Journal of
Infectious Diseases and Immunity

  • Abbreviation: J. Infect. Dis. Immun.
  • Language: English
  • ISSN: 2141-2375
  • DOI: 10.5897/JIDI
  • Start Year: 2009
  • Published Articles: 94

Full Length Research Paper

Seroepidemiology of Toxoplasmosis among Pregnant Women in Osogbo, Southwestern, Nigeria

Olusi Titus Adeniyi
  • Olusi Titus Adeniyi
  • Department of Biology, Federal University of Technology Akure, Ondo State, Nigeria.
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Salawu Saheed Adekola
  • Salawu Saheed Adekola
  • Department of Zoology, Obafemi Awolowo University, Ile Ife Osun State, Nigeria.
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Oniya Mobolanle Oladipo
  • Oniya Mobolanle Oladipo
  • Department of Biology, Federal University of Technology Akure, Ondo State, Nigeria.
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  •  Received: 26 February 2018
  •  Accepted: 22 March 2018
  •  Published: 31 March 2018

 ABSTRACT

Infection with Toxoplasma gondii during pregnancy represents a risk of congenital infection. Simple hygienic practices due to adequate knowledge about the parasite is one of the major keys to avoiding this preventable infection among pregnant women and women of child bearing age. The present cross sectional study was carried out to investigate the seroprevalence of anti-Toxoplasma Immunoglobulin G (IgG) and Immunoglobulin M (IgM) antibodies, associated risk factors of infection and knowledge about T. gondii, its transmission, treatment and prevention among pregnant women in Osogbo, Southwestern Nigeria.  A total of 391 serum samples were collected from consenting pregnant women aged 16-50 years attending ante-natal clinic in four major hospitals within Osogbo between October and December, 2015. The samples were screen for toxoplasmosis using specific Toxo IgG and IgM Enzyme-Linked Immunosorbent Assay (ELISA) kits. Information on sociodemographic data, associated risk factors and knowledge about the T. gondii were obtained from the women using a structured questionnaire. The results indicated that 30.44% and 17.14% of the women had anti-Toxoplasma IgG and IgM antibodies respectively. Seropositivity of Toxoplasma infection was found to increase positively with the age of the pregnant women and decreases with increase in level of education. Logistic regression analysis showed a significant association between participant’s age, habit of tasting meat while cooking and cat ownership. A generally low knowledge of T. gondii was observed in this study whereby majority (90.76%) of the pregnant women claimed not to have any knowledge about toxoplasmosis while none of the participant admitted to been previously tested for the disease. 
 
Key words:  Seroprevalence, Infection, pregnant women, IgG and IgM antibodies, Toxoplasma gondii


 INTRODUCTION

Toxoplasma gondii is an obligate intracellular coccidian parasite found in many species of animals in virtually all parts of the world (Ishaku et al., 2009) except the Antarctica (Uttah et al., 2013) and approximately one third of the world’s population is infected with the parasite (Tenter et al., 2000). T. gondii infection is asymptomatic in the immunocompetent but causes a severe clinical complication in immunecompromised individuals and to the foetuses of mothers suffering from primary infection during pregnancy (Torda, 2001; Remington et al., 2001). Humans are infected majorly through consumption of contaminated foods, fruits, vegetables and water while pregnant women can transfer the infection through placenta to unborn foetuses (Remington et al., 2001). Maternal infection acquired before pregnancy does not affect foetus (Montaya & Liesenfeld, 2004) but those acquired during pregnancy can lead to complication for the foetus most especially if primary infection is acquired during the first trimester when the disease causes severe neurological damage, miscarriage or death. Foetal infection during second and third trimesters may result in either congenital disease or subclinical infection (Remington et al., 2005). Most congenitally infected babies appear normal at birth, however, serious sequelae such as neurological impairment and chorioretinitis can manifest in the second or third decades of life (Dunn et al., 1999). Seroconversion of susceptible women of child-bearing age are preventable by simple precautions if such women are well informed. These precautions include consumption of well cooked meat, avoidance of ingesting fruits and vegetable contaminated with T. gondii oocyst and observance of improved personal hygiene in the handling of cat litters and in gardening. Routine screening for toxoplasmosis among pregnant women is the key to early detection of infection which can assist in early chemotherapy to avert any impending damage to the foetus. This practice is the norm in some European countries including France, Germany and Austria but this has not been introduced / included in the tests mandated for pregnant women attending ante-natal care clinic in Nigeria. It is very germane that studies on the seroepidemiology of the parasite partially, knowledge about the parasite, its transmission, treatment and prevention are necessary in Nigeria as they would provide a baseline on the disease thereby justifying the need for inclusion of toxoplasmosis tests in the routine screening of pregnant women and the need for health care providers to step up sensitization of pregnant women about the devastating consequence of toxoplasmosis in Nigeria. Here lays the significance of the present study.


