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. 2026 Jul 22;73(6):481–501. doi: 10.1111/zph.70080

Worldwide Seroprevalence and Risk Factors of Toxoplasma gondii Exposure Among Students: A Systematic Review and Meta‐Analysis

Sara Lesani 1, Mohammad Javad Boozhmehrani 2,3,✉
PMCID: PMC13535722  PMID: 42487234

ABSTRACT

Background

Toxoplasma gondii, a zoonotic protozoan parasite, affects approximately one‐third of the global population and is associated with congenital and neurological complications. While seroprevalence has been extensively studied in high‐risk groups such as pregnant women, data on students, a population spanning childhood to young adulthood, are fragmented. We aimed to systematically assess the global seroprevalence and risk factors of T. gondii exposure among students to inform public health strategies for this demographic.

Methods

We conducted a systematic review and meta‐analysis following PRISMA guidelines, with the protocol submitted to PROSPERO (CRD42025637197). We searched PubMed, Scopus and Web of Science from database inception to January 2025 for cross‐sectional and observational studies reporting T. gondii seroprevalence in students (primary, secondary, undergraduate or postgraduate) using serological methods, with no language restrictions. Random‐effects models were used to estimate pooled seroprevalence and risk factors, with heterogeneity assessed via I2 statistics and meta‐regression. Bias was evaluated using Begg's and Egger's tests.

Results

From 50 studies involving 32,054 students across 24 countries, the pooled global seroprevalence of T. gondii was 14.0% (95% CI 11.7–16.6; I 2 = 98.33%). Seroprevalence varied by educational level: 28.5% (95% CI 20.6–37.7) in primary school students, 19.3% (95% CI 14.1–25.8) in secondary school students, 19.4% (95% CI 14.5–25.5) in undergraduates and 2.5% (95% CI 0.2–27.8) in postgraduates (based on one study). Significant risk factors included contact with cats (RR 1.888, p < 0.001), soil exposure (RR 1.940, p < 0.001) and consumption of undercooked meat (RR 1.450, p = 0.003). Meta‐regression identified diagnostic methods and geographic coordinates as key sources of heterogeneity (explaining 35%–73%). High between‐study heterogeneity was observed across most analyses.

Conclusions

Health education programs in schools, promoting hand hygiene, safe food practices and responsible pet care, could reduce T. gondii exposure among students, particularly in high‐prevalence regions. Further research is needed to explore the cognitive and behavioural impacts of infection in this population and to better characterize regional sources of heterogeneity.

Keywords: adolescents, children, health education, toxoplasmosis, zoonotic disease

Impacts

  • This study provides the first global summary of Toxoplasma gondii exposure among students, combining data from more than 32,000 participants across 24 countries.

  • Around one in seven students showed evidence of previous infection. Contact with cats, exposure to soil and consumption of undercooked meat were identified as important and potentially preventable risk factors.

  • The findings support school‐based health education promoting hand hygiene, safe food handling and responsible pet care, while helping public health authorities target prevention efforts and guide future research in regions with higher infection rates.

1. Introduction

Toxoplasma gondii is an obligate intracellular protozoan parasite responsible for toxoplasmosis, a globally prevalent zoonotic infection that affects nearly one‐third of the world's population (Wang et al. 2016). The parasite infects virtually all warm‐blooded animals, including humans and is considered one of the most widespread eukaryotic pathogens due to its broad host range, multiple transmission routes and global distribution. Humans typically acquire infection through ingestion of tissue cysts in undercooked or raw meat, consumption of food or water contaminated with sporulated oocysts shed by cats, or via congenital transmission from mother to fetus (Smith et al. 2021).

Although most infections in immunocompetent individuals are asymptomatic or mild, T. gondii can cause severe disease in immunocompromised patients (e.g., transplant recipients, individuals with cancer or AIDS) and in congenitally infected infants. Complications include neurological disorders, ocular toxoplasmosis, hydrocephalus and mental retardation, with congenital toxoplasmosis being a major cause of visual and neurological impairment worldwide. In addition, recent studies suggest associations between latent toxoplasmosis and behavioural alterations such as increased aggression, impulsivity and even mental illness in humans (Dubey et al. 1998; Tyebji et al. 2019).

Toxoplasmosis has been extensively studied in high‐risk groups such as pregnant women and immunocompromised patients, with congenital toxoplasmosis alone accounting for an estimated 190,100 cases and 1.20 million disability‐adjusted life years (DALYs) globally each year (Torgerson and Mastroiacovo 2013); however, limited attention has been given to its prevalence among students, including primary schoolchildren, adolescents and university students. This demographic represents a substantial proportion of the global population and is particularly relevant due to behavioural risk factors such as consumption of fast food, close contact with pets and often limited health awareness. Moreover, the impact of T. gondii infection during adolescence or early adulthood, which are critical periods for cognitive and psychological development, raises additional public health concerns (Rodrigues et al. 2015).

The global variation in T. gondii seroprevalence among student populations is striking, with reported rates ranging from less than 2% to over 60%, depending on geographic location, lifestyle, climate, socioeconomic status and diagnostic methods (Kouakou et al. 2024; Souza et al. 1987; Yang et al. 2017). Such variability underscores the importance of synthesizing existing data to gain a clearer picture of the global burden of toxoplasmosis among students.

In light of these considerations, understanding the epidemiology of T. gondii infection in student populations is essential for informing targeted prevention strategies, health education and future research. Therefore, this study conducted a comprehensive systematic review and meta‐analysis to synthesize the available evidence and quantify the global seroprevalence and associated risk factors of T. gondii exposure among students worldwide.

2. Methods

2.1. Protocol and Registration

This systematic review and meta‐analysis adhered to the guidelines outlined in the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses (PRISMA) framework (Kouakou et al. 2024). The study protocol was submitted to PROSPERO (Registration number: CRD42025637197) prior to conducting the review.

2.2. Search Strategy

A systematic and comprehensive literature search was conducted across three major electronic databases: PubMed (MEDLINE), Scopus and Web of Science, covering records from database inception through January 2025. The search strategy was meticulously designed using a combination of Medical Subject Headings (MeSH) terms and free‐text keywords to ensure the retrieval of all relevant studies on Toxoplasma gondii infection, seroprevalence and student populations.

