Prospective Risk Factors of Toxoplasmosis Seropositivity in Pregnant Women: The Fundamental Role of Community Healthcare Education

Lienda Bashier Eltayeb, Nasir Abdelrafie Hamad, Abeer Abd Alla Ellhassan Babiker

 
International Journal of Biomedicine. 2021;11(4):558-563.
DOI: 10.21103/Article11(4)_OA26
Originally published December 10, 2021

Abstract: 

Background: The present study conducted a survey on awareness of toxoplasmosis infection, with an emphasis on risk factors, and an assessment of toxoplasmosis prevalence in pregnant women in Al-Kharj province of KSA.
Methods and Results: A cross-sectional study with a qualitative approach was carried out from August 2018 to February 2019. The study recruited all pregnant women who attended maternity and children’s outpatient clinics. The non-probability sampling approach was used to select 345 blood samples from study subjects. T. gondii-specific IgG and IgM antibodies were identified using ELISA. Each participant enrolled in the study was provided with a validated questionnaire to fill out by an assistant of the laboratory technician or an antenatal care nurse. In addition to socio-demographic data, simple closed-ended questions about established risk factors for T. gondii exposure were included in the questionnaire items, and answers were listed in a three-point Likert scale (agree, disagree, I am not sure). The overall prevalence of T. gondii-specific antibodies among study subjects was 12.75%; 29(8.40%) women were positive for IgG only, 9(2.6%) - for IgM, and 6(1.7%) - for both IgG and IgM antibodies.
About 41.4% of participants were in the first trimester of pregnancy; among them 31(9%) were positive for T. gondii antibodies.  82.8% of pregnant women had chronic infection in the first trimester, while 44.4% of those women also had an acute infection.  The number of respondents to the questionnaire was 345 participants with a response rate of about 100%. It is important to note that 81.5% of women were unaware that toxoplasmosis is dangerous, and two-thirds of them didn't know the dangerous complications for the fetus and newborn.
Conclusion: The current study concludes that there is a low prevalence of toxoplasmosis among Saudi pregnant women in Al-Kharj province. A general program must be implemented to increase population awareness, especially among the at-risk populations.

