1. Describing fine spatiotemporal dynamics of rat fleas in an insular ecosystem enlightens abiotic drivers of murine typhus incidence in humans
- Author
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Tran, Annelise, Le Minter, Gildas, Balleydier, Elsa, Etheves, Anaïs, Laval, Morgane, Boucher, Floriane, Guernier, Vanina, Lagadec, Erwan, Mavingui, Patrick, Cardinale, Eric, Tortosa, Pablo, Territoires, Environnement, Télédétection et Information Spatiale (UMR TETIS), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-AgroParisTech-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Département Environnements et Sociétés (Cirad-ES), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Processus Infectieux en Milieu Insulaire Tropical (PIMIT), Centre National de la Recherche Scientifique (CNRS)-IRD-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de La Réunion (UR), Santé publique France - French National Public Health Agency [Saint-Maurice, France], Animal, Santé, Territoires, Risques et Ecosystèmes (UMR ASTRE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Département Systèmes Biologiques (Cirad-BIOS), This study was funded by the Regional Health Agency in Reunion Island (https://www.ocean-indien.ars.sante.fr/), FEDER INTERREG TROI project, and FEDER-POCT LeptOI project, under the platform in partnership One Health Indian Ocean (www.onehealth-oi.org)., Université de La Réunion (UR)-Institut National de la Santé et de la Recherche Médicale (INSERM)-IRD-Centre National de la Recherche Scientifique (CNRS), and LESUR, Hélène
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Bacterial Diseases ,Topography ,Atmospheric Science ,Epidemiology ,Rain ,[SDV]Life Sciences [q-bio] ,animal diseases ,RC955-962 ,L73 - Maladies des animaux ,Rodent Diseases ,Medical Conditions ,Arctic medicine. Tropical medicine ,Medicine and Health Sciences ,Dynamique des populations ,Xenopsylla ,Rickettsia ,Mammals ,Islands ,U10 - Informatique, mathématiques et statistiques ,Incidence ,Eukaryota ,Typhus, Endemic Flea-Borne ,Animal Models ,[SDV] Life Sciences [q-bio] ,Insects ,Infectious Diseases ,Fleas ,Experimental Organism Systems ,S50 - Santé humaine ,Vertebrates ,Île ,Seasons ,Public aspects of medicine ,RA1-1270 ,Research Article ,zoonose ,Arthropoda ,Research and Analysis Methods ,Rodents ,Typhus ,Flea Infestations ,Spatio-Temporal Analysis ,Meteorology ,Model Organisms ,Animals ,Humans ,Surveillance épidémiologique ,Ecosystem ,Transmission des maladies ,Landforms ,Organisms ,Biology and Life Sciences ,Geomorphology ,Distribution spatiale ,facteurs abiotiques ,bacterial infections and mycoses ,Invertebrates ,Rats ,[SDV.SPEE] Life Sciences [q-bio]/Santé publique et épidémiologie ,Modélisation ,Murine Typhus ,Amniotes ,Earth Sciences ,Animal Studies ,[SDV.SPEE]Life Sciences [q-bio]/Santé publique et épidémiologie ,Reunion ,Zoology ,Entomology - Abstract
Murine typhus is a flea-borne zoonotic disease that has been recently reported on Reunion Island, an oceanic volcanic island located in the Indian Ocean. Five years of survey implemented by the regional public health services have highlighted a strong temporal and spatial structure of the disease in humans, with cases mainly reported during the humid season and restricted to the dry southern and western portions of the island. We explored the environmental component of this zoonosis in an attempt to decipher the drivers of disease transmission. To do so, we used data from a previously published study (599 small mammals and 175 Xenopsylla fleas from 29 sampling sites) in order to model the spatial distribution of rat fleas throughout the island. In addition, we carried out a longitudinal sampling of rats and their ectoparasites over a 12 months period in six study sites (564 rats and 496 Xenopsylla fleas) in order to model the temporal dynamics of flea infestation of rats. Generalized Linear Models and Support Vector Machine classifiers were developed to model the Xenopsylla Genus Flea Index (GFI) from climatic and environmental variables. Results showed that the spatial distribution and the temporal dynamics of fleas, estimated through the GFI variations, are both strongly controlled by abiotic factors: rainfall, temperature and land cover. The models allowed linking flea abundance trends with murine typhus incidence rates. Flea infestation in rats peaked at the end of the dry season, corresponding to hot and dry conditions, before dropping sharply. This peak of maximal flea abundance preceded the annual peak of human murine typhus cases by a few weeks. Altogether, presented data raise novel questions regarding the ecology of rat fleas while developed models contribute to the design of control measures adapted to each micro region of the island with the aim of lowering the incidence of flea-borne diseases., Author summary Murine typhus is a neglected zoonotic disease, as the number of human cases is likely underestimated in the absence of specific symptoms. It is caused by Rickettsia typhi, a pathogenic bacterium transmitted by rat fleas (Xenospylla spp). The distribution and dynamics of this disease result from complex interactions involving vectors, reservoirs and humans within a shared environment. In this study, we explored the environmental drivers of rat fleas’ abundance on Reunion Island, where murine typhus has recently emerged. Results showed that i) rat fleas’ abundance is highly dynamic, characterized by a peak at the end of the dry season and ii) among the factors investigated, rainfall, temperature and land cover are the main determinants of rat fleas’ abundance. We modeled a predictive map of flea distribution that strongly correlates with the spatial distribution of human cases on the island. This study highlights the importance of accounting for environmental and climatic characteristics to better understand the spatial and temporal drivers of flea-borne diseases.
- Published
- 2021
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