Journal of Womens Health, Issues and Care ISSN: 2325-9795

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Research Article, J Womens Health Issues Care Vol: 5 Issue: 6

Prevalence and Factors Associated with Toxoplasma Gondii Immunization among Pregnant Women in Douala – Cameroon

Charlotte Tchente Nguefack1*, Isabelle Kenmegne Meumeu2, Guy Pascal Ngaba3, Eugene Kongnyuy4, Théophile Nana Njamen5, Halle Ekane Gregory5 and Emile Mboudou6
1Obstetrician and Gynecologist; Douala General Hospital, Faculty of Medicine and Pharmaceutical Sciences, University of Douala, Douala, Cameroon
2General Practitioner; Douala General Hospital, Douala, Cameroon
3Medical Biologist; Gynaecologic and Paediatric Hospital of Douala, Faculty of Medicine and Pharmaceutical Sciences, University of Douala, Cameroon
4Reproductive Health Solutions, Sycamore Drive, SP1 3GZ, Salisbury, United Kingdom
5Obstetrician and Gynecologist, Douala General Hospital, Faculty of Medicine, University of Buéa, Cameroon
6Obstetrician and Gynecologist; Gynaecologic and Paediatric Hospital of Douala, Faculty of Medicine and Biomedical Sciences, University of Yaoundé I, Cameroon
Corresponding author : Charlotte Tchente Nguefack
Obstetrician and Gynecologist, Douala General Hospital, PO BOX 4856, Douala, Cameroon
Tel:
(237) 675305341
Fax: (237) 233370146
E-mail: [email protected]
Received: July 13, 2016 Accepted: September 20, 2016 Published: September 25, 2016
Citation: Nguefack CT, Meumeu IK, Ngaba GP, Kongnyuy E, Njamen TN, et al. (2016) Prevalence and Factors Associated with Toxoplasma Gondii Immunization among Pregnant Women in Douala – Cameroon. J Womens Health, Issues Care 5:6. doi:10.4172/2325-9795.1000248

Abstract

Background: Toxoplasmosis, an infection by Toxoplasma (T.) gondii, often occurs without symptoms in immune competent adults, but can affect the fetus, causing miscarriage or severe complications if the infection takes place during pregnancy. Its prevalence varies widely and depends on dietary habits and hygiene levels within the population. The objective was to determine the seroprevalence and factors associated with T. gondii among pregnant women in three health care units in Douala, Cameroon.
Method: A cross-sectional, descriptive and analytic study was conducted from January 10 to April 30, 2015. Pregnant women were interviewed after informed consent during antenatal care. Data were obtained on socio-demographic characteristics, dietary and hygiene habits, and cohabitation with cats. Serological diagnosis of T. gondii was obtained through the ELISA technique (Enzyme- Linked Immuno-Sorbant Assay) to measure values of IgG and IgM. Data were analyzed using Epi Info 7, Excel 2007 and XLSTAT 7.5.2. Associations between variables of interest and T. gondii immunization were investigated using the Chi–Square analysis, with p values less than 0.05 considered statistically significant.
Results: The average age of the 327 pregnant women who took part in the study was 31 ± 5 years. The seroprevalence of T. gondii was 78.6%. There was no significant association between the seroprevalence and age, cohabitation with cats, eating uncooked food, and source of drinking water (p>0.05). The lower the educational level, the higher the prevalence of T. gondii antibodies (p=0.0003). The mean value of IgG was 183 ± 1126 IU/ml with a minimum of 0.0 IU/ml and maximum of 19714 IU/ml.
Conclusion: There is high seroprevalence of T. gondii among pregnant women in Douala. The educational level is the main associated factor. Health education and awareness of the disease and its transmission to pregnant women could be created during antenatal follow up to reduce the risk of first infection during pregnancy.

