Risk factors for sporadic toxoplasmosis: A systematic review and meta-analysis
Introduction
Toxoplasma gondii, an obligate protozoan parasite of the Apicomplexa phylum, is a worldwide parasite that can infect humans and a large range of warm-blooded vertebrates. Three major clonal lineages (type I to III) differ in pathogenicity and prevalence around the world, with genotype II dominating in congenital toxoplasmosis cases in Europe and the USA (Hosseini et al., 2019). The disease is generally benign, but some severe or life-threatening effects can occur in children (Dunn et al., 1999), when the transmission is congenital, and in immunocompromised patients (Robert-Gangneux and Darde, 2012). Since the conventional designation assumed this clonal population structure, other genotypes have been identified worldwide and termed as “atypical” or “exotic” (Dardé et al., 2014). Among these, highly virulent strains circulating mainly in South America have been responsible for severe cases in immunocompetent people (Carme et al., 2009). Approximately 30% of the human population is considered infected (Montoya and Liesenfeld, 2004). Serological tests are usually used to detect the infection, with detection of anti-T gondii specific IgG and/or IgM antibodies (Montoya, 2002). T. gondii is globally distributed and results in a high public health impact. The Global Disease Burden 2015 Study estimated that foodborne toxoplasmosis was responsible for 10.3 million (95% UI 7.40–14.9 million) cases in 2010, and 825,000 DALYs (95% UI 561,000–1.26 million) DALYs (Torgerson et al., 2015).
The parasitic cycle of toxoplasmosis is complex. During its primary infection, the cat (or other felines), the definitive host, excretes parasites (oocyst form) in its stool. Excretion in cats is limited in time (about two to three weeks) until immunity is established. Oocysts can contaminate the environment: the soil, water, and therefore shellfish that filter water and plant products directly or via irrigation water. Excreted oocysts are not infectious and become infective after sporulation, after few days in the environment depending on climate conditions, and become infectious with long resistance in environmental conditions (oocysts can survive for long periods, up to years, in a favorable environment). The remarkable resistance of the oocyst wall enables the dissemination of T. gondii through watersheds and ecosystems, and long-term persistence in diverse foods such as shellfish and fresh produce (Shapiro et al., 2019). Humans and all warm-blooded mammals are infected through the environment or food. Parasites encyst in all tissues, especially striated muscles and the brain. These cysts persist throughout life and can be a source of contamination of new hosts through meat ingestion (carnivorism) (Tenter et al., 2000).
T. gondii exposure to humans may have multiple origins, and the prevalence is high (and protective for pregnant women). So, numerous epidemiological studies investigate the main transmission pathways of sporadic T. gondii infection by serological studies. A systematic review of outbreaks was recently published (Meireles et al., 2015), still a systematic review and a meta-analysis of case-control, cohort, and cross-sectional studies have to be performed to determine the main risk factors associated with sporadic T. gondii infection. Characterization of risk factors of T. gondii could contribute to identify recommendations for susceptible populations such as pregnant women or immunocompromised patients. The objective of this meta-analysis is to summarize the evidence on risk factors for sporadic T. gondii infection regardless of the country of origin from relevant scientific information contained in epidemiological case-control/cohort/cross-sectional studies.
Section snippets
Material and methods
The protocol of the systematic review and the meta-analysis model are described in depth in the methodological paper of this issue (Gonzales–Barron et al., 2019).
Descriptive statistics
The quality assessment stage was passed by 213 primary studies investigating risk factors for sporadic infection with T. gondii, which were conducted between 1983 and 2016 (80.5% after 2000). Excluding susceptible populations other than pregnant women, and some risk factors (see above), 187 publications were retained for meta-analysis (Fig. 1 and Appendix 1). Primary studies investigated risk factors in different types of population, namely children (16 studies), mixed population (98 studies),
Discussion
The measurement of seroprevalence is an indicator of T. gondii infection, but it does not provide information on the time of infection. Besides, there may be a significant lapse of time between contamination and the collection of information on the exposures of infected persons (most often identified by serological research of IgG) during studies. Consequently, the results are conditioned on the absence of any change in the respondents' exposures over time. Cases could have been identified
Conclusion
The risk factors identified in this meta-analysis could complement those already established in future sporadic case-control studies quantifying the attributable risk fraction: mollusks (regarding the species), raw milk (goat/cows), vegetables (including the type of vegetable and the preparation i.e., washing), game meat and drinking water. Furthermore, the development of sensitive methods for the detection and isolation of T. gondii in these matrices is needed to confirm the causal association
CRediT authorship contribution statement
Anne Thebault: Methodology, Formal analysis, Writing - original draft, Writing - review & editing. Pauline Kooh: Methodology, Project administration, Writing - original draft, Writing - review & editing. Vasco Cadavez: Methodology, Investigation, Formal analysis. Ursula Gonzales-Barron: Methodology, Investigation, Formal analysis, Writing - review & editing. Isabelle Villena: Supervision, Writing - original draft, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
The authors would like to thank ANSES staff and the members of the ANSES Working Group on Source Attribution of Foodborne Diseases: Moez Sanaa, Laurence Watier, Jean Christophe Augustin, Frédéric Carlin, Julie David, Philippe Fravalo, Laurent Guillier, Nathalie Jourdan-Da Silva, Alexandre Leclercq, Lapo Mughini-Gras, Nicole Pavio. U. Gonzales-Barron and V. Cadavez are grateful to the Foundation for Science and Technology (FCT, Portugal) and FEDER under Programme PT2020 for the financial support
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