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African Swine Fever: current knowledge and gaps

The causative agent of African swine fever is a unique member of the Asfarviridae family, the Asfivirus (ASFV) (1); a genetically complex double-stranded DNA virus. Twenty-three genotypes have been described based on the partial sequences of the p72 gene (2, 3). All of them are present in Africa, whereas only genotypes I and II have been found outside of the African continent. The sole European territory where ASF Genotype I (vp72) has been present for a long time is the Italian island of Sardinia (4). The same genotype has been present in Spain and Portugal from 1960 to 1995 and caused outbreaks in some other European countries [France (1964, 1967, and 1977), Belgium (1985), Italy (1967, 1980) Malta (1978), and the Netherlands (1986)] (5). This genotype was also responsible for several outbreaks in the Caribbean and South America from 1971 to 1981 (6). Since 1995, all affected European and south American countries had successfully eradicated the disease (4), with only Sardinia being the exception. However, all ASFV isolates circulating in Azerbaijan, Armenia, the Russian Federation, in other Eastern and Central European countries since 2007, are all clustered within Genotype II (7).

Virulent ASFV strains cause peracute or acute hemorrhagic fever in infected animals, with up to 100% mortality (8). Generally, clinical disease can manifest in multiple ways, ranging from death, with no signs (peracute, mortality nearing 100%), to an asymptomatic infection. However, most isolates of ASFV cause acute hemorrhagic fever in domestic pigs and result in mortality nearing 100% (9, 10). European wild boar (Sus scrofa) is highly susceptible to the disease and shows similar clinical signs and lethality as domestic pigs (Sus scrofa domesticus). In contrast, infected wild African suids usually have occult infections and develop subclinical and asymptomatic long-term persistent infections, acting as ASFV reservoirs in Africa.

African swine fever virus is primarily transmitted via direct and indirect contact between animals, through infected swine and their products, and via contaminated fomites or uncooked meat from infected animals. Its ability to persist for a long time in the environment or in infected biological samples makes eradication difficult once the disease has become established. Soft ticks of the Ornithodoros spp. can be an effective reservoir of infection (11, 12), with documented trans-stadial, trans-ovarial, and sexual transmission (13). However, these tick species have not been shown to be involved in transmission of ASFV in Eastern Europe, Russia, or the trans-Caucasus region (14), whereas potential sources of infection in Europe are represented by infectious domestic pigs (Sus scrofa domesticus) and wild boar (Sus scrofa), contaminated carcasses, food waste, and vehicles or equipment. Furthermore, in Sardinia (Italy), where the disease has been persisting for more than 35 years, recent studies have reaffirmed the absence a role of O. erraticus ticks in the ASF cycle, despite strong climatic and ecological similarities with the Iberian Peninsula, where this tick was involved in ASFV transmission and the persistence of ASF (15, 16).

In addition to the presence of carrier animals (17), there are several other mechanisms that can lead to long-term circulation of ASFV in pig or wild boar populations. The most important are human-induced factors, such as illegal movement of infected pork and swill feeding (18, 19, 20, 21, 22, 23, 24, 25), as well as free-range pig management systems as it was observed in some regions of Russia (26, 27).

ASF was confined to Africa until the end of the 1950's, when Genotype I ASFV strains first appeared in Portugal, in 1957, probably via a single-source introduction from Angola (28). This epidemic wave involved different countries in Europe and then also in some Central and South American countries. After the virus introduction into the Russian Federation in 2007 (29), in order to mitigate the risk of ASFV spread toward the EU, the EU Member States bordering the Russian Federation implemented specific protection measures. Despite this, in 2014 ASF entered Estonia, Latvia, Lithuania, and Poland, where the disease has become endemic in the wild boar population (30), whereas the sporadic outbreaks occurring in domestic pigs have been efficiently controlled, thus preventing extensive secondary spread (31). However, in 2016 ASFV spread into Moldova and in 2017 it was reported for the first time in Czech Republic, Romania (32), Bulgaria, and Hungary (33). In September 2018 the virus made a big leap, infecting hundreds of wild boars in Southern Belgium, in a well-limited and confined area of the Walloon region (33). There were also large outbreaks in Asia, starting in China, where a wide part of the territory has been infected since August 2018. In July 2019 the disease was notified for the first time in Slovakia and a month later, in August 2019 (33), it appeared for the first time in Serbia (33).

