Seroprevalence of Toxoplasma gondii immunoglobulins and its association with systemic lupus erythematosus: A systematic review and meta-analysis

Abstract

Background

The exact cause of systemic lupus erythematosus (SLE) is still unknown. However, hormonal, genetic, and environmental factors may play significant roles in its development. Infection has been recognized as a crucial trigger for SLE development. Several studies have reported a higher prevalence of Toxoplasma gondii infections in patients with SLE than in healthy individuals. However, these results were inconsistent. Therefore, this study aimed to conduct a systematic review and meta-analysis of published studies to provide a definitive conclusion regarding the relationship between T. gondii infection and SLE.

Materials and methods

We conducted a comprehensive search across diverse databases using an array of search tools to uncover pertinent literature. Following the stringent application of the inclusion and exclusion criteria, we carefully selected the appropriate reports for our meta-analysis. Using Comprehensive Meta-Analysis software v4, we analyzed the data and determined the prevalence of antibodies against T. gondii in patients affected with SLE. To investigate the correlation between T. gondii seropositivity and SLE, we computed the risk ratios (RRs) and 95% confidence intervals (CI).

Results

Eleven studies were considered eligible for inclusion in the present study. The prevalence of anti-IgG and IgM antibodies against T. gondii was 33.9% and 7.7%, respectively. A significant association between T. gondii IgG seropositivity and SLE was observed when compared to the controls (risk ratio = 2.14, 95% CI = 1.42 to 3.22, p = .000). However, IgM seropositivity against T. gondii was comparable between patients with SLE and healthy controls.

Conclusions

In summary, this study suggests that T. gondii IgG is more prevalent in patients with SLE than in healthy individuals in areas where T. gondii infections are more frequent. However, an exact cause-and-effect relationship still needs to be established. Therefore, additional research is necessary to validate these findings and to investigate the underlying mechanisms.

Keywords

systemic lupus erythematosus meta-analysis immunoglobulin G immunoglobulin M

Introduction

Autoimmune diseases are characterized by a breakdown in immune tolerance, where the body’s defense mechanisms erroneously target its own tissues.^1,2 Systemic lupus erythematosus (SLE) stands as a notable autoimmune inflammatory condition characterized by a spectrum of clinical manifestations, including constitutional, musculoskeletal, dermatological, renal, neuropsychiatric, pulmonary, gastrointestinal, cardiac, vascular, ocular, obstetric, endocrine and haematological.^3,4 Despite extensive research, the etiology of SLE remains elusive and environmental factors such as various infections, have been one of the important aspects of SLE development.^5,6 Infections pose significant risks for SLE individuals, contributing substantially to mortality, morbidity, and hospitalization rates in this population.⁷ Various pathogens, including bacteria, viruses, fungi, and protozoa infections have been linked with the development of SLE and clinical manifestations.^8–10

Out of the various infections, Toxoplasmosis, caused by the obligate apicomplexan protozoan parasite Toxoplasma gondii has been linked with SLE in different populations.^10–12 A recent meta-analysis¹³ revealed the seroprevalence rate of T. gondii to be 10%-90% worldwide with significant deviations among populations: with a higher frequency reported from Africa, Southeast Asia, Middle East, Central/Eastern Europe, and Latin America. Despite host immune responses, T. gondii can persist indefinitely within the host, forming metabolically active cysts in muscle and brain tissues.¹⁴ Infection with T. gondii poses severe risks for pregnant women and immunocompromised individuals, potentially resulting in miscarriage, stillbirth, or severe systemic infection.¹⁵ Conversely, in immunocompetent individuals, initial infection may manifest as asymptomatic or present with mild symptoms such as lymphadenopathy.¹⁶ However, accumulating evidence suggests potential associations between T. gondii infection and behavioural,¹⁷ cognitive,¹⁸ and psychiatric alterations,¹⁹ as well as autoimmune diseases including SLE²⁰ and rheumatoid arthritis.²¹ Interestingly, some studies suggested a potential protective effect of T. gondii against multiple sclerosis.²²

Several investigations have been conducted in a wide range of populations^{10–12,20,23–26} to explore the role of T. gondii infections in the pathogenesis of SLE; however, the results have remained contradictory. Furthermore, the prevalence of immunoglobulin G and M against T. gondii in SLE patients varied from population to population (Abbas et al., 2019; Aboukamar et al., 2023; Berkun et al., 2009; Hamza et al., 2015; Li et al., 2024; Ping-Ping et al., 2021; Shapira et al., 2012; Wilcox et al., 1990). The present study aimed to find out the overall prevalence of IgG and IgM against T. gondii and elucidate the potential role of T. gondii infection as a risk factor for SLE development.