The search strategy was structured around three core concepts: (1) T. gondii infection, (2) seroprevalence and infection‐related terms and (3) student populations. For T. gondii, the following terms were used: MeSH terms included ‘Toxoplasma’[Mesh] and ‘Toxoplasmosis’[Mesh], while free‐text keywords included ‘Toxoplasm*’ and ‘T. gondii’. To capture studies related to seroprevalence and infection, the following terms were included: MeSH terms such as ‘Seroepidemiologic Studies’[Mesh], ‘Prevalence’[Mesh] and ‘Disease Transmission, Infectious’[Mesh], alongside free‐text keywords including ‘seropreval*’, ‘prevalence’, ‘seropositiv*’, ‘seronegativ*’, ‘infection rate*’, ‘infection status’, ‘epidemiol*’, ‘occurrence’ and ‘distribution’.

To identify studies focusing on student populations, the search incorporated MeSH terms like ‘Schools’[Mesh], ‘Students’[Mesh], ‘Universities’[Mesh] and ‘Education’[Mesh]. Additionally, free‐text keywords such as ‘student*’, ‘pupil*’, ‘learner*’, ‘school child*’, ‘schoolchild*’, ‘primary school*’, ‘elementary school*’, ‘secondary school*’, ‘high school*’, ‘middle school*’, ‘undergraduate*’, ‘graduate student*’, ‘postgraduate*’, ‘college student*’, ‘university student*’, ‘medical student*’, ‘nursing student*’, ‘PhD student*’, ‘doctoral student*’, ‘education* institution*’, ‘academic institution*’ and ‘higher education’ were employed.

These three concept groups were combined using Boolean operators (AND, OR) to construct the final search string, ensuring a balance between sensitivity and specificity. The search was conducted in the title and abstract fields of the records to enhance the relevance of retrieved studies. No restrictions were applied regarding language or publication date to maximize the inclusivity of the search. This rigorous and systematic approach was implemented to ensure the retrieval of all pertinent literature for this meta‐analysis. The complete database‐specific search strategies are provided in Appendix S1.

2.3. Selection Criteria

The selection criteria for this systematic review and meta‐analysis were designed to ensure the inclusion of high‐quality and relevant studies while maintaining a comprehensive and representative sample of the global seroprevalence and risk factors of T. gondii exposure among students. We included publication types that reported primary data, specifically original articles and letters to the editor, provided that sufficient data were available in the full text or abstract for extraction. Key information required for inclusion consisted of the type of serological test used, sample size, number of seropositive individuals, educational level of the students (primary school, high school, undergraduate or postgraduate) and the country or region where the study was conducted. To achieve global coverage and minimize language bias, we considered studies published in all languages. Non‐English articles were translated and interpreted using Google Translate and Claude Pro Version 3.5 to ensure accurate data extraction and comprehension.

Only studies reporting serological cases of T. gondii exposure were included, as our focus was on seroprevalence and cumulative exposure, while also ensuring methodological comparability across studies (Barendregt et al. 2013). Molecular diagnostic methods, such as PCR, were excluded to maintain consistency in the type of data analysed. For the evaluation of risk factors, we established a minimum threshold of three independent studies reporting complete data for each specific factor. This threshold was selected to ensure the statistical power and reliability of the meta‐analysis, as fewer than three studies could compromise the robustness of pooled estimates and limit the ability to assess heterogeneity across studies.

Studies were excluded if they lacked essential data, such as sample size, seropositivity rates, or details on the student population, even after attempts to contact the authors for clarification. Additionally, studies that focused exclusively on non‐student populations, utilized non‐serological diagnostic methods, or provided insufficient information on risk factors were excluded. Case reports, review articles and studies with overlapping or duplicate data identified based on article title, journal, publication year and author order were also withdrawn from the analysis to prevent redundancy and ensure the integrity of the findings.

2.4. Data Extraction

Data extraction was conducted systematically using a pre‐defined, comprehensive checklist to ensure consistency and accuracy in capturing relevant information from the included studies. The extracted data encompassed several critical parameters, organized into bibliographic, geographic, demographic, methodological and quantitative categories.

First, bibliographic details were recorded, including the author names and the year of publication, to uniquely identify each study and facilitate proper referencing. Geographic information was meticulously documented to determine the location of each study. If the study was conducted in a specific province, city, or region within a country, this information was included in parentheses following the country name to provide granularity and context. The demographic and educational characteristics of the study populations were also extracted. This included the level of education of the participants (primary school, high school, undergraduate, or postgraduate), as well as the gender distribution (male, female, or both). Study design characteristics were recorded to assess the methodological quality and robustness of the evidence. In accordance with the objectives of this meta‐analysis, which aimed to estimate pooled seroprevalence and evaluate exposure‐related risk factors, the included studies were primarily cross‐sectional and case–control studies, as these designs provided the necessary data for the analyses. Given the focus of this meta‐analysis on serological research, diagnostic methods were restricted to serological techniques, such as enzyme‐linked immunosorbent assay (ELISA), indirect fluorescent antibody test (IFAT) and other serological assays. Quantitative data extraction included the total sample size of students studied and the number of seropositive cases, which were used to calculate prevalence rates. These data were systematically organized and categorized by educational level in Table 1. Studies reporting data for multiple educational levels were included in each relevant category, ensuring comprehensive representation across all levels of education.

TABLE 1.

Characteristics of included studies on the seroprevalence of T. gondii exposure among students, stratified by educational level.

