Abstract
Background
Toxoplasmosis in pregnancy is associated with serious and irreversible maternal and fetal detrimental consequences. Also, different seroprevalence of Toxoplasma gondii in pregnancy is reported in many countries. The present systematic review and meta-analysis study aimed to determine the global seroprevalence of Toxoplasma gondii in pregnant women.
Methods
This study was conducted based on the PRISMA 2020 criteria. Initial searching was conducted using MeSH (Medical Subject Headings)-based keywords with no time limitation (by August 1, 2024). Collected papers were transferred to Citation Management Software (EndNote). Duplicate studies were merged and primary and secondary screenings were applied based on the inclusion/exclusion criteria. Validation was considered to find high-quality assessments. Finally, eligible extractable papers were enrolled for data collection. Data was analyzed using Comprehensive Meta-Analysis software (v.2) The random effects model was used in case of I2 index above 50%.In order to investigate the factors affecting the heterogeneity of studies, meta-regression tests were used to examine factors such as sample size and year of study.
Results
One hundred thirty-eight eligible studies with a total sample size of 135,098 pregnant women individuals were selected for data extraction and analysis. The heterogeneity index was found high (I2:98.9) and the random effect model was used for analysis. The egger test revealed the absence of publication bias in collected studies (p:0.088). Thus, the global seroprevalence of Toxoplasma gondii in pregnant women was reported at 36.6% (95%CI:33.7–39.6). the highest prevalence reported based on meta-analysis was reported in South America with 52.8% (95% CI:46.6–59), while only 15 studies were reviewed in this continent, most of which were in Brazil. Therefore, after the continent, the highest prevalence reported was reported in Africa with 46.8% (95% CI:39.5–54.3). Also, the lowest prevalence reported based on meta-analysis was in North America with 19.7% (95% CI:8.4–39.6) and Europe with 24.6% (95% CI:17.8–32.9).
Conclusion
This study revealed a high level of seroprevalence of Toxoplasma gondii in pregnant women worldwide. This value mostly depends on the individual's age, lifestyle, and disease awareness regarding toxoplasmosis in pregnant women. Thus, public awareness, along with comprehensive health programs regarding the detrimental effects of toxoplasmosis in pregnant women, seems necessary for prevention or even early diagnosis of toxoplasmosis in pregnant women.
Keywords: Toxoplasma gondii, Pregnant women, Pregnancy, Meta-analysis
Background
Toxoplasmosis is an infectious-parasitic disease in humans and animals, caused by Toxoplasma gondii (TG) [1]. Felines are the only definitive hosts of this parasite and other vertebrates are considered intermediate hosts [2]. TG infection is transmitted through the presence of oocytes in water and food or soil (contaminated with cat feces), raw meat, organ transplantation, blood transfusion, and also placenta to fetus transfer during pregnancy [3–5].
Toxoplasmosis can affect healthy and immunocompromised individuals and can also be a life-threatening disease in immunosuppressed individuals [3–5]. The parasite is transmitted through raw meat containing TG cysts or water containing oocysts from cat feces. Although felines are the only definitive host, TG can infect and replicate in almost any nucleated vertebrate cell [4, 5]. The life cycle TG has an asexual phase that occurs in nucleated cells and a sexual phase in the digestive tract of cats. Fertilized gametes from sexual reproduction are produced in the cat's small intestine, and excreted oocysts can persist in the environment for up to 18 months. Both waterborne and foodborne transmission have been reported [5].
This pathology is demonstrated in three forms of acute, latent, or cutaneous. Although TG infection is often asymptomatic, the acute type of TG infection is resembling the Influenza symptoms such as fever, sore throat, weakness, inflamed lymph nodes, and muscle pain [6–9]. However, Toxoplasmosis is more severe in immunocompromised individuals with detrimental effects on the fetus [10].
Toxoplasmosis is often self-limiting in people with healthy immune systems, but it is a significant risk in immunocompromised individuals and pregnant women [4, 11]. Acute TP is associated with many complications for the fetus and pregnant mother [12, 13]. The risk of vertical transmission of TG from the placenta to the fetus increases from 25% in the first to 65% in the third trimesters followed by more severe complications such as miscarriage, premature birth, congenital-related Toxoplasmosis, retinopathy, neuropathy, homeopathy, hydrocephaly, microcephaly, and cerebral calcification. Thus, early diagnosis and treatment of acute Toxoplasmosis in pregnant women are necessary to reduce the severity of complications [3, 4, 12–20].
The TG seroprevalence of women in reproductive age or pregnant cases ranges from 1.4% to 85%, globally [18–20]. If this infection occurs during pregnancy and infects the pregnant mother, it can lead to congenital toxoplasmosis, which can be a threat to the health of the baby. Clinical manifestations of the infection can be observed later in infancy, childhood, or adolescence. Epidemiological studies of this disease show that from 1988 to 1994, the seroprevalence of infected women aged 15 to 44 years was 15%, while the prevalence decreased to 11% in 1999–2004, and in 2009–2010, the seroprevalence was reported to be 9.1% [19]. The highest TG seroprevalence is related to tropical regions, lower altitudes areas, developing (South America and Africa), and Middle East countries [4, 21]. However, high seroprevalence of TG is reported in many developed countries (like France) where people consume uncooked meat [21]. These differences indicate the alteration in reported cases of TG seroprevalence in different regions [21].
Serological screening is a valid procedure for diagnosis of acute (or chronic TG infection [16, 17]. After acute infection diagnosis in a pregnant mother, some antibiotics such as Spiramycin are prescribed with an effectiveness rate of > 60% to inhibit fetal congenital infection [7, 18, 19].
Assessment of the scientific dimensions of Toxoplasma gondii in pregnant women is important due to the development of preventive measures, early diagnosis, and treatment of acute Toxoplasmosis. Given that different reports of the prevalence of this disease in pregnant women around the world report different prevalences and high heterogeneity, Thus, this systematic review and meta-analysis study aimed to report the Global seroprevalence of Toxoplasma gondii in pregnant women.
