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Prevalence and risk factors profile of seropositive Toxoplasmosis gondii infection among apparently immunocompetent Sudanese women

BMC Research Notes volume 12, Article number: 279 (2019) Cite this article

Abstract

Objectives

Toxoplasma gondii is an opportunistic parasite that causes a clinical manifestation known as toxoplasmosis. We investigated the prevalence and potential risk factors of T. gondii infection among women in Khartoum, Sudan. A sero-parasitological cross-sectional study included 100 women aging between 15 and 50 years old was conducted between January and November 2018. Serum samples were collected and investigated for the presence of anti-T. gondii immunoglobulins.

Results

Mean age of the women population included was 26.75 ± 8.25 with a range between 15 and 50 years. Sero-prevalence of T. gondii antibodies was 27% (27/100) with a 95% confidence interval (CI) of 18.6–36.8%. Among seropositive population 81% (22/27), 15% (4/27) and 4% (1/27) were seropositive for IgG antibodies, IgM antibodies and both antibodies respectively. Age group 21–30 years old had the highest frequency of detected IgG (10/45) and IgM (3/45). Married women had the highest frequency of detected IgG or IgM, 18/79 and 3/79, respectively. Risk factors analysis showed a total of 37/100 participants were having direct contact with cats and 66/100 have a frequent raw meat consumption, neither direct cats contact nor raw meat consumption had a statistically significant association with seropositivity to T. gondii (P value = 0.052 and 0.565, respectively).

Introduction

Toxoplasmosis is an opportunistic parasitic infection caused by the parasite Toxoplasma gondii. Toxoplasmosis constitutes a major public health problem especially in low- and middle-income countries (LMICs) [1]. More than 29% of people worldwide show serological evidence of encountering T. gondii infection [2]. Though T. gondii parasite stays in a dormant stage called bradyzoites [3], the parasite transforms into an active form when the immune system becomes compromised which leads to the clinical manifestation that known as toxoplasmosis [4]. Decreased immunity could be attributed to infections such as HIV [5, 6], disease e.g. fatty liver disease [7], or normal alterations in physiological response as in case of pregnancy [8,9,10,11].

Congenital toxoplasmosis is another form of toxoplasmosis defined by the vertical transmission T. gondii tachyzoites parasite from an infected pregnant woman to a fetus through the placenta [12]. Congenital toxoplasmosis occurs approximately in 1 per 1000 pregnant women [13, 14]. It can cause severe damages to the fetus brain, cerebral calcification, hydrocephaly, chorioretinitis, and mental retardation [15]. Some patients with congenital toxoplasmosis are likely to develop other clinical manifestations like toxoplasma encephalitis [16], lymphadenopathy [17], schizophrenia [18], ophthalmitis [19], and organ dysfunction such as liver cirrhosis [20].

In Sudan, toxoplasmosis was firstly reported in 1966 in 61% patients in Darfur state [21] In 1991 it was reported that high prevalence rate in Sudan is due to some habits like consumption of raw or partially cooked liver, viscera and meat [22]. In 2013, an overall seroprevalence of 43.6% has been reported in samples donated for the central blood bank and samples investigated to issue travel cards. Higher prevalence of the disease was reported in HIV patients (75%) and women with abortion history (55.5%) in Khartoum state [23].

Early diagnosis of toxoplasmosis especially among females in childbearing age is recommended since the disease can cause miscarriage, stillbirth or congenital toxoplasmosis to their infants [24] when they get pregnant. Therefore, pre-diagnosis even with a first line detection method especially in the LMICs such as Sudan will help in the management of pregnant females with T. gondii infection. This study aimed at investigating the prevalence of T. gondii among Sudanese women in Khartoum state, Sudan and identification of risk factors associated with seropositive candidates.

Main text

Materials and methods

A sero-parasitological cross-sectional study was conducted in Sharq El-Nile hospital, Khartoum, Sudan between January and November 2018. The study included a total number of 100 females age 15 to 45 years. Patients subjected to immunosuppressive factors (pregnant women, transplant, HIV patients and other immunosuppressed) were excluded from the study. Sample collection was linked with a questionnaire guided interview. The confidentiality and anonymity of the participants were maintained throughout the research steps. Demographic information included age, educational level, marital status, occupation, and family size were collected. Other expected risk factors like contact with felines, consumption of raw meat or unwashed vegetables, drinking of unpasteurized milk, sources of drinking water, rearing of rabbits and previous history of spontaneous abortion were considered as well.

