Serological Evaluation and Molecular Genotyping of Toxoplasma gondii in Pregnant Women in Meshkin-Shahr District, Northwestern Iran
-
Shabnam Asfaram
,
Zabih Zarei
,
Roghayeh Teimoorpour
,
Zahra Heidari
,
Sohrab Iranpour
,
Payman Azghani
,
Seyed Eghbal Motavallibashi
,
Zahra Rakhshidan
,
Zahra Khademi
,
Behnam Mohammadi-Ghalehbin
,
Shahram Habibzadeh
,
Soheila Molaie
Abstract
Background: We aimed to investigate the serological and molecular characteristics of Toxoplasma gondii infection among pregnant women and their aborted placentas in Meshkin-Shahr City during 2019-2020.
Methods: Blood samples of 210 pregnant women were evaluated for anti-T. gondii antibodies and related risk factors were determined. Also, the sera of aborted women and their buffy coats and aborted placenta tissues were used to detect anti-Toxoplasma antibodies and the parasite’s DNA, respectively. The parasite genotypes were determined by the PCR-RFLP using the SAG3 gene.
Results: The overall prevalence of anti-Toxoplasma IgG was 24.3% and only 1% of participants were seropositive for the IgM antibody. There was a significant relationship between raw or unwashed vegetable consumption, contact with soil, vegetable/fruit washing type, and seropositivity (P<0.05). During pregnancy, 4.7% of women encountered an abortion and 30% and 50% of cases were positive for IgG antibodies before and after abortion, respectively. Only two cases were IgM seropositive after abortion. In the avidity IgG test, 20% of cases showed low avidity. BLAST and phylogenetic analysis exhibited that all isolates belonged to the type III T. gondii genotype. Although two women with spontaneous abortions showed seropositivity for IgM T. gondii antibody, parasite DNA was detected in three cases.
Conclusion: The seroprevalence of Toxoplasma infection is not high in pregnant women. Seropositive women are not safe from congenital transmission. T. gondii type III is the etiology of fetus infection in mothers with spontaneous abortion. It seems that screening and essential care are still necessary during pregnancy.
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2. World Health Organization (WHO). Multicriteria-based ranking for risk management of food-borne parasites. Microbiological Risk Assessment Series, 23.2014.
3. Shapiro K, Bahia-Oliveira L, Dixon B, et al. Environmental transmission of Toxoplasma gondii: Oocysts in water, soil, and food. Food Waterborne Parasitol. 2019;15:e00049.
4. Hussain MA, Stitt V, Szabo EA, et al. Toxoplasma gondii in the Food Supply. Pathogens. 2017;6(2):21.
5. Norrby SR, Whitley RJ. Evaluation of new anti-infective drugs for the treatment of infection with human immunodeficiency virus. Clin Infect Dis. 1993;17(4):794-801.
6. Berthélémy S. Toxoplasmosis and pregnancy. Actual Pharm. 2014;53(541):43-5.
7. Campero LM, Schott F, Gottstein B, et al. Detection of antibodies to Toxoplasma gondii in oral fluid from pigs. Int J Parasitol. 2020;50(5):349-355.
8. Alghamdi AJ, Alabbas A, Tadla M, et al. Is congenital toxoplasmosis still an important clinical problem? J Pre-Clin Clin Res. 2017;11(2):167-170.
9. Robert-Gangneux F, Dardé ML. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012;25(2):264-296.
10. Fisch D, Clough B, Frickel EM. Human immunity to Toxoplasma gondii. PLoS Pathog. 2019;15(12):e1008097.
11. MR CN, Shemshadi B, Shayan P, et al. Serological determination of Toxoplasma gondii among sheep (ovis aries) in Guilan Province, Iran. Arch Razi Inst. 2021;75(4):463-471.
12. Rozental AJ, Partnow AB, Shomper JL, et al. What Is Your Neurologic Diagnosis? J Am Vet Med Assoc. 2020;256(7):771-774.
13. Piccolo FL, Busch K, Palić J, et al. Toxoplasma gondii-associated cholecystitis in a cat receiving immunosuppressive treatment. Tierarztl Prax Ausg K Kleintiere Heimtiere. 2019;47(6):453-457.
14. Nayeri T, Sarvi S, Moosazadeh M, et al. The global seroprevalence of anti-Toxoplasma gondii antibodies in women who had spontaneous abortion: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2020;14(3):e0008103.
