Current and Emerging Techniques for Diagnosis of Toxoplasmosis in Pregnancy: A Narrative Review
-
Aref Teimouri
,
Shima Mahmoudi
,
Atefeh Behkar
,
Keivan Sahebi
,
Hassan Foroozand
,
Gholamreza Hassanpour
,
Hossein Keshavarz
Abstract
Toxoplasma gondii is an intracellular parasite capable of crossing the placenta in pregnancy and infecting the developing fetus, leading to various congenital anomalies and even abortion. Acute Toxoplasma infection is responsible for almost all cases of congenital toxoplasmosis in immunocompetent pregnant women. Prenatal screening for acute toxoplasmosis primarily involves maternal serology and fetal ultrasound imaging. When serological or ultrasound findings suggest acute infection, further diagnostic tests are necessary to confirm fetal infection. Currently, molecular methods to detect the parasite’s DNA, including polymerase chain reaction-based methods, on amniotic fluid are the gold standard tests for the diagnosis of congenital toxoplasmosis. In this review, we aim to discuss various aspects of screening and diagnostic methods for toxoplasmosis in pregnancy, including (i) current serological assays, screening approaches, and future perspectives; (ii) the role of imaging techniques, with an emphasis on ultrasound; (iii) principles and recent advances in diagnostic molecular methods; (iv) emerging techniques, such as point-of-care-based tests and biosensors, and microRNAs as novel biomarkers of acute infection; and (v) an overview of screening programs in different countries, important epidemiological determinants, and recommendations for Toxoplasma screening health policies.
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5. Bigna JJ, Tochie JN, Tounouga DN, et al. Global, regional, and country seroprevalence of Toxoplasma gondii in pregnant women: a systematic review, modelling and meta-analysis. Sci Rep. 2020; 10(1):12102.
6. Rostami A, Riahi SM, Contopoulos-Ioannidis DG, et al. Acute Toxoplasma infection in pregnant women worldwide: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2019; 13(10): e0007807.
7. Torgerson PR, Mastroiacovo P. The global burden of congenital toxoplasmosis: a systematic review. Bull World Health Organ. 2013; 91:501-508.
8. Ali-Heydari S, Keshavarz H, Shojaee S, et al. Diagnosis of antigenic markers of acute toxoplasmosis by IgG avidity immunoblotting. Parasite. 2013; 20:18.
9. Teimouri A, Mohtasebi S, Kazemirad E, et al. Role of Toxoplasma gondii IgG avidity testing in discriminating between acute and chronic toxoplasmosis in pregnancy. J Clin Microbiol. 2020; 58(9):e00505-20.
10. Teimouri A, Modarressi MH, Shojaee S, et al. Detection of Toxoplasma-specific immunoglobulin G in human sera: Performance comparison of in-house Dot-ELISA with ECLIA and ELISA. Eur J Clin Microbiol Infect Dis. 2018; 37:1421-1429.
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12. Gras L, Gilbert R, Wallon M, et al. Duration of the IgM response in women acquiring Toxoplasma gondii during pregnancy: implications for clinical practice and cross-sectional incidence studies. Epidemiol Infect. 2004; 132(3):541-548.
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14. Olariu TR, Blackburn BG, Press C, et al. Role of Toxoplasma IgA as part of a reference panel for the diagnosis of acute toxoplasmosis during pregnancy. J Clin Microbiol. 2019; 57(2): e01357-18.
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21. Buffolano W, Lappalainen M, Hedman L, et al. Delayed maturation of IgG avidity in congenital toxoplasmosis. Eur J Clin Microbiol Infect Dis. 2004; 23:825-830.
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23. Fricker-Hidalgo H, L’Ollivier C, Bosson C, et al. Interpretation of the Elecsys Toxo IgG avidity results for very low and very high index: study on 741 sera with a determined date of toxoplasmosis. Eur J Clin Microbiol Infect Dis. 2017; 36:847-852.
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25. Noruzi R, Dalimi A, Forouzandeh M, et al. Identification of live Toxoplasma gondii by the NASBA method in rat. Pathobiol Res. 2012; 15(1):73-80.
26. Costa JM, Ernault P, Gautier E, et al. Prenatal diagnosis of congenital toxoplasmosis by duplex real-time PCR using fluorescence resonance energy transfer hybridization probes. Prenat Diagn. 2001; 21(2):85-88.
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34. Teixeira LE, Kanunfre KA, Shimokawa PT, et al. The performance of four molecular methods for the laboratory diagnosis of congenital toxoplasmosis in amniotic fluid samples. Rev Soc Bras Med Trop. 2013; 46:584-588.
