Integrated Analysis of Environment, Cattle and Human Serological Data: Risks and Mechanisms of Transmission of Rift Valley Fever in Madagascar

Abstract

BackgroundRift Valley fever (RVF) is a vector-borne disease affecting ruminants and humans. Madagascar was heavily affected by RVF in 2008–2009, with evidence of a large and heterogeneous spread of the disease. The identification of at-risk environments is essential to optimize the available resources by targeting RVF surveillance in Madagascar. Herein, the objectives of our study were: (i) to identify the environmental factors and areas favorable to RVF transmission to both cattle and human and (ii) to identify human behaviors favoring human infections in Malagasy contexts.Methodology/Principal FindingsFirst, we characterized the environments of Malagasy communes using a Multiple Factor Analysis (MFA). Then, we analyzed cattle and human serological data collected at national level using Generalized Linear Mixed Models, with the individual serological status (cattle or human) as the response, and MFA factors, as well as other potential risk factors (cattle density, human behavior) as explanatory variables. Cattle and human seroprevalence rates were positively associated to humid environments (p<0.001). Areas with high cattle density were at risk (p<0.01; OR = 2.6). Furthermore, our analysis showed that frequent contact with raw milk contributed to explain human infection (OR = 1.6). Finally, our study highlighted the eastern-coast, western and north-western parts as high-risk areas for RVF transmission in cattle.Conclusions/SignificanceOur integrated approach analyzing environmental, cattle and human datasets allow us to bring new insight on RVF transmission patterns in Madagascar. The association between cattle seroprevalence, humid environments and high cattle density suggests that concomitant vectorial and direct transmissions are critical to maintain RVF enzootic transmission. Additionally, in the at-risk humid environment of the western, north-western and the eastern-coast areas, suitable to Culex and Anopheles mosquitoes, vectorial transmission probably occurs in both cattle and human. The relative contribution of vectorial or direct transmissions could be further assessed by mathematic modelling.

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

“…At first glance, the variation of RVF FOIs estimated from mid-1992 to mid-2014 is in accordance with the historical report of RVF transmission in Madagascar: high transmission during the 2008–09 outbreaks and low transmission outside this period12161718192021. Then, our results are consistent with the hypothesis of contrasted patterns of long-term RVFV enzootic circulation in the different Malagasy eco-regions.…”

“…Only cattle which breeding location was known were considered in the present study (n = 1,432). Animal sera were analyzed using commercial ELISA kits (BDSL) to detect anti-RVFV immunoglobulin (Ig) G22. The sensitivity and specificity of the serological test for bovines were estimated to be 96.3% and 99.7% respectively22.…”

“…Even though most of the RVF outbreaks were reported on the Highlands, a recent study suggested that some areas –i.e. the western and northwestern parts, were favorable to enzootic dynamics whereas others were suitable for epizootic dynamics21. Such differences indicated that the RVF dynamic patterns vary among Malagasy regions.…”

High seroprevalence of Rift Valley fever phlebovirus in domestic ruminants and African Buffaloes in Mozambique shows need for intensified surveillance

“…Despite the high precipitation (between 800 – 2000 mm) in the hot and rainy season (from October to March) [37], the low temperature may not favor the breeding of the potential vectors of the RVFPV. Another factor may be related to the low density of animals and large dispersion among herds, which may hamper the ability of the vectors to spread the virus [50]. The high seroprevalence observed in Cabo Delgado, for this region, may be explained by the fact that in this province the altitude and forest density decrease eastward (Figure 1), and the annual average temperatures tend to increase (>24°C), which, in comparison to Niassa, may increase the survival rate of RVFPV mosquitos’ vectors, and hence increase the vectorial transmission of RVFPV to the animals.…”

“…This situation has led to the opening of more irrigation ditches [37], which may have contributed to the increase in mosquito breeding and greater exposure of animals [50]. …”