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Assessment of simultaneous IgM, IgG avidity, and IgA testing in diagnosis of acute toxoplasmosis in pregnant women: a systematic review and meta-analysis study

BMC Pregnancy and Childbirth volume 25, Article number: 537 (2025) Cite this article

Abstract

Backgrounds

Toxoplasma gondii is a relatively common parasite with a global prevalence that can cause toxoplasmosis. This infection usually does not have clear symptoms, so timely and accurate detection plays a major role in the treatment of this disease. This study reviewed Toxoplasma antibodies dependent serologic tests in pregnancy, assessing their diagnostic effectiveness to guide healthcare providers, particularly obstetricians and gynecologists.

Methods

In this systematic review and meta-analysis, we utilized four different databases for our search and adhered to the PRISMA guidelines to collect pertinent studies in duration of 2000 to April 2024. After carefully evaluating the inclusion/exclusion criteria list, we ultimately selected 67 qualifying studies for our analysis and subjecting the obtained data to statistical scrutiny.

Results

Data analysis revealed that the pooled seroprevalence of IgM anti-T. gondii among pregnant women tested were 2.1% (95% CI = 1.67 to 3.03). Moreover, the weighted seroprevalence rate estimate of low IgG avidity in IgM-positive pregnant women was 30% (95% CI = 28 to 31) and the seroprevalence of IgA in IgM-positive pregnant women was 43% (95% CI = 18 to 70). Combining the IgG avidity test results with those of IgM and IgA can significantly improve the accuracy of diagnosing recent and past Toxoplasma infections.

Conclusions

This approach is particularly valuable for pregnant women, as it improves the reliability of serological test outcomes and helps to provide timely treatment and mitigate irreversible complications associated with toxoplasmosis.

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Backgrounds

Toxoplasmosis is a common disease between humans and animals, which is caused by a eukaryotic parasite from the phylum Apicomplexa called Toxoplasma gondii (T. gondii). T. gondii can cause disease in humans by consuming meat (cysts), water, food, and contaminated soil (oocytes) [1, 2].

About one-third of the world’s individuals have anti-Toxoplasma antibodies in their blood [3]. T. gondii infection can range from asymptomatic disease in individuals with complete immunity to severe cases in individuals with weak immune systems [4]. Also, about 200,000 cases of toxoplasmosis occur during pregnancy [4].

In the initial infection, if T. gondii is transmitted through the placenta, it can lead to irreparable consequences in the fetus [5]. The stage of pregnancy at which the infection occurs is the primary determinant of the risk of fetal harm [6]. Past maternal infection with parasites has no effect on fetal development [5]. Fetal infection occurs when the parasite is present in the mother’s blood and before the appearance of anti-T. gondii antibodies [7].

The most serious consequence of toxoplasmosis occurs in the first and second trimesters during pregnancy and causes vertical transmission to the fetus [8, 9]. The rate of this form of the disease is 1–14 cases per 10,000 pregnancies [10]. Congenital infected babies can show specific signs and symptoms such as hydrocephalus, microcephaly, chorioretinitis, brain calcification, mental disorders, movement, and seizures [11, 12]. The parasite strain can have a great impact on the clinical condition of the baby or fetus [13].

Evaluation of antibodies is common in the diagnosis of toxoplasmosis, but it is relatively difficult to diagnose it quickly and definitively [14, 15]. Serological methods are common in the diagnosis of toxoplasmosis, but the results of these methods collect indirect information that must be interpreted carefully. A positive serological test (IgG, IgM, and IgA) alone does not indicate an existing infection, as Toxoplasma antibodies are present in the blood of many humans for various reasons [16]. On the other hand, to prove the acute disease of toxoplasmosis, the high level of toxoplasma antibody in the blood is not enough, although it is a suitable guide for diagnosis evaluations. Sometimes, for various reasons, only antibodies evaluation is not useful for the acute stages of T. gondii, including long-term responses, delay in the production of these antibodies, or non-specific polyclonal responses against various factors [17, 18].