 MATERIALS AND METHODS

A cross sectional study was conducted between October and December 2015 to determine the seroprevalence and knowledge about T. gondii among pregnant women attending ante-natal care clinic in two major hospitals and two primary heath care centre in Osogbo, Southwestern Nigeria. Osogbo is the capital of Osun State and lies on coordinates, 07° 46’ N and 04° 34’ E with elevation of 320 m above the sea level. According to the NPC, (2006) the city has a population of about 250,951 people and a landmass of 47 km2. Osogbo has tropical climate with an annual average temperature and precipitation of 26.1°C and 1, 241 mm respectively (Yusuf, 2016). The vegetation of the area is described as derived savannah characterized by a gallery of forest and tall grasses with scattered perennial trees (Ola and Adewale, 2014). The inhabitants are predominantly Yoruba speaking ethnic extraction of the Southwest Nigeria with a few representations of people from other ethnic groups of Nigeria.
 
Consent and Ethical Issues
 
Ethical clearance was sought and collected from Osun State Ministry of Health and the Ethical Boards of the hospitals involved in this study before the commencement of blood sample collection. The pregnant women who were recruited in this study were adequately enlightened on the purpose and importance of the study. Participants who consented were assured of confidentiality.
 
Questionnaire administration
 
A well-structured, pre-tested and closed-ended questionnaire was administered orally to extract from participants their socio-demographic (sex, age, place of residence) and socio-economic (occupation, literacy, ethic group) information/details, risk factors associated with toxoplasmosis acquisition including habit of tasting of meat while cooking, owning of cats and knowledge about the parasite, its transmission, treatment and prevention. Subjects’ local language/ dialect was used to extract information and their responses were recorded by ticking the appropriate boxes in the questionnaire.
 
Collection of blood samples
 
5 ml of venous blood was collected from each participant by a qualified phlebotomist following the standard procedure for blood collection. Each blood sample was collected into a plain vacutainer and was allow to clot. The clots were removed and the sample was centrifuged at 2000 rpm for 10 min. The resulting clear serum samples was carefully collected in a vial and kept at -20°C in the Parasitology Laboratory, Department of Zoology, Obafemi Awolowo University Ile Ife prior to serological examination. Each serum was tested for the presence of anti-Toxoplasma IgG and IgM antibodies in duplicate using commercially procured Enzyme Linked Immunosorbent Assay Elisa Kit (Microwell Toxo Kit) (Bio-Inteco Diagnostic Ltd. UK) designed for this purpose and strictly following the manufacturer’s instruction. The mean value for each sample was calculated by dividing the mean absorbance values of duplicate wells of each sample by the cut off calibrator mean value.
 
Statistical analysis
 
All statistical analyses were performed using SPSS for windows version 20.0. Relationship between antibodies seroprevalence was determined by Pearson chi-square test at 95% confidence interval and 0.05 level of significant. Bivariate logistic regression was further carried out to assess the predictive effect of the various risk factors on the seroprevalence of T. gondii in this study.


