Evaluation of Toxoplasma gondii, CMV, and Rubella Seropositivity and Avidity Tests in the First Trimester of Pregnancy: Why to Test?

Year 2023, , 174 - 182, 25.10.2023

Ayşe Rüveyda Uğur , Ümmügülsüm Esenkaya , Oğuzhan Günenc

https://doi.org/10.34084/bshr.1361444

Abstract

Objective: The influence of intrauterine and perinatal infections on fetal and neonatal mortality rates and childhood morbidity is substantial. Toxoplasmosis gondii, cytomegalovirus (CMV), and rubella are widely recognized as the major causative agents of in utero infection. The surveillance of preventable and treatable diseases within populations at risk are crucial for public health. The objective of this study is to investigate the seropositivity rates and avidity incidences of T. gondii, CMV, and rubella in pregnant women during the first trimester.
Methods: The electrochemiluminescence immunoassay method (Elecsys, Roche, Germany) was employed for the detection of the anti-Toxo IgM, anti-Toxo IgG, anti-CMV IgM, anti-CMV IgG, anti-rubella IgM, and anti-rubella IgG during the time period of January 1, 2021, to June 15, 2023. The anti-Toxo IgG, anti-CMV, and anti-rubella IgG avidity tests were performed with the enzyme-linked fluorescent assay method (VIDAS, bioMérieux, France).
Results: The T. gondii IgM incidance was 2.1%; and the T. gondii IgG seroprevalance was 22%. For T. gondii, low avidity was observed in 13.6% (n = 31) of cases, while high avidity index was detected in 75.8% (n = 172) of cases. The anti-CMV IgM incidance was 1.6%; while IgG seroprevalance was 96.9%. The IgG avidity with a high index for CMV was determined as 99.4%. The anti-rubella IgM incidance was 0.8%; while the IgG seroprevalance was found to be 98.7%. The IgG avidity with a high index for Rubella was 99.1%.
Conclusion: Seroprevalance of T.gondii, CMV, and rubella may vary according to geographical and socioeconomic conditions. Treatment for T. gondii diagnosed during pregnancy, preventive behavioral measures for CMV and vaccination against rubella prior to pregnancy may help reduce congenital infections. The prioritization of T. gondii, CMV, and rubella screening in high-risk populations, including women of reproductive age and pregnant women, is crucial for public health.

Keywords

Toxoplasma gondii, CMV, rubella, Serology, pregnancy, congenital infection

Ethical Statement

The study was approved by the Ethics Board of the Faculty of Medicine of the University of Karatay, KTO, for drug and non-medical device research (Decree no. 2023/024).

Gebeliğin İlk Üç Ayında Toxoplasma gondii, CMV ve Rubella Seropozitifliği ve Avidite Testlerinin Değerlendirilmesi: Neden Test Etmeli?

