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      Seropositivity and Risk Factors Associated with Toxoplasma gondii Infection in Wild Birds from Spain

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          Abstract

          Toxoplasma gondii is a zoonotic intracellular protozoan parasite of worldwide distribution that infects many species of warm-blooded animals, including birds. To date, there is scant information about the seropositivity of T. gondii and the risk factors associated with T. gondii infection in wild bird populations. In the present study, T. gondii infection was evaluated on sera obtained from 1079 wild birds belonging to 56 species (including Falconiformes (n = 610), Strigiformes (n = 260), Ciconiiformes (n = 156), Gruiformes (n = 21), and other orders (n = 32), from different areas of Spain. Antibodies to T. gondii (modified agglutination test, MAT titer ≥1∶25) were found in 282 (26.1%, IC 95%:23.5–28.7) of the 1079 birds. This study constitute the first extensive survey in wild birds species in Spain and reports for the first time T. gondii antibodies in the griffon vulture ( Gyps fulvus), short-toed snake-eagle ( Circaetus gallicus), Bonelli's eagle ( Aquila fasciata), golden eagle ( Aquila chrysaetos), bearded vulture ( Gypaetus barbatus), osprey ( Pandion haliaetus), Montagu's harrier ( Circus pygargus), Western marsh-harrier ( Circus aeruginosus), peregrine falcon ( Falco peregrinus), long-eared owl ( Asio otus), common scops owl ( Otus scops), Eurasian spoonbill ( Platalea leucorodia), white stork ( Ciconia ciconia), grey heron ( Ardea cinerea), common moorhen ( Gallinula chloropus); in the International Union for Conservation of Nature (IUCN) “vulnerable” Spanish imperial eagle ( Aquila adalberti), lesser kestrel ( Falco naumanni) and great bustard ( Otis tarda); and in the IUCN “near threatened” red kite ( Milvus milvus). The highest seropositivity by species was observed in the Eurasian eagle owl ( Bubo bubo) (68.1%, 98 of 144). The main risk factors associated with T. gondii seropositivity in wild birds were age and diet, with the highest exposure in older animals and in carnivorous wild birds. The results showed that T. gondii infection is widespread and can be at a high level in many wild birds in Spain, most likely related to their feeding behaviour.

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          Most cited references36

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          Waterborne toxoplasmosis--recent developments.

          Humans become infected with Toxoplasma gondii mainly by ingesting uncooked meat containing viable tissue cysts or by ingesting food or water contaminated with oocysts from the feces of infected cats. Circumstantial evidence suggests that oocyst-induced infections in humans are clinically more severe than tissue cyst-acquired infections. Until recently, waterborne transmission of T. gondii was considered uncommon, but a large human outbreak linked to contamination of a municipal water reservoir in Canada by wild felids and the widespread infection of marine mammals in the USA provided reasons to question this view. The present paper examines the possible importance of T. gondii transmission by water. Published by Elsevier Inc.
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            Toxoplasma gondii and Neospora caninum in sparrows (Passer domesticus) in the Northeast of Brazil.

            Toxoplasma gondii is a cosmopolitan protozoan parasite of warm-blooded animals that causes high rates of infection in mammals and birds. Sparrows (Passer domesticus) are synantropic birds which are distributed worldwide. They serve as intermediate hosts for the parasite but are quite resistant to toxoplasmosis. The aims of this study were to determine the frequency of T. gondii infection in sparrows using serologic and molecular tests, and to investigate related parasites, such as Neospora caninum and Hammondia sp., using a nested PCR for Toxoplasmatinae DNA followed by sequence analysis of the PCR amplicons. A total of 293 sparrows were trapped at the states of Bahia and Pernambuco, Brazil. Tissues of 40 animals were available for molecular tests. Antibodies to T. gondii were found in 1.02% (3/293) of animals using a hemagglutination test, with titers ranging from 1:32 to 1:128. Toxoplasmatinae DNA was detected in 10/40 (25%) sparrows; after nucleotide sequencing, T. gondii was confirmed in 7/40 (17.5%) birds and N. caninum in 3/40 (7.5%) animals. Sparrows from Brazil were confirmed as intermediate hosts of T. gondii, that reinforces the potential importance of these birds on the transmission of the parasite to cats and other animals that may predate sparrows. In addition, N. caninum was detected for the first time in sparrows. To the authors' knowledge, this is the first wild synantropic bird species identified as intermediate host of N. caninum. These findings seem to have a great epidemiologic impact because of the cosmopolitan distribution of sparrows and due to their increasing population in urban and rural areas.
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              Prevalence of Toxoplasma gondii antibodies in red deer (Cervus elaphus) and other wild ruminants from Spain.