 RESULTS

A total of 391 pregnant women were recruited from four hospitals in Osogbo metropolis between October and December 2015. Most of the pregnant women (153, 39.1%) were from State Hospital, Asubiaro followed by Atelewo Primary Healthcare (104, 26.6%), Oke-Baale Primary Healthcare (80, 20.5%) and Ladoke Akintola University Teaching Hospital (54, 13.8%) (Table 1). 
 
 
 
 
Knowledge about the parasite, its transmission, causes, treatment and prevention
 
 
Table 2 summarizes respondence response regarding their knowledge, transmission, treatment and prevention of T. gondi. Thirty-six (9.21%) claimed to have knowledge about the existence of the parasite while majority (355, 90.79%) of the pregnant women claimed not to know anything about the parasite. None of the participants indicated that they had ever been tested for toxoplasmosis; however approximately 40% were uncertain if they had been tested before. Fourteen (3.58%) participants indicated that they heard about toxoplasmosis on radio programme while 47 (12.02%) believed that bacteria was the etiologic agent of toxoplasmosis. There was under spread ignorance on the mode of transmission, treatment and preventive measures of toxoplasmosis among population understudy. This is because 30 (7.67%) indicated that the disease could be contacted by insect bites while 280 (71.61%) did not have an idea on how the parasite is contracted. Seventeen (4.34%) claimed toxoplasmosis does not have cure while 47.47% indicated that it could be cured by chemotherapy. Majority (53.96%) of the participant do not know any preventive measures to adopt in order to avoid contracting toxoplasmosis while 28.13% claimed that improved personal hygiene can prevent toxoplasmosis.

 

 
Seroprevalence of T. gondii antibodies among pregnant women in Osogbo
 
The overall seroprevalence of anti-Toxoplasma IgG and IgM antibodies recorded in this study were 30.43 and 17.14% respectively (Table 3). The highest prevalence of both IgG (36.67%) and IgM (19.17%) antibodies were recorded among pregnant women aged 31-40 years while least prevalences of both IgG (13.64%) and IgM (9.09) were recorded among the ≤20 years age group. None of the pregnant women at age group 41-50 years had anti-Toxoplasma IgM antibodies. The seroprevalence of both IgG and IgM antibodies increased as the age of the women increased. There was a significant relationship between age distribution and seropositivity to anti-Toxoplasma IgG and IgM antibodies among the pregnant women. (PË‚0.05). It was observed from the result (Table 3) that significantly high seroprevalence to anti-Toxoplasma antibodies was recorded in all pregnant women based on marital status except the widowed who recorded the least prevalence of IgG (9.09%) and IgM (9.09%) antibodies in the category (PË‚0.05). Considering the effect of occupational affiliations on seropositivity of Toxoplasma infection among the women studied, a non-significantly higher seroprevalence of anti-Toxoplasma antibodies was recorded among the artisans than any other in the category P˃0.05. Considering the influence of level of educational attainment on the prevalence of anti-T. gondii antibodies, results indicate that seropositivity to IgM antibodies decreased as the level of education increases (P˃0.05). High seroprevalence of anti-Toxoplasma antibodies were recorded in all the pregnant women in all gestational ages in this study; highest IgG (31.25%) and IgM (20.39%) were recorded among those in their first and third trimesters respectively (P˃0.05).
 
 
 
 
 
