vincent.gervasi@gmail.com
Running title: African swine fever endemic persistence mechanisms. Summary: African swine fever (ASF), is a serious global concern from an ecological and economic point of view. While it is well established that its main transmission routes comprise contact between infected and susceptible animals and transmission through contaminated carcasses, the specific mechanism leading to its long-term persistence is still not clear. Among others, a proposed mechanism involves the potential role of convalescent individuals, which would be able to shed the virus after the end of the acute infection. Using a spatially explicit, stochastic, individual-based model, we tested: 1) if ASF can persist when transmission occurs only through infected wild boars and infected carcasses; 2) if the animals that survive ASF can play a relevant role in increasing ASF persistence chances; 3) how hunting pressure can affect the ASF probability to persist. The scenario in which only direct and carcass-mediated transmission were contemplated had 52% probability of virus persistence 10 years after the initial outbreak. The inclusion of survivor-mediated transmission corresponded to slightly higher persistence probabilities (57%). ASF prevalence during the endemic phase was generally low, ranging 0.1-0.2%. The proportion of seropositive individuals gradually decreased with time and ranged 4.5 – 6.6%. Our results indicate that direct and carcass-mediated infection routes are sufficient to explain and justify the long-term persistence of ASF at low wild boar density and the ongoing geographic expansion of the disease front in the European continent. During the initial years of an ASF outbreak, hunting should be carefully evaluated as a management tool, in terms of potential benefits and negative side-effects, and combined with an intensive effort for the detection and removal of wild boar carcasses. During the endemic phase, further increasing hunting effort should not be considered as an effective strategy. Additional effort should be dedicated to finding and removing as many wild boar carcasses as possible.
Keywords : ASF transmission, convalescent, chronic carrier, individual-based model, Sus scrofa, virus persistence.
INTRODUCTION
African swine fever (ASF) and its ongoing spread in several European and Asian countries (Depner et al., 2017; Lu et al., 2020; Penrith, 2020) is a serious global concern from an ecological and economic point of view (Guberti et al., 2019; Pitts and Whitnall, 2019). The disease is caused by a highly virulent virus of the Asfaviridae family, which affects wild boar (Sus scrofa ), domestic pigs and African wild suids (Blome et al., 2013; de Carvalho Ferreira et al., 2013), leading to almost 100% lethality of infected individuals (Blome et al., 2013). After its first Eurasian appearance in Georgia in 2007, the disease has spread to the Russian Federation through trans-Caucasian countries, to Belarus and Ukraine, then to Belarus and Ukraine, Lithuania, Estonia, Latvia, Poland, Czech Republic, Hungary, Romania, Bulgaria, Belgium, Slovakia, Greece, Serbia and Germany (Depner et al., 2017; Blome et al., 2020). A similar eastward spreading is occurring in Asia, currently affecting China, Hong Kong, North Korea, South Korea, Laos, Vietnam, Myanmar, Cambodia, Indonesia, Philippines, Timor-Leste, Papua New Guinea, and India (Blome et al., 2020; Penrith, 2020).
At the arrival of the virus in the EU, ASF was expected to exhibit the typical epidemic pattern of highly virulent acute infections, which often generate self-limiting localized epidemic waves with a high probability of a rapid fade-out. Such expectation was justified by the fact that the wild boar was the sole infected host, and by the absence of a competent arthropod vector (Gabriel et al., 2011; Chenais et al., 2019; O’Neill et al., 2020). After few years of field experiences, however, it is now evident that the virus is able to persist in low density wild boar populations several years after the first epidemic outbreak, with an endemic prevalence usually around 1%, although some local variation has been observed (Nurmoja, Schulz et al., 2017; Pautienius et al., 2018). The virus endemic persistence at low wild boar density is enhanced by its stability at a wide range of environmental conditions (Mazur-Panasiuk et al., 2019). ASF virus has been shown to persist in frozen meat for several months, and may persist in carcasses, forest soil and water for several weeks (Mebus et al., 1997) allowing an efficient indirect transmission through both contaminated carcasses and the environment (De Carvalho Ferreira et al., 2014; Probst et al., 2017; Carlson et al., 2020; Fischer et al., 2020). However, the inner mechanism leading to the long-term persistence at both low wild boar density and prevalence is still not clear, as virus persistence in the environment and in wild boar carcasses is highly variable and mediated by wild boar behaviour, while the endemic persistence of the virus is invariably observed (Blome et al., 2020). Several alternative hypotheses have been advanced and are currently being explored, but no one has been confirmed and validated so far.