Methods
This study was conducted based on the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) statement criteria (2020) [22]. The initial search was conducted on August 1, 2024, and updated on August 28, 2024 with no time limitation. The searching strategy was designed using the MeSH-based keywords of “Prevalence”, “Factors”, “Outcome”, “Toxoplasma gondii”, “Pregnant women”, and “Pregnancy” in major electronic databases, including PubMed, ScienceDirect, Scopus, Web of Sciences (WoS), Embase, and G.Scholar. References of included papers were also reviewed to cover the maximum number of eligible studies. All papers reporting the seroprevalence of Toxoplasma gondii in pregnant women were included in this study. Also, other variables (e.g., geographic location, diagnostic method, Age, Sample size) were collected for comprehensive assessment of data. The search strategy in the various databases examined is reported in Table 1.
Table 1.
Search strategy in various databases studied
| Database | Search Type | Search strategy |
|---|---|---|
| PubMed | Advanced search | (((("prevalence"[Title/Abstract]) OR ("outcome"[Title/Abstract])) AND ("factors"[Title/Abstract])) AND ("toxoplasma gondii"[Title/Abstract])) AND ("pregnant women"[Title/Abstract]) |
| ScienceDirect | Advanced search | Titke, abstract, keywords: (prevalence OR outcome) AND (factors) AND ("toxoplasma gondii") AND ("pregnant women") |
| Scopus | basic search | Titke, abstract, keywords: (prevalence OR outcome) AND (factors) AND ("toxoplasma gondii") AND ("pregnant women") |
| WOS | basic search | TS = (prevalence OR outcome) AND (factors) AND ("toxoplasma gondii") AND ("pregnant women" OR pregnancy) |
| Embase | Advanced search | prevalence:ab,ti AND 'toxoplasma gondii':ab,ti AND 'pregnant women':ab,ti |
| Google scholar | Advanced search | prevalence "pregnant women" OR pregnancy "toxoplasma gondii" |
Inclusion and exclusion criteria
Inclusion criteria: Studies that reported the prevalence of Toxoplasma gondii in pregnant women. Studies for which the full text was available. Studies that provided sufficient data (sample size, prevalence percentage). Studies whose text was in English. Analytical observational studies (cross-sectional). Studies conducted in countries around the world and on different continents all Toxoplasma gondii diagnostic methods.
Exclusion criteria were reviews studies, intervention studies, cohorts, case-controls, duplicate papers, non-English investigations, and all articles with insufficient or unextractable data.
Study selection and quality assessment
In this process, initial searching was applied and selected papers were transferred to the Citation Management Software (EndNote). Duplicate articles were detected and excluded. Following the primary screening, the “Title” and “Abstract” of all studies were evaluated and un-eligible studies were excluded. In the second screening, full-text of remaining papers was examined and the articles with insufficient or unextractable data were ignored. Selected papers were enrolled for quality control step. The Newcastle–Ottawa Scale (NOS), a quality assessment tool for observational studies, was used to assess the quality of the articles reviewed in this study. The NOS assigns a maximum of 9 points for the lowest risk of bias for three areas examined in the articles: four points for the selection of study groups, two points for the comparison of groups, and three points for the determination of exposure and outcomes for case–control and cohort studies, respectively. Finally, in this review, articles were considered as high quality (score ≥ 5) or low quality (score less than 5). Finally, 138 articles were reviewed and analyzed in this study.
Data extraction and meta-analysis
Data extraction was applied using a previously prepared checklist including Name of first author, Year of publication, Type of study, Study location, Sample size, Age range, Mean age, Number (or percentage of seroprevalence in 4 ranges of total, first, second, and third trimesters), and Number (or percentage) of IgG, IgM, and IgG/IgM antibodies (Table 2). After statistical extraction of data, Comprehensive Meta-Analysis software (CMA, v2) was hired for data analysis. Heterogeneity of the studies was assessed through the I2 index and the Egger test was used to check publication bias followed by the Funnel Plot diagram. The random effects model was used in case of I2 index above 50%.In order to investigate the factors affecting the heterogeneity of studies, meta-regression tests were used to examine factors such as sample size and year of study. Also, given the geographical scope of the study and the studies conducted in different countries around the world, subgroup analysis was also conducted based on continent.
