Skip to main content
Download PDF

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

Parasites & Vectors volume 7, Article number: 239 (2014) Cite this article

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.

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
Full size table

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
Full size table

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 [10–18]. 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 [19–21]. 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 [30–32].

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 [39–41]. Toxoplasma cysts infected animals’ tissues for human consumption is a mode of disease transmission [42–44]. 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.

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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Singh S: Mother-to-child transmission and diagnosis of Toxoplasma gondii infection during pregnancy. Indian J Med Microbiol. 2003, 21: 69-76.

    CAS  PubMed  Google 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 Central  CAS  PubMed  Google Scholar 

  5. Montoya JG, Remington JS: Management of Toxoplasma gondii infection during pregnancy. Clin Infect Dis. 2008, 47: 554-566. 10.1086/590149.

    Article  PubMed  Google 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.

    PubMed  Google 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.

    Article  PubMed  Google 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 Central  CAS  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    PubMed  Google 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.

    Article  PubMed Central  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Kieffer F, Wallon M: Congenital toxoplasmosis. Handb Clin Neurol. 2013, 112: 1099-1101.

    Article  PubMed  Google 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.

    Article  PubMed Central  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    PubMed  Google 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.

    Article  PubMed Central  CAS  PubMed  Google 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.

    PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google Scholar 

  42. Hill DE, Dubey JP: Toxoplasma gondii prevalence in farm animals in the United States. Int J Parasitol. 2013, 42: 107-113.

    Article  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, 50603, Malaysia

    Hemah Andiappan, Veeranoot Nissapatorn, Yee Ling Lau, Thulasi Kumar & Subashini Onichandran

  2. Department of Microbiology, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, 90112, Thailand

    Nongyao Sawangjaroen & Waenurama Chemoh

  3. Department of Obstetrics and Gynecology, Faculty of Medicine, Prince of Songkla University, Hat Yai, Songkhla, 90112, Thailand

    Chitkasaem Suwanrath & Verapol Chandeying

  4. Faculty of Medicine, University of Phayao, Phayao, 56000, Thailand

    Verapol Chandeying

Authors
  1. Hemah Andiappan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Veeranoot Nissapatorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nongyao Sawangjaroen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Waenurama Chemoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yee Ling Lau
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thulasi Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Subashini Onichandran
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chitkasaem Suwanrath
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Verapol Chandeying
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Veeranoot Nissapatorn.

Additional information

Competing interest

All authors declare having no conflicts of interest.

Authors’ contributions

All authors were involved in the design of the study. VN was the principal investigator. VN and NS drafted the protocol, consent forms, and paper with input from the other authors. HA, TK, SO and WC were responsible for sample collection, serological analysis and data analysis. HA and WC were responsible for statistical analysis and interpretation. LYL, NS, CS, VC and VN were involved in data analysis, statistical analysis and interpretation and results discussion and inputs. All authors contributed to the writing of the paper and approved the final version.

Electronic supplementary material

13071_2014_1422_MOESM1_ESM.doc

Additional file 1: Health care education on Toxoplasmosis in pregnant women. Brochures in English Language. Brochures in Thai language. (DOC 2 MB)

Authors’ original submitted files for images

Below are the links to the authors’ original submitted files for images.

Authors’ original file for figure 1

Rights and permissions

Open Access  This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.

The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/.

The Creative Commons Public Domain Dedication waiver (https://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andiappan, H., Nissapatorn, V., Sawangjaroen, N. et al. Toxoplasma infection in pregnant women: a current status in Songklanagarind hospital, southern Thailand. Parasites Vectors 7, 239 (2014). https://0-doi-org.brum.beds.ac.uk/10.1186/1756-3305-7-239

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://0-doi-org.brum.beds.ac.uk/10.1186/1756-3305-7-239

Keywords

Parasites & Vectors

ISSN: 1756-3305

Contact us