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Impact of vector and host distribution on the processes of introduction, amplification and emergence of a multi-host infectious disease: : an integrative ecological and landscape study on West Nile virus in southern France

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(1)

Impact of vector and host distribution on the

processes of introduction, amplification and

emergence of a multi-host infectious disease:

An integrative ecological and landscape study

on West Nile virus in southern France

Tran A, L’Ambert G, Balança G, Pradier S, Grosbois V, Roche B,

Etter E, Balenghien T, Baldet T, Leblond A, Fontenille D, Reiter P & Gaidet N.

(2)

West Nile Virus in the Camargue region,

Southern France

WNV:

flavivirus

WNF:

an emerging arbovirosis with a complex

epidemiological cycle:

– Birds

– Mosquitoes (mainly

Culex

genus)

– Horse and man: accidental hosts

A multi-host disease

Bird Bird Mosquito Mosquito Human Horse

Accidental hosts

Emergence in the Camargue region

– Recurring outbreaks (2000, 2004)

Low level virus circulation in wild birds

– Overall seroprevalence < 1% (Balança et al., 2009) Epizootic areas (year) Virus circulation areas in the 1960s Cities Bird ? ? Eggs

(3)

Which are the

vectors?

Culex modestus

or/and

Culex pipiens

Which are the

reservoirs?

– Magpies and sparrows only

– All species are able to transmit the virus

– Some species have a higher receptivity/competence

The transmission stops in winter…how to explain WNV persistence?

– Virus overwintering

– WNV is chronically reintroduced by migrating birds

Does the reservoir host

community composition

affect WNV

transmission

?

– Dilution effect?

A lot of questions

(Balenghien, 2008) (Jourdain, 2008) (Hubalek, 1999) (Ezenwa, 2006) (Jourdain, 2007)

(4)

Ecological and landscape approach

• Hypothesis:

Some associations in time and space between vectors and reservoirs are favourable to the occurrence of WNV

• Study area: Camargue region, France

• A large diversity of potential reservoirs and vectors

Season Year Horse - Man Bird Habitat Landscape Mosquito • Diversity structured by : - a temporal component - a spatial component

a wide range in the types of

association between reservoirs and vectors

Identification of specific environmental configurations favourable to

(5)

Method

1.

Map the seasonal distribution of mosquito and bird populations

– Expert-based knowledge

– Geographic Information Systems

– Field validation

2.

Building of risk maps corresponding to different hypotheses

– Identification of introduction and amplification areas

– Combination of the different steps -> a scenario

3.

Compare model outputs of each scenario with results of

seroprevalence studies

– Ouput: a risk index

– Regression model: prevalence ~ risk_index

– Use of Akaike information criterion to compare the resulting models

(6)

Ecological map

Common typology birds / mosquitoes

Landsat ETM+ images

Bird database

180 species

4 seasons

– Definition of a probability occurrence index for each ecological unit and

each season

– Migration

– Spread

– Reservoir index

1 to 10 individual observed at a site during a visit common

3

Observed frequently at a site, but not at every visit frequent

2

Observed every year, but with only few observations per year

uncommon 1

Never or accidentally observed at a site absent 0 Definition Probability of occurrence Code

1. Map the seasonal distribution of mosquito

and bird populations

(7)

2. Building of risk maps corresponding to

different hypotheses

Introduction Amplification I2: Virus overwintering in vectors I2a: Cx modestus I2b: Cx pipiens I2c: Cx modestus and Cx pipiens Host amplification Ax1x: Magpies / sparrows Ax2x: Some reservoir species

Ax3x: All species I1: Virus introduction

by migratory birds

I1b: From Eastern and Northern Europe, summer I1a: From sub-saharan Africa and Maghreb, spring Vector amplification A1xx: Cx modestus A2xx: Cx pipiens A3xx: Cx modestus and Cx pipiens Diversity effects Axx1: No dilution effect Axx2: Dilution effect: Risk decreases with the number of non-competent species Emergence Introduction Amplification Risk_index 75 scenarios

(8)

3. Compare model outputs of each scenario with

results of seroprevalence studies

Serological survey

(2004-2007) on black-billed magpies (

Pica pica

)

(Balança, 2009; Jourdain, 2007)

For each scenario:

– Regression model: seroprevalence ~ risk_index

Akaike information criterion (AIC)

to compare the models

(

i=AIC

i

-AICmin)

Weighted AIC (wAIC)

to compare different groups of models:

– Introduction 1a, 1b, 2a, 2b, 2c

– Vector amplification 1, 2, 3

– Host amplification 1, 2, 3

– Diversity effects 1, 2

(9)

Results (1)

Heterogeneous spatial patterns

All scenarios outputs (risk indices) are

positively

correlated

with prevalence

Considering the

i

=AIC

i

-AIC

min

:

3 models have substantial support (

i

≤ 2)

3 models have slightly less support (2 <

i

≤ 4)

25 models have considerably less support (4 <

i

≤ 7)

(10)

Example of « best » risk map of WNV in the

Camargue area

Introduction

By migratory birds from sub-saharan Africa and Maghreb

Amplification

By

Culex modestus

By all reservoir species (no dilution effect)

(11)

Results (2)

0.070 Both species 0.066 Culex pipiens 0.090 Culex modestus Virus overwintering 0.553 From Eastern and

Northern Europe

0.221 From Sub-saharan Africa

and Maghreb Introduction by migratory birds ΣwAIC Scenario

Introduction

 By migratory birds

Vector amplification



Culex modestus

Reservoir amplification

 Magpies and sparrows are not the only

reservoirs

Dilution effect

 No 0.561 All species 0.773 No dilution effect Diversity effects 0.344 Some competent species

0.095 Magpies and sparrows

Reservoir amplification 0.370 Both species Vector amplification 0.227 Dilution effect 0.131 Culex pipiens 0.499 Culex modestus

(12)

Discussion and perspectives

Multi-host diseases: difficult to study!

First integrative ecological and landscape study of WNV in France

Contribute to a better understanding of WNV circulation in Southern

France

– Some hypotheses relative to WNV epidemiological cycle may be rejected

in the Camargue context

– Role of migratory birds also demonstrated by recent studies

(Durand, 2010)

Production of risk maps which match observed seroprevalence

patterns

Tool for surveillance / studies

Towards dynamic modelling approaches (ABM)

(Roche, 2008)

(13)

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