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      DNA multigene characterization of Fasciola hepatica and Lymnaea neotropica and its fascioliasis transmission capacity in Uruguay, with historical correlation, human report review and infection risk analysis

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          Abstract

          Background

          Fascioliasis is a pathogenic disease transmitted by lymnaeid snails and recently emerging in humans, in part due to effects of climate changes, anthropogenic environment modifications, import/export and movements of livestock. South America is the continent presenting more human fascioliasis hyperendemic areas and the highest prevalences and intensities known. These scenarios appear mainly linked to altitude areas in Andean countries, whereas lowland areas of non-Andean countries, such as Uruguay, only show sporadic human cases or outbreaks. A study including DNA marker sequencing of fasciolids and lymnaeids, an experimental study of the life cycle in Uruguay, and a review of human fascioliasis in Uruguay, are performed.

          Methodology/Principal findings

          The characterization of Fasciola hepatica from cattle and horses of Uruguay included the complete sequences of the ribosomal DNA ITS-2 and ITS-1 and mitochondrial DNA cox1 and nad1. ITS-2, ITS-1, partial cox1 and rDNA 16S gene of mtDNA were used for lymnaeids. Results indicated that vectors belong to Lymnaea neotropica instead of to Lymnaea viator, as always reported from Uruguay. The life cycle and transmission features of F. hepatica by L. neotropica of Uruguay were studied under standardized experimental conditions to enable a comparison with the transmission capacity of F. hepatica by Galba truncatula at very high altitude in Bolivia. On this baseline, we reviewed the 95 human fascioliasis cases reported in Uruguay and analyzed the risk of human infection in front of future climate change estimations.

          Conclusions/Significance

          The correlation of fasciolid and lymnaeid haplotypes with historical data on the introduction and spread of livestock into Uruguay allowed to understand the molecular diversity detected. Although Uruguayan L. neotropica is a highly efficient vector, its transmission capacity is markedly lower than that of Bolivian G. truncatula. This allows to understand the transmission and epidemiological differences between Andean highlands and non-Andean lowlands in South America. Despite rainfall increase predictions for Uruguay, nothing suggests a trend towards a worrying human infection scenario as in Andean areas.

          Author summary

          Fascioliasis is a highly pathogenic zoonotic disease emerging in recent decades, in part due to the effects of climate and global changes. South America is the continent presenting more numerous human fascioliasis endemic areas and the highest Fasciola hepatica infection prevalences and intensities known in humans. These serious public health scenarios appear mainly linked to altitude areas in Andean countries, whereas lowland areas of non-Andean countries, such as Uruguay, only show sporadic human cases or outbreaks. To understand this difference, we characterized F. hepatica from cattle and horses and lymnaeids of Uruguay by sequencing of ribosomal DNA ITS-2 and ITS-1 spacers and mitochondrial DNA cox1, nad1 and 16S genes. Results indicate that vectors belong to Lymnaea neotropica instead of to Lymnaea viator, as always reported from Uruguay. Our correlation of fasciolid and lymnaeid haplotypes with historical data on the introduction and spread of livestock species into Uruguay allow to understand the molecular diversity detected. We study the life cycle and transmission features of F. hepatica by L. neotropica of Uruguay under standardized experimental conditions to enable a comparison with the transmission capacity of F. hepatica by Galba truncatula at very high altitude in Bolivia. Results demonstrate that although L. neotropica is a highly efficient vector in the lowlands, its transmission capacity is markedly lower than that of G. truncatula in the highlands. On this baseline, we review the human fascioliasis cases reported in Uruguay and analyze the present and future risk of human infection in front of future climate change estimations.

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          Most cited references 60

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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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            Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study.

