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      Potential linkage between Toxoplasma gondii infection and physical education scores of college students

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          Abstract

          Objective

          Toxoplasma gondii is a worldwide protozoan parasite that could infect virtually all warm-blooded animals, including humans. Our study aimed to investigate the prevalence of T. gondii infection in college students at Anhui province, China and to assess risk factors for T. gondii infection in college students. Moreover, growing studies demonstrated the association between T. gondii infection and host behavioral changes. We also studied the linkage between T. gondii and physical education (PE) scores of college students.

          Methods

          A total of 2704 serum samples of medical school students attending physical education lessons were collected from September 2017 to September 2019 and evaluated for T. gondii IgG antibodies using an enzyme-linked immunosorbent assay (ELISA). Questionnaires and statistical analysis were used to determine the risk factors for T. gondii infection. We also analysed PE scores of T. gondii -infected students and T. gondii-uninfected students.

          Results

          The overall seroprevalence of T. gondii was 11.5%. The main risk factors related to T. gondii infection in college students were cat in the household and gardening or agriculture activity. Furthermore, in the basketball group and the soccer group, scores of T. gondii seropositive students were significantly higher than those of seronegative students, while in other sports there was no difference between scores of T. gondii-infected students and T. gondii uninfected students.

          Conclusion

          This is the first report of T. gondii seroprevalence in college students in Anhui province, China.

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          Most cited references18

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          The Neurotropic Parasite Toxoplasma Gondii Increases Dopamine Metabolism

          The highly prevalent parasite Toxoplasma gondii manipulates its host's behavior. In infected rodents, the behavioral changes increase the likelihood that the parasite will be transmitted back to its definitive cat host, an essential step in completion of the parasite's life cycle. The mechanism(s) responsible for behavioral changes in the host is unknown but two lines of published evidence suggest that the parasite alters neurotransmitter signal transduction: the disruption of the parasite-induced behavioral changes with medications used to treat psychiatric disease (specifically dopamine antagonists) and identification of a tyrosine hydroxylase encoded in the parasite genome. In this study, infection of mammalian dopaminergic cells with T. gondii enhanced the levels of K+-induced release of dopamine several-fold, with a direct correlation between the number of infected cells and the quantity of dopamine released. Immunostaining brain sections of infected mice with dopamine antibody showed intense staining of encysted parasites. Based on these analyses, T. gondii orchestrates a significant increase in dopamine metabolism in neural cells. Tyrosine hydroxylase, the rate-limiting enzyme for dopamine synthesis, was also found in intracellular tissue cysts in brain tissue with antibodies specific for the parasite-encoded tyrosine hydroxylase. These observations provide a mechanism for parasite-induced behavioral changes. The observed effects on dopamine metabolism could also be relevant in interpreting reports of psychobehavioral changes in toxoplasmosis-infected humans.
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            Fatal attraction in rats infected with Toxoplasma gondii.

            We tested the hypothesis that the parasite Toxoplasma gondii manipulates the behaviour of its intermediate rat host in order to increase its chance of being predated by cats, its feline definitive host, thereby ensuring the completion of its life cycle. Here we report that, although rats have evolved anti-predator avoidance of areas with signs of cat presence, T. gondii's manipulation appears to alter the rat's perception of cat predation risk, in some cases turning their innate aversion into an imprudent attraction. The selectivity of such behavioural changes suggests that this ubiquitous parasite subtly alters the brain of its intermediate host to enhance predation rate whilst leaving other behavioural categories and general health intact. This is in contrast to the gross impediments frequently characteristic of many other host parasite systems. We discuss our results in terms of their potential implications both for the epidemiology of toxoplasmosis and the neurological basis of anxiety and cognitive processes in humans and other mammals.
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              Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors.