Table 2.
Summary of the seroprevalence studies included in the review
| Author | Year | Study | Region | Sample size | Age | Seroprevalence, n(%) | SP trimesters, n (%) | Total | SM | |||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Range | Mean | IgG | IgM | IgG/ IgM | 1st | 2nd | 3rd | |||||||
| Abamecha et al [23] | 2016 | Cross sectional | Ethiopia | 232 | - | 23.65 | 191 (82.3) | 0 (0) | 7 (3) | 56 (28.3) | 100 (50.5) | 42 (21.2) | 198 (85.3) | ELISA |
| Abdelbaset et al [6] | 2020 | Cross sectional | Egypt | 96 | - | 26.3 | - | - | - | 0 (0) | 10 (35.7) | 12 (23) | 22 (22.9) | LAT/ ELISA |
| Addo et al [1] | 2023 | Cross sectional | Ghana | 84 | - | 26.96 | 44 (52.38) | 3 (3.57) | - | 11 (45.83) | 17 (58.62) | 19 (61.29) | 47 (55.95) | ELISA |
| Agmas et al [24] | 2015 | Cross sectional | Ethiopia | 263 | 18-44 | 29.56 | - | - | - | - | - | - | 180 (68.4) | LAT |
| Ahmadi et al [25] | 2023 | Retrospective crosssectional | Iran | 4225 | 15- 45 | - | 885 (20.8) | 405 (9.5) | 510 (12) | - | - | - | 1800 (42.6) | ELISA |
| Ahmadpour et al [12] | 2019 | Cross sectional | Iran | 276 | - | 33.1 | 55 (19.92) | 6 (2.17) | 5 (1.81) | - | - | - | 66 (23.9) | ELISA CLIA |
| Ahmed et al [26] | 2014 | Cross sectional | Egypt | 100 | 21-35 | 26,95 | 63 (63) | 11 (11) | 8 (8) | - | - | - | 82 (82) | IHA |
| Akinbami et al [27] | 2010 | Cross sectional | Nigeria | 179 | 25 -30 | - | 73 (40.8) | - | - | - | - | - | 73 (40.8) | ELISA |
| Akpınar et al [28] | 2017 | Retrospective crosssectional | Turkey | 3140 | - | - | 344 (28.4) | 34 (1.8) | - | 378 (12) | 0 (0) | 0 (0) | 378 (12) | Macro ELISA |
| Al Mohammad et al [29] | 2010 | Cross sectional | SAR | 554 | 18 -41 | 24.1 | 285 (51.4) | 49 (8.8) | 11 (2) | - | - | - | 345 (62.3) | ELISA |
| Al-Adhroey et al [16] | 2019 | Cross sectional | Yemen | 420 | 16 -45 | - | 54 (12.9) | 5 (1.2) | 30 (7.1) | 16 (18.8) | 32 (21.3) | 41 (22.2) | 89 (21.2) | ECL / ELISA |
| Al-Eryani et al [30] | 2016 | Cross sectional | Yemen | 593 | 15 -48 | - | 259 (43.7) | 54 (9.1) | 44 (7.4) | _ | _ | _ | 269 (45.4) | ELISA |
| Al-Harthi et al [31] | 2006 | Cross sectional | SAR | 197 | 17 -45 | - | 58 (29.4) | 11 (5.6) | 4 (2) | 64 (37.8) | 9 (42.8) | 0 (0) | 73 (37) | ELISA |
| Alghamdi et al [32] | 2016 | Cross sectional | SAR | 203 | 15 -45 | 32 | 66 (32.5) | 13 (6.4) | - | - | - | - | 79 (38.9) | ELISA |
| Almogren [33] | 2011 | Retrospective crosssectional | SAR | 2176 | - | 25 | 825 (38) | - | - | - | - | - | 825 (38) | IHA |
| Alvarado et al [34] | 2006 | Cross sectional | Mexico | 343 | 13 ≤ | - | 21 (6.1) | 0 (0) | - | - | - | - | 21 (6.1) | ELISA |
| Amar et al [35] | 2015 | Cross sectional | India | 103 | - | - | 26 (25.2) | 2 (1.9) | - | 4 (21) | 16 (27) | 8 (32) | 28 (27.18) | ELISA |
| Andiappan et al [36] | 2014 | Prospective crosssectional | Thailand | 760 | 14 -47 | 29.5 | 167 (22) | - | 23 (3) | 162 (26.1) | 27 (20.9) | 1 (10) | 190 (25) | ELISA |
| Andiappan et al [37] | 2014 | Prospective crosssectional | Malaysia | 219 | - | - | 93 (42.4) | - | - | 3 (60) | 32 (40.5) | 58 (43) | 93 (42.4) | ELISA |
| Andiappan et al [37] | 2014 | Prospective crosssectional | Myanmar | 215 | - | - | 66 (30.7) | - | - | 4 (66.7) | 27 (28.4) | 35 (30.7) | 66 (30.7) | ELISA |
| Antinarelli et al [38] | 2021 | Retrospective crosssectional | Brazil | 5895 | - | - | 2591 (44.4) | 5 (0.1) | 110 (1.9) | - | - | - | 27.06 (45.9) | CMIA |
| Asthana et al [39] | 2006 | Cross sectional | Grenada | 534 | - | - | 304 (57) | - | - | - | - | - | 304 (57) | ELISA |
| Atakorah et al [40] | 2022 | Cross sectional | Ghana | 150 | 18 - 40 | 27.83 | 72 (48) | 17 (11.3) | 11 (7.3) | - | - | - | 100 (66.66) | ELISA |
| Awoke et al [41] | 2015 | Cross sectional | Ethiopia | 384 | - | 26.96 | 71 (18.5) | - | - | 7 (17.9) | 28 (20.6) | 36 (17.2) | 71 (18.5) | LAT |
| Ayeah et al [4] | 2022 | Cross sectional | Cameroon | 300 | 16 - 41 | 28.05 | 218 (72.7) | 4 (1.3) | 18 (6) | - | - | - | 240 (80) | ELISA |
| Aynioglu et al [42] | 2015 | Retrospective crosssectional | Turkey | 910 | 17 - 46 | 29 13 | 400 (43.9) | 23 (2.5) | - | - | - | - | 423 (46.48) | CLIA |
| Baghel et al [43] | 2020 | Cross sectional | India | 200 | 35 ≤ | - | 11 (5.5) | 0 (0) | - | - | - | - | 11 (5.5) | ELISA |
| Bamba et al [5] | 2017 | Cross sectional | Burkina Faso | 316 | - | 26.9 | 98 (31.1) | - | - | - | - | - | 98 (31.1) | ELISA/ ELFA |