Educational level References Country (region) Gender Diagnostic method Study type Sample size (n) PC (n) P (%)
Primary school Wang et al. (2020) China (Henan) Both ELISA (IgG/IgM) Cross‐sectional 2451 233 9.51
Thái et al. (2019) Myanmar Both ELISA (IgG/IgM) Cross‐sectional 143 27 18.88
Macre et al. (2019) Brazil (São Paulo) N/A ELISA (IgG) Cross‐sectional 164 82 50.00
Xin et al. (2015) China (Shandong) Both ELISA (IgG/IgM) Cross‐sectional 6000 961 16.02
Mendy et al. (2015) United States Both EIA (IgG) Cross‐sectional 1755 135 7.69
Gyang et al. (2015) Nigeria (Lagos) Both LA Cross‐sectional 248 65 26.21
Fu et al. (2014) Marshall Islands Both LA Cross‐sectional 166 91 54.82
Mizgajska‐Wiktor et al. (2013) Poland (Poznań) Both ELISA (IgG) Cross‐sectional 115 47 40.87
Fan et al. (2012) São Tomé and Príncipe Both LA Cross‐sectional 255 161 63.14
Sharif et al. (2010) Iran (sari) Both ELISA (IgG) Cross‐sectional 196 53 27.04
Lopes et al. (2008) Brazil (Jataizinho) Both IFA Cross‐sectional 276 128 46.38
Zamani et al. (2007) Iran (Tehran) Both CLIA (IgG) Cross‐sectional 1529 152 9.94
Giraldi et al. (2002) Brazil (Paraná) Both IFA Cross‐sectional 343 184 53.64
Taylor et al. (1997) Ireland (Dublin) Both LA Cross‐sectional 921 119 12.92
Singh et al. (1994) India (Maharashtra) Both ELISA (IgG) Cross‐sectional 75 22 29.33
Souza et al. (1987) Brazil (Rio de Janeiro) Both IF (IgG/IgM) Cross‐sectional 608 416 68.42
Ziobrowski (1984) Poland (Zakopane) N/A IFAT Cross‐sectional 322 42 13.04
Total 15,567 2918
High school Sampaio et al. (2020) Brazil (São Paulo) N/A ELISA (IgG) Cross‐sectional 249 21 8.43
Thái et al. (2019) Myanmar Both ELISA (IgG/IgM) Cross‐sectional 324 83 25.62
Liassides et al. (2016) Cyprus Female ELISA (IgG/IgM) Cross‐sectional 1056 69 6.53
Gyang et al. (2015) Nigeria (Lagos) Both LA Cross‐sectional 103 18 17.48
Fallah et al. (2014) Iran (East Azarbaijan) Female ELISA (IgG/IgM) Cross‐sectional 549 84 15.30
Mizgajska‐Wiktor et al. (2013) Poland (Poznań) Both ELISA (IgG) Cross‐sectional 75 30 40.00
Çetinkaya et al. (2011) Türkiye (Kayseri) Both IFAT (IgG/IgM) Cross‐sectional 347 89 25.65
Sharif et al. (2010) Iran (sari) Both ELISA (IgG) Cross‐sectional 808 206 25.50
Fouladvand et al. (2010) Iran (Bushehr) Female ELISA (IgG/IgM) Cross‐sectional 516 114 22.09
Galván‐Ramírez et al. (2010) Mexico (Jalisco) Both IFAT (IgG/IgM) Cross‐sectional 174 36 20.69
Taylor et al. (1997) Ireland (Dublin) Both LA Cross‐sectional 259 38 14.67
Singh et al. (1994) India (Maharashtra) Both ELISA (IgG) Cross‐sectional 103 34 33.01
Sadaruddin et al. (1991) Pakistan (Islamabad) N/A ELISA (IgG) Cross‐sectional 270 47 17.41
Total 4833 869
Undergraduate Kouakou et al. (2024) Ivory Coast (Bouaké) Female ELISA (IgG/IgM) Cross‐sectional 168 114 67.86
Jimenez‐Chunga et al. (2024) Peru (Lima) Both ELISA (IgG/IgM) Cross‐sectional 100 7 7.00
Ignacio Troncoso et al. (2022) Chile (Concepción) Both CLIA (IgG) Cross‐sectional 74 16 21.62
Cai et al. (2021) China (Anhui) Both ELISA (IgG) Cross‐sectional 2704 311 11.50
Barzinij (2021) Iraq (Kirkuk) Female ELISA (IgG/IgM) Cross‐sectional 210 26 12.38
Kalantari et al. (2020) Iran (Fars) Female ELISA (IgG/IgM) Cross‐sectional 504 36 7.14
Jafari‐Modrek et al. (2019) Iran (Zahedan) Female ELISA (IgG/IgM) Cross‐sectional 80 8 10.00
Sánchez Artigas et al. (2018) Ecuador (Riobamba) Female CLIA (IgG) Cross‐sectional 105 38 36.19
Hajikolaei et al. (2018) Iran (Ahvaz) Both ELISA (IgG/IgM) Case–control 219 76 34.70
Al‐Sadoon et al. (2018) Iraq (Basra) Female ELISA (IgG/IgM) Cross‐sectional 177 23 12.99
Yang et al. (2017) China Both MAT (IgG) Cross‐sectional 2756 45 1.63
Taghizadeh et al. (2017) Iran (Fars) Female ELISA (IgG/IgM) Cross‐sectional 503 43 8.55
Clazer et al. (2017) Brazil (Paraná) Both IIF (IgG) Cross‐sectional 157 46 29.30
Alzaheb and Al‐Amer (2017) Saudi Arabia Female ELISA (IgG/IgM) Cross‐sectional 180 17 9.44
Sadaghian and Jafari (2016) Iran (Shabestar) Male ELISA (IgG) Case–control 80 27 33.75
Rosypal et al. (2015) United States (Virginia) Both ELISA (IgG) Cross‐sectional 336 16 4.76
Rodrigues et al. (2015) Brazil (São Paulo) Male ELISA (IgG) Cross‐sectional 112 27 24.11
Obaidat et al. (2015) Jordan Female ELISA (IgG/IgM) Cross‐sectional 202 135 66.83
Gyang et al. (2015) Nigeria (Lagos) Both LA Cross‐sectional 32 8 25.00
Xin and Song (2013) China (Shijiazhuang) Both ELISA (IgG) Case–control 864 44 5.09
Souza et al. (2010) Brazil (São Paulo) Female ELISA (IgG/IgM) Cross‐sectional 80 27 33.75
Sharif et al. (2010) Iran (sari) Both ELISA (IgG) Cross‐sectional 205 41 20.00
Rezende‐Figueiredo et al. (2010) Brazil (Campo Grande) Both ELISA (IgG/IgM) Cross‐sectional 100 39 39.00
Safar et al. (1986) Egypt (Cairo) Female IFAT (IgG) Cross‐sectional 100 31 31.00
Zimmermann (1976) United States (Iowa) Both IFA Cross‐sectional 142 29 20.42
Partono and Cross (1975) Indonesia (Jakarta) Both IHA Cross‐sectional 293 30 10.24
Riemann et al. (1974) United States (California) Both IHA Cross‐sectional 138 27 19.57
Riemann et al. (1974) Brazil (Belo Horizonte) Both IHA Cross‐sectional 219 100 45.66
Corrêa et al. (1972) Brazil (São Paulo) N/A IIF Cross‐sectional 338 151 44.67
Total 11,178 1538
Postgraduate Yang et al. (2017) China Both MAT (IgG) Cross‐sectional 813 20 2.46
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Abbreviations: CLIA, chemiluminescent immunoassay; ELISA, enzyme‐linked immunosorbent assay; IF, immunofluorescence; IFA, immunofluorescence assay; IFAT, indirect fluorescent antibody test; IgG, immunoglobulin G; IgM, immunoglobulin M; IHA, indirect hemagglutination assay; IIF, indirect immunofluorescence; LA, latex agglutination; MAT, modified agglutination test.