Abstract

References

• 1. Ostrander B, Bale JF. Congenital and perinatal infections. Handb Clin Neurol 2019; 162: 133-153. doi: 10.1016/B978-0-444-64029-1.00006-0.
• 2. Melchor SJ, Ewald SE. Disease Tolerance in Toxoplasma Infection. Front Cell Infect Microbiol 2019; 9: 185.
• 3. Cook AJ, Gilbert RE, Buffolano W, et al. Sources of toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. BMJ. 2000;321(7254):142-147. doi:10.1136/bmj.321.7254.142.
• 4. Montoya JG, Kovacs JA, Remington JS. Toxoplasma gondii. In: Mandell GL, Bennett JE, Dolin R, eds. Principles and Practice of Infectious Diseases. 6th ed. Philadelphia: Elsevier Churchill Livingstone, 2005:3170-198.
• 5. Robert-Gangneux F, Murat JB, Fricker-Hidalgo H, et al. The placenta: a main role in congenital toxoplasmosis? Trends Parasitol 2011; 27 :530.
• 6. McAuley JB. Congenital Toxoplasmosis. J Pediatric Infect Dis Soc 2014; 3 Suppl 1(Suppl 1): S30-5. doi: 10.1093/jpids/piu077.
• 7. Navti OB, Al-Belushi M, Konje JC; FRCOG. Cytomegalovirus infection in pregnancy - An update. Eur J Obstet Gynecol Reprod Biol. 2021;258:216-222. doi:10.1016/j.ejogrb.2020.12.006.
• 8. Nolan N, Halai UA, Regunath H, et al. Primary cytomegalovirus infection in immunocompetent adults in the United States - A case series. IDCases 2017; 10: 123-126. doi: 10.1016/j.idcr.2017.10.008.
• 9. Picone O, Vauloup-Fellous C, Cordier AG, et al. A series of 238 cytomegalovirus primary infections during pregnancy: description and outcome. Prenat Diagn 2013; 33: 751.
• 10. Raynor BD. Cytomegalovirus infection in pregnancy. Semin Perinatol 1993; 17: 394.
• 11. Marsico C, Kimberlin DW. Congenital Cytomegalovirus infection: advances and challenges in diagnosis, prevention and treatment. Ital J Pediatr 2017; 43(1): 38. doi: 10.1186/s13052-017-0358-8.
• 12. Society for Maternal-Fetal Medicine (SMFM), Hughes BL, Gyamfi-Bannerman C. Diagnosis and antenatal management of congenital cytomegalovirus infection. Am J Obstet Gynecol. 2016;214(6):B5-B11. doi:10.1016/j.ajog.2016.02.042.
• 13. Ornoy A, Diav-Citrin O. Fetal effects of primary and secondary cytomegalovirus infection in pregnancy. Reprod Toxicol 2006; 21: 399-409. https://doi.org/10.1016/j.reprotox.2005.02.002.
• 14. CDC. Rubella. In: Epidemiology and Prevention of Vaccine-Preventable Diseases, 14th Ed, Hall E, Wodi AP, Hamborsky J, et al. (Eds), Public Health Foundation, Washington, DC 2021.
• 15. Winter AK, Moss WJ. Rubella. Lancet. 2022; 399(10332): 1336-1346. doi: 10.1016/S0140-6736(21)02691-X.
• 16. Morgan-Capner P, Miller E, Vurdien JE, Ramsay ME. Outcome of pregnancy after maternal reinfection with rubella. CDR (Lond Engl Rev) 1991; 1: R57.
• 17. Sheridan E, Aitken C, Jeffries D, et al. Congenital rubella syndrome: a risk in immigrant populations. Lancet 2002; 359: 674.
• 18. Bukasa A, Campbell H, Brown K, et al. Rubella infection in pregnancy and congenital rubella in United Kingdom, 2003 to 2016. Euro Surveill 2018; 23.
• 19. SYROCOT (Systematic Review on Congenital Toxoplasmosis) study group, Thiébaut R, Leproust S, et al. Effectiveness of prenatal treatment for congenital toxoplasmosis: a meta-analysis of individual patients' data. Lancet 2007; 369: 115.
• 20. Gilbert R, Gras L; European Multicentre Study on Congenital Toxoplasmosis. Effect of timing and type of treatment on the risk of mother to child transmission of Toxoplasma gondii. BJOG. 2003; 110(2): 112-120. doi:10.1016/s1470-0328(02)02325-x.
• 21. Prusa AR, Kasper DC, Sawers L, et al. Congenital toxoplasmosis in Austria: Prenatal screening for prevention is cost-saving. PLoS Negl Trop Dis 2017; 11:e0005648.