High seroprevalence of anti-Toxoplasma IgG (31.90) and IgM (17.56%) antibodies was recorded among pregnant women that engaged in habit of tasting raw or undercooked meat while cooking than their counterparts who do not engaged in tasting of undercooked meat while cooking (P˃0.05). Effect of backyard gardening was assessed with respect to seropositivity of Toxoplasma infection; the result shows that higher prevalence of infection was recorded among pregnant women that do not engaged in backyard gardening than their counterpart that engaged in backyard gardening (P˃0.05). Majority of the pregnant women in the study admitted to habouring of rodents/cockroaches in their household; consequently highest prevalence of anti-Toxoplasma IgG (31.14%) and IgM (17.96%) antibodies where recorded among them (P˃0.05). Also, a higher seroprevalence of T. gondii infection was recorded among pregnant women that are unaware of any cat visiting their premises (P˃0.05). Potential risk factors were identified in this study, after adjusting for the effect of individual variables. Toxoplasmosis infection can be explained by three of the variables entered into the model (Table 4). These are the participant’s age, cat ownership and tasting of raw/undercooked meat. The risk factors analysis showed that the odds of being infected with toxoplasmosis are more likely among younger pregnant women within the child bearing age. Pregnant women whose ages are ≤ 20 years and 21-30 years were approximately 4.0 and 2.5 times more likely to be infected with T. gondii than their older counterpart’s age (41-50 years). The risk factors also showed that pregnant women who owned cat were 3 times more likely to be infected with T. gondii than those who did not own a cat. According to habit of tasting raw/ undercooked meat among the pregnant women, the odd of being infected with T. gondii was observed to be 4 times more likely in pregnant women that engaged in the habit than those who did not.
 
 


 DISCUSSION

Several reports on the seroprevalence of toxoplasmosis among pregnant women has been reported from various part of the world (Dubey, 2004) but this current study is one of the few from Nigeria that explore the seroprevalence and knowledge about T. gondii, its transmission, causes and prevention among pregnant women who stands the risk of congenitally infected babies if and when they contract the disease. In this study, the overall seroprevalence of T. gondii antibodies among pregnant women was 40.59%. High seroprevalence of IgG (30.44%) and IgM (17.15%) representing chronic/ latent and recently acquired toxoplasmosis respectively were recorded among the sampled pregnant women. The result of IgG antibodies recorded in this study is comparable to 31.5% reported elsewhere in Nigeria by Emmanuel et al. (2011) and 35.1% reported in Qatar by Abu Madi et al. (2010), but higher than 27.9% reported in Palestine (Nijem and Al-Amleh, 2009). The varied prevalence rates been reported by various authors might be due to differences in geographical location, levels of exposure, methodology, sample size and behavioral attitudes of the population (Yusuf et al., 2016). The result of this study suggest that considerable number of pregnant women (69.56%) sampled in Osogbo, Southwest Nigeria are seronegative that is they have not been exposed to T. gondii. This group is at risk of becoming infected later in life if they come in contact with the parasite. According to Moura et al. (2013) guidance on primary preventive measures and serological monitoring of pregnant women in the at-risk (seronegative) group are important measures for preventing congenital toxoplasmosis.
 
An increase in seropositivity of anti-Toxoplasma antibodies was observed with increasing age in this study. This is in agreement with other studies (Bobic et al., 1998; Ertug et al., 2005; Ishaku et al., 2009; Zeneme et al., 2012). Findings also suggest that low level of education was associated with higher rate of toxoplasmosis infection among pregnant women in this study. This is in agreement with reports of previous studies (Jones et al; 2001; Hajsoleimani et al., 2012; Ataenia and Tadavon, 2008; Varella et al., 2003; Ishaku et al., 2009). Pregnant women that were artisan and civil servants recorded a non-significantly higher prevalence in anti-Toxoplasma antibodies while lower seropositivity of T. gondii antibodies was observed among pregnant women that were students. This is in line with the findings of Zemene et al. (2012) and Ahmed et al. (1988) who recorded higher seropositivity to T. gondii antibodies among employed pregnant women. The explanation for this might be that employed pregnant women are financially stable with incomes that enable them buy meat compared to students who essentially dependent financially on either parents or guardian. A non- significant association was recorded between T. gondii infection and gestational age in this study. This result is in agreement with studies in Saudi Arabia (Al-Harthi et al., 2006) and Addis Ababa (Gelaye et al., 2014) but in contrary to a previous study by Aqeely et al. (2014). Pregnant women in their first and second trimester recorded high prevalence of IgG (chronic) and IgM (recently acquired infection) respectively. Infection of pregnant women with T. gondii in their first trimester according to Dunn et al. (1999) could lead to miscarriage or foetal death while infection acquired during the second trimester may result in either congenital disease or subclinical infection (Remington et al., 2005). Contact with cat as resulting from cat ownership was assessed in this study and cat contact was significant associated with  T. gondii infection.
 
