Abstract
This study aimed to determine the seroprevalence of Toxoplasma gondii in pregnant women in the south western region of Saudi Arabia and to find out the possible risk factors that may lead to infection. This cross sectional hospital based study was carried out at three hospitals in the south western region of Saudi Arabia from January 2008 to August 2010. Blood samples from 487 pregnant women were collected and used to detect anti-T. gondii antibodies IgM and IgG by enzyme linked immunosorbent assay (ELISA). A questionnaire interview was carried out to ask about some risk factors of infection. Among the 487 studied pregnant women, 38.8 % were seropositive for anti T. gondii IgG while 6.2 % were positive for anti T. gondii IgM and 3.3 % were positive for both anti T. gondii IgG & IgM. The only risk factor associated with seropositive anti T. gondii IgM was the history of the intake of immunosuppressive drugs. Regarding anti T. gondii IgG seropositivity, it was found to increase significantly with increased age, number of gravida and parities, and previous history of toxoplasmosis. The seroprevalence of T. gondii IgG & IgM by ELISA among pregnant women in the south western region of Saudi Arabia is considerable with few identifiable significant risk factors reported.
Keywords: Toxoplasma gondii, ELISA, Seroprevalence, Risk factors, Pregnant women
Introduction
Toxoplasma infection is often benign, yet congenital toxoplasmosis can lead to severe sequelae for the foetus and the newborn. Mother-to-child transmission depends on the gestational age. When infections occur soon before or during the first trimester of pregnancy it may cause miscarriage, death in utero, or severe neurological lesions. Whereas fetal infection occurring later in pregnancy may result in either congenital disease or sub–clinical infection (Remington et al. 2005).
Toxoplasma gondii seroprevalence is evolving worldwide and is subjected to complex environmental, socioeconomic and health-related practices (Pappas et al. 2009). It is more prevalent in some regions than in others and varies between different population groups within the same region (Asthana et al. 2006). In Saudi Arabia, the seroprevalence among pregnant women varies according to the region from 25 % in Jeddah (Tonkal 2008) to 42.1 % in Dammam (Abbas et al. 1986).
Undoubtedly, the early and proper diagnosis of infection in pregnant women (with the possible risk of transplacental transmission) or their babies leads to effective treatment and minimizes complications (Nagaty et al. 2009). Serological diagnosis represents the first and most widely used approach to define the stage of infection, whether current, recent or past (Sensini 2006).
Pregnant women have a great vulnerability to Toxoplasma due to the alterations in the immune mechanisms inherent to gestation. So, this study is of the utmost importance to determine the immunity of pregnant women in the south western region to this parasite. Provided with this, we can estimate the magnitude of toxoplasmosis among this critical group. This study will also help to define the possible risk factors that may lead to toxoplasma infection in order to develop extensive health education campaigns to increase the awareness and the knowledge of preventive behavior among Saudi population toward toxoplasmosis.
Materials and methods
Study population
This cross sectional hospital based study was conducted in three hospitals: (a) King Faisal Armed Forces Hospital (KFAFH) in Khamis Mushait, (b) Abha General Hospital (AGH) and (c) Maternal and Child Hospital (MCH) in Abha, south western region of Saudi Arabia from January 2008 to August 2010. A total sample of 487 pregnant women attending the antenatal clinics of the three hospitals was enrolled randomly in the study.
An approval was taken from the Ethical Committee of King Khalid University and the previously mentioned hospitals to conduct the study. An informed written consent of the pregnant women who accepted to participate in the study was secured.
Questionnaire interview on T. gondii infection
A short face to face questionnaire interview for pregnant women was carried out in the antenatal clinics of the three hospitals to obtain information regarding T. gondii infection including age, residential address, consumption of raw or undercooked meat products, drinking unboiled milk, keeping pets including cats, intake of immunosuppressive drugs, known previous history of toxoplasmosis, and history of blood transfusion or organ transplantation. Additional information about number of pregnancies, children, abortion, and ultrasonographic follow-up was collected.