35. de Oliveira Azevedo CT, do Brasil PEA, Guida L, et al. Performance of polymerase chain reaction analysis of the amniotic fluid of pregnant women for diagnosis of congenital toxoplasmosis: a systematic review and meta-analysis. PLoS One. 2016; 11(4) e0149938.
36. Romand S, Wallon M, Franck J, et al. Prenatal diagnosis using polymerase chain reaction on amniotic fluid for congenital toxoplasmosis. Obstet Gynecol. 2001; 97(2):296-300.
37. Rabilloud M, Wallon M, Peyron F. In utero and at birth diagnosis of congenital toxoplasmosis: Use of likelihood ratios for clinical management. Pediatr Infect Dis J. 2010; 29(5):421-425.
38. Santana SS, Paiva VF, Carvalho FR, et al. A peptide originated from Toxoplasma gondii microneme 8 displaying serological evidence to differentiate recent from chronic human infection. Parasitol Int. 2021; 84:102394.
39. Frickel E-M, Sahoo N, Hopp J, et al. Parasite stage-specific recognition of endogenous Toxoplasma gondii-derived CD8+ T cell epitopes. J Infect Dis. 2008; 198(11):1625-1633.
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41. Costa JG, Peretti LE, García VS, et al. P35 and P22 Toxoplasma gondii antigens abbreviate regions to diagnose acquired toxoplasmosis during pregnancy: toward single-sample assays. Clin Chem Lab Med. 2017; 55(4):595-604.
42. Teimouri A, Modarressi MH, Shojaee S, et al. Development, optimization, and validation of an in-house Dot-ELISA rapid test based on SAG1 and GRA7 proteins for serological detection of Toxoplasma gondii infections. Infect Drug Resist. 2019:2657-2669.
43. Teimouri A, Abbaszadeh Afshar MJ, Mohtasebi S, et al. Assessment of an in-house enzyme-linked immunosorbent assay and IgG avidity test based on SAG1 and GRA7 proteins for discriminating between acute and chronic toxoplasmosis in humans. J Clin Microbiol. 2021; 59(8): e0041621.
44. Dai J, Jiang M, Wang Y, et al. Evaluation of a recombinant multiepitope peptide for serodiagnosis of Toxoplasma gondii infection. Clin Vaccine Immunol. 2012; 19(3):338-342.
45. Dai J-f, Jiang M, Qu L-l, et al. Toxoplasma gondii: enzyme-linked immunosorbent assay based on a recombinant multi-epitope peptide for distinguishing recent from past infection in human sera. Exp Parasitol. 2013; 133(1):95-100.
46. Mahinc C, Flori P, Delaunay E, et al. Evaluation of a new immunochromatography technology test (LDBio Diagnostics) to detect Toxoplasma gondii IgG and IgM: comparison with the routine architect technique. J Clin Microbiol. 2017; 55(12):3395-3404.
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48. Molaei S, Dadkhah M, Fathi F. Toxoplasmosis diagnostic techniques: Current developed methods and biosensors. Talanta. 2023; 252:123828.
49. Prakrankamanant P. Quartz crystal microbalance biosensors: Prospects for point-of-care diagnostics. J Med Assoc Thai. 2014; 97 Suppl 4:S56-64.
50. Cho I-H, Kim DH, Park S. Electrochemical biosensors: Perspective on functional nanomaterials for on-site analysis. Biomater Res. 2020; 24:6.
51. Jiang S, Pu Q, Zhu W, et al. Modeling Analysis and Performance Study of Toxoplasma gondii IgM Antibody Immunosensor Based on Graphene and Au–Fe3O4. J Nanoelectronics Optoelectron. 2020; 15(3):353-360.
52. Takara EA, Pereira SV, Scala-Benuzzi ML, et al. Novel electrochemical sensing platform based on a nanocomposite of PVA/PVP/RGO applied to IgG anti-Toxoplasma gondii antibodies quantitation. Talanta. 2019; 195:699-705.
53. Alves LM, Rodovalho VR, Castro AC, et al. Development of direct assays for Toxoplasma gondii and its use in genomic DNA sample. J Pharm Biomed Anal. 2017; 145:838-844.
54. Hu R-S, He J-J, Elsheikha HM, et al. Differential brain microRNA expression profiles after acute and chronic infection of mice with Toxoplasma gondii oocysts. Front Microbiol. 2018; 9:2316.
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56. Xu M, Zhou D, Huang S, et al. Comparative characterization of microRNA profiles of different genotypes of Toxoplasma gondii. Parasitology. 2013; 140(9):1111-1118.