• 22. Maldonado YA, Read JS, COMMITTEE ON INFECTIOUS DISEASES. Diagnosis, Treatment, and Prevention of Congenital Toxoplasmosis in the United States. Pediatrics 2017; 139.
• 23. Guerina NG, Hsu HW, Meissner HC, et al. Neonatal serologic screening and early treatment for congenital Toxoplasma gondii infection. The New England Regional Toxoplasma Working Group. N Engl J Med 1994; 330: 1858.
• 24. Varol FG, Sayın NC, Soysüren S. Trakya yöresinde antenatal bakım alan gebelerde Toxoplasma gondii antikor seroprevalansı. J Turk Soc Obstet Gynecol 2011; 8(2): 93-9.
• 25. Gonca S, Serin MS, Halepliler S, Erden Ertürk S. Mersin’de bir devlet hastanesine başvuran gebelerde Toxoplasma gondii seroprevalansı, 2019. Turkiye Parazitol Derg 2021; 45(3): 176-80.
• 26. Miman Ö, Altındiş M, Er H, Aktepe O.C. Toxoplasmosis Ön Tanılı Hastalarda Seropozitiflik Oranlarımız: Afyon Deneyimi. KTD 2009; 10(1): 59-61.
• 27. Alaçam S, Bakır A, Karatas A, et al. Investigation of seroprevalence of Toxoplasma gondii, rubella and cytomegalovirus in pregnant population in Istanbul. JAMER 2020; 5(3): 19-24.
• 28. Ezer B, Kaya H, Kılıç F, Özdemir M, Kaba K. Konya ili Meram Tıp Fakültesi Hastanesi’ne başvuran hamilelerde Enzyme Linked Fluorescent Assay yöntemiyle tespit edilen Toxoplasma gondii, Rubella, Sitomegalovirüs seroprevalansı. Turk Mikrobiyol Cemiy Derg 2023; 53(1): 28-34.
• 29. Harma M, Harma M, Gungen N, et al. Toxoplasmosis in pregnant women in Sanliurfa, Southeastern Anatolia City, Turkey. J Egypt Soc Parasitol 2004; 34(2): 519-25.
• 30. Aynioglu A, Aynioglu O, Altunok ES. Seroprevalence of Toxoplasma gondii, rubella and cytomegalovirus among pregnant females in north-western Turkey Acta Clin Belg 2015; 70(5): 321-4.
• 31. Yazar S, Yaman O, Şahin İ. Toxoplasma gondii Seropozitif Gebelerde IgG-Avidite Sonuçlarının Değerlendirilmesi. Turkiye Parazitol Derg 2005; 29 (4): 221-223.
• 32. Güngör S , Aksoy Gökmen A, Uzun B, et al. Evaluation of the Toxoplasma gondii IgG Avidity request and results in a tertiary care hospital. J Clin Exp Invest 2014; 5 (2): 246-249.
• 33. Durdu B, Mutlu M. Sağlıklı Gebelerde Toksoplazma Seroprevelansı ve IgG Avidite Değerlerinin İncelenmesi Bakırköy Tıp Derg 2017; 13: 140-144.
• 34. Gilbert RE, Peckham CS. Congenital toxoplasmosis in the United Kingdom: to screen or not to screen? J Med Screen 2002; 9:135.
• 35. American College of Obstetricians and Gynecologists. Practice bulletin no. 151: Cytomegalovirus, parvovirus B19, varicella zoster, and toxoplasmosis in pregnancy. Obstet Gynecol 2015; 125:1510. Reaffirmed 2019.
• 36. Paquet C, Yudin MH, Society of Obstetricians and Gynaecologists of Canada. Toxoplasmosis in pregnancy: prevention, screening, and treatment. J Obstet Gynaecol Can 2013; 35: 78.
• 37. Picone O, Fuchs F, Benoist G, et al. Toxoplasmosis screening during pregnancy in France: Opinion of an expert panel for the CNGOF. J Gynecol Obstet Hum Reprod 2020; 49:101814.
• 38. Gras L, Gilbert RE, 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: 541.
• 39. Villard O, Breit L, Cimon B, et al. Comparison of four commercially available avidity tests for Toxoplasma gondii-specific IgG antibodies. Clin Vaccine Immunol 2013; 20:197.
• 40. Lefevre-Pettazzoni M, Le Cam S, Wallon M, Peyron F. Delayed maturation of immunoglobulin G avidity: implication for the diagnosis of toxoplasmosis in pregnant women. Eur J Clin Microbiol Infect Dis 2006; 25:687.
• 41. Zuhair M, Smit GSA, Wallis G, et al. Estimation of the worldwide seroprevalence of cytomegalovirus: A systematic review and meta-analysis. Rev Med Virol 2019; 29:e2034.
