A Spatially Explicit Metapopulation Model and Cattle Trade Analysis Suggests Key Determinants for the Recurrent Circulation of Rift Valley Fever Virus in a Pilot Area of Madagascar Highlands

Abstract

Rift Valley fever (RVF) is a vector-borne zoonotic disease that causes high morbidity and mortality in ruminants. In 2008–2009, a RVF outbreak affected the whole Madagascar island, including the Anjozorobe district located in Madagascar highlands. An entomological survey showed the absence of Aedes among the potential RVF virus (RVFV) vector species identified in this area, and an overall low abundance of mosquitoes due to unfavorable climatic conditions during winter. No serological nor virological sign of infection was observed in wild terrestrial mammals of the area, suggesting an absence of wild RVF virus (RVFV) reservoir. However, a three years serological and virological follow-up in cattle showed a recurrent RVFV circulation. The objective of this study was to understand the key determinants of this unexpected recurrent transmission. To achieve this goal, a spatial deterministic discrete-time metapopulation model combined with cattle trade network was designed and parameterized to reproduce the local conditions using observational data collected in the area. Three scenarios that could explain the RVFV recurrent circulation in the area were analyzed: (i) RVFV overwintering thanks to a direct transmission between cattle when viraemic cows calve, vectors being absent during the winter, (ii) a low level vector-based circulation during winter thanks to a residual vector population, without direct transmission between cattle, (iii) combination of both above mentioned mechanisms. Multi-model inference methods resulted in a model incorporating both a low level RVFV winter vector-borne transmission and a direct transmission between animals when viraemic cows calve. Predictions satisfactorily reproduced field observations, 84% of cattle infections being attributed to vector-borne transmission, and 16% to direct transmission. These results appeared robust according to the sensitivity analysis. Interweaving between agricultural works in rice fields, seasonality of vector proliferation, and cattle exchange practices could be a key element for understanding RVFV circulation in this area of Madagascar highlands.

Reconstruction of Rift Valley fever transmission dynamics in Madagascar: estimation of force of infection from seroprevalence surveys using Bayesian modelling

“…Indeed, vertical transmission has been described in Aedes subgenus Neomelaniconion mosquitoes38 which is present in all Malagasy eco-regions2939. The role of ruminant movements –barter and trade, in RVFV circulation and persistence, has already been shown at a local scale in a pilot area in the Highlands193340. A better understanding of these movements all over the island, using field records and mathematical modeling is essential to assess their role in RVF epidemiology in Madagascar40.…”

A Review of Mosquitoes Associated with Rift Valley Fever Virus in Madagascar

“…Excluding factors associated with vertebrates (species, movement, density, susceptibility, and vaccination), 69 mosquito vectors are major components of RVF risk, which we refer to as the entomological risk. Classically, this entomological risk takes into account mosquito density, population dynamics, trophic behavior, longevity of each mosquito population in a given place, and vector competence of each species/population for a given virus strain, including vertical transmission.…”

“…Classically, this entomological risk takes into account mosquito density, population dynamics, trophic behavior, longevity of each mosquito population in a given place, and vector competence of each species/population for a given virus strain, including vertical transmission. These variables are almost certainly influenced by climate (temperature and rainfall), biotic variables (breeding sites and presence of vertebrate hosts), and vector control as observed in Madagascar 15,69,70 and other countries. 71 In Madagascar, the distributions of mosquitoes classified as RVFV vectors, potential vectors, and candidate vector are notably different and associated with biogeographical domains.…”

“…72 Indeed, mosquitoes species already associated with RVFV in Madagascar colonize different types of larval breeding sites, with rice fields being a dominant habitat. 33,69 In Madagascar, vector control is primarily targeted against mosquitoes transmitting malaria through the use of indoor residual spraying (IRS) and nets (insecticide-treated mosquito nets and long-lasting insecticidal mosquitoes nets). 73 No larvicidal measures have been undertaken on the island.…”

“…1,79,80 In Madagascar, this technique was used on a local scale of one domain during a malaria study 81 and could provide interesting insights associated with RVF entomological surveys, particularly in the southwestern domain, where RVF is considered to be endemic. 6 Variation in monthly and annual precipitations (http://iridl.ldeo.columbia.edu/) and patterns of variation in larval development are important factors that vary between biogeographical domains 69 ; hence, this technology should be used for the identification RVF risk areas. It could be very useful to estimate the relationship between abundance of breeding sites and density of adult vectors for additional vector surveillance and control.…”