# Toxoplasma gondii seroprevalence among pregnant women in Africa: A systematic review and meta-analysis

Yared Mulu Gelaw, Gizachew Worku Dagnew, Getu Degu Alene, Jean-Pierre Gangneux, Florence Robert-Gangneux

► To cite this version:

Yared Mulu Gelaw, Gizachew Worku Dagnew, Getu Degu Alene, Jean-Pierre Gangneux, Florence Robert-Gangneux. Toxoplasma gondii seroprevalence among pregnant women in Africa: A systematic review and meta-analysis. PLoS Neglected Tropical Diseases, 2024, 18 (5), pp.e0012198. 10.1371/journal.pntd.0012198. [https://doi.org/10.1371/journal.pntd.0012198](https://doi.org/10.1371/journal.pntd.0012198). [hal-04605096](https://hal.science/hal-04605096)

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# Toxoplasma gondii seroprevalence among pregnant women in Africa: A systematic review and meta-analysis

Yared Mulu Gelaw, Gizachew Worku Dagnew, Getu Degu Alene, Jean-Pierre Gangneux, Florence Robert-Gangneux

► To cite this version:

Yared Mulu Gelaw, Gizachew Worku Dagnew, Getu Degu Alene, Jean-Pierre Gangneux, Florence Robert-Gangneux. Toxoplasma gondii seroprevalence among pregnant women in Africa: A systematic review and meta-analysis. PLoS Neglected Tropical Diseases, 2024, 18 (5), pp.e0012198. 10.1371/journal.pntd.0012198. [https://doi.org/10.1371/journal.pntd.0012198](https://doi.org/10.1371/journal.pntd.0012198). [hal-04605096](https:// HAL Id: )

Submitted on 7 Jun 2024

**HAL** is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire **HAL**, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

<figure><img src="image_1.png" /></figure>
<figure><img src="image_2.png" /></figure>

RESEARCH ARTICLE

# *Toxoplasma gondii* seroprevalence among pregnant women in Africa: A systematic review and meta-analysis

Yared Mulu Gelaw¹,², Gizachew Worku Dagnew¹, Getu Degu Alene¹, Jean-Pierre Gangneux², Florence Robert-Gangneux*

1 School of Public Health, College of Medicine and Health Sciences, Bahir Dar University, Bahir Dar, Ethiopia, 2 Irset (Institut de Recherche en Santé, Environnement et Travail), UMR_S 1085, Université de Rennes, CHU Rennes, Inserm, EHESP, Rennes, France

* florence.robert-gangneux@univ-rennes.fr

## Abstract

### Background

Toxoplasmosis is a serious endemic zoonotic disease caused by the protozoan parasite *Toxoplasma gondii*. *Toxoplasma* infection during pregnancy can result in congenital transmission and serious fetal and neonatal complications. This systematic review and meta-analysis aimed to assess the pooled seroprevalence of *T. gondii* infection and its determinants among pregnant women in African countries.

### Methods

All articles reporting the seroprevalence of toxoplasmosis among pregnant women in African countries and published from 2010 to 2023 were searched using various databases. The pooled prevalence of toxoplasmosis was calculated using a random-effect model. The variation between the included studies was assessed using a funnel plot and $I^2$ heterogeneity statistics. To identify the sources of heterogeneity, sub-group analysis was further conducted by country, diagnostic method, and sub-African region. The association of prevalence rates with the socio-economic level and geoclimatic parameters was also explored.

### Results

In total, 29,383 pregnant women from 60 articles were included for analysis. The pooled *T. gondii* seroprevalence was 42.89% with high heterogeneity ($I^2$ = 99.4%, P < 0.001). Sub-group analysis revealed variation by country (ranging from 2.62% in Namibia to 80.28% in Congo), diagnostic method used (from 8.66% in studies using a rapid diagnostic test to 55.69% in those using an agglutination test), and sub-African region (from 4.14% in regions of Southern Africa to 53.96 in Central Africa). Cat ownership (OR = 1.58) and the consumption of raw meat (OR = 1.50) and raw vegetables (OR = 1.48) had a statistically significant combined effect on *T. gondii* seroprevalence. No association was found between *T. gondii* prevalence and the level of income of the country or geoclimatic parameters.

<figure><img src="image_3.png" /></figure>

OPEN ACCESS

**Citation:** Mulu Gelaw Y, Worku Dagnew G, Degu Alene G, Gangneux J-P, Robert-Gangneux F (2024). *Toxoplasma gondii* seroprevalence among pregnant women in Africa: A systematic review and meta-analysis. PLoS Negl Trop Dis 18(5): e0012198. https://doi.org/10.1371/journal.pntd.0012198

**Editor:** Craig W. Roberts, University of Strathclyde, UNITED KINGDOM

**Received:** September 4, 2023

**Accepted:** May 6, 2024

**Published:** May 23, 2024

**Copyright:** © 2024 Mulu Gelaw et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

**Data Availability Statement:** All relevant data are within the manuscript and its Supporting Information files.

**Funding:** YMG received a grant (#135485R) from Campus France (https://www.campusfrance.org/fr). The funder had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.

**Competing interests:** The authors have declared that no competing interests exist.
<figure><img src="image_2.png" /></figure>

RESEARCH ARTICLE

# *Toxoplasma gondii* seroprevalence among pregnant women in Africa: A systematic review and meta-analysis

Yared Mulu Gelaw¹,², Gizachew Worku Dagnew¹, Getu Degu Alene¹, Jean-Pierre Gangneux², Florence Robert-Gangneux*

1 School of Public Health, College of Medicine and Health Sciences, Bahir Dar University, Bahir Dar, Ethiopia, 2 Irset (Institut de Recherche en Santé, Environnement et Travail), UMR_S 1085, Université de Rennes, CHU Rennes, Inserm, EHESP, Rennes, France

* florence.robert-gangneux@univ-rennes.fr

## Abstract

### Background

Toxoplasmosis is a serious endemic zoonotic disease caused by the protozoan parasite *Toxoplasma gondii*. *Toxoplasma* infection during pregnancy can result in congenital transmission and serious fetal and neonatal complications. This systematic review and meta-analysis aimed to assess the pooled seroprevalence of *T. gondii* infection and its determinants among pregnant women in African countries.

### Methods

All articles reporting the seroprevalence of toxoplasmosis among pregnant women in African countries and published from 2010 to 2023 were searched using various databases. The pooled prevalence of toxoplasmosis was calculated using a random-effect model. The variation between the included studies was assessed using a funnel plot and $I^2$ heterogeneity statistics. To identify the sources of heterogeneity, sub-group analysis was further conducted by country, diagnostic method, and sub-African region. The association of prevalence rates with the socio-economic level and geoclimatic parameters was also explored.

### Results

In total, 29,383 pregnant women from 60 articles were included for analysis. The pooled *T. gondii* seroprevalence was 42.89% with high heterogeneity ($I^2$ = 99.4%, P < 0.001). Sub-group analysis revealed variation by country (ranging from 2.62% in Namibia to 80.28% in Congo), diagnostic method used (from 8.66% in studies using a rapid diagnostic test to 55.69% in those using an agglutination test), and sub-African region (from 4.14% in regions of Southern Africa to 53.96 in Central Africa). Cat ownership (OR = 1.58) and the consumption of raw meat (OR = 1.50) and raw vegetables (OR = 1.48) had a statistically significant combined effect on *T. gondii* seroprevalence. No association was found between *T. gondii* prevalence and the level of income of the country or geoclimatic parameters.

<figure><img src="image_3.png" /></figure>

OPEN ACCESS

**Citation:** Mulu Gelaw Y, Worku Dagnew G, Degu Alene G, Gangneux J-P, Robert-Gangneux F (2024). *Toxoplasma gondii* seroprevalence among pregnant women in Africa: A systematic review and meta-analysis. PLoS Negl Trop Dis 18(5): e0012198. https://doi.org/10.1371/journal.pntd.0012198

**Editor:** Craig W. Roberts, University of Strathclyde, UNITED KINGDOM

**Received:** September 4, 2023

**Accepted:** May 6, 2024

**Published:** May 23, 2024

**Copyright:** © 2024 Mulu Gelaw et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

**Data Availability Statement:** All relevant data are within the manuscript and its Supporting Information files.

**Funding:** YMG received a grant (#135485R) from Campus France (https://www.campusfrance.org/fr). The funder had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.

**Competing interests:** The authors have declared that no competing interests exist.
## Conclusion

The prevalence of toxoplasmosis infection among pregnant women in Africa is high, particularly in Central and Eastern Africa. The determinants of prevalence are multifactorial. Therefore, efforts should be made to increase the awareness of women concerning the risk factors for toxoplasmosis.

## Author summary

*Toxoplasma gondii* is a zoonotic protozoan parasite that infects both humans and animals. *T. gondii* infection during pregnancy causes congenital transmission and serious fetal and neonatal complications. Estimating the pooled prevalence of toxoplasmosis in high-risk population groups could catch the attention of policymakers and prompt them to develop a policy brief and guidelines to reduce toxoplasmosis sequelae. In this systematic review and meta-analysis, we aimed to assess the pooled seroprevalence of *T. gondii* infection and its determinants among pregnant women in Africa. All articles reporting recent data on the seroprevalence of toxoplasmosis among pregnant women in African countries were systematically searched using various databases. Sixty articles published from 2010 to 2023 were included for analysis, representing a total of 29,383 pregnant women. The pooled prevalence of toxoplasmosis was 42.89% (95%CI: 36.75–49.03). Cat ownership and the consumption of raw meat and raw vegetables had a statistically significant effect on the seroprevalence of toxoplasmosis among pregnant women in Africa. The infection is more prevalent in countries of Central and East Africa. These findings should increase the awareness of health workers and their understanding of toxoplasmosis among pregnant women and motivate them to conduct integrated community awareness creation activities concerning the risk factors for toxoplasmosis.

## Introduction

Toxoplasmosis is an endemic zoonotic disease caused by *Toxoplasma gondii*, a protozoan parasite with a worldwide distribution [1,2]. Cats and other felids are the definitive hosts of the parasite and humans, as well as virtually all warm-blooded animals, are intermediate hosts. They are contaminated by the ingestion of food or water containing oocysts spread in the environment through cat feces [2]. Intermediate hosts undergo a systemic infection that can be controlled by an efficient Th1 immune response, but not eradicated, leading to the lifelong persistence of encysted parasites, mainly in the muscles, brain, and eyes. Therefore, the infection can also be acquired through the ingestion of contaminated meat if eaten undercooked [2–4]. When primary infection occurs in a pregnant women, *T. gondii* can be transmitted through the placental barrier, resulting in congenital infection of varying severity, depending on the stage of gestation, or loss of the fetus [2,5].

An estimated one-third of the world population is infected with *T. gondii*, which is responsible for 1.2 million disability-adjusted life years (DALYs) each year [6]. The seroprevalence of toxoplasmosis among pregnant women varies greatly between geographical areas as a result of combined factors, including the climate, socio-economic level and standard of living, quality of the drinking water, and proximity with cats or other felids. There is a trend towards a decreasing prevalence in European countries, such as France [7], likely related to
## Conclusion

The prevalence of toxoplasmosis infection among pregnant women in Africa is high, particularly in Central and Eastern Africa. The determinants of prevalence are multifactorial. Therefore, efforts should be made to increase the awareness of women concerning the risk factors for toxoplasmosis.

## Author summary

*Toxoplasma gondii* is a zoonotic protozoan parasite that infects both humans and animals. *T. gondii* infection during pregnancy causes congenital transmission and serious fetal and neonatal complications. Estimating the pooled prevalence of toxoplasmosis in high-risk population groups could catch the attention of policymakers and prompt them to develop a policy brief and guidelines to reduce toxoplasmosis sequelae. In this systematic review and meta-analysis, we aimed to assess the pooled seroprevalence of *T. gondii* infection and its determinants among pregnant women in Africa. All articles reporting recent data on the seroprevalence of toxoplasmosis among pregnant women in African countries were systematically searched using various databases. Sixty articles published from 2010 to 2023 were included for analysis, representing a total of 29,383 pregnant women. The pooled prevalence of toxoplasmosis was 42.89% (95%CI: 36.75–49.03). Cat ownership and the consumption of raw meat and raw vegetables had a statistically significant effect on the seroprevalence of toxoplasmosis among pregnant women in Africa. The infection is more prevalent in countries of Central and East Africa. These findings should increase the awareness of health workers and their understanding of toxoplasmosis among pregnant women and motivate them to conduct integrated community awareness creation activities concerning the risk factors for toxoplasmosis.

## Introduction

Toxoplasmosis is an endemic zoonotic disease caused by *Toxoplasma gondii*, a protozoan parasite with a worldwide distribution [1,2]. Cats and other felids are the definitive hosts of the parasite and humans, as well as virtually all warm-blooded animals, are intermediate hosts. They are contaminated by the ingestion of food or water containing oocysts spread in the environment through cat feces [2]. Intermediate hosts undergo a systemic infection that can be controlled by an efficient Th1 immune response, but not eradicated, leading to the lifelong persistence of encysted parasites, mainly in the muscles, brain, and eyes. Therefore, the infection can also be acquired through the ingestion of contaminated meat if eaten undercooked [2-4]. When primary infection occurs in a pregnant women, *T. gondii* can be transmitted through the placental barrier, resulting in congenital infection of varying severity, depending on the stage of gestation, or loss of the fetus [2,5].

An estimated one-third of the world population is infected with *T. gondii*, which is responsible for 1.2 million disability-adjusted life years (DALYs) each year [6]. The seroprevalence of toxoplasmosis among pregnant women varies greatly between geographical areas as a result of combined factors, including the climate, socio-economic level and standard of living, quality of the drinking water, and proximity with cats or other felids. There is a trend towards a decreasing prevalence in European countries, such as France [7], likely related to
modifications in dietary habits or food hygiene or handling. In Africa, a previous meta-analysis
estimated that more than half of African pregnant women are chronically infected with *Toxo-
plasma* [8] but the selection criteria and inclusion period were not clear. Several studies from
African countries reported high variability in *T. gondii* seroprevalence among pregnant
women, ranging from below 5 to 80% [9,10]. In a recent Egyptian review, Abbas et al. [11]
reported a seroprevalence ranging from 4 to 71% among pregnant women, depending on the
geographical location. Interestingly, it was as high as 27 to 100% among women with a history
of recent abortion, suggesting that the burden of toxoplasmosis could be higher than sus-
pected. In addition, epidemiological studies have shown that 95% of cats are seropositive for *T.
gondii*, suggesting massive contamination of the environment with oocysts.

Although there are limited country- and sub-continent-level data about *T. gondii* seroprevalence among pregnant women in Africa, there have been no studies to assess its predictors across this continent. Knowing the seroprevalence and predictors of *T. gondii* infection could help health authorities to have a better understanding of the level of risk according to local factors and design targeted intervention measures to reduce fetal sequelae related to the infection. This systematic review and meta-analysis aimed to assess the seroprevalence of *Toxoplasma gondii* infection and its predictors among pregnant women in Africa.

**Methods and materials**

**Study protocol and eligibility**

This systematic review and meta-analysis is reported using the preferred Reporting Items for Systematic Review and Meta-analysis (PRISMA) reporting checklist.

All cross-sectional and cohort observational studies conducted in various countries of Africa on the prevalence of toxoplasmosis among pregnant women published in the English language from January 1, 2010, to March 30, 2023, were included.

**Sources of information and search strategies**

We searched through various databases to retrieve pertinent findings about the prevalence of
toxoplasmosis infection among pregnant women (PubMed, Researchgate, Africa Journal
Online (AJOL), and Europe PMC using the following Mesh terms (“Toxoplasmosis” OR
“Toxoplasma gondii”), AND (“Pregnant Women” OR “Prenatal care”), AND (“Africa”) or
combining with every individual African country (S1 File).

**Study selection, data extraction, and quality assurance**

Duplicated articles were removed using Endnote X8 citation manager. Initially, all retrieved
articles were screened against the eligibility criteria via careful reading of the article title and
abstract using the CoCoPoP (Condition, Context, and Population) framework. The condition
(Co) was the prevalence of *T. gondii* and was the main outcome of interest, the study popula-
tion (Pop) was pregnant women, and the context (Co) was a study conducted in all African
countries. Articles fulfilling the inclusion criteria were included and reviewed. The eligibility
of each study was assessed by two independent investigators. The inter-rater agreement
between the two reviewers was rated using the “kappa index” tool [12] and the result showed
almost perfect agreement between them (observed agreement (Po) = 0.94, kappa coefficient (k)
= 0.832) (S2 File). Discrepancies between the two investigators were resolved by consensus
after the paper was reviewed by a third reviewer.

The reviewers independently collected data from all eligible publications using a standard-
ized form. The following data were captured and recorded using Microsoft Excel 2016: author,
modifications in dietary habits or food hygiene or handling. In Africa, a previous meta-analysis
estimated that more than half of African pregnant women are chronically infected with *Toxo-
plasma* [8] but the selection criteria and inclusion period were not clear. Several studies from
African countries reported high variability in *T. gondii* seroprevalence among pregnant
women, ranging from below 5 to 80% [9,10]. In a recent Egyptian review, Abbas et al. [11]
reported a seroprevalence ranging from 4 to 71% among pregnant women, depending on the
geographical location. Interestingly, it was as high as 27 to 100% among women with a history
of recent abortion, suggesting that the burden of toxoplasmosis could be higher than sus-
pected. In addition, epidemiological studies have shown that 95% of cats are seropositive for *T.
gondii*, suggesting massive contamination of the environment with oocysts.

Although there are limited country- and sub-continent-level data about *T. gondii* seroprevalence among pregnant women in Africa, there have been no studies to assess its predictors across this continent. Knowing the seroprevalence and predictors of *T. gondii* infection could help health authorities to have a better understanding of the level of risk according to local factors and design targeted intervention measures to reduce fetal sequelae related to the infection. This systematic review and meta-analysis aimed to assess the seroprevalence of *Toxoplasma gondii* infection and its predictors among pregnant women in Africa.

**Methods and materials**

**Study protocol and eligibility**

This systematic review and meta-analysis is reported using the preferred Reporting Items for Systematic Review and Meta-analysis (PRISMA) reporting checklist.

All cross-sectional and cohort observational studies conducted in various countries of Africa on the prevalence of toxoplasmosis among pregnant women published in the English language from January 1, 2010, to March 30, 2023, were included.

**Sources of information and search strategies**

We searched through various databases to retrieve pertinent findings about the prevalence of
toxoplasmosis infection among pregnant women (PubMed, Researchgate, Africa Journal
Online (AJOL), and Europe PMC using the following Mesh terms (“Toxoplasmosis” OR
“Toxoplasma gondii”), AND (“Pregnant Women” OR “Prenatal care”), AND (“Africa”) or
combining with every individual African country (S1 File).

**Study selection, data extraction, and quality assurance**

Duplicated articles were removed using Endnote X8 citation manager. Initially, all retrieved
articles were screened against the eligibility criteria via careful reading of the article title and
abstract using the CoCoPoP (Condition, Context, and Population) framework. The condition
(Co) was the prevalence of *T. gondii* and was the main outcome of interest, the study popula-
tion (Pop) was pregnant women, and the context (Co) was a study conducted in all African
countries. Articles fulfilling the inclusion criteria were included and reviewed. The eligibility
of each study was assessed by two independent investigators. The inter-rater agreement
between the two reviewers was rated using the “kappa index” tool [12] and the result showed
almost perfect agreement between them (observed agreement (Po) = 0.94, kappa coefficient (k)
= 0.832) (S2 File). Discrepancies between the two investigators were resolved by consensus
after the paper was reviewed by a third reviewer.

The reviewers independently collected data from all eligible publications using a standard-
ized form. The following data were captured and recorded using Microsoft Excel 2016: author,
year of publication, country, study subject, study design, sample population, number of cases (participants with an outcome), diagnostic tool/method, and prevalence. The quality of the included studies and the risk of bias were critically evaluated using the revised Joanna Briggs Institute (JBI) eight-item critical appraisal tool to assess the quality of observational studies (analytical cross-sectional studies) [13] (S3 File). The quality ranking of each full extracted article was scored as low (≤ 3 of 8), medium (between 3 and 6 of 8), or high (≥ 6 of 8). To reduce the risk of bias, we only included articles with higher quality assessment scores.

## Strategy of data analysis

Data were imported to Stata version 15.1 from a Microsoft Excel sheet for analysis. The pooled prevalence of toxoplasmosis, with the 95% confidence interval (95%CI), was determined using a random effect model. Heterogeneity between the included studies was examined using I² statistics. Heterogeneity is considered when the p-value of I² is < 0.05. I² statistics results of 25, 50, and 75% represent low, moderate, and high heterogeneity, respectively. An Egger regression asymmetry test for meta-analysis was used to assess publication bias. An Egger test p-value < 0.05 shows the presence of publication bias. Subgroup analysis and meta-regression were performed to verify the sources of heterogeneity. Moreover, sensitivity analysis was carried out to ensure the robustness of the result and to determine the influence of a single study. To assess the influence of a single study, the pooled prevalence was calculated leaving one study out at a time.

Data on potential predictor variables such as residence, cat ownership, the consumption of raw meat or raw vegetables, the drinking of raw milk, contact with soil, a history of blood transfusion, and HIV status were recorded and analyzed.

## Results

In total, 189 articles were initially identified from various electronic databases, of which 74 were removed due to duplication. After screening using the article title and abstract, 82 articles were selected for full retrieval. Twenty-two were further excluded due to the inability to retrieve the full text of the article, the use of a language other than English, or an inadequate target population, outcome, or diagnostic method. Finally, 60 articles were included for analysis (Fig 1).