| Barbosa et al [44] | 2009 | Cross sectional | Brazil | 190 | 13 - 45 | - | 126 (66.3) | 1 (0.52) | - | 16 (12.6) | 53 (41.7) | 58 (45.7) | 127 (66.8) | ELISA |
| Bashour et al [13] | 2024 | Cross sectional | Iran | 340 | 16 - 46 | 29.13 | 101 (29.7) | - | 2 (0.6) | - | - | - | 103 (30.3) | ELISA/ PCR |
| Barzgar et al [2] | 2024 | Cross sectional | Iran | 1200 | 18 - 42 | - | 381 (31.7) | 41 (3.4) | - | - | - | - | 422 (35.1) | ELISA |
| Bassiony et al [45] | 2016 | Cross sectional | Egypt | 382 | 17 - 44 | 26.71 | 219 (57.33) | 43 (11.3) | 41 (10.7) | 77 (58.8) | 98 (55) | 46 (63) | 221 (57.9) | ELISA |
| Bjerke et al [46] | 2011 | Cross sectional | Pakistani immigrants in Norway | 206 | 18 - 44 | 27.3 | 36 (17.4) | - | - | - | - | - | 36 (17.4) | EIA |
| Chandrasena et al [47] | 2016 | Cross sectional | Sri Linka | 293 | - | 27 | 36 (12.3) | 0 | - | - | - | - | 36 (12.3) | RDT |
| Chemoh et al [9] | 2019 | Cross sectional | Malaysia | 219 | 20–40< | - | 67 (30.6) | 5 (2.3) | 4 (1.8) | 4 (23.5) | 38 (33.3) | 34 (38.6) | 76 (34.7) | ELISA |
| Costa et al [48] | 2018 | Cross sectional | Brazil | 463 | 13 - 44 | 24 | 335 (72.3) | 17 (3.7) | - | - | - | - | 352 (76.02) | ELISA |
| Cvetković et al [49] | 2010 | Retrospective Crosssectional | Macedonia | 235 | 15 - 45 | - | 48 (20.4) | - | - | - | - | - | 48 (20.4) | ELISA |
| da Rocha et al [50] | 2015 | Cross sectional | Brazil | 338 | - | - | 240 (71) | 0 | 0 (0) | - | - | - | 240 (71) | MEIA |
| Daka et al [11] | 2024 | Cross sectional | Zambia | 401 | 24 - 30 | 27 | 17 (4.2) | 3 (0.7) | 1 (0.2) | 0 (0) | 11 (57.9) | 8 (42.1) | 19 (4.7) | ELISA |
| De Paschale et al [51] | 2008 | Cross sectional | Italy | 3426 | 15 - 44 | - | 737 (21.5) | 42 (1.2) | - | - | - | - | 779 (22.7) | ELISA |
| De Paschale et al [52] | 2014 | Cross sectional | Benin | 283 | 15 - 41 | 26.2 | 737 (21.5) | 42 (1.2) | - | - | - | - | 86 (30) | ELISA |
| De Quadros et al [53] | 2015 | Cross sectional | Brazil | 148 | 14 - 41 | - | 24 (16) | 1 (0.6) | - | - | - | - | 25 (16.9) | - |
| Deka et al [54] | 2022 | Cross sectional | India | 165 | - | 27.6 | 63 (38.2) | 22 (13.3) | 18 (10.9) | - | - | - | 68 (41.2) | ELISA |
| Duarte et al [55] | 2020 | Cross sectional | Brazil | 201 | - | 27.5 | 54 (26.8) | 0 | - | - | - | - | 54 (26.8) | IFA |
| Dwinata et al [56] | 2017 | Cross sectional | Indonesia | 330 | 17 - 40 | 27 | 36 (10.9) | - | - | - | - | - | 36 (10.9) | ELISA |
| Edrees et al [18] | 2020 | Cross sectional | Iraq | 150 | - | 29.9 | 40 (26.7) | 0 | - | 9 (16.9) | 19 (28.3) | 12 (40) | 40 (26.7) | ELISA |
| El Deeb et al [57] | 2012 | Cross sectional | Egypt | 323 | 19 - 39 | - | 218 (67.5) | 9 (2.8) | 9 (2.8) | 80 (69.6) | 46 (63.9) | 92 (67.6) | 218 (67.5) | ELFA/ VIDAS |
| Elsheikha [58] | 2008 | Cross sectional | Egypt | 350 | - | 25.2 | 211 (60.3) | - | - | - | - | - | 211 (60.3) | ELISA |
| Endris et al [59] | 2014 | Cross sectional | Ethiopia | 385 | 20 - 30 | - | 341 (88.6) | - | - | 14 (70) | 228 (89.8) | 99 (89.2) | 341 (88.6) | LAT |
| Eshratkhah et al [60] | 2018 | Cross sectional | Iran | 620 | 14 - 47 | - | 114 (18.4) | - | 3 (0.5) | 117 (18.9) | 0 | 0 | 117 (18.9) | ELISA |
| Fenta [61] | 2019 | Cross sectional | Ethiopia | 494 | 15 - 42 | 26.47 | 370 (74.9) | 19 (3.8) | 15 (3.1) | 79 (19.6) | 140 (34.7) | 185 (45.8) | 404 (81.8) | ELISA |
| Findal et al [62] | 2015 | Cross sectional | Norway | 1922 | 15 - 46 | - | 179 (9.3) | - | - | - | - | - | 179 (9.3) | ELISA |
| Flores et al [63] | 2021 | Cross sectional | Panama | 2326 | - | - | 997 (42.9) | 5 (0.21) | 31 (1.33) | - | - | - | 1033 (44.4) | avidity test |
| Fonseca et al [64] | 2012 | Cross sectional | BrazilL | 2136 | 20 - 49 | - | 1057 (49.5) | 77 (3.6) | - | - | - | - | 1134 (53) | - |
| Frimpong et al [65] | 2017 | Cross sectional | Zambia | 411 | 15 - 49 | - | 24 (5.87) | 0 | - | 3 (3.57) | 11 (8.21) | 10 (5.18) | 24 (5.87) | RDT |
| Garedaghi et al [66] | 2017 | Cross sectional | Iran | 200 | - | - | 79 (39.5) | 5 (2.5) | 2 (1) | 40 (43.4) | 11 (44) | 33 (39.7) | 82 (41) | ELISA |
| Gelaye et al [67] | 2015 | Cross sectional | Ethiopia | 288 | 18 - 42 | 28.41 | - | - | - | 14 (77.8) | 52 (88.1) | 180 (85.3) | 246 (85.4) | LAT |
| Gheshlaghi et al [15] | 2022 | Cross sectional | Iran | 740 | 14 - 48 | 28.1 | 157 (21.2) | 2 (0.27) | - | - | - | - | 159 (21.5) | ELISA |
| Hajsoleimani et al [68] | 2012 | Cross sectional | Iran | 500 | - | - | 186 (37.2) | 7 (1.4) | - | 74 (43.5) | 52 (35.9) | 63 (34) | 189 (37.8) | ELISA |
| Hansu et al [69] | 2021 | Retrospective crosssectional | Turkey | 29424 | 15 -45 | - | 6035 (20.5) | 502 (1.7) | 255 (0.86) | 6282 (21.34) | 0 | 0 | 6282 (21.34) | - |
