Heterogeneity of Rift Valley fever virus transmission potential across livestock hosts, quantified through a model-based analysis of host viral load and vector infection

Cecilia, Hélène; Vriens, Roosmarie; Schreur, Paul J. Wichgers; Wit, Mariken de; Métras, Raphaëlle; Ezanno, Pauline; Bosch, Quirine A. ten

doi:10.1371/journal.pcbi.1010314

Cited by 11 publications

(11 citation statements)

References 72 publications

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“…The viremia levels are coupled with estimations of how these levels relate to transmission efficiency. This dose response relationship has been estimated for RVFV based on a meta-analysis of available literature and presents a composite estimate across vertebrate species and the Aedes genera (Cecilia et al, 2022). Our results (31% from 4.35 to 7.15 log10 TCID50/ml) are consistent with the described relationships.…”

Section: Discussionsupporting

confidence: 85%

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Quantifying Rift Valley fever virus transmission efficiency in a lamb-mosquito-lamb model

Bron

Wichgers-Schreur

Jong

et al. 2023

Preprint

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Rift Valley fever virus (RVFV) is a (re)emerging mosquito-borne pathogen impacting human and animal health. How RVFV spreads through a population depends on population-level interactions between hosts and vectors (e.g., vector-to-host ratio and biting preference) and also on potential differences in individual following virus exposure (e.g., transmission efficiencies from host to vector and vice versa). Here, we estimated the probability for RVFV to transmit to naive animals by experimentally exposing lambs to a bite of an infectious mosquito (the transmission efficiency) and assessed if and how RVFV infection subsequently developed in the exposed animal. Aedes aegypti mosquitoes, previously infected via feeding on a viremic lamb, were used to expose naive lambs to the virus. Lambs were either exposed to 1-3 (low exposure) or 7-9 (high exposure) infectious mosquitoes. All lambs in the high exposure group became viremic and showed characteristic signs of Rift Valley fever within 2-4 days post exposure. In contrast, 3 out of 12 lambs in the low exposure group developed viremia and disease, with similar peaks in viremia as the high exposure group but with some heterogeneity in the onset of viremia. These results suggest that the likelihood for successful infection of a ruminant host is affected by the number of infectious mosquitoes biting, but also highlights that a lamb can be infected by a single mosquito. The per bite mosquito-to-host transmission efficiency was estimated at 28% (95% confidence interval: 15 - 47%). We subsequently combined this transmission efficiency with estimates for mosquito life traits into a Ross-McDonald mathematical model to illustrate scenarios under which major RVFV outbreaks could occur in naive populations (i.e., R0 >1). The model revealed that for efficient RVFV transmission relatively high vector-to-host ratios as well as strong feeding preference for competent hosts are required. Altogether, this study highlights the importance of experiments that mimic natural exposure to RVFV. The experiments facilitate a better understanding of the natural progression of disease and a direct way to obtain epidemiological parameters for mathematical models.

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Section: Discussionsupporting

confidence: 85%

“…Infectious period host (days) 1/r 4 This study (Barker et al, 2013;Oymans et al, 2020;Cecilia et al, 2022)…”

Section: Parametermentioning

confidence: 99%

Quantifying Rift Valley fever virus transmission efficiency in a lamb-mosquito-lamb model

Bron

Wichgers-Schreur

Jong

et al. 2023

Preprint

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“…Infectiousness of both host and mosquitoes is a function of viral load, with a higher viral load corresponding to a higher transmission probability [94]. Additionally, individuals with low viral titres can also contribute significantly to the transmission dynamics, depending on their numerical prominence [95, 96]. Defining a cut-off value for the extrinsic incubation period is therefore a somewhat arbitrary choice.…”

Section: Discussionmentioning

confidence: 99%

Mechanistic models for West Nile Virus transmission: A systematic review of features, aims, and parameterisation

de Wit,

Dimas Martins,

Delecroix

et al. 2023

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Mathematical models within the Ross-Macdonald framework increasingly play a role in our understanding of vector–borne disease dynamics and as tools for assessing scenarios to respond to emerging threats. These threats are typically characterised by a high degree of heterogeneity, introducing a range of possible complexities in models and challenges to maintain the link with empirical evidence. We systematically identified and analysed a total of 67 published papers presenting compartmental West Nile Virus (WNV) models that use parameter values derived from empirical studies. Using a set of fifteen criteria, we measured the dissimilarity compared to the Ross–Macdonald framework. We also retrieved the purpose and type of models and traced the empirical sources of their parameters. Our review highlights the increasing refinements in WNV models. Models for prediction included the highest number of refinements. We found uneven distributions of refinements and of evidence for parameter values. We identified several challenges in parameterising such increasingly complex models. For parameters common to most models, we also synthesise the empirical evidence for their values and ranges. The study highlights the potential to improve the quality of WNV models and their applicability for policy by establishing closer collaboration between mathematical modelling and empirical work.

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“…Quantifying these roles is crucial to design targeted and efficient control strategies, and will require more knowledge on the intrinsic heterogeneity between host and vector species. Within-host modeling can help in this matter, but such models for RVF are rare [97,158]. Besides, a paramount hypothesis driving model behavior is the contact structure assumed between hosts and vectors, mathematically embodied by the force of infection.…”

Section: Plos Neglected Tropical Diseasesmentioning

confidence: 99%

Mechanistic models of Rift Valley fever virus transmission: A systematic review

et al. 2022

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Rift Valley fever (RVF) is a zoonotic arbovirosis which has been reported across Africa including the northernmost edge, South West Indian Ocean islands, and the Arabian Peninsula. The virus is responsible for high abortion rates and mortality in young ruminants, with economic impacts in affected countries. To date, RVF epidemiological mechanisms are not fully understood, due to the multiplicity of implicated vertebrate hosts, vectors, and ecosystems. In this context, mathematical models are useful tools to develop our understanding of complex systems, and mechanistic models are particularly suited to data-scarce settings. Here, we performed a systematic review of mechanistic models studying RVF, to explore their diversity and their contribution to the understanding of this disease epidemiology. Researching Pubmed and Scopus databases (October 2021), we eventually selected 48 papers, presenting overall 49 different models with numerical application to RVF. We categorized models as theoretical, applied, or grey, depending on whether they represented a specific geographical context or not, and whether they relied on an extensive use of data. We discussed their contributions to the understanding of RVF epidemiology, and highlighted that theoretical and applied models are used differently yet meet common objectives. Through the examination of model features, we identified research questions left unexplored across scales, such as the role of animal mobility, as well as the relative contributions of host and vector species to transmission. Importantly, we noted a substantial lack of justification when choosing a functional form for the force of infection. Overall, we showed a great diversity in RVF models, leading to important progress in our comprehension of epidemiological mechanisms. To go further, data gaps must be filled, and modelers need to improve their code accessibility.

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Heterogeneity of Rift Valley fever virus transmission potential across livestock hosts, quantified through a model-based analysis of host viral load and vector infection

Cited by 11 publications

References 72 publications

Quantifying Rift Valley fever virus transmission efficiency in a lamb-mosquito-lamb model

Quantifying Rift Valley fever virus transmission efficiency in a lamb-mosquito-lamb model

Mechanistic models for West Nile Virus transmission: A systematic review of features, aims, and parameterisation

Mechanistic models of Rift Valley fever virus transmission: A systematic review

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