Open Access

Toxoplasma infection in pregnant women: a current status in Songklanagarind hospital, southern Thailand

  • Hemah Andiappan1,
  • Veeranoot Nissapatorn1Email author,
  • Nongyao Sawangjaroen2,
  • Waenurama Chemoh2,
  • Yee Ling Lau1,
  • Thulasi Kumar1,
  • Subashini Onichandran1,
  • Chitkasaem Suwanrath3 and
  • Verapol Chandeying3, 4
Parasites & Vectors20147:239

https://doi.org/10.1186/1756-3305-7-239

Received: 28 March 2014

Accepted: 19 May 2014

Published: 22 May 2014

Abstract

Background

Toxoplasmosis, being one of the TORCH’s infections in pregnant women, is caused by Toxoplasma gondii, an obligate intracellular protozoan parasite. This parasitic infection in pregnancy congenitally causes severe outcomes to their fetus and newborn. This study aimed to determine the seroprevalence and stages of Toxoplasma infection in pregnant women and its associated risks exposures.

Methods

The study was conducted within the pregnant women attending the antenatal clinic (ANC) at Songklanagarind hospital, Hat Yai, Songkhla province, Thailand. The sera of a total of 760 consecutive pregnant women were screened using standard commercial ELISA kits for detection of anti-Toxoplasma IgG and IgM antibodies. IgG avidity in the seropositive for both anti-Toxoplasma IgG and IgM antibodies were also assessed. The pregnant women’s socio-demographic, obstetrics and risk factors associated with Toxoplasma seropositivity data were analyzed using univariate and multivariate analyses.

Results

From the total 760 pregnant women, 190 (25%, 95% CI = 22.05-28.20) were positive for anti-Toxoplasma antibodies. Of these, 167 (22.0%, 95% CI = 19.0-25.0) were positive for only anti-Toxoplasma IgG antibody and 23 (3.0%, 95% CI = 2.0-4.0) were positive for both anti-Toxoplasma IgG and IgM antibodies. All these samples were high avidity, indicated the infection occured prior to four to five months. By applying statistical univariate analysis, age group, occupation and sources of drinking water showed a significant association with Toxoplasma seropositivity (p < 0.05). Multivariate logistic regression analysis further indicated that the significant factors associated with Toxoplasma seropositivity are age ≥26 (OR = 1.65, 95% CI = 1.11-2.44), working as laborer (OR = 1.57, 95% CI = 1.13-2.18) and drinking unclean (piped/tap/rain) water (OR = 1.75, 95% CI = 1.08-2.84).

Conclusion

The pregnant women in the active age group, working as laborers and exposure to unclean drinking water from various sources were at higher risk of Toxoplasma infection. Therefore, health education and the awareness of risk exposures regarding this parasitic disease are required to minimize the effects of this parasitic infection in pregnant women as well as in the general population.

Keywords

Toxoplasmosis Toxoplasma gondii Seroprevalence Risk factors Pregnant women Thailand

Background

Toxoplasma gondii, an obligate intracellular protozoan parasite [1], is capable of causing severe and life threatening conditions in pregnant women and immunocompromised individuals. The sources of this parasitic infection are by the ingestion of raw and/or undercooked meat containing parasite cysts in the animal tissues, by consuming oocysts infected water and/or food, or having contact with cat fecal contaminated soil [2]. Toxoplasma infection in pregnant women, poses great concern to the fetus. Severe impairment occurs internally, i.e. hydrocephalus, intracerebral calcification, retinochoroiditis and mental retardation, however, clinical presentation in the newborn is asymptomatic at birth in general [3].

Detection of anti-Toxoplasma antibodies in pregnant women is the most widely used approach in diagnosis of this parasitic infection [4]. The detected antibodies, which indicate recent or past infection in the pregnant women, are important to confirm whether the fetus is at risk [5]. The presence of anti-Toxoplasma IgG antibodies represents past infection meanwhile the detection of anti-Toxoplasma IgM antibodies indicates recent infection [6]. However, the specified IgM antibodies remain for several months or years after initial infection [7]. This limitation causes a problem in diagnosis of whether the maternal infection occurs prior to or after conception. Misinterpretation of IgM positive results in conventional single-serum assay may lead to misdirection in treatment and termination of pregnancy [8]. The assessment of IgG avidity for Toxoplasma infection in pregnant women has been introduced in recent studies to assist in discrimination between past and recently acquired infection. The result of this avidity test is most helpful in determining the infection of Toxoplasma in pregnant woman, especially for those who are in their first trimester [9].