Keywords: 
Toxoplasma gondii • risk factors • IgG • IgM • pregnancy
References: 
  1. Zhou JJ, Tao LL. [Seroprevalence and risk factors of Toxoplasma gondii infection among pregnant women in Wuxi region]. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi. 2015 Dec;27(6):604-7. [Article in Chinese].
  2. Montoya JG, Remington JS. Management of Toxoplasma gondii infection during pregnancy. Clin Infect Dis. 2008 Aug 15;47(4):554-66. doi: 10.1086/590149.
  3. Foroutan-Rad M, Khademvatan S, Majidiani H, Aryamand S, Rahim F, Malehi AS. Seroprevalence of Toxoplasma gondii in the Iranian pregnant women: A systematic review and meta-analysis. Acta Trop. 2016 Jun;158:160-169. doi: 10.1016/j.actatropica.2016.03.003.
  4. Tarekegn ZS, Dejene H, Addisu A, Dagnachew S. Potential risk factors associated with seropositivity for Toxoplasma gondii among pregnant women and HIV infected individuals in Ethiopia: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2020 Dec 15;14(12):e0008944.
  5. Chaudhry SA, Gad N, Koren G. Toxoplasmosis and pregnancy. Can Fam Physician. 2014 Apr;60(4):334-6. 
  6. 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. 
  7.  Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet. 2004;363(9425):1965–76. doi: 10.1016/S0140-6736(04)16412-X
  8. Saadatnia G, Golkar M. A review on human toxoplasmosis. Scand J Infect Dis. 2012;44(11):805–14. doi: 10.3109/00365548.2012.693197. 
  9. Kieffer F, Wallon M. Congenital toxoplasmosis. Handb Clin Neurol. 2013;112:1099–101. doi: 10.1016/B978-0-444-52910-7.00028-3. 
  10. Elmore SA, Jones JL, Conrad PA, Patton S, Lindsay DS, Dubey JP. Toxoplasma gondii: epidemiology, feline clinical aspects, and prevention. Trends Parasitol. 2010 Apr;26(4):190-6. doi: 10.1016/j.pt.2010.01.009.
  11. Preventing Congenital Toxoplasmosis-CDC. Available from: 
    1. https://www.cdc.gov/mmwr/preview/mmwrhtml/rr4902a5.htm
  12. Wilson M, McAuley JB. Toxoplasma. In: Murray P, ed. Manual of clinical microbiology. 7th ed. Washington, DC: ASM Press, 1999:1374-82.
  13. Lappalainen M, Hedman K. Serodiagnosis of toxoplasmosis. The impact of measurement of IgG avidity. Ann Ist Super Sanita. 2004;40(1):81-8. PMID: 15269456.
  14. Machumi I, Mirambo MM, Ruganuza D, Rambau P, Massinde AN, Kihunrwa A, Mshana SE, Morona D. Factors Associated With Toxoplasma gondii IgG and IgM Antibodies, and Placental Histopathological Changes Among Women With Spontaneous Abortion in Mwanza City, Tanzania. East Afr Health Res J. 2017;1(2):86-94. doi: 10.24248/EAHRJ-D-16-00408.
  15. Sardarian K, Maghsood AH, Farimani M, Hajilooi M, Saidijam M, Ghane ZZ, Mahaki H, Zamani A. Detection of Toxoplasma gondii B1 Gene and IgM in IgG Seropositive Pregnant Women. Clin Lab. 2019 Jan 1;65(1). doi: 10.7754/Clin.Lab.2018.180425. PMID: 30775900.
  16. Rostami A, Riahi SM, Contopoulos-Ioannidis DG, Gamble HR, Fakhri Y, Shiadeh MN, Foroutan M, Behniafar H, Taghipour A, Maldonado YA, Mokdad AH, Gasser RB. Acute Toxoplasma infection in pregnant women worldwide: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2019 Oct 14;13(10):e0007807. doi: 10.1371/journal.pntd.0007807.
  17. Dhakal R, Gajurel K, Pomares C, Talucod J, Press CJ, Montoya JG. Significance of a Positive Toxoplasma Immunoglobulin M Test Result in the United States. J Clin Microbiol. 2015 Nov;53(11):3601-5. doi: 10.1128/JCM.01663-15. 
  18. Del Bono V, Canessa A, Bruzzi P, Fiorelli MA, Terragna A. 1989. Significance of specific immunoglobulin M in the chronological diagnosis of 38 cases of toxoplasmic lymphadenopathy. J Clin Microbiol 27:2133–2135. 
  19. Gras L, Gilbert RE, Wallon M, Peyron F, Cortina-Borja M. 2004. Duration of the IgM response in women acquiring Toxoplasma gondii during pregnancy: implications for clinical practice and cross-sectional incidence studies. Epidemiol Infect 132:541–548. doi:10.1017/S0950268803001948. 
  20. Roozbehani M, Gharavi MJ, Moradi M, Razmjou E. Detection of acute Toxoplasma gondii infection in pregnant women by IgG avidity and PCR analysis. Trop Biomed. 2018 Dec 1;35(4):908-914. PMID: 33601840.
  21. Hampton MM. Congenital Toxoplasmosis: A Review. Neonatal Netw. 2015;34(5):274-8. doi: 10.1891/0730-0832.34.5.274. PMID: 26802827.
  22. Naot Y, Remington JS. An enzyme-linked immunosorbent assay for detection of IgM antibodies to Toxoplasma gondii: use for diagnosis of acute acquired toxoplasmosis. J Infect Dis. 1980 Nov;142(5):757-66. doi: 10.1093/infdis/142.5.757. 