Serological detection of T. gondii infection
From each pregnant woman, five ml of blood was withdrawn upon the first visit to the antenatal clinic to determine serum IgM and IgG antibody (Ab) levels against T. gondii antigens using the TOXO IgM μ-capture enzyme linked immunosorbent assay (ELISA) for direct IgM antibody detection (REF 51119) (Human GMBH, Wiesbaden Germany, www.human.de) in which the microtitre wells were coated with anti-human IgM antibodies (mouse) and the HUMAN TOXO IgG ELISA (REF 51209) (Human GMBH, Wiesbaden Germany, www.human.de) which is based on the classical ELISA technique. The microtitre strip wells were coated with Toxoplasma antigens prepared from sonicated whole T. gondii parasites (ELISA). Methodology was done as described by the manufacturer. Equivocal results were supposed to be verified 2–3 weeks latter to be considered as positive or negative, but this was not done and were excluded.
Statistical analysis
Data were coded, validated and analyzed using SPSS PC+ version 13 software package. Frequency, percentage, arithmetic mean, median and mode were used to present the data. Chi square and Student “t” test were used as tests of significance at 5 % level of significance.
Results
The present study included a total sample of 487 pregnant women recruited from three hospitals. Most of them were from King Faisal Armed Forces Hospital (252, 51.7 %) followed by Abha General Hospital (184, 37.8 %) and the Maternal and Child Hospital (51, 10.5 %).
Socio-demographic profile
Table 1 shows the age of pregnant women in the study sample ranged from 16 years to more than 41 years. The average age was 28.6 ± 5.5 years and the median age was 28 years. The majority of the study sample were housewives (400, 82.1 %). Only 87 women were working, the majority of them were teachers (63, 12.9 %).
Table 1.
Socio-demographic profile and obstetric history of the study sample
| Socio-demographic profile and obstetric history | N (n = 487) | % |
|---|---|---|
| (1) Age groups (years) | ||
| 16–19 | 14 | 2.9 |
| 20–30 | 323 | 66.3 |
| 31–40 | 143 | 29.4 |
| ≥41 | 7 | 1.4 |
| (2) Occupation | ||
| Housewife | 400 | 82.1 |
| Teacher | 63 | 12.9 |
| Student | 12 | 2.5 |
| Nurse | 8 | 1.6 |
| Governmental employee | 4 | 0.8 |
| (3) Gravida | ||
| 1 | 141 | 29 |
| 2–4 | 201 | 41.3 |
| ≥5 | 145 | 29.8 |
| (4) Parity | ||
| Zero | 166 | 34.1 |
| 1 | 79 | 16.2 |
| 2–4 | 177 | 36.3 |
| ≥5 | 65 | 13.3 |
| (5) Gestational age | ||
| First trimester | 94 | 19.3 |
| Second trimester | 271 | 55.6 |
| Third trimester | 122 | 25.1 |
| (6) Abnormal previous pregnancy outcomes: | ||
| Abortions | ||
| 0 | 325 | 66.7 |
| 1–2 | 142 | 29.2 |
| ≥3 | 20 | 4.1 |
| Malformed fetus | ||
| Yes | 7 | 1.4 |
| No | 480 | 98.6 |
Obstetric history
The average number of pregnancies was 3.6 ± 2.8 with a median of three pregnancies. The most frequent gravida history was 2–4 pregnancies in 41.3 % (201/487) of the pregnant women. Regarding “parity” of the studied sample, the average number of deliveries was 2.1 ± 2.3 with a median of 1 delivery. The most frequent “parity” history was 2–4 deliveries (177, 36.3 %). The gestational age ranged from 4 to 39 weeks with an average of 21.2 ± 8.7 weeks and a median of 20 weeks. More than half of the study sample were recruited during the second trimester of pregnancy (n = 271, 55.6 %). Two-thirds of the sample had no history of abnormal pregnancy outcomes in the form of abortions (n = 325, 66.7 %) while most of it did not give birth to a malformed fetus (480, 98.6 %) (Table 1).
Past history of toxoplasma infection and exposure to risk factors
Around 97 % had neither previous history of toxoplasmosis, nor did they give history of intake of spiramycin to treat toxoplasmosis. The majority of the pregnant women (97–100 %) had no history of exposure to different risk factors.
Seroprevalence of “anti-Toxoplasma” antibodies among pregnant women
The seroprevalence of “Anti-Toxoplasma” antibodies is shown in Table 2. The seroprevalence of anti-Toxoplasma IgG & IgM was found to be 38.8 % (189 out of 487) and 6.2 % (30 out of 487), respectively. Combined anti Toxoplasma IgG & IgM antibodies were found in 3.3 % (16 out of 487).