Given the summer peaks observed in several countries, one hypothesis is that the ASF virus might have found an alternative competent arthropod vector species that could replace the Ornithodoros ticks, absent in Eurasia. Soft and hard ticks, different species of flies, tabanids and mosquitoes have been proposed (Bonnet et al., 2020), but arthropods do not influence the spread of the virus in wild boar populations (Herm et al., 2021). Another hypothesis relies on the possibility that during its spreading in recent years, the ASF virus might have gone through a process of attenuation, thus reducing its virulence and lethality (Gallardo et al., 2017; Nurmoja, Petrov et al., 2017). Although different wild boar mortality rates have been observed during the ASF spreading in different parts of Estonia and in Latvia (Zani et al., 2018; Gallardo et al., 2019), suggesting the possibility that moderately virulent variants of the ASF virus might be present in the population, no confirmation has been provided so far that a low virulent ASF virus might play a role in its persistence (Blome et al., 2020). Moreover, modelling work shows that, even if the two variants were both present in a wild boar population, the attenuated ASF virus would rapidly go extinct at the expense of the highly virulent one (Nielsen et al., 2021).
A third proposed mechanism involves the potential role of infectious survivors, which would still be able to shed the virus after the end of the acute infection, thus favouring the long-term persistence of the disease. Current knowledge (Sánchez-Vizcaíno et al., 2015; Ståhl et al., 2019) suggests that ASF survivors (hereafter called convalescents) may still carry and transmit the virus after the acute disease phase, but then fully recover from the infection and become immune for life (i.e. category 2 according to Stahl et al., 2019). The possibility that some of them might develop a persistent infection, accompanied by a subacute, chronic disease, has also been proposed (Arias and Sánchez-Vizcaíno, 2002; Category 1 according to Sthal et al., 2019).
The role of infectious survivors is therefore still discussed. It is known that the virus can still be present in survivors for roughly 60–70 days and up to 91days (Petrov et al., 2018). However, lab experiments suggest a very low probability of infection between convalescent and susceptible individuals, and no virus survival beyond 100 days (Nurmoja, Petrov et al., 2017; Petrov et al., 2018; Ståhl et al., 2019). Other experiments on domestic pigs in a controlled environment, though, seem to indicate that transmission of the ASF virus via infectious survivors does occur at least in a 55 days post-exposure window (Eblé et al., 2019). Lacking a conclusive evidence, though, the possibility that surviving wild boars carrying both virus and antibodies could shed and transmit the virus, even though at a very low rate, cannot be disregarded (Blome et al., 2020).
The lack of a clear and verified persistence mechanism for ASF also has consequences on the available management options for its containment and eradication. Currently, carcass removal and wild boar culling are the two main available strategies implemented in the affected areas (Lange et al., 2018), but their effectiveness strongly depends on the relative importance of the different ASF transmission routes. Wild boar culling, which aims at a reduction in wild boar density, mainly affects virus transmission rates between live individuals; therefore, the effectiveness of culling as a control measure depends on how relevant infected and convalescent individuals are in ASF persistence. Carcass removal, on the other hand, only affects the ASF transmission route which involves dead wild boar; its effectiveness, therefore, strongly depends on the importance of carcass-mediated transmission in ASF persistence. Accordingly, it is of paramount importance that all the ASF persistence mechanisms be determined and ranked.
In this paper, we explored the relative role of different ecological and epidemiological factors in the long- term persistence of ASF in wild boar populations. We first assessed the likelihood of the disease to persist through direct and carcass-mediated infection, but without the contribution of any survivor-mediated transmission; in a second scenario we explored the potential for ASF convalescents to play a role in disease persistence. To this aim, we ran and analysed a spatially explicit, stochastic, individual-based model, which mimicked the demography and spatial dynamics of a wild boar population, the epidemiology of the ASF virus through the different proposed transmission routes, and population management through wild boar harvest. Finally, we assessed the sensitivity of ASF persistence to changes in all the main ecological, epidemiological, and management-related parameters, including hunting rate, thus ranking them in order of importance as determinants of ASF persistence probability. We discuss the implications of our results for the disease surveillance and control in the affected countries, and for the ongoing effort to limit its spread in new, still unaffected areas.
METHODS