Distribution of Toxoplasma gondii IgM and IgG antibody seropositivity among age groups and gestational periods in pregnant women

Introduction

Toxoplasmosis is a widely distributed zoonotic illness caused by Toxoplasma gondii, an obligate intracellular parasite^1,2. Globally, the distribution of this disease is extremely variable even inside the countries^3,4. In all host species, including humans, Toxoplasmosis is generally acquired either vertically from mother to fetus (congenital infection), or through ingestion of oocysts in contaminated food or water⁵. Rarely, T. gondii can transmit through organ transplantation and the transfusion of infected blood^6,7. Following ingestion, the intestinal epithelium is the primary portal of entrance for T. gondii; next, it spreads to other tissues, where it can cause more severe pathogenesis^8,9. If toxoplasmosis is acquired during pregnancy, severe infection may develop, especially in immunocompromised individuals, such as those with defects in T-cell-mediated immunity¹⁰. In patients with AIDS, toxoplasmosis may leads to severe, life-threatening disease¹¹. For example, cerebral focal lesions are caused by cerebral toxoplasmosis (CT) in HIV-infected patients¹².

The signs and symptoms of this illness are markedly divergent and range from asymptomatic to serious infection¹³. This variation depends on several factors includes inoculums size, virulence of the strain of toxoplasma, the individual’s genetic background and the status of the immune system of the infected individual¹⁴. In addition, since the organism has an affinity for muscular and neural tissues as well as the other visceral organs, many hosts harboring latent tissue cysts following toxoplasmosis¹⁵.

Fetuses may acquire toxopasmosis during delivery or through the placenta during pregnancy¹⁶. Early infection of the fetus may cause severe damage, or either pre- or post-natal death¹⁷. The clinical manifestation of congenital toxoplasmosis generally depends on the gestational stage, and can includes seizures, mental retardation, severe neurological defects, chorioretinitis, epilepsy and blindness^10,16,18.

Approximately 90% of pregnant women infected with T. gondii are asymptomatic, and recover spontaneously^19,20. Only a small percentage of pregnant women show the clinical symptoms of disease^19,21. In pregnant women, the clinical signs are no more severe than in non-pregnant women, and typically an influenza-like illness is seen after an incubation period of 5 to 18 days^19,22,23. Early diagnosis and treatment of mothers during pregnancy prevents fetal infection and minimizes the probability of complications^24,25.

Laboratory diagnosis of toxoplasmosis is usually performed by serological detection of T. gondii-specific IgG and IgM antibodies²⁶. Worldwide, the screening of T. gondii infection in pregnant women is preferably performed during the first trimester and subsequently every month or trimester in seronegative women, as applied in many countries²⁷.

Our study was undertaken to determine the prevalence and geographic distribution of toxoplasmosis. In addition, it sought to evaluate the role of animal contact in disease development among pregnant women through the serological detection of toxoplasma IgM and IgG antibodies, as well as to estimate the seropositivity of these antibodies among different age groups. It also attempted to identify the percentage of toxoplasma IgM seropositivity (indicative of acute infection) among different pregnancy trimesters.

Methods

This was a descriptive cross-sectional hospital-based study carried out in the District Head quarter Hospital (Mansehra, Hazara, Pakistan) and Ayub Medical Complex Hospital (Abbottabad, Khyber Pakhtunkhwa, Pakistan) over a period of 4 months (April to July 2015).

Results

Seroprevalence of toxoplasmosis

Out of 500 women, using ELISA the overall seroprevalence of toxoplasmosis was 24.8% (124/500). Statistically significant differences were observed between the seroprevalence of disease in Abbottabad and Mansehra district (Figure 1). In addition, the prevalence of toxoplasma antibodies among pregnant women revealed out of the total of 500 participants, only 8% had a serological marker of acute toxoplasmosis (Figure 2).

Figure 1. Seroprevalence of toxoplasmosis in different districts.

Out of the total of participants in every district, 38.7% (79/204) had the serologic marker of toxoplasmosis in Abbottabad district and 15% (45/296) in Mansehra. ***P = 0.0002.

Figure 2. The overall prevalence of Toxoplasma IgM (acute infection) and IgG (chronic infection).

Out of 500 pregnant women, 8% (40/500) were positive to IgM, 10.8% (54/500) to IgG, and 6% (30/500) to both antibodies. P = 0.567.

Toxoplasma antibodies seropositivity among age group and gestational periods of positive cases

Among the positive cases (n=124), the seropositivity of toxoplasma antibodies was shown to be statistically significant different among different age groups (Table 1). There was also a statistically significant difference in the seropositivity of toxoplasma IgM (indicating acute infection) between different gestational trimesters, the highest level of IgM seropositivity was observed in first trimester (54.34%) (Figure 3).

Table 1. Percentage of Toxoplasma gondii antibodies seropositivity among the total of positive cases in each age group.