## Characteristics of included studies

In total, 60 full document articles published between January 1, 2010, and March 30, 2023, from 19 different African countries were included in this systematic review and meta-analysis [10,14–73]. Approximately half (48.4%) of the included studies were from three countries: Ethiopia (14 studies), Nigeria (9 studies), and Tanzania (6 studies). In terms of the sub-regions of Africa, most of the included articles were from East Africa (28 studies) or West Africa (17 studies). In total, 29,383 pregnant women were included. An average of 490 pregnant women were included in each study, ranging from 90 in a Nigerian study [64] to 5,578 in one from Morocco [21]. Most studies (87.1%) used a cross-sectional study design. The presence of anti-Toxoplasma gondii antibodies was assessed by enzyme-immunoassay (EIA) (48 studies), agglutination tests (AT) (10 studies), or rapid diagnostic tests (RDTs) (2 studies) (Table 1).

## Toxoplasma seroprevalence among pregnant women in Africa

Across the 60 studies included in this systematic review, the prevalence of toxoplasmosis in pregnant women ranged from 2.61% in Namibia [9] to 88.6% in Ethiopia [61]. The pooled
year of publication, country, study subject, study design, sample population, number of cases (participants with an outcome), diagnostic tool/method, and prevalence. The quality of the included studies and the risk of bias were critically evaluated using the revised Joanna Briggs Institute (JBI) eight-item critical appraisal tool to assess the quality of observational studies (analytical cross-sectional studies) [13] (S3 File). The quality ranking of each full extracted article was scored as low (≤ 3 of 8), medium (between 3 and 6 of 8), or high (≥ 6 of 8). To reduce the risk of bias, we only included articles with higher quality assessment scores.

## Strategy of data analysis

Data were imported to Stata version 15.1 from a Microsoft Excel sheet for analysis. The pooled prevalence of toxoplasmosis, with the 95% confidence interval (95%CI), was determined using a random effect model. Heterogeneity between the included studies was examined using I² statistics. Heterogeneity is considered when the p-value of I² is < 0.05. I² statistics results of 25, 50, and 75% represent low, moderate, and high heterogeneity, respectively. An Egger regression asymmetry test for meta-analysis was used to assess publication bias. An Egger test p-value < 0.05 shows the presence of publication bias. Subgroup analysis and meta-regression were performed to verify the sources of heterogeneity. Moreover, sensitivity analysis was carried out to ensure the robustness of the result and to determine the influence of a single study. To assess the influence of a single study, the pooled prevalence was calculated leaving one study out at a time.

Data on potential predictor variables such as residence, cat ownership, the consumption of raw meat or raw vegetables, the drinking of raw milk, contact with soil, a history of blood transfusion, and HIV status were recorded and analyzed.

## Results

In total, 189 articles were initially identified from various electronic databases, of which 74 were removed due to duplication. After screening using the article title and abstract, 82 articles were selected for full retrieval. Twenty-two were further excluded due to the inability to retrieve the full text of the article, the use of a language other than English, or an inadequate target population, outcome, or diagnostic method. Finally, 60 articles were included for analysis (Fig 1).

## Characteristics of included studies

In total, 60 full document articles published between January 1, 2010, and March 30, 2023, from 19 different African countries were included in this systematic review and meta-analysis [10,14–73]. Approximately half (48.4%) of the included studies were from three countries: Ethiopia (14 studies), Nigeria (9 studies), and Tanzania (6 studies). In terms of the sub-regions of Africa, most of the included articles were from East Africa (28 studies) or West Africa (17 studies). In total, 29,383 pregnant women were included. An average of 490 pregnant women were included in each study, ranging from 90 in a Nigerian study [64] to 5,578 in one from Morocco [21]. Most studies (87.1%) used a cross-sectional study design. The presence of anti-Toxoplasma gondii antibodies was assessed by enzyme-immunoassay (EIA) (48 studies), agglutination tests (AT) (10 studies), or rapid diagnostic tests (RDTs) (2 studies) (Table 1).

## Toxoplasma seroprevalence among pregnant women in Africa

Across the 60 studies included in this systematic review, the prevalence of toxoplasmosis in pregnant women ranged from 2.61% in Namibia [9] to 88.6% in Ethiopia [61]. The pooled
<figure><img src="image_4.png" /><figcaption>Fig 1. PRISMA flow diagram of the studies included in the systematic review and meta-analysis using the updated 2020 PRISMA flow diagram.</figcaption></figure>

https://doi.org/10.1371/journal.pntd.0012198.g001

prevalence of toxoplasmosis was 42.12% (95%CI: 36.01–48.22). I² statistics showed the presence of heterogeneity (I² = 99.3%, 95%CI: 98.7% - 99.6%, P < 0.001) (Fig 2). Cochran’s Q statistic was 9127.26, with a p-value < 0.001, and the test of overall effect was 0 (z = 13.524, p < 0.001). Subgroup analysis was thus carried out to identify the sources of heterogeneity.

## Publication bias

The funnel plot and bias coefficient (Egger's test; b = 35.2%, 95%CI: 9.6–60.9, P = 0.008) for studies published on *T. gondii* seroprevalence among pregnant women in Africa confirmed the presence of publication bias and a small-study effect. The results of trim analysis also revealed the presence of publication bias (Q = 14.162 on 61 degrees of freedom (p = 1.000) and Moment-based estimate of between-study variance = 0.000), with a pooled estimate of 3.299, 95%CI: 2.826–3.773, p-value < 0.001) (Fig 3).

## Sub-group analysis

Sub-group analysis was conducted using the following variables: country, sub-African region, publication period, serological method, and type of study design. Sub-group analysis by country showed the highest mean seroprevalence to be observed in Congo (80.28%), followed by 64.28% in Ethiopia, whereas the lowest was 2.62% in Namibia and 5.84% in Zambia (Table 2). The results of country-level I² statistics showed the presence of heterogeneity between studies of the same country, except for the studies included in Sudan (I² = 65.1%, P = 0.057). On the other hand, the sub-group analysis by Sub-African region showed the highest prevalence of
<figure><img src="image_4.png" /><figcaption>Fig 1. PRISMA flow diagram of the studies included in the systematic review and meta-analysis using the updated 2020 PRISMA flow diagram.</figcaption></figure>

https://doi.org/10.1371/journal.pntd.0012198.g001

prevalence of toxoplasmosis was 42.12% (95%CI: 36.01–48.22). I² statistics showed the presence of heterogeneity (I² = 99.3%, 95%CI: 98.7% - 99.6%, P < 0.001) (Fig 2). Cochran’s Q statistic was 9127.26, with a p-value < 0.001, and the test of overall effect was 0 (z = 13.524, p < 0.001). Subgroup analysis was thus carried out to identify the sources of heterogeneity.

## Publication bias

The funnel plot and bias coefficient (Egger's test; b = 35.2%, 95%CI: 9.6–60.9, P = 0.008) for studies published on *T. gondii* seroprevalence among pregnant women in Africa confirmed the presence of publication bias and a small-study effect. The results of trim analysis also revealed the presence of publication bias (Q = 14.162 on 61 degrees of freedom (p = 1.000) and Moment-based estimate of between-study variance = 0.000), with a pooled estimate of 3.299, 95%CI: 2.826–3.773, p-value < 0.001) (Fig 3).

## Sub-group analysis

Sub-group analysis was conducted using the following variables: country, sub-African region, publication period, serological method, and type of study design. Sub-group analysis by country showed the highest mean seroprevalence to be observed in Congo (80.28%), followed by 64.28% in Ethiopia, whereas the lowest was 2.62% in Namibia and 5.84% in Zambia (Table 2). The results of country-level I² statistics showed the presence of heterogeneity between studies of the same country, except for the studies included in Sudan (I² = 65.1%, P = 0.057). On the other hand, the sub-group analysis by Sub-African region showed the highest prevalence of
<table><caption>Table 1. Characteristics of the 60 studies included in the systematic review and meta-analysis to estimate the seroprevalence of toxoplasmosis among pregnant women in Africa.</caption><thead><tr><td>First author, year</td><td>Reference no</td><td>Country</td><td>Study design</td><td>Sample size</td><td>Number of seropositive women</td><td>Prevalence (%)</td><td>Diagnostic tool</td><td>Quality score</td></tr></thead><tbody><tr><td>Hassan SA et al., 2023</td><td>14</td><td>Somalia</td><td>CS</td><td>403</td><td>182</td><td>45.16</td><td>EIA</td><td>6</td></tr><tr><td>Okojokwu O et al., 2023</td><td>15</td><td>Nigeria</td><td>CS</td><td>158</td><td>44</td><td>27.8</td><td>EIA</td><td>7</td></tr><tr><td>Dambrun M et al., 2022</td><td>16</td><td>Benin</td><td>RS</td><td>974</td><td>512</td><td>52.56</td><td>EIA</td><td>8</td></tr><tr><td>Lushina M et al., 2022</td><td>17</td><td>Tanzania</td><td>CS</td><td>383</td><td>104</td><td>27.15</td><td>EIA</td><td>8</td></tr><tr><td>Laboudi M et al., 2021</td><td>18</td><td>Morocco</td><td>RS</td><td>637</td><td>274</td><td>43</td><td>EIA</td><td>6</td></tr><tr><td>Adugna B et al., 2021</td><td>19</td><td>Ethiopia</td><td>CS</td><td>401</td><td>284</td><td>70.82</td><td>AT</td><td>6</td></tr><tr><td>Singh B et al., 2021</td><td>20</td><td>Ghana</td><td>CS</td><td>400</td><td>229</td><td>57.25</td><td>EIA</td><td>8</td></tr><tr><td>Hoummadi L et al., 2020</td><td>21</td><td>Morocco</td><td>RS</td><td>5578</td><td>1611</td><td>28.88</td><td>EIA</td><td>6</td></tr><tr><td>Khames M et al., 2020</td><td>72</td><td>Algeria</td><td>CS</td><td>1012</td><td>252</td><td>24.9</td><td>EIA</td><td>6</td></tr><tr><td>Akubuilo AS et al., 2020</td><td>22</td><td>Nigeria</td><td>CS</td><td>384</td><td>45</td><td>11.72</td><td>RDT</td><td>6</td></tr><tr><td>Van der Colf BE et al., 2020</td><td>9</td><td>Namibia</td><td>CS</td><td>344</td><td>9</td><td>2.62</td><td>EIA</td><td>7</td></tr><tr><td>Zakari, M et al., 2020</td><td>24</td><td>Nigeria</td><td>CS</td><td>320</td><td>92</td><td>28.75</td><td>EIA</td><td>7</td></tr><tr><td>Mulugeta et al., 2020</td><td>25</td><td>Ethiopia</td><td>CS</td><td>233</td><td>158</td><td>67.81</td><td>AT</td><td>8</td></tr><tr><td>Tecle AS et al., 2020</td><td>26</td><td>Eritrea</td><td>CS</td><td>210</td><td>112</td><td>53.33</td><td>EIA</td><td>6</td></tr><tr><td>Nguemaïm NF et al., 2020</td><td>27</td><td>Cameroon</td><td>CS</td><td>127</td><td>44</td><td>34.65</td><td>EIA</td><td>7</td></tr><tr><td>Abdelbaset AE et al., 2020</td><td>28</td><td>Egypt</td><td>CS</td><td>96</td><td>22</td><td>22.92</td><td>EIA</td><td>6</td></tr><tr><td>Fenta., 2019</td><td>29</td><td>Ethiopia</td><td>CS</td><td>500</td><td>409</td><td>81.8</td><td>EIA</td><td>8</td></tr><tr><td>Teweldemedihin et al., 2019</td><td>30</td><td>Ethiopia</td><td>CS</td><td>360</td><td>128</td><td>35.56</td><td>EIA</td><td>8</td></tr><tr><td>Mirambo MM.et al., 2019</td><td>31</td><td>Tanzania</td><td>CS</td><td>300</td><td>92</td><td>30.67</td><td>EIA</td><td>7</td></tr><tr><td>Todjom FG et al., 2019</td><td>32</td><td>Cameroon</td><td>CS</td><td>200</td><td>91</td><td>45.5</td><td>EIA</td><td>7</td></tr><tr><td>Mabeku LB et al., 2018</td><td>33</td><td>Cameroon</td><td>CS</td><td>643</td><td>230</td><td>35.77</td><td>EIA</td><td>7</td></tr><tr><td>Jula et al., 2018</td><td>34</td><td>Ethiopia</td><td>CS</td><td>401</td><td>96</td><td>23.94</td><td>EIA</td><td>7</td></tr><tr><td>Adeniyi OT et al., 2018</td><td>35</td><td>Nigeria</td><td>CS</td><td>391</td><td>119</td><td>30.43</td><td>EIA</td><td>7</td></tr><tr><td>Hafez Hassanain et al., 2018</td><td>73</td><td>Egypt</td><td>CS</td><td>388</td><td>79</td><td>20.36</td><td>EIA</td><td>6</td></tr><tr><td>Dairo MD et al., 2018</td><td>37</td><td>Nigeria</td><td>CS</td><td>377</td><td>135</td><td>35.81</td><td>EIA</td><td>8</td></tr><tr><td>Mohammed WM et al., 2018</td><td>38</td><td>Sudan</td><td>CS</td><td>300</td><td>68</td><td>22.67</td><td>EIA</td><td>6</td></tr><tr><td>Paul et al., 2018</td><td>39</td><td>Tanzania</td><td>CS</td><td>254</td><td>113</td><td>44.49</td><td>EIA</td><td>7</td></tr><tr><td>Tlamcani Z et al., 2017</td><td>40</td><td>Morocco</td><td>PS</td><td>3440</td><td>1367</td><td>39.74</td><td>EIA</td><td>6</td></tr><tr><td>Pegha Moukandja et al., 2017</td><td>41</td><td>Gabon</td><td>RS</td><td>973</td><td>557</td><td>57.25</td><td>EIA</td><td>6</td></tr><tr><td>El-Shqanqery HE et al., 2017</td><td>42</td><td>Egypt</td><td>CS</td><td>693</td><td>209</td><td>30.16</td><td>EIA</td><td>6</td></tr><tr><td>Frimpong et al., 2017</td><td>43</td><td>Zambia</td><td>CS</td><td>411</td><td>24</td><td>5.84</td><td>RDT</td><td>8</td></tr><tr><td>Ballah F et al., 2017</td><td>44</td><td>Nigeria</td><td>CS</td><td>400</td><td>112</td><td>28</td><td>EIA</td><td>7</td></tr><tr><td>Murebwayire E et al., 2017</td><td>45</td><td>Rwanda</td><td>CS</td><td>384</td><td>47</td><td>12.24</td><td>EIA</td><td>8</td></tr><tr><td>Saajan AM et al., 2017</td><td>46</td><td>Tanzania</td><td>CS</td><td>347</td><td>154</td><td>44.38</td><td>EIA</td><td>6</td></tr><tr><td>Bamba et al., 2017</td><td>47</td><td>Burkina Faso</td><td>CS</td><td>316</td><td>98</td><td>31</td><td>AT</td><td>8</td></tr><tr><td>Negussie A et al., 2017</td><td>48</td><td>Ethiopia</td><td>CS</td><td>301</td><td>105</td><td>34.88</td><td>AT</td><td>7</td></tr><tr><td>Yohanes T et al., 2017</td><td>49</td><td>Ethiopia</td><td>CS</td><td>232</td><td>184</td><td>79.31</td><td>EIA</td><td>8</td></tr><tr><td>Negero et al., 2017</td><td>50</td><td>Ethiopia</td><td>CS</td><td>210</td><td>159</td><td>75.71</td><td>AT</td><td>8</td></tr><tr><td>Völker et al., 2017</td><td>51</td><td>Ghana</td><td>CS</td><td>168</td><td>123</td><td>73.21</td><td>EIA</td><td>7</td></tr><tr><td>Oboro IL et al., 2016</td><td>52</td><td>Nigeria</td><td>CS</td><td>288</td><td>189</td><td>65.62</td><td>EIA</td><td>6</td></tr><tr><td>Abamecha et al., 2016</td><td>53</td><td>Ethiopia</td><td>CS</td><td>232</td><td>198</td><td>85.34</td><td>EIA</td><td>8</td></tr><tr><td>Ayi I et al., 2016</td><td>54</td><td>Ghana</td><td>CS</td><td>125</td><td>64</td><td>51.2</td><td>EIA</td><td>6</td></tr></tbody></table>

(Continued)
<table><caption>Table 1. Characteristics of the 60 studies included in the systematic review and meta-analysis to estimate the seroprevalence of toxoplasmosis among pregnant women in Africa.</caption><thead><tr><td>First author, year</td><td>Reference no</td><td>Country</td><td>Study design</td><td>Sample size</td><td>Number of seropositive women</td><td>Prevalence (%)</td><td>Diagnostic tool</td><td>Quality score</td></tr></thead><tbody><tr><td>Hassan SA et al., 2023</td><td>14</td><td>Somalia</td><td>CS</td><td>403</td><td>182</td><td>45.16</td><td>EIA</td><td>6</td></tr><tr><td>Okojokwu O et al., 2023</td><td>15</td><td>Nigeria</td><td>CS</td><td>158</td><td>44</td><td>27.8</td><td>EIA</td><td>7</td></tr><tr><td>Dambrun M et al., 2022</td><td>16</td><td>Benin</td><td>RS</td><td>974</td><td>512</td><td>52.56</td><td>EIA</td><td>8</td></tr><tr><td>Lushina M et al., 2022</td><td>17</td><td>Tanzania</td><td>CS</td><td>383</td><td>104</td><td>27.15</td><td>EIA</td><td>8</td></tr><tr><td>Laboudi M et al., 2021</td><td>18</td><td>Morocco</td><td>RS</td><td>637</td><td>274</td><td>43</td><td>EIA</td><td>6</td></tr><tr><td>Adugna B et al., 2021</td><td>19</td><td>Ethiopia</td><td>CS</td><td>401</td><td>284</td><td>70.82</td><td>AT</td><td>6</td></tr><tr><td>Singh B et al., 2021</td><td>20</td><td>Ghana</td><td>CS</td><td>400</td><td>229</td><td>57.25</td><td>EIA</td><td>8</td></tr><tr><td>Hoummadi L et al., 2020</td><td>21</td><td>Morocco</td><td>RS</td><td>5578</td><td>1611</td><td>28.88</td><td>EIA</td><td>6</td></tr><tr><td>Khames M et al., 2020</td><td>72</td><td>Algeria</td><td>CS</td><td>1012</td><td>252</td><td>24.9</td><td>EIA</td><td>6</td></tr><tr><td>Akubuilo AS et al., 2020</td><td>22</td><td>Nigeria</td><td>CS</td><td>384</td><td>45</td><td>11.72</td><td>RDT</td><td>6</td></tr><tr><td>Van der Colf BE et al., 2020</td><td>9</td><td>Namibia</td><td>CS</td><td>344</td><td>9</td><td>2.62</td><td>EIA</td><td>7</td></tr><tr><td>Zakari, M et al., 2020</td><td>24</td><td>Nigeria</td><td>CS</td><td>320</td><td>92</td><td>28.75</td><td>EIA</td><td>7</td></tr><tr><td>Mulugeta et al., 2020</td><td>25</td><td>Ethiopia</td><td>CS</td><td>233</td><td>158</td><td>67.81</td><td>AT</td><td>8</td></tr><tr><td>Tecle AS et al., 2020</td><td>26</td><td>Eritrea</td><td>CS</td><td>210</td><td>112</td><td>53.33</td><td>EIA</td><td>6</td></tr><tr><td>Nguemaïm NF et al., 2020</td><td>27</td><td>Cameroon</td><td>CS</td><td>127</td><td>44</td><td>34.65</td><td>EIA</td><td>7</td></tr><tr><td>Abdelbaset AE et al., 2020</td><td>28</td><td>Egypt</td><td>CS</td><td>96</td><td>22</td><td>22.92</td><td>EIA</td><td>6</td></tr><tr><td>Fenta., 2019</td><td>29</td><td>Ethiopia</td><td>CS</td><td>500</td><td>409</td><td>81.8</td><td>EIA</td><td>8</td></tr><tr><td>Teweldemedihin et al., 2019</td><td>30</td><td>Ethiopia</td><td>CS</td><td>360</td><td>128</td><td>35.56</td><td>EIA</td><td>8</td></tr><tr><td>Mirambo MM.et al., 2019</td><td>31</td><td>Tanzania</td><td>CS</td><td>300</td><td>92</td><td>30.67</td><td>EIA</td><td>7</td></tr><tr><td>Todjom FG et al., 2019</td><td>32</td><td>Cameroon</td><td>CS</td><td>200</td><td>91</td><td>45.5</td><td>EIA</td><td>7</td></tr><tr><td>Mabeku LB et al., 2018</td><td>33</td><td>Cameroon</td><td>CS</td><td>643</td><td>230</td><td>35.77</td><td>EIA</td><td>7</td></tr><tr><td>Jula et al., 2018</td><td>34</td><td>Ethiopia</td><td>CS</td><td>401</td><td>96</td><td>23.94</td><td>EIA</td><td>7</td></tr><tr><td>Adeniyi OT et al., 2018</td><td>35</td><td>Nigeria</td><td>CS</td><td>391</td><td>119</td><td>30.43</td><td>EIA</td><td>7</td></tr><tr><td>Hafez Hassanain et al., 2018</td><td>73</td><td>Egypt</td><td>CS</td><td>388</td><td>79</td><td>20.36</td><td>EIA</td><td>6</td></tr><tr><td>Dairo MD et al., 2018</td><td>37</td><td>Nigeria</td><td>CS</td><td>377</td><td>135</td><td>35.81</td><td>EIA</td><td>8</td></tr><tr><td>Mohammed WM et al., 2018</td><td>38</td><td>Sudan</td><td>CS</td><td>300</td><td>68</td><td>22.67</td><td>EIA</td><td>6</td></tr><tr><td>Paul et al., 2018</td><td>39</td><td>Tanzania</td><td>CS</td><td>254</td><td>113</td><td>44.49</td><td>EIA</td><td>7</td></tr><tr><td>Tlamcani Z et al., 2017</td><td>40</td><td>Morocco</td><td>PS</td><td>3440</td><td>1367</td><td>39.74</td><td>EIA</td><td>6</td></tr><tr><td>Pegha Moukandja et al., 2017</td><td>41</td><td>Gabon</td><td>RS</td><td>973</td><td>557</td><td>57.25</td><td>EIA</td><td>6</td></tr><tr><td>El-Shqanqery HE et al., 2017</td><td>42</td><td>Egypt</td><td>CS</td><td>693</td><td>209</td><td>30.16</td><td>EIA</td><td>6</td></tr><tr><td>Frimpong et al., 2017</td><td>43</td><td>Zambia</td><td>CS</td><td>411</td><td>24</td><td>5.84</td><td>RDT</td><td>8</td></tr><tr><td>Ballah F et al., 2017</td><td>44</td><td>Nigeria</td><td>CS</td><td>400</td><td>112</td><td>28</td><td>EIA</td><td>7</td></tr><tr><td>Murebwayire E et al., 2017</td><td>45</td><td>Rwanda</td><td>CS</td><td>384</td><td>47</td><td>12.24</td><td>EIA</td><td>8</td></tr><tr><td>Saajan AM et al., 2017</td><td>46</td><td>Tanzania</td><td>CS</td><td>347</td><td>154</td><td>44.38</td><td>EIA</td><td>6</td></tr><tr><td>Bamba et al., 2017</td><td>47</td><td>Burkina Faso</td><td>CS</td><td>316</td><td>98</td><td>31</td><td>AT</td><td>8</td></tr><tr><td>Negussie A et al., 2017</td><td>48</td><td>Ethiopia</td><td>CS</td><td>301</td><td>105</td><td>34.88</td><td>AT</td><td>7</td></tr><tr><td>Yohanes T et al., 2017</td><td>49</td><td>Ethiopia</td><td>CS</td><td>232</td><td>184</td><td>79.31</td><td>EIA</td><td>8</td></tr><tr><td>Negero et al., 2017</td><td>50</td><td>Ethiopia</td><td>CS</td><td>210</td><td>159</td><td>75.71</td><td>AT</td><td>8</td></tr><tr><td>Völker et al., 2017</td><td>51</td><td>Ghana</td><td>CS</td><td>168</td><td>123</td><td>73.21</td><td>EIA</td><td>7</td></tr><tr><td>Oboro IL et al., 2016</td><td>52</td><td>Nigeria</td><td>CS</td><td>288</td><td>189</td><td>65.62</td><td>EIA</td><td>6</td></tr><tr><td>Abamecha et al., 2016</td><td>53</td><td>Ethiopia</td><td>CS</td><td>232</td><td>198</td><td>85.34</td><td>EIA</td><td>8</td></tr><tr><td>Ayi I et al., 2016</td><td>54</td><td>Ghana</td><td>CS</td><td>125</td><td>64</td><td>51.2</td><td>EIA</td><td>6</td></tr></tbody></table>