| Hariri et al [70] | 2023 | Cross sectional | Iran | 244 | 16 -43 | 23.06 | 54 (22.1) | 0 (0) | - | - | - | - | 54 (22.1) | ELISA |
| Hassanain et al [71] | 2018 | Cross sectional | Egypt | 388 | 18 -44 | 27 | - | - | - | 0 (0) | 40 (33.1) | 39 (35.8) | 79 (20.4) | ELISA |
| Hosseini et al [72] | 2023 | Cross sectional | Iran | 100 | - | - | 68 (68) | 1 (1) | - | - | - | 69 (69) | ELISA | |
| Hung et al [73] | 2007 | Cross sectional | Sao Tome and Principe | 499 | - | 25.4 | - | - | - | - | - | 375 (75.2) | LAT | |
| Hung et al [74] | 2015 | Cross sectional | Taiwan | 104 | 20 -42 | 30.91 | 7 (6.7) | 0 | 1 (1) | - | - | - | 8 (7.7) | ELISA |
| Ijaz et al [75] | 2020 | Prospective Crosssectional | Pakistan | 418 | - | 33 | 140 (33.5) | 28 (6.7) | 12 (2.9) | - | - | - | 180 (43) | ELISA |
| Iqbal et al [76] | 2007 | Cross sectional | Kuwait | 224 | 19 -41 | 27 | 119 (53.1) | 31 (13.8) | - | 150 (66.96) | 0 (0) | 0 (0) | 150 (66.96) | ELFA/ VIDAS |
| Jahantigh et al [77] | 2020 | Cross sectional | Iran | 90 | - | - | 13 (14) | 0 (0) | - | 6 (15) | 7 (14) | 0 (0) | 13 (14) | ELISA |
| Jiang et al [78] | 2018 | Cross sectional | China | 313 | - | - | 43 (13.74) | 4 (1.28) | 4 (1.28) | - | - | - | 51 (16.29) | ELISA |
| Jula et al [79] | 2018 | Prospective cross sectional | Ethiopia | 401 | - | 23.1 | - | - | - | 19 (25.3) | 42 (26.6) | 35 (20.8) | 96 (23.9) | EIA |
| Karabulut et al [80] | 2011 | Cross sectional | Turkey | 1102 | 18-40 | 29.8 | 408 (37) | 15 (1.4) | 97 (8.8) | 520 (47.2) | 0 (0) | O (0) | 520 (47.2) | Vitros ECiQ |
| Kassie et al [81] | 2024 | Cross sectional | Ethiopia | 340 | 18-44 | - | 132 (38.8) | - | - | - | - | - | 132 (38.8) | ELISA |
| Kaur et al [82] | 1999 | Prospective cross sectional | India | 120 | 16-36< | - | - | 14 (11.6) | - | - | - | - | 14 (11.6) | - |
| Khademi et al [83] | 2019 | Cross sectional | Iran | 360 | 14-55 | 27 | 100 (27.8) | - | 3 (0.83) | - | - | - | 103 (28.6) | ELISA |
| Khames et al [84] | 2020 | Cross sectional | Algeria | 1012 | - | - | 187 (18.5) | 16 (1.6) | 49 (4.8) | - | - | - | 252 (25) | ELISA |
| Kledmanee et al [85] | 2019 | Cross sectional | Thailand | 105 | 15-49 | - | - | - | - | - | - | - | 33 (31.4) | ELISA |
| Linguissi et al [86] | 2012 | Retrospective crosssectional | Burkina Faso | 182 | 18≤ | - | 37 (20.3) | 7 (3.8) | - | 44 (24.17) | 0 (0) | 0 (0) | 44 (24.17) | ELISA |
| Liu et al [87] | 2009 | Cross sectional | China | 235 | 21 -38 | - | 25 (10.6) | 0 (0) | - | - | - | - | 25 (10.6) | ELISA |
| Lobo et al [20] | 2017 | Cross sectional | Portugal | 155 | 15 -44 | - | 17 (10.95) | 0 (0) | 17 (10.95) | - | - | - | 34 (21.9) | DAT/ ISAGA |
| Lobo et al [20] | 2017 | Cross sectional | Angola | 300 | 15 - 44 | - | 71 (23.7) | 6 (2) | 5 (1.7) | 18 (26.9) | 41 (27.5) | 23 (27.4) | 82 (27.3) | DAT/ ISAGA |
| Lopes-Mori et al [88] | 2013 | Cross sectional | Brazil | 2226 | - | 25 | 1122 (50.4) | - | - | - | - | 93 (55) | 1151 (51.7) | ELISA |
| Mahdy et al [89] | 2017 | Cross sectional | Yemen | 359 | 22 - 30 | 26 | 154 (42.89) | 7 (1.9) | - | - | - | 55 (46.2) | 166 (46.2) | ELISA |
| Majid et al [90] | 2016 | Cross sectional | Pakistan | 733 | 15 - 40 | - | 135 (18.41) | - | - | 21 (7.17) | 43 (20.19) | 71 (31.28) | 135 (18.41) | IFA |
| Marković et al [91] | 2023 | Cross sectional | Serbia | 300 | 15≤ | - | - | 0 (0) | - | 13 (34.2) | 6 (15.8) | 19 (50) | 38 (12.7) | VIDAS |
| Mohamed et al [92] | 2016 | Cross sectional | SAR | 326 | 16 - 40 | 30.19 | 69 (21.2) | 4 (1.2) | - | 18 (25.7) | 20 (23.5) | 35 (20.8) | 73 (22.4) | ELISA |
| Mosawi et al [93] | 2019 | Cross sectional | Afghanistan | 431 | - | - | - | - | - | - | - | - | 207 (48.03) | CLIA |
| Motoi et al [94] | 2020 | Cross sectional | Romania | 6889 | 18–36< | - | 2746 (39.86) | - | - | - | - | - | 2746 (39.86) | CLIA |
| Mulugeta et al [10] | 2020 | Cross sectional | Ethiopia | 233 | 18 - 42 | 26.11 | - | - | - | 27 (79.4) | 59 (64.1) | 72 (67.3) | 158 (67.8) | LAT |
| Murad et al [95] | 2023 | Cross sectional | Iraq | 180 | 15 - 50 | - | 110 (61.1) | - | - | 33 (76.7) | 27 (55.1) | 50 (56.8) | 110 (61.1) | ELISA |
| Murad et al [96] | 2023 | Cross sectional | Iraq | 400 | 15 - 50 | - | 205 (51.3) | - | - | - | - | - | 205 (51.3) | ELISA |
| Mwambe et al [97] | 2013 | Cross sectional | Tanzania | 350 | 15 - 44 | - | - | - | - | 4 (26.7) | 50 (33.3) | 55 (29.7) | 108 (30.9) | ELISA |
| Nasir et al [98] | 2015 | Cross sectional | Nigeria | 360 | 18 - 40 | 30 | 144 (40) | 32 (8.9) | 6 (1.7) | 38 (-) | 44 (-) | 94 (-) | 176 (48.88) | ELISA |
| Ndumbe et al [99] | 1992 | Cross sectional | Cameroon | 192 | - | - | 148 (77.1) | - | - | - | - | - | 148 (77.1) | EIA |
