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      Outcomes of Trypanosoma cruzi and Trypanosoma evansi infections on health of Southern coati ( Nasua nasua), crab-eating fox ( Cerdocyon thous), and ocelot ( Leopardus pardalis) in the Brazilian Pantanal

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          Abstract

          The occurrence of Trypanosoma spp. in wild carnivore populations has been intensively investigated during the last decades. However, the impact of these parasites on the health of free-living infected animals has been largely neglected. The Pantanal biome is the world’s largest seasonal wetland, harboring a great diversity of species and habitats. This includes 174 species of mammals, of which 20 belong to the order Carnivora. The present study aimed to investigate the effect of Trypanosoma evansi and Trypanosoma cruzi infections and coinfections on the health of the most abundant carnivores in the Pantanal: coati ( Nasua nasua), crab-eating fox ( Cerdocyon thous), and ocelot ( Leopardus pardalis). We captured 39 coatis, 48 crab-eating foxes, and 19 ocelots. Diagnostic tests showed T. cruzi infection in 7 crab-eating foxes and 5 coatis. Additionally, 7 crab-eating foxes, 10 coatis, and 12 ocelots were positive for T. evansi. We observed coinfections in 9 crab-eating foxes, 8 coatis, and 2 ocelots. This is the first report of T. evansi and T. cruzi infection on the health of free-living ocelots and crab-eating foxes. We showed that single T. evansi or T. cruzi infection, as well as coinfection, caused some degree of anemia in all animals, as well as an indirect negative effect on body condition in coatis and crab-eating foxes via anemia indicators and immune investment, respectively. Furthermore, the vigorous immune investment observed in sampled coatis, crab-eating foxes and ocelots infected by T. evansi, T. cruzi and coinfected can be highly harmful to their health. Overall, our results indicate that single and combined infection with T. evansi and T. cruzi represent a severe risk to the health of wild carnivores in the Pantanal region.

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          Most cited references63

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          Synergism of nutrition, infection, and immunity: an overview

          Infections, no matter how mild, have adverse effects on nutritional status. The significance of these effects depends on the previous nutritional status of the individual, the nature and duration of the infection, and the diet during the recovery period. Conversely, almost any nutrient deficiency, if sufficiently severe, will impair resistance to infection. Iron deficiency and protein-energy malnutrition, both highly prevalent, have the greatest public health importance in this regard. Remarkable advances in immunology of recent decades have increased insights into the mechanisms responsible for the effects of infection. These include impaired antibody formation; loss of delayed cutaneous hypersensitivity; reduced immunoglobulin concentrations; decreased thymic and splenic lymphocytes; reduced complement formation, secretory immunoglobulin A, and interferon; and lower T cells and T cells subsets (helper, suppressor-cytotoxic, and natural killer cells) and interleukin 2 receptors. The effects observed with single or multiple nutrient deficiencies are due to some combination of these responses. In general, cell-mediated and nonspecific immunity are more sensitive than humoral immunity.
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            The haematocrit centrifuge technique for the diagnosis of African trypanosomiasis.

            P Woo (1969)
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              The role of parasite persistence in pathogenesis of Chagas heart disease.

              Chagas disease (CD) is caused by the infection with the protozoan haemoflagellate Trypanosoma cruzi. This disease is still a great menace to public health, and is largely neglected as it affects mostly the poorest populations of Latin America. Nonetheless, there are neither effective diagnostic markers nor therapeutic options to accurately detect and efficiently cure this chronic infection. In spite of the great advances in the knowledge of the biology of natural transmission, as well as the immunobiology of the host-parasite interaction, the understanding of the pathogenesis of CD remains largely elusive. In the recent decades, a controversy in the research community has developed about the relevance of parasite persistence or autoimmune phenomena in the development of chronic cardiac pathology. One of the most notable aspects of chronic CD is the progressive deterioration of cardiac function, derived mostly from structural derangement, as a consequence of the intense inflammatory process. Here we review the evidence supporting the multifactorial nature of Chagas heart disease comprising pathogen persistence and altered host immunoregulatory mechanisms.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draft
                Role: InvestigationRole: Methodology
                Role: Data curationRole: InvestigationRole: Methodology
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: Methodology
                Role: InvestigationRole: Methodology
                Role: InvestigationRole: Methodology
                Role: InvestigationRole: Methodology
                Role: InvestigationRole: Methodology
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                15 August 2018
                2018
                : 13
                : 8
                : e0201357
                Affiliations
                [1 ] Programa de Pós-Graduação em Ciências Ambientais e Sustentabilidade Agropecuária, Universidade Católica Dom Bosco, Campo Grande, Mato Grosso do Sul, Brazil
                [2 ] Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal de Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil
                [3 ] Laboratório de Vida Selvagem, Centro de Pesquisa Agropecuária do Pantanal, Empresa Brasileira de Pesquisa Agropecuária, Corumbá, Mato Grosso do Sul, Brazil
                [4 ] Universidade Estadual Paulista, Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal, São Paulo, Brazil
                [5 ] Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Rio de Janeiro, Brazil
                Universidade Federal de Minas Gerais, BRAZIL
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2032-8129
                http://orcid.org/0000-0002-8300-4191
                Article
                PONE-D-18-16029
                10.1371/journal.pone.0201357
                6093643
                30110344
                7fd1ab50-a3c8-422a-b510-b27c894e8a4d
                © 2018 Martins Santos 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.

                History
                : 28 May 2018
                : 14 July 2018
                Page count
                Figures: 0, Tables: 4, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100005672, Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul;
                Award ID: 006/2015
                Award Recipient :
                The study was funded by Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (FUNDECT; grant PRONEX 006/2015) to GMM and FMS, and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) to the first author, FMS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Trypanosoma
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Trypanosoma
                Trypanosoma Cruzi
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Cats
                Ocelots
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Foxes
                Medicine and Health Sciences
                Hematology
                Anemia
                Medicine and Health Sciences
                Parasitic Diseases
                Medicine and Health Sciences
                Infectious Diseases
                Co-Infections
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Blood Cells
                White Blood Cells
                Lymphocytes
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Immune Cells
                White Blood Cells
                Lymphocytes
                Biology and Life Sciences
                Immunology
                Immune Cells
                White Blood Cells
                Lymphocytes
                Medicine and Health Sciences
                Immunology
                Immune Cells
                White Blood Cells
                Lymphocytes
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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