An Integrative Eco-Epidemiological Analysis of West Nile Virus Transmission

Annelise Tran,Thierry Baldet,Sylvie Lecollinet,Agnès Leblond,Sophie Pradier,Thomas Balenghien,Vladimir Grosbois,Nicolas Gaidet-Drapier,Grégory L’Ambert,Gilles Balança

doi:10.1007/s10393-017-1249-6

Abstract

West Nile disease, caused by the West Nile virus (WNV), is a mosquito-borne zoonotic disease affecting humans and horses that involves wild birds as amplifying hosts. The mechanisms of WNV transmission remain unclear in Europe where the occurrence of outbreaks has dramatically increased in recent years. We used a dataset on the competence, distribution, abundance, diversity and dispersal of wild bird hosts and mosquito vectors to test alternative hypotheses concerning the transmission of WNV in Southern France. We modelled the successive processes of introduction, amplification, dispersal and spillover of WNV to incidental hosts based on host–vector contact rates on various land cover types and over four seasons. We evaluated the relative importance of the mechanisms tested using two independent serological datasets of WNV antibodies collected in wild birds and horses. We found that the same transmission processes (seasonal virus introduction by migratory birds, Culex modestus mosquitoes as amplifying vectors, heterogeneity in avian host competence, absence of ‘dilution effect’) best explain the spatial variations in WNV seroprevalence in the two serological datasets. Our results provide new insights on the pathways of WNV introduction, amplification and spillover and the contribution of bird and mosquito species to WNV transmission in Southern France.

Highlights

AND PURPOSEThere is a growing consensus that an understanding of the interactions between hosts, vectors and pathogens is crucial to describe and predict the epidemiological dynamics of vector-borne zoonotic diseases (Allan et al 2009; Lambin et al 2010)
We developed an original method within a spatial modelling framework to test a range of alternative hypotheses underpinning West Nile virus (WNV) introduction, amplification, dispersal and spillover in an area of Southern France where there have been recurrent outbreaks (Murgue et al 2001; Bournez et al 2015)
We provided an original geographic information system (GIS)-based framework to help understanding the complex interactions between hosts and vectors and their impact on the transmission of a multihost pathogen, WNV

Summary

Introduction

There is a growing consensus that an understanding of the interactions between hosts, vectors and pathogens is crucial to describe and predict the epidemiological dynamics of vector-borne zoonotic diseases (Allan et al 2009; Lambin et al 2010) To achieve such an understanding, ecology, epidemiology and geography approaches must be integrated within a cross-disciplinary research framework (Tompkins et al 2010), as the eco-epidemiological approach proposed by Susser and Susser (1996) that takes into account multi-level factors. In Europe, WNV has been reported for many years (Hubalek and Halouzka 1999), and despite a drastic increase of outbreaks since 2010 (ECDC 2015), the mechanisms of WNV transmission remain poorly understood This is due to lack of information on the host competence (i.e. the capacity of a particular host species to infect a vector) of most Eurasian bird species, the vector competence and distribution of European mosquito species, and the environmental context promoting WNV transmission (Kilpatrick 2011).

Methods

Results

Discussion

Conclusion