Therefore, this study was conducted to determine the current seroprevalence of Toxoplasma infection among pregnant women attending the ANC at Songklanagarind hospital, southern Thailand, to investigate the association between plausible risk factors of Toxoplasma infection with the seropositive pregnant women and to validate the stages of Toxoplasma infection in these pregnant women using avidity measurement.

Methods

Study site and population

A prospective cross-sectional study was carried out at the ANC of Songklanagarind hospital, Hat Yai, Songkhla province, Thailand from December 2012 to August 2013. This public hospital attached to Prince of Songkla University, with its capacity of 850 in-patient beds, is located in the south of Thailand and was built to facilitate the teaching, research, and training for medical personnel in various disciplines, and for the provision of healthcare to the general public, particularly among Southern Thais. The study included 760 eligible pregnant women who gave informed consent before this study. The questionnaire [10] was designed to detect socio-demographic and biologically plausible risk factors associated with Toxoplasma infection, and clinical history and presenting signs and symptoms relating to toxoplasmosis (if any). This study was conducted with the approval from the ethical committee of the Faculty of Medicine, Prince of Songkla University, Thailand (Ethics number: EC 52-268-12-1-3).

Serum collection

Approximately 5 mL of venous blood samples were drawn and their sera were collected and kept at −20°C until further testing.

Screening for anti-Toxoplasma IgG and IgM antibodies

Anti-Toxoplasma IgG and IgM antibodies were screened by using a standard ELISA commercial kit (IgG-Trinity Biotech and IgM-Trinity Biotech, New York) in accordance with the manufacturer's instructions. A positive sample for the anti-Toxoplasma IgG and IgM antibodies was also tested for its avidity using a standard ELISA commercial kit (IgG-NovaLisa Dietzenbach, Germany); high avidity (>40%) indicated a past infection (of at least 4–5 months) and a low avidity (<40%) indicated a recently acquired infection (within 4–5 months).

Statistical analysis

Data obtained from both the questionnaire and laboratory tests were entered, edited, and analyzed using the statistical software SPSS version 17.0 (SPSS, Inc., Chicago, IL). The data with quantitative variables were expressed as the mean (±SD) and range, whereas qualitative variables were estimated and presented as frequencies and percentages. Univariate analyses and the 2 test were used to investigate the association between Toxoplasma seropositivity as a dependent variable and possible demographic and risk factors as independent variables; p < 0.05 was regarded as being statistically significant.

Results

A total of 760 pregnant women were recruited. Their age range was from 14 to 47 years with a mean of 29.5 ± 6.34 years. The majority of these women was between 26 and 35 years (408, 53.7%), had tertiary education (369, 48.6%) and worked as laborers (317, 41.7%). Most of these pregnant women were in their first trimester of pregnancy (621, 81.7%), had no history of receiving antibiotic treatment (664, 87.4%), have one or no child (637, 83.8%) and had no experience of miscarriage (592, 77.9%) as shown in Table 1.
Table 1

Socio-demographic, obstetric profiles and risk factors associated with Toxoplasma seropositivity in pregnant women by univariate analysis

Variable

No. of pregnant women

P-value

 

Total (n, %)

Toxoplasma seropositive (n, %)

 
 

N = 760

N = 190

 

Demographic profile

   

Age

  Range 14–47 years

   

  Mean 29.5 ± 6.34 years

   

Age group

  

0.042

  14–25

214 (28.2)

40 (18.7)

 

  26–35

408 (53.7)

112 (27.5)

 

  36-47

138 (18.2)

38 (27.5)

 

Education

  

0.311

  Primary

48 (6.3)

