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      Lymnaea schirazensis, an Overlooked Snail Distorting Fascioliasis Data: Genotype, Phenotype, Ecology, Worldwide Spread, Susceptibility, Applicability


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          Lymnaeid snails transmit medical and veterinary important trematodiases, mainly fascioliasis. Vector specificity of fasciolid parasites defines disease distribution and characteristics. Different lymnaeid species appear linked to different transmission and epidemiological patterns. Pronounced susceptibility differences to absolute resistance have been described among lymnaeid populations. When assessing disease characteristics in different endemic areas, unexpected results were obtained in studies on lymnaeid susceptibility to Fasciola. We undertook studies to understand this disease transmission heterogeneity.

          Methodology/Principal Findings

          A ten-year study in Iran, Egypt, Spain, the Dominican Republic, Mexico, Venezuela, Ecuador and Peru, demonstrated that such heterogeneity is not due to susceptibility differences, but to a hitherto overlooked cryptic species, Lymnaea schirazensis, confused with the main vector Galba truncatula and/or other Galba/ Fossaria vectors. Nuclear rDNA and mtDNA sequences and phylogenetic reconstruction highlighted an old evolutionary divergence from other Galba/ Fossaria species, and a low intraspecific variability suggesting a recent spread from one geographical source. Morphometry, anatomy and egg cluster analyses allowed for phenotypic differentiation. Selfing, egg laying, and habitat characteristics indicated a migration capacity by passive transport. Studies showed that it is not a vector species (n = 8572 field collected, 20 populations): snail finding and penetration by F. hepatica miracidium occur but never lead to cercarial production (n = 338 experimentally infected).


          This species has been distorting fasciolid specificity/susceptibility and fascioliasis geographical distribution data. Hence, a large body of literature on G. truncatula should be revised. Its existence has henceforth to be considered in research. Genetic data on livestock, archeology and history along the 10,000-year post-domestication period explain its wide spread from the Neolithic Fertile Crescent. It is an efficient biomarker for the follow-up of livestock movements, a crucial aspect in fascioliasis emergence. It offers an outstanding laboratory model for genetic studies on susceptibility/resistance in F. hepatica/lymnaeid interaction, a field of applied research with disease control perspectives.

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          Most cited references 148

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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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              Epidemiology of fascioliasis in human endemic areas.

               S Mas-Coma (2005)
              Considered a secondary zoonotic disease until the mid-1990s, human fascioliasis is at present emerging or re-emerging in many countries, including increases of prevalence and intensity and geographical expansion. Research in recent years has justified the inclusion of fascioliasis in the list of important human parasitic diseases. At present, fascioliasis is a vector-borne disease presenting the widest known latitudinal, longitudinal and altitudinal distribution. Fasciola hepatica has succeeded in expanding from its European original geographical area to colonize five continents, despite theoretical restrictions related to its biology and in turn dependent upon environmental and human activities. Among the different epidemiological situations, human hypo- to hyperendemic areas, including epidemics, are noteworthy. A global analysis of the distribution of human cases shows that the expected correlation between animal and human fascioliasis only appears at a basic level. Areas presenting very high human prevalences and intensities, especially in children and females, have been recently described. In hypo- to hyperendemic areas of Central and South America, Europe, Africa and Asia, human fascioliasis presents a range of epidemiological characteristics related to a wide diversity of environments. Thus far well-known epidemiological patterns of fascioliasis may not always explain the transmission characteristics in any given area and control measures should consider the results of ecoepidemiological studies undertaken in the zones concerned.

                Author and article information

                Role: Editor
                PLoS One
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                29 September 2011
                : 6
                : 9
                [1 ]Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Valencia, Spain
                [2 ]Münchner Malakologische Mitteilungen Heldia, Friedrich-Held Gesellschaft, Hetlingen, Germany
                [3 ]Laboratorio de Biología de Parásitos y Vectores, Escuela de Biología, Benemérita Universidad Autónoma de Puebla, Puebla, México
                [4 ]Department of Medical Microbiology and Parasitology, School of Medicine, Gilan University of Medical Sciences, Rasht, Iran
                [5 ]Staatliches Museum für Naturkunde Stuttgart, Stuttgart, Germany
                [6 ]Département Systématique et Evolution, UMS “Taxonomie et Collections”, Muséum National d’Histoire Naturelle, Paris, France
                Universidade Federal de Minas Gerais, Brazil
                Author notes

                Conceived and designed the experiments: SM-C. Performed the experiments: MB PA MK RF PG RR-G. Analyzed the data: MB PG RR-G GF SM-C. Contributed reagents/materials/analysis tools: MB PA MK RR-G KA SM-C. Wrote the paper: SM-C. Analyzed old snail literature: GF SM-C. Revision and final approval of the article: MB GF SM-C.

                Bargues et al. 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.
                Page count
                Pages: 33
                Research Article
                Global Change Ecology
                Evolutionary Biology
                Population Genetics
                Animal Phylogenetics
                Animal Taxonomy
                Comparative Anatomy
                Biomarker Epidemiology
                Infectious Disease Epidemiology
                Molecular Epidemiology
                Global Health
                Infectious Diseases
                Neglected Tropical Diseases
                Parasitic Diseases
                Public Health
                Disease Ecology
                Veterinary Science
                Veterinary Diseases
                Zoonotic Diseases
                Foodborne Diseases
                Veterinary Epidemiology



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