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Pathogenic landscapes: interactions between land, people, disease vectors, and their animal hosts.

Lambin EF, Tran A, Vanwambeke SO, Linard C, Soti V - Int J Health Geogr (2010)

Bottom Line: We formulated ten propositions that are related to landscape attributes, spatial patterns and habitat connectivity, pathways of pathogen transmission between vectors and hosts, scale issues, land use and ownership, and human behaviour associated with transmission cycles.We also highlight the complementarity of the modelling approaches used in our case studies.Integrated analyses at the landscape scale allows a better understanding of interactions between changes in ecosystems and climate, land use and human behaviour, and the ecology of vectors and animal hosts of infectious agents.

View Article: PubMed Central - HTML - PubMed

Affiliation: Georges LemaƮtre Centre for Earth and Climate Research, Earth and Life Institute, University of Louvain, 3 place Pasteur, Louvain-la-Neuve, B-1348, Belgium. eric.lambin@uclouvain.be

ABSTRACT

Background: Landscape attributes influence spatial variations in disease risk or incidence. We present a review of the key findings from eight case studies that we conducted in Europe and West Africa on the impact of land changes on emerging or re-emerging vector-borne diseases and/or zoonoses. The case studies concern West Nile virus transmission in Senegal, tick-borne encephalitis incidence in Latvia, sandfly abundance in the French Pyrenees, Rift Valley Fever in the Ferlo (Senegal), West Nile Fever and the risk of malaria re-emergence in the Camargue, and rodent-borne Puumala hantavirus and Lyme borreliosis in Belgium.

Results: We identified general principles governing landscape epidemiology in these diverse disease systems and geographic regions. We formulated ten propositions that are related to landscape attributes, spatial patterns and habitat connectivity, pathways of pathogen transmission between vectors and hosts, scale issues, land use and ownership, and human behaviour associated with transmission cycles.

Conclusions: A static view of the "pathogenecity" of landscapes overlays maps of the spatial distribution of vectors and their habitats, animal hosts carrying specific pathogens and their habitat, and susceptible human hosts and their land use. A more dynamic view emphasizing the spatial and temporal interactions between these agents at multiple scales is more appropriate. We also highlight the complementarity of the modelling approaches used in our case studies. Integrated analyses at the landscape scale allows a better understanding of interactions between changes in ecosystems and climate, land use and human behaviour, and the ecology of vectors and animal hosts of infectious agents.

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Spread of the mosquito Culex poicilipes around a breeding site in different hypothetical landscapes in the semi-arid region of the Ferlo, Senegal, based on model simulations. Red isolines depict the mosquito density. Vegetation is represented in green and bare soil in yellow.
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Figure 3: Spread of the mosquito Culex poicilipes around a breeding site in different hypothetical landscapes in the semi-arid region of the Ferlo, Senegal, based on model simulations. Red isolines depict the mosquito density. Vegetation is represented in green and bare soil in yellow.

Mentions: The proximity of vector and host habitats may not result in a high level of risk if these critical habitats are not connected spatially by landscape features favourable to the circulation of vectors and/or hosts. Spatial diffusion of vectors is particularly crucial in the case of mosquito-borne diseases. At night, when female mosquitoes generally feed, most of the hosts (e.g., humans, cattle) are immobile. The ability of female vectors to spread from their breeding sites to hosts increases host/vector contacts. Landscape features largely control these movements [47]. The study of RVF in the semi-arid region of the Ferlo in Senegal showed that ruminant herds living around temporary water bodies were at greater risk of RVF if they were located close to ponds surrounded by vegetation [22]. A landscape closure index - representing the proportion of surface around each pond covered by vegetation such as dense forest and shrub savannah - was positively correlated with higher serologic incidence. The presence of dense vegetation around water bodies favours the spread of mosquitoes from the pond where they breed to the nearby ruminant herds (Figure 3). The importance of connectivity between habitats for the spread of mosquitoes was also demonstrated for Culex species in Southern France [48]. The connectivity between forest patches may also influence rodent populations and therefore the transmission of rodent-borne diseases such as hantavirus. Linard et al. [24] found that the spatial distribution of bank voles was different during epidemic and non-epidemic years. The number of bank voles captured was higher in more isolated forest patches during the non-epidemic year, whereas it was higher in less isolated patches during the epidemic year. Well-connected patches have more chances to be recolonized after local extinctions [49]. Habitat connectivity could also influence the virus occurrence in hosts by controlling movements of individuals and thus contact rate between infected and susceptible rodents. Langlois et al. [50] observed that hantavirus incidence in deer mice was higher in landscapes with a higher level of fragmentation of the preferred habitat. In Western Africa, Guerrini et al. [51] showed that the riverine forest fragmentation level is a critical factor to determine the habitat of riverine tsetse species, vectors of animal trypanosomosis.