(Continued)
<table><caption>**Table 1.** (Continued)</caption><thead><tr><th>First author, year</th><th>Reference no</th><th>Country</th><th>Study design</th><th>Sample size</th><th>Number of seropositive women</th><th>Prevalence (%)</th><th>Diagnostic tool</th><th>Quality score</th></tr></thead><tbody><tr><td>Kwofie KD et al., 2016</td><td>55</td><td>Ghana</td><td>CS</td><td>100</td><td>38</td><td>38</td><td>EIA</td><td>6</td></tr><tr><td>Awoke K et al., 2015</td><td>56</td><td>Ethiopia</td><td>CS</td><td>384</td><td>71</td><td>18.49</td><td>AT</td><td>8</td></tr><tr><td>Nasir IA et al., 2015</td><td>57</td><td>Nigeria</td><td>CS</td><td>360</td><td>176</td><td>48.89</td><td>EIA</td><td>6</td></tr><tr><td>Gelaye et al., 2015</td><td>10</td><td>Ethiopia</td><td>CS</td><td>288</td><td>246</td><td>85.42</td><td>AT</td><td>8</td></tr><tr><td>Agmas et al., 2015</td><td>58</td><td>Ethiopia</td><td>CS</td><td>263</td><td>180</td><td>68.44</td><td>AT</td><td>8</td></tr><tr><td>Elichilia R Shao et al., 2015</td><td>59</td><td>Tanzania</td><td>CS</td><td>144</td><td>60</td><td>41.67</td><td>EIA</td><td>8</td></tr><tr><td>Doudou et al., 2014</td><td>60</td><td>Congo</td><td>CS</td><td>781</td><td>627</td><td>80.28</td><td>EIA</td><td>6</td></tr><tr><td>Endris M et al., 2014</td><td>61</td><td>Ethiopia</td><td>CS</td><td>385</td><td>341</td><td>88.57</td><td>AT</td><td>8</td></tr><tr><td>Bamba S et al., 2014</td><td>62</td><td>Burkina Faso</td><td>CS</td><td>348</td><td>121</td><td>34.77</td><td>EIA</td><td>6</td></tr><tr><td>Abdel-Raouff M et al., 2014</td><td>63</td><td>Sudan</td><td>CS</td><td>163</td><td>33</td><td>20.25</td><td>EIA</td><td>6</td></tr><tr><td>Oyinloye SO et al., 2014</td><td>64</td><td>Nigeria</td><td>CS</td><td>90</td><td>20</td><td>22.22</td><td>EIA</td><td>6</td></tr><tr><td>Mwambe et al., 2013</td><td>65</td><td>Tanzania</td><td>CS</td><td>350</td><td>108</td><td>30.86</td><td>EIA</td><td>8</td></tr><tr><td>EI Deeb et al., 2012</td><td>66</td><td>Egypt</td><td>CS</td><td>323</td><td>218</td><td>67.49</td><td>EIA</td><td>6</td></tr><tr><td>Zemene et al., 2012</td><td>67</td><td>Ethiopia</td><td>CS</td><td>201</td><td>168</td><td>83.58</td><td>EIA</td><td>7</td></tr><tr><td>Linguissi et al., 2012</td><td>68</td><td>Burkina Faso</td><td>RS</td><td>182</td><td>37</td><td>20.33</td><td>EIA</td><td>6</td></tr><tr><td>Sattti, A.B et al., 2011</td><td>69</td><td>Sudan</td><td>PS</td><td>455</td><td>72</td><td>15.82</td><td>AT</td><td>6</td></tr><tr><td>Njunda AL et al., 2011</td><td>70</td><td>Cameroon</td><td>CS</td><td>110</td><td>77</td><td>70</td><td>EIA</td><td>7</td></tr><tr><td>Sitoe et al., 2010</td><td>71</td><td>Mozambique</td><td>CS</td><td>150</td><td>28</td><td>18.67</td><td>EIA</td><td>6</td></tr></tbody></table>

CS: cross-cectional ctudy, RS: retrospective study, PS: prospective study EIA: enzyme immunoassay, AT: agglutination test, RDT: rapid diagnostic test

https://doi.org/10.1371/journal.pntd.0012198.t001

toxoplasmosis to be in Central Africa (53.96%, 95%CI: 37.30–70.63) and the lowest in the South African region (4.14%, 95%CI: 0.98–7.29). As indicated by overlapping of the 95%CI, there was a significant difference between the South African region and other sub-African regions (Table 2).

## Sensitivity analysis

We further investigated the sources of heterogeneity in the pooled *T. gondii* seroprevalence in Africa and ensured the robustness of the data by performing a sensitivity analysis. The removal of each study one by one and subsequent calculation of the pooled prevalence showed the seroprevalence of toxoplasmosis among pregnant women to vary between 42.11% (95%CI: 36.20–48.01) following the removal of the study of Endris et al. (2014) [61] and 43.58% (95%CI: 37.73, 49.42) following the removal of that of Van der Colf et al. (2020) [9]. Based on this analysis, we concluded that our estimation of the pooled prevalence was robust and showed no evidence in favor of a single-study influence (S4 File).

Of the 19 countries with documented seroprevalence among pregnant women from 2010 onwards, six had a seroprevalence of < 25%, five of 25% to 45%, and eight of > 45% (Table 3 and Fig 4). Half of the countries with a *Toxoplasma* prevalence > 45% were low-income countries (Table 3). However, 4/6 countries with a seroprevalence < 25%, were also low-income countries, showing that poverty cannot solely explain the risk of *Toxoplasma* exposure.

We found no association between *Toxoplasma* seroprevalence and geographical features, such as the type of climate, average elevation, or annual rainfall observed in the countries (Table 4).

## Factors associated with *T. gondii* seroprevalence

The meta-analysis was performed on 38 of the 60 included articles with eight identified potential predictor variables. The results show that pregnant women who own a cat (OR = 1.584,
<table><caption>**Table 1.** (Continued)</caption><thead><tr><th>First author, year</th><th>Reference no</th><th>Country</th><th>Study design</th><th>Sample size</th><th>Number of seropositive women</th><th>Prevalence (%)</th><th>Diagnostic tool</th><th>Quality score</th></tr></thead><tbody><tr><td>Kwofie KD et al., 2016</td><td>55</td><td>Ghana</td><td>CS</td><td>100</td><td>38</td><td>38</td><td>EIA</td><td>6</td></tr><tr><td>Awoke K et al., 2015</td><td>56</td><td>Ethiopia</td><td>CS</td><td>384</td><td>71</td><td>18.49</td><td>AT</td><td>8</td></tr><tr><td>Nasir IA et al., 2015</td><td>57</td><td>Nigeria</td><td>CS</td><td>360</td><td>176</td><td>48.89</td><td>EIA</td><td>6</td></tr><tr><td>Gelaye et al., 2015</td><td>10</td><td>Ethiopia</td><td>CS</td><td>288</td><td>246</td><td>85.42</td><td>AT</td><td>8</td></tr><tr><td>Agmas et al., 2015</td><td>58</td><td>Ethiopia</td><td>CS</td><td>263</td><td>180</td><td>68.44</td><td>AT</td><td>8</td></tr><tr><td>Elichilia R Shao et al., 2015</td><td>59</td><td>Tanzania</td><td>CS</td><td>144</td><td>60</td><td>41.67</td><td>EIA</td><td>8</td></tr><tr><td>Doudou et al., 2014</td><td>60</td><td>Congo</td><td>CS</td><td>781</td><td>627</td><td>80.28</td><td>EIA</td><td>6</td></tr><tr><td>Endris M et al., 2014</td><td>61</td><td>Ethiopia</td><td>CS</td><td>385</td><td>341</td><td>88.57</td><td>AT</td><td>8</td></tr><tr><td>Bamba S et al., 2014</td><td>62</td><td>Burkina Faso</td><td>CS</td><td>348</td><td>121</td><td>34.77</td><td>EIA</td><td>6</td></tr><tr><td>Abdel-Raouff M et al., 2014</td><td>63</td><td>Sudan</td><td>CS</td><td>163</td><td>33</td><td>20.25</td><td>EIA</td><td>6</td></tr><tr><td>Oyinloye SO et al., 2014</td><td>64</td><td>Nigeria</td><td>CS</td><td>90</td><td>20</td><td>22.22</td><td>EIA</td><td>6</td></tr><tr><td>Mwambe et al., 2013</td><td>65</td><td>Tanzania</td><td>CS</td><td>350</td><td>108</td><td>30.86</td><td>EIA</td><td>8</td></tr><tr><td>Ei Deeb et al., 2012</td><td>66</td><td>Egypt</td><td>CS</td><td>323</td><td>218</td><td>67.49</td><td>EIA</td><td>6</td></tr><tr><td>Zemene et al., 2012</td><td>67</td><td>Ethiopia</td><td>CS</td><td>201</td><td>168</td><td>83.58</td><td>EIA</td><td>7</td></tr><tr><td>Linguissi et al., 2012</td><td>68</td><td>Burkina Faso</td><td>RS</td><td>182</td><td>37</td><td>20.33</td><td>EIA</td><td>6</td></tr><tr><td>Sattti, A.B et al., 2011</td><td>69</td><td>Sudan</td><td>PS</td><td>455</td><td>72</td><td>15.82</td><td>AT</td><td>6</td></tr><tr><td>Njunda AL et al., 2011</td><td>70</td><td>Cameroon</td><td>CS</td><td>110</td><td>77</td><td>70</td><td>EIA</td><td>7</td></tr><tr><td>Sitoe et al., 2010</td><td>71</td><td>Mozambique</td><td>CS</td><td>150</td><td>28</td><td>18.67</td><td>EIA</td><td>6</td></tr></tbody></table>

CS: cross-cectional ctudy, RS: retrospective study, PS: prospective study EIA: enzyme immunoassay, AT: agglutination test, RDT: rapid diagnostic test

https://doi.org/10.1371/journal.pntd.0012198.t001

toxoplasmosis to be in Central Africa (53.96%, 95%CI: 37.30–70.63) and the lowest in the South African region (4.14%, 95%CI: 0.98–7.29). As indicated by overlapping of the 95%CI, there was a significant difference between the South African region and other sub-African regions (Table 2).

## Sensitivity analysis

We further investigated the sources of heterogeneity in the pooled *T. gondii* seroprevalence in Africa and ensured the robustness of the data by performing a sensitivity analysis. The removal of each study one by one and subsequent calculation of the pooled prevalence showed the seroprevalence of toxoplasmosis among pregnant women to vary between 42.11% (95%CI: 36.20–48.01) following the removal of the study of Endris et al. (2014) [61] and 43.58% (95%CI: 37.73, 49.42) following the removal of that of Van der Colf et al. (2020) [9]. Based on this analysis, we concluded that our estimation of the pooled prevalence was robust and showed no evidence in favor of a single-study influence (S4 File).

Of the 19 countries with documented seroprevalence among pregnant women from 2010 onwards, six had a seroprevalence of < 25%, five of 25% to 45%, and eight of > 45% (Table 3 and Fig 4). Half of the countries with a *Toxoplasma* prevalence > 45% were low-income countries (Table 3). However, 4/6 countries with a seroprevalence < 25%, were also low-income countries, showing that poverty cannot solely explain the risk of *Toxoplasma* exposure.

We found no association between *Toxoplasma* seroprevalence and geographical features, such as the type of climate, average elevation, or annual rainfall observed in the countries (Table 4).

## Factors associated with *T. gondii* seroprevalence

The meta-analysis was performed on 38 of the 60 included articles with eight identified potential predictor variables. The results show that pregnant women who own a cat (OR = 1.584,
<figure><img src="image_5.png" /><figcaption>Fig 2. Pooled prevalence of toxoplasmosis among pregnant women in Africa (n = 60 articles included, references #9,10, 14–73).</figcaption></figure>

https://doi.org/10.1371/journal.pntd.0012198.g002
<figure><img src="image_5.png" /><figcaption>Fig 2. Pooled prevalence of toxoplasmosis among pregnant women in Africa (n = 60 articles included, references #9,10, 14–73).</figcaption></figure>

https://doi.org/10.1371/journal.pntd.0012198.g002
<figure><img src="image_6.png" /><figcaption>**Fig 3.** Funnel plot (A), Egger publication bias plot (B) of the logit event rate, and filled funnel plot of the logit event rate (C) of toxoplasmosis among pregnant women in Africa.</figcaption></figure>

https://doi.org/10.1371/journal.pntd.0012198.g003

95%CI: 1.288–1.948) or consume raw meat (OR = 1.741, 95%CI:1.176–1.842) or raw vegetables (OR = 1.476, 95%CI: 1.079–2.018) were more likely to be seropositive for *Toxoplasma*, with an overall effect, P < 0.05 (Table 5).

Discussion

Africa is a continent with a multicultural community that has highly varying living conditions and feeding habits, a high prevalence of communicable diseases, including HIV/AIDS, and most often a low and traditional agriculture-dependent economy level, which can favor the seroprevalence of toxoplasmosis. This systematic review and meta-analysis is the first to assess the predictive factors for *T. gondii* chronic infection among pregnant women in Africa. We did not report the pooled prevalence of acute infection because of the unavailability of clearly stated data (IgM or IgG avidity results) in most of the included studies. Nonetheless, the estimation of the prevalence of chronic infection is a widely recognized indicator of parasite circulation in a given population.

We observed a 42% pooled seroprevalence of *T. gondii* infection. The I² statistics results showed the presence of heterogeneity and Egger's test and trim analysis revealed the presence of publication bias. However, based on the sensitivity analysis, the value for the pooled seroprevalence is robust and high, suggesting a potentially high impact on pregnancy outcomes due to the possible transmission of infection to the fetus. A high level of congenital toxoplasmosis has already been reported for Northern Africa [74–75] but it is still widely unrecognized in sub-Saharan Africa. Recent epidemiological studies reported recombinant and atypical
<figure><img src="image_6.png" /><figcaption>**Fig 3.** Funnel plot (A), Egger publication bias plot (B) of the logit event rate, and filled funnel plot of the logit event rate (C) of toxoplasmosis among pregnant women in Africa.</figcaption></figure>

https://doi.org/10.1371/journal.pntd.0012198.g003

95%CI: 1.288–1.948) or consume raw meat (OR = 1.741, 95%CI:1.176–1.842) or raw vegetables (OR = 1.476, 95%CI: 1.079–2.018) were more likely to be seropositive for *Toxoplasma*, with an overall effect, P < 0.05 (Table 5).

Discussion

Africa is a continent with a multicultural community that has highly varying living conditions and feeding habits, a high prevalence of communicable diseases, including HIV/AIDS, and most often a low and traditional agriculture-dependent economy level, which can favor the seroprevalence of toxoplasmosis. This systematic review and meta-analysis is the first to assess the predictive factors for *T. gondii* chronic infection among pregnant women in Africa. We did not report the pooled prevalence of acute infection because of the unavailability of clearly stated data (IgM or IgG avidity results) in most of the included studies. Nonetheless, the estimation of the prevalence of chronic infection is a widely recognized indicator of parasite circulation in a given population.

We observed a 42% pooled seroprevalence of *T. gondii* infection. The I² statistics results showed the presence of heterogeneity and Egger's test and trim analysis revealed the presence of publication bias. However, based on the sensitivity analysis, the value for the pooled seroprevalence is robust and high, suggesting a potentially high impact on pregnancy outcomes due to the possible transmission of infection to the fetus. A high level of congenital toxoplasmosis has already been reported for Northern Africa [74–75] but it is still widely unrecognized in sub-Saharan Africa. Recent epidemiological studies reported recombinant and atypical
<table><caption>Table 2. Sub-group analysis for the seroprevalence of toxoplasmosis among pregnant women in Africa.</caption><thead><tr><th rowspan="2">Sub-group</th><th rowspan="2">No. of included studies</th><th rowspan="2">Total sample size</th><th rowspan="2">Prevalence (95%CI)</th><th colspan="3">Heterogeneity statistics</th></tr><tr><th>Cochran's Q</th><th>I<sup>2</sup></th><th>P-value</th></tr></thead><tbody><tr><td colspan="7"><strong>By Country</strong></td></tr><tr><td>Somalia</td><td>1</td><td>403</td><td>45.16 (40.30–50.02)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Nigeria</td><td>09</td><td>2768</td><td>33.27 (22.42–44.11)</td><td>347.52</td><td>97.7%</td><td>0.000</td></tr><tr><td>Benin</td><td>1</td><td>974</td><td>52.57 (49.43–55.70)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Tanzania</td><td>06</td><td>1778</td><td>36.30 (29.87–42.72)</td><td>41.63</td><td>88.0%</td><td>0.000</td></tr><tr><td>Morocco</td><td>03</td><td>9655</td><td>37.10 (28.23–45.97)</td><td>137.08</td><td>98.5%</td><td>0.000</td></tr><tr><td>Ethiopia</td><td>14</td><td>4391</td><td>64.26 (50.35–78.18)</td><td>1758.89</td><td>99.3%</td><td>0.000</td></tr><tr><td>Ghana</td><td>04</td><td>793</td><td>55.26 (42.37–68.15)</td><td>39.21</td><td>92.3%</td><td>0.000</td></tr><tr><td>Eritrea</td><td>01</td><td>210</td><td>53.33 (46.59–60.08)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Namibia</td><td>01</td><td>344</td><td>2.62 (0.93–4.30)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Algeria</td><td>01</td><td>1012</td><td>24.90 (22.24–27.57)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Cameroon</td><td>04</td><td>1080</td><td>46.25 (32.25–60.24)</td><td>55.60</td><td>94.6%</td><td>0.000</td></tr><tr><td>Egypt</td><td>04</td><td>1500</td><td>35.28 (15.07–55.49)</td><td>221.13</td><td>98.6</td><td>0.000</td></tr><tr><td>Sudan</td><td>03</td><td>918</td><td>19.26 (14.72–23.80)</td><td>5.72</td><td>65.1%</td><td>0.057</td></tr><tr><td>Burkina Faso</td><td>03</td><td>846</td><td>28.83 (20.71–36.95)</td><td>14.05</td><td>85.8%</td><td>0.001</td></tr><tr><td>Gabon</td><td>01</td><td>973</td><td>57.25 (54.14–60.35)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Zambia</td><td>01</td><td>411</td><td>5.84 (3.57–8.11)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Rwanda</td><td>01</td><td>384</td><td>12.24 (8.96–15.52)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Congo</td><td>01</td><td>781</td><td>80.28 (77.49–83.07)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Mozambique</td><td>01</td><td>150</td><td>18.67 (12.43–24.90)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td colspan="7"><strong>By Sub-African Region</strong></td></tr><tr><td>East Africa</td><td>27</td><td>9234</td><td>48.41 (37.50–59.32)</td><td>3859.33</td><td>99.3%</td><td>0.000</td></tr><tr><td>West Africa</td><td>17</td><td>5381</td><td>38.66 (30.32–47.01)</td><td>736.5</td><td>97.8%</td><td>0.000</td></tr><tr><td>North Africa</td><td>08</td><td>12167</td><td>34.72 (27.74–41.71)</td><td>393.12</td><td>98.2%</td><td>0.000</td></tr><tr><td>Central Africa</td><td>06</td><td>2831</td><td>53.96 (37.30–70.63)</td><td>428.52</td><td>98.8%</td><td>0.000</td></tr><tr><td>South Africa</td><td>02</td><td>755</td><td>4.14 (0.98–7.29)</td><td>5.00</td><td>80.0%</td><td>0.025</td></tr><tr><td colspan="7"><strong>By diagnostic method</strong></td></tr><tr><td>EIA</td><td>48</td><td>25340</td><td>41.65 (35.51–47.79)</td><td>5851.67</td><td>99.2%</td><td>0.000</td></tr><tr><td>AT</td><td>10</td><td>3236</td><td>55.69 (36.07–75.31)</td><td>1781.96</td><td>99.5%</td><td>0.000</td></tr><tr><td>RDT</td><td>02</td><td>795</td><td>8.66 (2.91–14.42)</td><td>8.57</td><td>88.3%</td><td>0.003</td></tr><tr><td colspan="7"><strong>By type of study design</strong></td></tr><tr><td>Cross-sectional study</td><td>53</td><td>17132</td><td>43.70 (36.01–51.39)</td><td>8594.62</td><td>99.4%</td><td>0.000</td></tr><tr><td>Retrospective study</td><td>05</td><td>8344</td><td>40.49 (26.71–54.26)</td><td>459.76</td><td>99.1%</td><td>0.000</td></tr><tr><td>Prospective study</td><td>02</td><td>3895</td><td>27.83 (4.39–51.26)</td><td>157.82</td><td>99.4%</td><td>0.000</td></tr></tbody></table>