For risk factor analysis, the total number of participants and seropositive cases were extracted for each category of the variables of interest. Gender was classified as male or female; cat contact and soil contact as yes or no; dietary habits, including consumption of raw vegetables and undercooked meat, as consumer or non‐consumer; and place of residence as urban or rural according to the definitions reported in the original included studies. No independent reclassification was performed by the authors (Table 2). Risk factors were included based on reporting frequency and comparability across studies. The risk estimates were derived from extracted raw count data for each category and therefore represent unadjusted estimates.

TABLE 2.

Risk factors for T. gondii prevalence in students.

Characteristic Educational level References Subcategories
Male Female
Total (n) Positive (n) Total (n) Positive (n)
Gender Primary school Wang et al. (2020) 1289 126 1162 107
Thái et al. (2019) 243 54 224 56
Xin et al. (2015) 3498 665 2502 296
Mendy et al. (2015) 818 77 937 58
Gyang et al. (2015) 187 49 195 42
Fu et al. (2014) 90 49 76 42
Mizgajska‐Wiktor et al. (2013) 51 21 64 26
Fan et al. (2012) 123 77 132 84
Souza et al. (1987) 311 222 297 194
Overall 6610 1340 5589 905
High school Fallah et al. (2014) 0 0 549 84
Mizgajska‐Wiktor et al. (2013) 27 7 48 23
Fouladvand et al. (2010) 0 0 516 114
Galván‐Ramírez et al. (2010) 65 11 109 20
Overall 92 18 1222 241
Undergraduate Jimenez‐Chunga et al. (2024) 42 4 58 3
Ignacio Troncoso et al. (2022) 21 4 53 12
Barzinij (2021) 0 0 210 26
Kalantari et al. (2020) 0 0 504 36
Jafari‐Modrek et al. (2019) 0 0 80 8
Sánchez Artigas et al. (2018) 0 0 105 38
Yang et al. (2017) 1360 26 2209 29
Clazer et al. (2017) 83 20 74 26
Rosypal et al. (2015) 68 5 268 9
Rodrigues et al. (2015) 112 25 0 0
Obaidat et al. (2015) 0 0 202 135
Rezende‐Figueiredo et al. (2010) 17 8 76 28
Zimmermann (1976) 172 42 78 23
Overall 1875 134 3917 373
Characteristic Educational level References Yes No
Total (n) Positive (n) Total (n) Positive (n)
Contact with cats Primary school Wang et al. (2020) 989 121 1462 112
Fan et al. (2012) 126 123 115 0
Lopes et al. (2008) 46 28 119 37
Overall 1161 272 1696 149
High school Fouladvand et al. (2010) 81 28 434 86
Galván‐Ramírez et al. (2010) 49 11 121 18
Overall 130 39 555 104
Undergraduate Jimenez‐Chunga et al. (2024) 58 5 29 2
Ignacio Troncoso et al. (2022) 53 15 21 1
Cai et al. (2021) 1006 150 1698 161
Barzinij (2021) 16 13 194 13
Jafari‐Modrek et al. (2019) 11 1 69 7
Yang et al. (2017) 299 5 3270 60
Alzaheb and Al‐Amer (2017) 14 3 166 14
Rosypal et al. (2015) 283 15 53 1
Rodrigues et al. (2015) 29 23 83 2
Overall 1769 230 5583 261
Contact with soil Primary school Wang et al. (2020) 1792 197 659 36
Fan et al. (2012) 66 43 4 2
Overall 1858 240 663 38
Undergraduate Jimenez‐Chunga et al. (2024) 50 2 36 5
Cai et al. (2021) 1378 175 1326 136
Barzinij (2021) 31 17 179 9
Yang et al. (2017) 644 26 2925 39
Alzaheb and Al‐Amer (2017) 19 4 161 13
Rodrigues et al. (2015) 2 0 110 25
Overall 2124 224 4737 227
Raw vegetable consumption Primary school Fan et al. (2012) 223 142 23 16
Lopes et al. (2008) 148 57 18 8
Overall 371 199 41 24
High school Fouladvand et al. (2010) 442 102 73 12
Galván‐Ramírez et al. (2010) 160 28 10 1
Overall 602 130 83 13
Undergraduate Ignacio Troncoso et al. (2022) 6 0 68 16
Cai et al. (2021) 465 53 2239 258
Barzinij (2021) 31 6 179 20
Yang et al. (2017) 2198 34 1371 31
Clazer et al. (2017) 52 10 128 7
Rodrigues et al. (2015) 106 24 6 1
Overall 2858 127 3991 333
Undercooked meat consumption Primary school Lopes et al. (2008) 5 2 142 56
Fan et al. (2012) 66 65 4 4
Overall 71 67 146 60
High school Galván‐Ramírez et al. (2010) 11 7 159 22
Undergraduate Cai et al. (2021) 172 19 2532 292
Barzinij (2021) 5 3 205 23
Jafari‐Modrek et al. (2019) 2 0 78 8
Yang et al. (2017) 240 3 3329 62
Alzaheb and Al‐Amer (2017) 36 6 144 11
Rosypal et al. (2015) 330 15 6 1
Rodrigues et al. (2015) 37 23 75 2
Overall 822 69 6369 399
Characteristic Education level References Urban Rural
Total (n) Positive (n) Total (n) Positive (n)
Place of residence Primary school Wang et al. (2020) 1127 71 1324 162
Fu et al. (2014) 93 57 73 34
Lopes et al. (2008) 144 57 2 0
Giraldi et al. (2002) 276 116 158 68
Overall 1640 301 1557 264
High school Fallah et al. (2014) 402 50 147 34
Fouladvand et al. (2010) 472 109 44 5
Overall 874 159 191 39
Undergraduate Cai et al. (2021) 1392 156 1312 155
Barzinij (2021) 154 18 56 8
Jafari‐Modrek et al. (2019) 74 7 6 1
Yang et al. (2017) 2183 29 1386 36
Alzaheb and Al‐Amer (2017) 62 9 118 8
Zimmermann (1976) 95 22 141 40
Overall 3960 241 3019 248
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2.5. Data Analysis and Evidence Synthesis