| Nijem et al [100] | 2009 | Cross sectional | Palestine | 204 | 16 - 43 | 26.4 | 57 (27.9) | 36 (17.6) | - | 93 (45.5) | 0 (0) | 0 (0) | 93 (45.5) | ELISA |
| Nissapatorn et al [101] | 2003 | Cross sectional | Malaysia | 200 | 18 - 43 | 29.6 | 78 (39) | 8 (4) | 12 (6) | 2 (33.3) | 19 (45.2) | 77 (49) | 98 (49) | ELISA |
| Njunda et al [102] | 2011 | Cross sectional | Cameroon | 110 | 18 - 41 | - | 69 (62.7) | 0 (0) | 3 (2.7) | 30 (75) | 40 (60.6) | 2 (50) | 72 (65.4) | ELISA |
| Njunda et al [103] | 2011 | Cross sectional | Cameroon | 110 | 20 - 44 | - | 77 (70) | 3 (2.7) | - | 14 (87.5) | 39 (66.1) | 24 (70) | 77 (70) | ELISA |
| Nowakowska et al [104] | 2006 | Cross sectional | Poland | 4916 | 19 - 46 | 26.7 | 2030 (41.3) | - | - | - | - | - | 2030 (41.3) | IDAT/ ELISA |
| Ocak et al [105] | 2007 | Cross sectional | Turkey | 1652 | 16 - 42 | 27.2 | 860 (52.1) | 9 (0.54) | - | - | - | - | 869 (52.6) | ELISA |
| Olariu et al [106] | 2020 | Cross sectional | Romania | 208 | Dec-41 | 27.1 | - | - | - | - | - | - | 116 (55.8) | Vitros ECIQ |
| Oliveira et al [107] | 2019 | Cross sectional | Brazil | 196 | - | - | 133 (67.9) | 3 (1.5) | - | - | - | - | 136 (69.3) | CLIA |
| Ouermi et al [108] | 2009 | Cross sectional | Burkina Faso | 276 | 19 - 42 | 27.65 | 75 (27.2) | 13 (4.7) | - | - | - | - | 88 (31.9) | ELISA |
| Oyinloye et al [109] | 2014 | Cross sectional | Nigeria | 90 | 15–35< | - | 20 (22.2) | - | - | 2 (18.1) | 8 (29.6) | 10 (19.4) | 20 (22.2) | ELISA |
| Pereira et al [110] | 2024 | Cross sectional | Brazil | 280 | 15 - 43 | 26 | 69 (24.6) | - | - | 35 (27.13) | 9 (16) | 25 (26.3) | 69 (24.6) | CLIA |
| Qamer et al [111] | 2020 | Cross sectional | SAR | 306 | 16 - 45 | 29.9 | 99 (32.4) | 3 (1) | - | - | - | - | 101 (33) | ECL |
| Rocha et al [112] | 2015 | Cross sectional | Brazil | 338 | - | - | 240 (71) | 0 (0) | - | - | - | - | 240 (71) | MEIA |
| Rosso et al [113] | 2008 | Cross sectional | Colombia | 955 | 14 - 40 | 25.1 | 437 (45.8) | 27 (2.8) | - | - | - | - | 464 (48.5) | MEIA |
| Sakikawa et al [114] | 2012 | Cross sectional | Japan | 4466 | 16 - 46 | 27.4 | - | - | - | - | - | - | 459 (10.3) | LAa titer |
| Salih [115] | 2010 | Cross sectional | Iraq | 260 | 15 - 44 | - | 80 (30.76) | 31 (11.92) | - | - | - | - | 111 (42.7) | ELISA |
| Sandoval et al [116] | 2020 | Cross sectional | Mexico | 311 | 18 - 44 | - | 13 (4.2) | 0 (0) | - | - | - | - | 13 (4.2) | ELISA |
| Santos et al [117] | 2017 | Cross sectional | Brazil | 200 | - | - | 125 (62.5) | - | - | - | - | - | 125 (62.5) | IFA |
| Sen et al [118] | 2012 | Cross sectional | India | 380 | - | - | - | 74 (19.4) | - | 74 (19.4) | 0 (0) | 0 (0) | 74 (19.4) | ELISA |
| Sharbatkhori et al [119] | 2014 | Cross sectional | Iran | 555 | - | - | 221 (39.8) | 19 (3.4) | 8 (1.4) | 97 (47.3) | 76 (45.7) | 67 (36.4) | 232 (41.8) | ELISA |
| Silva-Díaz et al [120] | 2020 | Cross sectional | Peru | 218 | - | 25.5 | 66 (30.3) | 12 (5.5) | - | 20 34.4) | 26 (38.8) | 32 (34.4) | 78 (35.8) | ELISA |
| Singh et al [121] | 2021 | Cross sectional | Ghana | 400 | - | - | 229 (57.3) | 14 (3.5) | 12 (3) | 231 (57.8) | 0 (0) | 0 (0) | 231 (57.8) | ELISA |
| Sirin et al [122] | 2017 | Retrospective Cross sectional | Turkey | 7513 | 18 - 45 | - | 2427 (32.3) | 138 (1.9) | - | - | - | - | 2565 (34.1) | CEIM |
| Sitoe et al [123] | 2010 | Cross sectional | Mozambique | 150 | 15 - 50 | 32 | 28 (18.7) | 1 (3.6) | - | 29 (19.3) | 0 (0) | 0 (0) | 29 (19.3) | - |
| Sroka et al [124] | 2010 | Cross sectional | Brazil | 963 | Dec-44 | - | 661 (68.6) | 5 (0.5) | - | - | - | - | 666 (69.1) | MEIA |
| Tamer et al [125] | 2009 | Retrospecrive Cross sectional | Turkey | 1972 | - | 28.56 | 952 (48.3) | 8 (0.4) | 31 (1.6) | 991 (50.2) | 0 (0) | 0 (0) | 991 (50.2) | ELISA |
| Teweldemedhin et al [126] | 2019 | Cross sectional | Ethiopia | 360 | 15 - 49 | - | 117 (32.5) | - | 11 (3.1) | 41 (36) | 42 (32.3) | 45 (38.8) | 128 (35.5) | ELISA |
| Uysal et al [127] | 2013 | Retrospective crosssectional | Turkey | 4691 | 15 - 45 | - | 1871 (39.9) | 0 (0) | 48 (1.02) | 1919 (41) | 0 (0) | 0 (0) | 1919 (41) | ELISAVIDAS |
| van Enter et al [128] | 2017 | Retrospective crosssectional | Thailand | 199 | 16 - 46 | 26 | - | - | - | - | - | - | 63 (31.7) | ELISA |
| Vueba et al [129] | 2020 | Cross sectional | Angola | 878 | 15 - 47 | 29.7 | 346 (39.4) | 0 (0) | 2 (0.2) | 97 (35.2) | 148 (39.1) | 103 (45.7) | 348 (39.6) | ECL |
| Yasmeen et al [130] | 2017 | Cross sectional | India | 251 | 18 - 35 | - | 53 (21.1) | - | - | - | - | - | 53 (21.1) | ELISA |
