No hasty solutions for African swine fever
Dolores Gavier-Widén, Karl Ståhl & Linda Dixon, Science Magazine
Science 07 Feb 2020: Vol. 367, Issue 6478, pp. 622-624
An epidemic of African swine fever (ASF), a lethal viral hemorrhagic disease of swine, is devastating pig production in Asia and is a global threat. The ASF virus (ASFV) reached the European Union (EU) in 2014, affecting pig production. ASFV continues to spread through wild boar (Sus scrofa), which form interconnected populations across Europe and which maintain the infection and can cause infection in pigs. A vaccine is not yet available and is urgently needed, both for pigs and wild boar. Live attenuated virus (LAV) vaccines are the most promising way forward in the short term (1), and recent advances have been made in constructing gene-deleted LAV vaccines. Naturally attenuated LAVs have also been shown to confer protection as vaccines in pigs and wild boar. However, previous experience with vaccination failures using naturally attenuated LAVs emphasizes the need for caution because of safety concerns.
ASF was first described in Kenya in 1921 (2) and today is endemic in most countries of sub-Saharan Africa. Local dispersion of the virus can occur through contact between animals, whereas long-distance spread results from the movement of contaminated pork products, in which the virus can survive for months or years depending on temperature. Feeding of food waste to pigs can thus establish new foci of infection. Twenty-four genotypes of ASFV have been identified. A genotype I ASFV escaped twice from West Africa into Portugal in 1957 and 1960. The later infection affected the Iberian Peninsula, where the virus persisted for more than 30 years, spreading sporadically to other countries in Europe, the Caribbean, and Brazil. ASF was eradicated from most of these countries by the mid-1990s through culling and movement bans of pigs and their products. However, genotype I ASFV still persists in the Italian island of Sardinia.
A new transcontinental spread of ASFV, this time genotype II, occurred from southeast Africa into Georgia in 2007, probably through catering waste brought by a ship (3). Subsequently, the virus spread to the Caucasus, the Russian Federation, Ukraine, and Belarus. It entered the EU Baltic states and Poland in 2014, where the virus is maintained in wild boar populations. Continued spread to other EU countries, including Romania and Bulgaria, has also involved the domestic pig population, with outbreaks mainly in small farms. The natural movements of infected wild boar result in local expansion of the virus; the infection front has been estimated to advance at ∼1 to 2 km per month (4). In 2018, genotype II ASFV entered China, which contains nearly half of the world's pig population, with catastrophic socioeconomic consequences, particularly for small and underprivileged pig farmers (5) who comprise ∼30% of the 26 million pig farmers in China (6). It then dispersed further to Southeast Asia. A year after its incursion into Asia, genotype II ASFV had caused the death or destruction of ∼5 million pigs (6) and an estimated reduction of 40% of the Chinese pig herd, thus affecting global food markets (7).
It was not until genotype II ASFV entered the EU in 2014 that the capacity of wild boar to maintain circulation of the virus independently of outbreaks in domestic pigs was revealed (8). Control of ASFV in wild boar is challenging and has not been achieved in most of the affected countries. There are exceptions, however: The Czech Republic was declared officially free from ASF by the EU ∼18 months after the first report, and disease spread seems to have halted in Belgium. Early detection, prompt and coordinated implementation of measures to restrict movements of potentially infected wild boar, and public-access restrictions to infected areas to prevent further ASFV spread are key factors for success. Such measures include carcass finding and removal, fencing, and strategic wild boar hunting and culling operations (4).
A combination of direct transmission between wild boar and indirect transmission by contact with infected wild boar carcasses or wild boar scavenging on carcasses (intraspecies scavenging) provides long-term persistence of ASFV in the environment (8). Thus, infection in pigs can potentially occur not only from their contact with wild boar—for example, in outdoor holdings—but also from transmission of ASFV from the environment through, for example, vehicles, shoes, and feed. High-biosecurity pig production is better protected from ASF, but it is put at risk if the environment around farms is contaminated, and even such establishments have been infected in Europe (9).
Populations of wild boar have been expanding throughout Europe during the past 40 years (10). Sustainable reduction in free-ranging wild boar populations is very difficult because wild boar have a high reproductive rate, such that culling results in compensatory growth of the population and influx from adjacent areas. In addition, intensive hunting leads to dispersion of wild boar and can result in expansion of the infected area. ASFV has also been reported in wild boar in China, Far East Russia, and the northern region of South Korea (11). However, information about populations of wild boar and the epidemiology of ASF in Asia is scarce.
Developing an ASFV vaccine presents many challenges. ASFV is a large, double-stranded DNA virus of the Asfarviridae family (12). The virus is complex; its genome is about 170 to 190 kilobases in length and encodes ∼170 proteins, of which ∼70 are packaged into the multilayered virus particle (12). Identification of antigens that might elicit vaccine-mediated protection among this very large number of proteins is difficult. Immune correlates of protection in swine to enable evaluation of vaccine candidates are insufficiently identified. Moreover, current experimental testing of vaccine candidates can only be conducted in pigs and wild boar and in high-containment facilities.
An ASFV vaccine for wild boar must also overcome the challenges of vaccinating wildlife...