16 (33.3)

 

  Secondary

343 (45.1)

80 (23.3)

 

  Tertiary

369 (48.6)

94 (25.5)

 

Occupation

  

0.002

  Labourer

317 (41.7)

95 (29.9)

 

  Non-Labourer

275 (36.2)

69 (25.0)

 

  Unemployed

168 (22.1)

26 (15.5)

 

Obstetric history

   

Antibiotic usage

  

0.801

  No

664 (87.4)

167 (25.2)

 

  Yes

96 (12.6)

23 (23.9)

 

Trimester

   

  First

621 (81.7)

162 (26.1)

0.255

  Second

129 (17.0)

27 (20.9)

 

  Third

10 (1.3)

1 (10.0)

 

No. children

  

0.460

  ≤1

637 (83.8)

156 (24.5)

 

  ≥2

123 (16.2)

34 (27.6)

 

History of abortion

  

1.000

  No

592 (77.9)

148 (25.0)

 

  Yes

168 (22.1)

42 (25.0)

 

Awareness of toxoplasmosis

  

0.320

  No

708 (93.2)

180 (25.4)

 

  Yes

52 (6.8)

10 (19.2)

 

Risk factors of toxoplasmosis

   

Close contact with cats

  

0.258

  No

482 (63.4)

114 (23.7)

 

  Yes

278 (36.6)

76 (27.3)

 

Consumption of undercooked meat

  

0.408

  No

275 (36.2)

64 (23.3)

 

  Yes

485 (63.8)

126 (25.9)

 

Receiving blood transfusion

  

0.414

  No

758 (99.7)

190 (25.1)

 

  Yes

2 (0.26)

0 (0)

 

Drinking water from various source

  

0.013

  Boiled

75 (9.8)

24 (32.0)

 

  Mineral/Filtered

597 (78.6)

135 (22.6)

 

  Piped/tap/rain

88 (11.6)

31 (35.2)

 

Drinking milk

  

0.693

  No

97 (12.8)

27 (27.8)

 

  Boiled

8 (1.1)

3 (37.5)

 

  Pasteurized

649 (85.4)

158 (24.3)

 

  Non-Pasteurized

6 (0.8)

2 (33.3)

 

Having contact with soil

  

0.395

  No

316 (41.6)

74 (23.4)

 

  Yes

444 (58.4)

116 (26.1)

 

Close contact with other animals

  

0.967

  No

369 (48.6)

92 (24.9)

 

  Yes

391 (51.4)

98 (25.0)

 

Overall, the seroprevalence of Toxoplasma infection in our study was 190 (25.0%, 95% CI = 22.05-28.20) of which 167 (22.0%, 95% CI = 19.0-25.0) were positive for only anti-Toxoplasma IgG antibodies and 23 (3.0%, 95% CI = 2.0-4.0) were positive for both anti-Toxoplasma IgG and IgM antibodies. Serum samples positive for only anti-Toxoplasma IgM antibodies (19, 2.5%) were re-screened by collecting second serum samples after intervals of four weeks apart. These serum samples were later reported as false positive since there was no sero-conversion found.

The 23 samples that were seropositive for both anti-Toxoplasma IgG and IgM antibodies were subsequently assessed by IgG avidity test. All these samples showed high avidity, indicating they may have acquired the infection four to five months earlier. It was noted that 20 of these samples were in their first trimester and the remaining three were in their second trimester of pregnancy.

For univariate analysis, this study verified that age group, occupation and source of drinking water had significant associations with seropositive pregnant women (p < 0.05), as shown in Table 1. After the multivariate logistic regression analysis was performed, it was confirmed that age ≥26 (OR = 1.65, 95% CI = 1.11-2.44), working as a laborer (OR = 1.57, 95% CI = 1.13-2.18) and drinking unclean (piped/tap/rain) water (OR = 1.75, 95% CI = 1.08-2.84) were identified as significant risk factors for Toxoplasma acquisition, as shown in Table 2.
Table 2

Multivariate logistic regression analysis for demographic profiles and risk factors associated with Toxoplasma seropositive pregnant women

Variable

Adjusted odds ratio

95% CI

P value

Age ≥26

1.65

1.11

2.44

0.012

Working as labourer

1.57

1.13

2.18

0.007

Drinking Piped/tap/rain water

1.75

1.08

2.84

0.018

Adjusted variables include age group, occupation and source of drinking water in this statistical analysis.

