Anti-Toxoplasma gondii Antibodies: Prevalence and Risk Factors among Pregnant Women Accessing Antenatal Care in Some Primary Health Centers in Jos Metropolis, Nigeria

Introduction

Toxoplasma gondii, which occurs worldwide, is an obligate intracellular apicomplexan protozoan parasite that is responsible for toxoplasmosis in animals and humans¹,2. It is estimated that over one-third of the world human population is infected, with reported incidence rate of congenital toxoplasmosis ranging from 400 to 4000 cases per year^3,4. The parasite is implicated for 1.2 million disability-adjusted life years annually⁵.

The main transmission pathway of T. gondii includes vertical transmission (from pregnant mother to fetus), eating raw or undercooked meat, and consumption of vegetables, water, and foods contaminated with oocysts of the parasites⁶. Should primary infection occurs during pregnancy, the parasite could cross the placental barrier causing congenital toxoplasmosis, which may lead to myriad of health problems such as spontaneous miscarriage, stillbirth, or congenital abnormalities such as mental retardation, hydrocephalus, intracerebral calcifications, and chorioretinitis^7-11. Awoke et al.⁹ reported that antenatal screening of pregnant women for T. gondii infection is based on IgG and IgM antibodies detection and is the main means of monitoring the risk for congenital toxoplasmosis.

The danger of congenital toxoplasma infection and the seriousness of fetal harm are reliant on the gestational age when the maternal infection takes place¹². The general danger of congenital maternal infection from primary toxoplasmosis during pregnancy varies from 20% to 50% if left untreated¹³. Prevention of congenital toxoplasmosis can be achieved by identifying non-immunized women at the onset of pregnancy and enlighten them on how to prevent the infection, and by serological follow-up. Multiple testing for Toxoplasma-specific IgG and IgM helps to differentiate between acute and chronic infections¹².

Prevalence of congenital toxoplasmosis across the globe vary between 4.3 and 75.0% in Africa^14-17, 6.8–51.8% in Europe^18-20, 14.0–96.3% in Asia^21-23, 10.6–13.0% in North America,^24-26 and 26.3–80.0% in South America^27-29.

Despite the risk of vertical transmission of toxoplasmosis, serological tests for T. gondii infection are not routinely performed during pregnancy in Nigeria. Hence, prevalence and the burden of toxoplasmosis are poorly understood. The aim of this study, therefore, was to investigate the seroprevalence and risk factors of T. gondii infection by determining (1) the seroprevalence of IgG and IgM specific to T. gondii and (2) risk factors that are associated with toxoplasmosis.

Material and Methods

Results

Overall, 182 subjects were included in this study; 84 (46.2%) had anti-Toxoplasma IgG antibody, while 2 (1.1%) were positive for IgM antibody. Two study subjects that had IgM antibody were also seropositive for anti-Toxoplasma IgG antibody representing 2.4% (2/84) of the women who were seropositive for anti-Toxoplasma IgG. Ninety-eight (98 [53.4%]) of the subjects were seronegative for both anti-Toxoplasma IgG and IgM antibodies (Figure 1).

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Figure 1.

Relationship between Anti-Toxoplasma antibodies (IgG and IgM) status of the study subjects.

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Although the demographic parameters show no association (P > 0.05) with the prevalence of anti-Toxoplasma antibodies, the age group 11–20 years had the highest prevalence of IgG antibody, while women within the age group 41–50 years had 0.0% prevalence of IgG antibody to T. gondii. On the other hand, all the 2 subjects that tested positive to IgM antibody were in the age bracket of 31–40 years. With respect to educational status, the seroprevalence anti-Toxoplasma IgG antibody decreased from 100% in women without formal education to 40.0% in women with tertiary level of education. The two women who were seropositive for IgM antibody had secondary level of education (Table 1). In terms of occupation of the pregnant women, majority of the women were unemployed (53.8%), while 46.2% of them were employed. The highest prevalence (66.7%) of IgG antibody was detected among students, while the least (44.2%) was detected among housewives. In similar vein, the housewives 2.3% prevalence of IgM antibody (Figure 2).

There was statistically significant association (χ² = 14.324; P = 0.001) between trimester and prevalence of anti-Toxoplasma IgM antibody. None of all the other risk factors studied in the present research had association (P > 0.05) with anti-Toxoplasma antibodies (Table 2).

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Figure 2.

Prevalence of anti-Toxoplasma antibodies based on employment status (IgG: χ² = 1.137; P = 0.768 and IgM: χ² = 1.129; P = 0.770).

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Discussion

The present study is among the few works in Nigeria that explore the seroprevalence of T. gondii infection in pregnant women and to determine the risk factors associated with the infection in this cohort. Toxoplasmosis is a treatable though likely fatal disease. The problem with most communities with substantial prevalence of T. gondii infection is the long-term complications which follows congenital infections and the ability to cause opportunistic infections that are life-threatening in immunocompromised or immunosuppressed individuals^3,31.