Keywords: Seroprevalence; Toxoplasma gondii; Associated factors; Pregnancy

Keywords

Seroprevalence; Toxoplasma gondii; Associated factors; Pregnancy

Abbreviations

T gondii: Toxoplasma gondii; IgG: Immunoglobulin G; IgM: Immunoglobulin M; CFA: Communauté Financière d'Afrique (African Financial Community); US Dollar: United States Dollar

Introduction and Brief Review of Relevant Literature

Toxoplasmosis is a parasitic zoonotic disease caused by Toxoplasma gondii [1]. The T gondii infection is generally mild in immune competent adults, but it can affect the fetus and cause miscarriage or severe complications if it takes place during pregnancy. Fetal complications include cerebral (intracranial calcification, hydrocephalus etc.), ocular (chorioretinitis, optic atrophy, etc.) and visceral complications (hepatosplenomegaly, jaundice etc.).
The prevalence of T. gondii varies widely and depends on dietary habits and hygiene levels within the population [2]. It then varies in different parts of the world. In Asia, the prevalence was 3.7%; 10.6%; 11.2 %; 17.2% and 28.3% respectively in Korea, China, Vietnam, Singapore and Thailand [3-7]. Studies conducted in these countries revealed that the prevalence was associated with age, drinking untreated water and cohabitation with cats. In the United States of America, the prevalence was 9.1% among women of childbearing age [8]. In Brazil, the prevalence is higher than it is in most countries (68.6%) [9]. In Canada, the national prevalence was estimated to be 20 to 40% [10]; however, in Nunavik, Quebec, the prevalence was 59.8% [11]. In the Quebec study, the prevalence was associated with maternal age, low educational level, and the use of contaminated water for drinking. In Europe, the prevalence of toxoplasmosis is decreasing. In France, for example, the prevalence of toxoplasmosis in pregnant women has declined steadily over the last fifty years. It varies by region and is related to geo-climatic factors and food habits. It was estimated at nearly 80% in 1960, 63.3% in the early 1980s, 54.3% in 1995, 43.8% in 2003 and 36.7% in 2010 [12]. In a French study, the prevalence was significantly higher among older women with lower level of education [12]. In Serbia, the seroprevalence of toxoplasmosis decreased from 86% in 1988 to 39% in 1997 [13].
Studies conducted in Africa (using the same methodology), showed wide variation in prevalence from one country to another and within the same country. In Northwest Ethiopia, Nigeria, Morocco, Gabon, Southwest Ethiopia and Ghana, the prevalence was 18.5%, 40.8%, 50.6%, 56%, 83.6% and 92.5% respectively [14- 19]. In Cameroon, where some consultants do routine screening for toxoplasmosis, a cross-sectional study was performed on 110 pregnant women in 2009 and revealed a prevalence of 70% for IgG and 2.73% for IgM [20]. Factors associated with the rise in seroprevalence included the consumption of untreated water and unclean vegetables.
Given that the seroprevalence of T gondii changes over time, and because the 2009 Cameroon study was conducted in one center with a small sample size, the current multicenter study was conducted to assess the present seroprevalence of T gondii among pregnant women as well as its associated factors in order to enhance the guidelines for control and monitoring of toxoplasmosis during pregnancy in Cameroon.

Methodology

The current study is a descriptive and analytical cross-sectional study conducted from January to April 2015. Participants were pregnant women attending antenatal care in three hospitals in Douala (Douala General Hospital, Rond-Point Maetur Polyclinic, and Daniel Muna Memorial Clinic). All pregnant women who attended antenatal consultations and gave their informed consent were eligible. They were recruited consecutively. All included pregnant women performed serological test for Toxoplasmosis in one of the laboratories of the three centers. Those who had serological text for Toxoplasmosis performed elsewhere rather than the three centers were excluded because technical procedures and reagents used were not the same. It should be noted that the three laboratories of the three centers used the same technic to measure blood levels of antibodies (detection of IgG and IgM using Biorex immunoassay).
Before the study was conducted, administrative permissions and ethical approval from the Ethics Committee of the University of Douala (number: CEI-UD/64/02/2015/T) were obtained. A questionnaire was used to collect data on the demographics, obstetric history, dietary habits, and environmental, biological and morphological entries. Serological tests were performed using the Biorex immunoassay and the results were obtained using the ELISA technique for both IgG than IgM. According to the manufacturer's instructions, an IgG ≥ 10 IU / ml and an IgM ≥ 1.1IU / ml were considered positive. This test is routinely ordered for prenatal diagnosis. The cost of the serological test was 40000 Francs CFA for both IgG and IgM detection (equivalent to 68,7179 US Dollar).
Data were entered and processed using the Epi Info 7 software and Excel 2007 (Microsoft Office), then analyzed using the XLSTAT 7.5.2 software. Quantitative variables were presented as mean ± standard deviation and categorical variables as numbers and percentages. The Chi-square test was used to determine factors associated with toxoplasmosis seroprevalence. Differences were considered significant if p < 0.05.