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2. Teimouri A, Goudarzi F, Goudarzi K, et al. Toxoplasma gondii infection in immunocompromised patients in Iran (2013–2022): A systematic review and meta-analysis. Iran J Parasitol. 2022; 17(4):443-457.
3. Márquez-Mauricio A, Caballero-Ortega H, Gómez-Chávez F. Congenital Toxoplasma gondii diagnosis: current approaches and new insights. Acta Parasitol. 2023; 68(3):473-480.
4. Dubey JP. Outbreaks of clinical toxoplasmosis in humans: five decades of personal experience, perspectives and lessons learned. Parasit Vectors. 2021;14(1):263.
5. Bigna JJ, Tochie JN, Tounouga DN, et al. Global, regional, and country seroprevalence of Toxoplasma gondii in pregnant women: a systematic review, modelling and meta-analysis. Sci Rep. 2020; 10(1):12102.
6. Rostami A, Riahi SM, Contopoulos-Ioannidis DG, et al. Acute Toxoplasma infection in pregnant women worldwide: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2019; 13(10): e0007807.
7. Torgerson PR, Mastroiacovo P. The global burden of congenital toxoplasmosis: a systematic review. Bull World Health Organ. 2013; 91:501-508.
8. Ali-Heydari S, Keshavarz H, Shojaee S, et al. Diagnosis of antigenic markers of acute toxoplasmosis by IgG avidity immunoblotting. Parasite. 2013; 20:18.
9. Teimouri A, Mohtasebi S, Kazemirad E, et al. Role of Toxoplasma gondii IgG avidity testing in discriminating between acute and chronic toxoplasmosis in pregnancy. J Clin Microbiol. 2020; 58(9):e00505-20.
10. Teimouri A, Modarressi MH, Shojaee S, et al. Detection of Toxoplasma-specific immunoglobulin G in human sera: Performance comparison of in-house Dot-ELISA with ECLIA and ELISA. Eur J Clin Microbiol Infect Dis. 2018; 37:1421-1429.
11. Dard C, Fricker-Hidalgo H, Brenier-Pinchart M-P, et al. Relevance of and new developments in serology for toxoplasmosis. Trends Parasitol. 2016; 32(6):492-506.
12. Gras L, Gilbert R, Wallon M, et al. Duration of the IgM response in women acquiring Toxoplasma gondii during pregnancy: implications for clinical practice and cross-sectional incidence studies. Epidemiol Infect. 2004; 132(3):541-548.
13. Pinard JA, Leslie NS, Irvine PJ. Maternal serologic screening for toxoplasmosis. J Midwifery Womens Health. 2003; 48(5):308-316.
14. Olariu TR, Blackburn BG, Press C, et al. Role of Toxoplasma IgA as part of a reference panel for the diagnosis of acute toxoplasmosis during pregnancy. J Clin Microbiol. 2019; 57(2): e01357-18.
15. Matowicka-Karna J, Kemona H. IgE antibodies in toxoplasmosis. Postepy Hig Med Dosw (Online). 2014:68:597-602.
16. Pinon J, Toubas D, Marx C, et al. Detection of specific immunoglobulin E in patients with toxoplasmosis. J Clin Microbiol. 1990; 28(8):1739-1743.
17. Gross U, Keksel O, Dardé ML. Value of detecting immunoglobulin E antibodies for the serological diagnosis of Toxoplasma gondii infection. Clin Diagn Lab Immunol. 1997; 4(3):247-251.
18. Wong S, Hajdu M, Ramirez R, et al. Role of specific immunoglobulin E in diagnosis of acute Toxoplasma infection and toxoplasmosis. J Clin Microbiol. 1993; 31(11):2952-2959.
19. Meroni V, Genco F, Tinelli C, et al. Spiramycin treatment of Toxoplasma gondii infection in pregnant women impairs the production and the avidity maturation of T. gondii-specific immunoglobulin G antibodies. Clin Vaccine Immunol. 2009; 16(10):1517-1520.
20. Flori P, Tardy L, Patural H, et al. Reliability of immunoglobulin G anti-Toxoplasma gondii avidity test and effects of treatment on avidity indexes of infants and pregnant women. Clin Vaccine Immunol. 2004; 11(4):669-674.
21. Buffolano W, Lappalainen M, Hedman L, et al. Delayed maturation of IgG avidity in congenital toxoplasmosis. Eur J Clin Microbiol Infect Dis. 2004; 23:825-830.