EIA: enzyme immunoassay, AT: agglutination test, RDT: rapid diagnostic test

https://doi.org/10.1371/journal.pntd.0012198.t002

*Toxoplasma* genotypes in severe cases of congenital toxoplasmosis in Tunisia [76–77], as well as in breeding animals [78], showing the circulation of virulent genotypes. Little is known about the distribution of circulating genotypes in sub-Saharan Africa and their virulence. To date, a virulent genotype, Africa-1, has been identified in a few immunocompetent travelers returning to France from Senegal, the Ivory Coast, and the Republic of Congo presenting with fever, myalgia, and neurological signs [79]. These observations suggest that severe congenital cases are likely to occur in sub-Saharan Africa. Knowledge acquired from South America showed that virulent atypical strains can be responsible for fetal loss at any stage of pregnancy and for severe sequelae [80]. In Africa, the presence of virulent genotypes may also be
<table><caption>Table 2. Sub-group analysis for the seroprevalence of toxoplasmosis among pregnant women in Africa.</caption><thead><tr><th rowspan="2">Sub-group</th><th rowspan="2">No. of included studies</th><th rowspan="2">Total sample size</th><th rowspan="2">Prevalence (95%CI)</th><th colspan="3">Heterogeneity statistics</th></tr><tr><th>Cochran's Q</th><th>I<sup>2</sup></th><th>P-value</th></tr></thead><tbody><tr><td colspan="7"><strong>By Country</strong></td></tr><tr><td>Somalia</td><td>1</td><td>403</td><td>45.16 (40.30–50.02)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Nigeria</td><td>09</td><td>2768</td><td>33.27 (22.42–44.11)</td><td>347.52</td><td>97.7%</td><td>0.000</td></tr><tr><td>Benin</td><td>1</td><td>974</td><td>52.57 (49.43–55.70)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Tanzania</td><td>06</td><td>1778</td><td>36.30 (29.87–42.72)</td><td>41.63</td><td>88.0%</td><td>0.000</td></tr><tr><td>Morocco</td><td>03</td><td>9655</td><td>37.10 (28.23–45.97)</td><td>137.08</td><td>98.5%</td><td>0.000</td></tr><tr><td>Ethiopia</td><td>14</td><td>4391</td><td>64.26 (50.35–78.18)</td><td>1758.89</td><td>99.3%</td><td>0.000</td></tr><tr><td>Ghana</td><td>04</td><td>793</td><td>55.26 (42.37–68.15)</td><td>39.21</td><td>92.3%</td><td>0.000</td></tr><tr><td>Eritrea</td><td>01</td><td>210</td><td>53.33 (46.59–60.08)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Namibia</td><td>01</td><td>344</td><td>2.62 (0.93–4.30)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Algeria</td><td>01</td><td>1012</td><td>24.90 (22.24–27.57)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Cameroon</td><td>04</td><td>1080</td><td>46.25 (32.25–60.24)</td><td>55.60</td><td>94.6%</td><td>0.000</td></tr><tr><td>Egypt</td><td>04</td><td>1500</td><td>35.28 (15.07–55.49)</td><td>221.13</td><td>98.6</td><td>0.000</td></tr><tr><td>Sudan</td><td>03</td><td>918</td><td>19.26 (14.72–23.80)</td><td>5.72</td><td>65.1%</td><td>0.057</td></tr><tr><td>Burkina Faso</td><td>03</td><td>846</td><td>28.83 (20.71–36.95)</td><td>14.05</td><td>85.8%</td><td>0.001</td></tr><tr><td>Gabon</td><td>01</td><td>973</td><td>57.25 (54.14–60.35)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Zambia</td><td>01</td><td>411</td><td>5.84 (3.57–8.11)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Rwanda</td><td>01</td><td>384</td><td>12.24 (8.96–15.52)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Congo</td><td>01</td><td>781</td><td>80.28 (77.49–83.07)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td>Mozambique</td><td>01</td><td>150</td><td>18.67 (12.43–24.90)</td><td>0.00</td><td>---</td><td>---</td></tr><tr><td colspan="7"><strong>By Sub-African Region</strong></td></tr><tr><td>East Africa</td><td>27</td><td>9234</td><td>48.41 (37.50–59.32)</td><td>3859.33</td><td>99.3%</td><td>0.000</td></tr><tr><td>West Africa</td><td>17</td><td>5381</td><td>38.66 (30.32–47.01)</td><td>736.5</td><td>97.8%</td><td>0.000</td></tr><tr><td>North Africa</td><td>08</td><td>12167</td><td>34.72 (27.74–41.71)</td><td>393.12</td><td>98.2%</td><td>0.000</td></tr><tr><td>Central Africa</td><td>06</td><td>2831</td><td>53.96 (37.30–70.63)</td><td>428.52</td><td>98.8%</td><td>0.000</td></tr><tr><td>South Africa</td><td>02</td><td>755</td><td>4.14 (0.98–7.29)</td><td>5.00</td><td>80.0%</td><td>0.025</td></tr><tr><td colspan="7"><strong>By diagnostic method</strong></td></tr><tr><td>EIA</td><td>48</td><td>25340</td><td>41.65 (35.51–47.79)</td><td>5851.67</td><td>99.2%</td><td>0.000</td></tr><tr><td>AT</td><td>10</td><td>3236</td><td>55.69 (36.07–75.31)</td><td>1781.96</td><td>99.5%</td><td>0.000</td></tr><tr><td>RDT</td><td>02</td><td>795</td><td>8.66 (2.91–14.42)</td><td>8.57</td><td>88.3%</td><td>0.003</td></tr><tr><td colspan="7"><strong>By type of study design</strong></td></tr><tr><td>Cross-sectional study</td><td>53</td><td>17132</td><td>43.70 (36.01–51.39)</td><td>8594.62</td><td>99.4%</td><td>0.000</td></tr><tr><td>Retrospective study</td><td>05</td><td>8344</td><td>40.49 (26.71–54.26)</td><td>459.76</td><td>99.1%</td><td>0.000</td></tr><tr><td>Prospective study</td><td>02</td><td>3895</td><td>27.83 (4.39–51.26)</td><td>157.82</td><td>99.4%</td><td>0.000</td></tr></tbody></table>

EIA: enzyme immunoassay, AT: agglutination test, RDT: rapid diagnostic test

https://doi.org/10.1371/journal.pntd.0012198.t002

Toxoplasma genotypes in severe cases of congenital toxoplasmosis in Tunisia [76–77], as well as in breeding animals [78], showing the circulation of virulent genotypes. Little is known about the distribution of circulating genotypes in sub-Saharan Africa and their virulence. To date, a virulent genotype, Africa-1, has been identified in a few immunocompetent travelers returning to France from Senegal, the Ivory Coast, and the Republic of Congo presenting with fever, myalgia, and neurological signs [79]. These observations suggest that severe congenital cases are likely to occur in sub-Saharan Africa. Knowledge acquired from South America showed that virulent atypical strains can be responsible for fetal loss at any stage of pregnancy and for severe sequelae [80]. In Africa, the presence of virulent genotypes may also be
<table><caption>Table 3. Characteristics of the 19 African countries (60 articles included).</caption><thead><tr><th>Country</th><th>Prevalence<br>(%, 95%CI)</th><th>African geographical<br>area</th><th>Average elevation<br>(m)</th><th>Annual average<br>precipitation (mm)</th><th>Climate</th><th>GDP per capita<br>(USD, 2022)<sup>a</sup></th><th>Income<br>group<br>(World<br>Bank)</th></tr></thead><tbody><tr><td>Somalia</td><td>45.16 (40.30–<br>50.02)</td><td>East</td><td>410</td><td>282</td><td>Arid</td><td>470</td><td>Low</td></tr><tr><td>Nigeria</td><td>33.27 (22.42–<br>44.11)</td><td>West</td><td>380</td><td>1150</td><td>Mixt</td><td>2140</td><td>Lower-<br>middle</td></tr><tr><td>Benin</td><td>52.57 (49.43–<br>55.70)</td><td>West</td><td>273</td><td>1039</td><td>Tropical</td><td>1400</td><td>Lower<br>-middle</td></tr><tr><td>Tanzania</td><td>36.30 (29.87–<br>42.72)</td><td>East</td><td>1018</td><td>1071</td><td>Tropical</td><td>1200</td><td>Lower<br>-middle</td></tr><tr><td>Morocco</td><td>37.10 (28.23–<br>45.97)</td><td>North</td><td>909</td><td>346</td><td>Mixt</td><td>3710</td><td>Lower-<br>middle</td></tr><tr><td>Ethiopia</td><td>64.26 (50.35–<br>78.18)</td><td>East</td><td>1330</td><td>848</td><td>Tropical</td><td>1020</td><td>Low</td></tr><tr><td>Ghana</td><td>55.26 (42.37–<br>68.15)</td><td>West</td><td>190</td><td>1187</td><td>Tropical</td><td>2350</td><td>Lower<br>-middle</td></tr><tr><td>Eritrea</td><td>53.33 (46.59–<br>60.08)</td><td>East</td><td>853</td><td>384</td><td>Mixt</td><td>646</td><td>Low</td></tr><tr><td>Namibia</td><td>2.62 (0.93–4.30)</td><td>South</td><td>1141</td><td>285</td><td>Arid</td><td>4880</td><td>Upper-<br>middle</td></tr><tr><td>Algeria</td><td>24.90 (22.24–<br>27.57)</td><td>North</td><td>800</td><td>89</td><td>Mixt</td><td>3900</td><td>Lower<br>-middle</td></tr><tr><td>Cameroon</td><td>46.25 (32.25–<br>60.24)</td><td>West</td><td>667</td><td>1604</td><td>Tropical</td><td>1660</td><td>Lower<br>-middle</td></tr><tr><td>Egypt</td><td>35.28 (15.07–<br>55.49)</td><td>North</td><td>321</td><td>18</td><td>Arid</td><td>4100</td><td>Lower<br>-middle</td></tr><tr><td>Sudan</td><td>19.26 (14.72–<br>23.80)</td><td>East</td><td>568</td><td>250</td><td>Arid</td><td>760</td><td>Low</td></tr><tr><td>Burkina Faso</td><td>28.83 (20.71–<br>36.95)</td><td>West</td><td>297</td><td>748</td><td>Arid</td><td>840</td><td>Low</td></tr><tr><td>Gabon</td><td>57.25 (54.14–<br>60.35)</td><td>Central</td><td>377</td><td>1831</td><td>Tropical</td><td>7540</td><td>Upper-<br>middle</td></tr><tr><td>Zambia</td><td>5.84 (3.57–8.11)</td><td>Central</td><td>1138</td><td>1020</td><td>Tropical</td><td>1170</td><td>Low</td></tr><tr><td>Rwanda</td><td>12.24 (8.96–<br>15.52)</td><td>East</td><td>1598</td><td>1212</td><td>Tropical</td><td>930</td><td>Low</td></tr><tr><td>Democratic Republic of<br>Congo</td><td>80.28 (77.49–<br>83.07)</td><td>Central</td><td>726</td><td>1543</td><td>Tropical</td><td>590</td><td>Low</td></tr><tr><td>Mozambique</td><td>18.67 (12.43–<br>24.90)</td><td>South</td><td>345</td><td>1032</td><td>Tropical</td><td>500</td><td>Low</td></tr></tbody></table>

associated with a high burden of disease. In the absence of documentation, these cases are probably not diagnosed. A major study by Mercier et al. [81] showed that nearly half of *Toxoplasma* strains isolated from domestic animals in Gabon were identified as Africa-1 or Africa-3 genotypes, both highly virulent in mice, with a lethal outcome in > 90% of animals. Their phylogenetic analysis concluded that African and American strains share a common ancestor. Thus, given the high observed pooled seroprevalence, it would be of great interest to better evaluate the burden of toxoplasmosis in humans in Africa.

Similar seroprevalence estimates have been reported in systematic reviews conducted on pregnant women in Iran (43%) [82], the general population in Iran (39.3%) [83], and pregnant

<footnote>ª Income level of African country (World Bank 2022–2023): low ≤ 1,085 USD; low-middle = 1,086–4,255 USD; upper middle income = 4,256–13,205, high ≥ 13,205</footnote>
<table><caption>Table 3. Characteristics of the 19 African countries (60 articles included).</caption><thead><tr><th>Country</th><th>Prevalence<br>(%, 95%CI)</th><th>African geographical<br>area</th><th>Average elevation<br>(m)</th><th>Annual average<br>precipitation (mm)</th><th>Climate</th><th>GDP per capita<br>(USD, 2022)<sup>a</sup></th><th>Income<br>group<br>(World<br>Bank)</th></tr></thead><tbody><tr><td>Somalia</td><td>45.16 (40.30–<br>50.02)</td><td>East</td><td>410</td><td>282</td><td>Arid</td><td>470</td><td>Low</td></tr><tr><td>Nigeria</td><td>33.27 (22.42–<br>44.11)</td><td>West</td><td>380</td><td>1150</td><td>Mixt</td><td>2140</td><td>Lower-<br>middle</td></tr><tr><td>Benin</td><td>52.57 (49.43–<br>55.70)</td><td>West</td><td>273</td><td>1039</td><td>Tropical</td><td>1400</td><td>Lower<br>-middle</td></tr><tr><td>Tanzania</td><td>36.30 (29.87–<br>42.72)</td><td>East</td><td>1018</td><td>1071</td><td>Tropical</td><td>1200</td><td>Lower<br>-middle</td></tr><tr><td>Morocco</td><td>37.10 (28.23–<br>45.97)</td><td>North</td><td>909</td><td>346</td><td>Mixt</td><td>3710</td><td>Lower-<br>middle</td></tr><tr><td>Ethiopia</td><td>64.26 (50.35–<br>78.18)</td><td>East</td><td>1330</td><td>848</td><td>Tropical</td><td>1020</td><td>Low</td></tr><tr><td>Ghana</td><td>55.26 (42.37–<br>68.15)</td><td>West</td><td>190</td><td>1187</td><td>Tropical</td><td>2350</td><td>Lower<br>-middle</td></tr><tr><td>Eritrea</td><td>53.33 (46.59–<br>60.08)</td><td>East</td><td>853</td><td>384</td><td>Mixt</td><td>646</td><td>Low</td></tr><tr><td>Namibia</td><td>2.62 (0.93–4.30)</td><td>South</td><td>1141</td><td>285</td><td>Arid</td><td>4880</td><td>Upper-<br>middle</td></tr><tr><td>Algeria</td><td>24.90 (22.24–<br>27.57)</td><td>North</td><td>800</td><td>89</td><td>Mixt</td><td>3900</td><td>Lower<br>-middle</td></tr><tr><td>Cameroon</td><td>46.25 (32.25–<br>60.24)</td><td>West</td><td>667</td><td>1604</td><td>Tropical</td><td>1660</td><td>Lower<br>-middle</td></tr><tr><td>Egypt</td><td>35.28 (15.07–<br>55.49)</td><td>North</td><td>321</td><td>18</td><td>Arid</td><td>4100</td><td>Lower<br>-middle</td></tr><tr><td>Sudan</td><td>19.26 (14.72–<br>23.80)</td><td>East</td><td>568</td><td>250</td><td>Arid</td><td>760</td><td>Low</td></tr><tr><td>Burkina Faso</td><td>28.83 (20.71–<br>36.95)</td><td>West</td><td>297</td><td>748</td><td>Arid</td><td>840</td><td>Low</td></tr><tr><td>Gabon</td><td>57.25 (54.14–<br>60.35)</td><td>Central</td><td>377</td><td>1831</td><td>Tropical</td><td>7540</td><td>Upper-<br>middle</td></tr><tr><td>Zambia</td><td>5.84 (3.57–8.11)</td><td>Central</td><td>1138</td><td>1020</td><td>Tropical</td><td>1170</td><td>Low</td></tr><tr><td>Rwanda</td><td>12.24 (8.96–<br>15.52)</td><td>East</td><td>1598</td><td>1212</td><td>Tropical</td><td>930</td><td>Low</td></tr><tr><td>Democratic Republic of<br>Congo</td><td>80.28 (77.49–<br>83.07)</td><td>Central</td><td>726</td><td>1543</td><td>Tropical</td><td>590</td><td>Low</td></tr><tr><td>Mozambique</td><td>18.67 (12.43–<br>24.90)</td><td>South</td><td>345</td><td>1032</td><td>Tropical</td><td>500</td><td>Low</td></tr></tbody></table>

associated with a high burden of disease. In the absence of documentation, these cases are probably not diagnosed. A major study by Mercier et al. [81] showed that nearly half of *Toxoplasma* strains isolated from domestic animals in Gabon were identified as Africa-1 or Africa-3 genotypes, both highly virulent in mice, with a lethal outcome in > 90% of animals. Their phylogenetic analysis concluded that African and American strains share a common ancestor. Thus, given the high observed pooled seroprevalence, it would be of great interest to better evaluate the burden of toxoplasmosis in humans in Africa.

Similar seroprevalence estimates have been reported in systematic reviews conducted on pregnant women in Iran (43%) [82], the general population in Iran (39.3%) [83], and pregnant

<footnote>ª Income level of African country (World Bank 2022–2023): low ≤ 1,085 USD; low-middle = 1,086–4,255 USD; upper middle income = 4,256–13,205, high ≥ 13,205</footnote>
<figure><img src="image_7.png" /><figcaption>**Fig 4.** Toxoplasma seroprevalence among pregnant women in different African countries (A) and the income level of the countries with an indicated seroprevalence (B). Maps were built using the free website MapChart (https://www.mapchart.net/index.html).</figcaption></figure>

https://doi.org/10.1371/journal.pntd.0012198.g004

women who had a history of abortion worldwide (43%) [84]. A similar pooled seroprevalence estimate of toxoplasmosis has also been reported in a systematic review and meta-analysis conducted on HIV-infected pregnant women worldwide (45.7%) [85]. Noteworthy, in this latter study, 10 out of the 14 included studies originated from African countries, which could explain the very similar prevalence, as that observed in our study on non-immunocompromised women. Indeed, the immune background, particularly HIV infection in not known to influence the seroprevalence rate [86].