15. Kalantari N, Gorgani-Firouzjaee T, Moulana Z, et al. Toxoplasma gondii infection and spontaneous abortion: A systematic review and meta-analysis. Microb Pathog. 2021;158:105070.
16. Khademi SZ, Ghaffarifar F, Dalimi A, et al. Spontaneous abortion among Toxoplasma gondii IgG seropositive women: molecular detection, genotype identification, and serological assessment with conventional ELISA and avidity ELISA. J Obstet Gynaecol Res. 2022;48(10):2479-2485.
17. Borna S, Shariat M, Fallahi M, et al. Prevalence of immunity to toxoplasmosis among Iranian childbearing age women: Systematic review and meta-analysis. Iran J Reprod Med. 2013;11(11):861-868.
18. 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.
19. Homan WL, Vercammen M, De Braekeleer J, et al. Identification of a 200-to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. Int J Parasitol. 2000;30(1):69-75.
20. Grigg ME, Ganatra J, Boothroyd JC, et al. Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J Infect Dis. 2001; 184(5):633-639.
21. Su C, Shwab EK, Zhou P, et al. Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology. 2010; 137(1):1-11.
22. Hall T, Biosciences I, Carlsbad CJ. BioEdit: an important software for molecular biology. Bull Biosci. 2011;2(1):60-61.
23. Kazemi F, Arjmand R, Dousti M, et al. Toxoplasma and risk of spontaneous abortion: a meta-analysis in a population of Iranian women. Int J Fertil Steril. 2023;17(1):7-11.
24. Saeedi M, Veghari GR, Marjani A. Seroepidemiologic evaluation of anti-Toxoplasma antibodies among women in the north of Iran. Pak J Biol Sci. 2007;10(14):2359-2362.
25. Abdi J, Shojaee S, Mirzaee A, Keshavarz H. Seroprevalence of toxoplasmosis in pregnant women in Ilam province, Iran. Iran J Parasitol. 2008;3(2):34-7.
26. Hajsoleimani F, Ataeian A, Nourian AA, et al. Seroprevalence of Toxoplasma gondii in pregnant women and bioassay of IgM positive cases in Zanjan, Northwest of Iran. Iran J Parasitol. 2012;7(2):82-86.
27. Hariri SS, Heidari Z, Habibzadeh S, et al. Seroprevalence of Toxoplasma gondii among Pregnant Women in Ardabil, Iran (2021–2022). Iran J Parasitol. 2023;18(1):93-99.
28. Shahighi M, Heidari A, Keshavarz H, et al. Seroepidemiological study of toxoplasmosis in women referred to a pre-marriage counseling center in Alborz Province, Iran. BMC Research Notes. 2021;14:163.
29. Mohammadi A, Shojaee S, Salimi M, et al. Seroepidemiological study of toxoplasmosis in women referred to arak marriage consulting center during 2012–2013. Iran J Public Health. 2015;44(5):654 –658.
30. Simon L, Trastour C, Soler A, et al. A case of congenital toxoplasmosis-associated miscarriage with maternal infection four months prior to conception. Parasitol Int. 2020;79:102165.
31. Ali-Heydari S, Keshavarz H, Shojaee S, Mohebali M. Diagnosis of antigenic markers of acute toxoplasmosis by IgG avidity immunoblotting. Parasite. 2013; 20:18.
32. 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.
33. Sharifi K, Farash BR, Fatemeh TA, et al. Diagnosis of acute toxoplasmosis by IgG and IgM antibodies and IgG avidity in pregnant women from Mashhad, Eastern Iran. Iran J Parasitol. 2019;14(4):639–645.
34. Rahbari AH, Keshavarz H, Shojaee S, et al. IgG avidity ELISA test for diagnosis of acute toxoplasmosis in humans. Korean J Parasitol. 2012;50(2):99–102.
35. Faral-Tello P, Pagotto R, Bollati-Fogolín M, et al. Modeling the human placental barrier to understand Toxoplasma gondii´s vertical transmission. Front Cell Infect Microbiol. 2023;13:1130901.
36. Kaňková Š, Flegr J. Longer pregnancy and slower fetal development in women with latent" asymptomatic" toxoplasmosis. BMC Infect Dis. 2007;7:114.
37. Kaňková Š, Šulc J, Křivohlavá R, et al. Slower postnatal motor development in infants of mothers with latent toxoplasmosis during the first 18 months of life. Early Hum Dev. 2012;88(11):879-884.
