Abstract
Isolations of sylvatic dengue-2 virus from mosquitoes, humans and non-human primates in Senegal show synchronized multi-annual dynamics over the past 50 years. Host demography has been shown to directly affect the period between epidemics in other pathogen systems, therefore, one might expect unsynchronized multi-annual cycles occurring in hosts with dramatically different birth rates and life spans. However, in Senegal, we observe a single synchronized eight-year cycle across all vector species, suggesting synchronized dynamics in all vertebrate hosts. In the current study, we aim to explore two specific hypotheses: 1) primates with different demographics will experience outbreaks of dengue at different periodicities when observed as isolated systems, and that coupling of these subsystems through mosquito biting will act to synchronize incidence; and 2) the eight-year periodicity of isolations observed across multiple primate species is the result of long-term cycling in population immunity in the host populations. To test these hypotheses, we develop a multi-host, multi-vector Susceptible, Infected, Removed (SIR) model to explore the effects of coupling multiple host-vector systems of dengue virus transmission through cross-species biting rates. We find that under small amounts of coupling, incidence in the host species synchronize. Long-period multi-annual dynamics are observed only when prevalence in troughs reaches vanishingly small levels (), suggesting that these dynamics are inconsistent with sustained transmission in this setting, but are consistent with local dengue virus extinctions followed by reintroductions. Inclusion of a constant introduction of infectious individuals into the system causes the multi-annual periods to shrink, while the effects of coupling remain the same. Inclusion of a stochastic rate of introduction allows for multi-annual periods at a cost of reduced synchrony. Thus, we conclude that the eight-year period separating amplifications of dengue may be explained by cycling in immunity with stochastic introductions.
Highlights
IntroductionDengue virus occurs in two distinct transmission cycles: transmission among non-human primates (and occasionally among humans) by Aedes and other mosquitoes in the forest canopy (the sylvatic cycle) and transmission among humans primarily by Aedes aegypti in rural villages and urban communities (the human cycle) [1]
Dengue virus occurs in two distinct transmission cycles: transmission among non-human primates by Aedes and other mosquitoes in the forest canopy and transmission among humans primarily by Aedes aegypti in rural villages and urban communities [1]
Stochastic Model We developed a stochastic version of the model simulated using a Gillespie stochastic simulation algorithm [40] with the Binomial Tau leap approximation (BTL) [41] to examine the effects of population size on dengue isolation periodicity
Summary
Dengue virus occurs in two distinct transmission cycles: transmission among non-human primates (and occasionally among humans) by Aedes and other mosquitoes in the forest canopy (the sylvatic cycle) and transmission among humans primarily by Aedes aegypti in rural villages and urban communities (the human cycle) [1]. A sylvatic cycle of dengue virus has been documented in Senegal by the detection of dengue-2 antibodies and isolation of sylvatic dengue-2 virus from non-human primate blood [2]. Sylvatic dengue-2 virus has been isolated from mosquitoes captured in the gallery forest [2]. Though sylvatic and endemic human strains are genetically distinct, they perform in many experimental assays that characterize transmissibility [5], suggesting that the sylvatic strains have a high potential for emergence as human pathogens [6]. Several studies have demonstrated that sylvatic dengue strains can cause febrile illness and hemorrhagic syndromes in humans [7,5,8,9,10] and that infections with sylvatic or human dengue strains are clinically indistinguishable [10,11]
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