Pathogenic landscapes: interactions between land, people, disease vectors, and their animal hosts.

Lambin EF, Tran A, Vanwambeke SO, Linard C, Soti V - Int J Health Geogr (2010)

Spread of the mosquito Culex poicilipes around a breeding site in different hypothetical landscapes in the semi-arid region of the Ferlo, Senegal, based on model simulations. Red isolines depict the mosquito density. Vegetation is represented in green and bare soil in yellow.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2984574&req=5

Figure 3: Spread of the mosquito Culex poicilipes around a breeding site in different hypothetical landscapes in the semi-arid region of the Ferlo, Senegal, based on model simulations. Red isolines depict the mosquito density. Vegetation is represented in green and bare soil in yellow.
Mentions: The proximity of vector and host habitats may not result in a high level of risk if these critical habitats are not connected spatially by landscape features favourable to the circulation of vectors and/or hosts. Spatial diffusion of vectors is particularly crucial in the case of mosquito-borne diseases. At night, when female mosquitoes generally feed, most of the hosts (e.g., humans, cattle) are immobile. The ability of female vectors to spread from their breeding sites to hosts increases host/vector contacts. Landscape features largely control these movements [47]. The study of RVF in the semi-arid region of the Ferlo in Senegal showed that ruminant herds living around temporary water bodies were at greater risk of RVF if they were located close to ponds surrounded by vegetation [22]. A landscape closure index - representing the proportion of surface around each pond covered by vegetation such as dense forest and shrub savannah - was positively correlated with higher serologic incidence. The presence of dense vegetation around water bodies favours the spread of mosquitoes from the pond where they breed to the nearby ruminant herds (Figure 3). The importance of connectivity between habitats for the spread of mosquitoes was also demonstrated for Culex species in Southern France [48]. The connectivity between forest patches may also influence rodent populations and therefore the transmission of rodent-borne diseases such as hantavirus. Linard et al. [24] found that the spatial distribution of bank voles was different during epidemic and non-epidemic years. The number of bank voles captured was higher in more isolated forest patches during the non-epidemic year, whereas it was higher in less isolated patches during the epidemic year. Well-connected patches have more chances to be recolonized after local extinctions [49]. Habitat connectivity could also influence the virus occurrence in hosts by controlling movements of individuals and thus contact rate between infected and susceptible rodents. Langlois et al. [50] observed that hantavirus incidence in deer mice was higher in landscapes with a higher level of fragmentation of the preferred habitat. In Western Africa, Guerrini et al. [51] showed that the riverine forest fragmentation level is a critical factor to determine the habitat of riverine tsetse species, vectors of animal trypanosomosis.

Bottom Line: We formulated ten propositions that are related to landscape attributes, spatial patterns and habitat connectivity, pathways of pathogen transmission between vectors and hosts, scale issues, land use and ownership, and human behaviour associated with transmission cycles.We also highlight the complementarity of the modelling approaches used in our case studies.Integrated analyses at the landscape scale allows a better understanding of interactions between changes in ecosystems and climate, land use and human behaviour, and the ecology of vectors and animal hosts of infectious agents.

View Article: PubMed Central - HTML - PubMed

Affiliation: Georges LemaƮtre Centre for Earth and Climate Research, Earth and Life Institute, University of Louvain, 3 place Pasteur, Louvain-la-Neuve, B-1348, Belgium. eric.lambin@uclouvain.be

ABSTRACT

Background: Landscape attributes influence spatial variations in disease risk or incidence. We present a review of the key findings from eight case studies that we conducted in Europe and West Africa on the impact of land changes on emerging or re-emerging vector-borne diseases and/or zoonoses. The case studies concern West Nile virus transmission in Senegal, tick-borne encephalitis incidence in Latvia, sandfly abundance in the French Pyrenees, Rift Valley Fever in the Ferlo (Senegal), West Nile Fever and the risk of malaria re-emergence in the Camargue, and rodent-borne Puumala hantavirus and Lyme borreliosis in Belgium.

Results: We identified general principles governing landscape epidemiology in these diverse disease systems and geographic regions. We formulated ten propositions that are related to landscape attributes, spatial patterns and habitat connectivity, pathways of pathogen transmission between vectors and hosts, scale issues, land use and ownership, and human behaviour associated with transmission cycles.

Conclusions: A static view of the "pathogenecity" of landscapes overlays maps of the spatial distribution of vectors and their habitats, animal hosts carrying specific pathogens and their habitat, and susceptible human hosts and their land use. A more dynamic view emphasizing the spatial and temporal interactions between these agents at multiple scales is more appropriate. We also highlight the complementarity of the modelling approaches used in our case studies. Integrated analyses at the landscape scale allows a better understanding of interactions between changes in ecosystems and climate, land use and human behaviour, and the ecology of vectors and animal hosts of infectious agents.

Show MeSH
Related in: MedlinePlus