22. Murat J-B, L'Ollivier C, Fricker-Hidalgo H, et al. Evaluation of the new Elecsys Toxo IgG avidity assay for toxoplasmosis and new insights into the interpretation of avidity results. Clin Vaccine Immunol. 2012; 19(11):1838-1843.
23. Fricker-Hidalgo H, L’Ollivier C, Bosson C, et al. Interpretation of the Elecsys Toxo IgG avidity results for very low and very high index: study on 741 sera with a determined date of toxoplasmosis. Eur J Clin Microbiol Infect Dis. 2017; 36:847-852.
24. Rostami A, Karanis P, Fallahi S. Advances in serological, imaging techniques, and molecular diagnosis of Toxoplasma gondii infection. Infection. 2018; 46:303-315.
25. Noruzi R, Dalimi A, Forouzandeh M, et al. Identification of live Toxoplasma gondii by the NASBA method in rat. Pathobiol Res. 2012; 15(1):73-80.
26. Costa JM, Ernault P, Gautier E, et al. Prenatal diagnosis of congenital toxoplasmosis by duplex real-time PCR using fluorescence resonance energy transfer hybridization probes. Prenat Diagn. 2001; 21(2):85-88.
27. Romand S, Chosson M, Franck J, et al. Usefulness of quantitative polymerase chain reaction in amniotic fluid as early prognostic marker of fetal infection with Toxoplasma gondii. Am J Obstet Gynecol. 2004;190(3):797-802.
28. Yamamoto L, Targa LS, Sumita LM, et al. Association of parasite load levels in amniotic fluid with clinical outcome in congenital toxoplasmosis. Obstet Gynecol. 2017;130(2):335-45.
29. Cargill Y, Morin L, Bly S, et al. Content of a complete routine second trimester obstetrical ultrasound examination and report. J Obstet Gynaecol Can. 2009; 31(3):272-275.
30. Codaccioni C, Picone O, Lambert V, et al. Ultrasound features of fetal toxoplasmosis: a contemporary multicenter survey in 88 fetuses. Prenat Diagn. 2020; 40(13):1741-1752.
31. Werner H, Daltro P, Fazecas T, et al. Neuroimaging findings of congenital toxoplasmosis, cytomegalovirus, and Zika virus infections: A comparison of three cases. J Obstet Gynaecol Can. 2017; 39(12):1150-1155.
32. Lazarte-Rantes C, Rodríguez-Anccasi R, Rivas-Campos C, et al. Congenital Toxoplasma gondii: Findings in fetal MRI. Cureus. 2021; 13(8): e16894.
33. Paquet C, Yudin MH, Allen VM, et al. Toxoplasmosis in pregnancy: Prevention, screening, and treatment. J Obstet Gynaecol Can. 2013; 35(1):78-81.
34. Teixeira LE, Kanunfre KA, Shimokawa PT, et al. The performance of four molecular methods for the laboratory diagnosis of congenital toxoplasmosis in amniotic fluid samples. Rev Soc Bras Med Trop. 2013; 46:584-588.
35. de Oliveira Azevedo CT, do Brasil PEA, Guida L, et al. Performance of polymerase chain reaction analysis of the amniotic fluid of pregnant women for diagnosis of congenital toxoplasmosis: a systematic review and meta-analysis. PLoS One. 2016; 11(4) e0149938.
36. Romand S, Wallon M, Franck J, et al. Prenatal diagnosis using polymerase chain reaction on amniotic fluid for congenital toxoplasmosis. Obstet Gynecol. 2001; 97(2):296-300.
37. Rabilloud M, Wallon M, Peyron F. In utero and at birth diagnosis of congenital toxoplasmosis: Use of likelihood ratios for clinical management. Pediatr Infect Dis J. 2010; 29(5):421-425.
38. Santana SS, Paiva VF, Carvalho FR, et al. A peptide originated from Toxoplasma gondii microneme 8 displaying serological evidence to differentiate recent from chronic human infection. Parasitol Int. 2021; 84:102394.
39. Frickel E-M, Sahoo N, Hopp J, et al. Parasite stage-specific recognition of endogenous Toxoplasma gondii-derived CD8+ T cell epitopes. J Infect Dis. 2008; 198(11):1625-1633.
40. Myjak PA. Efficient production of the Toxoplasma gondii GRA6, p35, and SAG2 recombinant antigens and their applications in the serodiagnosis of toxoplasmosis. Acta Parasitol. 2005; 50(3):249-254.