Discussion

Toxoplasma infection in pregnant women shows variation in seroprevalence globally. From our findings, the overall seroprevalence of chronic Toxoplasma infection was 25% in the recruited Thai pregnant women. This finding fell within the range of 2.6% - 28% of seroprevalence that have been reported in Thailand [1018]. However, our prevalence rate is still higher compared to previous studies conducted recently in our Asian counterparts such as China, Japan and Taiwan being 3.98%, 10.3% and 11.8%, respectively [1921]. Globally, the seroprevalence of Toxoplasma infection remains high in many countries across the continents, e.g., 84.7% in Congo [22], 83.6% in Ethiopia [23], 45% in India [24], 59% in Brazil [25] and 30.9% in Tanzania [26]. The seroprevalence may vary in a global view, but the risk of this parasitic infection in human populations, especially in pregnant women, still holds a great interest. Our findings imply that we need to take a holistic approach to educate our pregnant women on toxoplasmosis in order to reduce the infection rate and the overall disease burden in our society.

In this study, 2.5% of pregnant women were false positive for anti-Toxoplasma IgM antibodies after re-screening their second serum sample collected four weeks later to test for seroconversion. This phenomenon could be due to host natural IgM antibodies reacting with Toxoplasma antigens without infection [1, 8]. Meanwhile, the pregnant women who were positive for both anti-Toxoplasma IgG and IgM antibodies have high IgG avidity, indication of past infection. The specified IgM antibodies may remain for several months or years after initial infection [7]. The majority of these pregnant women were in their first trimester of pregnancy. This is of great concern as the effect of Toxoplasma infection is more severe to the fetus during the first trimester of pregnancy [27]. In the incidence of positive for both anti-Toxoplasma IgG and IgM antibodies, possibilities of acute infection or false IgM positive results were predicted. IgG avidity measurement assists as a confirmatory tool in the determination of infection stages in the suspected pregnant women with the availability of a single serum sample [28]. A high avidity of IgG antibodies indicates that there is no risk for congenital toxoplasmosis in the fetus, especially for pregnant women in their first trimester, regardless of the IgM antibodies results [5].

Our epidemiological data showed that age ≥ 26 years, working as a laborer and drinking unclean water were significant factors associated with Toxoplasma infection. This could be generally explained that the seroprevalence of Toxoplasma infection increases by age [29] and also specifically by their low-socioeconomic and poor hygiene practice which can play as an important role in the transmission of the parasites [3032].

Pregnant women with more than one child have been shown a significant association with Toxoplasma infection [33] and this could be due to lack of cleanliness among their children [34]. However, no significant association was found between obstetric histories and Toxoplasma seropositivity in our study. Most of these pregnant women were not aware of toxoplasmosis and this could lead to high Toxoplasma seropositivity, as they do not know how to protect themselves from this parasitic infection [35, 36].

Concerning other plausible risk factors, some of our pregnant women had a history of close contacts with cats (37%) but had no significant association with Toxoplasma infection. This finding is, however, contrary to a few of the previous studies reported, where having close contact with felines was shown as one of the vital factors in transmission of Toxoplasma infection [37, 38]. Studies have also shown that Toxoplasma infection can be transmitted by other animals to their owners [3941]. Toxoplasma cysts infected animals’ tissues for human consumption is a mode of disease transmission [4244]. Most of our pregnant women had consumed undercooked meat but there is no significant association with high Toxoplasma infection. This could be due to absence of contamination by Toxoplasma cysts in the consumed meat and needs to be further studied. Our finding is consistent with a previous study reported in this region [11], showing that drinking unclean water (pipe/tap/rain) had significant association with Toxoplasma seropositive pregnant women, indicating the water may be contaminated with Toxoplasma oocysts. However, high seropositive (32%) were also found in pregnant women who consumed boiled water but were not statistically significant. Based on the above results, this could be a good indicator of other confounding factors contributing to Toxoplasma infection and requires further studies.

