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      Bovine fasciolosis at increasing altitudes: Parasitological and malacological sampling on the slopes of Mount Elgon, Uganda

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          Abstract

          Background

          To clarify the extent and putative transmission zone of bovine fasciolosis on the slopes of Mount Elgon, Uganda, conjoint parasitological and malacological surveys, inclusive of inspection of animals at slaughter, were undertaken at increasing altitudes.

          Results

          A total of 239 cattle were sampled across eight locations ranging in elevation from 1112-2072 m. Faecal material was examined for presence of Fasciola eggs and sera were tested by ELISA for antibodies against Fasciola antigens. Bolstering this, 38 cattle at slaughter from 2 abattoir sites at 1150 m and 1947 m were inspected; in addition, wild buffalo stool (n = 10) opportunistically picked within Mount Elgon National Park (MENP) at 3640 m was examined. By faecal egg detection, prevalence of Fasciola gigantica at low (<1500 m) and high (>1500 m) altitude sites was 43.7% (95% CI 35.4-52.2) and 1.1% (95% CI 0.0-6.0), respectively, while by ELISA was much higher, low altitude - 77.9% (95% CI 69.7-85.4) and high altitude - 64.5% (95% CI 51.3-76.3). The decline in prevalence with increasing altitude was corroborated by abattoir sampling. Thirty seven aquatic habitats, ranging from 1139-3937 m in altitude were inspected for freshwater snails, 12 of which were within MENP. At lower altitudes, Lymnaea (Radix) natalensis was common, and often abundant, but at higher altitudes became much rarer ceasing to be found above 1800 m. On the other hand, Lymnaea (Galba) truncatula was found only at altitudes above 3000 m and within MENP alone. The snail identifications were confirmed by DNA analysis of the ribosomal 18S gene.

          Conclusions

          Active infections of F. gigantica in cattle are common in lower altitude settings but appear to diminish with increasing elevation. This is likely due to a growing paucity of intermediate hosts, specifically populations of L. natalensis for which a natural boundary of 1800 m appeared. Although F. hepatica was not encountered, the presence of several populations of L. truncatula at elevations over 3000 m point towards a potential transmission zone within MENP should this parasite be introduced.

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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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            Relative importance of management, meteorological and environmental factors in the spatial distribution of Fasciola hepatica in dairy cattle in a temperate climate zone.

            Fasciola hepatica, a trematode parasite with a worldwide distribution, is the cause of important production losses in the dairy industry. Diagnosis is hampered by the fact that the infection is mostly subclinical. To increase awareness and develop regionally adapted control methods, knowledge on the spatial distribution of economically important infection levels is needed. Previous studies modelling the spatial distribution of F. hepatica are mostly based on single cross-sectional samplings and have focussed on climatic and environmental factors, often ignoring management factors. This study investigated the associations between management, climatic and environmental factors affecting the spatial distribution of infection with F. hepatica in dairy herds in a temperate climate zone (Flanders, Belgium) over three consecutive years. A bulk-tank milk antibody ELISA was used to measure F. hepatica infection levels in a random sample of 1762 dairy herds in the autumns of 2006, 2007 and 2008. The infection levels were included in a Geographic Information System together with meteorological, environmental and management parameters. Logistic regression models were used to determine associations between possible risk factors and infection levels. The prevalence and spatial distribution of F. hepatica was relatively stable, with small interannual differences in prevalence and location of clusters. The logistic regression model based on both management and climatic/environmental factors included the factors: annual rainfall, mowing of pastures, proportion of grazed grass in the diet and length of grazing season as significant predictors and described the spatial distribution of F. hepatica better than the model based on climatic/environmental factors only (annual rainfall, elevation and slope, soil type), with an Area Under the Curve of the Receiver Operating Characteristic of 0.68 compared with 0.62. The results indicate that in temperate climate zones without large climatic and environmental variation, management factors affect the spatial distribution of F. hepatica, and should be included in future spatial distribution models. Copyright © 2010 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
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              Qualitative and quantitative evaluation of coprological and serological techniques for the diagnosis of fasciolosis in cattle.

              The objectives of this study were (1) to evaluate available coprological and serological tests for detection of Fasciola hepatica infection in field conditions, (2) to investigate if the season when samples were collected affects the interpretation of the test results, and (3) to evaluate if the test results are associated with the level of infection. During weekly visits to an abattoir, the whole liver, a rectal faecal sample and a blood sample were collected from 100 cows in two seasons each ("spring"=February-May 2006 and "autumn"=October-December 2006). A sedimentation-flotation technique on 4g (SF 4g) or 10g (SF 10g) of faeces, a copro-antigen ELISA and two indirect serum F. hepatica ELISAs (excretory-secretory (ES) and Pourquier ELISA) were performed and the test results were compared with the presence of infection and worm counts at liver necropsy. Over both seasons the sensitivity (Se) and specificity (Sp) were for the SF 4g 43% and 100%, for the SF 10g 64% and 93%, for the copro-antigen ELISA 94% and 93%, for the ES ELISA 87% and 90% and for the Pourquier ELISA 88% and 84%. Significant between-season differences (P 10 flukes) than that is free of infection or lightly infected (< or = 10 flukes). Weak ( approximately 0.3) and moderate ( approximately 0.6) correlations were observed within infected animals of level of infection with ES and copro-antigen ELISA results, respectively.
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                Author and article information

                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central
                1756-3305
                2012
                7 September 2012
                : 5
                : 196
                Affiliations
                [1 ]Disease Control Strategy Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, United Kingdom
                [2 ]College of Veterinary Medicine, Animal Resources & Biosecurity, Makerere University, Kampala, Uganda
                [3 ]Conservation & Ecosystem Health Alliance (CEHA), P.O. Box 34153, Kampala, Uganda
                [4 ]Veterinary Parasitology, Institute of Infection and Global Health, School of Veterinary Science, University of Liverpool, Liverpool, L69 7ZJ, United Kingdom
                [5 ]Vector Control Division, Ministry of Health, Kampala, Uganda
                Article
                1756-3305-5-196
                10.1186/1756-3305-5-196
                3464174
                22958402
                3fa8581c-67b4-4664-a3c3-77913e8cf2dd
                Copyright ©2012 Howell et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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                Research

                Parasitology

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