Table 2.
Seroprevalence of anti-Toxoplasma antibodies (IgM & IgG) among pregnant women
| Anti-toxoplasma IgM | Anti-toxoplasma IgG | Total | ||||
|---|---|---|---|---|---|---|
| Negative | Positive | |||||
| N | % | N | % | N | % | |
| Negative count | 260 | 53.4 | 158 | 32.4 | 418 | 85.8 |
| Positive count | 14 | 2.9 | 16 | 3.3 | 30 | 6.2 |
| Equivocal count | 24 | 4.9 | 15 | 3.1 | 39 | 8 |
| Total | 298 | 61.2 | 189 | 38.8 | 487 | 100 |
Determinants of sero-positive “Toxoplasma gondii” IgM among pregnant women
Table 3 shows that the IgM anti T. gondii seropositivity was higher although not statistically significant among pregnant women aged 16–19 years, housewives, and among those who were pregnant for 2–4 times.
Table 3.
Seroprevalence of T. gondii IgM and IgG antibodies in pregnant women on admission by age and occupation and obstetric history
| Variable | T. gondii IgM | T. gondii IgG | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Negative | Positive | P | Negative | Positive | P | |||||
| N | % | N | % | N | % | N | % | |||
| Age groups (years) | ||||||||||
| 16–19 years (n = 14) | 12 | 85.7 | 2 | 14.3 | χ2 = 4.71 P = 0.58 (NS) |
9 | 64.3 | 5 | 35.7 | χ2 = 7.97 P = 0.048 Significant |
| 20–30 years (n = 323) | 274 | 84.8 | 22 | 6.8 | 211 | 65.3 | 112 | 34.7 | ||
| 31–40 years (n = 143) | 126 | 88.1 | 6 | 4.2 | 75 | 52.4 | 68 | 47.6 | ||
| ≥41 (n = 7) | 6 | 85.7 | 0 | .0 | 3 | 42.9 | 4 | 57.1 | ||
| Occupation | ||||||||||
| Housewife (n = 400) | 342 | 85.5 | 27 | 6.8 | χ2 = 7.69 P = 0.46 (NS) |
242 | 60.5 | 158 | 39.5 | χ2 = 5.25 P = 0.26 (NS) |
| Teacher (n = 63) | 55 | 87.3 | 3 | 4.8 | 37 | 58.7 | 26 | 41.3 | ||
| Student (n = 12) | 9 | 75 | 0 | 0.0 | 10 | 83.3 | 2 | 16.7 | ||
| Nurse (n = 8) | 8 | 100 | 0 | 0.0 | 7 | 87.5 | 1 | 12.5 | ||
| Governmental employee (n = 4) | 4 | 100 | 0 | 0.0 | 2 | 50 | 2 | 50 | ||
| Obstetric History | ||||||||||
| Gravida | ||||||||||
| 1 (n = 41) | 124 | 87.9 | 8 | 5.7 | χ2 = 1.86 P = 0.76 (NS) |
95 | 67.4 | 46 | 32.6 | χ2 = 5.70 P = 0.05 Significant |
| 2–4 (n = 201) | 169 | 84.1 | 15 | 7.5 | 125 | 62.2 | 76 | 37.8 | ||
| ≥5 (n = 145) | 125 | 86.2 | 7 | 4.8 | 78 | 53.8 | 67 | 46.2 | ||
| Parity | ||||||||||
| 0 (n = 166) | 145 | 87.3 | 12 | 7.2 | χ2 = 4.4 P = 61 (NS) |
113 | 68.1 | 53 | 31.9 | χ2 = 7.99 P = 0.046 Significant |
| 1 (n = 79) | 68 | 86.1 | 5 | 6.3 | 52 | 65.8 | 27 | 34.2 | ||
| 2–4 (n = 177) | 150 | 84.7 | 8 | 4.5 | 97 | 54.8 | 80 | 45.2 | ||
| ≥5 (n = 65) | 55 | 84.6 | 5 | 7.7 | 36 | 55.4 | 29 | 44.6 | ||
| Gestational age | ||||||||||
| First trimester (n = 94) | 80 | 85.1 | 8 | 8.5 | χ2 = 7.4 P = 0.11 (NS) |
56 | 59.6 | 38 | 40.4 | χ2 = 1.86 P = 0.39 (NS) |
| Second trimester (n = 271) | 233 | 86 | 11 | 4.1 | 161 | 59.4 | 110 | 40.6 | ||
| Third trimester (n = 122) | 105 | 86.1 | 11 | 9 | 81 | 66.4 | 41 | 33.6 | ||
| Abnormal previous pregnancy outcomes | ||||||||||
| Abortions | ||||||||||
| 0 (n = 325) | 282 | 86.8 | 18 | 5.5 | χ2 = 2.24 P = 0.69 (NS) |
207 | 63.7 | 118 | 36.3 | χ2 = 3.32 P = 0.19 (NS) |
| 1–2 (n = 142) | 120 | 84.5 | 11 | 7.7 | 78 | 54.9 | 64 | 45.1 | ||