Data analysis and evidence synthesis were conducted using Comprehensive Meta‐Analysis software (Version 3.3.070). Pooled seroprevalence rates of T. gondii exposure and their corresponding 95% confidence intervals (CIs) were calculated using a random‐effects model based on proportion data to account for anticipated heterogeneity between studies (Barendregt et al. 2013). Associations between T. gondii seropositivity and potential risk factors (e.g., gender, contact with cats, soil contact, consumption of raw vegetables, consumption of undercooked meat, and place of residence) were assessed using risk ratios (RRs) and 95% confidence intervals (CIs). Subgroup analyses based on educational level (primary school, high school, undergraduate and postgraduate) were conducted using both event rates and a random‐effects model to ensure comprehensive and robust comparisons across subgroups.

Heterogeneity among studies was evaluated using Cochran's Q test, with statistical significance set at p < 0.05 and the I 2 statistic. I 2 values of 25%, 50% and 75% were interpreted as indicating low, moderate and high heterogeneity, respectively (Higgins et al. 2003). Publication bias was assessed through visual inspection of funnel plots and quantified using Begg's and Egger's tests (Egger et al. 1997). To explore potential sources of heterogeneity, meta‐regression analyses were performed, examining variables such as publication year, sample size, geographical location and diagnostic methods used in the studies. Meta‐regression was performed using univariable models, with each moderator assessed separately.

3. Results

3.1. Study Selection Process and Characteristics

The systematic literature search initially identified 1555 records across multiple databases. Following the removal of 638 duplicate entries, the titles and abstracts of the remaining 917 articles were screened for relevance. This screening process led to the exclusion of 574 records that did not meet the predefined inclusion criteria. The full texts of the remaining 343 articles were then rigorously evaluated for eligibility. Of these, 50 studies satisfied all inclusion criteria and were subsequently included in the meta‐analysis. A detailed flowchart illustrating the study selection process, in accordance with the PRISMA guidelines, is presented in Figure 1.

FIGURE 1.

FIGURE 1

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PRISMA flow diagram illustrating the systematic review and study selection process for assessing global seroprevalence and risk factors of T. gondii exposure among students.

3.2. Event Rates of T. gondii Seropositivity

The meta‐analysis encompassed a diverse range of studies investigating the seroprevalence of T. gondii exposure among students across various educational levels. The pooled event rate for T. gondii seropositivity, derived from all included studies, was 0.140 (95% CI: 0.117–0.166), corresponding to an overall seroprevalence of 14.0%. This finding was statistically significant (Z‐value = −17.571, p < 0.001). Given the substantial heterogeneity observed among the studies (I 2 = 98.33%, p < 0.001), a random‐effects model was employed to account for variability in study design, population characteristics and methodological differences, ensuring a more accurate and generalizable estimate of seroprevalence.

When stratified by educational level, the highest event rate was observed among primary school students, with a pooled estimate of 0.285 (95% CI: 0.192–0.399), suggesting a higher exposure risk in this group. Undergraduate students exhibited a similar pooled event rate of 0.194 (95% CI: 0.135–0.272), followed by high school students, who had a slightly lower estimate of 0.193 (95% CI: 0.149–0.247). The lowest event rate was reported among postgraduate students, with a pooled estimate of 0.025 (95% CI: 0.016–0.038). However, it is important to note that this estimate is based on a single study (Figure 2).

FIGURE 2.

FIGURE 2

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Forest plot of T. gondii seroprevalence by educational level.

3.3. Association of Risk Factors With T. gondii Exposure

3.3.1. Gender Distribution

The meta‐analysis of 18 studies, comprising a total population of 10,728 females and 8577 males, found no significant difference in T. gondii seroprevalence between genders (RR = 0.918, 95% CI: 0.803–1.050, p = 0.214). Subgroup analyses across educational levels showed inconsistent patterns, with risk ratios ranging from 0.543 (95% CI: 0.128–2.300) to 1.848 (95% CI: 0.916–3.731), none reaching statistical significance (Figure 3A).

FIGURE 3.

FIGURE 3

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Forest plots summarizing relative risk estimates for key exposure factors associated with T. gondii seroprevalence among students: (A) comparison of risk in females relative to males, (B) risk in cat‐contact group compared to no‐contact, (C) risk in soil‐contact group compared to no‐contact, (D) risk in raw‐vegetable consumers compared to non‐consumers, (E) risk in undercooked‐meat consumers compared to non‐consumers and (F) risk in urban residents compared to rural residents. Pooled risk ratios with 95% confidence intervals are presented for each comparison.