38. El-Tantawy N, Taman A, Shalaby H. Toxoplasmosis and female infertility: is there a correlation. Am J Epidemiol Infect Dis. 2014;2(1):29-32.
39. Malik A, Rizvi M, Khan F, et al. Toxoplasma gondii in women with bad obstetric history and infertility: a five-year study. Asian Pac J Trop Dis. 2014;4 Supple 1:S236-S239.
40. Hoveyda L, Shanehsazzadeh M, Behbahani M. Toxoplasmosis in Iranian abortion cases with appendectomy. J Appl Biol Sci. 2012;6(2):31-36.
41. Zia-Ali N, Fazaeli A, Khoramizadeh M, et al. Isolation and molecular characterization of Toxoplasma gondii strains from different hosts in Iran. Parasitol Res. 2007;101:111-115.
42. Sibley LD, Khan A, Ajioka JW, Rosenthal BM. Genetic diversity of Toxoplasma gondii in animals and humans. Philos Trans R Soc Lond B Biol Sci. 2009;364(1530):2749-2761.
43. Shwab EK, Zhu XQ, Majumdar D, et al. Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology. 2014;141(4):453-461.
44. Tavalla M, Oormazdi H, Akhlaghi L, et al. Genotyping of Toxoplasma gondii isolates from soil samples in Tehran, Iran. Iran J Parasitol. 2013;8(2):227–233.
45. Danehchin L, Razmi G, Naghibi A. Isolation and genotyping of Toxoplasma gondii strains in ovine aborted fetuses in Khorasan Razavi Province, Iran. Korean J Parasitol. 2016;54(1):15-20
46. Saki J, Khademvatan S, Yousefi E, et al. Detection and genotyping of Toxoplasma gondii isolated from soil in Ahvaz, southwest of Iran. J Parasit Dis. 2017;41:202-205.
47. Xiao J, Yolken RH. Strain hypothesis of Toxoplasma gondii infection on the outcome of human diseases. Acta Physiol (Oxf). 2015;213(4):828-845.
48. Asgari Q, Fekri M, Monabati A, et al. Molecular genotyping of Toxoplasma gondii in human spontaneous aborted fetuses in Shiraz, Southern Iran. Iran J Public Health. 2013;42(6):620-625.
49. Ajzenberg D, Cogné N, Paris L, et al. Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J Infect Dis. 2002;186(5):684-689.
50. Messaritakis I, Detsika M, Koliou M, Sifakis S, Antoniou M. Prevalent genotypes of Toxoplasma gondii in pregnant women and patients from Crete and Cyprus. Am J Trop Med Hyg. 2008;79(2):205-209.
51. Elbez-Rubinstein A, Ajzenberg D, Dardé ML, et al. Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J Infect Dis. 2009;199(2):280-285.
52. Sadeghi M, Hosseini SA, Sarvi S, et al. More than Seventy Years of Research (1948–November 2021) on Toxoplasma gondii in Iran: A Narrative Review. Iran J Parasitol. 2022;17(2):124-137.
2. World Health Organization (WHO). Multicriteria-based ranking for risk management of food-borne parasites. Microbiological Risk Assessment Series, 23.2014.
3. Shapiro K, Bahia-Oliveira L, Dixon B, et al. Environmental transmission of Toxoplasma gondii: Oocysts in water, soil, and food. Food Waterborne Parasitol. 2019;15:e00049.
4. Hussain MA, Stitt V, Szabo EA, et al. Toxoplasma gondii in the Food Supply. Pathogens. 2017;6(2):21.
5. Norrby SR, Whitley RJ. Evaluation of new anti-infective drugs for the treatment of infection with human immunodeficiency virus. Clin Infect Dis. 1993;17(4):794-801.
6. Berthélémy S. Toxoplasmosis and pregnancy. Actual Pharm. 2014;53(541):43-5.
7. Campero LM, Schott F, Gottstein B, et al. Detection of antibodies to Toxoplasma gondii in oral fluid from pigs. Int J Parasitol. 2020;50(5):349-355.
8. Alghamdi AJ, Alabbas A, Tadla M, et al. Is congenital toxoplasmosis still an important clinical problem? J Pre-Clin Clin Res. 2017;11(2):167-170.
9. Robert-Gangneux F, Dardé ML. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012;25(2):264-296.
10. Fisch D, Clough B, Frickel EM. Human immunity to Toxoplasma gondii. PLoS Pathog. 2019;15(12):e1008097.
11. MR CN, Shemshadi B, Shayan P, et al. Serological determination of Toxoplasma gondii among sheep (ovis aries) in Guilan Province, Iran. Arch Razi Inst. 2021;75(4):463-471.
