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      Environmental determinants of spatial and temporal variations in the transmission of Toxoplasma gondii in its definitive hosts

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          Highlights

          • Toxoplasma gondii seroprevalences in 112 European wildcats, 20 domestic cats and 47 hybrids are reported.

          • The seroprevalence (overall 65.2%) did not differ with the type of cat.

          • High farm densities and mild winters are associated with the highest seroprevalence.

          Abstract

          Toxoplasmosis is a major zoonosis, and its prevention requires multiple approaches due to the complex life-cycle of its causative agent, Toxoplasma gondii. Environmental contamination by oocysts is a key factor in the transmission of T. gondii to both humans and meat-producing animals; however, its spatial and temporal variations are poorly understood. We analysed the distribution of T. gondii seropositivity in a sample of 210 cats, including the European wildcat ( Felis silvestris silvestris), the domestic cat ( Felis silvestris catus) and their hybrids that were collected in Central and Eastern France between 1996 and 2006. We searched for spatial variability among communes and temporal variations among years to relate this variability to landscape and meteorological conditions, which can affect the population dynamics of rodent hosts and the survival of oocysts. The overall seroprevalence was 65.2% (95% CI: 58.6–71.4). As expected, adults were more often infected than young individuals, while the occurrence of infection was not related to cat genotypes. Seroprevalence correlated significantly with farm density and the North-Atlantic Oscillation index, which describes temporal variations of meteorological conditions at the continental scale. The highest seroprevalence values were obtained in areas with high farm densities and during years with cool and moist winters. These results suggest that both farming areas and years with cool and wet winters are associated with increased T. gondii seroprevalence in cats. As cat infection determines the environmental contamination by oocysts, climate and landscape characteristics should be taken into account to improve the risk analysis and prevention of T. gondii.

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          Most cited references67

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          Ecological effects of climate fluctuations.

          Climate influences a variety of ecological processes. These effects operate through local weather parameters such as temperature, wind, rain, snow, and ocean currents, as well as interactions among these. In the temperate zone, local variations in weather are often coupled over large geographic areas through the transient behavior of atmospheric planetary-scale waves. These variations drive temporally and spatially averaged exchanges of heat, momentum, and water vapor that ultimately determine growth, recruitment, and migration patterns. Recently, there have been several studies of the impact of large-scale climatic forcing on ecological systems. We review how two of the best-known climate phenomena-the North Atlantic Oscillation and the El Niño-Southern Oscillation-affect ecological patterns and processes in both marine and terrestrial systems.
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            Effects of environmental change on emerging parasitic diseases.

            Ecological disturbances exert an influence on the emergence and proliferation of malaria and zoonotic parasitic diseases, including, Leishmaniasis, cryptosporidiosis, giardiasis, trypanosomiasis, schistosomiasis, filariasis, onchocerciasis, and loiasis. Each environmental change, whether occurring as a natural phenomenon or through human intervention, changes the ecological balance and context within which disease hosts or vectors and parasites breed, develop, and transmit disease. Each species occupies a particular ecological niche and vector species sub-populations are distinct behaviourally and genetically as they adapt to man-made environments. Most zoonotic parasites display three distinct life cycles: sylvatic, zoonotic, and anthroponotic. In adapting to changed environmental conditions, including reduced non-human population and increased human population, some vectors display conversion from a primarily zoophyllic to primarily anthrophyllic orientation. Deforestation and ensuing changes in landuse, human settlement, commercial development, road construction, water control systems (dams, canals, irrigation systems, reservoirs), and climate, singly, and in combination have been accompanied by global increases in morbidity and mortality from emergent parasitic disease. The replacement of forests with crop farming, ranching, and raising small animals can create supportive habitats for parasites and their host vectors. When the land use of deforested areas changes, the pattern of human settlement is altered and habitat fragmentation may provide opportunities for exchange and transmission of parasites to the heretofore uninfected humans. Construction of water control projects can lead to shifts in such vector populations as snails and mosquitoes and their parasites. Construction of roads in previously inaccessible forested areas can lead to erosion, and stagnant ponds by blocking the flow of streams when the water rises during the rainy season. The combined effects of environmentally detrimental changes in local land use and alterations in global climate disrupt the natural ecosystem and can increase the risk of transmission of parasitic diseases to the human population.
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              Control of the risk of human toxoplasmosis transmitted by meat.

              One-third of the human world population is infected with the protozoan parasite Toxoplasma gondii. Recent calculations of the disease burden of toxoplasmosis rank this foodborne disease at the same level as salmonellosis or campylobacteriosis. The high disease burden in combination with disappointing results of the currently available treatment options have led to a plea for more effective prevention. In this review we describe Toxoplasma as a hazard associated with the consumption of undercooked meat or meat products and provide an analysis of the various options to control the risk of human toxoplasmosis via this source. Monitoring and surveillance programs may be implemented for pre-harvest control of Toxoplasma infection of farm animals, with the reduction of environmental oocyst load as the most important milestone. Alternatively, Toxoplasma safe meat can be obtained through simple post-harvest decontamination procedures, whereby freezing the meat may currently be the best option, although new technologies using irradiation or high-pressure treatment may offer promising alternatives. Influence of culture, religion and food handling customs may predispose a certain type of meat as an important source of infection, indicating that prevention needs to be tailored according to social habits in different regions in the world. The rationale for more stringent control measures to prevent toxoplasmosis both from disease and economic points of view is emphasized.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol Parasites Wildl
                Int J Parasitol Parasites Wildl
                International Journal for Parasitology. Parasites and Wildlife
                Elsevier
                2213-2244
                23 September 2013
                23 September 2013
                December 2013
                : 2
                : 278-285
                Affiliations
                [a ]Université de Lyon, Université Lyon 1, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, 43 bd du 11 novembre 1918, 69622 Villeurbanne Cedex, France
                [b ]CROC, Carnivores Recherche Observation Communication, 57590 Fonteny, France
                [c ]Université de Reims Champagne-Ardenne, UFR Médecine, SFR CAP-Santé, EA3800, 51 rue Cognacq Jay, 51095 Reims Cedex, France
                [d ]Université de Reims Champagne-Ardenne, Centre de Recherche et de Formation en Eco-éthologie, 08240 Boult-aux-Bois, France
                [e ]Office National de la Chasse et de la Faune Sauvage, CNERA PAD, Montfort, 01330 Birieux, France
                [f ]Université de Lyon, VetAgro-sup, Département de Santé Publique Vétérinaire, 1 avenue Bourgelat, 69280 Marcy l’Etoile, France
                Author notes
                [* ]Corresponding author. Present address: Université de Franche-Comté, Laboratoire Chrono-Environnement, UMR CNRS 6249 USC INRA, Place Leclerc, 25030 Besançon Cedex, France. Tel.: +33 3 81 66 57 91. eve.afonso@ 123456univ-fcomte.fr
                Article
                S2213-2244(13)00030-8
                10.1016/j.ijppaw.2013.09.006
                3862504
                24533347
                292bf2ab-89c3-4d1d-bf66-a794436a78a2
                © 2013 The Authors

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.

                History
                : 2 May 2013
                : 3 September 2013
                : 4 September 2013
                Categories
                Article

                toxoplasmosis,meteorological variations,farm density,north-atlantic oscillation index,felis silvestris,felis catus

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