In recent years, the discovery of the IgG avidity ELISA method, which only evaluates IgG class antibodies, is a suitable solution for differentiating between acute and chronic T. gondii infections. At the beginning of the infection, the affinity of the antibody to bind to the antigen is in a low avidity (Acute toxoplasmosis). With the continuation of the infection, the tendency these antibodies to bind to the antigen of the T. gondii parasite increases and is in a high avidity, which is a sign of a long-term infection [10, 19].

This study aims to investigate serology tests related to T. gondii and pregnancy, determine the effectiveness of these tests in diagnosis, and inform healthcare providers, including obstetricians and gynecologists.

Methods

Study design and search strategy

Search based on keywords Toxoplasma infection, Toxoplasma gondii, T. gondii, pregnancy, Toxoplasma antibodies (IgG, IgM, and IgA), IgG avidity, congenital, diagnosis and “AND”, “OR” operators by two independent reviewers (M.T and B.B) in four databases (PubMed, Scopus, Web of Science and Google Scholar) in duration of 2000 to April 2024 were performed. Based on PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analysis) principles, two independent reviewers screened titles and abstracts against predefined inclusion criteria (Fig. 1). In the case of disagreement on the eligibility of the two authors, the third author made the final decision (S.A.H). Potentially eligible studies were retrieved, and M.T and B.B independently assessed them for final inclusion (Fig. 1). Conflicts were resolved through discussion or consultation with a third reviewer (S.A.H). Furthermore, End Note 21 software was used for initial screening to remove duplicates and assist in title/abstract screening.

Fig. 1
figure 1

Flow diagram of the study process based on PRISMA statement

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Quality assessment

The quality of reporting in the studies was evaluated using the Standardized Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklist, which was completed by two authors (M.T and B.B) [20]. The checklist consists of six main sections (Title and Abstract, Introduction, Methods, Results, Discussion, and Other Information) and evaluates various aspects of study design, methods, and reporting, such as sample size, statistical tests, and limitations. Based on the STROBE assessment, we categorized the studies into three quality levels: low (scores below 16.5), moderate (scores ranging from 16.6 to 25.5), and high (scores between 25.6 and 34). The articles included in this study were found to be of acceptable quality.

Inclusion and exclusion criteria

Inclusion criteria included (1) cross-sectional studies on Toxoplasma IgG avidity and pregnancy; (2) articles available from 2000 to April 2024; (3) English text of studies; and (4) human studies. Exclusion criteria included (1) Studies in languages other than English; (2) unrelated articles on Toxoplasma IgG avidity and pregnancy; and (3) lack of access to the full text of the article.

Data extraction

Two authors (M.T and B.B) thoroughly examined the selected articles and extracted relevant data and S.A.H resolved disagreements consensus. Primary outcomes including: The name of first author and the publication year of paper, as well as Secondary outcomes such as country, mean age of participants, total sample, number and percentage of positive IgM, and number of low avidity index. Moreover, no automation tools were used for data extraction. Finally, a baseline table based on study characteristics was designed.

Statistical analysis

In our study, StatsDirect statistical software package version 2.6.1 was used for data meta-analysis. Cochrane test based on χ2 (Q) test and I2 index was used to show heterogeneity between studies [21]. The results from the individual studies were combined using a random effects model. A forest plot was utilized to display the low IgG avidity of toxoplasmosis in pregnant women across each study, as well as to calculate the overall pooled seroprevalence estimate of the studies included in the meta-analysis. Additionally, we performed funnel plots and Egger’s regression test to assess publication bias (PB) and statistical significance [22], respectively. This study was registered in the open-access online database PROSPERO (International Prospective Register of Systematic Reviews) with code CRD42024542274.