<table><caption>**Table 4.** Prevalence according to income level and geographical characteristics.</caption><thead><tr><th rowspan="2"></th><th colspan="3">No of countries with indicated prevalence</th><th rowspan="2">p-value</th></tr><tr><th>&lt; 25%</th><th>25-45%</th><th>&gt; 45%</th></tr></thead><tbody><tr><td>Income level (GDP per capita)</td><td></td><td></td><td></td><td>0.318</td></tr><tr><td>Low income</td><td>4</td><td>1</td><td>4</td><td></td></tr><tr><td>Low-middle income</td><td>1</td><td>4</td><td>3</td><td></td></tr><tr><td>Upper-middle income</td><td>1</td><td>0</td><td>1</td><td></td></tr><tr><td>Annual rainfall (mm)</td><td></td><td></td><td></td><td>0.280</td></tr><tr><td>Low (&lt; 500)</td><td>3</td><td>2</td><td>2</td><td></td></tr><tr><td>Moderate (500-1500)</td><td>3</td><td>3</td><td>3</td><td></td></tr><tr><td>High (&gt; 1500)</td><td>0</td><td>0</td><td>3</td><td></td></tr><tr><td>Climate</td><td></td><td></td><td></td><td>0.404</td></tr><tr><td>Tropical humid</td><td>3</td><td>1</td><td>6</td><td></td></tr><tr><td>Arid</td><td>2</td><td>2</td><td>1</td><td></td></tr><tr><td>Mixt</td><td>1</td><td>2</td><td>1</td><td></td></tr><tr><td>Average elevation (m)</td><td></td><td></td><td></td><td>0.293</td></tr><tr><td>&lt; 800</td><td>2</td><td>3</td><td>6</td><td></td></tr><tr><td>&ge; 800</td><td>4</td><td>2</td><td>2</td><td></td></tr></tbody></table>

https://doi.org/10.1371/journal.pntd.0012198.t004
<figure><img src="image_7.png" /><figcaption>**Fig 4.** Toxoplasma seroprevalence among pregnant women in different African countries (A) and the income level of the countries with an indicated seroprevalence (B). Maps were built using the free website MapChart (https://www.mapchart.net/index.html).</figcaption></figure>

https://doi.org/10.1371/journal.pntd.0012198.g004

women who had a history of abortion worldwide (43%) [84]. A similar pooled seroprevalence estimate of toxoplasmosis has also been reported in a systematic review and meta-analysis conducted on HIV-infected pregnant women worldwide (45.7%) [85]. Noteworthy, in this latter study, 10 out of the 14 included studies originated from African countries, which could explain the very similar prevalence, as that observed in our study on non-immunocompromised women. Indeed, the immune background, particularly HIV infection in not known to influence the seroprevalence rate [86].

<table><caption>**Table 4.** Prevalence according to income level and geographical characteristics.</caption><thead><tr><th rowspan="2"></th><th colspan="3">No of countries with indicated prevalence</th><th rowspan="2">p-value</th></tr><tr><th>&lt; 25%</th><th>25-45%</th><th>&gt; 45%</th></tr></thead><tbody><tr><td>Income level (GDP per capita)</td><td></td><td></td><td></td><td>0.318</td></tr><tr><td>Low income</td><td>4</td><td>1</td><td>4</td><td></td></tr><tr><td>Low-middle income</td><td>1</td><td>4</td><td>3</td><td></td></tr><tr><td>Upper-middle income</td><td>1</td><td>0</td><td>1</td><td></td></tr><tr><td>Annual rainfall (mm)</td><td></td><td></td><td></td><td>0.280</td></tr><tr><td>Low (&lt; 500)</td><td>3</td><td>2</td><td>2</td><td></td></tr><tr><td>Moderate (500-1500)</td><td>3</td><td>3</td><td>3</td><td></td></tr><tr><td>High (&gt; 1500)</td><td>0</td><td>0</td><td>3</td><td></td></tr><tr><td>Climate</td><td></td><td></td><td></td><td>0.404</td></tr><tr><td>Tropical humid</td><td>3</td><td>1</td><td>6</td><td></td></tr><tr><td>Arid</td><td>2</td><td>2</td><td>1</td><td></td></tr><tr><td>Mixt</td><td>1</td><td>2</td><td>1</td><td></td></tr><tr><td>Average elevation (m)</td><td></td><td></td><td></td><td>0.293</td></tr><tr><td>&lt; 800</td><td>2</td><td>3</td><td>6</td><td></td></tr><tr><td>&ge; 800</td><td>4</td><td>2</td><td>2</td><td></td></tr></tbody></table>

https://doi.org/10.1371/journal.pntd.0012198.t004
<table><caption>Table 5. Factors associated with seroprevalence of toxoplasmosis among pregnant women in Africa.</caption><thead><tr><th rowspan="2">Variables</th><th colspan="2">Toxoplasma seropositive</th><th rowspan="2">OR (95%CI)</th><th rowspan="2">Overall effect (P-value)</th><th rowspan="2">Number of studies</th><th rowspan="2">References (p&lt;0.05)</th><th rowspan="2">References (p&gt;0.05)</th></tr><tr><th>Yes, n (%)</th><th>No, n (%)</th></tr></thead><tbody><tr><td><strong>Residence (n = 6,594)</strong></td><td></td><td></td><td></td><td>0.839</td><td>22</td><td>22, 28, 29, 37, 48, 56, 63</td><td>13, 17, 21, 23, 25, 27, 32, 35, 37, 46, 47, 57, 59, 64</td></tr><tr><td>Rural</td><td>1173 (44.1)</td><td>1488 (55.9)</td><td>1.03 (0.767-1.387)</td><td></td><td></td><td></td><td></td></tr><tr><td>Urban</td><td>1966 (50.0)</td><td>1967 (50.0)</td><td>1</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Cat ownership (n = 11,555)</strong></td><td></td><td></td><td></td><td>&lt; 0.001</td><td>35</td><td>25, 26, 28, 30, 37, 40, 45, 48, 54, 56, 59, 65</td><td>9, 10, 13, 17, 18, 21, 23, 24, 27, 29, 31, 32, 36, 37, 41, 43, 47, 57, 58, 63, 64, 68</td></tr><tr><td>Yes</td><td>1739 (52.3)</td><td>1586 (47.7)</td><td>1.583 (1.272-1.969)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>3446 (41.9)</td><td>4784 (58.1)</td><td>1</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Consumption of raw meat (n = 10,761)</strong></td><td></td><td></td><td></td><td>0.001</td><td>32</td><td>15, 26, 31, 40, 43, 47, 48, 54</td><td>9, 10, 17, 18, 23-25, 27-30, 32, 35-37, 41, 46, 57-59, 63, 65, 68</td></tr><tr><td>Yes</td><td>1970 (46.5)</td><td>2264 (53.5)</td><td>1.503 (1.193-1.895)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>3002 (46.0)</td><td>3525 (54.00)</td><td>1</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Consumption of raw milk (n = 3,260)</strong></td><td></td><td></td><td></td><td>0.147</td><td>9</td><td>32, 64</td><td>9, 15, 27, 28, 41, 47, 59</td></tr><tr><td>Yes</td><td>764 (56.4)</td><td>591 (43.6)</td><td>1.510 (0.866-2.636)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>669 (35.1)</td><td>1236 (64.9)</td><td>1</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Consumption of raw vegetables (n = 7,812)</strong></td><td></td><td></td><td></td><td>0.015</td><td>23</td><td>15, 28, 35, 37, 47, 48, 55, 59</td><td>9, 10, 13, 17, 18, 24, 25, 27, 30-32, 41, 46, 54, 58</td></tr><tr><td>Yes</td><td>2361 (50.2)</td><td>2346 (49.8)</td><td>1.476 (1.079-2.018)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>1474 (45.5)</td><td>1769 (54.5)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Contact with soil (n = 49,999)</strong></td><td></td><td></td><td></td><td>0.142</td><td>16</td><td>15, 37, 40, 64</td><td>13, 18, 23-27, 30, 47, 56, 58, 65</td></tr><tr><td>Yes</td><td>1610 (70.3)</td><td>681 (29.6)</td><td>1.258 (0.926-1.710)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>1509 (51.0)</td><td>1449 (49.0)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Blood transfusion (n = 3,936)</strong></td><td></td><td></td><td></td><td>0.367</td><td>12</td><td>35</td><td>9, 10, 17, 23, 25, 27, 28, 37, 47, 54, 64</td></tr><tr><td>Yes</td><td>118 (53.4)</td><td>103 (46.6)</td><td>1.244 (0.774-2.001)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>1838 (49.5)</td><td>1877 (50.5)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>HIV status (n = 3,351)</strong></td><td></td><td></td><td></td><td>0.086</td><td>12</td><td>30, 35</td><td>31, 10, 23, 24, 37, 43, 46, 48, 57, 59</td></tr><tr><td>Positive</td><td>149 (52.5)</td><td>1135 (47.5)</td><td>1.547 (0.941-2.543)</td><td></td><td></td><td></td><td></td></tr><tr><td>Negative</td><td>1422 (46.4)</td><td>1645 (53.6)</td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

https://doi.org/10.1371/journal.pntd.0012198.t005

Our finding is higher than the overall worldwide prevalence of toxoplasmosis among pregnant women (33.8%, 95%CI: 31.5% - 35.9%) [87]. In particular, it is higher than prevalence rates reported in Asia (28.5% in Saudi Arabia [88], 29.9% in Sri Lanka [89], 10% in Japan [90]) and Europe (31% in France [7] and 9% in Norway [91]). Several factors, such as the climate, standard of living, quality of the drinking water, cooking habits of meat, and density of felids, could account for these differences in seroprevalence. Few data are available regarding the prevalence of toxoplasmosis in felids in Africa, and even fewer in wild felids, compared to Europe or America. However, two recent meta-analyses [92,93] reported that the highest *T. gondii* pooled seroprevalences in domestic cats worldwide were observed in Australia (52% and 66.6%, respectively) and in Africa (51% and 55.7%, respectively). Interestingly, the highest rate of seroprevalence in wild felids was observed in lions (87.6%) [93]. Besides, the highest rate of *Toxoplasma* oocysts detection in feces from domestic cats (9.8%) was reported from African studies [93]. Although these data need to be consolidated, they indicate that the high prevalence in African felids could support the overall high seroprevalence observed in pregnant women on this continent.

We observed that the Central and East African regions had the highest pooled *T. gondii* seroprevalence, whereas the lowest was reported in the South African region. Moreover, the
<table><caption>Table 5. Factors associated with seroprevalence of toxoplasmosis among pregnant women in Africa.</caption><thead><tr><th rowspan="2">Variables</th><th colspan="2">Toxoplasma seropositive</th><th rowspan="2">OR (95%CI)</th><th rowspan="2">Overall effect (P-value)</th><th rowspan="2">Number of studies</th><th rowspan="2">References (p&lt;0.05)</th><th rowspan="2">References (p&gt;0.05)</th></tr><tr><th>Yes, n (%)</th><th>No, n (%)</th></tr></thead><tbody><tr><td><strong>Residence (n = 6,594)</strong></td><td></td><td></td><td></td><td>0.839</td><td>22</td><td>22, 28, 29, 37, 48, 56, 63</td><td>13, 17, 21, 23, 25, 27, 32, 35, 37, 46, 47, 57, 59, 64</td></tr><tr><td>Rural</td><td>1173 (44.1)</td><td>1488 (55.9)</td><td>1.03 (0.767-1.387)</td><td></td><td></td><td></td><td></td></tr><tr><td>Urban</td><td>1966 (50.0)</td><td>1967 (50.0)</td><td>1</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Cat ownership (n = 11,555)</strong></td><td></td><td></td><td></td><td>&lt; 0.001</td><td>35</td><td>25, 26, 28, 30, 37, 40, 45, 48, 54, 56, 59, 65</td><td>9, 10, 13, 17, 18, 21, 23, 24, 27, 29, 31, 32, 36, 37, 41, 43, 47, 57, 58, 63, 64, 68</td></tr><tr><td>Yes</td><td>1739 (52.3)</td><td>1586 (47.7)</td><td>1.583 (1.272-1.969)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>3446 (41.9)</td><td>4784 (58.1)</td><td>1</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Consumption of raw meat (n = 10,761)</strong></td><td></td><td></td><td></td><td>0.001</td><td>32</td><td>15, 26, 31, 40, 43, 47, 48, 54</td><td>9, 10, 17, 18, 23-25, 27-30, 32, 35-37, 41, 46, 57-59, 63, 65, 68</td></tr><tr><td>Yes</td><td>1970 (46.5)</td><td>2264 (53.5)</td><td>1.503 (1.193-1.895)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>3002 (46.0)</td><td>3525 (54.00)</td><td>1</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Consumption of raw milk (n = 3,260)</strong></td><td></td><td></td><td></td><td>0.147</td><td>9</td><td>32, 64</td><td>9, 15, 27, 28, 41, 47, 59</td></tr><tr><td>Yes</td><td>764 (56.4)</td><td>591 (43.6)</td><td>1.510 (0.866-2.636)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>669 (35.1)</td><td>1236 (64.9)</td><td>1</td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Consumption of raw vegetables (n = 7,812)</strong></td><td></td><td></td><td></td><td>0.015</td><td>23</td><td>15, 28, 35, 37, 47, 48, 55, 59</td><td>9, 10, 13, 17, 18, 24, 25, 27, 30-32, 41, 46, 54, 58</td></tr><tr><td>Yes</td><td>2361 (50.2)</td><td>2346 (49.8)</td><td>1.476 (1.079-2.018)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>1474 (45.5)</td><td>1769 (54.5)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Contact with soil (n = 49,999)</strong></td><td></td><td></td><td></td><td>0.142</td><td>16</td><td>15, 37, 40, 64</td><td>13, 18, 23-27, 30, 47, 56, 58, 65</td></tr><tr><td>Yes</td><td>1610 (70.3)</td><td>681 (29.6)</td><td>1.258 (0.926-1.710)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>1509 (51.0)</td><td>1449 (49.0)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Blood transfusion (n = 3,936)</strong></td><td></td><td></td><td></td><td>0.367</td><td>12</td><td>35</td><td>9, 10, 17, 23, 25, 27, 28, 37, 47, 54, 64</td></tr><tr><td>Yes</td><td>118 (53.4)</td><td>103 (46.6)</td><td>1.244 (0.774-2.001)</td><td></td><td></td><td></td><td></td></tr><tr><td>No</td><td>1838 (49.5)</td><td>1877 (50.5)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>HIV status (n = 3,351)</strong></td><td></td><td></td><td></td><td>0.086</td><td>12</td><td>30, 35</td><td>31, 10, 23, 24, 37, 43, 46, 48, 57, 59</td></tr><tr><td>Positive</td><td>149 (52.5)</td><td>1135 (47.5)</td><td>1.547 (0.941-2.543)</td><td></td><td></td><td></td><td></td></tr><tr><td>Negative</td><td>1422 (46.4)</td><td>1645 (53.6)</td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

https://doi.org/10.1371/journal.pntd.0012198.t005

Our finding is higher than the overall worldwide prevalence of toxoplasmosis among pregnant women (33.8%, 95%CI: 31.5% - 35.9%) [87]. In particular, it is higher than prevalence rates reported in Asia (28.5% in Saudi Arabia [88], 29.9% in Sri Lanka [89], 10% in Japan [90]) and Europe (31% in France [7] and 9% in Norway [91]). Several factors, such as the climate, standard of living, quality of the drinking water, cooking habits of meat, and density of felids, could account for these differences in seroprevalence. Few data are available regarding the prevalence of toxoplasmosis in felids in Africa, and even fewer in wild felids, compared to Europe or America. However, two recent meta-analyses [92,93] reported that the highest *T. gondii* pooled seroprevalences in domestic cats worldwide were observed in Australia (52% and 66.6%, respectively) and in Africa (51% and 55.7%, respectively). Interestingly, the highest rate of seroprevalence in wild felids was observed in lions (87.6%) [93]. Besides, the highest rate of *Toxoplasma* oocysts detection in feces from domestic cats (9.8%) was reported from African studies [93]. Although these data need to be consolidated, they indicate that the high prevalence in African felids could support the overall high seroprevalence observed in pregnant women on this continent.

We observed that the Central and East African regions had the highest pooled *T. gondii* seroprevalence, whereas the lowest was reported in the South African region. Moreover, the
sub-group analysis conducted by country showed four countries from Central and East Africa (Congo, Gabon, Ethiopia, and Eritrea) to be among the top five countries with the highest pooled seroprevalence. The possible reason for the highest seroprevalence in Central and East Africa may be due to the frequency of contact with domestic or stray cats or other felids, and poor environmental hygiene [94]. Geoclimatic conditions in Central Africa, which has a tropical warm humid climate and small temperature range, may also favor long-term survival of oocysts in the environment, as observed in South America, where a high seroprevalence has been documented [95]. Some authors have also postulated that climate could affect the life cycle and population dynamics of prey species, thereby providing favorable conditions for cat reproduction and increasing numbers of young, naive definitive hosts susceptible to *T. gondii* infection [96].

The serological test used to diagnose *T. gondii* infection in the included studies was recorded, as this could introduce bias depending on its performance [97]. Indeed, latex agglutination is known to yield a certain number of false positive results, whereas the sensitivity of certain RDTs can be lower than that of EIA, as already observed in field studies [98]. However, the prevalence estimates obtained in Ethiopian studies using AT and EIA did not significantly differ (median seroprevalence of 80.55% and 69.60%, respectively, p = 0.74). Interestingly, the sole two studies using RDTs, performed in Nigeria and Zambia, showed the lowest prevalence rates (11.7% and 5.8%, respectively) [22,43] observed in central African countries. Both countries have a humid tropical climate and a low or lower-middle income. *Toxoplasma* seroprevalence was, thus, expected to be high. The study performed in Nigeria by Akubuilo et al. [22] contrasted with other Nigerian studies using EIA, as Dairo et al. [37], Nasir et al. [57], and Oboro et al. [52] reported a seroprevalence of 35.9%, 48.9%, and 65.6%, respectively. This supports the hypothesis of poor sensitivity of the RDT used by Akubuilo et al. [22]. The RDT used in the study performed in Zambia [43] showed poor efficiency in a study comparing three RDTs for *Toxoplasma* diagnosis [99], which could also explain such an unexpectedly low seroprevalence. However, no other data are available from Zambia for other patient groups, and thus these data still need to be consolidated.

In this systematic review and meta-analysis, we confirmed that pregnant women owning a cat had higher odds of seropositivity for toxoplasmosis than those who did not, as observed in previous individual studies from various countries [100–104], including Ethiopia [105,106]. Following primary infection, young cats can spread several hundred thousand oocysts per day for three weeks, and thus play a crucial role in *T. gondii* transmission through direct contact or the handling of litter. In addition, stray cats also massively contaminate the environment, water, and vegetables [1,2]. Although experimental infection of cats has shown that re-infection with a same genotype strain did not lead to re-shedding of oocysts in feces, infection with other genotypes did. In Africa, cats are mostly free-ranging or feral animals, thus are likely to encounter multiple genotypes of *T. gondii* via hunting various infected preys. The same applies even more likely to wild felids, ensuring multiple re-infections and re-shedding of oocysts in the environment [96].

Another important risk factor was the consumption of raw meat, which is currently practiced in Eastern Africa. A similar finding was reported in studies conducted in Saudi Arabia, the Philippines, and Brazil [107–109]. Consistent with this finding, a systematic review and meta-analysis of case-controlled studies showed that the consumption of raw meat is a risk factor significantly associated with acute *T. gondii* infection in humans (OR = 3.44 (1.29–9.16) [110]. In other studies, not only eating raw meat but also contact with raw meat was shown to be associated with a higher risk of acquiring *Toxoplasma* infection [106].

In accordance with the results of previous studies from other continents [104,109,111–113], we found that the consumption of raw vegetables had a significant overall effect on
sub-group analysis conducted by country showed four countries from Central and East Africa (Congo, Gabon, Ethiopia, and Eritrea) to be among the top five countries with the highest pooled seroprevalence. The possible reason for the highest seroprevalence in Central and East Africa may be due to the frequency of contact with domestic or stray cats or other felids, and poor environmental hygiene [94]. Geoclimatic conditions in Central Africa, which has a tropical warm humid climate and small temperature range, may also favor long-term survival of oocysts in the environment, as observed in South America, where a high seroprevalence has been documented [95]. Some authors have also postulated that climate could affect the life cycle and population dynamics of prey species, thereby providing favorable conditions for cat reproduction and increasing numbers of young, naive definitive hosts susceptible to *T. gondii* infection [96].

The serological test used to diagnose *T. gondii* infection in the included studies was recorded, as this could introduce bias depending on its performance [97]. Indeed, latex agglutination is known to yield a certain number of false positive results, whereas the sensitivity of certain RDTs can be lower than that of EIA, as already observed in field studies [98]. However, the prevalence estimates obtained in Ethiopian studies using AT and EIA did not significantly differ (median seroprevalence of 80.55% and 69.60%, respectively, p = 0.74). Interestingly, the sole two studies using RDTs, performed in Nigeria and Zambia, showed the lowest prevalence rates (11.7% and 5.8%, respectively) [22,43] observed in central African countries. Both countries have a humid tropical climate and a low or lower-middle income. *Toxoplasma* seroprevalence was, thus, expected to be high. The study performed in Nigeria by Akubuilo et al. [22] contrasted with other Nigerian studies using EIA, as Dairo et al. [37], Nasir et al. [57], and Oboro et al. [52] reported a seroprevalence of 35.9%, 48.9%, and 65.6%, respectively. This supports the hypothesis of poor sensitivity of the RDT used by Akubuilo et al. [22]. The RDT used in the study performed in Zambia [43] showed poor efficiency in a study comparing three RDTs for *Toxoplasma* diagnosis [99], which could also explain such an unexpectedly low seroprevalence. However, no other data are available from Zambia for other patient groups, and thus these data still need to be consolidated.

In this systematic review and meta-analysis, we confirmed that pregnant women owning a cat had higher odds of seropositivity for toxoplasmosis than those who did not, as observed in previous individual studies from various countries [100–104], including Ethiopia [105,106]. Following primary infection, young cats can spread several hundred thousand oocysts per day for three weeks, and thus play a crucial role in *T. gondii* transmission through direct contact or the handling of litter. In addition, stray cats also massively contaminate the environment, water, and vegetables [1,2]. Although experimental infection of cats has shown that re-infection with a same genotype strain did not lead to re-shedding of oocysts in feces, infection with other genotypes did. In Africa, cats are mostly free-ranging or feral animals, thus are likely to encounter multiple genotypes of *T. gondii* via hunting various infected preys. The same applies even more likely to wild felids, ensuring multiple re-infections and re-shedding of oocysts in the environment [96].