12. Rozental AJ, Partnow AB, Shomper JL, et al. What Is Your Neurologic Diagnosis? J Am Vet Med Assoc. 2020;256(7):771-774.
13. Piccolo FL, Busch K, Palić J, et al. Toxoplasma gondii-associated cholecystitis in a cat receiving immunosuppressive treatment. Tierarztl Prax Ausg K Kleintiere Heimtiere. 2019;47(6):453-457.
14. Nayeri T, Sarvi S, Moosazadeh M, et al. The global seroprevalence of anti-Toxoplasma gondii antibodies in women who had spontaneous abortion: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2020;14(3):e0008103.
15. Kalantari N, Gorgani-Firouzjaee T, Moulana Z, et al. Toxoplasma gondii infection and spontaneous abortion: A systematic review and meta-analysis. Microb Pathog. 2021;158:105070.
16. Khademi SZ, Ghaffarifar F, Dalimi A, et al. Spontaneous abortion among Toxoplasma gondii IgG seropositive women: molecular detection, genotype identification, and serological assessment with conventional ELISA and avidity ELISA. J Obstet Gynaecol Res. 2022;48(10):2479-2485.
17. Borna S, Shariat M, Fallahi M, et al. Prevalence of immunity to toxoplasmosis among Iranian childbearing age women: Systematic review and meta-analysis. Iran J Reprod Med. 2013;11(11):861-868.
18. 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.
19. Homan WL, Vercammen M, De Braekeleer J, et al. Identification of a 200-to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. Int J Parasitol. 2000;30(1):69-75.
20. Grigg ME, Ganatra J, Boothroyd JC, et al. Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J Infect Dis. 2001; 184(5):633-639.
21. Su C, Shwab EK, Zhou P, et al. Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology. 2010; 137(1):1-11.
22. Hall T, Biosciences I, Carlsbad CJ. BioEdit: an important software for molecular biology. Bull Biosci. 2011;2(1):60-61.
23. Kazemi F, Arjmand R, Dousti M, et al. Toxoplasma and risk of spontaneous abortion: a meta-analysis in a population of Iranian women. Int J Fertil Steril. 2023;17(1):7-11.
24. Saeedi M, Veghari GR, Marjani A. Seroepidemiologic evaluation of anti-Toxoplasma antibodies among women in the north of Iran. Pak J Biol Sci. 2007;10(14):2359-2362.
25. Abdi J, Shojaee S, Mirzaee A, Keshavarz H. Seroprevalence of toxoplasmosis in pregnant women in Ilam province, Iran. Iran J Parasitol. 2008;3(2):34-7.
26. Hajsoleimani F, Ataeian A, Nourian AA, et al. Seroprevalence of Toxoplasma gondii in pregnant women and bioassay of IgM positive cases in Zanjan, Northwest of Iran. Iran J Parasitol. 2012;7(2):82-86.
27. Hariri SS, Heidari Z, Habibzadeh S, et al. Seroprevalence of Toxoplasma gondii among Pregnant Women in Ardabil, Iran (2021–2022). Iran J Parasitol. 2023;18(1):93-99.
28. Shahighi M, Heidari A, Keshavarz H, et al. Seroepidemiological study of toxoplasmosis in women referred to a pre-marriage counseling center in Alborz Province, Iran. BMC Research Notes. 2021;14:163.
29. Mohammadi A, Shojaee S, Salimi M, et al. Seroepidemiological study of toxoplasmosis in women referred to arak marriage consulting center during 2012–2013. Iran J Public Health. 2015;44(5):654 –658.
30. Simon L, Trastour C, Soler A, et al. A case of congenital toxoplasmosis-associated miscarriage with maternal infection four months prior to conception. Parasitol Int. 2020;79:102165.
31. Ali-Heydari S, Keshavarz H, Shojaee S, Mohebali M. Diagnosis of antigenic markers of acute toxoplasmosis by IgG avidity immunoblotting. Parasite. 2013; 20:18.
32. 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.
33. Sharifi K, Farash BR, Fatemeh TA, et al. Diagnosis of acute toxoplasmosis by IgG and IgM antibodies and IgG avidity in pregnant women from Mashhad, Eastern Iran. Iran J Parasitol. 2019;14(4):639–645.