41. Costa JG, Peretti LE, García VS, et al. P35 and P22 Toxoplasma gondii antigens abbreviate regions to diagnose acquired toxoplasmosis during pregnancy: toward single-sample assays. Clin Chem Lab Med. 2017; 55(4):595-604.
42. Teimouri A, Modarressi MH, Shojaee S, et al. Development, optimization, and validation of an in-house Dot-ELISA rapid test based on SAG1 and GRA7 proteins for serological detection of Toxoplasma gondii infections. Infect Drug Resist. 2019:2657-2669.
43. Teimouri A, Abbaszadeh Afshar MJ, Mohtasebi S, et al. Assessment of an in-house enzyme-linked immunosorbent assay and IgG avidity test based on SAG1 and GRA7 proteins for discriminating between acute and chronic toxoplasmosis in humans. J Clin Microbiol. 2021; 59(8): e0041621.
44. Dai J, Jiang M, Wang Y, et al. Evaluation of a recombinant multiepitope peptide for serodiagnosis of Toxoplasma gondii infection. Clin Vaccine Immunol. 2012; 19(3):338-342.
45. Dai J-f, Jiang M, Qu L-l, et al. Toxoplasma gondii: enzyme-linked immunosorbent assay based on a recombinant multi-epitope peptide for distinguishing recent from past infection in human sera. Exp Parasitol. 2013; 133(1):95-100.
46. Mahinc C, Flori P, Delaunay E, et al. Evaluation of a new immunochromatography technology test (LDBio Diagnostics) to detect Toxoplasma gondii IgG and IgM: comparison with the routine architect technique. J Clin Microbiol. 2017; 55(12):3395-3404.
47. Gomez CA, Budvytyte LN, Press C, et al. Evaluation of three point-of-care tests for detection of Toxoplasma gondii immunoglobulin IgG and IgM in the United States: proof of concept and challenges. Open Forum Infect Dis. 2018; 5(10): ofy215.
48. Molaei S, Dadkhah M, Fathi F. Toxoplasmosis diagnostic techniques: Current developed methods and biosensors. Talanta. 2023; 252:123828.
49. Prakrankamanant P. Quartz crystal microbalance biosensors: Prospects for point-of-care diagnostics. J Med Assoc Thai. 2014; 97 Suppl 4:S56-64.
50. Cho I-H, Kim DH, Park S. Electrochemical biosensors: Perspective on functional nanomaterials for on-site analysis. Biomater Res. 2020; 24:6.
51. Jiang S, Pu Q, Zhu W, et al. Modeling Analysis and Performance Study of Toxoplasma gondii IgM Antibody Immunosensor Based on Graphene and Au–Fe3O4. J Nanoelectronics Optoelectron. 2020; 15(3):353-360.
52. Takara EA, Pereira SV, Scala-Benuzzi ML, et al. Novel electrochemical sensing platform based on a nanocomposite of PVA/PVP/RGO applied to IgG anti-Toxoplasma gondii antibodies quantitation. Talanta. 2019; 195:699-705.
53. Alves LM, Rodovalho VR, Castro AC, et al. Development of direct assays for Toxoplasma gondii and its use in genomic DNA sample. J Pharm Biomed Anal. 2017; 145:838-844.
54. Hu R-S, He J-J, Elsheikha HM, et al. Differential brain microRNA expression profiles after acute and chronic infection of mice with Toxoplasma gondii oocysts. Front Microbiol. 2018; 9:2316.
55. Jia B, Chang Z, Wei X, et al. Plasma microRNAs are promising novel biomarkers for the early detection of Toxoplasma gondii infection. Parasit Vectors. 2014; 7:433.
56. Xu M, Zhou D, Huang S, et al. Comparative characterization of microRNA profiles of different genotypes of Toxoplasma gondii. Parasitology. 2013; 140(9):1111-1118.
57. Zouei N, Dalimi A, Pirestani M, Ghaffarifar F. Assessment of tissue levels of miR-146a and proinflammatory cytokines in experimental cerebral toxoplasmosis following atovaquone and clindamycin treatment: An in vivo study. Microb Pathog. 2023;184:106340.
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| Files | ||
| Issue | Vol 19 No 4 (2024) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i4.17159 | |
| Keywords | ||
| Toxoplasma gondii Pregnancy Congenital toxoplas-mosis Serological assays Molecular diagnostics | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Teimouri A, Mahmoudi S, Behkar A, Sahebi K, Foroozand H, Hassanpour G, Keshavarz H. Current and Emerging Techniques for Diagnosis of Toxoplasmosis in Pregnancy: A Narrative Review. Iran J Parasitol. 2024;19(4):384-396.
