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Epidemiological significance of dengue virus genetic variation in mosquito infection dynamics

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Listed:
  • Albin Fontaine
  • Sebastian Lequime
  • Isabelle Moltini-Conclois
  • Davy Jiolle
  • Isabelle Leparc-Goffart
  • Robert Charles Reiner Jr
  • Louis Lambrechts

Abstract

The kinetics of arthropod-borne virus (arbovirus) transmission by their vectors have long been recognized as a powerful determinant of arbovirus epidemiology. The time interval between virus acquisition and transmission by the vector, termed extrinsic incubation period (EIP), combines with vector mortality rate and vector competence to determine the proportion of infected vectors that eventually become infectious. However, the dynamic nature of this process, and the amount of natural variation in transmission kinetics among arbovirus strains, are poorly documented empirically and are rarely considered in epidemiological models. Here, we combine newly generated empirical measurements in vivo and outbreak simulations in silico to assess the epidemiological significance of genetic variation in dengue virus (DENV) transmission kinetics by Aedes aegypti mosquitoes. We found significant variation in the dynamics of systemic mosquito infection, a proxy for EIP, among eight field-derived DENV isolates representing the worldwide diversity of recently circulating type 1 strains. Using a stochastic agent-based model to compute time-dependent individual transmission probabilities, we predict that the observed variation in systemic mosquito infection kinetics may drive significant differences in the probability of dengue outbreak and the number of human infections. Our results demonstrate that infection dynamics in mosquitoes vary among wild-type DENV isolates and that this variation potentially affects the risk and magnitude of dengue outbreaks. Our quantitative assessment of DENV genetic variation in transmission kinetics contributes to improve our understanding of heterogeneities in arbovirus epidemiological dynamics.Author summary: Transmission of arboviruses by mosquitoes is a time-dependent process because dissemination of the virus from the insect’s digestive tract, where the infection is initially established, to the salivary glands, where it can be transmitted to the next host, typically takes several days. The duration of this time interval is an important determinant of the proportion of infected mosquitoes that live long enough to become infectious. Due to the lack of available data, epidemiological models rarely account for the dynamic nature of this process and its natural variation among arbovirus strains. In this study, we experimentally monitored the dynamics of mosquito infection by eight strains of dengue virus and found significant differences between them. In addition, we used the empirical data obtained in a simulation model to show that the differences observed among the strains are expected to result in human dengue outbreaks of different probability and size. Together, our results indicate that natural variation in mosquito infection dynamics between arbovirus strains may contribute to the unexplained heterogeneity of dengue virus transmission patterns.

Suggested Citation

  • Albin Fontaine & Sebastian Lequime & Isabelle Moltini-Conclois & Davy Jiolle & Isabelle Leparc-Goffart & Robert Charles Reiner Jr & Louis Lambrechts, 2018. "Epidemiological significance of dengue virus genetic variation in mosquito infection dynamics," PLOS Pathogens, Public Library of Science, vol. 14(7), pages 1-21, July.
    • Handle: RePEc:plo:ppat00:1007187
    DOI: 10.1371/journal.ppat.1007187
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    References listed on IDEAS

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    1. Wickham, Hadley, 2007. "Reshaping Data with the reshape Package," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 21(i12).
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