Results

Of the 402 potential participants, 327 gave consent and performed the serologic test for toxoplasmosis, thus a participation rate of 81.3%. The average age was 31 ± 5 years, and the ages ranged from 18 to 44 years. The most common age group was 30-34 years (117, 35.8%). Majority of the pregnant women were married (249, 76.1%) and had a university education (223, 68.2%) (Table 1). The seroprevalence of toxoplasmosis found in the sample population was 78.6% (21.4% had a negative serologic test); 78.6% of pregnant women had positive IgG and 0.9% had both IgG and IgM positive. The average value of IgG was 183 ± 1126 IU / ml with a minimum of 0.0 IU / ml and a maximum of 19714 IU / ml. 27.2% of pregnant women had an IgG between 10 and 59 IU / ml (Table 2).
Table 1: Sociodemographic characteristics of participants.
Table 2: Distribution of study population by Toxoplasma IgG values.
The seroprevalence of Toxoplasmosis did not varied significantly with age, cohabitation with cats, eating uncooked vegetables, and drinking untreated water (p>0.05). The seroprevalence was 75.7% among women aged 25-29 and 84.2% among women aged 35 -39 years (Table 3). According to lifestyle, pregnant women living with cats had a prevalence of 88.2% compared to 78.1% among women living without cats. Pregnant women who ate vegetables from multiple places had a prevalence of 87.5% compared to 77.2% who ate vegetables only at home. The seroprevalence was not statistically different between pregnant women who drank water from the Cameroon Water Company (public supplier of domestic water) and those who drank water from other sources. The seroprevalence was significantly higher in pregnant women who had primary or secondary level education compared to those who had a university education (p=0.0003) (Table 4).
Table 3: Variation of seroprevalence by age, matrimonial status, educational level and parity.
Table 4: Variation of Toxoplamosis by food habits.

