISK project (EC, FP7‐KBBE‐2007‐1, Project #211691) and by the Ministry of Education and Science of Spain (FPU Program).
Conflict of Interest Statement
All authors declare no conflict of interests.