3.3.2. Cat Exposure

Analysis of 14 studies, including 3060 students with cat contact and 7834 without exposure, revealed significantly higher T. gondii seropositivity among students with cat contact (RR = 1.888, 95% CI: 1.439–2.478, p < 0.001). Risk ratios varied considerably across educational levels, with particularly strong associations observed in some studies of undergraduate students (RR ranging from 0.896 to 32.914). Primary school studies showed the highest individual risk ratio (RR = 225.606, 95% CI: 14.194–3585.933), though with lower precision reflected in the wide confidence intervals (Figure 3B).

3.3.3. Soil Contact

Eight studies examining soil exposure, including 3982 exposed students and 5400 unexposed students, demonstrated significantly increased risk of T. gondii exposure among students with soil contact (RR = 1.940, 95% CI: 1.432–2.628, p < 0.001). In undergraduate students, although the pooled risk was elevated (RR = 2.07, 95% CI: 0.88–4.85), this association was not statistically significant (p = 0.095). Individual studies reported risk ratios ranging from 3.02 to 10.90, indicating substantial heterogeneity in findings (Figure 3C).

3.3.4. Raw Vegetable Consumption

Analysis of 10 studies, including 3831 consumers and 4115 non‐consumers, found no significant association between raw vegetable consumption and T. gondii seroprevalence (RR = 1.022, 95% CI: 0.831–1.258, p = 0.836). Moderate heterogeneity was observed (I 2 = 38.85%, p = 0.099), with inconclusive findings in the undergraduate subgroup analysis (Figure 3D).

3.3.5. Undercooked Meat Consumption

Ten studies examining undercooked meat consumption, including 904 consumers and 6674 non‐consumers, showed a significant association with T. gondii exposure (RR = 1.450, 95% CI: 1.133–1.857, p = 0.003). High heterogeneity among studies (I 2 = 83.01%, p < 0.001) reflected considerable variability in findings, particularly among undergraduate students (Figure 3E).

3.3.6. Residential Setting

Analysis of 12 studies, including 6474 urban and 4767 rural students, found no significant difference in T. gondii seroprevalence between urban and rural residents (RR = 0.866, 95% CI: 0.669–1.120, p = 0.272). Substantial heterogeneity was observed (I 2 = 85.20%, p < 0.001), with inconsistent patterns across all educational levels (Figure 3F).

3.4. Meta‐Regression

To investigate sources of heterogeneity in T. gondii seroprevalence among student populations, meta‐regression analyses were conducted using several moderators, including diagnostic method, publication year, geographic coordinates (latitude and longitude) and sample size (Figure 4). Diagnostic method emerged as a key contributor to heterogeneity, with significant effects observed in the overall model (Q = 28.17, df = 9, p = 0.0009; R 2 = 0.35), where ELISA was used as the reference method. Compared to ELISA, studies using immunofluorescence (IF) (coefficient = 2.1820, p = 0.0072) and immunofluorescence assay (IFA) (coefficient = 0.9697, p = 0.0469) reported significantly higher seroprevalence, while the modified agglutination test (MAT) showed a significant negative association (coefficient = −2.6896, p = 0.0010) and other diagnostic techniques had no statistically significant effects. Subgroup analyses revealed that diagnostic method explained 44% of the heterogeneity in primary school studies (Q = 15.64, df = 6, p = 0.0158), with IF again associated with higher prevalence compared to ELISA (coefficient = 1.8876, p = 0.0306), while no significant associations were found in high school students (Q = 0.56, df = 2, p = 0.7547) or undergraduates (Q = 8.18, df = 7, p = 0.3166), although MAT remained a significant negative predictor in the latter group (coefficient = −2.5913, p = 0.0218). Temporal trends assessed via publication year showed a non‐significant negative association in the overall analysis (coefficient = −0.0134, p = 0.1275; R 2 = 0.12), with similarly non‐significant findings across all educational subgroups, indicating limited influence of publication date on seroprevalence estimates. Geographic factors yielded more substantial effects: longitude was inversely associated with seroprevalence overall (coefficient = −0.0038, p = 0.0432; R 2 = 0.11) and remained significant among undergraduates (coefficient = −0.0061, p = 0.0330; R 2 = 0.24), while latitude had a stronger negative association both overall (coefficient = −0.0168, p < 0.001; R 2 = 0.41) and in subgroups, particularly in primary school students (coefficient = −0.0291, p < 0.001; R2 = 0.73), followed by undergraduates (coefficient = −0.0164, p = 0.0344; R 2 = 0.21), but not high school students. Finally, sample size was inversely associated with seroprevalence in the overall model (coefficient = −0.0004, p = 0.0072), albeit with no explanatory power (R 2 = 0.00), while subgroup results showed significant effects in undergraduates (coefficient = −0.0008, p = 0.0063; R 2 = 0.17) and marginal effects in high school students (coefficient = −0.0010, p = 0.0642; R 2 = 0.06), but no significant association among primary school studies. Collectively, these findings suggest that diagnostic method (with ELISA as the reference), along with geographic variables (especially latitude) and sample size, are notable contributors to heterogeneity in T. gondii seroprevalence estimates among student populations, with varying effects across educational levels.

FIGURE 4.

FIGURE 4

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Meta‐regression analyses examining the influence of diagnostic method, publication year, longitude, latitude and sample size on the logit event rate of T. gondii seroprevalence. Each row represents analyses for different educational levels (all students, primary school, high school and undergraduate). Circle sizes are proportional to study weights and regression lines indicate model‐estimated trends.