Our findings showed that the seroprevalence of anti-T. gondii antibodies in women visiting antenatal clinic in PHC in Jos was 46.2% and 1.1% for IgG and IgM, respectively. This implies that 46.2% of the study subjects had been exposed and possibly recovered from the infection, while 1.1% of the women have ongoing or current Toxoplasma infection. Hence, the finding suggests that the parasitic infection is endemic in the study area. The anti-T. gondii IgG prevalence reported that in the current study was higher than previously reported ones for Sudan (41.7%), Somalia (29.6%), and Algeria (52.2%)³². When compared with findings from other parts of Nigeria, the seroprevalence was higher than the 32.6% and 40.6% reported by Deji-Agboola³³ and Akinbami et al.³⁴ in Lagos and 29.1% obtained among pregnant women in Zaria³⁵. These various findings lend credence to the fact that Toxoplasma infection varies significantly within and between countries^5,36-39. The difference in the seroprevalence of T. gondii infection could be attributed to the variation in geographic locations of the study areas as manifested in differences in humidity and temperature. Higher temperatures and/or humid environments favor sporulation of oocysts^40,41. Furthermore, the variation in prevalence of T. gondii infection could be partly due to the use of different analytic techniques such as the use of ELISA versus rapid diagnostic tool and/or polymerase chain reaction. This is because these analytic techniques have different rates of sensitivity and specificity⁴². In addition, difference in socioeconomic status of the women and variation in samples could have impacted on prevalence reported in the various findings, thus bringing about the discrepancies in the reported figures.

The correlation between sociodemographic characteristics of the pregnant women and prevalence of anti-T. gondii antibodies were assessed in the current study. In concordance with findings from other authors^43,44, there was no significant association between Toxoplasma seroprevalence and increasing maternal age, but younger women (21–30 years) were found to have a relatively higher seroprevalence rate compared to older women (>30 years). This might be explained by younger rather than older women’s preference for outings overeating at home. During those outings, the women are exposed to grilled meat which might be undercooked. Fruits and salads which may be contaminated with the parasite oocysts are also often eaten in such outings hence increasing the risk of infections^45-47. Prevalence of anti-T. gondii antibody (IgG) in this study decreased with increasing educational level. This finding was in accordance with the study done in Debre Tabor, Northwest Ethiopia, where pregnant women who could neither read nor write had the highest toxoplasmosis infection rate compared with those with primary, secondary, and tertiary levels of education^48,49. Illiterate women are more likely to engage in more risky unsanitary and unhygienic practices hence are more liable to be infected by T. gondii. Though significant association was not observed between prevalence of anti-Toxoplasma gondii antibodies and both occupation and educational level, the prevalence increases with decrease in educational level. This is in concordance with reported findings from Africa^50-52.

However, there was a significant relationship between trimester of pregnancy and prevalence of anti-T. gondii IgM antibody. Women in the first trimester of pregnancy had the highest prevalence of Toxoplasma infection. Although the gravidity of the women was not established in this study, Mandour et al.⁵³ reported an increased percentage of multigravid women, in whom complicated pregnancy outcomes have been reported compared with primigravid females. In view of that finding, it is likely that the majority of the women in the first trimester of their pregnancy were multigravid females.

Our findings showed no association between T. gondii infection and contact with cats. This suggests that contact with cats does not translate to zoonosis, but more pertinent in causing zoonosis is the improper handling of cats’ fecal matter⁵⁴. While this finding disagrees with the reports of Lim et al.⁵⁵ and Adeniyi et al.,⁵⁶ where they showed a significant association between contact with cats and seroprevalence of T. gondii infection, it is consistent with the findings of Doehring et al.⁵⁷, Nijem and Al-Amleh,⁴⁰ and Wang et al.⁵⁸. It was also found that though immune-compromised individuals were reported to be more prone to toxoplasmosis⁵⁹, HIV-negative women had a higher prevalence of the infection in comparison with HIV-positive pregnant counterparts. It is likely that the use of antiretroviral therapy by HIV-positive women reduced the probability of opportunistic infections.

Two pregnant women with active/ongoing toxoplasmosis were detected. This implies that their fetuses were at risk of congenital T. gondii infection with attendant adverse and sometime fatal consequences. The presence of active cases of toxoplasmosis in this study, therefore, underscores the need and importance of screening of pregnant women to control congenital transmission of toxoplasmosis and its unfavorable birth outcomes such as miscarriages, hydrocephalus, cerebral calcification, poor cognitive development, and fetal death⁵⁹.

Conclusion and Recommendation

This study confirms prevalence of T. gondii infection among pregnant women accessing antenatal care in Jos metropolis, Plateau State, Nigeria. None of the risk factors studied with respect to IgG antibody was associated with toxoplasmosis. In spite of the absence of a significant association between possible risk factors and the infection, there is a need for the enlightenment of women, particularly pregnant women, on the risk factors and how to prevent the contraction of toxoplasmosis.

Authors’ Contributions

OJO: Conceptualization, investigation, methodology, validation, writing original draft manuscript/review and editing. IAO: Data curation, formal analysis, review and editing of final manuscript. EEE: Supervision, validation, review and editing of final manuscript. BSA: Data curation, investigation, methodology, validation. MBA: Formal analysis, investigation, methodology, writing of original draft manuscript/review, and editing. NAA: Data curation, investigation, methodology. IAY: Data curation, investigation, methodology, validation. AOO: Data curation, methodology, resources. MAA: Data curation, investigation, review and editing of final manuscript. JAA: Formal analysis, investigation, methodology, writing of original draft manuscript/review and editing. All the authors approved the final manuscript before submission.