Comparative vector competence of the Afrotropical soft tick Ornithodoros moubata and Palearctic species, O. erraticus and O. verrucosus, for African swine fever virus strains circulating in Eurasia

Abstract

African swine fever (ASF) is a lethal hemorrhagic disease in domestic pigs and wild suids caused by African swine fever virus (ASFV), which threatens the swine industry globally. In its native African enzootic foci, ASFV is naturally circulating between soft ticks of the genus Ornithodoros, especially in the O. moubata group, and wild reservoir suids, such as warthogs (Phacochoerus spp.) that are bitten by infected soft ticks inhabiting their burrows. While the ability of some Afrotropical soft ticks to transmit and maintain ASFV is well established, the vector status of Palearctic soft tick species for ASFV strains currently circulating in Eurasia remains largely unknown. For example, the Iberian soft tick O. erraticus is a known vector and reservoir of ASFV, but its ability to transmit different ASFV strains has not been assessed since ASF re-emerged in Europe in 2007. Little is known about vector competence for ASFV in other species, such as O. verrucosus, which occurs in southern parts of Eastern Europe, including Ukraine and parts of Russia, and in the Caucasus. Therefore, we conducted transmission trials with two Palearctic soft tick species, O. erraticus and O. verrucosus, and the Afrotropical species O. moubata. We tested the ability of ticks to transmit virulent ASFV strains, including one of direct African origin (Liv13/33), and three from Eurasia that had been involved in previous (OurT88/1), and the current epizooties (Georgia2007/1 and Ukr12/Zapo). Our experimental results showed that O. moubata was able to transmit the African and Eurasian ASFV strains, whereas O. erraticus and O. verrucosus failed to transmit the Eurasian ASFV strains. However, naïve pigs showed clinical signs of ASF when inoculated with homogenates of crushed O. erraticus and O. verrucosus ticks that fed on viraemic pigs, which proved the infectiousness of ASFV contained in the ticks. These results documented that O. erraticus and O. verrucosus are unlikely to be capable vectors of ASFV strains currently circulating in Eurasia. Additionally, the persistence of infection in soft ticks for several months reaffirms that the infectious status of a given tick species is only part of the data required to assess its vector competence for ASFV.

African swine fever virus-like integrated elements in a soft tick genome – an ancient virus vector arms race?

“…In addition to the hypothesised protective function, our results might suggest that the ASFLI-elementbased protection could be selective for specific ASFV genotypes and therefore different in O. porcinus and O. moubata. This observation is supported by data from the literature in which clear differences were observed in tick infection rates using different ASFV genotype isolates and tick species (44)(45)(46).…”

“…and experiments with the Pirbright and French O. moubata colonies and genotype I viruses (46)(47)(48) further strengthen this hypothesis.…”

No Experimental Evidence of Co-Feeding Transmission of African Swine Fever Virus between Ornithodoros Soft Ticks

“…The resulting O. moubata-Liv13/33 tick-virus pair (OmL) was used as the "source" for the co-feeding transmission trial 8 months post infection. OmL was previously confirmed to be competent to transmit ASFV to pigs through biting, 2 and 8 months post infection [24]. Furthermore, all OmL tested by real-time PCR were highly positive for ASFV [24].…”

“…The experimental design defined in the study was able to guarantee the reliability of the results obtained. Indeed, to maximize the success of transmission we used the African tick species O. moubata, which is known to acquire the Liv13/33 virus strain in salivary glands after infectious engorgement [21] and to transmit this virus to domestic pigs through biting [24]. To mimic as much as possible the natural conditions leading to tick infection through co-feeding [26], the transmission trial was carried out in small Petri dishes conducive to natural soft tick aggregation during the blood meal [27].…”

“…A specific real-time polymerase chain reaction (PCR) for the detection of the ASFV VP72 gene [25] and beta-actin of ticks was used on individual DNA extracts from both tick samples, OmCF and OmCTR, two months after the co-feeding trial, as previously described [24]. Tick excretions and/or secretions collected from the Petri dishes were also tested for viral genome detection.…”