Detection of toxoplasmosis in aborted women in Alexandria, Egypt using ELISA and PCR

Abstract

Toxoplasmosis is a worldwide infection that can be acquired through the ingestion of tissue cysts in poorly cooked meat, and/or oblivious intake of sporulated oocysts in cat faeces, and transplacental. The infection in pregnant women is mainly asymptomatic. It produces abortion or congenital infection. The present study aimed to test the utility of polymerase chain reaction (PCR) on placental tissues in comparison to enzyme-linked immunosorbent assay (ELISA) to detect infections with Toxoplasma gondii in aborted women presented to Al-Shatby Maternity Hospital, Alexandria University, Egypt. Specific Toxoplasma gondii IgG and IgM were detected in serum by ELISA. Placental tissues from each participant were subjected to DNA extraction and PCR amplification. It was found that overall seroprevalence was 73%, DNA was detected in placenta tissues by using PCR analysis in 46% of cases. {× 2 (p) 18.124(< 0.001)}. Toxoplasma IgG/IgM by ELISA was positive in 23% of the cases, 20% showed amplified DNA by PCR. Positive IgG without IgM was seen in 27% cases, only 2% of them were positive by PCR. Moreover, positive PCR among positive ELISA IgM aborted women was 21 of the 23 cases. Positive PCR was obtained in three seronegative women. Our results showed that PCR sensitivity was 58.90 specificity 88.89, positive predictive value was 93.48%, and negative predictive value 44.44%. Although ELISA assay is still the gold standard of diagnosis of Toxoplasmosis, other diagnostic modalities are highly required particularly in those ELISA seronegative cases. PCR can be used as a sensitive and precise modality.

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References

  1. Abdel-Hameed DM, Hassanein O (2004) Evaluation of semi-quantitative PCR and IgG & IgM ELISA in the diagnosis of toxoplasmosis in females with miscarriage. J Egypt Soc Parasitol 34(2):559–570

    PubMed  Google Scholar 

  2. Abo EL Naga AM, Shaltot AA, El-Baz R, Fayad E (2008) PCR detection of Toxoplasma gondii DNA versus serological diagnosis in women suffering from repeated abortion. Egypt J Hosp Med 33:577–586

    Google Scholar 

  3. Awadalla HN, El-Temsahy MM, Sharaki OA, El Zawawy LA (2008) The validity of IgG avidity enzyme-linked immunosorbent assay and polymerase chain reaction for the determination of Toxoplasma infections during pregnancy. PUJ 1:23–30

    Google Scholar 

  4. Barakat AMA, Ahmed SO, Zaki MS, El FadalyAbd El-Razik HAKA, El-Hariri HM, Johar D (2018) New approach to differentiate primary from latent Toxoplasma gondii abortion through immunoglobulin and DNA interpretation. Microb Pathog 125:66–71. https://doi.org/10.1016/j.micpath.2018.09.001

    CAS  Article  PubMed  Google Scholar 

  5. Bassiony H, Soliman N, El-Tawab S, Eassa S, Eissa A (2016) Sero-prevalence and risk factors associated with Toxoplasma gondii infection among pregnant women in Alexandria, Egypt. Int J Reprod Contracept Obstet Gynecol 5:4220–4227. https://doi.org/10.18203/2320-1770.ijrcog20164318

    Article  Google Scholar 

  6. Bin Dajem SM, Almushait MA (2012) Detection of Toxoplasma gondii DNA by PCR in blood samples collected from pregnant Saudi women from the Aseer region, Saudi Arabia. Ann Saudi Med. 32(5):507–512. https://doi.org/10.5144/0256-4947.2012.14.7.1200

    Article  PubMed  PubMed Central  Google Scholar 

  7. Calabrese K, Roberto T, Ricardo S, Corte-Real S (2004) Ocular toxoplasmosis: the role of retinal pigment epithelium migration in infection. Parasitol Res 92:467–472. https://doi.org/10.1007/s00436-003-1031-2

    Article  PubMed  Google Scholar 

  8. Chaudhry SA, Gad N, Koren G (2014) Toxoplasmosis and pregnancy. Can Fam Phys 60(4):334–336

    Google Scholar 

  9. Chen ZY, Li AM, Lin GC, Wang XZ (2005) Serological investigation of Toxoplasma infection among different populations of people in Guizhou Province. Acta Academiae Med Zunyi 28:382–383 (Translated from Chinese)

    Google Scholar 

  10. Cook A, Gilbert R, Buffolano W, Zufferey J, Petersen E, Jenum P (2000) Sources of Toxoplasma infection in pregnant women: a European multicenter case-control study. BMJ 321:142–147