Age, years	Positive cases	IgG	IgM	IgG and IgM
17–24	46	43.5% (20/46)	32.6% (15/46)	23.9% (11/46)
25–32	54	40.7% (22/54)	35.2% (19/54)	24.1% (13/54)
33–40	24	50% (12/24)	25% (6/24)	25% (6/24)
P value		0.003

Figure 3. Percentage of IgM seropositivity among the total of positive cases in each pregnancy trimesters.

Among the total of positive cases in every trimester, the seropositivity of IgM revealed statistically significant difference. Out of 46, 51, and 27 toxoplamosis infected cases in first, second and third trimesters, respectively, 54.34% (25/46) were seropositive to IgM (acute infection) in first trimester, 21.56% (11/51) seropositive to IgM in second trimester, and 14.81% (4/27) seropositive to IgM in third trimester. ****P = 0.0001.

Discussion

Toxoplasmosis in pregnancy can predispose the fetus to serious complications²⁸. The fetus can be severely damaged when the infection is acquired during pregnancy²⁹. Therefore, testing the serum of pregnant women for toxoplasma IgG and IgM is important to avoid intrauterine infection and complications. The current study was conducted on 500 blood samples collected from pregnant women in Mansehra and Abbottabad district of Pakistan, and examined for T. gondii IgM (acute infection) and IgG (chronic infection) antibodies. Out of the total of 500 pregnant women, 24.8% (124 women) had serologic marker of toxoplasmosis. Among the 124 positive cases, 54 were seropositive for toxoplasma IgG antibody, 40 cases for Toxo-IgM and 30 cases for both IgM and IgG antibody. In addition, out of 500 participants, 8% had a serologic marker of acute toxoplasmosis. In 2007, Obeed reported the prevalence of IgG (chronic infection) and IgM (acute infection) antibodies were 36% and 26.6%, respectively, which are greater than those seen in our study results³⁰. In addition, the seroprevalence of toxoplasmosis in Saudi Arabia was reported as 21.8%³¹. In pregnant women from South Korea, a low prevalence rate was observed (0.79%)³², with rates of 20% reported in Finland³³ and 24% in Prague³⁴. These findings indicate the prevalence of toxoplasmosis is markedly difference in different countries.

Moreover, our study revealed that the geographic distribution of toxoplasmosis is significantly different among the study areas. Out of the 296 participants analyzed from Mansehra and 204 from Abbottabad, the overall prevalence of toxoplasmosis was 15% and 38.7%, respectively. The higher prevalence in Abbottabad when compared with Mansehra may because Abbottabad is an area where agricultural practices are common, and domestic animals like cats and goats were generally kept in or near the homes. Thus, contact with these animals may be the main risk factor of the disease. In addition, low educational and socioeconomic level may have contributed.

In our study, a high percentage of IgM seropositivity was reported in the 1st trimester, which indicated a high prevalence of acute toxoplasmosis or recent infection in this trimester compared with the others. Furthermore, as reported in this study, there is a mild difference in the seropositivity of toxoplasma antibodies among age groups, which requires further study to assess whether, is there any significant association exists between toxoplasmosis and age.

Usually T. gondii does not cause clinical illness in the majority of animal species³⁵. Human often acquire this infection from animals by ingestion of improperly cooked or raw animal meat, or via consumption of contaminated food and water with animals waste³⁶. However, there is a need for detailed knowledge about the risk factors of toxoplasmosis. Previously, it was reported that there are some of risk factors are associated with toxoplasmosis, such as owning cats³⁷. Our study found that a considerable percentage of acute toxoplasmosis-infected women had a previous history of close contact with animals; for example, 15% had the history of contact with cats, 16.66% with dogs, 35% with goats and 40% with cows/buffalos. These results indicate that contact with domestic animals carry a risk for this disease. Similar results are also reported by many studies^38,39.

In this study, a high prevalence of toxoplasmosis was revealed. Lack of awareness together with contact with domestic animals are potential risk factors in Mansehra and Abbottabad district of Pakistan. Moreover, in the first and second trimester of pregnancy, the prevalence of acute toxoplasmosis seems to be higher compare with third. Thus it is necessary to test every pregnant women for toxoplasmosis and distinguish the type of infection. In addition, urgent treatment and medicine is essential to decrease the risk of intra-uterine infection and congenital toxoplasmosis. Additionally, there is a need to conduct public health education to create greater awareness about the disease, its transmission, symptoms, and prevention. In addition, screening of T. gondii infection and maternal care should be considered as the main stratagem to reduce the risks of congenital toxoplasmosis.

Data availability

Dataset 1. Raw data associated with this study. The results of immunochromatographic and ELISA screening, and history of animal contact are included. DOI: https://doi.org/10.5256/f1000research.15344.d224335⁴⁰.