Seasonal and spatial heterogeneities in host and vector abundances impact the spatiotemporal spread of bluetongue.

Bluetongue (BT) can cause severe livestock losses and large direct and indirect costs for farmers. To propose targeted control strategies as alternative to massive vaccination, there is a need to better understand how BT virus spread in space and time according to local characteristics of host and vector populations. Our objective was to assess, using a modelling approach, how spatiotemporal heterogeneities in abundance and distribution of hosts and vectors impact the occurrence and amplitude of local and regional BT epidemics. We built a reaction-diffusion model accounting for the seasonality in vector abundance and the active dispersal of vectors. Because of the scale chosen, and movement restrictions imposed during epidemics, host movements and wind-induced passive vector movements were neglected. Four levels of complexity were addressed using a theoretical approach, from a homogeneous to a heterogeneous environment in abundance and distribution of hosts and vectors. These scenarios were illustrated using data on abundance and distribution of hosts and vectors in a real geographical area. We have shown that local epidemics can occur earlier and be larger in scale far from the primary case rather than close to it. Moreover, spatial heterogeneities in hosts and vectors delay the epidemic peak and decrease the infection prevalence. The results obtained on a real area confirmed those obtained on a theoretical domain. Although developed to represent BTV spatiotemporal spread, our model can be used to study other vector-borne diseases of animals with a local to regional spread by vector diffusion.

Seasonal spread and control of Bluetongue in cattle.

Bluetongue is a seasonal midge-borne disease of ruminants with economic consequences on herd productivity and animal trade. Recently, two new modes of transmission have been demonstrated in cattle for Bluetongue virus serotype 8 (BTV8): vertical and pseudo-vertical transmission. Our objective was to model the seasonal spread of BTV8 over several years in a homogeneous population of cattle, and to evaluate the effectiveness of vaccination strategies. We built a deterministic mathematical model accounting for the seasonality in vector abundance and all the modes of transmission. We proposed a counterpart of the basic reproduction number (R(0)) in a seasonal context (R(S)). Set A(t) is the number of secondary cases produced by a primary case introduced at time t. R(S) is the average of A(t). It is a function of midge abundance and vaccination strategy. We also used A*, the maximum of A(t), as an indicator of the risk of an epidemic. Without vaccination, the model predicted a large first epidemic peak followed by smaller annual peaks if R(S)>1. When R(S)<1, small epidemics could occur if A* >1. Vaccination reduced R(S) and A* to less than one, but almost perfect vaccine efficacy and coverage were required to ensure no epidemics occurred. However, a lower coverage resulting in R(S)>1 could decrease infection prevalence. A further step would be to optimize vaccination strategies by targeting an appropriate period of the year to implement the vaccination.

A Stochastic Model to Study Rift Valley Fever Persistence with Different Seasonal Patterns of Vector Abundance: New Insights on the Endemicity in the Tropical Island of Mayotte.

Rift Valley fever (RVF) is a zoonotic vector-borne disease causing abortion storms in cattle and human epidemics in Africa. Our aim was to evaluate RVF persistence in a seasonal and isolated population and to apply it to Mayotte Island (Indian Ocean), where the virus was still silently circulating four years after its last known introduction in 2007. We proposed a stochastic model to estimate RVF persistence over several years and under four seasonal patterns of vector abundance. Firstly, the model predicted a wide range of virus spread patterns, from obligate persistence in a constant or tropical environment (without needing vertical transmission or reintroduction) to frequent extinctions in a drier climate. We then identified for each scenario of seasonality the parameters that most influenced prediction variations. Persistence was sensitive to vector lifespan and biting rate in a tropical climate, and to host viraemia duration and vector lifespan in a drier climate. The first epizootic peak was primarily sensitive to viraemia duration and thus likely to be controlled by vaccination, whereas subsequent peaks were sensitive to vector lifespan and biting rate in a tropical climate, and to host birth rate and viraemia duration in arid climates. Finally, we parameterized the model according to Mayotte known environment. Mosquito captures estimated the abundance of eight potential RVF vectors. Review of RVF competence studies on these species allowed adjusting transmission probabilities per bite. Ruminant serological data since 2004 and three new cross-sectional seroprevalence studies are presented. Transmission rates had to be divided by more than five to best fit observed data. Five years after introduction, RVF persisted in more than 10% of the simulations, even under this scenario of low transmission. Hence, active surveillance must be maintained to better understand the risk related to RVF persistence and to prevent new introductions.

How much can diptera-borne viruses persist over unfavourable seasons?

Diptera are vectors of major human and animal pathogens worldwide, such as dengue, West-Nile or bluetongue viruses. In seasonal environments, vector-borne disease occurrence varies with the seasonal variations of vector abundance. We aimed at understanding how diptera-borne viruses can persist for years under seasonal climates while vectors overwinter, which should stop pathogen transmission during winter. Modeling is a relevant integrative approach for investigating the large panel of persistence mechanisms evidenced through experimental and observational studies on specific biological systems. Inter-seasonal persistence of virus may occur in hosts due to viremia duration, chronic infection, or vertical transmission, in vector resistance stages, and due to a low continuous transmission in winter. Using a generic stochastic modeling framework, we determine the parameter ranges under which virus persistence could occur via these different mechanisms. The parameter ranges vary according to the host demographic regime: for a high host population turnover, persistence increases with the mechanism parameter, whereas for a low turnover, persistence is maximal for an optimal range of parameter. Persistence in hosts due to long viremia duration in a few hosts or due to vertical transmission is an effective strategy for the virus to overwinter. Unexpectedly, a low continuous transmission during winter does not give rise to certain persistence, persistence barely occurring for a low turnover of the susceptible population. We propose a generic framework adaptable to most diptera-borne diseases. This framework allows ones to assess the plausibility of each persistence mechanism in real epidemiological situations and to compare the range of parameter values theoretically allowing persistence with the range of values determined experimentally.