Samples collection

Two ml blood samples were collected in plain vacutainers after obtaining informed consent from human subjects included in the study. Samples were then transported to the molecular biology lab of the National University Biomedical Research Institute—National University, Sudan. Samples were then left on the bench for 30 min at room temperature to allow blood clotting and serum separation. Serum samples were then transferred into new plain labeled containers and stored at − 20 °C till further processing.

Serological diagnosis of toxoplasmosis

A total of 100 serum samples were serologically tested for IgM and IgG against T. gondii antigens. The sera were subjected to Toxoplasma-specific rapid diagnostic testing (RDT), according to the manufacturer’s instructions (Biopanda Reagents, Belfast, UK). Briefly, 20 µl serum were added to the pore in the cellulose strip of the test device and then allowed to migrate through the whole strip. Results were positive when obtaining two or three lines of reaction, one for the control showing the validity of the test device and the second one for the positive serum sample. Three lines were obtained when both IgM and IgG detected in addition to the control line. In order to obtain a valid test result, samples were run in triplicates.

RDT seropositive samples were subjected to latex indirect agglutination test card in accordance with the manufacturer’s instructions (Rapid Labs, United Kingdom). Briefly, 20 µl serum sample was placed on the test spot next to the controls’ spots; positive and negative controls. 3 drops of the antigen provided with the test kits were added and mixed slowly with the serum followed by 15 min incubation at room temperature. Direct agglutination confirmatory tests were done in duplicates before tabulation of the results.

Statistical analysis

Statistical analysis was performed using the statistical package for social sciences (SPSS version 20). Demographic data were categorized and means were compared using the student T test. Chi square test was used to test the significance of risk factors associated with seropositive patients; results considered to be statistically significant if P value < 0.05.

Results

Study population characteristics

Our study population consisted of 100 women aged 15 to 50 years (mean age 26.75 ± 8.25 years). Participants were grouped according to their ages into 4 groups; 15–20, 21–30, 31–40, and 41–50 years. Most of the participants (45%) were in the 21–30 years age group. Information about participants residence, marital status, water source and contact with cats is in Table 1.

Table 1 Characteristics of the study participants
Full size table

Serological detection of T. gondii infection

The overall prevalence of T. gondii infection in the study population was (27%, 95% confidence interval [CI] 18.6–36.8%) (Table 2). Results of detection were further classified based on the type of immunoglobulins present in the serum. T. gondii-specific IgG and IgM antibodies were detected in 22 (22%) and 4 (4%) of the seropositive participants respectively. Only one serum sample was positive for both IgG and IgM anti-T. gondii antibodies. Women aged 21–30 years had the highest frequency of detected IgG and IgM; 10/45 (22.2%) and 3/45 (6.7%), respectively (Table 2). When analyzing the immunoglobulins results based on the marital status of the participated women, married women had the highest frequency of detected IgG or IgM, 18/79 (22.8%) and 3/79 (3.8%) respectively. Similarly, the single woman, 1/79 (1.3%), concurrently seropositive for both IgG and IgM was married. Five of the 22 married women with positive serology for anti-T. gondii IgG and/or IgM antibodies also have a history of spontaneous abortion. However, most married women (72.1%) were negative for the presence of anti-T. gondii immunoglobulins (Table 2).

Table 2 Results of serological diagnosis among the study participants
Full size table

Risk factors analysis

A total of 37 (37%) participants were having direct contact with cats and 66 (66%) reported frequent raw meat consumption. However, neither direct cats contact nor raw meat consumption had a statistically significant association with seropositivity to T. gondii (P value = 0.052 and 0.565, respectively). Other factors related to the risk of having T. gondii infection including consumption of unwashed vegetables, drinking of unpasteurized milk, owing of rabbits and, the source of drinking water was described in Table 3.

Table 3 Risk factors analysis with the prevalence of toxoplasmosis among the seropositive participants
Full size table

Six (22.2%) seropositive women had a previous history of abortion. Four of those participants positive for T. gondii IgG and one positive for T. gondii IgM had a history of two episodes of abortion while one woman who was seropositive for both IgM and IgG immunoglobulins had one previous abortion. Analysis of risk factors of having toxoplasmosis and its relation to the frequency of abortion is found in Additional file 1.