Materials and methods

Literature search

This study was conducted in compliance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2020 guidelines.^27,28 We searched various databases, including PubMed (Medline), PubMed Central, Science Direct, and Scopus, to identify eligible published reports. The last database search was performed on February 3, 2024. To explore the databases, we used the following keywords: “systemic lupus erythematosus”, “SLE”, “T. gondii”, and “toxoplasmosis”. Figure 1 shows the details of this search strategy.

Inclusion and exclusion criteria

To ensure a thorough and reliable meta-analysis, we established specific criteria for inclusion and exclusion before conducting a literature survey across various databases. Our study only considered studies that met the following eligibility requirements: a) they reported on the seroprevalence of IgG and/or IgM in SLE patients, b) they presented IgG or IgM prevalence data for both SLE patients and controls for comparison, and c) they were either case-control or cross-sectional studies conducted on SLE patients. Reports that fell under the following categories were excluded from our investigation: a) review studies, b) case reports, and c) animal or cell line studies.

Data extraction and quality assessment

Two independent authors conducted a thorough search and extracted the data. The information collected from each relevant article included the author’s name, publication year, study location, number of cases of SLE, control groups, number of cases positive for T. gondii antibodies, and the type of diagnostic assay used to determine T. gondii seropositivity. In the case of any discrepancies in the collected data, the authors discussed the issues thoroughly until a consensus was reached.

Statistical analysis

The meta-analysis was performed using the Comprehensive Meta-analysis (CMA) version 4 software. To assess the potential for publication bias, a funnel plot was visually inspected and Egger’s regression analysis was conducted. Heterogeneity among the included reports was also evaluated using the Cochrane Q test and the I square test. Based on the outcome of the heterogeneity test, a fixed (homogenous) or random effects model (heterogeneous) was selected for the meta-analysis. The prevalence of IgG and IgM antibodies against T. gondii in patients with SLE was calculated by determining the combined event rate. The relationship between IgG and IgM seroprevalence and SLE was examined by calculating pooled odds ratios (ORs), 95% confidence intervals (CIs) and probability values. Sensitivity analyses were conducted to determine the robustness of the meta-analysis by excluding one study at a time and comparing the results with the original meta-analysis.

Results

Literature search and eligible reports

Based on the materials and methods outlined in the manuscript, a thorough search of several databases yielded a total of 2165 articles. These databases included Science Direct (959 articles), Scopus (27 articles), PubMed Medline (26 articles), and PubMed Central (1153 articles). After meticulous consideration of our inclusion and exclusion criteria, we were able to find 11 articles that were appropriate for our investigation.^{10–12,20,23–26,29–31} Of the 11 articles, nine were case-control studies with 1518 cases and 1895 controls.^{10–12,20,24–26} Further, one study²⁰ had data from two distinct populations (European and Latin American). A study conducted by Wilcox et al²⁶ investigated the presence of T. gondii antibodies in a set of samples using both the latex and dye test methods. As indicated earlier, the dye test was more reliable than the latex test,³² for the present study, we have included data from the dye test. In addition, three cross-sectional studies were further included for the seroprevalence analysis.^29–31 A study by Cao et al. 2020³³ was not included in the current analysis as its publication language is Chinese, making it impossible to access and extract relevant data from the full paper. Figure 1 shows the details of the inclusion and exclusion of reports depicted as a PRISMA 2020 flow chart. The baseline characteristics of the included reports are documented in Table 1.

Table 1.

Baseline characteristics of included studies to explore the prevalence and association of antibodies (IgG & IgM) against Toxoplasma gondii in SLE groups and healthy control.

First author & year	Country	Study design	Diagnostic method for T. gondii seroprevalence	Control group		SLE group
First author & year	Country	Study design	Diagnostic method for T. gondii seroprevalence	Total (n)	Antibody positivity (n)	Total (n)	Antibody positivity (n)
IgG
Li et al., 2024	China	Case-control	Serological	908	53	863	144
Aboukamar et al., 2023	Egypt	Case-control	Serological	61	24	23	18
Ping-Ping et al., 2021	China	Case-control	Serological	237	10	79	25
Abbas et al., 2019	Iraq	Case-control	Serological	32	0	64	0
Hamza et al., 2015	Egypt	Case-control	Serological	30	9	30	16
Shapira et al., 2012	Europe	Case-control	Serological	297	77	169	54
Shapira et al., 2012	Latin America	Case-control	Serological	140	50	120	42
Berkun et al., 2009	Israel	Case-control	Serological	140	5	120	13
Wilcox et al., 1990	England	Case-control	Dye test	50	10	50	25
Gonzalez Vatteone et al., 2022	Paraguay	Cross-sectional	Serological	--	--	106	77
Hezarjaribi et al., 2021	Iran	Cross-sectional	Serological	--	--	33	11
Kalaby et al., 2016	Iraq	Cross-sectional	Serological	--	--	8	0
IgM
Aboukamar et al., 2023	Egypt	Case-control	Serological	61	3	23	6
Abbas et al., 2019	Iraq	Case-control	Serological	32	0	64	0
Hamza et al., 2015	Egypt	Case-control	Serological	30	9	30	4
Berkun et al., 2009	Israel	Case-control	Serological	140	4	120	4

