The tortoise or the hare? Impacts of within-host dynamics on transmission success of arthropod-borne viruses

Althouse, Benjamin M.; Hanley, Kathryn A.

doi:10.1098/rstb.2014.0299

Cited by 47 publications

(65 citation statements)

References 100 publications

(136 reference statements)

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“…Our model extends, to our knowledge, the only previous dynamic model of mosquito-borne viruses in non-human primate hosts [54, 55]. While our previous modeling study was focused on sylvatic DENV [54], the strong similarities between sylvatic DENV and sylvatic ZIKV transmission cycle make the model a good fit for both viruses.…”

Section: Establishing a Sylvatic Zikv Cyclementioning

confidence: 68%

“…These studies should (i) incorporate multiple species of New World primates, (ii) compare virus dynamics resulting from virus delivery by needle versus mosquito vector, (iii) monitor intra-host infection dynamics over a duration that exceeds that currently documented for viremia in humans, (iv) utilize both culture and direct mosquito feeding to detect viremia, and (v) monitor pathogenesis of the virus with a focus on potential impact of the virus on survival [55]. …”

Section: Discussionmentioning

confidence: 99%

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Potential for Zika Virus to Establish a Sylvatic Transmission Cycle in the Americas

et al. 2016

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Zika virus (ZIKV) originated and continues to circulate in a sylvatic transmission cycle between non-human primate hosts and arboreal mosquitoes in tropical Africa. Recently ZIKV invaded the Americas, where it poses a threat to human health, especially to pregnant women and their infants. Here we examine the risk that ZIKV will establish a sylvatic cycle in the Americas, focusing on Brazil. We review the natural history of sylvatic ZIKV and present a mathematical dynamic transmission model to assess the probability of establishment of a sylvatic ZIKV transmission cycle in non-human primates and/or other mammals and arboreal mosquito vectors in Brazil. Brazil is home to multiple species of primates and mosquitoes potentially capable of ZIKV transmission, though direct assessment of host competence (ability to mount viremia sufficient to infect a feeding mosquito) and vector competence (ability to become infected with ZIKV and disseminate and transmit upon subsequent feedings) of New World species is lacking. Modeling reveals a high probability of establishment of sylvatic ZIKV across a large range of biologically plausible parameters. Probability of establishment is dependent on host and vector population sizes, host birthrates, and ZIKV force of infection. Research on the host competence of New World monkeys or other small mammals to ZIKV, on vector competence of New World Aedes, Sabethes, and Haemagogus mosquitoes for ZIKV, and on the geographic range of potential New World hosts and vectors is urgently needed. A sylvatic cycle of ZIKV would make future elimination efforts in the Americas practically impossible, and paints a dire picture for the epidemiology of ZIKV and our ability to end the ongoing outbreak of congenital Zika syndrome.

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Section: Establishing a Sylvatic Zikv Cyclementioning

confidence: 68%

Section: Discussionmentioning

confidence: 99%

Potential for Zika Virus to Establish a Sylvatic Transmission Cycle in the Americas

et al. 2016

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“…Another major factor in vector transmission is the amount of virus inoculated in the saliva, which can affect pathogenesis ( 21 ); this value is critical for determining realistic animal model doses. We found saliva titers of up to 4 log 10 FFU per collection, with the following mean ±SD log 10 FFU/collection for each mosquito–virus strain combination: Salvador mosquitoes, DAK AR 41525: 2.49 ±2.93; DR mosquitoes, DAK AR 41525: 2.72 ±3.26; DR mosquitoes, MEX1–7: 2.30 ±2.35; RGV mosquitoes, DAK AR: 2.20 ±1.96; Salvador mosquitoes, FSS 13025 infected through a murine blood meal: 2.77 ±3.00.…”

Section: Discussionmentioning

confidence: 99%

“…Because geographically disparate populations of this species can vary in their susceptibility to flaviviruses ( 20 ), including Zika virus ( 15 ), we tested populations from 3 at-risk sites in the Americas—Brazil (Salvador), the Caribbean (Dominican Republic [DR]), and the United States (Rio Grande Valley [RGV], Texas)—with Zika virus strains from Senegal (DAK AR 41525), Cambodia (FSS 13025), and a 2015 Mexico outbreak (MEX1–7) ( 14 ). We also estimated the extrinsic incubation period (EIP) and viral titers in mosquito saliva and characterized differences in infection and dissemination between artificial and viremic blood meals ( 21 ). …”

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confidence: 99%

Variation inAedes aegyptiMosquito Competence for Zika Virus Transmission

Roundy¹,

Azar²,

Rossi³

et al. 2017

Emerg. Infect. Dis.