Results

After an initial search based on keywords from 4 internet databases, a total of 2460 studies were obtained. After screening and removing duplicates, 67 studies were eligible in the study based on inclusion and exclusion criteria. Analysis of heterogeneity (95.7%, 95% CI = 95.2–96.1%, P value < 0.001) demonstrated heterogeneity between included studies in this systematic review since we selected a random effect for obtaining estimation of results. Data analysis in this study, the pooled seroprevalence of low avidity in pregnant women with suspected acute toxoplasmosis (IgM+) was 30% (95% CI = 28 to 31) (Fig. 2). The results of Egger’s test (Egger bias = 1.11, 95% CI = -1.79 to 4.02, P = 0.447) do not show a significant publication bias in low avidity in IgM-positive pregnant women (Fig. 3). The analysis results in different groups showed that the overall seroprevalence of IgG antibodies in pregnant women in this study was 39% (95% CI = 35 to 43). In addition, the pooled seroprevalence of IgM antibodies in these individuals was 2.3%. (95% CI = 1.67 to 3.03). The pooled seroprevalence of IgA antibodies during pregnancy with suspected acute toxoplasmosis (IgM+) was estimated to be 43% (95% CI = 18 to 70) (Table 1). More information is available in Table 2. The mean age of the individuals involved in the study was 28.2 years. In total, studies were conducted in 36 countries. The number of studies conducted in Asia, Europe, America, and Africa was 25, 23, 10 and 9 studies, respectively. The most studies conducted in Asia, Europe, America, and Africa were in Iran (n = 9), Turkey (n = 8), Brazil (n = 8) and Egypt (n = 3), respectively.

Fig. 2
figure 2

Forest plot of prevalence of low IgG avidity in pregnant women with suspected acute toxoplasmosis (IgM+)

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Fig. 3
figure 3

Bias assessment plot based on standard error in pregnant women with acute toxoplasmosis (low IgG avidity in IgM+)

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Table 1 Pooled seroprevalence of acute and chronic toxoplasmosis (IgM+, IgG+, and IgA+) in pregnant women
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Table 2 Baseline characteristics of included studies
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Discussion

T. gondii is a highly significant opportunistic pathogen in humans, posing a silent threat to many populations globally, and the differential diagnosis of recent infection from past infection during pregnancy is a great challenge [7]. Toxoplasmosis presents a notable risk during pregnancy, as it endangers the developing fetus. This parasite breaches the placental barrier, leading to fetal involvement and potentially resulting in adverse outcomes. The likelihood of infection transmission from mother to child escalates with pregnancy stage, underscoring the need for preventive measures and vigilance in monitoring throughout gestation. Scientific studies consistently demonstrate that Toxoplasma infection heightens the risk of miscarriage, emphasizing the critical role of proper prenatal care and condition management [16, 17]. The United Nations (UN) focus on preventing preventable deaths before 2030 is in line with sustainable development programs. By improving the conditions of mother and baby, these programs greatly reduce the mortality and adverse consequences of toxoplasmosis in babies and children. Since the lack of early and accurate diagnosis of toxoplasmosis during pregnancy may have irreparable consequences for the fetus or newborn, it seems that the effort to find a group of serological tests that have the maximum efficiency for distinguishing recent infection from chronic seems necessary. Classification of included studies in this review showed that 67 collected studies were conducted in 36 countries. The low number of countries indicates that the avidity-based toxoplasmosis-screening programs is not widely implemented. Countries have different policies regarding screening for toxoplasmosis in pregnant women. In France, Italy, Austria, Lithuania, and Slovenia, mandatory screening is performed on pregnant women [88], but in some other countries, such as the United States [89] or Canada [90], and other countries, they do not recommend this screening.

Based on the results of this systematic review, it was observed that IgG antibodies were prevalent in 39% of pregnant women. Notably, IgG antibodies typically appear in the bloodstream approximately 14 days after infection, with their maximum concentration occurring at 3 months. Subsequently, the antibody levels often decline but remain detectable throughout an individual’s lifetime. In the context of toxoplasmosis screening programs (prevent and control), the absence of IgG antibodies before pregnancy and the positivity of these antibodies during pregnancy can be a warning signal for potentially in the diagnosis of acute toxoplasmosis [91].