| Zemene et al [131] | 2012 | Cross sectional | Ethiopia | 201 | 17 - 35 | 23.64 | 163 (81.1) | 2 (1) | 3 (1.5) | 23 (79.3) | 86 (82.7) | 59 86.8) | 168 (83.6) | ELISA |
| Adeniyi et al [7] | 2023 | Cross sectional | Nigeria | 320 | 14 - 50 | - | 76 (23.75) | 35 (10.94) | - | - | - | - | 111 (34.69) | RDT |
| ALANAZI et al [3] | 2017 | Prospective Crosssectional | Saudi Arabia | 461 | 16 - 45 | 26.3 | 189 (40.9) | 0 (0) | - | 8 (21.6) | 77 (37.3) | 104 (47.7) | 189 (40.99) | ELISA |
| Aleem et al [17] | 2018 | Cross sectional | Pakistan | 360 | 18 - 33 | - | - | - | - | 71 (61.7) | 59 (58.4) | 40 (27.7) | 170 (47.2) | LAT |
| Ballah et al [8] | 2017 | Prospective Crosssectional | Nigeria | 400 | 15 - 49 | - | - | - | - | 38 (21.3) | 57 (33.5) | 17 (32.7) | 112 (28) | ELISA |
| Cédric et al [22] | 2022 | Cross sectional | Cameroon | 117 | 14 - 40 | - | 27 (23.1) | 1 (0) | 2 (1.7) | 3 (20) | 27 (30) | 0 (0) | 28 (24) | - |
| Dawet et al [14] | 2022 | Cross sectional | Nigeria | 356 | 15 - 49 | - | 105 (29.5) | - | - | 25 (27.78) | 55 (26.57) | 25 (42.37) | 105 (29.5) | ELISA |
| Khan et al [21] | 2018 | Cross sectional | Pakistan | 150 | 20 – 50< | - | 1 (0.6) | 1 (0.6) | - | - | - | - | 2 (1.32) | RDT |
| Lushina et al [132] | 2023 | Cross sectional | Tanzania | 383 | - | - | 102 (26.6) | 2 (0.52) | - | 25 (31.3) | 40 (26) | 39 (29.2) | 104 (27.2) | - |
| Murebwayire et al [133] | 2017 | Cross sectional | Rwanda | 384 | 18 - 45 | 27 | 37 (9.6) | 15 (3.9) | 5 (1.3) | 8 (10) | 26 (12.6) | 13 13.4) | 47 (12.2) | ELISA |
| Nadia et al [134] | 2023 | Cross sectional | Cameroon | 242 | 16 - 46 | - | 152 (62.8) | 28 (11.6) | 20 (8.3) | 79 (75.2) | 77 (80.2) | 24 (58.5) | 200 (82.7) | ELISA |
| Negero et al [135] | 2017 | Cross sectional | Ethiopia | 210 | 15 - 44 | - | - | - | - | 20 (74) | 62 (77.5) | 77 (74.8) | 159 (75.7) | LAT |
| Paul et al [136] | 2018 | Cross sectional | Tanzania | 254 | - | 29.9 | 102 (40.2) | 23 (9.1) | 12 (4.7) | - | - | - | 113 (44.5) | ELISA |
| Shah et al [137] | 2017 | Cross sectional | Pakistan | 100 | 17 - 36 | - | 7 (7) | 12 (12) | 7 (7) | 2 (6.45) | 3 (8.82) | 7 (20) | 12 (12) | RDT |
| Song et al [138] | 2005 | Cross sectional | Korea | 5725 | 20 - 40 | - | - | - | - | - | - | - | 51 (0.88) | ELISA/LAT |
Results
Following initial searching using valid databases and manual reviewing (Checking references of peer-reviewed articles), 1443 (PubMed (125), ScienceDirect (28), Scopus (308), Web of Sciences (WoS) (515), Embase (367), and Google Scholar (100) and 15 articles were selected in other resources, respectively (n:1458 in total). 898 duplicate articles were merged using EndNote software. During primary and secondary screenings, 560 and 411 studies were excluded, respectively and 11 low-quality articles were ignored. Finally, 138 eligible studies were included for data extraction (Fig. 1 and Table 2).
Fig. 1.
Flowchart of PRISMA criteria (2020) indicating the stages of article selection
Meta-analysis
In the review of 138 studies with a sample size of 135,098 prgnant women individuals, heterogeneity index was found high (I2:98.9); thus, random effect model was used for data analysis. The overall seroprevalence of Toxoplasma gondii in pregnant women was found 36.6% (95%CI:33.7–39.6) (Fig. 2). Also, Egger test showed no publication bias among the studies (p:0.088) (Fig. 3).
Fig. 2.

Forest plot of TP seroprevalence based on random effect model. TP: Toxoplasmosis in pregnant
Fig. 3.
Funnel plot representing distribution bias in selected eligible studies
Meta-regression analysis
Meta-regression analysis showed that following the increase in sample size (Fig. 4) and year of paper publication (Fig. 5), the seroprevalence of Toxoplasma gondii in pregnant women decreased significantly (p < 0.05).
Fig. 4.
Meta-regression represents the effect of sample size on the prevalence of Toxoplasma in pregnant women
Fig. 5.
Meta-regression represents the effect of the year of publication on the prevalence of Toxoplasma serum in pregnant women
Subgroup analysis
According to the results of Table 3, which reports the Global seroprevalence of Toxoplasma gondii in pregnant women by continent, the highest prevalence reported based on meta-analysis was reported in South America with 52.8% (95% CI:46.6–59), while only 15 studies were reviewed in this continent, most of which were in Brazil. Therefore, after the continent, the highest prevalence reported was reported in Africa with 46.8% (95% CI:39.5–54.3). Also, the lowest prevalence reported based on meta-analysis was in North America with 19.7% (95% CI:8.4–39.6) and Europe with 24.6% (95% CI:17.8–32.9) (Table 3).