Another important risk factor was the consumption of raw meat, which is currently practiced in Eastern Africa. A similar finding was reported in studies conducted in Saudi Arabia, the Philippines, and Brazil [107–109]. Consistent with this finding, a systematic review and meta-analysis of case-controlled studies showed that the consumption of raw meat is a risk factor significantly associated with acute *T. gondii* infection in humans (OR = 3.44 (1.29–9.16) [110]). In other studies, not only eating raw meat but also contact with raw meat was shown to be associated with a higher risk of acquiring *Toxoplasma* infection [106].

In accordance with the results of previous studies from other continents [104,109,111–113], we found that the consumption of raw vegetables had a significant overall effect on
*Toxoplasma gondii* seropositivity among pregnant women, who had a 47.6% higher risk of acquiring *T. gondii* infection. However, the risk associated with raw vegetable consumption was not unanimously recognized, as observed in Iran [82,104], as well as in African countries (9, 10, 14, 18, 19, 24, 26, 28, 31–33, 42, 47, 55, 59). This discrepancy could be due to the type of agriculture, the hygiene of the food market and food handling, the washing habits of vegetables and quality of the water supply, soil contamination by felids, and the density of cats.

This study confirms that the seroprevalence of toxoplasmosis in Africa is high. Recent epidemiological data from animals showed that the Africa-1 genotype predominates in Benin [114] and Gabon [81], meaning that similar strains are likely to infect humans and could be responsible for congenital infection. A retrospective study conducted in Benin on pregnant women estimated that the *Toxoplasma* seroconversion rate was 3.4% [16], which is more than 10-fold higher than that estimated among French pregnant women [7]. Further studies should be undertaken in African countries to evaluate the rate of infected newborns, for example by serological screening at birth, as already carried out in Colombia [115]. The incidence and burden of toxoplasmosis in African countries is currently unknown, whether in the setting of pregnancy or among HIV-infected patients, as biological confirmation is rarely obtained [116]. A call for raising awareness concerning toxoplasmosis and fungal diseases was made several years ago [117], but actions are still pending to better diagnose toxoplasmosis and characterize its true burden. If a high incidence rate is confirmed, serological screening and counseling of all pregnant women for toxoplasmosis infection as a part of antenatal care would be crucial to minimize congenital transmission and its complications.

We were unable to identify new predictors for acquiring toxoplasmosis infection other than those already reported, i.e., contact with cats and the consumption of raw meat and unwashed vegetables. Therefore, efforts should be made towards prevention programs targeting women of child-bearing age, raising awareness of the clinical signs and possible consequences for the fetus, and focusing on hygienic prevention measures to avoid infection, such as the proper handling and cooking of meat, washing of vegetables and hands, and management of domestic cats [2]. We believe that our study should pave the way for epidemiological studies on humans and encourage policymakers to fund prevention programs.

**Supporting information**

S1 File. Searching strategy.

(DOCX)

S2 File. Measure of the true agreement (K) between the raters.

(DOCX)

S3 File. The revised 2023 JBI checklist for analytical cross-sectional studies to assess the quality ranking of the full extracted articles.

(DOCX)

S4 File. Sensitivity analysis of the pooled prevalence of *T. gondii* infection among pregnant women in Africa for a single study omitted.

(DOCX)

S5 File. Database.

(XLSX)
*Toxoplasma gondii* seropositivity among pregnant women, who had a 47.6% higher risk of acquiring *T. gondii* infection. However, the risk associated with raw vegetable consumption was not unanimously recognized, as observed in Iran [82,104], as well as in African countries (9, 10, 14, 18, 19, 24, 26, 28, 31–33, 42, 47, 55, 59). This discrepancy could be due to the type of agriculture, the hygiene of the food market and food handling, the washing habits of vegetables and quality of the water supply, soil contamination by felids, and the density of cats.

This study confirms that the seroprevalence of toxoplasmosis in Africa is high. Recent epidemiological data from animals showed that the Africa-1 genotype predominates in Benin [114] and Gabon [81], meaning that similar strains are likely to infect humans and could be responsible for congenital infection. A retrospective study conducted in Benin on pregnant women estimated that the *Toxoplasma* seroconversion rate was 3.4% [16], which is more than 10-fold higher than that estimated among French pregnant women [7]. Further studies should be undertaken in African countries to evaluate the rate of infected newborns, for example by serological screening at birth, as already carried out in Colombia [115]. The incidence and burden of toxoplasmosis in African countries is currently unknown, whether in the setting of pregnancy or among HIV-infected patients, as biological confirmation is rarely obtained [116]. A call for raising awareness concerning toxoplasmosis and fungal diseases was made several years ago [117], but actions are still pending to better diagnose toxoplasmosis and characterize its true burden. If a high incidence rate is confirmed, serological screening and counseling of all pregnant women for toxoplasmosis infection as a part of antenatal care would be crucial to minimize congenital transmission and its complications.

We were unable to identify new predictors for acquiring toxoplasmosis infection other than those already reported, i.e., contact with cats and the consumption of raw meat and unwashed vegetables. Therefore, efforts should be made towards prevention programs targeting women of child-bearing age, raising awareness of the clinical signs and possible consequences for the fetus, and focusing on hygienic prevention measures to avoid infection, such as the proper handling and cooking of meat, washing of vegetables and hands, and management of domestic cats [2]. We believe that our study should pave the way for epidemiological studies on humans and encourage policymakers to fund prevention programs.

**Supporting information**

S1 File. Searching strategy.

(DOCX)

S2 File. Measure of the true agreement (K) between the raters.

(DOCX)

S3 File. The revised 2023 JBI checklist for analytical cross-sectional studies to assess the quality ranking of the full extracted articles.

(DOCX)

S4 File. Sensitivity analysis of the pooled prevalence of *T. gondii* infection among pregnant women in Africa for a single study omitted.

(DOCX)

S5 File. Database.

(XLSX)
**Acknowledgments**

The authors are grateful to the French Foreign Office and the French Embassy in Ethiopia for their support. They thank William Hempel of Alex Edelman & Associated for editing the English.

**Author Contributions**

**Conceptualization:** Yared Mulu Gelaw, Jean-Pierre Gangneux, Florence Robert-Gangneux.

**Data curation:** Yared Mulu Gelaw.

**Formal analysis:** Yared Mulu Gelaw, Gizachew Worku Dagnew, Getu Degu Alene, Florence Robert-Gangneux.

**Investigation:** Yared Mulu Gelaw, Gizachew Worku Dagnew.

**Methodology:** Gizachew Worku Dagnew, Florence Robert-Gangneux.

**Supervision:** Florence Robert-Gangneux.

**Visualization:** Getu Degu Alene.

**Writing – original draft:** Yared Mulu Gelaw.

**Writing – review & editing:** Jean-Pierre Gangneux, Florence Robert-Gangneux.

**References**

1. Dubey JP. History of the discovery of the life cycle of Toxoplasma gondii. Int J Parasitol. 2009; 39: 877-882. https://doi.org/10.1016/j.ijpara.2009.01.005 PMID: 19630138

2. Robert-Gangneux F, Dardé M-L. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012; 25: 264-296. https://doi.org/10.1128/CMR.05013-11 PMID: 22491772

3. Pereira KS, Franco RM, Leal DA. Transmission of toxoplasmosis (Toxoplasma gondii) by foods. Adv Food Nutr Res. 2010; 60: 1-19. https://doi.org/10.1016/S1043-4526(10)60001-0 PMID: 20691951

4. Kijlstra A, Jongert E. Control of the risk of human toxoplasmosis transmitted by meat. Int J Parasitol. 2008; 38: 1359-1370. https://doi.org/10.1016/j.ijpara.2008.06.002 PMID: 18694755

5. Remington JS, Wilson CB, Nizet V, Klein JO, Maldonado Y. Infectious Diseases of the Fetus and New-born E-Book. Elsevier Health Sciences; 2010.

6. Torgerson PR, Mastroiacovo P. The global burden of congenital toxoplasmosis: a systematic review. Bull World Health Organ. 2013; 91: 501-508. https://doi.org/10.2471/BLT.12.111732 PMID: 23825877

7. Robinson E, de Valk H, Villena I, Le Strat Y, Tourdjman M. National perinatal survey demonstrates a decreasing seroprevalence of Toxoplasma gondii infection among pregnant women in France, 1995 to 2016: impact for screening policy. Eurosurveillance. 2021; 26: 1900710. https://doi.org/10.2807/1560-7917.ES.2021.26.5.1900710 PMID: 33541484

8. Dasa TT, Geta TG, Yalew AZ, Abebe RM, Kele HU. Toxoplasmosis infection among pregnant women in Africa: A systematic review and meta-analysis. PloS One. 2021; 16: e0254209. https://doi.org/10.1371/journal.pone.0254209 PMID: 34283858

9. Van der Colf BE, Ntirampeba D, Van Zyl GU, Noden BH. Seroprevalence of Toxoplasma gondii infection among pregnant women in Windhoek, Namibia, in 2016. South Afr J Infect Dis. 2020; 35: 1-7. https://doi.org/10.4102/sajid.v35i1.25 PMID: 34485464

10. Gelaye W, Kebede T, Hailu A. High prevalence of anti-toxoplasma antibodies and absence of Toxoplasma gondii infection risk factors among pregnant women attending routine antenatal care in two Hospitals of Addis Ababa, Ethiopia. Int J Infect Dis. 2015; 34: 41-45.

11. Abbas IE, Villena I, Dubey JP. A review on toxoplasmosis in humans and animals from Egypt. Parasitology. 2020; 147: 135-159. https://doi.org/10.1017/S0031182019001367 PMID: 31559938

12. Sim J, Wright CC. The kappa statistic in reliability studies: use, interpretation, and sample size requirements. Phys Ther. 2005; 85: 257-268. PMID: 15733050
**Acknowledgments**

The authors are grateful to the French Foreign Office and the French Embassy in Ethiopia for their support. They thank William Hempel of Alex Edelman & Associated for editing the English.

**Author Contributions**

**Conceptualization:** Yared Mulu Gelaw, Jean-Pierre Gangneux, Florence Robert-Gangneux.

**Data curation:** Yared Mulu Gelaw.

**Formal analysis:** Yared Mulu Gelaw, Gizachew Worku Dagnew, Getu Degu Alene, Florence Robert-Gangneux.

**Investigation:** Yared Mulu Gelaw, Gizachew Worku Dagnew.

**Methodology:** Gizachew Worku Dagnew, Florence Robert-Gangneux.

**Supervision:** Florence Robert-Gangneux.

**Visualization:** Getu Degu Alene.

**Writing – original draft:** Yared Mulu Gelaw.

**Writing – review & editing:** Jean-Pierre Gangneux, Florence Robert-Gangneux.

**References**

1. Dubey JP. History of the discovery of the life cycle of Toxoplasma gondii. Int J Parasitol. 2009; 39: 877–882. https://doi.org/10.1016/j.ijpara.2009.01.005 PMID: 19630138

2. Robert-Gangneux F, Dardé M-L. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012; 25: 264–296. https://doi.org/10.1128/CMR.05013-11 PMID: 22491772

3. Pereira KS, Franco RM, Leal DA. Transmission of toxoplasmosis (Toxoplasma gondii) by foods. Adv Food Nutr Res. 2010; 60: 1–19. https://doi.org/10.1016/S1043-4526(10)60001-0 PMID: 20691951

4. Kijlstra A, Jongert E. Control of the risk of human toxoplasmosis transmitted by meat. Int J Parasitol. 2008; 38: 1359–1370. https://doi.org/10.1016/j.ijpara.2008.06.002 PMID: 18694755

5. Remington JS, Wilson CB, Nizet V, Klein JO, Maldonado Y. Infectious Diseases of the Fetus and New-born E-Book. Elsevier Health Sciences; 2010.

6. Torgerson PR, Mastroiacovo P. The global burden of congenital toxoplasmosis: a systematic review. Bull World Health Organ. 2013; 91: 501–508. https://doi.org/10.2471/BLT.12.111732 PMID: 23825877

7. Robinson E, de Valk H, Villena I, Le Strat Y, Tourdjman M. National perinatal survey demonstrates a decreasing seroprevalence of Toxoplasma gondii infection among pregnant women in France, 1995 to 2016: impact for screening policy. Eurosurveillance. 2021; 26: 1900710. https://doi.org/10.2807/1560-7917.ES.2021.26.5.1900710 PMID: 33541484

8. Dasa TT, Geta TG, Yalew AZ, Abebe RM, Kele HU. Toxoplasmosis infection among pregnant women in Africa: A systematic review and meta-analysis. PloS One. 2021; 16: e0254209. https://doi.org/10.1371/journal.pone.0254209 PMID: 34283858

9. Van der Colf BE, Ntirampeba D, Van Zyl GU, Noden BH. Seroprevalence of Toxoplasma gondii infection among pregnant women in Windhoek, Namibia, in 2016. South Afr J Infect Dis. 2020; 35: 1–7. https://doi.org/10.4102/sajid.v35i1.25 PMID: 34485464

10. Gelaye W, Kebede T, Hailu A. High prevalence of anti-toxoplasma antibodies and absence of Toxoplasma gondii infection risk factors among pregnant women attending routine antenatal care in two Hospitals of Addis Ababa, Ethiopia. Int J Infect Dis. 2015; 34: 41–45.

11. Abbas IE, Villena I, Dubey JP. A review on toxoplasmosis in humans and animals from Egypt. Parasitology. 2020; 147: 135–159. https://doi.org/10.1017/S0031182019001367 PMID: 31559938

12. Sim J, Wright CC. The kappa statistic in reliability studies: use, interpretation, and sample size requirements. Phys Ther. 2005; 85: 257–268. PMID: 15733050
13. Barker TH, Stone JC, Sears K, Klugar M, Leonardi-Bee J, Tufanaru C, et al. Revising the JBI quantitative critical appraisal tools to improve their applicability: an overview of methods and the development process. JBI Evid Synth. 2023; 21: 478–493. https://doi.org/10.11124/JBIES-22-00125 PMID: 36121230

14. Hassan SA, Tamomh AG, Hassan DA, Ahmed NR. Seroprevalence of anti-Toxoplasma gondii antibodies and associated risk factors in pregnant women in Somalia. Acta Trop. 2023; 238: 106774. https://doi.org/10.1016/j.actatropica.2022.106774 PMID: 36417981

15. Okojokwu O, Nwachukwu E, Ali M, Agabi Y. Seroprevalence of Anti-toxoplasma IgG and IgM among pregnant women attending antenatal clinic in Jos-North, Plateau State, Nigeria. Microbes Infect Dis. 2023; 4: 285–295.

16. Dambrun M, Dechavanne C, Guigue N, Briand V, Candau T, Fievet N, et al. Retrospective study of toxoplasmosis prevalence in pregnant women in Benin and its relation with malaria. PLoS One. 2022; 17: e0262018. https://doi.org/10.1371/journal.pone.0262018 PMID: 34995295

17. Lushina M, Mushi V, Tarimo D, Babafemi EO. Seroprevalence of Toxoplasma gondii and associated risk factors among pregnant women attending antenatal care in Ilala Municipality, Dar es Salaam, Tanzania. 2022.

18. Laboudi M, Taghy Z, Duieb O, Peyron F, Sadak A. Toxoplasma gondii seroprevalence among pregnant women in Rabat, Morocco. Trop Med Health. 2021; 49: 1–8.

19. Adugna B, Tarekegn ZS, Damtie D, Woldegebreal SN, Raju RP, Maru M, et al. Seroepidemiology of Toxoplasma gondii Among Pregnant Women Attending Antenatal Care in Northwest Ethiopia. Infect Drug Resist. 2021; 1295–1303. https://doi.org/10.2147/IDR.S299106 PMID: 33883909

20. Singh B, Debrah LB, Acheampong G, Debrah AY. Seroprevalence and Risk Factors of Toxoplasma gondii Infection among Pregnant Women in Kumasi: A Cross-Sectional Study at a District-Level Hospital, Ghana. Infect Dis Obstet Gynecol. 2021; 2021.

21. Hoummadi L, Berrouch S, Amraouza Y, Adel A, Mriouch M, Soraa N, et al. Seroprevalence of toxoplasmosis in pregnant women of the Marrakech-Safi region, Morocco. Afr Health Sci. 2020; 20: 59–63. https://doi.org/10.4314/ahs.v20i1.10 PMID: 33402893

22. Akubuilo AS, Amali O, Onekutu A. Seroprevalence of toxoplasma gondii infection among pregnant women attending antenatal clinic in major health centers in Jos north, Nigeria. Open J Biosci Res ISSN 2734-2069. 2020; 1: 44–54.

23. van den Bogaart E, Berkhout MMZ, Adams ER, Mens PF, Sentongo E, Mbulamberi DB, et al. Prevalence, features and risk factors for malaria co-infections amongst visceral leishmaniasis patients from Amudat Hospital, Uganda. PLoS Negl Trop Dis. 2012; 6: e1617. https://doi.org/10.1371/journal.pntd.0001617 PMID: 22506087

24. Zakari MM, Isah AY, Offiong R, Yunusa T, Abdullahi IN. Serological survey and risk factors associated with Toxoplasma gondii infection among HIV-infected pregnant women attending Abuja Tertiary Hospital, Nigeria. Malawi Med J. 2020; 32: 160–167. https://doi.org/10.4314/mmj.v32i3.9 PMID: 33488988

25. Mulugeta S, Munshea A, Nibret E. Seroprevalence of Anti-Toxoplasma gondii antibodies and associated factors among pregnant women attending antenatal care at Debre Markos referral hospital, Northwest Ethiopia. Infect Dis Res Treat. 2020; 13: 1178633720948872. https://doi.org/10.1177/1178633720948872 PMID: 32922029

26. Tecle AS, Talha AA, Mohamedahmed KA, Abakar AD. Seroprevalence of toxoplasmosis among pregnant women attending antenatal care in Asmara, Eritrea: preliminary report. Int J Med Parasitol Epidemiol Sci. 2020; 1: 78–84.

27. Nguemaïm NF, Takang WA, Dobgima WP, Guebidiang BM, Foumane P, Kamga FHL. Seroprevalence of Toxoplasma gondii infection and associated risk factors among pregnant women attending antenatal clinic at the Bamenda Regional Hospital, Cameroon. Afr J Clin Exp Microbiol. 2020; 21: 123–131.

28. Abdelbaset AE, Hamed MI, Abushahba MF, Rawy MS, Sayed AS, Adamovicz JJ. Toxoplasma gondii seropositivity and the associated risk factors in sheep and pregnant women in El-Minya Governorate, Egypt. Vet World. 2020; 13: 54. https://doi.org/10.14202/vetworld.2020.54-60 PMID: 32158151

29. Fenta DA. Seroprevalence of Toxoplasma gondii among pregnant women attending antenatal clinics at Hawassa University comprehensive specialized and Yirgalem General Hospitals, in Southern Ethiopia. BMC Infect Dis. 2019; 19: 1056. https://doi.org/10.1186/s12879-019-4694-8 PMID: 31842783

30. Teweldemedhin M, Gebremichael A, Geberkirstos G, Hadush H, Gebrewahid T, Asgedom SW, et al. Seroprevalence and risk factors of Toxoplasma gondii among pregnant women in Adwa district, northern Ethiopia. BMC Infect Dis. 2019; 19: 327. https://doi.org/10.1186/s12879-019-3936-0 PMID: 30991956

31. Mirambo MM, Mshana SE, Groß U. Rubella virus, Toxoplasma gondii and Treponema pallidum genital infections among full term delivered women in an urban area of Tanzania: a call for improved
13. Barker TH, Stone JC, Sears K, Klugar M, Leonardi-Bee J, Tufanaru C, et al. Revising the JBI quantitative critical appraisal tools to improve their applicability: an overview of methods and the development process. JBI Evid Synth. 2023; 21: 478–493. https://doi.org/10.11124/JBIES-22-00125 PMID: 36121230

14. Hassan SA, Tamomh AG, Hassan DA, Ahmed NR. Seroprevalence of anti-Toxoplasma gondii antibodies and associated risk factors in pregnant women in Somalia. Acta Trop. 2023; 238: 106774. https://doi.org/10.1016/j.actatropica.2022.106774 PMID: 36417981

15. Okojokwu O, Nwachukwu E, Ali M, Agabi Y. Seroprevalence of Anti-toxoplasma IgG and IgM among pregnant women attending antenatal clinic in Jos-North, Plateau State, Nigeria. Microbes Infect Dis. 2023; 4: 285–295.

16. Dambrun M, Dechavanne C, Guigue N, Briand V, Candau T, Fievet N, et al. Retrospective study of toxoplasmosis prevalence in pregnant women in Benin and its relation with malaria. PLoS One. 2022; 17: e0262018. https://doi.org/10.1371/journal.pone.0262018 PMID: 34995295

17. Lushina M, Mushi V, Tarimo D, Babafemi EO. Seroprevalence of Toxoplasma gondii and associated risk factors among pregnant women attending antenatal care in Ilala Municipality, Dar es Salaam, Tanzania. 2022.

18. Laboudi M, Taghy Z, Duieb O, Peyron F, Sadak A. Toxoplasma gondii seroprevalence among pregnant women in Rabat, Morocco. Trop Med Health. 2021; 49: 1–8.

19. Adugna B, Tarekegn ZS, Damtie D, Woldegebreal SN, Raju RP, Maru M, et al. Seroepidemiology of Toxoplasma gondii Among Pregnant Women Attending Antenatal Care in Northwest Ethiopia. Infect Drug Resist. 2021; 1295–1303. https://doi.org/10.2147/IDR.S299106 PMID: 33883909

20. Singh B, Debrah LB, Acheampong G, Debrah AY. Seroprevalence and Risk Factors of Toxoplasma gondii Infection among Pregnant Women in Kumasi: A Cross-Sectional Study at a District-Level Hospital, Ghana. Infect Dis Obstet Gynecol. 2021; 2021.