3.5. Publication Bias

Publication bias assessment across multiple analytical parameters revealed heterogeneous distributions with limited statistical evidence of bias (Figure 5). In the overall pooled seroprevalence analysis, the trim and fill method estimated 16 potentially missing studies; however, Begg's rank correlation (p = 0.72) and Egger's regression (p = 0.19) did not indicate significant bias. Subgroup analyses by educational level showed varied outcomes. Primary school studies suggested 7 missing studies (Begg's p = 0.53, Egger's p = 0.09), undergraduate studies indicated one (Begg's p = 0.57, Egger's p = 0.64), and no missing studies were identified among high school studies (Begg's p = 0.85, Egger's p = 0.70). All tests were non‐significant, supporting the absence of substantial bias across these strata. In gender‐related risk ratio analyses, two studies were potentially missing, with a fail‐safe N of 19. No evidence of bias was found (Begg's p = 0.49, Egger's p = 0.27). For cat exposure, two missing studies were estimated, but Begg's (p = 0.15) and Egger's (p = 0.10) tests remained non‐significant, and the fail‐safe N of 357 suggested robust findings. Analyses for soil contact detected no missing studies. The results were further supported by a fail‐safe N of 73 and no evidence of bias (Begg's p = 0.71, Egger's p = 0.53). In contrast, raw vegetable consumption analysis indicated two potentially missing studies, yet both tests showed no evidence of bias (Begg's p = 0.59, Egger's p = 0.32). However, the fail‐safe N was zero, indicating the results may not be robust. For undercooked meat consumption, one missing study was suggested. The fail‐safe N was 40, and bias tests remained non‐significant (Begg's p = 0.85, Egger's p = 0.38). In the residential setting analysis (urban vs. rural), one missing study was identified, with no indication of bias (Begg's p = 0.73, Egger's p = 0.77) and a modest fail‐safe N of 3.

FIGURE 5.

FIGURE 5

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Funnel plots evaluating potential publication bias in studies of T. gondii seroprevalence and associated risk factors among students. Panels A–D show funnel plots for overall student populations, primary school, high school and undergraduate subgroups, respectively. Panels E–J present funnel plots for specific risk factors, including gender (E), contact with cats (F), contact with soil (G), consumption of raw vegetables (H), consumption of undercooked meat (I) and place of residence (J). Symmetry of the plots and regression lines is used to assess potential bias.

Taken together, while a few potentially missing studies were identified through trim and fill procedures, formal statistical evaluations provided no consistent evidence of publication bias.

4. Discussion

4.1. Global Seroprevalence Among Students

The present meta‐analysis revealed a pooled global seroprevalence of T. gondii exposure among students to be 14.0%, based on a comprehensive synthesis of data across educational levels. This estimate reflects a considerable level of exposure among students, though the rate varied notably depending on the educational stage. Specifically, primary school students exhibited the highest pooled seroprevalence at 28.5%, suggesting early and heightened exposure to the parasite, potentially due to increased environmental interaction or lower hygiene practices in younger populations. Undergraduate and high school students presented similar intermediate seroprevalence rates of approximately 19.4% and 19.3%, respectively, indicating a persistent yet somewhat lower exposure risk with advancing age and educational level. In contrast, the lowest seroprevalence was identified among postgraduate students (2.5%), although this finding stemmed from a single study and therefore lacks generalizability. The trend of decreasing seroprevalence with increasing educational level might be interpreted as a reflection of improved health education, better hygiene behaviours and more limited environmental exposure among older students. Nevertheless, it is also plausible that earlier infections confer lifelong seropositivity, thereby influencing age‐related trends. The level of knowledge and awareness about T. gondii and its transmission routes plays a critical role in mitigating infection risk among students, as demonstrated by various studies and supported by findings from a cross‐sectional study conducted among students at the Universidad Nacional Mayor de San Marcos (UNMSM) in Lima, Peru (Jimenez‐Chunga et al. 2024). Increased awareness of preventive measures, such as proper hand hygiene, safe food handling practices (e.g., thoroughly cooking meat and washing vegetables), and avoiding contact with contaminated soil or cat faeces, can significantly reduce exposure to the parasite.

At a regional level, the highest prevalence among individual studies was reported in primary school students from Brazil (Rio de Janeiro) (68.4%) (Souza et al. 1987), while the lowest prevalence was observed among undergraduate students in China (1.6%) (Yang et al. 2017). These findings indicate pronounced geographical differences in exposure risk, influenced by environmental, behavioural and socioeconomic factors that vary across continents. Such variability emphasizes the importance of implementing context‐specific preventive strategies, particularly in high‐prevalence regions.

Assessment of publication bias indicated no substantial distortion of the pooled estimates. Although the trim‐and‐fill method suggested the presence of potentially unpublished studies, statistical tests did not reveal significant asymmetry in the funnel plots. Subgroup analyses by educational level also supported the stability of the findings, with minimal evidence of bias.

4.2. Risk Factors for T. gondii Exposure Among Students

This meta‐analysis examined several behavioural and environmental risk factors associated with T. gondii exposure among students, revealing varying degrees of association. No significant gender difference was observed, indicating that seropositivity risk is likely influenced more by environmental exposure and lifestyle rather than biological sex. This finding is consistent with studies in general populations where sex‐specific prevalence differences were minimal, suggesting similar patterns of exposure among male and female students (Bahadori et al. 2025; Gargaté et al. 2016).

Cat exposure demonstrated a strong and consistent association with seropositivity (RR = 1.89), underscoring its importance as a key risk factor. The strongest effect sizes were observed in primary school populations, where contact with cats often occurs in unstructured environments with limited supervision and hygiene awareness. In some studies, individual effect estimates were exceptionally high, reflecting localized conditions where domestic and stray cat populations contribute significantly to environmental contamination. This finding highlights the vulnerability of younger students, who are more likely to engage in direct pet handling or unsupervised outdoor play, increasing the likelihood of oocyst exposure. In high school and undergraduate populations, while the association remained significant, risk estimates were comparatively lower, possibly reflecting improved hygiene behaviour and more structured living conditions at these educational stages.

Soil contact was another significant predictor (RR = 1.94), particularly in primary school students. This association aligns with the recognized role of soil as a reservoir of T. gondii oocysts, especially in warm and humid climates where oocyst survival is prolonged (Meerburg and Kijlstra 2009). Soil contact was less consistently associated with exposure risk among undergraduates, where the pooled estimate did not reach statistical significance. This likely reflects reduced direct soil exposure in older age groups, as outdoor recreational habits and occupational patterns differ from those of younger children. Nonetheless, individual undergraduate studies reported high relative risks, suggesting that certain subpopulations, such as students in agricultural fields or those engaged in outdoor activities, remain vulnerable.