    CAS  Article  Google Scholar 

  11. Dubey JP, Jones JL (2008) Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol 38:1257–1278

    CAS  Article  Google Scholar 

  12. El-Askari HMS (2007) Evaluation of serological and molecular techniques in clinical states of toxoplasmosis. MD thesis, Parasitology, Faculty of Medicine, Cairo University, Egypt

  13. El-Fakahany AF, Abdel-Maboud AI, El-Gar-hy MF, Eraky MA (2002) Comparative study between ELISA IgG, IgM & PCR in diagnosing and studying toxoplasmosis in Qualyobia Governorate, Egypt. J Egypt Soc Parasitol 2:475–486

    Google Scholar 

  14. Fallahi S, Rostami A, Birjandi M, Zebardast N, Kheirandish F, Spotin A (2017) Parkinson’s disease and Toxoplasma gondii infection: sero-molecular assess the possible link among patients. Acta Trop 173:97–101

    Article  Google Scholar 

  15. Field A (2013) Discovering statistics using IBM SPSS statistics. Sage, London (2013)

    Google Scholar 

  16. Filisetti D, Cocquerelle V, Pfaff A, Villard O, Candolfi E (2010) Placental testing for Toxoplasma gondii is not useful to diagnose congenital Toxoplasmosis. Pediatr Infect Dis J 29(7):665–667

    Article  Google Scholar 

  17. Flack VF, Afifi AA, Lachenbruch PA, Schouten HJ (1988) Sample size determinations for the two rater kappa statistic. Psychometrika 53(3):321–325

    Article  Google Scholar 

  18. Fuentes I, Rubio JM, Ramirez C, Alvar J (2001) Genotypic characterization of Toxoplasma gondii strains associated with human toxoplasmosis in Spain: direct analysis from clinical samples. J Clin Microbiol 39:1566–1570

    CAS  Article  Google Scholar 

  19. Gallego C, Saavedra-Matiz C, Gomez-Marin JE (2006) Direct genotyping of animal and human isolates of Toxoplasma gondii from Colombia (South America). Acta Trop 97:161–167

    CAS  Article  Google Scholar 

  20. Ghoneim NH, Shalaby SI, Hassanain NA, Zeedan GS, Soliman YA, Abdalhamed AM (2009) detection of genomic Toxoplasma gondii DNA and anti-toxoplasmosis antibodies. Life Sci J 6:45–60

    Google Scholar 

  21. Ibrahim HM, Mohamed AH, El-Sharaawy AA, El-Shqanqery HE (2017) Molecular and serological prevalence of Toxoplasma gondii in pregnant women and sheep in Egypt. Asian Pac J Trop Med 10(10):996–1001

    Article  Google Scholar 

  22. Jones J, Lopez A, Wilson M, Schulkin J, Gibbs R (2001) Congenital toxoplasmosis: a review. Obstet Gynecol Surv 56:296–305

    CAS  Article  Google Scholar 

  23. Kamal AM, Ahmed AK, Abdellatif MZ, Tawifik M, Hassan EE (2015) Seropositivity of Toxoplasmosis in pregnant women by ELIZA at Minia University Hospital, Egypt. Korean J Parasitol 53(5):605–610

    CAS  Article  Google Scholar 

  24. Kimball AC, Kean BH, Fuchs F (1971) Congenital toxoplasmosis: a prospective study of 4,048 obstetric patients. Am J Obstet Gynecol 111:211–218

    CAS  Article  Google Scholar 

  25. Khan A, Jordan C, Muccioli C, Vallochi AL, Rizzo LV, Belfort R Jr, Vitor RWA, Silveira C, Sibley LD (2006) Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplasmosis, Brazil. Emerg Infect Dis 12:942–949

    CAS  Article  Google Scholar 

  26. Liu Q, Wang ZD, Huang SY, Zhu XQ (2015) Diagnosis of toxoplasmosis and typing of Toxoplasma gondii. Parasites Vectors 28(8):292

    Article  Google Scholar 

  27. Mandrekar JN (2010) Receiver operating characteristic curve in diagnostic test assessment. J Thorac Oncol 5(9):1315–1316

    Article  Google Scholar 

  28. Messaritakis I, Detsika M, Koliou M, Sifakis S, Antoniou M (2008) Prevalent genotypes of Toxoplasma gondii in pregnant women and patients from Crete and Cyprus. Am J Trop Med Hyg 79:205–209