| ≥3 (n = 20) | 16 | 80 | 1 | 5 | 13 | 65 | 7 | 35 | ||
| Malformed fetus | ||||||||||
| Yes (n = 7) | 7 | 100 | 0 | 0.0 | χ2 = 1.17 P = 0.56 (NS) |
2 | 28.6 | 5 | 71.4 | χ2 = 3.18 P = 0.074 (NS) |
| No (n = 480) | 411 | 85.6 | 30 | 6.3 | 296 | 61.7 | 184 | 38.3 | ||
Moreover, the anti T. gondii IgG seroprevalence was found to increase significantly with age (χ2 = 7.97, P = 0.048), with increased number of pregnancies (χ2 = 5.70, P = 0.05) and with the increased number of parity (χ2 = 7.99, P = 0.046). On the other hand, gestational age, previous history of abortions or malformed fetuses, was of no significant value in developing seropositivity to T. gondii IgG.
Table 4 shows that the seroprevalence of anti T. gondii IgM was significantly higher among pregnant women who had a history of intake of immunosuppressive drugs (P = 0.03). On the other hand, other risk factors were of no statistical significant value in developing T. gondii IgM. Previous history of toxoplasmosis was significantly associated with the development of anti T. gondii IgG seropositivity (χ2 = 3.94, P = 0.047) while there were no significant associations with other risk factors.
Table 4.
Seroprevalence of T. gondii IgM and IgG antibodies in pregnant women by past history of infection and exposure to risk factor
| Variable | T. gondii IgM | T. gondii IgG by ELISA | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Negative | Positive | P | Negative | Positive | P | |||||
| N | % | N | % | N | % | N | % | |||
| Previous history of toxoplasmosis | ||||||||||
| No (473) | 406 | 85.8 | 29 | 6.1 | χ2 = 0.04 P = 0.98 (NS) |
293 | 61.9 | 180 | 38.1 | χ2 = 3.94 P = 0.047 (Significant) |
| Yes (14) | 12 | 85.7 | 1 | 7.1 | 5 | 35.7 | 9 | 64.3 | ||
| Previous history of treatment with spiramycin | ||||||||||
| No (475) | 408 | 85.9 | 29 | 6.1 | χ2 = 10 P = 0.95 (NS) |
293 | 61.7 | 182 | 38.3 | χ2 = 1.97 P = 0.160 (NS) |
| Yes (12) | 10 | 83.3 | 1 | 8.3 | 5 | 41.7 | 7 | 58.3 | ||
| Previous history of blood transfusion | ||||||||||
| No (480) | 412 | 85.8 | 30 | 6.3 | χ2 = 0.79 P = 0.67 (NS) |
295 | 61.5 | 185 | 38.5 | χ2 = 1.005 P = 0.316 (NS) |
| Yes (7) | 6 | 85.7 | 0 | 0.0 | 3 | 42.9 | 4 | 57.1 | ||
| Consumption of undercooked meat | ||||||||||
| No (483) | 415 | 85.9 | 29 | 6 | χ2 = 2.7 P = 0.26 (NS) |
296 | 61.3 | 187 | 38.7 | χ2 = 0.213 P = 0.645 (NS) |
| Yes (4) | 3 | 75 | 1 | 25 | 2 | 50 | 2 | 50 | ||
| Drinking unboiled goat milk | ||||||||||
| No (477) | 410 | 86 | 28 | 5.93 | χ2 = 4.0 P = 0.13 (NS) |
293 | 61.4 | 184 | 38.6 | χ2 = 0.54 P = 0.463 (NS) |
| Yes (10) | 8 | 80 | 2 | 13.3 | 5 | 50 | 5 | 50 | ||
| Owing a cat | ||||||||||
| No (472) | 406 | 86 | 28 | 5.93 | χ2 = 1.71 P = 2.7 (NS) |
289 | 61.2 | 183 | 38.8 | χ2 = 0.14 P = 0.75 (NS) |
| Yes (15) | 12 | 80 | 2 | 13.3 | 9 | 60 | 6 | 40 | ||
| Intake of immunosuppressive drugs | ||||||||||
| No (n = 484) | 417 | 86.2 | 29 | 6 | χ2 = 7 P = 0.03 Significant |
296 | 61.2 | 188 | 38.8 | χ2 = 0.038 P = 0.845 (NS) |
| Yes (n = 3) | 1 | 33.3 | 1 | 33.3 | 2 | 66.7 | 1 | 33.3 | ||
| Total | 418 | 85.8 | 30 | 6.2 | ||||||
Discussion