Discussion

This study showed 27% seroprevalence of anti-T. gondii antibodies among Sudanese women in Khartoum. This finding was lower than the seroprevalence of toxoplasmosis reported by Khalil et al. in which 45% of the sampled population had serological evidence of T. gondii infection [25]. Also, our result was lower than those reported in different countries as Ghana [26], Cameroon [27] and Ethiopia [28,29,30,31,32,33]. However, this seroprevalence of T. gondii antibodies was higher than that reported in European, North and West American continents [9, 34]. Such variations could be due to different study settings in terms of multiple climatic conditions, heterogeneous study population and risk factors profile such as contact with pets, hygienic practice, and feeding habit [28, 29, 31, 35, 36]. The result of those who aged 21–30 years having the highest frequency of T. gondii infection (28.9%) was similar to previous reports [28, 29, 36] with the exception of one study conducted in Burkina Faso that showed these who aged more than 30 years were the most infected age group [35].

The results of risk factors associated with toxoplasmosis including direct contact with cats, consumption of raw meat, consumption of unwashed vegetables, drinking of unpasteurized milk, owing rabbits at home, and source of drinking water were statistically insignificant (P values = 0.052, 0.565, 0.540, 0.706, 0.483 and 0.413, respectively). It is worth noting the tendency of association between seropositivity and direct contact with cats. Although, its noted that direct contact or owing a cat can act as a risk factor for toxoplasmosis [37]. While others reported the role of direct contact instead of owing a cat is highly significant [38]. In general, these study results were similar to other reports in which no significant association between these risk factors and having anti-T. gondii immunoglobulins [35, 39] and in contrast to previous reports that showed consumption of raw meat was significantly associated with toxoplasmosis infection [35, 40].

In this study, the history of two spontaneous abortion was statistically significant with having seropositive anti-T. gondii immunoglobulins (P value 0.038). This result was higher compared to previous studies conducted among women with history of miscarriage in Mexico [40], but similar to spontaneous abortion rate in seropositive women for T. gondii infection reported in Pakistan (17%) [41], and lower than other studies done in Egypt [42], Iran [43], and India [44]. When we linked the frequency of abortion to the presence of direct contact with cats, which was considered as a risk factor for having toxoplasmosis, the relationship was statistically significant (P value = 0.031), similar to an association reported in Zambia [36].

Conclusion

Toxoplasmosis is an opportunistic parasitic infection; apparently immunocompetent women can contract the infection with not a low rate. All women in childbearing age should be tested for T. gondii especially when they are planning to get pregnant to avoid the infection and its sequelae.

Limitations

  • Although the studied sample size is very small, it provides an insight into the situation of toxoplasmosis among Sudanese women. Therefore, a large-scale study with large sample size is required to provide accurate prevalence of this infection.

  • The ting of significance reported in this study cannot be generalized, but can be used as a pre-epidemiological data on the situation of toxoplasmosis in Sudan.

  • Presence of the toxoplasmosis infection and miscarriage among women still unknown whether the exposure occurred before or after pregnancy, therefore, examining detection of infection before and after pregnancy and at different time intervals following pregnancy duration would significantly improve future studies.

  • An accurate estimation for the toxoplasma antibodies in women serum is required in order to investigate active and past infections which can provide good follow up during pregnancy.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. World Health Organization. WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference grou. Geneva: World Health Organization; 2015. p. 2007–15.

    Google Scholar 

  2. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet. 2004;363:1965–76 (1474–547X Electronic).

    Article  CAS  Google Scholar 

  3. Sullivan WJ Jr, Jeffers V. Mechanisms of Toxoplasma gondii persistence and latency. Federat Eur Microbiol Soc. 2012;36:717–33 (1574–6976 Electronic).

    CAS  Google Scholar 

  4. Dubey JP, Beattie C. Toxoplasmosis of animals and man. New York: CRC Press, Inc.; 1988.

    Google Scholar 

  5. Pereira-Chioccola VL, Vidal JE, Su C. Toxoplasma gondii infection and cerebral toxoplasmosis in HIV-infected patients. Future Microbiol. 2009;4(10):1363–79.

    Article  Google Scholar 

  6. Dupouy-Camet J, De Souza SL, Maslo C, Paugam A, Saimot A, Benarous R, et al. Detection of Toxoplasma gondii in venous blood from AIDS patients by polymerase chain reaction. J Clin Microbiol. 1993;31(7):1866–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Cong W, Elsheikha HM, Zhou N, Peng P, Qin SY, Meng QF, et al. Prevalence of antibodies against Toxoplasma gondii in pets and their owners in Shandong province, Eastern China. BMC Infect Dis. 2018;18:430 (1471–2334 (Electronic)).