Publication bias

The current meta-analysis examined publication bias in relation to T. gondii IgG and IgM prevalence and association studies in SLE patients and controls. Egger’s regression analysis and funnel plots were employed for this purpose. As shown in Table 2, no publication bias was identified when comparing the prevalence and association of T. gondii IgG and IgM in SLE patients. Additionally, the funnel plots for both the prevalence of antibodies against T. gondii and association studies showed no evidence of publication bias (supplemental Figure 1).

Table 2.

Publication bias and heterogeneity investigations in the meta-analysis.

Description	Intercept	95% confidence interval	p Value	Q value	P Heterogeneity	I² value	Model used
Prevalence of T. gondii IgG in SLE patients	2.52	−2.27 to 7.31	0.26	199.78	0.000	94.49	Random
Prevalence of T. gondii IgM in SLE patients	−3.33	−18.84 to 12.16	0.45	15.08	0.002	80.11	Random
Association of T. gondii IgG with SLE	1.77	−3.08 to 6.64	0.40	40.00	0.000	82.50	Random
Association of T. gondii IgM with SLE	11.02	−120.61 to 142.67	0.48	8.37	0.01	76.10	Random

Heterogeneity analysis

The heterogeneity of the studies included in the analysis was assessed using the Cochrane Q, and I square tests for prevalence and association of T. gondii IgG and IgM in SLE patients. Table 2 documents the results of the heterogeneity tests. The heterogeneity for the prevalence of T. gondii IgG and IgM in SLE patients was significant (IgG: Q = 199.78, I² = 94.49; IgM: Q = 15.08, I² = 80.11). Additionally, the heterogeneity for the association of T. gondii IgG and IgM in SLE patients was also significantly higher (IgG: Q = 40, I² = 82.50; IgM: Q = 8.37, I² = 76.10). Based on the results of the heterogeneity test, a random effect model (heterogenous) was used for the meta-analysis.

Prevalence of T. gondii IgG and IgM antibodies in SLE

To investigate the prevalence of T. gondii IgG and IgM, we analysed data from 12 to 4 populations, consisting of 1665 and 237 SLE patients, respectively, using CMA v4 software. The seroprevalence of T. gondii IgG antibody in SLE patients was found to be 33.9% (95% CI, 21.8 to 48.5%) as shown in Figure 2(a). On the other hand, the prevalence of T. gondii IgM antibody in the SLE patients was found to be 7.7% (95% CI: 2.1 to 24.7%) as shown in Figure 2(b).

Association of T. gondii with susceptibility to the development of SLE

In the study, eight data sets were analyzed to compare the presence of T. gondii IgG in patients and controls. The results showed that T. gondii IgG is a risk factor for the development of SLE, with a risk ratio of 2.14, 95% CI of 1.42 to 3.22, and a p-value of 0.000 (Figure 3(a)). However, there was no significant association between the prevalence of T. gondii IgM and the development of SLE in patients, with a risk ratio of 1.35, 95% CI of 0.31 to 5.85, and a p-value of 0.68 (Figure 3(B)). This suggests that T. gondii IgM does not play a role in the development of SLE.

Sensitivity analysis

A sensitivity analysis was carried out to evaluate the reliability of a meta-analysis. This involved excluding data from one study at a time and comparing the results with the original meta-analysis. Any significant difference between the two sets of results was considered weak and had to be interpreted with caution. The sensitivity analysis showed that the prevalence and association of T. gondii IgG in SLE patients was robust, as there was very little deviation from the original analysis when each study was excluded. However, the prevalence and association of T. gondii IgM in SLE patients was not robust, as there was substantial variation observed in the sensitivity analysis (as shown in Supplemental Figure 2).

Discussion

The present meta-analysis deciphered the prevalence of IgG and IgM against T. gondii in the SLE patients as 33.9 and 7.7%, respectively. In addition, the distribution of T. gondii antibodies revealed a significant association with susceptibility to SLE development only for immunoglobulin G type, suggesting a potential association between T. gondii IgG seropositivity and SLE. Considering T. gondii’s status as a cosmopolitan pathogen with heightened virulence in immunocompromised individuals, understanding host-pathogen interactions is crucial.^34–36 Therefore, in genetically predisposed individuals, SLE may manifest as a plausible response to T. gondii infection.³⁷ Supporting this notion, SLE patients often undergo immunosuppressive therapies, such as corticosteroids, which elevate susceptibility to opportunistic infections like T. gondii.^38–41 T. gondii could exacerbate cellular immune responses and immune cell infiltration, potentially worsening tissue damage.⁴² Therefore, further investigation into concurrent T. gondii infection in SLE is warranted, considering the burden, localization, and strain diversity of the parasite in influencing the immune response to SLE.