    CAS  Article  Google Scholar 

  29. Mitchell CD, Erlich SS, Mastrucci MT, Hutto SC, Parks WP, Scott GB (1990) Congenital toxoplasmosis occurring in infants perinatally infected with human immunodeficiency virus 1. Pediatr Infect Dis J 9:512–518

    CAS  Article  Google Scholar 

  30. Nimri L, Pelloux H, Elkhatib L (2004) Detection of Toxoplasma gondii DNA and specific antibodies in high-risk pregnant women. Am J Trop Med Hyg 71:831–835

    CAS  Article  Google Scholar 

  31. Pignanelli S (2011) Laboratory diagnosis of Toxoplasma gondii infection with direct and indirect diagnostic techniques. Indian J Pathol Microbiol 54(4):786–789

    PubMed  Google Scholar 

  32. Remington JS, Thullizies P, Montoya JG (2004) Recent developments for diagnosis of toxoplasmosis. J Clin Microbiol 42:941–945

    Article  Google Scholar 

  33. Robert-Gangneux F, Dardé M (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Micro Biol Rev 25(2):264–296

    CAS  Article  Google Scholar 

  34. Robert-Gangneux F, Dupretz P, Yvenou C, Quinio D, Poulain P, Guiguen C, Gangneux J-P (2009) Clinical relevance of placenta examination for the diagnosis of congenital toxoplasmosis. Pediatr Infect Dis J 29:33–38. https://doi.org/10.1097/INF.0b013e3181b20ed1

    Article  Google Scholar 

  35. Romand S, Wallon M, Franck J, Thulliez P, Peyron F, Dumon H (2001) Prenatal diagnosis using polymerase chain reaction on amniotic fluid for congenital toxoplasmosis. Obstet Gynecol 97(2):296–300

    CAS  PubMed  Google Scholar 

  36. Rosso F, Les JT, Agudelo A, Villalobos C, Chaves JA, Tunubala GA (2008) Prevalence of infection with Toxoplasma gondii among pregnant women in Cali, Colombia, South America. Am J Trop Med Hyg 78(3):504–508

    Article  Google Scholar 

  37. Sahwi SY, Zaki MS, Haiba NY, Elsaid OK, Anwar MY, AbdRabbo SA (1995) Toxoplasmosis as a cause of repeated abortion. J Obstet Gynaecol 21(2):145–148

    CAS  Article  Google Scholar 

  38. Sarvi S, Nayeri Chegeni T, Sharif M et al (2019) Congenital toxoplasmosis among Iranian neonates: a systematic review and meta-analysis. Epidemiol Health 41:e2019021. https://doi.org/10.4178/epih.e2019021

    Article  PubMed  PubMed Central  Google Scholar 

  39. Sharifi K, Hosseini Farash BR, Tara F, Khaledi A, Sharifi K, Shamsian SAA (2019) Diagnosis of acute toxoplasmosis by IgG and IgM antibodies and IgG avidity in pregnant women from Mashhad, Eastern Iran. Iran J Parasitol 14(4):639–645

    PubMed  PubMed Central  Google Scholar 

  40. Shojaee S, Keshavarz H (2014) Detection of acute toxoplasmosis: the genitally transmittable infection. Int J Women’s Health Reprod Sci 2:90–93

    CAS  Article  Google Scholar 

  41. Switaj K, Master A, Skrzypczak M, Zaborowski P (2005) Recent trends in molecular diagnostics for Toxoplasma gondii infections. Clin Microbiol Infect 11:170–176

    CAS  Article  Google Scholar 

  42. Villena I, Ancelle T, Delmas C, Garcia P, Brezin AP, Thulliez P, Wallon M, King L, Goulet V (2010) Toxosurv network and National Reference Centre for Toxoplasmosis. Congenital toxoplasmosis in France in 2007: first results from a national surveillance system. Euro Surveill 15(25):1960

    Article  Google Scholar 

  43. Zhang K, Lin G, Han Y, Li J (2016) Serological diagnosis of toxoplasmosis and standardization. Clin Chim Acta 461:83–89

    CAS  Article  Google Scholar 

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Correspondence to Naglaa Fathi Abd El-Latif.

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El-Sayad, M.H., Salem, A.I., Fazary, H. et al. Detection of toxoplasmosis in aborted women in Alexandria, Egypt using ELISA and PCR. J Parasit Dis (2021). https://doi.org/10.1007/s12639-020-01327-0

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Keywords

  • Toxoplasma gondii
  • ELISA
  • PCR
  • Aborted women
  • Egypt