    Article  Google Scholar 

  8. Cong W, Dong X-Y, Meng Q-F, Zhou N, Wang X-Y, Huang S-Y, et al. Toxoplasma gondii infection in pregnant women: a seroprevalence and case–control study in Eastern China. Biomed Res Int. 2015;2015:17028.

    Article  Google Scholar 

  9. 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(12):1385–94.

    Article  Google Scholar 

  10. Jenum PA, Stray-Pedersen B, Melby KK, Kapperud G, Whitelaw A, Eskild A, et al. Incidence of Toxoplasma gondii infection in 35,940 pregnant women in Norway and pregnancy outcome for infected women. J Clin Microbiol. 1998;36(10):2900–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Ertug S, Okyay P, Turkmen M, Yuksel H. Seroprevalence and risk factors for Toxoplasma infection among pregnant women in Aydin province, Turkey. BMC Public heAlth. 2005;5(1):66.

    Article  Google Scholar 

  12. McAuley JB. Congenital toxoplasmosis. J Pediatr Infect Dis Soc. 2014;3(suppl_1):S30–5.

    Article  Google Scholar 

  13. Cook A, Holliman R, Gilbert R, Buffolano W, Zufferey J, Petersen E, et al. Sources of toxoplasma infection in pregnant women: European multicentre case-control study. Commentary: congenital toxoplasmosis—further thought for food. BMJ. 2000;321(7254):142–7.

    Article  CAS  Google Scholar 

  14. Vasconcelos-Santos DV, Azevedo DOM, Campos WR, Oréfice F, Queiroz-Andrade GM, Carellos ÉVM, et al. Congenital toxoplasmosis in southeastern Brazil: results of early ophthalmologic examination of a large cohort of neonates. Ophthalmology. 2009;116(11):2199–205.

    Article  Google Scholar 

  15. Koppe J, Loewer-Sieger D, de Roever-Bonnet H. Results of 20-year follow-up of congenital toxoplasmosis. Lancet. 1986;327(8475):254–6.

    Article  Google Scholar 

  16. Luma HN, Tchaleu BCN, Mapoure YN, Temfack E, Doualla MS, Halle MP, et al. Toxoplasma encephalitis in HIV/AIDS patients admitted to the Douala general hospital between 2004 and 2009: a cross sectional study. BMC Res Notes. 2013;6(1):146.

    Article  Google Scholar 

  17. McCabe RE, Brooks RG, Dorfman RF, Remington JS. Clinical spectrum in 107 cases of toxoplasmic lymphadenopathy. Rev Infect Dis. 1987;9(4):754–74.

    Article  CAS  Google Scholar 

  18. Hamidinejat H, Ghorbanpoor M, Hosseini H, Alavi SM, Nabavi L, Jalali MHR, et al. Toxoplasma gondii infection in first-episode and inpatient individuals with schizophrenia. Int J Infect Dis. 2010;14(11):e978–81.

    Article  Google Scholar 

  19. Bosch-Driessen LE, Berendschot TT, Ongkosuwito JV, Rothova A. Ocular toxoplasmosis: clinical features and prognosis of 154 patients. Ophthalmology. 2002;109(5):869–78.

    Article  Google Scholar 

  20. El-Henawy AAE-R, Abdel-Razik A, Zakaria S, Elhammady D, Saudy N, Azab MS. Is toxoplasmosis a potential risk factor for liver cirrhosis? Asian Pac J Trop Med. 2015;8(10):784–91.

    Article  Google Scholar 

  21. Carter F, Fleck D. The incidence of Toxoplasma antibodies in the Sudanese. Trans R Soc Trop Med Hyg. 1966;60(4):539–43.

    Article  CAS  Google Scholar 

  22. El-Hassan AM, Eltoum IA, El-Asha BM. The Marrara syndrome: isolation of Linguatula serrata nymphs from a patient and the viscera of goats. Trans R Soc Trop Med Hyg. 1991;85(2):309.

    Article  CAS  Google Scholar 

  23. Abdel-Raouff M, Elbasheir MM. Sero-prevalence of Toxoplasma gondii infection among pregnant women attending antenatal clinics in Khartoum and Omdurman Maternity Hospitals, Sudan. J Coastal Life Med. 2014;2(6):496–9.

    Google Scholar 

  24. Fallahi S, Rostami A, Shiadeh MN, Behniafar H, Paktinat S. An updated literature review on maternal-fetal and reproductive disorders of Toxoplasma gondii infection. J Gynecol Obstetr Hum Reprod. 2018;47(3):133–40.