Dietary exposure also contributed to seropositivity risk, but patterns differed by food type. Consumption of undercooked meat was significantly associated with seropositivity (RR = 1.45), highlighting its role as a major foodborne transmission route. This association was particularly pronounced among undergraduate students, reflecting differences in dietary independence and consumption habits compared to primary and high school students, who often rely on parental or institutional meal preparation. In contrast, raw vegetable consumption showed no significant association with seropositivity. While vegetables can be contaminated with oocysts, proper washing and food safety practices may mitigate this risk, and variability in exposure sources may have obscured potential associations in the pooled analysis.

No significant difference was observed between urban and rural students, despite expectations of higher exposure risk in rural areas. This lack of difference may reflect converging lifestyles across settings, including improved sanitation and living conditions in rural areas and increasing pet ownership and indoor living in urban areas, thereby narrowing historical exposure differences.

Publication bias analyses indicated no consistent evidence of bias across the evaluated risk factors. Although a few potentially missing studies were detected for gender, cat exposure, raw vegetable consumption, undercooked meat consumption and residential setting, formal statistical tests (Begg's and Egger's) were non‐significant. Most findings, particularly for cat and soil contact, appeared robust based on fail‐safe N values. However, the association related to raw vegetable consumption demonstrated limited robustness, as indicated by a fail‐safe N value of zero and should therefore be interpreted with caution.

4.3. Sources of Heterogeneity in Seroprevalence Estimates

The meta‐regression analyses identified key factors contributing to heterogeneity in T. gondii seroprevalence among student populations. Diagnostic method was the most prominent source of variability, accounting for more than one‐third of the between‐study differences in the overall model and nearly half of the heterogeneity in primary school subgroups. Studies utilizing IF and IFA methods reported higher prevalence estimates compared to ELISA, while MAT was associated with lower prevalence. These findings are likely attributable to differences in analytical sensitivity and specificity across diagnostic platforms and highlight the importance of methodological standardization in prevalence studies to enhance comparability.

Geographic factors also contributed to heterogeneity. In our meta‐regression analyses, both latitude and longitude were inversely associated with seroprevalence, with latitude showing the strongest association, particularly in primary school studies where it explained more than 70% of the observed heterogeneity. This pattern suggests that lower‐latitude regions may have higher seroprevalence. One possible explanation is that warmer and more humid environmental conditions in such settings may enhance oocyst survival in soil and water, thereby increasing opportunities for transmission. This interpretation is in line with previous epidemiological evidence showing that climatic and environmental factors can influence the persistence of T. gondii and the risk of human exposure (Yan et al. 2016).

Temporal variation, represented by publication year, did not significantly influence prevalence estimates, suggesting that overall exposure risks among students have remained relatively stable during the study periods. Similarly, sample size was inversely associated with seroprevalence, most notably among undergraduate studies, although it accounted for minimal heterogeneity overall. This may reflect differences in population characteristics or the tendency for smaller studies to focus on high‐risk settings.

5. Limitations

This meta‐analysis is limited by the high heterogeneity among included studies, reflecting differences in diagnostic methods, geographic settings and study populations. Most included studies were cross‐sectional, which precludes causal inference. Some subgroups, such as postgraduate students, were represented by only a small number of studies, limiting generalizability. In addition, variations in exposure measurement and reporting, as well as potential unmeasured confounders, may have affected the pooled estimates despite no strong evidence of publication bias. Moreover, the pooled risk estimates were derived from raw extracted data and therefore represent unadjusted estimates, which should be interpreted cautiously because of the potential for confounding. Additionally, meta‐regression analyses were conducted using univariable models, which did not allow the simultaneous assessment of the combined effects of multiple moderators. Furthermore, although non‐English articles were translated and interpreted using Google Translate and Claude Pro Version 3.5 to support accurate comprehension and data extraction, minor interpretation variability cannot be entirely excluded. In addition, a formal GRADE assessment and a standardized study quality scoring system were not applied. Given that the primary aim of this review was to estimate pooled seroprevalence and summarize associated risk factors from predominantly cross‐sectional observational studies, the findings should be interpreted in conjunction with the reported heterogeneity, publication bias analyses, subgroup analyses and meta‐regression results. Finally, exposure to cats could not be consistently distinguished between pet cats and stray cats across the primary studies, which limited more specific interpretation of this risk factor.

6. Conclusion

This meta‐analysis demonstrates that T. gondii exposure remains a public health concern among students, with exposure risk varying by educational level and influenced by distinct environmental and behavioural factors. Younger students are more vulnerable to environmentally mediated exposures, whereas foodborne transmission plays a greater role in older students. Geographic and methodological differences further contribute to variability in prevalence estimates, highlighting the need for standardized diagnostic approaches and region‐specific preventive strategies. Targeted health education focusing on safe food handling, environmental hygiene and responsible pet care is essential for reducing infection risk in student populations worldwide. Future research should prioritize well‐designed longitudinal studies and the use of standardized diagnostic methods to better clarify exposure dynamics and improve comparability of seroprevalence estimates across different settings.

Author Contributions

The authors' contributions to this research are detailed below, following the CASRAI CRediT Taxonomy: Sara Lesani contributed to Conceptualization, methodology, data curation, writing – original draft and writing – review and editing. Mohammad Javad Boozhmehrani contributed to Project administration, supervision, software, formal analysis, methodology and writing – original draft and review and editing.

Funding

The authors have nothing to report.

Disclosure

Transparency Statement: The authors affirm that this research is an accurate, transparent and honest account of the study being reported. No important aspects of the research have been omitted, and any discrepancies from the study as planned have been explained.

Conflicts of Interest

The authors declare no conflicts of interest.

Supporting information

Appendix S1: Detailed search strategies.

ZPH-73-481-s001.docx (13.4KB, docx)

Acknowledgements

We express our gratitude to the authors of the studies included in this meta‐analysis for their valuable contributions to the field of Toxoplasma gondii research, which made this work possible.

AI Use Declaration: We acknowledge that Claude Pro Version 3.5, an AI language model, was utilized during the preparation of this manuscript. The AI was employed specifically to enhance the fluency of the English text and to assist with grammar checking. All intellectual content, ideas and conclusions presented in this manuscript are the sole work of the authors. The AI was used solely as a tool for linguistic refinement.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Appendix S1: Detailed search strategies.

ZPH-73-481-s001.docx (13.4KB, docx)

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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