34. Rahbari AH, Keshavarz H, Shojaee S, et al. IgG avidity ELISA test for diagnosis of acute toxoplasmosis in humans. Korean J Parasitol. 2012;50(2):99–102.
35. Faral-Tello P, Pagotto R, Bollati-Fogolín M, et al. Modeling the human placental barrier to understand Toxoplasma gondii´s vertical transmission. Front Cell Infect Microbiol. 2023;13:1130901.
36. Kaňková Š, Flegr J. Longer pregnancy and slower fetal development in women with latent" asymptomatic" toxoplasmosis. BMC Infect Dis. 2007;7:114.
37. Kaňková Š, Šulc J, Křivohlavá R, et al. Slower postnatal motor development in infants of mothers with latent toxoplasmosis during the first 18 months of life. Early Hum Dev. 2012;88(11):879-884.
38. El-Tantawy N, Taman A, Shalaby H. Toxoplasmosis and female infertility: is there a correlation. Am J Epidemiol Infect Dis. 2014;2(1):29-32.
39. Malik A, Rizvi M, Khan F, et al. Toxoplasma gondii in women with bad obstetric history and infertility: a five-year study. Asian Pac J Trop Dis. 2014;4 Supple 1:S236-S239.
40. Hoveyda L, Shanehsazzadeh M, Behbahani M. Toxoplasmosis in Iranian abortion cases with appendectomy. J Appl Biol Sci. 2012;6(2):31-36.
41. Zia-Ali N, Fazaeli A, Khoramizadeh M, et al. Isolation and molecular characterization of Toxoplasma gondii strains from different hosts in Iran. Parasitol Res. 2007;101:111-115.
42. Sibley LD, Khan A, Ajioka JW, Rosenthal BM. Genetic diversity of Toxoplasma gondii in animals and humans. Philos Trans R Soc Lond B Biol Sci. 2009;364(1530):2749-2761.
43. Shwab EK, Zhu XQ, Majumdar D, et al. Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology. 2014;141(4):453-461.
44. Tavalla M, Oormazdi H, Akhlaghi L, et al. Genotyping of Toxoplasma gondii isolates from soil samples in Tehran, Iran. Iran J Parasitol. 2013;8(2):227–233.
45. Danehchin L, Razmi G, Naghibi A. Isolation and genotyping of Toxoplasma gondii strains in ovine aborted fetuses in Khorasan Razavi Province, Iran. Korean J Parasitol. 2016;54(1):15-20
46. Saki J, Khademvatan S, Yousefi E, et al. Detection and genotyping of Toxoplasma gondii isolated from soil in Ahvaz, southwest of Iran. J Parasit Dis. 2017;41:202-205.
47. Xiao J, Yolken RH. Strain hypothesis of Toxoplasma gondii infection on the outcome of human diseases. Acta Physiol (Oxf). 2015;213(4):828-845.
48. Asgari Q, Fekri M, Monabati A, et al. Molecular genotyping of Toxoplasma gondii in human spontaneous aborted fetuses in Shiraz, Southern Iran. Iran J Public Health. 2013;42(6):620-625.
49. Ajzenberg D, Cogné N, Paris L, et al. Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J Infect Dis. 2002;186(5):684-689.
50. Messaritakis I, Detsika M, Koliou M, Sifakis S, Antoniou M. Prevalent genotypes of Toxoplasma gondii in pregnant women and patients from Crete and Cyprus. Am J Trop Med Hyg. 2008;79(2):205-209.
51. Elbez-Rubinstein A, Ajzenberg D, Dardé ML, et al. Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J Infect Dis. 2009;199(2):280-285.
52. Sadeghi M, Hosseini SA, Sarvi S, et al. More than Seventy Years of Research (1948–November 2021) on Toxoplasma gondii in Iran: A Narrative Review. Iran J Parasitol. 2022;17(2):124-137.
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| Toxoplasma gondii Pregnant women Abortion Seroprevalence Genotype Iran | ||
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How to Cite
1.
Asfaram S, Zarei Z, Teimoorpour R, Heidari Z, Iranpour S, Azghani P, Motavallibashi SE, Rakhshidan Z, Khademi Z, Mohammadi-Ghalehbin B, Habibzadeh S, Molaie S. Serological Evaluation and Molecular Genotyping of Toxoplasma gondii in Pregnant Women in Meshkin-Shahr District, Northwestern Iran. Iran J Parasitol. 2025;20(1):44-53.