Analysis of our study showed that only 30% of pregnant women with positive IgM (suspected acute toxoplasmosis) had low IgG avidity, indicating that the false positives of this test are very significant. IgM antibodies can be measured about 7 days after acute infection, and they are among the first antibodies to appear in the blood. The titer of these antibodies reaches its maximum value after 1–3 months and then slowly decreases until 9 months until it becomes undetectable. However, in 9 to 27% of infected individuals, IgM antibodies persist in the blood for 2 years or more [92, 93].

False-positive outcomes in IgM tests can occur due to various factors, including Autoimmune antibodies, such as rheumatoid factor (RF) and antinuclear antibodies (ANA), acute viral infections, non-specific binding in laboratory conditions, also known as the prozone phenomenon, different sensitivity of diagnostic kits, and severe hemolytic and lipemic samples. Therefore, these reasons can lead to misinterpretation, inappropriate use of medication, and sometimes worry about the decision to have an abortion [1, 3, 7].

A positive result for IgM antibodies suggests the likelihood of an acute infection. Scientific studies consistently show that when IgG avidity measurements are combined with sensitive tests for Toxoplasma-specific IgM antibodies, it leads to the most precise diagnoses of acute toxoplasmosis [94]. Measuring IgG avidity is because the affinity of IgG antibodies to their target antigens increases over time after infonecit [95]. The strength of antibody binding can be measured using ELISA with a washing step and neutralizing buffer (such as urea) to remove low-affinity antibodies. The benefits of using this method in pregnant women include reduced need for frequent follow-ups, eliminating the need for PCR testing of amniotic fluid, avoiding unnecessary treatment with spiramycin or other drugs, and lowering costs [96, 97]. Numerous studies have demonstrated that IgG avidity is a valuable tool for distinguishing between acute and chronic toxoplasmosis with high sensitivity and specificity.

One limitation of this method is its ability to accurately diagnose active toxoplasmosis in individuals with compromised immune systems [1, 16]. Also, in some individuals, low or intermediate IgG avidity may remain for months to more than a year due to differences in the maturation of immune system responses [60, 98]. Therefore, the IgG avidity test lonely should not be decisive in the decision for recent infection. Because it may confuse the diagnosis of the stage (acute or chronic) of the disease [95]. To confirm the recent infection, a test panel is essential to make the necessary decisions and management about the conditions of pregnant women. Performing low avidity tests and reports in the early months of pregnancy should be more accurate and sensitive. Recently, numerous researches have been conducted on the design of IgG avidity diagnostic kits using recombinant and chimeric antigens. However, the antigen combination that is a definitive marker for differentiating between acute and chronic toxoplasmosis has not yet been discovered. Nevertheless, studies have emphasized the use of recombinant and chimeric proteins for maximum detection efficiency. To increase the specificity of the avidity test and eliminate the mentioned disadvantages, it is possible to achieve higher confidence by making changes in the protocols of the test, such as changing different dilution, which affects the results of the avidity test [14, 19, 99].

The analysis of the results of this systematic review showed that the amount of IgA in pregnant women suspected to acute toxoplasmosis (IgM positive) is 43%. The kinetics of IgA production is similar to IgM and after that, it reaches its peak and remains positive for longer time (usually 6–7 months) [100].

The simultaneous presence of anti-Toxoplasma IgA with IgM probably indicates an acute infection, because the production of this antibodies during acquired immunity is not common, furthermore, it is rarely seen in chronic toxoplasmosis infection.

Our study shows that the presence of IgA antibodies in pregnant women, in the context of a serological panel, can significantly help in distinguishing between acute and chronic infection compared to patients without these antibodies. Similar to the results reported in this systematic review, several researchers have found that the Toxoplasma IgA assay is useful for differentiating the stages of infection during pregnancy [8, 11]. However, in some other studies, they have found that due to insensitivity and long reaction time, IgA assay is not a reliable indicator for detecting the stages of infection [7, 101]. However, the use of Toxoplasma IgA in the diagnosing of recent infection is controversial.

A study by Olariu et al. (2019) discovered that women who were positive for both anti-Toxoplasma IgA and IgM antibodies were four times more likely to have recently contracted the infection compared to those who were only positive for IgM antibodies [102]. According to these findings, including the Toxoplasma IgA antibodies test as part of the standard serological panel used to diagnose toxoplasmosis increases the accuracy of detecting recent infections.

