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

Authors: PEREIRIA DE OLIVEIRA, REMI - Health, Environment And Microbiology Laboratory; HUTET, EVELYNE - Health, Environment And Microbiology Laboratory; PABOEUF, FREDERIC - Health, Environment And Microbiology Laboratory; DUHAYON, MAXIME - Cirad, France; BOINAS, FERNANDO - Non ARS Employee; Perez De Leon, Adalberto - Beto; FILATOV, SERHII - National Scientific Center; VIAL, LAURENCE - Cirad, France; LE POTIER, MARIE-FREDERIQU - Health, Environment And Microbiology Laboratory

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/8/2019
Publication Date: 11/27/2019
Citation: Pereiria De Oliveira, R., Hutet, E., Paboeuf, F., Duhayon, M., Boinas, F., Perez De Leon, A.A., Filatov, S., Vial, L., Le Potier, M. 2019. 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. PLoS One. 14(11):e0225657. https://doi.org/10.1371/journal.pone.0225657.
DOI: https://doi.org/10.1371/journal.pone.0225657

Interpretive Summary: African swine fever (ASF) is a lethal hemorrhagic disease in domestic pigs and wild boars caused by African swine fever virus (ASFV), which threatens the swine industry worldwide. In certain parts of Africa where it is established, infected soft ticks species in the genus Ornithodoros are vectors transmitting ASFV to local wild pig species. However, the vector competence of Ornithodoros soft ticks native to Eurasia, where ASFV emerged recently, remains unknown. Here, we describe the outcomes of experiments where the vector competence of Ornithodoros soft ticks native to Eurasia for ASFV strains circulating in the region was tested. Comparative experiments with known soft tick vectors and several ASFV strains showed that O. verrucosus from Eurasia was not able to transmit ASFV when biting susceptible domestic pigs. However, pigs showed clinical signs of ASF when they were injected with the liquid fraction obtained from crushed O. verrucosus that had obtained a blood meal when biting pigs that had ASFV circulating in their blood. Transmission to pigs through biting during blood feeding is required to document that an infected Ornithodoros soft tick is a competent vector of ASFV.

Technical Abstract: African swine fever (ASF) is a lethal hemorrhagic fever disease in domestic pigs and wild boars caused by African swine fever virus (ASFV), which threatens the swine industry. In its native African endemic area, ASFV is naturally circulating between soft ticks of the genus Ornithodoros, especially in the O. moubata complex, and wild reservoir suids that are bitten by infected soft ticks inhabiting the same burrows. While the ability of some Afrotropical soft ticks to transmit and maintain ASFV is established, the vector status of Palearctic soft ticks remains unknown for ASFV strains currently circulating in Eurasia. The Iberian O. erraticus is a known vector and reservoir of ASFV, but ASFV re-emerged in Europe after eradication resulting in the circulation of new ASFV strains that have been spreading westward since 2007. Therefore, we conducted transmission trials with the Palearctic soft tick species O. erraticus and O. verrucosus, and the Afrotropical O. moubata, that fed on viremic pigs infected with highly virulent ASFV strains including one directly from Africa (Liv13/33), and three from Eurasia 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 did not 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. Persistent infection for several months reaffirms that the infectious status of a soft tick species is only part of the data required to assess its vector competence for ASFV.