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      Determination of zones at risk for fasciolosis in the department of Haute-Vienne, central France: a retrospective study on natural infections detected in 108,481 Galba truncatula for 37 years Translated title: Détermination des zones à risque pour la fasciolose dans le département de la Haute-Vienne (France) : une étude rétrospective sur les infestations naturelles détectées chez 108.481 Galba truncatula pendant 37 années

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      Parasite
      EDP Sciences
      Altitude, at risk zones, climate, Fasciola hepatica, Galba truncatula, Haute-Vienne, snails

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          Abstract

          A retrospective study on the natural infection of Galba truncatula by Fasciola hepatica was carried out in the French department of Haute-Vienne to determine whether there are areas at risk for fasciolosis. Adult snails included in this analysis came from samples collected from pastures on 259 farms and from 121 wild watercress beds between 1970 and 2006. Fasciola hepatica infection rates were examined in relation to altitude and climatic data (mean annual rainfall, mean annual temperature) of each municipality. In a total of 108,481 snails collected in 151 municipalities, the overall prevalence of infection was 3.8% but varied according to the municipalities from which samples were taken (from 1% to 7.4%). The prevalence of F. hepatica infection in snails significantly decreased when the mean altitude of municipalities or their mean annual rainfall increased. However, this prevalence significantly increased with increasing mean annual temperatures. Studying the prevalence of infection in these snails makes it possible to delineate zones at risk for fasciolosis on the acid soils of Haute-Vienne. The risk of infection for livestock would be greater in areas of Haute-Vienne below 400 m above sea level and would gradually decrease when the altitude of the land increases.

          Translated abstract

          Une étude rétrospective sur l'infestation naturelle de Galba truncatula par Fasciola hepatica a été effectuée dans le département de la Haute-Vienne pour déterminer s'il existe des zones à risque pour la fasciolose. Les limnées adultes impliquées dans cette analyse proviennent d'échantillons prélevés dans les pâturages de 259 fermes et dans 121 cressonnières sauvages entre 1970 et 2006. Les taux d'infection par Fasciola hepatica ont été mis en relation avec l'altitude et les données climatiques (précipitations annuelles moyennes, température annuelle moyenne) de chaque municipalité. Sur un total de 108.481 limnées récoltées dans 151 municipalités, la prévalence globale de l'infestation était de 3,8 %, mais variait selon les municipalités dans lesquelles les échantillons ont été prélevés (de 1 % à 7,4 %). La prévalence de l'infestation par F. hepatica diminue considérablement lorsque l'altitude moyenne des municipalités ou leurs précipitations annuelles moyennes augmente. D'autre part, cette prévalence augmente considérablement avec l'augmentation de la température annuelle moyenne des municipalités. L'étude de la prévalence de l'infestation chez ces limnées permet de délimiter des zones à risque pour la fasciolose sur les sols acides de la Haute-Vienne. Le risque d'infestation pour le bétail serait plus élevé dans les zones de la Haute-Vienne situées en dessous de 400 m d'altitude et diminuerait graduellement lorsque l'altitude de ces terrains augmente.

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          Most cited references64

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          Fascioliasis and other plant-borne trematode zoonoses.

