Abstract
African swine fever is a haemorrhagic disease in pig production that can have disastrous financial consequences for farming. No vaccines are currently available and animal slaughtering or area zoning to restrict risk-related movements are the only effective measures to prevent the spread of the disease. Ornithodoros soft ticks are known to transmit the African swine fever virus (ASFV) to pigs in farms, following the natural epidemiologic cycle of the virus. Tick saliva has been shown to modulate the host physiological and immunological responses during feeding on skin, thus affecting viral infection. To better understand the interaction between soft tick, ASFV and pig at the bite location and the possible influence of tick saliva on pig infection by ASFV, salivary gland extract (SGE) of Ornithodoros porcinus, co-inoculated or not with ASFV, was used for intradermal auricular inoculation. Our results showed that, after the virus triggered the disease, pigs inoculated with virus and SGE presented greater hyperthermia than pigs inoculated with virus alone. The density of Langerhans cells was modulated at the tick bite or inoculation site, either through recruitment by ASFV or inhibition by SGE. Additionally, SGE and virus induced macrophage recruitment each. This effect was enhanced when they were co-inoculated. Finally, the co-inoculation of SGE and virus delayed the early local spread of virus to the first lymph node on the inoculation side. This study has shown that the effect of SGE was powerful enough to be quantified in pig both on the systemic and local immune response. We believe this model should be developed with infected tick and could improve knowledge of both tick vector competence and tick saliva immunomodulation.
Highlights
Complex interactions have been described in many host-vector-pathogen associations
The mean daily weight gain (MDWG) was evaluated and all the infected groups (ID African swine fever virus (ASFV), ID ASFV+salivary gland extract (SGE)) lost weight from 3 dpi whatever the virus doses expressed in mean ± standard deviation (SD), -0.9 ± 0.1 (n = 5) kg/day for the high ASFV dose (HD) trial and -0.7 ± 0.1 (n = 4) kg/day for the low ASFV dose (LD) trial, whereas the non-infected groups (NEG, TICK, ID SGE, ID MEM) gained weight up to 8 dpi (0.9 ± 0.1 (n = 7) kg/day)
To recreate as closely as possible natural conditions of contamination by tick bites, we selected a combination of ticks and viral isolate collected from a restricted geographical zone (Madagascar), along with intradermal administration of a low virus dose presumed to better mimic the quantity of virus inoculated by ticks during their blood meal [27]
Summary
Complex interactions have been described in many host-vector-pathogen associations. Most of these associations are highly adaptive, especially for vectors and pathogens that try to escape host defence responses by particular behavioural or immunological control strategies [1].Ticks play an important role in pathogen transmission and emergence and are considered of great importance in veterinary and public health domains [2]. The host reacts to the dilacerations of its own skin barrier by ticks’ mouthparts and activates an early response to infestation at the bite site [3]. This immune response involves haemostasis and inflammation modulation, as well as the development of cellular and humoral responses through the early recruitment of mononuclear phagocytic cells and polymorphonuclear cells, the maturation of antigen-presenting cells (APCs), the activation of mast cells, and other modulation of antibodies, cytokines, chemokines and the complement system [4,5]. Ticks produce pharmacologically active molecules in their saliva to escape host immune defences [6], incidentally improving pathogen transmission [7]
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