Conclusions

In summary, the findings from this review emphasize the significance of addressing hurdles related to consistent screening practices and accurate differentiation between recent and past Toxoplasma infections during pregnancy. By combining IgG avidity assessments with sensitive IgM testing and IgA, we have the potential to precisely identify acute infection stages. Furthermore, ongoing advancements in diagnostic methodologies, especially with molecular technologies and comprehensive antibodies analyses, hold promise for enhancing clinical approaches in managing the complex challenges posed by toxoplasmosis in pregnant women.

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

CT:

Chronic toxoplasmosis

AT:

Acute toxoplasmosis

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Acknowledgements

We extend our sincere appreciation to our colleagues in the Department of Medical Parasitology and Mazandaran University of Medical Sciences, Sari, Iran, for their contributions to this research. We are also grateful for the support provided by the Deputy of Research and Technology of Mazandaran University of Medical Sciences, Sari, Iran and The Higher Education and Science Committee of RA (Research project No. 23RL-1F014). Their support enabled us to conduct this study and we are thankful for their commitment to advancing medical research.

Funding

This research received no specific grant from any funding agency, commercial or not-for-profit sectors.

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Authors and Affiliations

  1. Toxoplasmosis Research Center, Communicable Diseases Institute, Department of Parasitology, Mazandaran University of Medical Sciences, Sari, Iran

    Mostafa Tork, Mitra Sadeghi, Bahareh Basirpour, Somayeh Ahmadi, Shahabeddin Sarvi, Shirzad Gholami, Seyed Abdollah Hosseini & Ahmad Daryani

  2. Student Research Committee, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran

    Mostafa Tork, Bahareh Basirpour & Somayeh Ahmadi

  3. Department of Immunology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran

    Hossein Asgarian-Omran

  4. Gastrointestinal Cancer Research Center, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran

    Hossein Asgarian-Omran

  5. Department of Obstetrics and Gynaecology, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran

    Fatemeh Ghasemzadeh

  6. Department of Parasitology and Mycology, faculty of Medicine, Mazandaran University of Medical Science, Sari, Iran

    Shahabeddin Sarvi, Shirzad Gholami & Seyed Abdollah Hosseini

  7. Laboratory of Molecular Parasitology, Scientific Center of Zoology and Hydroecology, NASRA, 7P. Sevak st, Yerevan, 0014, Armenia

    Ahmad Daryani & Sargis A. Aghayan

  8. Laboratory of Zoology, Research Institute of Biology, Yerevan State University, Yerevan, Republic of Armenia

    Sargis A. Aghayan

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  1. Mostafa Tork
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  2. Mitra Sadeghi
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  3. Hossein Asgarian-Omran
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  4. Bahareh Basirpour
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  6. Fatemeh Ghasemzadeh
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  8. Shirzad Gholami
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  9. Seyed Abdollah Hosseini
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  10. Ahmad Daryani
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  11. Sargis A. Aghayan
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Contributions

Study concept design, A. D., H.A. O., and S.A.H.; Conduct experiments and acquire data, M. T., B.B., and S.A.; Analysis and interpretation of data, S. A. H.; drafting of the manuscript, A. D., M. S., and M. T.; critical revision of the manuscript for important intellectual content, Sh. Gh., Sh. S., and S. A. A.; statistical analysis, S. A. H.; Study supervision, A. D and S. A. H. All authors participated in reading and endorsing the final version of the manuscript.

Corresponding authors

Correspondence to Seyed Abdollah Hosseini or Ahmad Daryani.

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Tork, M., Sadeghi, M., Asgarian-Omran, H. et al. Assessment of simultaneous IgM, IgG avidity, and IgA testing in diagnosis of acute toxoplasmosis in pregnant women: a systematic review and meta-analysis study. BMC Pregnancy Childbirth 25, 537 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12884-025-07580-6

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12884-025-07580-6

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BMC Pregnancy and Childbirth

ISSN: 1471-2393

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