          Fascioliasis and other food-borne trematodiases are included in the list of important helminthiases with a great impact on human development. Six plant-borne trematode species have been found to affect humans: Fasciola hepatica, Fasciola gigantica and Fasciolopsis buski (Fasciolidae), Gastrodiscoides hominis (Gastrodiscidae), Watsonius watsoni and Fischoederius elongatus (Paramphistomidae). Whereas F. hepatica and F. gigantica are hepatic, the other four species are intestinal parasites. The fasciolids and the gastrodiscid cause important zoonoses distributed throughout many countries, while W. watsoni and F. elongatus have been only accidentally detected in humans. Present climate and global changes appear to increasingly affect snail-borne helminthiases, which are strongly dependent on environmental factors. Fascioliasis is a good example of an emerging/re-emerging parasitic disease in many countries as a consequence of many phenomena related to environmental changes as well as man-made modifications. The ability of F. hepatica to spread is related to its capacity to colonise and adapt to new hosts and environments, even at the extreme inhospitality of very high altitude. Moreover, the spread of F. hepatica from its original European range to other continents is related to the geographic expansion of its original European lymnaeid intermediate host species Galba truncatula, the American species Pseudosuccinea columella, and its adaptation to other lymnaeid species authochthonous in the newly colonised areas. Although fasciolopsiasis and gastrodiscoidiasis can be controlled along with other food-borne parasitoses, fasciolopsiasis still remains a public health problem in many endemic areas despite sustained WHO control programmes. Fasciolopsiasis has become a re-emerging infection in recent years and gastrodiscoidiasis, initially supposed to be restricted to Asian countries, is now being reported in African countries.
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            Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control.

            Fascioliasis, caused by liver fluke species of the genus Fasciola, has always been well recognized because of its high veterinary impact but it has been among the most neglected diseases for decades with regard to human infection. However, the increasing importance of human fascioliasis worldwide has re-launched interest in fascioliasis. From the 1990s, many new concepts have been developed regarding human fascioliasis and these have furnished a new baseline for the human disease that is very different to a simple extrapolation from fascioliasis in livestock. Studies have shown that human fascioliasis presents marked heterogeneity, including different epidemiological situations and transmission patterns in different endemic areas. This heterogeneity, added to the present emergence/re-emergence of the disease both in humans and animals in many regions, confirms a worrying global scenario. The huge negative impact of fascioliasis on human communities demands rapid action. When analyzing how better to define control measures for endemic areas differing at such a level, it would be useful to have genetic markers that could distinguish each type of transmission pattern and epidemiological situation. Accordingly, this chapter covers aspects of aetiology, geographical distribution, epidemiology, transmission and control in order to obtain a solid baseline for the interpretation of future results. The origins and geographical spread of F. hepatica and F. gigantica in both the ruminant pre-domestication times and the livestock post-domestication period are analyzed. Paleontological, archaeological and historical records, as well as genetic data on recent dispersal of livestock species, are taken into account to establish an evolutionary framework for the two fasciolids across all continents. Emphasis is given to the distributional overlap of both species and the roles of transportation, transhumance and trade in the different overlap situations. Areas with only one Fasciola spp. are distinguished from local and zonal overlaps in areas where both fasciolids co-exist. Genetic techniques applied to liver flukes in recent years that are useful to elucidate the genetic characteristics of the two fasciolids are reviewed. The intra-specific and inter-specific variabilities of 'pure'F. hepatica and 'pure'F. gigantica were ascertained by means of complete sequences of ribosomal deoxyribonucleic acid (rDNA) internal transcribed spacer (ITS)-2 and ITS-1 and mitochondrial deoxyribonucleic acid (mtDNA) cox1 and nad1 from areas with only one fasciolid species. Fasciolid sequences of the same markers scattered in the literature are reviewed. The definitive haplotypes established appear to fit the proposed global evolutionary scenario. Problems posed by fasciolid cross-breeding, introgression and hybridization in overlap areas are analyzed. Nuclear rDNA appears to correlate with adult fluke characteristics and fasciolid/lymnaeid specificity, whereas mtDNA does not. However, flukes sometimes appear so intermediate that they cannot be ascribed to either F. hepatica-like or F. gigantica-like forms and snail specificity may be opposite to the one deduced from the adult morphotype. The phenotypic characteristics of adults and eggs of 'pure'F. hepatica and F. gigantica, as well as of intermediate forms in overlap areas, are compared, with emphasis on the definitive host influence on egg size in humans. Knowledge is sufficient to support F. hepatica and F. gigantica as two valid species, which recently diverged by adaptation to different pecoran and lymnaeid hosts in areas with differing environmental characteristics. Their phenotypic differences and ancient pre-domestication origins involve a broad geographical area that largely exceeds the typical, more local scenarios known for sub-species units. Phenomena such as abnormal ploidy and aspermic parthenogenesis in hybrids suggest that their separate evolution in pre-domestication times allowed them to achieve almost total genetic isolation. Recent sequencing results suggest that present assumptions on fasciolid-lymnaeid specificity might be wrong. The crucial role of lymnaeids in fascioliasis transmission, epidemiology and control was the reason for launching a worldwide lymnaeid molecular characterization initiative. This initiative has already furnished useful results on several continents. A standardized methodology for fasciolids and lymnaeids is proposed herein in order that future work is undertaken on a comparable basis. A complete understanding of molecular epidemiology is expected to help greatly in designing global actions and local interventions for control of fascioliasis.
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              Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis.