            Schistosomiasis is a snail-borne parasitic disease endemic in several tropical and subtropical countries. However, in the summer of 2013, an unexpected outbreak of urogenital schistosomiasis occurred in Corsica, with more than 120 local people or tourists infected. We used a multidisciplinary approach to investigate the epidemiology of urogenital schistosomiasis in Corsica, aiming to elucidate the origin of the outbreak.
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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

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                3 February 2017
                February 2017
                : 11
                : 2
                Affiliations
                [1 ]Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Valencia, Spain
                [2 ]Departamento de Parasitología, División de Laboratorios Veterinarios (DILAVE), "Miguel C. Rubino", Ministerio de Ganadería, Agricultura y Pesca (MGAP), Montevideo, Uruguay
                [3 ]Departamento de Parasitologia, Universidad de la República (Regional Norte), Salto, Uruguay
                [4 ]Facultad de Veterinaria, Universidad de la República Oriental del Uruguay, Montevideo, Uruguay
                Queen's University Belfast, IRELAND
                Author notes

                The authors have declared that no competing interests exist.

                • Conceptualization: MDB SMC.

                • Formal analysis: MDB MK SMC.

                • Funding acquisition: MDB VG SMC.

                • Investigation: MDB JS PA MK SMC.

                • Methodology: MDB VG JS PA MK SMC.

                • Project administration: SMC MDB.

                • Resources: MDB VG JS SB SMC.

                • Supervision: SMC.

                • Validation: MDB SMC.

                • Visualization: SMC.

                • Writing – original draft: MDB SMC.

                • Writing – review & editing: MDB VG SMC.

                Article
                PNTD-D-16-01504
                10.1371/journal.pntd.0005352
                5310921
                28158188
                © 2017 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
                Figures: 8, Tables: 2, Pages: 33
                Product
                Funding
                Funded by: Ministry of Economy and Competitiveness, Madrid, Spain
                Award ID: SAF2006-09278
                Award Recipient :
                Funded by: Ministry of Economy and Competitiveness, Madrid, Spain
                Award ID: SAF2010-20805
                Award Recipient :
                Funded by: ISCIII-Subdirección General de Redes y Centros de Investigación Cooperativa RETICS, Ministry of Health and Consumption, Madrid
                Award ID: Red de Investigación Cooperativa en Enfermedades Tropicales – RICET (Project No. RD12/0018/0013)
                Award Recipient :
                Funded by: Generalitat Valenciana, Valencia, Spain
                Award ID: Projects 2012/042 and 2016/099 of the PROMETEO Program
                Award Recipient :
                Funded by: The International Atomic Energy Agency (Animal Production and Health Section, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Department of Nuclear Sciences and Applications, IAEA Headquaters Vienna, Austria)
                Award ID: Project No. RLA5049
                Award Recipient :
                Joint coordination activities carried out within Project No. RLA5049 of the International Atomic Energy Agency (Animal Production and Health Section, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Department of Nuclear Sciences and Applications, IAEA Headquaters Vienna, Austria). Spanish collaboration supported by Projects Nos. SAF2006-09278 and SAF2010-20805 of the Ministry of Economy and Competitiveness, Madrid, Spain; by the Red de Investigación Cooperativa en Enfermedades Tropicales – RICET (Projects Nos. RD12/0018/0013 and RD16/0027/0023 of the PN de I+D+I 2008-2011 and 2013-2016, ISCIII-Subdirección General de Redes y Centros de Investigación Cooperativa RETICS), Ministry of Health and Consumption, Madrid; and by Projects Nos. 2012/042 and 2016/099 of the PROMETEO Program, Generalitat Valenciana, Valencia, Spain. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                People and places
                Geographical locations
                South America
                Uruguay
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Bovines
                Cattle
                Biology and Life Sciences
                Agriculture
                Livestock
                Cattle
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Ruminants
                Cattle
                Biology and Life Sciences
                Genetics
                Heredity
                Genetic Mapping
                Haplotypes
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Molluscs
                Gastropods
                Snails
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Molting
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Molting
                Biology and Life Sciences
                Agriculture
                Livestock
                Biology and Life Sciences
                Agriculture
                Livestock
                Sheep
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Ruminants
                Sheep
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Fascioliasis
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Fascioliasis
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-02-15
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology

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