              The protozoan parasite Toxoplasma gondii blocks the innate aversion of rats for cat urine, instead producing an attraction to the pheromone; this may increase the likelihood of a cat predating a rat. This is thought to reflect adaptive, behavioral manipulation by Toxoplasma in that the parasite, although capable of infecting rats, reproduces sexually only in the gut of the cat. The "behavioral manipulation" hypothesis postulates that a parasite will specifically manipulate host behaviors essential for enhancing its own transmission. However, the neural circuits implicated in innate fear, anxiety, and learned fear all overlap considerably, raising the possibility that Toxoplasma may disrupt all of these nonspecifically. We investigated these conflicting predictions. In mice and rats, latent Toxoplasma infection converted the aversion to feline odors into attraction. Such loss of fear is remarkably specific, because infection did not diminish learned fear, anxiety-like behavior, olfaction, or nonaversive learning. These effects are associated with a tendency for parasite cysts to be more abundant in amygdalar structures than those found in other regions of the brain. By closely examining other types of behavioral patterns that were predicted to be altered we show that the behavioral effect of chronic Toxoplasma infection is highly specific. Overall, this study provides a strong argument in support of the behavioral manipulation hypothesis. Proximate mechanisms of such behavioral manipulations remain unknown, although a subtle tropism on part of the parasite remains a potent possibility.
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                Author and article information

                Contributors
                Role: Formal analysisRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – original draft
                Role: InvestigationRole: Methodology
                Role: ConceptualizationRole: Data curationRole: Methodology
                Role: InvestigationRole: MethodologyRole: Supervision
                Role: ConceptualizationRole: MethodologyRole: Supervision
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                3 March 2021
                2021
                : 16
                : 3
                : e0241653
                Affiliations
                [1 ] Department of Physical Education of Anhui University of Chinese Medicine, Hefei, Anhui, P. R China
                [2 ] Department of Physical Education, College of Humanistic Medicine, Anhui Medical University, Hefei, Anhui, P. R China
                [3 ] Anhui Provincial Institute of Parasitic Diseases, Hefei, Anhui, P. R China
                [4 ] Department of Human Parasitology, Anhui Medical University, Hefei, Anhui, P. R China
                [5 ] Food Science and Engineering College of Inner Mongolia Agricultural University, Hohhot, China
                [6 ] College of Life Sciences, Anhui Medical University, Hefei, Anhui, P. R China
                University of Edinburgh Roslin Institute, UNITED KINGDOM
                Author notes

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

                Author information
                https://orcid.org/0000-0002-6317-6703
                Article
                PONE-D-20-32488
                10.1371/journal.pone.0241653
                7928503
                33657102
                4cc8ec24-aa42-4e7c-9877-f17699141da4
                © 2021 Cai 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
                : 15 October 2020
                : 16 February 2021
                Page count
                Figures: 1, Tables: 2, Pages: 8
                Funding
                Funded by: Research on the humanities and social sciences of Anhui Province
                Award ID: SK2017A0163
                Award Recipient :
                Funded by: Anhui high education quality elevation project
                Award ID: 2017jyxm0143
                Funded by: Research Foundation for Universities at Anhui
                Award ID: KJ2019A0264
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31701162
                Award Recipient :
                Funded by: Program of Inner Mongolia Natural Science Foundation of China
                Award ID: 2018BS03015
                Our study is financially supported by Research on the humanities and social sciences of Anhui Province (Grant #: SK2017A0163), Anhui high education quality elevation project (Grant #: 2017jyxm0143), Research Foundation for Universities at Anhui (Grant #: KJ2019A0264) and National Natural Science Foundation of China (Grant #: 31701162), and Program of Inner Mongolia Natural Science Foundation of China (No. 2018BS03015). 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
                Toxoplasma
                Toxoplasma Gondii
                Biology and Life Sciences
                Psychology
                Behavior
                Recreation
                Sports
                Social Sciences
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                Medicine and Health Sciences
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                Parasitic Diseases
                Protozoan Infections
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                Enzyme-Linked Immunoassays
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