21. Hoummadi L, Berrouch S, Amraouza Y, Adel A, Mriouch M, Soraa N, et al. Seroprevalence of toxoplasmosis in pregnant women of the Marrakech-Safi region, Morocco. Afr Health Sci. 2020; 20: 59–63. https://doi.org/10.4314/ahs.v20i1.10 PMID: 33402893

22. Akubuilo AS, Amali O, Onekutu A. Seroprevalence of toxoplasma gondii infection among pregnant women attending antenatal clinic in major health centers in Jos north, Nigeria. Open J Biosci Res ISSN 2734-2069. 2020; 1: 44–54.

23. van den Bogaart E, Berkhout MMZ, Adams ER, Mens PF, Sentongo E, Mbulamberi DB, et al. Prevalence, features and risk factors for malaria co-infections amongst visceral leishmaniasis patients from Amudat Hospital, Uganda. PLoS Negl Trop Dis. 2012; 6: e1617. https://doi.org/10.1371/journal.pntd.0001617 PMID: 22506087

24. Zakari MM, Isah AY, Offiong R, Yunusa T, Abdullahi IN. Serological survey and risk factors associated with Toxoplasma gondii infection among HIV-infected pregnant women attending Abuja Tertiary Hospital, Nigeria. Malawi Med J. 2020; 32: 160–167. https://doi.org/10.4314/mmj.v32i3.9 PMID: 33488988

25. Mulugeta S, Munshea A, Nibret E. Seroprevalence of Anti-Toxoplasma gondii antibodies and associated factors among pregnant women attending antenatal care at Debre Markos referral hospital, Northwest Ethiopia. Infect Dis Res Treat. 2020; 13: 1178633720948872. https://doi.org/10.1177/1178633720948872 PMID: 32922029

26. Tecle AS, Talha AA, Mohamedahmed KA, Abakar AD. Seroprevalence of toxoplasmosis among pregnant women attending antenatal care in Asmara, Eritrea: preliminary report. Int J Med Parasitol Epidemiol Sci. 2020; 1: 78–84.

27. Nguemaïm NF, Takang WA, Dobgima WP, Guebidiang BM, Foumane P, Kamga FHL. Seroprevalence of Toxoplasma gondii infection and associated risk factors among pregnant women attending antenatal clinic at the Bamenda Regional Hospital, Cameroon. Afr J Clin Exp Microbiol. 2020; 21: 123–131.

28. Abdelbaset AE, Hamed MI, Abushahba MF, Rawy MS, Sayed AS, Adamovicz JJ. Toxoplasma gondii seropositivity and the associated risk factors in sheep and pregnant women in El-Minya Governorate, Egypt. Vet World. 2020; 13: 54. https://doi.org/10.14202/vetworld.2020.54-60 PMID: 32158151

29. Fenta DA. Seroprevalence of Toxoplasma gondii among pregnant women attending antenatal clinics at Hawassa University comprehensive specialized and Yirgalem General Hospitals, in Southern Ethiopia. BMC Infect Dis. 2019; 19: 1056. https://doi.org/10.1186/s12879-019-4694-8 PMID: 31842783

30. Teweldemedhin M, Gebremichael A, Geberkirstos G, Hadush H, Gebrewahid T, Asgedom SW, et al. Seroprevalence and risk factors of Toxoplasma gondii among pregnant women in Adwa district, northern Ethiopia. BMC Infect Dis. 2019; 19: 327. https://doi.org/10.1186/s12879-019-3936-0 PMID: 30991956

31. Mirambo MM, Mshana SE, Groß U. Rubella virus, Toxoplasma gondii and Treponema pallidum genital infections among full term delivered women in an urban area of Tanzania: a call for improved
antenatal care. Afr Health Sci. 2019; 19: 1858–1865. https://doi.org/10.4314/ahs.v19i2.8 PMID: 31656468

32. Todjom FG, Tsapi EM, Gamago GA, Vignoles P, Pone JW, Teukeng FD. Seroprevalence of toxoplasmosis and associated risk factors in pregnant women at the Protestant Hospital, Mbouo-Bandjoun, Cameroon. Afr J Clin Exp Microbiol. 2019; 20: 221–230.

33. Mabeku LB, Tchakounte C, Bonsi S, Etoa F-X. Prevalence of Toxoplasma gondii and associated risk factors among pregnant women attending hospital centers in Penka-Michel, Cameroon. J Sci Res Rep. 2018; 21: 1–11.

34. Jula J, Girones G, Edao B, Deme C, Cebrian J, Butrón L, et al. Seroprevalence of Toxoplasma gondii infection in pregnant women attending antenatal care in southern Ethiopia. Rev Esp Quimioter. 2018; 31: 363–366. https://doi.org/10.1371/journal.pmed.1001920 PMID: 29978983

35. Adeniyi OT, Adekola SS, Oladipo OM. Seroepidemiology of toxoplasmosis among pregnant women in Osogbo, Southwestern, Nigeria. J Infect Dis Immun. 2018; 10: 8–16.

36. NA HH, Shaapan RM, Hassanain H. Associated Antenatal Health Risk Factors with Incidence of Toxoplasmosis in Egyptian Pregnant Women. Pak J Biol Sci PJBS. 2018; 21: 463–468. https://doi.org/10.3923/pjbs.2018.463.468 PMID: 30724048

37. Dairo MD, Ogunjimi T, Ayinmode AB. Knowledge, risk factors and prevalence of toxoplasmosis among pregnant women at primary health care level in Ibadan, Southwestern Nigeria. Afr J Biomed Res. 2018; 21: 267–271.

38. Mohammed WM, Abdalla HS, Satti AB, Mustafa TB, Kabbashi AS. Sero-prevalence and associated risk factors of Toxoplasma gondii infection among pregnant women attending Omdurman friendship hospital, Omdurman. Ment Health Addict Res. 2018; 3: 1–3.

39. Paul E, Kiwelu I, Mmbaga B, Nazareth R, Sabuni E, Maro A, et al. Toxoplasma gondii seroprevalence among pregnant women attending antenatal clinic in Northern Tanzania. Trop Med Health. 2018; 46: 39. https://doi.org/10.1186/s41182-018-0122-9 PMID: 30479556

40. Tlamcani Z, Yahyaoui G, Mahmoud M. Prevalence of immunity to toxoplasmosis among pregnant women in University Hospital center Hassan II of FEZ city (Morocco). Acta Medica Int. 2017; 4: 43.

41. Pegha Moukandja I, Ngoungou EB, Lemamy GJ, Bisvigou U, Gessain A, Toure Ndouo FS, et al. Non-malarial infectious diseases of antenatal care in pregnant women in Franceville, Gabon. BMC Pregnancy Childbirth. 2017; 17: 185. https://doi.org/10.1186/s12884-017-1362-0 PMID: 28606185

42. El-Shqanqery HE, Ibrahim HM, Mohamed AH, El-Sharaawy AA. Seroprevalence of Toxoplasma gondii infection and associated risk factors among asymptomatic pregnant females in Egypt. J Egypt Soc Parasitol. 2017; 47: 93–100.

43. Frimpong C, Makasa M, Sitali L, Michelo C. Seroprevalence and determinants of toxoplasmosis in pregnant women attending antenatal clinic at the university teaching hospital, Lusaka, Zambia. BMC Infect Dis. 2017; 17: 1–8.

44. Ballah F, Maikai B, Magaji A, Shuaibu A, El-Nafaty A, Sambo Y, et al. Seroprevalence and risk of Toxoplasma gondii infection among pregnant women at Federal Teaching Hospital Gombe, Nigeria. Asian J Med Health. 2017; 3: 1–5.

45. Murebwayire E, Njanaake K, Ngabonziza JCS, Jaoko W, Njunwa KJ. Seroprevalence and risk factors of Toxoplasma gondii infection among pregnant women attending antenatal care in Kigali, Rwanda. Tanzan J Health Res. 2017;19.

46. Saajan AM, Nyindo M, Gidabayda JG, Abdallah MS, Jaffer SH, Mukhtar AG, et al. TORCH Antibodies Among Pregnant Women and Their Newborns Receiving Care at Kilimanjaro Christian Medical Centre, Moshi, Tanzania. East Afr Health Res J. 2017; 1: 95. https://doi.org/10.24248/EAHRJ-D-16-00340 PMID: 34308164

47. Bamba S, Cissé M, Sangaré I, Zida A, Ouattara S, Guiguemdé RT. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women from Bobo Dioulasso, Burkina Faso. BMC Infect Dis. 2017; 17: 482. https://doi.org/10.1186/s12879-017-2583-6 PMID: 28693432

48. Negussie A, Beyene E, Palani S. Toxoplasmosis and associated risk factors in antenatal clinic follow up Pregnant Women in Selected Health Institutes of Jigjiga, East Ethiopia. Int J Trop Health. 2017; 21: 1–7.

49. Yohanes T, Zerdo Z, Chufamo N, Abossie A. Toxoplasma gondii infection: seroprevalence and associated factors among pregnant women attending in antenatal clinic of Arba Minch hospital, south Ethiopia: cross sectional study. Transl Biomed. 2017; 8: 2172–0479.1000105.

50. Negero J, Yohannes M, Woldemichael K, Tegegne D. Seroprevalence and potential risk factors of T. gondii infection in pregnant women attending antenatal care at Bonga Hospital, Southwestern Ethiopia. Int J Infect Dis. 2017; 57: 44–49. https://doi.org/10.1016/j.ijid.2017.01.013 PMID: 28167254
antenatal care. Afr Health Sci. 2019; 19: 1858–1865. https://doi.org/10.4314/ahs.v19i2.8 PMID: 31656468

32. Todjom FG, Tsapi EM, Gamago GA, Vignoles P, Pone JW, Teukeng FD. Seroprevalence of toxoplasmosis and associated risk factors in pregnant women at the Protestant Hospital, Mbouo-Bandjoun, Cameroon. Afr J Clin Exp Microbiol. 2019; 20: 221–230.

33. Mabeku LB, Tchakounte C, Bonsi S, Etoa F-X. Prevalence of Toxoplasma gondii and associated risk factors among pregnant women attending hospital centers in Penka-Michel, Cameroon. J Sci Res Rep. 2018; 21: 1–11.

34. Jula J, Girones G, Edao B, Deme C, Cebrian J, Butrón L, et al. Seroprevalence of Toxoplasma gondii infection in pregnant women attending antenatal care in southern Ethiopia. Rev Esp Quimioter. 2018; 31: 363–366. https://doi.org/10.1371/journal.pmed.1001920 PMID: 29978983

35. Adeniyi OT, Adekola SS, Oladipo OM. Seroepidemiology of toxoplasmosis among pregnant women in Osogbo, Southwestern, Nigeria. J Infect Dis Immun. 2018; 10: 8–16.

36. NA HH, Shaapan RM, Hassanain H. Associated Antenatal Health Risk Factors with Incidence of Toxoplasmosis in Egyptian Pregnant Women. Pak J Biol Sci PJBS. 2018; 21: 463–468. https://doi.org/10.3923/pjbs.2018.463.468 PMID: 30724048

37. Dairo MD, Ogunjimi T, Ayinmode AB. Knowledge, risk factors and prevalence of toxoplasmosis among pregnant women at primary health care level in Ibadan, Southwestern Nigeria. Afr J Biomed Res. 2018; 21: 267–271.

38. Mohammed WM, Abdalla HS, Satti AB, Mustafa TB, Kabbashi AS. Sero-prevalence and associated risk factors of Toxoplasma gondii infection among pregnant women attending Omdurman friendship hospital, Omdurman. Ment Health Addict Res. 2018; 3: 1–3.

39. Paul E, Kiwelu I, Mmbaga B, Nazareth R, Sabuni E, Maro A, et al. Toxoplasma gondii seroprevalence among pregnant women attending antenatal clinic in Northern Tanzania. Trop Med Health. 2018; 46: 39. https://doi.org/10.1186/s41182-018-0122-9 PMID: 30479556

40. Tlamcani Z, Yahyaoui G, Mahmoud M. Prevalence of immunity to toxoplasmosis among pregnant women in University Hospital center Hassan II of FEZ city (Morocco). Acta Medica Int. 2017; 4: 43.

41. Pegha Moukandja I, Ngoungou EB, Lemamy GJ, Bisvigou U, Gessain A, Toure Ndouo FS, et al. Non-malarial infectious diseases of antenatal care in pregnant women in Franceville, Gabon. BMC Pregnancy Childbirth. 2017; 17: 185. https://doi.org/10.1186/s12884-017-1362-0 PMID: 28606185

42. El-Shqanqery HE, Ibrahim HM, Mohamed AH, El-Sharaawy AA. Seroprevalence of Toxoplasma gondii infection and associated risk factors among asymptomatic pregnant females in Egypt. J Egypt Soc Parasitol. 2017; 47: 93–100.

43. Frimpong C, Makasa M, Sitali L, Michelo C. Seroprevalence and determinants of toxoplasmosis in pregnant women attending antenatal clinic at the university teaching hospital, Lusaka, Zambia. BMC Infect Dis. 2017; 17: 1–8.

44. Ballah F, Maikai B, Magaji A, Shuaibu A, El-Nafaty A, Sambo Y, et al. Seroprevalence and risk of Toxoplasma gondii infection among pregnant women at Federal Teaching Hospital Gombe, Nigeria. Asian J Med Health. 2017; 3: 1–5.

45. Murebwayire E, Njanaake K, Ngabonziza JCS, Jaoko W, Njunwa KJ. Seroprevalence and risk factors of Toxoplasma gondii infection among pregnant women attending antenatal care in Kigali, Rwanda. Tanzan J Health Res. 2017;19.

46. Saajan AM, Nyindo M, Gidabayda JG, Abdallah MS, Jaffer SH, Mukhtar AG, et al. TORCH Antibodies Among Pregnant Women and Their Newborns Receiving Care at Kilimanjaro Christian Medical Centre, Moshi, Tanzania. East Afr Health Res J. 2017; 1: 95. https://doi.org/10.24248/EAHRJ-D-16-00340 PMID: 34308164

47. Bamba S, Cissé M, Sangaré I, Zida A, Ouattara S, Guiguemdé RT. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women from Bobo Dioulasso, Burkina Faso. BMC Infect Dis. 2017; 17: 482. https://doi.org/10.1186/s12879-017-2583-6 PMID: 28693432

48. Negussie A, Beyene E, Palani S. Toxoplasmosis and associated risk factors in antenatal clinic follow up Pregnant Women in Selected Health Institutes of Jigjiga, East Ethiopia. Int J Trop Health. 2017; 21: 1–7.

49. Yohanes T, Zerdo Z, Chufamo N, Abossie A. Toxoplasma gondii infection: seroprevalence and associated factors among pregnant women attending in antenatal clinic of Arba Minch hospital, south Ethiopia: cross sectional study. Transl Biomed. 2017; 8: 2172–0479.1000105.

50. Negero J, Yohannes M, Woldemichael K, Tegegne D. Seroprevalence and potential risk factors of T. gondii infection in pregnant women attending antenatal care at Bonga Hospital, Southwestern Ethiopia. Int J Infect Dis. 2017; 57: 44–49. https://doi.org/10.1016/j.ijid.2017.01.013 PMID: 28167254
51. Völker F, Cooper P, Bader O, Uy A, Zimmermann O, Lugert R, et al. Prevalence of pregnancy-relevant infections in a rural setting of Ghana. BMC Pregnancy Childbirth. 2017; 17: 172. https://doi.org/10.1186/s12884-017-1351-3 PMID: 28583150

52. Oboro IL, Obunge OK, Wariso KT. Sero-epidemiology of toxoplasmosis among pregnant women in the University of Port Harcourt Teaching Hospital, Nigeria. Niger Health J. 2016;16.

53. Abamecha F, Awel H. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women following antenatal care at Mizan Aman General Hospital, Bench Maji Zone (BMZ), Ethiopia. BMC Infect Dis. 2016; 16: 460. https://doi.org/10.1186/s12879-016-1806-6 PMID: 27585863

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55. Kwofie KD, Ghansah A, Osei JH, Frempong KK, Obed S, Frimpong EH, et al. Indication of Risk of Mother-to-Child Toxoplasma gondii Transmission in the Greater Accra Region of Ghana. Matern Child Health J. 2016; 20: 2581-2588. https://doi.org/10.1007/s10995-016-2084-z PMID: 27465060

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70. Njunda AL, Nsagha DS, Assob JN, Kamga HF, Tafili RT, Achidi EA. Seroepidemiology of toxoplasmosis in pregnant women attending the University Teaching Hospital in Yaounde, Cameroon. Int J Health Res. 2011; 4: 1–9.

71. Sitoe SP, Rafael B, Meireles LR, Andrade HF, Thompson R. Preliminary report of HIV and Toxoplasma gondii occurrence in pregnant women from Mozambique. Rev Inst Med Trop Sao Paulo. 2010; 52: 291–5. https://doi.org/10.1590/s0036-46652010000600002 PMID: 21225211

72. Khames M, Sihem S, Hizia H, Nguewa P. High toxoplasmosis seroprevalence among young pregnant women in Medea, Algeria. Ann Parasitol. 2020; 66: 509–515. https://doi.org/10.17420/ap6604.292 PMID: 33730475

73. Hafez Hassanain NA, Shaapan RM, Hafez Hassanain MA. Associated Antenatal Health Risk Factors with Incidence of Toxoplasmosis in Egyptian Pregnant Women. Pak J Biol Sci PJBS. 2018; 21: 463–468. https://doi.org/10.3923/pjbs.2018.463.468

74. El Bissati K, Levigne P, Lykins J, Adlaoui EB, Barkat A, Berraho A, et al. Global initiative for congenital toxoplasmosis: an observational and international comparative clinical analysis. Emerg Microbes Infect. 2018; 7: 165. https://doi.org/10.1038/s41426-018-0164-4 PMID: 30262847

75. Boughattas S, Ben-Abdallah R, Siala E, Souissi O, Aoun K, Bouratbine A. Direct genotypic characterization of Toxoplasma gondii strains associated with congenital toxoplasmosis in Tunisia (North Africa). Am J Trop Med Hyg. 2010; 82: 1041–1046. https://doi.org/10.4269/ajtmh.2010.09-0691 PMID: 20519598

76. Boughattas S, Abdallah RB, Siala E, Aoun K, Bouratbine A. An atypical strain associated with congenital toxoplasmosis in Tunisia. New Microbiol. 2011; 34: 413–416. PMID: 22143816

77. Boughattas S, Ben-Abdallah R, Siala E, Souissi O, Maatoug R, Aoun K, et al. Case of fatal congenital toxoplasmosis associated with I/III recombinant genotype. Trop Biomed. 2011; 28: 615–619. PMID: 22433891

78. Lachkhem A, Galal L, Lahmar I, Passebosc K, Riahi H, Plault N, et al. First isolation and genotyping of Toxoplasma gondii strains from domestic animals in Tunisia. Sci Rep. 2021; 11: 9328. https://doi.org/10.1038/s41598-021-88751-1 PMID: 33927299

79. Leroy J, Houzé S, Dardé M-L, Yéra H, Rossi B, Delhaes L, et al. Severe toxoplasmosis imported from tropical Africa in immunocompetent patients: A case series. Travel Med Infect Dis. 2019; 10: 101509. https://doi.org/10.1016/j.tmaid.2019.101509 PMID: 31712179

80. Ajzenberg D, Cogné N, Paris L, Bessières M-H, Thulliez P, Filisetti D, et al. Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J Infect Dis. 2002; 186: 684–689. https://doi.org/10.1086/342663 PMID: 12195356

81. Mercier A, Devillard S, Ngoubangoye B, Bonnabau H, Bañuls A-L, Durand P, et al. Additional Haplogroups of Toxoplasma gondii out of Africa: Population Structure and Mouse-Virulence of Strains from Gabon. PLoS Negl Trop Dis. 2010; 4: e876. https://doi.org/10.1371/journal.pntd.0000876 PMID: 21072237

82. Mizani A, Alipour A, Sharif M, Sarvi S, Amouei A, Shokri A, et al. Toxoplasmosis seroprevalence in Iranian women and risk factors of the disease: a systematic review and meta-analysis. Trop Med Health. 2017; 45: 7. https://doi.org/10.1186/s41182-017-0048-7 PMID: 28413330

83. Daryani A, Sarvi S, Aarabi M, Mizani A, Ahmadpour E, Shokri A, et al. Seroprevalence of Toxoplasma gondii in the Iranian general population: a systematic review and meta-analysis. Acta Trop. 2014; 137: 185–194. https://doi.org/10.1016/j.actatropica.2014.05.015 PMID: 24887263

84. Nayeri T, Sarvi S, Moosazadeh M, Amouei A, Hosseininejad Z, Daryani A. The global seroprevalence of anti-Toxoplasma gondii antibodies in women who had spontaneous abortion: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2020; 14: e0008103. https://doi.org/10.1371/journal.pntd.0008103 PMID: 32168351

85. Shiadeh MN, Esfandyari S, Ashrafmansouri M, Mirzapour A, Taghipour A, Spotin A, et al. The prevalence of latent and acute toxoplasmosis in HIV-infected pregnant women: A systematic review and meta-analysis. Microb Pathog. 2020; 149: 104549. https://doi.org/10.1016/j.micpath.2020.104549 PMID: 33010362

86. Ogoina D, Onyemelukwe GC, Musa BO, Obiako RO. Seroprevalence of IgM and IgG antibodies to Toxoplasma infection in healthy and HIV-positive adults from Northern Nigeria. J Infect Dev Ctries. 2013; 7: 398–403. https://doi.org/10.3855/jidc.2797 PMID: 23669429

87. Rostami A, Riahi SM, Gamble HR, Fakhri Y, Shiadeh MN, Danesh M, et al. Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis. Clin Microbiol Infect. 2020; 26: 673–683. https://doi.org/10.1016/j.cmi.2020.01.008 PMID: 31972316
69. Sattti AB, Suliman H, Suad BM. Serological and molecular diagnosis of toxoplasmosis in pregnant women in. Sudan Med Lab J. 2011; 1: 48–60.

