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      Sheep and Cattle Reservoirs in the Highest Human Fascioliasis Hyperendemic Area: Experimental Transmission Capacity, Field Epidemiology, and Control Within a One Health Initiative in Bolivia

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          Abstract

          The Northern Bolivian Altiplano is the human fascioliasis hyperendemic area where the highest prevalences and intensities of infection by Fasciola hepatica in humans have been reported. Four animal species are the reservoir species for F. hepatica in this area, namely, sheep, cattle, pigs, and donkeys. Livestock for the Aymara inhabitants is crucial because vegetable cultures are not viable due to the inhospitality of the very high altitude of 3,820–4,100 m. A One Health initiative has been implemented in this area in recent years, as the first such control action in a human endemic area ever. Among the different control axes included, special focus is devoted to the two main reservoirs sheep and cattle. Egg embryonation, miracidial infectivity, intramolluscan development, cercarial production, infected snail survival, and metacercarial infectivity were experimentally studied in altiplanic sheep and cattle isolates. These laboratory studies were performed using altiplanic isolates of the lymnaeid species Galba truncatula, the only vector present in the hyperendemic area. Experiments were made at constant 12 h day/12 h night and varying 20/20°C and 22/5°C photoperiods. Infections were implemented using mono-, bi-, and trimiracidial doses. Results demonstrate that sheep and cattle have the capacity to assure F. hepatica transmission in this very high-altitude area. Field surveys included prevalence studies by coprology on fecal samples from 1,202 sheep and 2,690 cattle collected from different zones of the Northern Bolivian Altiplano. Prevalences were pronouncedly higher and more homogeneous in sheep (63.1%; range: 38.9–68.5%) than in cattle (20.6%; range: 8.2–43.3%) in each one of the different zones. Although similarities between the prevalences in sheep and cattle appeared in the zones of the highest and lowest infection rates, this disappeared in the other zones due to cattle treatments. Comparison with past surveys demonstrates that this hyperendemic area is stable from the disease transmission point of view. Therefore, the control design should prioritize sheep and cattle within the One Health action. Studies performed in the Bolivian Altiplano furnish a baseline for future initiatives to assess the transmission and epidemiological characteristics of fascioliasis in the way for its control in other high altitude Andean endemic areas.

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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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            The One Health Concept: 10 Years Old and a Long Road Ahead

            Over the past decade, a significant increase in the circulation of infectious agents was observed. With the spread and emergence of epizootics, zoonoses, and epidemics, the risks of pandemics became more and more critical. Human and animal health has also been threatened by antimicrobial resistance, environmental pollution, and the development of multifactorial and chronic diseases. This highlighted the increasing globalization of health risks and the importance of the human–animal–ecosystem interface in the evolution and emergence of pathogens. A better knowledge of causes and consequences of certain human activities, lifestyles, and behaviors in ecosystems is crucial for a rigorous interpretation of disease dynamics and to drive public policies. As a global good, health security must be understood on a global scale and from a global and crosscutting perspective, integrating human health, animal health, plant health, ecosystems health, and biodiversity. In this study, we discuss how crucial it is to consider ecological, evolutionary, and environmental sciences in understanding the emergence and re-emergence of infectious diseases and in facing the challenges of antimicrobial resistance. We also discuss the application of the “One Health” concept to non-communicable chronic diseases linked to exposure to multiple stresses, including toxic stress, and new lifestyles. Finally, we draw up a list of barriers that need removing and the ambitions that we must nurture for the effective application of the “One Health” concept. We conclude that the success of this One Health concept now requires breaking down the interdisciplinary barriers that still separate human and veterinary medicine from ecological, evolutionary, and environmental sciences. The development of integrative approaches should be promoted by linking the study of factors underlying stress responses to their consequences on ecosystem functioning and evolution. This knowledge is required for the development of novel control strategies inspired by environmental mechanisms leading to desired equilibrium and dynamics in healthy ecosystems and must provide in the near future a framework for more integrated operational initiatives.
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              A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants.

              Fasciolosis is an important plant borne trematode zoonosis in ruminants caused by the Fasciola hepatica and Fasciola gigentica, It is classified as a neglected tropical disease and found in more than 50 countries especially where sheep and cattle are reared. Fasciolosis is a serious animal health problems in many rural and urban areas of world, causing significant financial losses due to decrease in production and viscera condemnation in animals. Accurate diagnosis of fasciolosis is always remained a challenging task for the field practitioners. There is no comprehensive summary on the occurrence and distribution of the infection at international level. Therefore, we intended to provide a complete overview on the prevalence and epidemiology of fasciolosis in farm animals from a global prospective. It includes to map the global distribution of fasciolosis in different areas of the world to identify the endemic regions which may be a source of potential disease outbreak. The financial liability related to fasciolosis on the livestock production has also been addressed. For this purpose, the published data during 2000-2015 (15 years) on fasciolosis was reviewed and collected by electronic literature search of four databases including Google, PubMed, Science Direct, and Web of Science. Data presented are contemplated to enhance our current understanding of the parasite's geographical distribution, host range, and economic losses. Information provided would be useful for the application of more effective control strategies against fasciolosis in different geo-economics regions of the world.
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                Author and article information

                Contributors
                Journal
                Front Vet Sci
                Front Vet Sci
                Front. Vet. Sci.
                Frontiers in Veterinary Science
                Frontiers Media S.A.
                2297-1769
                27 October 2020
                2020
                : 7
                : 583204
                Affiliations
                [1] 1Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia , Valencia, Spain
                [2] 2Unidad de Limnología, Instituto de Ecología, Universidad Mayor de San Andrés , La Paz, Bolivia
                [3] 3Cátedra de Parasitología, Facultad de Medicina, Universidad Mayor de San Andrés , La Paz, Bolivia
                Author notes

                Edited by: Theo De Waal, University College Dublin, Ireland

                Reviewed by: Marcelo B. Molento, Federal University of Paraná, Brazil; Luis Alvarez, Universidad Nacional del Centro de Buenos Aires, Argentina

                *Correspondence: M. Dolores Bargues m.d.bargues@ 123456uv.es

                This article was submitted to Parasitology, a section of the journal Frontiers in Veterinary Science

                Article
                10.3389/fvets.2020.583204
                7655135
                33195605
                ced5f580-5d08-4f99-848d-d3493c283906
                Copyright © 2020 Mas-Coma, Buchon, Funatsu, Angles, Artigas, Valero and Bargues.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 14 July 2020
                : 24 September 2020
                Page count
                Figures: 3, Tables: 3, Equations: 0, References: 94, Pages: 14, Words: 11658
                Funding
                Funded by: Agencia Española de Cooperación Internacional para el Desarrollo 10.13039/501100004892
                Funded by: International Atomic Energy Agency 10.13039/501100004493
                Funded by: Ministerio de Economía, Industria y Competitividad, Gobierno de España 10.13039/501100010198
                Funded by: Ministerio de Sanidad, Consumo y Bienestar Social 10.13039/100016145
                Funded by: Conselleria de Cultura, Educación y Ciencia, Generalitat Valenciana 10.13039/501100014849
                Funded by: Universitat de València 10.13039/501100003508
                Categories
                Veterinary Science
                Original Research

                fasciola hepatica,sheep and cattle,reservoirs,transmission,epidemiology,human hyperendemic,very high altitude,bolivia

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