    Article  CAS  Google Scholar 

  25. Khalil M, Ahmed A, Elrayah I. Prevalence and Risk factors for Toxoplasma gondii infection in Humans from Khartoum State, Sudan. Int J Public Health Epidemiol. 2013;2(3):60–6.

    Google Scholar 

  26. Ayi I, Edu S, Apea-Kubi K, Boamah D, Bosompem K, Edoh D. Sero-epidemiology of toxoplasmosis amongst pregnant women in the greater Accra region of Ghana. Ghana Med J. 2009;43(3):107–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Wam EC, Sama LF, Ali IM, Ebile WA, Aghangu LA, Tume CB. Seroprevalence of Toxoplasma gondii IgG and IgM antibodies and associated risk factors in women of child-bearing age in Njinikom, NW Cameroon. BMC Res Notes. 2016;9(1):406.

    Article  Google Scholar 

  28. 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(1):337.

    Article  Google Scholar 

  29. Abamecha F, Awel H. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women following antenatal care at Mizan Aman General Hospital, Bench Maji Zone (BMZ), Ethiopia. BMC Infect Dis. 2016;16(1):460.

    Article  Google Scholar 

  30. Gelaye W, Kebede T, Hailu A. High prevalence of anti-toxoplasma antibodies and absence of Toxoplasma gondii infection risk factors among pregnant women attending routine antenatal care in two Hospitals of Addis Ababa, Ethiopia. Int J Infect Dis. 2015;34:41–5.

    Article  Google Scholar 

  31. Agmas B, Tesfaye R, Koye DN. Seroprevalence of Toxoplasma gondii infection and associated risk factors among pregnant women in Debre Tabor, Northwest Ethiopia. BMC Res Notes. 2015;8(1):107.

    Article  Google Scholar 

  32. Shimelis T, Tebeje M, Tadesse E, Tegbaru B, Terefe A. Sero-prevalence of latent Toxoplasma gondii infection among HIV-infected and HIV-uninfected people in Addis Ababa, Ethiopia: a comparative cross-sectional study. BMC Res Notes. 2009;2(1):213.

    Article  Google Scholar 

  33. Zeleke AJ, Melsew YA. Seroprevalence of Toxoplasma gondii and associated risk factors among HIV-infected women within reproductive age group at Mizan Aman General Hospital, Southwest Ethiopia: a cross sectional study. BMC Res Notes. 2017;10(1):70.

    Article  Google Scholar 

  34. Ferreira MN, Bonini-Domingos CR, Estevão I, Lobo CLC, Carrocini GC, Silveira-Carvalho AP, et al. Anti-Toxoplasma gondii antibodies in patients with beta-hemoglobinopathies: the first report in the Americas. BMC Res Notes. 2017;10(1):211.

    Article  Google Scholar 

  35. Bamba S, Cissé M, Sangaré I, Zida A, Ouattara S, Guiguemdé RT. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women from Bobo Dioulasso, Burkina Faso. BMC Infect Dis. 2017;17(1):482.

    Article  Google Scholar 

  36. Frimpong C, Makasa M, Sitali L, Michelo C. Seroprevalence and determinants of toxoplasmosis in pregnant women attending antenatal clinic at the university teaching hospital, Lusaka, Zambia. BMC Infect Dis. 2017;17(1):10.

    Article  Google Scholar 

  37. Vittecoq M, Lafferty KD, Elguero E, Brodeur J, Gauthier-Clerc M, Missé D, et al. Cat ownership is neither a strong predictor of Toxoplasma gondii infection nor a risk factor for brain cancer. Biol Let. 2012;8(6):1042.

    Article  Google Scholar 

  38. Wei H-X, He C, Yang P-L, Lindsay DS, Peng H-J. Relationship between cat contact and infection by Toxoplasma gondii in humans: a meta-analysis. Comp Parasitol. 2016;83(1):11–20.

    Article  Google Scholar 

  39. Arce-Estrada GE, Gómez-Toscano V, Cedillo-Peláez C, Sesman-Bernal AL, Bosch-Canto V, Mayorga-Butrón JL, et al. Report of an unusual case of anophthalmia and craniofacial cleft in a newborn with Toxoplasma gondii congenital infection. BMC Infect Dis. 2017;17(1):459.