  23. Sarah YA, Uzma AK, Asmaa IE: Prevalence of seropositive toxoplasmosis in pregnant women in Hail region. Int J Health Sci Res. 2014, 4:66-71.
  24. Mohajab AH, Alshehri HZ, Shati RO, Alshehri AA, Alafghani MA, Alasmari A, Almahi M, Oraif A. Anti-toxoplasma Antibody Prevalence and Cost-effectiveness in Pregnant Women at the King Abdulaziz University Hospital, Jeddah, Saudi Arabia. Cureus. 2020 Jan 16;12(1):e6675. doi: 10.7759/cureus.6675.
  25. Alghamdi J, Elamin MH, Alhabib S: Prevalence and genotyping of Toxoplasma gondii among Saudi pregnant women in Saudi Arabia. Saudi Pharm J. 2016, 24:645-51. 10.1016/j.jsps.2015.05.001
  26. Elsafi SH, Al-Mutairi WF, Al-Jubran KM, Abu Hassan MM, Al Zahrani EM. Toxoplasmosis seroprevalence in relation to knowledge and practice among pregnant women in Dhahran, Saudi Arabia. Pathog Glob Health. 2015;109(8):377-82. doi: 10.1080/20477724.2015.1103502. 
  27. Aqeely H, El-Gayar EK, Perveen Khan D, Najmi A, Alvi A, Bani I, Mahfouz MS, Abdalla SE, Elhassan IM. Seroepidemiology of Toxoplasma gondii amongst Pregnant Women in Jazan Province, Saudi Arabia. J Trop Med. 2014;2014:913950. doi: 10.1155/2014/913950. 
  28. Andiappan H, Nissapatorn V, Sawangjaroen N, Chemoh W, Lau YL, Kumar T, Onichandran S, Suwanrath C, Chandeying V. Toxoplasma infection in pregnant women: a current status in Songklanagarind hospital, southern Thailand. Parasit Vectors. 2014 May 22;7:239. doi: 10.1186/1756-3305-7-239. 
  29. Lin YL, Liao YS, Liao LR, Chen FN, Kuo HM, He S. Seroprevalence and sources of Toxoplasma infection among indigenous and immigrant pregnant women in Taiwan. Parasitol Res. 2008 Jun;103(1):67-74. doi: 10.1007/s00436-008-0928-1. 
  30. Paul E, Kiwelu I, Mmbaga B, Nazareth R, Sabuni E, Maro A, Ndaro A, Halliday JEB, Chilongola J. Toxoplasma gondii seroprevalence among pregnant women attending antenatal clinic in Northern Tanzania. Trop Med Health. 2018 Nov 19;46:39. doi: 10.1186/s41182-018-0122-9.
  31. Kieffer F, Wallon M. Congenital toxoplasmosis. Handb Clin Neurol. 2013;112:1099-1101. doi:10.1016/B978-0-444-52910-7.00028-3.
  32. Liu Q, Wei F, Gao S, Jiang L, Lian H, Yuan B, Yuan Z, Xia Z, Liu B, Xu X, Zhu XQ. Toxoplasma gondii infection in pregnant women in China. Trans R Soc Trop Med Hyg. 2009 Feb;103(2):162-6. doi: 10.1016/j.trstmh.2008.07.008. 
  33. Cong W, Dong XY, Meng QF, Zhou N, Wang XY, Huang SY, Zhu XQ, Qian AD. Toxoplasma gondii Infection in Pregnant Women: A Seroprevalence and Case-Control Study in Eastern China. Biomed Res Int. 2015;2015:170278. doi: 10.1155/2015/170278.
  34. Gebremedhin EZ, Abebe 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 Feb 26;13:101. doi: 10.1186/1471-2334-13-101. 
  35. Mwambe B, Mshana SE, Kidenya BR, Massinde AN, Mazigo HD, Michael 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 Aug 6;6:222. doi: 10.1186/1756-3305-6-222. 
  36. Makki SM, Abdel-Tawab AH. Anti-Toxoplasma gondii antibodies among volunteer blood donors in eastern Saudi Arabia. J Egypt Soc Parasitol. 2010 Aug;40(2):401-12. PMID: 21246947.
  37. Obaid HM. Toxoplasma Sero-Prevalence and Related Knowledge Survey in Pregnant Women and University Staff. Int J Curr Microbiol App Sci. 2019;8(02):2808-2816. doi: 10.20546/ijcmas.2019.802.330
  38. Abdalla Sayed Ahmed GM, Abo Elghite Elhossiny EE. Knowledge and Attitude of women regarding Toxoplasmosis during pregnancy and measures to overcome it in Slums areas. Int J Curr Res.2014;6(4):6365–71.
  39. Onduru OG, Rumisha SF, Munyeme M, Phiri AM. Evaluation of the level of awareness of congenital toxoplasmosis and associated practices among pregnant women and health workers in Tanzania's Temeke district in Dar es Salaam. Afr Health Sci. 2019 Dec;19(4):3027-3037. doi: 10.4314/ahs.v19i4.24. 
  40. Desta AH. Knowledge, Attitude and Practice of community towards zoonotic importance of Toxoplasma infection in Central Afar Region, North East Ethiopia. Int J Biomed Sci Eng. 2015;3(6):74-86.
  41. Ait Hamou S, Laboudi M. An analytical study on the awareness and practice relating toxoplasmosis among pregnant women in Casablanca, Morocco. BMC Public Health. 2021 Mar 16;21(1):507. doi: 10.1186/s12889-021-10474-9. 

Download Article
Received September 13, 2021.
Accepted November 29, 2021.
©2021 International Medical Research and Development Corporation.