Discussion

This study revealed that the seroprevalence of toxoplasmosis was 78.6%. The mean age was 31 ± 5 years, compared to 28.2 years in Thailand, 29.7 years in France and 29.9 years in Cameroon (2009) [7,12,20]. The mean age in this study was higher than that reported in other African studies: 25.3 ± 5.4 years in Tanzania [21], 23.64 and 26.96 years in Ethiopia [17,19]. The centers selected for this study have a relatively high cost of healthcare. Thus, women who are consulted in these centers, for the most part, have a higher income, meaning that most of them finished their studies and had good jobs before maternity. Many participants actually had a university degree (68.2%) compared to 4.0% of participants who had primary level of education.In recent years in Africa in general and Cameroon in particular, there is growing and widespread awareness of the importance of education as a key factor of women emancipation and development. It is important to note that these results could have been different if we had conducted the study in a rural or district hospital where healthcare is affordable for the majority of the population.
The overall seroprevalence of T gondii among pregnant women in three hospitals (78.6%) is higher than that reported in Asia (3.7 to 17.2%) [3-6], Canada (20-40%), France in 2010 (36.7%) and Serbia (39%) [10,12,13]. The prevalence is also higher than that reported in some African countries, including Tanzania (30.9%), Nigeria (40.8%), Morocco (50.6%) and Gabon (56%) [14-16,21], but lower than that reported in other African countries like Ethiopia 83.6% and Ghana 92.5% [17,18]. Indeed, the overall prevalence of T gondii is very heterogeneous across countries and even within the same country. This variation mainly depends on the level of hygiene within the population, dietary habits and climatic variations. The association with climate was reported in 2009 in France where the seroprevalence was high in the South-West region probably due to the higher temperate and humid climate of the region which promoted the conservation of oocysts in the soil compared to Eastern France (with a low seroprevalence) where temperatures are lower [12]. Moreover, in New Caledonia, the prevalence was highest in the North East (79.1%) which has the highest rain fall than the rest of the territory (56.7%) [22]. In Cameroon, the climate is hot and humid, which can facilitate the survival of oocysts.
The mean value of IgG was 183 ± 1126 IU / ml with some very high values (19714 IU / ml) with negative IgM. This was an important discovery because some practitioners believe that higher values of IgG represent active infection with risk of mother to child transmission. In fact, the immune response depends on the infecting strain, the amount of inoculated oocytes, the parasitic stage of the inoculum, and the route of inoculation. Furthermore, there are genetic factors that influence the cellular response in cases of toxoplasmosis [23].
Several studies have found a significant increase in the prevalence of toxoplasmosis with age [12,17,21], which is expected for an immunizing infection with a low mortality rate. Increasing age actually leads to longer time of exposure. Adults have probably been exposed for many years; due to the long persistence of Toxoplasma IgG into the bloodstream, serological tests remain positive. Thus, they remain positive even if they improve their level of hygiene which is supposed to reduce the seroprevalence. In this study, there was a higher prevalence among participants over 35 years, but the difference was not statistically significant. This could be due to the small sample size and big difference in the 2 comparison groups (257 participants had 35 years or less against 59 participants above 35 years).
Participants living with a cat had a higher prevalence of toxoplasmosis but the difference was not statistically significant as observed in some previous studies [17,19,24]. In the cycle of T gondii, the cat releases the resistant forms (oocysts) into the earth that contaminate drinking water, hands, and the food that will be consumed by the population (including those who do not have cats). This risk increases especially if the level of hygiene is low. Other previous studies did not find a significant association between the presence of a cat and the prevalence of T gondii [13,21,25].
Other factors associated with increased seroprevalence of Toxoplasmosis reported in previous studies include domestic water source and consumption of raw meat [13,19]. The lack of significant association between these factors and Toxoplasmosis in the current study does not mean they have no influence on transmission.
It is true that humans commonly acquire Toxoplasma gondii infection by ingesting food and water contaminated with the resistant stage of the parasite (oocyst) shed in the faeces of infected cats or by ingesting the encysted stage of the parasite (tissue cysts) in infected meat. These factors were not found to be associated in this study. Beef is the main meat consumed in the Littoral Region and has been found less likely to be a source of infection compared to others animals [26]. The thorough cooking of meat (habits of our population) significantly reduces the risk of meat-eating-related Toxoplasma infection and could also have contributed to the lack of association. Finally, the high level of education (68.2% of women had university level of education) could be associated with higher level of hygiene. It is true that there may be some biases in these results due to the fact that we didn’t asked questions on the consumption of raw sausages, salami, and cured meats which also increased the risk of contracting toxoplasmosis. Furthermore, we have to take in to account the reliability of personal interviews.
The low level of education was significantly associated with increased prevalence of T gondii in the current study. A high level of education could be associated with higher levels of hygiene which lead to the lower risk of contamination with T gondii. This association has been reported in a previous study in France [12], but not in other studies [17,19].

Conclusion

The data obtained from this study showed a high seroprevalence of toxoplasmosis among pregnant women in Douala, Cameroon. The low level of education is the main factor associated with Toxoplasmosis. The increase of the prevalence with the low level of education calls for intensive education of the population, especially, women of child-bearing age including pregnant women. Also, the high prevalence of antibodies necessitates a more comprehensive study to determinate the prevalence of recent infection and the mother-to-child transmission rate of toxoplasmosis in pregnancy. In addition, it is recommended that such studies include other possible infection risk factors that were not considered in this study in other to determine the common sources of Toxoplasma transmission. This will help provide substantive data that could contribute to policy formulation towards the institution of appropriate preventive and control measures especially in women of child-bearing age.

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