Conclusion

Our findings showed high Toxoplasma infection rates in this group of pregnant women and showed significantly higher risk with age group, low socioeconomic status and drinking unclean water. The following guidelines should be implemented to eliminate Toxoplasma infection and eventually eradicate its disease burden; Firstly, a routine screening for toxoplasmosis among women in the reproductive age group and pregnant women, especially for those in their early pregnancy is strongly encouraged for monitoring and preventive purposes. Secondly, health education on toxoplasmosis (brochures were attached as Additional file 1) and its risk exposures is required to increase the awareness about this disease and to minimize the effects of this Toxoplasma infection in the general population and pregnant women in particular. Lastly, serological diagnosis through the detection of anti-Toxoplasma antibodies and IgG avidity measurement in pregnant women assist the dating of the infection and as well as determining the decision for course of treatment especially those in their early pregnancies.

Declarations

Acknowledgments

We thank all the participating pregnant women for their consistent support and cooperation throughout this study. We also thank the doctors, nurses, and staffs of ANC at Songklanagarind Hospital, Hat Yai, Songkhla province, Thailand for their assistance and contribution in this study.

Funding

This study was supported by UM High Impact Research Grant UM-MOHE UM.C/625/1/HIR/MOHE/MED/18 from the Ministry of Higher Education Malaysia, and University of Malaya Research Grant (UMRG 488/12HTM and UMRG 544/14HTM).

Authors’ Affiliations

(1)
Department of Parasitology, Faculty of Medicine, University of Malaya
(2)
Department of Microbiology, Faculty of Science, Prince of Songkla University
(3)
Department of Obstetrics and Gynecology, Faculty of Medicine, Prince of Songkla University
(4)
Faculty of Medicine, University of Phayao

