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      Environmental transmission of Toxoplasma gondii: Oocysts in water, soil and food

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          Abstract

          Toxoplasma gondii is a zoonotic protozoan parasite that can cause morbidity and mortality in humans, domestic animals, and terrestrial and aquatic wildlife. The environmentally robust oocyst stage of T. gondii is fundamentally critical to the parasite's success, both in terms of its worldwide distribution as well as the extensive range of infected intermediate hosts. Despite the limited definitive host species (domestic and wild felids), infections have been reported on every continent, and in terrestrial as well as aquatic environments. The remarkable resistance of the oocyst wall enables dissemination of T. gondii through watersheds and ecosystems, and long-term persistence in diverse foods such as shellfish and fresh produce. Here, we review the key attributes of oocyst biophysical properties that confer their ability to disseminate and survive in the environment, as well as the epidemiological dynamics of oocyst sources including domestic and wild felids. This manuscript further provides a comprehensive review of the pathways by which T. gondii oocysts can infect animals and people through the environment, including in contaminated foods, water or soil. We conclude by identifying critical control points for reducing risk of exposure to oocysts as well as opportunities for future synergies and new directions for research aimed at reducing the burden of oocyst-borne toxoplasmosis in humans, domestic animals, and wildlife.

          Highlights

          • Oocyst ingestion constitutes a significant proportion of T. gondii infections.

          • Oocyst attributes facilitate T. gondii transmission in terrestrial and aquatic habitats.

          • Oocysts are persistent and prevalent in water, soil and foods.

          • Mitigating oocyst-borne infections requires transdisciplinary international efforts.

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          Most cited references166

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          Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis.

          Toxoplasma gondii's importance for humans refers mainly to primary infection during pregnancy, resulting in abortion/stillbirth or congenital toxoplasmosis. The authors sought to evaluate the current global status of T. gondii seroprevalence and its correlations with risk factors, environmental and socioeconomic parameters. Literature published during the last decade on toxoplasmosis seroprevalence, in women who were pregnant or of childbearing age, was retrieved. A total of 99 studies were eligible; a further 36 studies offered seroprevalence data from regions/countries for which no data on pregnancy/childbearing age were available. Foci of high prevalence exist in Latin America, parts of Eastern/Central Europe, the Middle East, parts of south-east Asia and Africa. Regional seroprevalence variations relate to individual subpopulations' religious and socioeconomic practices. A trend towards lower seroprevalence is observed in many European countries and the United States of America (USA). There is no obvious climate-related gradient, excluding North and Latin America. Immigration has affected local prevalence in certain countries. We further sought to recognise specific risk factors related to seropositivity; however, such risk factors are not reported systematically. Population awareness may affect recognition of said risks. Global toxoplasmosis seroprevalence is continuingly evolving, subject to regional socioeconomic parameters and population habits. Awareness of these seroprevalence trends, particularly in the case of women of childbearing age, may allow proper public health policies to be enforced, targeting in particular seronegative women of childbearing age in high seroprevalence areas.
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            History of the discovery of the life cycle of Toxoplasma gondii.

            J Dubey (2009)
            It has been 100 years since the discovery of Toxoplasma gondii in 1908. Its full life cycle was not discovered until 1970 when it was found that it is a coccidian parasite of cats with all non-feline warm blooded animals (including humans) as intermediate hosts. The discovery of the environmentally resistant stage of the parasite, the oocyst, made it possible to explain its worldwide prevalence. In the present paper, events associated with the discovery of its life cycle are recalled.
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              Toxoplasmosis - a waterborne zoonosis.

              J Dubey (2004)
              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, water-borne 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 by marine mammals in the USA provide reasons to question this view. The present paper reviews information on the biology of oocyst-induced infections of T. gondii in humans and animals and examines possible importance of transmission by water.
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                Author and article information

                Contributors
                Journal
                Food Waterborne Parasitol
                Food Waterborne Parasitol
                Food and Waterborne Parasitology
                Elsevier
                2405-6766
                01 April 2019
                June 2019
                01 April 2019
                : 15
                : e00049
                Affiliations
                [a ]Department of Pathology, Microbiology & Immunology, School of Veterinary Medicine, One Shields Ave, 4206 VM3A, University of California, Davis, CA 95616-5270, USA
                [b ]Laboratory of Immunoparasitology, Federal University of Rio de Janeiro, Macaé, RJ, Brazil
                [c ]Bureau of Microbial Hazards, Food Directorate, Health Canada, 251 Sir Frederick Banting Driveway, A.L. 2204E, Ottawa, ON K1A 0K9, Canada
                [d ]Aix Marseille Univ, IRD 257, AP-HM, SSA, VITROME, IHU-Méditerranée Infection, Marseille, France
                [e ]Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 130 McAllister Way, Santa Cruz, CA 95050, USA
                [f ]School of Veterinary Medicine and Biomedical Sciences, School of Natural Resources, University of Nebraska-Lincoln, VBS 111, Lincoln, NE 68583, USA
                [g ]EA 7510, UFR Medicine, University Reims Champagne-Ardenne, National Reference Center on Toxoplasmosis, Hospital Maison Blanche, Reims, France
                Author notes
                [* ]Corresponding author. kshapiro@ 123456ucdavis.edu
                Article
                S2405-6766(18)30042-8 e00049
                10.1016/j.fawpar.2019.e00049
                7033973
                32095620
                9c92b67e-ed1f-43a0-a672-83b4a6f994c6
                © 2019 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 20 December 2018
                : 19 March 2019
                : 19 March 2019
                Categories
                Article

                toxoplasma gondii,oocyst,transmission,water,soil,food
                toxoplasma gondii, oocyst, transmission, water, soil, food

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