How Much Can Diptera-Borne Viruses Persist over Unfavourable Seasons?

Abstract

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.

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

“…In scenario d , viraemia controlled the proportion of infected eggs in overwintering eggs; hence influenced the size of the emerging infectious vector population during the next rainy season, and consequently likelihood of RVF persistence. This mechanism of persistence was also suggested for overwintering by previous work [ 22 ]. Moreover, for persistence on a longer term, host birth rate became influential by allowing a larger susceptible population to be exposed to minor new epizootics when the favourable season resumes.…”

“…The average value of the emergence rate was equal to the constant emergence rate in scenario a . Sinusoidal functions have been widely used to describe vector abundance in the absence of more precise data [ 22 , 31 , 33 , 41 ]; - scenario c : emergence rate followed here a less favourable sinusoidal curve: same maximal and minimal values as scenario b but with a lower mean; - scenario d : the favourable season lasted for half a year during which emergence followed a bell curve pattern with the same maximal values as in scenarios b and c . In the second half of the year, emergence rate was nil.…”

“…The average value of the emergence rate was equal to the constant emergence rate in scenario a . Sinusoidal functions have been widely used to describe vector abundance in the absence of more precise data [ 22 , 31 , 33 , 41 ];…”

“…Vector population dynamics is complex but strongly influences vector-borne disease dynamics. For instance, overwintering is a burning issue in order to understand Bluetongue or West Nile Virus behaviour in temperate regions [ 22 ]. Concerning RVF, the first models were based on vector populations of constant sizes [ 20 , 21 ].…”

A Spatially Explicit Metapopulation Model and Cattle Trade Analysis Suggests Key Determinants for the Recurrent Circulation of Rift Valley Fever Virus in a Pilot Area of Madagascar Highlands

“…Observed mosquitoes rather belonged to Culex and Anopheles species, in which RVFV vertical transmission has never been demonstrated. Overwintering in adult Culex females (as it is the case for West Nile virus (WNV) [31] ) has never been demonstrated for RVFV, but certainly deserves to be studied in the vector species of this altitude area. Non-mosquito vectors could also play a role in the RVFV cycle of Madagascar highlands, such as ticks [32] or Stomoxys flies [33] .…”