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To test whether Zika virus has adapted for more efficient transmission by Aedes aegypti mosquitoes, leading to recent urban outbreaks, we fed mosquitoes from Brazil, the Dominican Republic, and the United States artificial blood meals containing 1 of 3 Zika virus strains (Senegal, Cambodia, Mexico) and monitored infection, dissemination, and virus in saliva. Contrary to our hypothesis, Cambodia and Mexica strains were less infectious than the Senegal strain. Only mosquitoes from the Dominican Republic transmitted the Cambodia and Mexica strains. However, blood meals from viremic mice were more infectious than artificial blood meals of comparable doses; the Cambodia strain was not transmitted by mosquitoes from Brazil after artificial blood meals, whereas 61% transmission occurred after a murine blood meal (saliva titers up to 4 log10 infectious units/collection). Although regional origins of vector populations and virus strain influence transmission efficiency, Ae. aegypti mosquitoes appear to be competent vectors of Zika virus in several regions of the Americas.

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“…also found that the temporality of transmission from non-human primates was sometimes more impactful than the magnitude of the viremia leading to transmission to the mosquito [48]. They proposed a "tortoise-or-the-hare" (TotH) model to describe this relationship between arboviral viremia profiles in non-human primates and the predicted transmission success to vectors, showing that the strategy of "slow and steady" viremia -lower levels for longer periods -resulted in higher predicted transmission success of arboviruses [48]. Here again we invoke the TotH model to describe the complimentary side of the vector-borne pathogen transmission cycles, in the direction of vector-to-vertebrate.…”

Section: Discussionmentioning

confidence: 95%

The tortoise strategy as an arbovirus fitness phenotype within the mosquito as revealed by a novel formulation of age-structured vectorial capacity

Mayton

Wearing²,

Tramonte

et al. 2019

Preprint

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The transmission of vector-borne diseases like Zika virus (ZIKV) is a dynamic process that is defined by intrinsic and extrinsic factors. One of the most important definers of the efficiency of the transmission is vector competence, or the ability of a vector to become infected with and eventually transmit a pathogen. Many things affect vector competence including vector species, discrete populations within species, and environmental factors. Several recent studies have focused on environmental factors such as temperature, and found that temperature not only affects vector competence of ZIKV in Aedes aegypti but also the life traits of the mosquito. Thus, we wanted to determine if the vector competence and extrinsic incubation period (EIP) of ZIKV was altered due to the age at which a mosquito becomes exposed. We found that there were virtually no differences in the proportion of infected, disseminated, or transmitting mosquitoes 5, 8, and 11 days post exposure among those mosquitoes exposed at 5 days post emergence versus those exposed at 12 days post emergence. However, to put this lack of differences into a more biologically relevant context, we investigated the interaction of vector competence, EIP, and age-dependent life traits of lifespan and biting rate. To illustrate the differences, we modified the vectorial capacity (VC) equation, which is a vector-centric equivalent to the basic reproduction number. VC describes the number of secondary cases of vector infection given the introduction of an infectious individual into a naïve population. By deriving an age-structure measure (VC age ), we are able to demonstrate the effect of age on the transmission of ZIKV by Ae. aegypti. While aging of mosquitoes in the field is limited to pre-parous and parous females, our VC age equation, like age-structured mathematical models, can be used to inform hypothesis regarding the effective density of mosquito vectors, those that are transmitting versus those that are unexposed or exposed but not transmitting due to the effects of age. These results are intuitive. However, our VC age model, like other models with age-structured vector populations, can be used to put this intuition into a quantitative framework and our experimental findings offer more insights into the importance of age-dependence of virus:vector interactions. Our experimental data further offer age-dependent parameterization of several components of VC age that could be used to inform mathematical models where age structure in a mosquito population is important.

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The tortoise or the hare? Impacts of within-host dynamics on transmission success of arthropod-borne viruses

Cited by 47 publications

References 100 publications

Potential for Zika Virus to Establish a Sylvatic Transmission Cycle in the Americas

Potential for Zika Virus to Establish a Sylvatic Transmission Cycle in the Americas

Variation inAedes aegyptiMosquito Competence for Zika Virus Transmission

The tortoise strategy as an arbovirus fitness phenotype within the mosquito as revealed by a novel formulation of age-structured vectorial capacity

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