              The capacity of climatic conditions to modulate the extent and intensity of parasitism is well known since long ago. Concerning helminths, among the numerous environmental modifications giving rise to changes in infections, climate variables appear as those showing a greater influence, so that climate change may be expected to have an important impact on the diseases they cause. However, the confirmation of the impact of climate change on helminthiases has been reached very recently. Only shortly before, helminthiases were still noted as infectious diseases scarcely affected by climate change, when compared to diseases caused by microorganisms in general (viruses, bacteriae, protozoans). The aim of the present paper is to review the impact of climate change on helminthiases transmitted by snails, invertebrates which are pronouncedly affected by meteorological factors, by focusing on trematodiases. First, the knowledge on the effects of climate change on trematodiases in general is reviewed, including aspects such as influence of temperature on cercarial output, cercarial production variability in trematode species, influences of magnitude of cercarial production and snail host size, cercarial quality, duration of cercarial production increase and host mortality, influence of latitude, and global-warming-induced impact of trematodes. Secondly, important zoonotic diseases such as fascioliasis, schistosomiasis and cercarial dermatitis are analysed from the point of view of their relationships with meteorological factors. Emphasis is given to data which indicate that climate change influences the characteristics of these trematodiases in concrete areas where these diseases are emerging in recent years. The present review shows that trematodes, similarly as other helminths presenting larval stages living freely in the environment and/or larval stages parasitic in invertebrates easily affected by climate change as arthropods and molluscs as intermediate hosts, may be largely more susceptible to climate change impact than those helminths in whose life cycle such phases are absent or reduced to a minimum. Although helminths also appear to be affected by climate change, their main difference with microparasites lies on the usually longer life cycles of helminths, with longer generation times, slower population growth rates and longer time period needed for the response in the definitive host to become evident. Consequently, after a pronounced climate change in a local area, modifications in helminth populations need more time to be obvious or detectable than modifications in microparasite populations. Similarly, the relation of changes in a helminthiasis with climatic factor changes, as extreme events elapsed relatively long time ago, may be overlooked if not concretely searched for. All indicates that this phenomenon has been the reason for previous analyses to conclude that helminthiases do not constitute priority targets in climate change impact studies.
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                Author and article information

                Journal
                Parasite
                Parasite
                parasite
                Parasite
                EDP Sciences
                1252-607X
                1776-1042
                2017
                22 December 2017
                : 24
                : ( publisher-idID: parasite/2017/01 )
                : 55
                Affiliations
                INSERM 1094, Faculties of Medicine and Pharmacy, 2 rue du Docteur Raymond Marcland, 87025 Limoges Cedex France
                Author notes
                [* ]Corresponding author: gilles.dreyfuss@ 123456unilim.fr
                Article
                parasite170120 10.1051/parasite/2017055
                10.1051/parasite/2017055
                5741376
                29272249
                6eb8ebae-5750-47d2-925e-0c7399dcdff1
                © P. Vignoles et al., published by EDP Sciences, 2017

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 October 2017
                : 3 December 2017
                Page count
                Figures: 4, Tables: 5, Equations: 0, References: 66, Pages: 12
                Categories
                Research Article

                altitude,at risk zones,climate,fasciola hepatica,galba truncatula,haute-vienne,snails

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