Currently, the disease is present in more than 20 sub-Saharan African countries (34), in some islands of the Indian Ocean (Madagascar and Mauritius), and from 2007 in some Eastern, Central European countries and in eight countries belonging to the European Union (Lithuania, Polonia, Latvia, Estonia, Romania, Belgium, Slovakia, the island of Sardinia in Italy). However, the positive resolution of an outbreak that occurred in a wild boar population resident in a restricted area of the Czech Republic should be considered (35).Nevertheless, there is great concern about the spread of ASFV infection in Asia: after the first occurrences of the disease in China, the largest world’s pork producer, a number of bordering countries notified many outbreaks and the epidemiological situation appears far from being effectively controlled (36).

African swine fever epidemiology is thus very complex, determining different epidemiological patterns of infection when considering Africa or Europe. From an epidemiological point of view, three independent epidemiologic cycles (sylvatic, tick–pig, and domestic) have been described (36) until recently in literature. After the ASF epizootic occurred in Central and Eastern EU Member States, the researchers could consider a fourth cycle in addition to the three already recognized: the “wild boar–habitat cycle” (37). This cycle focuses on the wild boar population and its habitat as a virus reservoir (38). Different epidemiological scenarios can be outlined according to the geographical area, the species involved, the transmission route, and the risk factors identified for ASF persistence and spread.

African swine fever can be controlled and eradicated through classical surveillance and control measures, as demonstrated in the past experiences of countries worldwide if the main epidemiological target remains the domestic pig population. Classical measures are based on disease control methods, including surveillance strategies, epidemiological investigation, tracing and culling of pigs in infected holdings, in combination with strict quarantine and biosecurity measures on domestic pigs, holdings, and the control of animal movement. These measures are currently in force within the EU legal framework for ASF control, as laid down by Council Directive 2002/60/EC (39). The Directive also requires that Member States develop and implement plans for the eradication of the disease (40). These measures were effective in addressing a few outbreaks, as showed in the Czech Republic's first experience of ASF. However, evidence also suggest that this strategy is difficult to sustain for a long period in endemic situations, such as in the Baltic States and Poland, where the disease affects larger areas (41). A successful strategy in this scenario has not yet been found. In fact, the experiences collected in recent years demonstrated that the involvement of wild boar population in the viral spread hampers the eradication and, for sure, it is a relevant risk factor facilitating the virus spread across the country borders (41).

Therefore, an efficient strategy for ASF prevention or control should be based on deep knowledge of target domestic and wild population, of environmental conditions and type of swine sector (41). Nevertheless, all the strategies must take in count that the disease knows no bounds and a common policy should be defined (41). The sole continuous presence of viral circulation in Africa gives the evidence that the risk of new incursions of the disease are possible and the current epidemiological situation multiplies the chances of ASF virus spread all over the world (41).

Currently, in the European context there is a need to better understand the evolution of ASF, the dynamics of the disease in wild boar and the key for successful interventions that have contributed to mitigating ASF impact (42). A commercial vaccine to control ASF is not yet available, and researchers are under pressure to obtain cost-effective, safe and efficient vaccines for the different epidemiological scenarios (Frontiers, 2020). Other gaps to explain the current challenges, concern the areas of molecular epidemiology, environmental modelling, transmission, pathology, wild boar-domestic pig interaction, socio-economic impact, prevention, diagnosis, and surveillance (42).

 

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Maria Luisa Danzetta
Centro Operativo Veterinario per l'Epidemiologia, Programmazione, Informazione e Analisi del Rischio
Istituto Zooprofilattico Sperimentale dell'Abruzzo e del Molise "G. Caporale"

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