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Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal.

ABSTRACT: Arboviruses spillover into humans either as a one-step jump from a reservoir host species into humans or as a two-step jump from the reservoir to an amplification host species and thence to humans. Little is known about arbovirus transmission dynamics in reservoir and amplification hosts. Here we elucidate the role of monkeys in the sylvatic, enzootic cycle of chikungunya virus (CHIKV) in the region around Kédougou, Senegal. Over 3 years, 737 monkeys were captured, aged using anthropometry and dentition, and tested for exposure to CHIKV by detection of neutralizing antibodies. Infant monkeys were positive for CHIKV even when the virus was not detected in a concurrent survey of mosquitoes and when population immunity was too high for monkeys alone to support continuous transmission. We conclude that monkeys in this region serve as amplification hosts of CHIKV. Additional efforts are needed to identify other hosts capable of supporting continuous circulation.

SUBMITTER: Althouse BM

PROVIDER: S-EPMC5849707 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal.

Althouse Benjamin M BM Guerbois Mathilde M Cummings Derek A T DAT Diop Ousmane M OM Faye Ousmane O Faye Abdourahmane A Diallo Diawo D Sadio Bakary Djilocalisse BD Sow Abdourahmane A Faye Oumar O Sall Amadou A AA Diallo Mawlouth M Benefit Brenda B Simons Evan E Watts Douglas M DM Weaver Scott C SC Hanley Kathryn A KA

Nature communications 20180313 1

Arboviruses spillover into humans either as a one-step jump from a reservoir host species into humans or as a two-step jump from the reservoir to an amplification host species and thence to humans. Little is known about arbovirus transmission dynamics in reservoir and amplification hosts. Here we elucidate the role of monkeys in the sylvatic, enzootic cycle of chikungunya virus (CHIKV) in the region around Kédougou, Senegal. Over 3 years, 737 monkeys were captured, aged using anthropometry and d ...[more]

PMID: 29535306

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Project description:BackgroundChikungunya virus (CHIKV) originated in a sylvatic cycle of transmission between non-human animal hosts and vector mosquitoes in the forests of Africa. Subsequently the virus jumped out of this ancestral cycle into a human-endemic transmission cycle vectored by anthropophilic mosquitoes. Sylvatic CHIKV cycles persist in Africa and continue to spill over into humans, creating the potential for new CHIKV strains to enter human-endemic transmission. To mitigate such spillover, it is first necessary to delineate the distributions of the sylvatic mosquito vectors of CHIKV, to identify the environmental factors that shape these distributions, and to determine the association of mosquito presence with key drivers of virus spillover, including mosquito and CHIKV abundance. We therefore modeled the distribution of seven CHIKV mosquito vectors over two sequential rainy seasons in Kédougou, Senegal using Maxent.MethodsMosquito data were collected in fifty sites distributed in five land cover classes across the study area. Environmental data representing land cover, topographic, and climatic factors were included in the models. Models were compared and evaluated using area under the receiver operating characteristic curve (AUROC) statistics. The correlation of model outputs with abundance of individual mosquito species as well as CHIKV-positive mosquito pools was tested.ResultsFourteen models were produced and evaluated; the environmental variables most strongly associated with mosquito distributions were distance to large patches of forest, landscape patch size, rainfall, and the normalized difference vegetation index (NDVI). Seven models were positively correlated with mosquito abundance and one (Aedes taylori) was consistently, positively correlated with CHIKV-positive mosquito pools. Eight models predicted high relative occurrence rates of mosquitoes near the villages of Tenkoto and Ngary, the areas with the highest frequency of CHIKV-positive mosquito pools.ConclusionsOf the environmental factors considered here, landscape fragmentation and configuration had the strongest influence on mosquito distributions. Of the mosquito species modeled, the distribution of Ae. taylori correlated most strongly with abundance of CHIKV, suggesting that presence of this species will be a useful predictor of sylvatic CHIKV presence.

Project description: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 (< 10(-10)), 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.

Dataset Information

Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal.

Publications

Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal.

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