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The possible route of introduction of bluetongue virus serotype 3 into Sicily by windborne transportation of infected Culicoides spp.

ABSTRACT: In October 2017, the first outbreak of bluetongue virus serotype 3 (BTV-3) began in Italy, specifically in western Sicily. The route of entrance remains unclear, although since 2016 the same strain had been circulating only 150 km away, on the Tunisian peninsula of Cape Bon. The present analysis assessed the feasibility that wind could have carried BTV-3-infected Culicoides spp. from Tunisia to Sicily. An advection-deposition-survival (ADS) model was used to estimate when and where Culicoides spp. were likely to be introduced prior to the first BTV-3 report in Italy. Additionally, the Hybrid Single-Particle Lagrangian Integrated Trajectory (HYSPLIT) model was used to support ADS outputs. The modelling suggests that during September 2017, strong wind currents and suitable climatic conditions could have allowed the transportation of Culicoides spp. from BTV-3-infected areas in Tunisia into Sicily. ADS simulations suggest that particles could have reached the province of Trapani in western Sicily on 2 and 12 September. These simulations suggest the feasibility of aerial transportation of infected Culicoides spp. from Tunisia into Sicily. They demonstrate the suitability of the ADS model for retrospective studies of long-range transportation of insects across large water bodies, which may enhance the early detection of vectorial disease introduction in a region.

SUBMITTER: Aguilar-Vega C

PROVIDER: S-EPMC6850078 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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The possible route of introduction of bluetongue virus serotype 3 into Sicily by windborne transportation of infected Culicoides spp.

Aguilar-Vega Cecilia C Fernández-Carrión Eduardo E Sánchez-Vizcaíno José M JM

Transboundary and emerging diseases 20190429 4

In October 2017, the first outbreak of bluetongue virus serotype 3 (BTV-3) began in Italy, specifically in western Sicily. The route of entrance remains unclear, although since 2016 the same strain had been circulating only 150 km away, on the Tunisian peninsula of Cape Bon. The present analysis assessed the feasibility that wind could have carried BTV-3-infected Culicoides spp. from Tunisia to Sicily. An advection-deposition-survival (ADS) model was used to estimate when and where Culicoides sp ...[more]

PMID: 30973674

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Project description:Outbreaks of the European Bluetongue virus (BTV) serotype 8 (BTV-8), which are characterized by activity cycles separated by years of inactivity, may be influenced by genetic changes of the virus or by herd immunity. BTV activity in Israel is characterized by similar dynamics, but differs from European countries in its vector population, environmental conditions, and lack of cattle vaccination against this serotype. Comparison of these two geographical systems and characterization of their epidemiological connection is therefore of high interest in-order to better understand the factors influencing BTV-8 evolution. BTV-8, closely related to the European strain, was introduced to Israel in 2008. It was at the center of BT outbreaks in 2010 and 2015-2016 and thereafter was lastly isolated in Israel in 2019. We performed genetic analyses of twelve BTV-8 Israeli strains isolated between 2008 and 2019 and compared them with published sequences of BTV-8 isolated in other countries. The analysis revealed a single introduction of BTV-8 into Israel and thereafter extensive occurrence of genomic drifts and multiple reassortments with local BTV strains. Comparison of the Israeli and Cypriot BTV-8 from 2015 to 2016 suggests transmission of the virus between the two countries and a separate and parallel development from European or other Israeli BTV-8 strains. The parallel development of other BTV-8 strains was demonstrated by the identification of the Israeli BTV-8 ISR-1194/1/19 strain, which exhibited common origin with reassorted Israeli BTV-8 strains from 2010 and additional reassortment of seven segments. In order to reveal the source of BTV-8 introduction into Israel we performed BEAST analysis which showed that a probable common ancestor for both European and Israeli BTV-8 presumably existed in 2003-2004. In 2019, a possible new introduction occurred in Israel, where a novel BTV-8 strain was detected, sharing ~95% identity by segments 2 and 6 with Nigerian BTV-8NIG1982/07 and European-Middle Eastern strains. The results of the study indicate that Israel and neighboring countries consist a separate environmental and evolutionary system, distinct from European ones.

Project description:Bluetongue virus (BTV) and epizootic haemorrhagic disease virus (EHDV) are related orbiviruses, transmitted between their ruminant hosts primarily by certain haematophagous midge vectors (Culicoides spp.). The larger of the BTV outer-capsid proteins, 'VP2', can be cleaved by proteases (including trypsin or chymotrypsin), forming infectious subviral particles (ISVP) which have enhanced infectivity for adult Culicoides, or KC cells (a cell-line derived from C. sonorensis). We demonstrate that VP2 present on purified virus particles from 3 different BTV strains can also be cleaved by treatment with saliva from adult Culicoides. The saliva proteins from C. sonorensis (a competent BTV vector), cleaved BTV-VP2 more efficiently than those from C. nubeculosus (a less competent/non-vector species). Electrophoresis and mass spectrometry identified a trypsin-like protease in C. sonorensis saliva, which was significantly reduced or absent from C. nubeculosus saliva. Incubating purified BTV-1 with C. sonorensis saliva proteins also increased their infectivity for KC cells ∼10 fold, while infectivity for BHK cells was reduced by 2-6 fold. Treatment of an 'eastern' strain of EHDV-2 with saliva proteins of either C. sonorensis or C. nubeculosus cleaved VP2, but a 'western' strain of EHDV-2 remained unmodified. These results indicate that temperature, strain of virus and protein composition of Culicoides saliva (particularly its protease content which is dependent upon vector species), can all play a significant role in the efficiency of VP2 cleavage, influencing virus infectivity. Saliva of several other arthropod species has previously been shown to increase transmission, infectivity and virulence of certain arboviruses, by modulating and/or suppressing the mammalian immune response. The findings presented here, however, demonstrate a novel mechanism by which proteases in Culicoides saliva can also directly modify the orbivirus particle structure, leading to increased infectivity specifically for Culicoides cells and, in turn, efficiency of transmission to the insect vector.

Dataset Information

The possible route of introduction of bluetongue virus serotype 3 into Sicily by windborne transportation of infected Culicoides spp.

Publications

The possible route of introduction of bluetongue virus serotype 3 into Sicily by windborne transportation of infected Culicoides spp.

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