References

  1. Sensini A: Toxoplasma gondii infection in pregnancy: opportunities and pitfalls of serological diagnosis. Clin Microbiol Infect. 2006, 12: 504-512. 10.1111/j.1469-0691.2006.01444.x.View ArticlePubMedGoogle Scholar
  2. Cook AJ, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenum PA, Foulon W, Semprini AE, Dunn DT: Sources of toxoplasmosis infection in pregnant women: European multicentre case–control study. BMJ. 2000, 321: 142-147. 10.1136/bmj.321.7254.142.PubMed CentralView ArticlePubMedGoogle Scholar
  3. Singh S: Mother-to-child transmission and diagnosis of Toxoplasma gondii infection during pregnancy. Indian J Med Microbiol. 2003, 21: 69-76.PubMedGoogle Scholar
  4. Giannoulis C, Zournatzi B, Giomisi A, Diza E, Tzafettas I: Toxoplasmosis during pregnancy: case report and review of the literature. Hippokratia. 2008, 12: 139-143.PubMed CentralPubMedGoogle Scholar
  5. Montoya JG, Remington JS: Management of Toxoplasma gondii infection during pregnancy. Clin Infect Dis. 2008, 47: 554-566. 10.1086/590149.View ArticlePubMedGoogle Scholar
  6. Lopes FM, Gonçalves DD, Mitsuka-Breganó R, Freire RL, Navarro IT: Toxoplasma gondii infection in pregnancy. Braz J Infect Dis. 2007, 11: 496-506.PubMedGoogle Scholar
  7. Leite M, Siciliano S, Rocha LS, Justa MT, César KR, Granato CF: Correlation between specific IgM levels and percentage IgG-class antibody avidity to Toxoplasma gondii. Rev Inst Med Trop Sao Paulo. 2008, 50: 237-242.View ArticlePubMedGoogle Scholar
  8. Liesenfeld O, Press C, Montoya JG, Gill R, Isaac-Renton JL, Hedman K, Remington JS: False-positive results in immunoglobulin M (IgM) Toxoplasma antibody tests and importance of confirmatory testing: the Platelia Toxo IgM test. J Clin Microbiol. 1997, 35: 174-178.PubMed CentralPubMedGoogle Scholar
  9. Remington JS, Thulliez P, Montoya JG: Recent developments for diagnosis of toxoplasmosis. J Clin Microbiol. 2004, 42: 941-945. 10.1128/JCM.42.3.941-945.2004.PubMed CentralView ArticlePubMedGoogle Scholar
  10. Nissapatorn V, Suwanrath C, Sawangjaroen N, Ling LY, Chandeying V: Toxoplasmosis-serological evidence and associated risk factors among pregnant women in southern Thailand. Am J Trop Med Hyg. 2011, 85: 243-247. 10.4269/ajtmh.2011.10-0633.PubMed CentralView ArticlePubMedGoogle Scholar
  11. Sakae C, Natphopsuk S, Settheetham-Ishida W, Ishida T: Low prevalence of Toxoplasma gondii infection among women in northeastern Thailand. J Parasitol. 2013, 99: 172-173. 10.1645/GE-3222.1.View ArticlePubMedGoogle Scholar
  12. Sukthana Y: Difference of Toxoplasma gondii antibodies between Thai and Austrian pregnant women. Southeast Asian J Trop Med Public Health. 1999, 30: 38-41.PubMedGoogle Scholar
  13. Chintana T: Pattern of antibodies in toxoplasmosis of pregnant women and their children in Thailand. Southeast Asian J Trop Med Public Health. 1991, 22 (Suppl): 107-110.PubMedGoogle Scholar
  14. Puthavathana P, Pimolpan K, Louisirirotchanakul S, Wasi C, Thongcharoen P: Sero-epidemiology of TORCH agents among pregnant Thais. Asian Pac J Allergy Immunol. 1983, 1: 11-14.PubMedGoogle Scholar
  15. Wanachiwanawin D, Sutthent R, Chokephaibulkit K, Mahakittikun V, Ongrotchanakun J, Monkong N: Toxoplasma gondii antibodies in HIV and non-HIV infected Thai pregnant women. Asian Pac J Allergy Immunol. 2001, 19: 291-293.PubMedGoogle Scholar
  16. Maleewong W, Lulitanond V, Pipitgool V, Auwijitaroon Y, Kuttsarejariya S, Morakote N: Prevalence of Toxoplasma antibodies in blood donors and pregnant women in Khon Kaen Province. J Med Assoc Thai. 1989, 72: 256-259.PubMedGoogle Scholar
  17. Chintana T, Sukthana Y, Bunyakai B, Lekkla A: Toxoplasma gondii antibody in pregnant women with and without HIV infection. Southeast Asian J Trop Med Public Health. 1998, 29: 383-386.PubMedGoogle Scholar