    Article  Google Scholar 

  40. Alvarado-Esquivel C, Pacheco-Vega S, Hernández-Tinoco J, Centeno-Tinoco M, Beristain-García I, Sánchez-Anguiano L, et al. Miscarriage history and Toxoplasma gondii infection: a cross-sectional study in women in Durango City, Mexico. Eur J Microbiol Immunol. 2014;4(2):117–22.

    Article  CAS  Google Scholar 

  41. Pal RA, Qayyum M, Yaseen M. Seroprevalence of antibodies to Toxoplasma gondii, with particular reference to obstetric history of patients in Rawalpindi-Islamabad, Pakistan. J Pak Med Assoc. 1996;46(3):56–8.

    CAS  PubMed  Google Scholar 

  42. Attia RA, El-Zayat M, Rizk H, Motawea S. Toxoplasma IgG & IgM antibodies: a case control study. J Egypt Soc Parasitol. 1995;25(3):877–82.

    CAS  PubMed  Google Scholar 

  43. Saki J, Mohammadpour N, Moramezi F, Khademvatan S. Seroprevalence of Toxoplasma gondii in women who have aborted in comparison with the women with normal delivery in Ahvaz, southwest of Iran. Sci World J. 2015;2015:764369.

    Article  CAS  Google Scholar 

  44. Gogate A, Deodhar L, Shah P, Vaidya P. Detection of Chlamydia trachomatis antigen & Toxoplasma gondii (IgM) & Mycoplasma hominis (IgG) antibodies by ELISA in women with bad obstetric history. Indian J Med Res. 1994;100:19–22.

    CAS  PubMed  Google Scholar 

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Acknowledgements

We are of great thanks for kind collaboration and assistance of the clinical staff of Sharq El-Nile hospital in Khartoum state, Sudan during patients’ reception and sampling. And also great thanks to all participants contributed to this work. We also thank Dr. Tarig B. Higazi, Professor of Biological Sciences, Ohio University Zanesville for his valuable comments.

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Authors and Affiliations

  1. Department of Parasitology and Medical Entomology, Faculty of Medical Laboratory Sciences, Nile College, Khartoum, Sudan

    Madinna Mustafa, Fatima Fathy, Abubaker Mirghani, Mona A. Mohamed, Nouh S. Mohamed & Amjed M. Abd Elkareem

  2. Department of Neurology, Mayo Clinic, Jacksonville, FL, USA

    Mohamed S. Muneer

  3. Department of Radiology, Mayo Clinic, Jacksonville, FL, USA

    Mohamed S. Muneer

  4. Department of Internal Medicine, Faculty of Medicine, University of Khartoum, Khartoum, Sudan

    Mohamed S. Muneer

  5. Department of Molecular Biology, National University Biomedical Research Institute, National University, Khartoum, Sudan

    Abdallah E. Ahmed, Mohamed Siralkhatim Ali, Rihab A. Omer & Nouh S. Mohamed

  6. Faculty of Medicine, Neelain University, Khartoum, Sudan

    Mohamed Siralkhatim Ali

  7. Mycetoma Research Center, University of Khartoum, Khartoum, Sudan

    Emmanuel E. Siddig

  8. Department of Parasitology and Medical Entomology, Faculty of Medical Laboratory Sciences, Sinnar University, Sinnar, Sudan

    Nouh S. Mohamed

  9. Parasitology Department, College of Medical Laboratory Sciences, Sudan University of Science and Technology, Khartoum, Sudan

    Amjed M. Abd Elkareem

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  1. Madinna Mustafa
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Contributions

MM, FF, AM, MAM and AMAE provided conceptual framework for the project, guidance for interpretation of the data, performed data analysis, NSM, EES, AEA, ROA and MSA participated in the performance of the Parasitological work. NSM, MSM and AMAE performed the statistical analysis and guidance for data interpretation. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Nouh S. Mohamed.

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Ethics approval and consent to participate

The study was approved by the National University Biomedical Research Institute Research Ethics Committee—National University, Sudan. Informed consent was obtained from each participant prior to enrollment in the study using written consent from adults, parents or legal custodians of children.

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The authors declare that they have no competing interests.

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Additional file

Additional file 1.

Analysis of risk factors of having toxoplasmosis and its relation to the frequency of abortion.

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Mustafa, M., Fathy, F., Mirghani, A. et al. Prevalence and risk factors profile of seropositive Toxoplasmosis gondii infection among apparently immunocompetent Sudanese women. BMC Res Notes 12, 279 (2019). https://doi.org/10.1186/s13104-019-4314-0

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