An earlier meta-analysis by Bassett et al. demonstrated higher seroprevalence of T. gondii in SLE patients compared to healthy controls⁴³ similar to the observation of the present study. The present report has several advantages over the earlier study.⁴³ First the number of reports including data of patients and controls considered for the present investigation was higher (Present study: number of datasheets = 9, SLE patients = 1518, healthy controls = 1895; Bassett et al: number of datasheets = 6, SLE patients = 568, healthy controls = 894). The consideration of more reports increases the strength of the conclusion derived from the study. Second, Bassett et al. included data of the latex agglutination test of the Wilcox et al. study.²⁶ However, among the latex and Dye tests, the dye test has been documented to be better compared to the agglutination test.³² In the present study, we included data from the dye test. Third, the present study investigated the overall prevalence of IgG and IgM against T. gondii and also explored the possible role of IgM in the susceptibility to SLE.

T. gondii infection may be an important environmental factor that could play a role in initiating or exacerbating the disease process, potentially interacting with other environmental, immunological, and genetic factors. However, the studies are limited to the role of T. gondii infection in the clinical severity and pathogenesis of SLE. An independent study in the Chinese population²⁵ showed a higher rate of moderate and severe clinical symptoms in SLE patients with anti-IgG against T. gondii. However, the other two reports from Egyptian²⁴ and South American²⁹ populations failed to demonstrate such association. Interestingly, SLE patients positive for the T. gondii anti-IgG had a higher prevalence of discoid rash, oral ulcer, myalgia and alopecia and were linked with autoantibodies like anti ribosomal RNA protein, anti dsDNA, Scl 70, anti-cardiolipin and rheumatoid factors.²⁵ Furthermore, it’s not clear whether the T. gondii infections predispose genetically susceptible subjects to the development of SLE or as the patients are treated with immunosuppressants, they are prone to T. gondii infections. Therefore, further experimental studies using animal models and longitudinal cohort studies in humans are recommended to provide additional evidence for the association between T. gondii infection and SLE and to ascertain whether T. gondii infection acts as an inducer in SLE development.

In the present meta-analysis, we observed that IgG antibodies were associated with SLE, while IgM antibodies were not linked to SLE. These observations may be attributed to the chronic nature of the infection and its effects on the immune system. Elevated levels of T. gondii IgG antibodies indicate past or long-term exposure, which can modulate immune responses and create a persistent inflammatory environment, potentially triggering or exacerbating autoimmune conditions like SLE. On the other hand, IgM antibodies signify recent infections and are not linked to SLE, suggesting that chronic immune system modulation is more significant in this context. Moreover, the present meta-analysis contained a smaller number of reports for IgM compared to the number of reports examined for IgG.

Our study presents a thorough systematic review and meta-analysis of case-control and cross-sectional studies focusing on the connection between human T. gondii infection/exposure and SLE risk. However, it is crucial to acknowledge certain limitations. First, the number of studies and participants included in our analysis is limited, primarily from a few countries, which restricts the generalizability of our findings. Second, our search was conducted across four different databases, which may have excluded articles from other databases. Third, data unavailability in the included reports prevented us from adjusting for factors such as age, gender, and animal exposure in the human case and control groups, as well as conducting systematic evaluations of potential risk factors. Therefore, it is essential to exercise caution when interpreting our results, and further research is necessary to address these limitations.

Conclusion

In conclusion, the present study has shown that in areas where infection with T. gondii is prevalent, T. gondii IgG is more common than IgM. Additionally, patients with SLE have a higher prevalence of T. gondii IgG compared to healthy individuals, suggesting that T. gondii infection may be a significant factor in the development of SLE. However, more in-depth research is needed to fully understand the relationship between T. gondii infection and SLE.

Supplemental Material

Supplemental Material - Seroprevalence of Toxoplasma gondii immunoglobulins and its association with systemic lupus erythematosus: A systematic review and meta-analysis

Supplemental Material for Seroprevalence of Toxoplasma gondii immunoglobulins and its association with systemic lupus erythematosus: A systematic review and meta-analysis by Shovit Ranjan and Aditya K Panda in Lupus

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Shovit Ranjan

Aditya K Panda

Supplemental Material

Supplemental material for this article is available online.

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