  18. Sukthana Y, Chintana T, Supatanapong W, Siripan C, Lekkla A, Cheabchalrad R: Predictive value of latex agglutination test in serological screening for Toxoplasma gondii. Southeast Asian J Trop Med Public Health. 2001, 32: 314-318.PubMedGoogle Scholar
  19. Hua HY, Tang F, Liu YX, You L, Dong MH, Chen YE, Chen H, Hu YH, Ding GS, Sun BC, Guo JH, Gao Q: Survey of Toxoplasma gondii infection among pregnant women in Jiangsu Province, China. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi. 2013, 25: 56-58.PubMedGoogle Scholar
  20. Sakikawa M, Noda S, Hanaoka M, Nakayama H, Hojo S, Kakinoki S, Nakata M, Yasuda T, Ikenoue T, Kojima T: Anti-Toxoplasma antibody prevalence, primary infection rate, and risk factors in a study of toxoplasmosis in 4,466 pregnant women in Japan. Clin Vaccine Immunol. 2012, 19: 365-367. 10.1128/CVI.05486-11.PubMed CentralView ArticlePubMedGoogle Scholar
  21. Chou CS, Lin LY, Chen KM, Lai SC: Flowcytomix analysis for Toxoplasma gondii infection in pregnant women in central Taiwan. J Obstet Gynaecol. 2011, 31: 375-379. 10.3109/01443615.2011.568073.View ArticlePubMedGoogle Scholar
  22. Doudou Y, Renaud P, Coralie L, Jacqueline F, Hypolite S, Hypolite M, Patrick M, Andreia Ida L, Van Sprundel M, Marleen B, Van Geertruyden JP, Pascal L: Toxoplasmosis among pregnant women: high seroprevalence and risk factors in Kinshasa, Democratic Republic of Congo. Asian Pac J Trop Biomed. 2014, 4: 69-74. 10.1016/S2221-1691(14)60211-2.View ArticlePubMedGoogle Scholar
  23. Zemene E, Yewhalaw D, Abera S, Belay T, Samuel A, Zeynudin A: Seroprevalence of Toxoplasma gondii and associated risk factors among pregnant women in Jimma town, Southwestern Ethiopia. BMC Infect Dis. 2012, 12: 337-10.1186/1471-2334-12-337.PubMed CentralView ArticlePubMedGoogle Scholar
  24. Singh S, Pandit AJ: Incidence and prevalence of toxoplasmosis in Indian pregnant women: a prospective study. Am J Reprod Immunol. 2004, 52: 276-283. 10.1111/j.1600-0897.2004.00222.x.View ArticlePubMedGoogle Scholar
  25. Ferezin RI, Bertolini DA, Demarchi IG: Prevalence of positive serology for HIV, hepatitis B, toxoplasmosis and rubella in pregnant women from the northwestern region of the state of Paraná. Rev Bras Ginecol Obstet. 2013, 35: 66-70. 10.1590/S0100-72032013000200005.View ArticlePubMedGoogle Scholar
  26. Mwambe B, Mshana SE, Kidenya BR, Massinde AN, Maziqo HD, Micheal D, Majinge C, Groß U: Sero-prevalence and factors associated with Toxoplasma gondii infection among pregnant women attending antenatal care in Mwanza, Tanzania. Parasit Vectors. 2013, 6: 222-10.1186/1756-3305-6-222.PubMed CentralView ArticlePubMedGoogle Scholar
  27. Kieffer F, Wallon M: Congenital toxoplasmosis. Handb Clin Neurol. 2013, 112: 1099-1101.View ArticlePubMedGoogle Scholar
  28. Ashburn D, Joss AW, Pennington TH, Ho-Yen DO: Do IgA, IgE and IgG avidity tests have any value in the diagnosis of Toxoplasma infection in pregnancy?. J Clin Pathol. 1998, 51: 312-315. 10.1136/jcp.51.4.312.PubMed CentralView ArticlePubMedGoogle Scholar
  29. Nowakowska D, Wujcicka W, Sobala W, Spiewak E, Gaj Z, Wilczynski J: Age associated prevalence of Toxoplasma gondii in 8281 pregnant women in Poland between 2004 and 2012. Epidemiol Infect. 2014, 142: 656-661. 10.1017/S0950268813001179.View ArticlePubMedGoogle Scholar
  30. Alvarado-Esquivel C, Torres-Castorena A, Liesenfeld O, Estrada-Martinez S, Urbina-Álvarez JD: High seroprevalence of Toxoplasma gondii infection in a subset of Mexican patients with work accidents and low socioeconomic status. Parasit Vectors. 2012, 5: 13-10.1186/1756-3305-5-13.PubMed CentralView ArticlePubMedGoogle Scholar