70. Njunda AL, Nsagha DS, Assob JN, Kamga HF, Tafili RT, Achidi EA. Seroepidemiology of toxoplasmosis in pregnant women attending the University Teaching Hospital in Yaounde, Cameroon. Int J Health Res. 2011; 4: 1–9.

71. Sitoe SP, Rafael B, Meireles LR, Andrade HF, Thompson R. Preliminary report of HIV and Toxoplasma gondii occurrence in pregnant women from Mozambique. Rev Inst Med Trop Sao Paulo. 2010; 52: 291–5. https://doi.org/10.1590/s0036-46652010000600002 PMID: 21225211

72. Khames M, Sihem S, Hizia H, Nguewa P. High toxoplasmosis seroprevalence among young pregnant women in Medea, Algeria. Ann Parasitol. 2020; 66: 509–515. https://doi.org/10.17420/ap6604.292 PMID: 33730475

73. Hafez Hassanain NA, Shaapan RM, Hafez Hassanain MA. Associated Antenatal Health Risk Factors with Incidence of Toxoplasmosis in Egyptian Pregnant Women. Pak J Biol Sci PJBS. 2018; 21: 463–468. https://doi.org/10.3923/pjbs.2018.463.468

74. El Bissati K, Levigne P, Lykins J, Adlaoui EB, Barkat A, Berraho A, et al. Global initiative for congenital toxoplasmosis: an observational and international comparative clinical analysis. Emerg Microbes Infect. 2018; 7: 165. https://doi.org/10.1038/s41426-018-0164-4 PMID: 30262847

75. Boughattas S, Ben-Abdallah R, Siala E, Souissi O, Aoun K, Bouratbine A. Direct genotypic characterization of Toxoplasma gondii strains associated with congenital toxoplasmosis in Tunisia (North Africa). Am J Trop Med Hyg. 2010; 82: 1041–1046. https://doi.org/10.4269/ajtmh.2010.09-0691 PMID: 20519598

76. Boughattas S, Abdallah RB, Siala E, Aoun K, Bouratbine A. An atypical strain associated with congenital toxoplasmosis in Tunisia. New Microbiol. 2011; 34: 413–416. PMID: 22143816

77. Boughattas S, Ben-Abdallah R, Siala E, Souissi O, Maatoug R, Aoun K, et al. Case of fatal congenital toxoplasmosis associated with I/III recombinant genotype. Trop Biomed. 2011; 28: 615–619. PMID: 22433891

78. Lachkhem A, Galal L, Lahmar I, Passebosc K, Riahi H, Plault N, et al. First isolation and genotyping of Toxoplasma gondii strains from domestic animals in Tunisia. Sci Rep. 2021; 11: 9328. https://doi.org/10.1038/s41598-021-88751-1 PMID: 33927299

79. Leroy J, Houzé S, Dardé M-L, Yéra H, Rossi B, Delhaes L, et al. Severe toxoplasmosis imported from tropical Africa in immunocompetent patients: A case series. Travel Med Infect Dis. 2019; 10: 101509. https://doi.org/10.1016/j.tmaid.2019.101509 PMID: 31712179

80. Ajzenberg D, Cogné N, Paris L, Bessières M-H, Thulliez P, Filisetti D, et al. Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J Infect Dis. 2002; 186: 684–689. https://doi.org/10.1086/342663 PMID: 12195356

81. Mercier A, Devillard S, Ngoubangoye B, Bonnabau H, Bañuls A-L, Durand P, et al. Additional Haplogroups of Toxoplasma gondii out of Africa: Population Structure and Mouse-Virulence of Strains from Gabon. PLoS Negl Trop Dis. 2010; 4: e876. https://doi.org/10.1371/journal.pntd.0000876 PMID: 21072237

82. Mizani A, Alipour A, Sharif M, Sarvi S, Amouei A, Shokri A, et al. Toxoplasmosis seroprevalence in Iranian women and risk factors of the disease: a systematic review and meta-analysis. Trop Med Health. 2017; 45: 7. https://doi.org/10.1186/s41182-017-0048-7 PMID: 28413330

83. Daryani A, Sarvi S, Aarabi M, Mizani A, Ahmadpour E, Shokri A, et al. Seroprevalence of Toxoplasma gondii in the Iranian general population: a systematic review and meta-analysis. Acta Trop. 2014; 137: 185–194. https://doi.org/10.1016/j.actatropica.2014.05.015 PMID: 24887263

84. Nayeri T, Sarvi S, Moosazadeh M, Amouei A, Hosseininejad Z, Daryani A. The global seroprevalence of anti-Toxoplasma gondii antibodies in women who had spontaneous abortion: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2020; 14: e0008103. https://doi.org/10.1371/journal.pntd.0008103 PMID: 32168351

85. Shiadeh MN, Esfandyari S, Ashrafmansouri M, Mirzapour A, Taghipour A, Spotin A, et al. The prevalence of latent and acute toxoplasmosis in HIV-infected pregnant women: A systematic review and meta-analysis. Microb Pathog. 2020; 149: 104549. https://doi.org/10.1016/j.micpath.2020.104549 PMID: 33010362

86. Ogoina D, Onyemelukwe GC, Musa BO, Obiako RO. Seroprevalence of IgM and IgG antibodies to Toxoplasma infection in healthy and HIV-positive adults from Northern Nigeria. J Infect Dev Ctries. 2013; 7: 398–403. https://doi.org/10.3855/jidc.2797 PMID: 23669429

87. Rostami A, Riahi SM, Gamble HR, Fakhri Y, Shiadeh MN, Danesh M, et al. Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis. Clin Microbiol Infect. 2020; 26: 673–683. https://doi.org/10.1016/j.cmi.2020.01.008 PMID: 31972316
88. Elsafi SH, Al-Mutairi WF, Al-Jubran KM, Abu Hassan MM, Al Zahrani EM. Toxoplasmosis seroprevalence in relation to knowledge and practice among pregnant women in Dhahran, Saudi Arabia. Pathog Glob Health. 2015; 109: 377–382. https://doi.org/10.1080/20477724.2015.1103502 PMID: 26924348

89. Iddawela D, Vithana SMP, Ratnayake C. Seroprevalence of toxoplasmosis and risk factors of Toxoplasma gondii infection among pregnant women in Sri Lanka: a cross sectional study. BMC Public Health. 2017; 17: 1–6.

90. Sakikawa M, Noda S, Hanaoka M, Nakayama H, Hojo S, Kakinoki S, et al. Anti-Toxoplasma antibody prevalence, primary infection rate, and risk factors in a study of toxoplasmosis in 4,466 pregnant women in Japan. Clin Vaccine Immunol. 2012; 19: 365–367. https://doi.org/10.1128/CVI.05486-11 PMID: 22205659

91. Findal G, Barlinn R, Sandven I, Stray-Pedersen B, Nordbø SA, Samdal HH, et al. Toxoplasma prevalence among pregnant women in Norway: a cross-sectional study. Apmis. 2015; 123: 321–325. https://doi.org/10.1111/apm.12354 PMID: 25628065

92. Montazeri M, Mikaeili Galeh T, Moosazadeh M, Sarvi S, Dodangeh S, Javidnia J, et al. The global serological prevalence of Toxoplasma gondii in felids during the last five decades (1967–2017): a systematic review and meta-analysis. Parasit Vectors. 2020; 13: 82. https://doi.org/10.1186/s13071-020-3954-1 PMID: 32066495

93. Hatam-Nahavandi K, Calero-Bernal R, Rahimi MT, Pagheh AS, Zarean M, Dezhkam A, et al. Toxoplasma gondii infection in domestic and wild felids as public health concerns: a systematic review and meta-analysis. Sci Rep. 2021; 11: 9509. https://doi.org/10.1038/s41598-021-89031-8 PMID: 33947922

94. Mose JM, Kagira JM, Kamau DM, Maina NW, Ngotho M, Karanja SM. A review on the present advances on studies of toxoplasmosis in eastern Africa. BioMed Res Int. 2020;2020. https://doi.org/10.1155/2020/7135268 PMID: 32724808

95. Dubey JP, Lago EG, Gennari SM, Su C, Jones JL. Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology. 2012; 139: 1375–1424. https://doi.org/10.1017/S0031182012000765 PMID: 22776427

96. Zhu S, Shapiro K, VanWormer E. Dynamics and epidemiology of Toxoplasma gondii oocyst shedding in domestic and wild felids. Transbound Emerg Dis. 2022; 69: 2412–2423. https://doi.org/10.1111/tbed.14197 PMID: 34153160

97. Robert-Gangneux F, Guegan H. Anti-Toxoplasma IgG assays: What performances for what purpose? A systematic review. Parasite. 2021;28.

98. Yéngué JF, Essomba CMN, Ndzengue GEA, Sonela N, Lobè EE, Tchouaket MCT, et al. Performance of immunochromatographic and immunoenzymatic techniques in the diagnosis of toxoplasmosis in pregnant women in Cameroon: need for harmonization.

99. Gomez CA, Budvytyte LN, Press C, Zhou L, McLeod R, Maldonado Y, et al. Evaluation of three point-of-care tests for detection of toxoplasma immunoglobulin IgG and IgM in the United States: proof of concept and challenges. Oxford University Press US; 2018. p. ofy215.

100. Foroutan-Rad M, Khademvatan S, Majidiani H, Aryamand S, Rahim F, Malehi AS. Seroprevalence of Toxoplasma gondii in the Iranian pregnant women: a systematic review and meta-analysis. Acta Trop. 2016; 158: 160–169. https://doi.org/10.1016/j.actatropica.2016.03.003 PMID: 26952970

101. Wei H-X, He C, Yang P-L, Lindsay DS, Peng H-J. Relationship between cat contact and infection by Toxoplasma gondii in humans: a meta-analysis. Comp Parasitol. 2016; 83: 11–19.

102. Malarvizhi A, Viswanathan T, Lavanya V, Arul Sheeba Malar S, Moorthy K. Seroprevalence of Toxoplasma gondii in pregnant women. J Public Health Epidemiol. 2012; 4: 170–7.

103. Olariu TR, Ursoniu S, Hotea I, Dumitrascu V, Anastasiu D, Lupu MA. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women from Western Romania. Vector-Borne Zoonotic Dis. 2020; 20: 763–767. https://doi.org/10.1089/vbz.2019.2599 PMID: 32589521

104. Al-Adhroey AH, Mehrass AA-KO, Al-Shammakh AA, Ali AD, Akabat MYM, Al-Mekhlafi HM. Prevalence and predictors of Toxoplasma gondii infection in pregnant women from Dhamar, Yemen. BMC Infect Dis. 2019; 19: 1089. https://doi.org/10.1186/s12879-019-4718-4 PMID: 31888517

105. Tarekegn ZS, Dejene H, Addisu A, Dagnachew S. Potential risk factors associated with seropositivity for Toxoplasma gondii among pregnant women and HIV infected individuals in Ethiopia: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2020; 14: e0008944. https://doi.org/10.1371/journal.pntd.0008944 PMID: 33320848

106. Retmanasari A, Widartono BS, Wijayanti MA, Artama WT. Prevalence and risk factors for toxoplasmosis in Middle Java, Indonesia. EcoHealth. 2017; 14: 162–170. https://doi.org/10.1007/s10393-016-1198-5 PMID: 27830388
88. Elsafi SH, Al-Mutairi WF, Al-Jubran KM, Abu Hassan MM, Al Zahrani EM. Toxoplasmosis seroprevalence in relation to knowledge and practice among pregnant women in Dhahran, Saudi Arabia. Pathog Glob Health. 2015; 109: 377–382. https://doi.org/10.1080/20477724.2015.1103502 PMID: 26924348

89. Iddawela D, Vithana SMP, Ratnayake C. Seroprevalence of toxoplasmosis and risk factors of Toxoplasma gondii infection among pregnant women in Sri Lanka: a cross sectional study. BMC Public Health. 2017; 17: 1–6.

90. Sakikawa M, Noda S, Hanaoka M, Nakayama H, Hojo S, Kakinoki S, et al. Anti-Toxoplasma antibody prevalence, primary infection rate, and risk factors in a study of toxoplasmosis in 4,466 pregnant women in Japan. Clin Vaccine Immunol. 2012; 19: 365–367. https://doi.org/10.1128/CVI.05486-11 PMID: 22205659

91. Findal G, Barlinn R, Sandven I, Stray-Pedersen B, Nordbø SA, Samdal HH, et al. Toxoplasma prevalence among pregnant women in Norway: a cross-sectional study. Apmis. 2015; 123: 321–325. https://doi.org/10.1111/apm.12354 PMID: 25628065

92. Montazeri M, Mikaeili Galeh T, Moosazadeh M, Sarvi S, Dodangeh S, Javidnia J, et al. The global serological prevalence of Toxoplasma gondii in felids during the last five decades (1967–2017): a systematic review and meta-analysis. Parasit Vectors. 2020; 13: 82. https://doi.org/10.1186/s13071-020-3954-1 PMID: 32066495

93. Hatam-Nahavandi K, Calero-Bernal R, Rahimi MT, Pagheh AS, Zarean M, Dezhkam A, et al. Toxoplasma gondii infection in domestic and wild felids as public health concerns: a systematic review and meta-analysis. Sci Rep. 2021; 11: 9509. https://doi.org/10.1038/s41598-021-89031-8 PMID: 33947922

94. Mose JM, Kagira JM, Kamau DM, Maina NW, Ngotho M, Karanja SM. A review on the present advances on studies of toxoplasmosis in eastern Africa. BioMed Res Int. 2020;2020. https://doi.org/10.1155/2020/7135268 PMID: 32724808

95. Dubey JP, Lago EG, Gennari SM, Su C, Jones JL. Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology. 2012; 139: 1375–1424. https://doi.org/10.1017/S0031182012000765 PMID: 22776427

96. Zhu S, Shapiro K, VanWormer E. Dynamics and epidemiology of Toxoplasma gondii oocyst shedding in domestic and wild felids. Transbound Emerg Dis. 2022; 69: 2412–2423. https://doi.org/10.1111/tbed.14197 PMID: 34153160

97. Robert-Gangneux F, Guegan H. Anti-Toxoplasma IgG assays: What performances for what purpose? A systematic review. Parasite. 2021;28.

98. Yéngué JF, Essomba CMN, Ndzengue GEA, Sonela N, Lobè EE, Tchouaket MCT, et al. Performance of immunochromatographic and immunoenzymatic techniques in the diagnosis of toxoplasmosis in pregnant women in Cameroon: need for harmonization.

99. Gomez CA, Budvytyte LN, Press C, Zhou L, McLeod R, Maldonado Y, et al. Evaluation of three point-of-care tests for detection of toxoplasma immunoglobulin IgG and IgM in the United States: proof of concept and challenges. Oxford University Press US; 2018. p. ofy215.

100. Foroutan-Rad M, Khademvatan S, Majidiani H, Aryamand S, Rahim F, Malehi AS. Seroprevalence of Toxoplasma gondii in the Iranian pregnant women: a systematic review and meta-analysis. Acta Trop. 2016; 158: 160–169. https://doi.org/10.1016/j.actatropica.2016.03.003 PMID: 26952970

101. Wei H-X, He C, Yang P-L, Lindsay DS, Peng H-J. Relationship between cat contact and infection by Toxoplasma gondii in humans: a meta-analysis. Comp Parasitol. 2016; 83: 11–19.

102. Malarvizhi A, Viswanathan T, Lavanya V, Arul Sheeba Malar S, Moorthy K. Seroprevalence of Toxoplasma gondii in pregnant women. J Public Health Epidemiol. 2012; 4: 170–7.

103. Olariu TR, Ursoniu S, Hotea I, Dumitrascu V, Anastasiu D, Lupu MA. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women from Western Romania. Vector-Borne Zoonotic Dis. 2020; 20: 763–767. https://doi.org/10.1089/vbz.2019.2599 PMID: 32589521

104. Al-Adhroey AH, Mehrass AA-KO, Al-Shammakh AA, Ali AD, Akabat MYM, Al-Mekhlafi HM. Prevalence and predictors of Toxoplasma gondii infection in pregnant women from Dhamar, Yemen. BMC Infect Dis. 2019; 19: 1089. https://doi.org/10.1186/s12879-019-4718-4 PMID: 31888517

105. Tarekegn ZS, Dejene H, Addisu A, Dagnachew S. Potential risk factors associated with seropositivity for Toxoplasma gondii among pregnant women and HIV infected individuals in Ethiopia: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2020; 14: e0008944. https://doi.org/10.1371/journal.pntd.0008944 PMID: 33320848

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114. Etougbétché JR, Hamidović A, Dossou H-J, Coan-Grosso M, Roques R, Plault N, et al. Molecular prevalence, genetic characterization and patterns of Toxoplasma gondii infection in domestic small mammals from Cotonou, Benin. Parasite Paris Fr. 2022; 29: 58. https://doi.org/10.1051/parasite/2022058 PMID: 36562439

115. Gómez-Marin JE, de-la-Torre A, Angel-Muller E, Rubio J, Arenas J, Osorio E, et al. First Colombian Multicentric Newborn Screening for Congenital Toxoplasmosis. Cappello M, editor. PLoS Negl Trop Dis. 2011; 5: e1195. https://doi.org/10.1371/journal.pntd.0001195 PMID: 21655304

116. Amagbégnon R, Dechavanne C, Dambrun M, Yehouénou U, Akondé N, Migot-Nabias F, et al. Seroepidemiology of toxoplasmosis in pregnant women and detection of infection acquired during pregnancy in Cotonou, Benin. 2023.

117. Bongomin F, Govender NP, Chakrabarti A, Robert-Gangneux F, Boulware DR, Zafar A, et al. Essential in vitro diagnostics for advanced HIV and serious fungal diseases: international experts' consensus recommendations. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2019; 38: 1581–1584. https://doi.org/10.1007/s10096-019-03600-4 PMID: 31175479
107. Mohamed K, Bahathiq A, Degnah N, Basuni S, Al Malki A, Babalghith A. Detection of Toxoplasma gondii infection and associated risk factors among pregnant women in Makkah Al Mukarramah, Saudi Arabia. Asian Pac J Trop Dis. 2016; 6: 113–119.

108. Ybañez RHD, Busmeon CGR, Viernes ARG, Langbid JZ, Nuevarez JP, Ybanez AP, et al. Endemicity of Toxoplasma infection and its associated risk factors in Cebu, Philippines. PloS One. 2019; 14: e0217989. https://doi.org/10.1371/journal.pone.0217989 PMID: 31188858

109. da Silva MG, Câmara JT, Vinaud MC, de Castro AM. Epidemiological factors associated with seropositivity for toxoplasmosis in pregnant women from Gurupi, State of Tocantins, Brazil. Rev Soc Bras Med Trop. 2014; 47: 469–475. https://doi.org/10.1590/0037-8682-0127-2014 PMID: 25229288

110. Belluco S, Simonato G, Mancin M, Pietrobelli M, Ricci A. Toxoplasma gondii infection and food consumption: a systematic review and meta-analysis of case-controlled studies. Crit Rev Food Sci Nutr. 2018; 58: 3085–3096. https://doi.org/10.1080/10408398.2017.1352563 PMID: 29020460

111. Hussain MA, Stitt V, Szabo EA, Nelan B. Toxoplasma gondii in the Food Supply. Pathogens. 2017; 6: 21. https://doi.org/10.3390/pathogens6020021 PMID: 28587147

112. Fakhfakh N, Kallel K, Ennigro S, Kaouech E, Belhadj S, Chaker E. Risk factors for Toxoplasma gondii and immune status of pregnant women: cause and effect? Tunis Med. 2013; 91: 188–190.

113. Alvarado-Esquivel C, Estrada-Martínez S, Liesenfeld O. Toxoplasma gondii infection in workers occupationally exposed to unwashed raw fruits and vegetables: a case control seroprevalence study. Parasit Vectors. 2011; 4: 235. https://doi.org/10.1186/1756-3305-4-235 PMID: 22177118

114. Etougbétché JR, Hamidović A, Dossou H-J, Coan-Grosso M, Roques R, Plault N, et al. Molecular prevalence, genetic characterization and patterns of Toxoplasma gondii infection in domestic small mammals from Cotonou, Benin. Parasite Paris Fr. 2022; 29: 58. https://doi.org/10.1051/parasite/2022058 PMID: 36562439

115. Gómez-Marin JE, de-la-Torre A, Angel-Muller E, Rubio J, Arenas J, Osorio E, et al. First Colombian Multicentric Newborn Screening for Congenital Toxoplasmosis. Cappello M, editor. PLoS Negl Trop Dis. 2011; 5: e1195. https://doi.org/10.1371/journal.pntd.0001195 PMID: 21655304

116. Amagbégnon R, Dechavanne C, Dambrun M, Yehouénou U, Akondé N, Migot-Nabias F, et al. Seroepidemiology of toxoplasmosis in pregnant women and detection of infection acquired during pregnancy in Cotonou, Benin. 2023.

117. Bongomin F, Govender NP, Chakrabarti A, Robert-Gangneux F, Boulware DR, Zafar A, et al. Essential in vitro diagnostics for advanced HIV and serious fungal diseases: international experts' consensus recommendations. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2019; 38: 1581–1584. https://doi.org/10.1007/s10096-019-03600-4 PMID: 31175479