These findings are in agreement with results obtained in Taiwan (Lin et al., 2008), Ethiopia (Zemene et al., 2012), France (Baril et al., 1999) and Brazil (Moura et al., 2013). Backyard gardening, tasting of raw/undercooked meat and presence of rodent/cockroaches in the households has been reported to be potential sources of T. gondii infection (Sroka et al., 2010; Koskiniemi et al., 1989; Alvarado et al., 2011; Moura et al., 2013), this probably explains why a significant relationship was recorded among pregnant women that are habitual taster of raw/undercooked meat in this study and T. gondii infection. Although in Nigeria, proper cooking of meat is the norm but the present study recorded a significantly higher prevalence of toxoplasmosis among pregnant women who engaged in the habit of tasting meat while cooking than their counterparts who do not. This result agrees with previous findings of Cook et al. (2000), Spalding et al. (2005) and Ishaku et al. (2009). Tasting of meat while cooking may serve as a route of ingesting tissue cysts that have not been killed thus causing toxoplasmosis infection. Also, logistic regression model showed that participant’s age, cat ownership and habit of meat tasting were significantly associated with toxoplasmosis infection among pregnant women. The odds of being infected by younger pregnant women were more likely than in the older ones. This observation is similar to the findings of Ertug et al. (2005) in Turkey, Esquivel et al. (2006) in Mexico and Walle et al. (2013) in Ethiopia. Consumption of raw/undercooked meat is common among some women who engaged in tasting of meat in the course of checking if the meat is well cooked thereby increasing the risk of infection. The odds of infection were more among those that taste undercooked meat while cooking than non-taster.
 
This result is not surprising because consumption of undercooked meat is one of the risk factors for T. gondii transmission therefore The finding is in line with the previous studies of Gelaye et al. (2012) and Endris et al. (2014).  According to Dubey, (2004) who reported that cats are definitive hosts that shed millions of oocysts within short period of time and play a major role in transmitting T. gondii infection, ownership of cat was found to be significantly associated with T. gondii infection. This is in agreement with other results reported from Jimmah town, Ethiopia (Zemene et al., 2012), Dabre Tabor, Ethiopia (Agmas et al., 2015) and Thailand (Nissapatorn et al., 2011).The results of the present study showed that there was absolutely low knowledge about the parasites, its transmission, causes and prevention among the pregnant women in the study area. Majority (355, 90.79%) of the women claimed not to have any knowledge about the parasite, a condition that put all these women at a great risk of infection as they will be expose them to the infection and other risk factors in the environment. Similar findings were recorded by Miller et al. (2014) among pregnant and postpartum women in Brazil where over 72% claimed not to have heard about the parasite. There was a relatively low knowledge about the role of contact with cats, consumption of raw/ undercooked meat and other risk factors in the study area which conforms with the observation of Jones et al. (2003).

 


 CONCLUSION

The findings of this study showed a high seroprevalence of toxoplasmosis and a very low level of awareness and understanding about the parasite (T. gondii), its transmission, causes and prevention among the study population. 


 RECOMMENDATIONS

There is a need for the inclusion of mandatory screening for toxoplasmosis in ante-natal care and the need to sensitize women of child bearing age about the disease and the risk factors that could predispose them to contracting the parasite, thereby, preventing maternal and congenital infections.
 

 


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.

 


 ACKNOWLEDGEMENTS

The authors sincerely appreciate the cooperation of the pregnant women that took part in this study and the support of the management of the following hospitals; Lautech Teaching Hospital, Osogbo, State Hospital Asubiaro, Atelewo Primary Healthcare Centre and Oke- baale Primary Healthcare Centre.

 



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