Temperature dependence of the extrinsic incubation period of orbiviruses in Culicoides biting midges

Abstract

Background: The rate at which viruses replicate and disseminate in competent arthropod vectors is limited by the temperature of their environment, and this can be an important determinant of geographical and seasonal limits to their transmission by arthropods in temperate regions.

Methodology/principal findings: Here, we present a novel statistical methodology for estimating the relationship between temperature and the extrinsic incubation period (EIP) and apply it to both published and novel data on virus replication for three internationally important orbiviruses (African horse sickness virus (AHSV), bluetongue virus (BTV) and epizootic haemorrhagic disease virus (EHDV)) in their Culicoides vectors. Our analyses show that there can be differences in vector competence for different orbiviruses in the same vector species and for the same orbivirus in different vector species. Both the rate of virus replication (approximately 0.017-0.021 per degree-day) and the minimum temperature required for replication (11-13°C), however, were generally consistent for different orbiviruses and across different Culicoides vector species. The estimates obtained in the present study suggest that previous publications have underestimated the replication rate and threshold temperature because the statistical methods they used included an implicit assumption that all negative vectors were infected.

Conclusions/significance: Robust estimates of the temperature dependence of arbovirus replication are essential for building accurate models of transmission and for informing policy decisions about seasonal relaxations to movement restrictions. The methodology developed in this study provides the required robustness and is superior to methods used previously. Importantly, the methods are generic and can readily be applied to other arbovirus-vector systems, as long as the assumptions described in the text are valid.

Figure 1. Observed and expected number of Culicoides sonorensis with a fully disseminated BTV-9 infection when reared at different temperatures.

(A,C,E,G) Number (out of 25) of C. sonorensis with a fully disseminated infection. (B,D,F,H) Observed (blue circles) and expected (posterior median (red diamonds) and 95% credible interval (error bars)) number of C. sonorensis with a fully disseminated infection. Results are shown for midges reared at (A,B) 15°C, (C,D) 20°C, (E,F) 25°C, or (G,H) 30°C; those for midges reared at 12°C (no midges with a fully disseminated infection) are not shown.

Figure 2. Temperature dependence of the extrinsic incubation period for six orbiviruses.

(A) Temperature dependence of the reciprocal of the mean EIP (equation (2) using posterior median estimates for α and T _min). Virus (and serotype) is indicated by the line colour (see legend). (B) Posterior median (bars) and 95% credible limits (error bars) for the threshold temperature for virus replication. Vector species is indicated by the bar colour (see legend).