Although toxoplasmosis is considered harmless for non-pregnant women, it is potentially harmful during pregnancy, especially at the first trimester (Giannoulis et al. 2008). In the current study, the seropositivity for anti T.gondii IgG & IgM was 38.8 % (189/487) and 6.2 % (30/487), respectively. The combined seropositivity for anti T. gondii IgG and IgM was found to be 3.3 % (16/487) using ELISA.
Compared to the outcomes of similar studies done in different regions of Saudi Arabia, the seroprevalence of T. gondii IgG is in agreement with that reported in a recent Saudi study in Riyadh in which anti T. gondii IgG was found in 38 % of the studied pregnant women (Almogren 2011). In addition to that, anti-Toxoplasma IgG seropositivity was reported in the Eastern province to be 39.4 % (69/175) (Al-Mulhim and Al Qurashi 2001). Our results are also comparable to the results of a study done in Makkah, where the anti Toxoplasma IgG seropositivity was found to be 35.6 % (Ghazi et al. 2002). On the other hand, the results of the current study are somewhat higher than those of other similarly designed Saudi studies. In Makkah Al–Mukkaramah, the seroprevalence of T. gondii IgG & IgM were 29.4 % (58/197) and 5.6 % (11/197), respectively (Al-Harthi et al. 2006). In a recent Saudi study, anti T. gondii IgG & IgM seropositivity by ELISA were reported in 27.5 and 46.3 % of the studied pregnant women, respectively (Al Mohammad et al. 2010). In Jeddah, T. gondii IgG seropositivity was found in 25 % of the pregnant women (Tonkal 2008). On the contrary, the seroprevalence reported in this study was lower than that of a study done in Dammam area (42.1 %) (Abbas et al. 1986).
It was noticeable that the 38.8 % seroprevalence rate obtained in this study lies within the range of the average prevalence rate of T. gondii in Asian countries. High prevalence foci exist in the Middle East including Turkey, Iran, Iraq, Kuwait, Saudi Arabia, Jordan, Oman, and Lebanon (Pappas et al. 2009; Abu-Madi et al. 2008). In Palestine, the seroprevalence of T. gondii IgG among the studied pregnant women was 27.9 % (Nijem and Al-Amleh 2009). In Qatar, it was 35.1 % among women of the childbearing age (Abu-Madi et al. 2010). In Jordan, the seroprevalence of anti T. gondii IgM was reported to be 47.1 % among pregnant women (Jumaian 2005). As for Kuwait, the T. gondii IgG & IgM seroprevalence among pregnant women were reported to be 53.1 and 13.8 %, respectively (Iqbal and Khalid 2007).
This variation has been attributed to climate, cultural differences regarding hygienic and feeding habits, as well as subpopulations’ religious and socioeconomic practice (Pappas et al. 2009). The phenomenon of mixed racial populations may explain some of the observed differences which may be due to differences in the daily practices and ethnic habits (Chan et al. 2008). In Qatar, the increase in T. gondii IgG seropositivity was found among women coming from the East Mediterranean region or Africa than among others (Abu-Madi et al. 2008). Another important factor is the different methods used to determine the seroprevalence in the previously mentioned studies.