• 42. Alain S, Garnier-Geoffroy F, Labrunie A, et al. Cytomegalovirus (CMV) Shedding in French Day-Care Centers: A Nationwide Study of Epidemiology, Risk Factors, Centers' Practices, and Parents' Awareness of CMV. J Pediatric Infect Dis Soc 2020; 9: 686.
• 43. Adler SP, Finney JW, Manganello AM, Best AM. Prevention of child-to-mother transmission of cytomegalovirus among pregnant women. J Pediatr 2004; 145:485.
• 44. Tanimura K, Tairaku S, Morioka I, et al. Universal Screening With Use of Immunoglobulin G Avidity for Congenital Cytomegalovirus Infection. Clin Infect Dis 2017; 65: 1652.
• 45. Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 2010; 20: 202.
• 46. Hyde TB, Schmid DS, Cannon MJ. Cytomegalovirus seroconversion rates and risk factors: implications for congenital CMV. Rev Med Virol 2010; 20: 311.
• 47. Fowler K, Mucha J, Neumann M, et al. A systematic literature review of the global seroprevalence of cytomegalovirus: possible implications for treatment, screening, and vaccine development. BMC Public Health 2022; 22(1): 1659. doi: 10.1186/s12889-022-13971-7.
• 48. Çetinkaya RA. Gebelerde sitomegalovirüs seroprevalansı ve Türkiye’nin dünyadaki seroepidemiyolojik durumu; Bir meta-analiz araştırması. Flora 2019; 24(2): 119-30. https://doi.org/10.5578/flora.67722.
• 49. Özdemir M, Esenkaya Taşbent F, Terzi HA, et al. Seroprevalence of Major Viral Pathogens during Pregnancy: A Multicenter Study in Turkey. Adv ClinMed Microbiol 2016; 1: 001.
• 50. Peker BO, Müderris T, Yurtsever SG, Kaya S. Seroprevalence of Cytomegalovirus (CMV) IgG and IgM Antibodies in Pregnant Women in Izmir: An Analysis of CMV IgG Avidity Tests.Turk Mikrobiyol Cemiy Derg 2022; 52(1): 56-62.
• 51. Gürbüz E, Baran Aİ. Comparison of Rubella, Cytomegalovirus, Toxoplasma Gondii Seroprevalence, Still Birth and Preterm Birth Rates In Pregnant Patients Admitted To Our Hospital, Igg Avidity In Igg Positive Patients. Van Tıp Derg 2021; 28(2): 300-306. DOI: 10.5505/vtd.2021.54036.
• 52. Gülseren YD, Esenkaya Taşbent F, Özdemir M. Investigation of Cytomegalovirus and Rubella Seroprevalence and Age Related Distribution in Pregnant Women. Türk Mikrobiyoloji Cem Derg 2019; 49(3): 154-161.
• 53. Louie JK, Shaikh-Laskos R, Preas C, et al. Re-emergence of another vaccine-preventable disease?-Two cases of rubella in older adults. J Clin Virol 2009; 46: 98.
• 54. Grant GB, Desai S, Dumolard L, et al. Progress Toward Rubella and Congenital Rubella Syndrome Control and Elimination - Worldwide, 2000-2018. MMWR Morb Mortal Wkly Rep 2019; 68:855.
• 55. McElroy R, Laskin M, Jiang D, et al. Rates of rubella immunity among immigrant and non-immigrant pregnant women. J Obstet Gynaecol Can 2009; 31:4 09.
• 56. Zipprich J, Winter K, Hacker J, Xia D, Watt J, Harriman K. Centers for Disease Control and Prevention (CDC), Measles outbreak - California, December 2014- February 2015. MMWR Morb Mortal Wkly Rep 2015; 64(6): 153-4. 57. Best JM, O'Shea S, Tipples G, et al. Interpretation of rubella serology in pregnancy--pitfalls and problems. BMJ 2002; 325:147.
• 58. Agbede OO, Adeyemi OO, Olatinwo AW. Significance of IgG-Avidity in Antenatal Rubella Diagnosis. J Family Reprod Health 2013; 7(3):131-7.
• 59. Şentürk Ş, Kağıtcı M, Balık G, Şahin K, Kır Şahin F. Seroprevalence of Rubella Virus among Pregnant Women in Eastern Black Sea Region. Van Tıp Derg 2016; 23(3): 242-245.
• 60. Uzun B, Güngör S, Er H, Gökmen A, Pektaş B, Şener AG. The evaluation of rubella and sitomegalovirus IgG avidity tests in pregnants: four-year experience. J Clin Exp Invest 2014; 5 (3): 420-423.