Table 3.
Global seroprevalence of Toxoplasma gondii in pregnant women by continent
| Continent | N | Sample size | Heterogenicity (I2) | Egger test | Prevalence (95% CI) |
|---|---|---|---|---|---|
| Africa | 47 | 14,579 | 98.4 | 0.345 | 46.8 (95% CI:39.5–54.3) |
| Asia | 64 | 84,001 | 98.9 | 0.385 | 29.4 (95% CI:25.9–33.1) |
| Europe | 9 | 18,257 | 99.1 | 0.150 | 24.6 (95% CI:17.8–32.9) |
| North America | 3 | 3514 | 98.8 | 0.256 | 19.7 (95% CI:8.4–39.6) |
| South America | 15 | 14,747 | 97.8 | 0.408 | 52.8 (95% CI:46.6–59) |
Discussion
This systematic review and meta-analysis study investigated the global seroprevalence of Toxoplasma gondii in pregnant women. In this regard, 138 eligible studies with the sample size of 135,098 prgnant women individuals were examined. The overall seroprevalence of Toxoplasma gondii in pregnant women was found 36.6%, the highest prevalence reported based on meta-analysis was reported in South America with 52.8%, while only 15 studies were reviewed in this continent, most of which were in Brazil. Therefore, after the continent, the highest prevalence reported was reported in Africa with 46.8% Also, the lowest prevalence reported based on meta-analysis was in North America with 19.7% and Europe with 24.6%.
According to the researches, Toxoplasmosis in pregnancy are mostly diagnosed in the third trimester of pregnancy [1, 4, 8, 13, 15]. This fact returns to the suppressive role of immune system in gestation, especially in third trimester [23].
However, the severity of fetal complications is higher in first months of pregnancy such as mental retardation, chorioretinitis, and blindness [3, 7, 13]. Thus, TG screening is strictly recommended for those exposed to the associated risk factors [3, 4]. The prevalence of TG infection depends on the presence of several risk factors such as living environment, education level, presence of cat in home, consumption of undercooked meat, and contact with contaminated soil. However, some other differences are associated with cultural beliefs and lifestyles [12, 17, 60, 71].
Most of the studies reported a considerable relationship between the prevalence of Toxoplasmosis and raw meat [2, 18, 31, 33, 61, 97, 134]. However, some studies reported no significant relationship in this regard [4, 23, 24, 67, 131]. These different reports also depend on the frequency of raw meat consumption and type of meat (pig, sheep) [23, 131]. According to studies, the educational status of women represents a considerable relationship with the seroprevalence of TG. Thus, a lower educational level is considered a risk factor for onset of TG in pregnant women [2, 4, 21, 24, 33, 85, 134].
Most studies reported a significant relationship between higher age and accelerated prevalence of Toxoplasmosis [4, 24, 26, 28, 31, 61, 85, 97, 131, 134]. For example, Mwambe et al. reported that the risk of TG infection in pregnant women increases by 7% in each year of the age [97]. According to studies, tropical and humid weather are important risk factors in increasing the prevalence of Toxoplasmosis in pregnant women [2, 8, 23]. In such areas, the growth and development of TG eggs are environmentally probable [2]. It should be noted that each of the above-mentioned risk factors alone has no considerable effect on Toxoplasmosis onset, however simultaneous presence of several risk factors could induce a higher rate of Toxoplasma gondii.
The most important measures are the use and benefit of primary and secondary prevention, that is, firstly, contact and disease development can be prevented and in case of contact, screening and diagnosis of the disease can be increased [139]. The primary prevention strategy includes providing educational materials on possible preventive measures that should be integrated into prenatal visits, classes, and programs [139]. Among the primary preventive measures, women should avoid sources of infection, not drink unfiltered water, and observe hand hygiene. Screening as a secondary prevention is essential for early identification of infected women. However, until screening programs are implemented, it can be said that primary prevention and the use of educational programs are much more effective in reducing the incidence [139].
Some important limitations were detected in this systematic review and meta-analysis, including non-uniformity of sample size or data and the use of different serological methods with unique sensitivity and characteristics. It is suggested that future studies in this field should consider population prevalence, as well as review interventional and diagnostic studies in this area and provide their results to researchers.
Conclusion
The overall seroprevalence of Toxoplasma gondii in pregnant women was high at 38.6% globally. Therefore, substantial efforts are needed to educate pregnant women and to implement policy measures globally. Therefore, increasing public awareness about Toxoplasma gondii and its associated risk factors is essential. In addition, rigorous health programs should be considered by health policymakers for the prevention and early detection of Toxoplasma gondii in pregnant women. In this context, screenings at specific times for pregnant women can be considered.
Acknowledgements
By Student Research Committee of Kermanshah University of Medical Sciences.
Abbreviations
- TP
Toxoplasmosis in pregnancy
- SM
Serological method
- ELISA
Enzyme-linked Immunosorbent assay
- LAT
Latex agglutination test
- CLIA
Chemiluminescence immunoassay
- ECL
Electrochemiluminescence
- IHA
Indirect hemagglutination test
- CMIA
Chemiluminescent microparticle immunoassay
- ELFA
Enzyme-linked fluorescence assay
- PCR
Polymerase chain reaction
- RDT
Rapid diagnostic test
- EIA
Enzyme-linked immunoassay
- MEIA
Microparticle enzyme-linked immunoassay
- IFA
Indirect immunofluorescence assay
- VIDAS
Vitek immunodiagnostic system
- ISAGA
Immunosorbent agglutination assay
- CEIM
Chemiluminescent enzyme immunoassay method
Authors’ contributions
NS and AR and MM contributed to the design, MM statistical analysis, and participated in most of the study steps. MM and AR and HZ and SR prepared the manuscript. MM and HZ and SHSH and AA assisted in designing the study, and helped in the, interpretation of the study. All authors have read and approved the content of the manuscript.
Funding
Not applicable.
Data availability
Datasets are available through the corresponding author upon reasonable request.
Declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Datasets are available through the corresponding author upon reasonable request.