The high prevalence of Toxoplasma in this region (south western region) of the KSA could be attributed to that this region is observed to have a high population of cats (the final host of the parasite). Cats have been reported by Dubey (2009) as a high risk factor causes infection to the intermediate hosts including humans.
In the current study, we found no significant association between any of the women’s characteristics and seropositivity for T. gondii IgM. Regarding exposure to possible risk factors, we found that pregnant women who reported history of intake of immunosuppressive drugs for different indications were significantly associated with T. gondii IgM seropositivity (χ2 = 7, P = 0.3). But exposure to various other risk factors was not significantly associated with Toxoplasma IgM seropositivity. These results are strongly supported by Petersen et al. (2010) who found that T. gondii cannot be explained by the presence of a risk factor.
In accordance with the results of the current study, a similar study on pregnant women in Makkah showed that the seroprevalence of IgM level had no significant difference among different age groups, whereas, the IgG level was significantly higher (P < 0.05) in older age groups. The highest level of T. gondii IgG seropositivity was found among pregnant women of 35–45 years (43 %). A recent Saudi study carried out in Al Hassa, also concluded that increased maternal age (>30 years) was significantly associated with increased risk of toxoplasmosis (Al Mohammad et al. 2010). The same finding was also reported in Qatar (Abu-Madi et al. 2008). The significant association with mother’s age has been well known (Remington et al. 2001).
There was no significant association between Toxoplasma seropositivity (IgM or IgG) and the previous history of abnormal pregnancy outcomes as abortions or malformed babies. This is in agreement with the results of a previous Saudi study which denoted the absence of significant associations with previous history of abortions (Al-Harthi et al. 2006). In addition, another Saudi study reported that the perinatal outcome of pregnancy was remarkably good with no abortions, stillbirths, premature deliveries or congenital anomalies associated with Toxoplasma seropositivity (Al-Mulhim and Al Qurashi 2001).
In a recent study, fourteen case–control studies evaluating the importance of different risk factors for infection of humans with T. gondii were identified. Surprisingly, up to two-thirds of infections could not be explained by presence of risk factors (Petersen et al. 2010). In conclusion, considerable T. gondii IgM & IgG seropositivity by ELISA with limited identifiable significant risk factors are revealed in the study.
Acknowledgments
The authors extend their appreciation to King Abdulaziz City for Science and Technology (KACST) for providing fund through the Research Project No. AT–27–112.
References
- Abbas SA, Basalamah A, Serebour F, Alfonso M. The prevalence of Toxoplasma gondii antibodies in Saudi women and the outcome of congenital infection among newborns in Saudi Arabia. Saudi Med J. 1986;7:346–354. [Google Scholar]
- Abu-Madi MA, Al-Molawi N, Behnke JM. Seroprevalence and epidemiological correlates of Toxoplasma gondii infections among patients referred for hospital-based serological testing in Doha, Qatar. Parasitol Vectors. 2008;1:39. doi: 10.1186/1756-3305-1-39. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Abu-Madi MA, Behnke JM, Dabritz HA. Toxoplasma gondii seropositivity and co-infection with TORCH pathogens in high-risk patients from Qatar. Am J Trop Med Hyg. 2010;82(4):626–633. doi: 10.4269/ajtmh.2010.09-0530. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Al Mohammad HI, Balaha MH, Amin TT, El Damarany EE, Dwedar A. The accuracy of IgG avidity for detection of acute toxoplasmosis among pregnant Saudi women. TAF Prevent Med Bull. 2010;9(1):7–14. [Google Scholar]