  31. Dattoli VC, Veiga RV, Cunha SS, Pontes-de-Carvalho L, Barreto ML, Alcantara-Neves NM: Oocyst ingestion as an important transmission route of Toxoplasma gondii in Brazilian urban children. J Parasitol. 2011, 97: 1080-1084. 10.1645/GE-2836.1.View ArticlePubMedGoogle Scholar
  32. Francisco Fde M, De Souza SL, Gennari SM, Pinheiro SR, Muradian V, Soares RM: Seroprevalence of toxoplasmosis in a low-income community in the Sao Paulo municipality, SP, Brazil. Rev Inst Med Trop Sao Paulo. 2006, 48: 167-170.PubMedGoogle Scholar
  33. Jenum PA, Kapperud G, Stray-Pedersen B, Melby KK, Eskild A, Eng J: Prevalence of Toxoplasma gondii specific immunoglobulin G antibodies among pregnant women in Norway. Epidemiol Infect. 1998, 120: 87-92. 10.1017/S0950268897008480.PubMed CentralView ArticlePubMedGoogle Scholar
  34. Mohan B, Dubey ML, Malla N, Kumar R: Seroepidemiological study of toxoplasmosis in different sections of population of Union Territory of Chandigarh. J Commun Dis. 2002, 34: 15-22.PubMedGoogle Scholar
  35. Ferguson W, Mayne PD, Cafferkey M, Butler K: Lack of awareness of risk factors for primary toxoplamosis in pregnancy. Ir J Med Sci. 2011, 180: 807-811. 10.1007/s11845-011-0723-3.View ArticlePubMedGoogle Scholar
  36. Pappas G, Roussos N, Falagas ME: Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplamosis. Int J Parasitol. 2009, 39: 1385-1394. 10.1016/j.ijpara.2009.04.003.View ArticlePubMedGoogle Scholar
  37. Gebremedhin EZ, Abede AH, Tessema TS, Tullu KD, Medhin G, Vitale M, Di Marco V, Cox E, Dorny P: Seroepidemiology of Toxoplasma gondii infection in women of child-bearing age in central Ethiopia. BMC Infect Dis. 2013, 13: 101-10.1186/1471-2334-13-101.PubMed CentralView ArticlePubMedGoogle Scholar
  38. Ngui R, Lim YA, Amir NF, Nissapatorn V, Mahmud R: Seroprevalence and sources of toxoplasmosis among Orang Asli (indigenous) communities in Peninsular Malaysia. Am J Trop Med Hyg. 2011, 85: 660-666. 10.4269/ajtmh.2011.11-0058.PubMed CentralView ArticlePubMedGoogle Scholar
  39. Yang N, Mu M, Li H, Hu J, Gao W, Yang S, He J: Seroprevalence of Toxoplasma gondii infection in pet dogs in Shenyang, northeastern China. J Parasitol. 2013, 99: 176-177. 10.1645/GE-3211.1.View ArticlePubMedGoogle Scholar
  40. Hemsworth S, Pizer B: Pet ownership in immunocompromised children- a review of the literature and survey of existing guidelines. Eur J Oncol Nurs. 2006, 10: 117-127. 10.1016/j.ejon.2005.08.001.View ArticlePubMedGoogle Scholar
  41. Schurer JM, Hill JE, Fernando C, Jenkins EJ: Sentinel surveillance for zoonotic parasites in companion animals in indigenous communities of Saskatchewan. Am J Trop Med Hyg. 2012, 87: 495-498. 10.4269/ajtmh.2012.12-0273.PubMed CentralView ArticlePubMedGoogle Scholar
  42. Hill DE, Dubey JP: Toxoplasma gondii prevalence in farm animals in the United States. Int J Parasitol. 2013, 42: 107-113.View ArticleGoogle Scholar
  43. Kang SW, Doan HT, Noh JH, Choe SE, Yoo MS, Kim YH, Reddy KE, Nguyen TT, Van Quyen D, Nguyen LT, Kweon CH, Jung SC: Seroprevalence of Toxoplasma gondii and Trichinella spiralis infections in wild boars (Sus scrofa). Parasitol Int. 2013, 62: 583-585. 10.1016/j.parint.2013.08.015.View ArticlePubMedGoogle Scholar
  44. Wang L, Cheng HW, Huang KQ, Xu YH, Li YN, Du J, Yu L, Luo QL, Wei W, Jiang L, Shen JL: Toxoplasma gondii prevalence in food animals and rodents in different regions of China: isolation genotyping and mouse pathogenicity. Parasit Vectors. 2013, 6: 273-10.1186/1756-3305-6-273.PubMed CentralView ArticlePubMedGoogle Scholar

Copyright

© Andiappan et al.; licensee BioMed Central Ltd. 2014

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Advertisement