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