- Al-Harthi SA, Jamaoom MB, Ghazi HO. Seroprevalence of Toxoplasma gondii among pregnant women in Makkah, Saudi Arabia. Umm Al-Qura Univ. J Sci Med Eng. 2006;18(2):217–227. [Google Scholar]
- Almogren A. Antenatal screening for Toxoplasma gondii infection at a tertiary care hospital in Riyadh, Saudi Arabia. Ann Saudi Med. 2011;31(6):569–572. doi: 10.4103/0256-4947.87090. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Al-Mulhim AA, Al Qurashi MA. Seroprevalence of toxoplasmosis in pregnant mothers and new born infants in eastern province, Saudi Arabia. J Family Community Med. 2001;8(1):45–53. [PMC free article] [PubMed] [Google Scholar]
- Asthana SP, Macpherson CN, Weiss SH, Stephens R, et al. Seroprevalence of Toxoplasma gondii in pregnant women and cats in Grenada, West Indies. J Parasitol. 2006;92:644–645. doi: 10.1645/GE-762R.1. [DOI] [PubMed] [Google Scholar]
- Chan BT, Amal RN, Hayati MI, Kino H, Anisa N, Norhayati M, et al. Seroprevalence of toxoplasmosis among migrant workers from different Asian countries working in Malaysia. Southeast Asian J Trop Med Public Health. 2008;39:9–13. [PubMed] [Google Scholar]
- Dubey JP. History of the discovery of the life cycle of Toxoplasma gondii. Int J Parasitol. 2009;39(8):877–882. doi: 10.1016/j.ijpara.2009.01.005. [DOI] [PubMed] [Google Scholar]
- Ghazi HO, Telmesani AM, Mahomed MF. TORCH agents in pregnant Saudi women. Med Princ Pract. 2002;11(4):180. doi: 10.1159/000065813. [DOI] [PubMed] [Google Scholar]
- Giannoulis C, Zournatzi B, Giomisi A, Diza E, Tzafettas I. Toxoplasmosis during pregnancy: a case report and review of literature. Hippokratia. 2008;12(3):139–143. [PMC free article] [PubMed] [Google Scholar]
- Iqbal K, Khalid N. Detection of acute Toxoplasma gondii infection in early pregnancy by IgG avidity and PCR analysis. J Med Microbiol. 2007;56(11):1495–1503. doi: 10.1099/jmm.0.47260-0. [DOI] [PubMed] [Google Scholar]
- Jumaian NF. Seroprevalence and risk factors for Toxoplasma infection in pregnant women in Jordan. East Mediterr Health J. 2005;11:45–51. [PubMed] [Google Scholar]
- Nagaty IM, Ibrahim KM, Abdel-Tawab AH, Hassan AE. Diagnosis of Toxoplasma gondii by ELISA and PCR mothers and their infants. J Egypt Soc Parasitol. 2009;39(2):625–632. [PubMed] [Google Scholar]
- Nijem KI, Al-Amleh S. Seroprevalence and associated risk factors of toxoplasmosis in pregnant women in Hebron district, Palestine. East Mediterr Health J. 2009;15(5):1278–1284. [PubMed] [Google Scholar]
- Pappas G, Roussos N, Falagas ME. Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol. 2009;39:1385. doi: 10.1016/j.ijpara.2009.04.003. [DOI] [PubMed] [Google Scholar]
- Petersen E, Vesco G, Villari S, Buffolano W. What do we know about risk factors for infection in humans with Toxoplasma gondii and how can we prevent infections? Zoonoses Public Health. 2010;57(1):8–17. doi: 10.1111/j.1863-2378.2009.01278.x. [DOI] [PubMed] [Google Scholar]
- Remington JS, McLeod R, Thulliez P, Desmonts G. Toxoplasmosis. In: Remington JS, Klein JO, editors. Infectious diseases of the fetus and newborn infant. 5. Philadelphia: Saunders; 2001. pp. 205–346. [Google Scholar]
- Remington JS, McLeod R, Thullie P, Desmonts G. Toxoplasmosis. In: Remington JS, Baker C, Wilson E, Klein JO, editors. Infectious diseases of the fetus and newborn infant. 6. Philadelphia: WB Saunders; 2005. pp. 947–1091. [Google Scholar]
- Sensini A. Toxoplasma gondii infection in pregnancy: opportunities and pitfalls of serological diagnosis. Clin Microbiol Infect. 2006;12(6):504–512. doi: 10.1111/j.1469-0691.2006.01444.x. [DOI] [PubMed] [Google Scholar]
- Tonkal A. PCR versus ELISA in diagnosis of human toxoplasmosis in Jeddah, Saudi Arabia. J Egypt Soc Parasitol. 2008;38(3):707–714. [PubMed] [Google Scholar]