              Serum samples from 441 red deer (Cervus elaphus) and 161 other wild ruminant species, collected between 1993 and 2005 from six regions of Spain were tested for antibodies against Toxoplasma gondii by the modified agglutination test (MAT). Antibodies to T. gondii (MAT 1:25 or higher) were detected in 15.6% of red deer. Statistically significant differences were observed among sampling sites with seroprevalence in red deer from Catalonia (42.2%) being significantly higher compared with other Spanish regions (8.7%) (P < 0.05). Statistically significant differences were not observed between T. gondii seroprevalence and sex, age or management of hunting estates (open versus fenced). Seroprevalence of T.gondii infection in other ruminants species was 24% of 79 fallow deer (Dama dama), 21.8% of 33 in roe deer (Capreolus capreolus), 33.3% of three Spanish ibex (Capra pyrenaica), 20% of 10 chamois (Rupicapra pyrenaica), 10% of 10 barbary sheep (Ammotragus lervia), and 14.8% of 27 mouflon (Ovis ammon) in areas not including Catalonia, where no samples from these species were available. Serological results indicated a widespread exposure to T. gondii among wildlife in Spain and suggest that consumption of raw or inadequately cooked meat, as well as handling carcasses of wild game, should be taken into account as a source of infection for humans.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                22 December 2011
                : 6
                : 12
                : e29549
                Affiliations
                [1 ]Servei d'Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Facultat de Veterinaria, Universitat Autònoma de Barcelona, Bellaterra, Spain
                [2 ]Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Córdoba, Córdoba, Spain
                [3 ]Centre de Fauna Salvatge de Torreferrussa, Direcció General del Medi Natural i de la Biodiversitat-Forestal Catalana, Generalitat de Catalunya, Santa Perpètua de la Mogoda, Barcelona, Spain
                [4 ]Centro de Estudios de Rapaces Ibéricas, Sevilleja de la Jara, Castilla-la-Mancha, Spain
                [5 ]Instituto de Investigación en Recursos Cinegéticos (IREC) (Centro Superior de Investigaciones Científicas-Universidad de Castilla-La Mancha-Junta de Castilla-La Mancha), Ciudad Real, Spain
                [6 ]Bearded Vulture Study and Protection Group, El Pont de Suert, Lleida, Spain
                [7 ]Division of Conservation Biology, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
                [8 ]Centre de Recerca en Sanitat Animal (CReSA), Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain
                [9 ]Departament de Sanitat i d'Anatomia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, Bellaterra, Spain
                [10 ]Clínica Veterinaria Oftalmológica (OCUVET), Torrelodones, Madrid, Spain
                [11 ]Animal Parasitic Diseases Laboratory, Animal and Natural Resources Institute, Agriculture Research Service, United States Department of Agriculture, Beltsville, Maryland, United States of America
                Charité, Campus Benjamin Franklin, Germany
                Author notes

                Conceived and designed the experiments: OC SA IGB. Performed the experiments: OC LD IE. Analyzed the data: IGB. Contributed reagents/materials/analysis tools: RML IM JMB UH AM EBR EO MH SL JPD. Wrote the paper: OC SA IGB AM.

                Article
                PONE-D-11-20821
                10.1371/journal.pone.0029549
                3245288
                22216311
                6e5832a2-2e76-47cf-9381-4f0dd2b88f1e
                Cabezón 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
                : 14 October 2011
                : 30 November 2011
                Page count
                Pages: 7
                Categories
                Research Article
                Biology
                Microbiology
                Protozoology
                Parastic Protozoans
                Toxoplasma Gondii
                Zoology
                Ornithology
                Medicine
                Infectious Diseases
                Neglected Tropical Diseases
                Toxoplasmosis
                Parasitic Diseases
                Toxoplasmosis
                Veterinary Science
                Animal Types
                Wildlife
                Veterinary Diseases
                Zoonotic Diseases
                Foodborne Diseases
                Veterinary Parasitology
                Veterinary Epidemiology

                Uncategorized
                Uncategorized

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