Simultaneous Seroprevalence to Toxoplasma gondii, Cytomegalovirus and Rubella Virus in Childbearing Women from Western Romania
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design
2.2. Setting
2.3. Participants
2.4. Laboratory Analysis
2.5. Statistical Methods
2.6. Ethical Issues
3. Results
3.1. Demographic Features of Participants
3.2. Prevalence of IgG and IgM Antibodies against a Single Pathogen: 2008–2010 vs. 2015–2018
3.3. Simultaneous IgG Seroprevalence against Two or Three Pathogens in Women from Urban and Rural Areas: 2008–2010 vs. 2015–2018
3.4. Simultaneous Susceptibility to Two or Three Pathogens in Women from Urban and Rural Areas: 2008–2010 vs. 2015–2018
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Jaan, A.; Rajnik, M. TORCH Complex. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2021. [Google Scholar]
- Fallahi, S.; Rostami, A.; Shiadeh, M.N.; Behniafar, H.; Paktinat, S. An updated literature review on maternal-fetal and reproductive disorders of Toxoplasma gondii infection. J. Gynecol. Obstet. Hum. Reprod. 2018, 47, 133–140. [Google Scholar] [CrossRef] [PubMed]
- Halonen, S.K.; Weiss, L.M. Toxoplasmosis. Handb. Clin. Neurol. 2013, 114, 125–145. [Google Scholar] [PubMed] [Green Version]
- Jones, J.; Lopez, A.; Wilson, M. Congenital Toxoplasmosis. Am. Fam. Phys. 2003, 67, 2131–2138. [Google Scholar]
- McAuley, J.B. Congenital Toxoplasmosis. J. Pediatr. Infect. Dis. Soc. 2014, 3, 30–33. [Google Scholar] [CrossRef] [PubMed]
- Kagan, K.O.; Hamprecht, K. Cytomegalovirus infection in pregnancy. Arch. Gynecol. Obstet. 2017, 296, 15–26. [Google Scholar] [CrossRef]
- Swanson, E.C.; Schleiss, M.R. Congenital Cytomegalovirus Infection: New Prospects for Prevention and Therapy. Pediatr. Clin. N. Am. 2013, 60, 1–17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leung, A.K.C.; Hon, K.L.; Leong, K.F. Rubella (German measles) revisited. Hong Kong Med. J. 2019, 25, 134–141. [Google Scholar] [CrossRef] [Green Version]
- Dontigny, L.; Arsenault, M.; Martel, M.J. No.203-Rubella in Pregnancy. J. Obstet. Gynaecol. Can. 2018, 40, e615–e621. [Google Scholar] [CrossRef]
- Bouthry, E.; Picone, O.; Hamdi, G.; Grangeot-Keros, L.; Ayoubi, J.; Vauloup-Fellous, C. Rubella and pregnancy: Diagnosis, management and outcomes. Prenat. Diagn. 2014, 13, 1246–1253. [Google Scholar] [CrossRef]
- Motoi, S.; Navolan, D.B.; Malita, D.; Ciohat, I.; Nemescu, D.; Manciuc, C.; Gorun, F.; Vilibic-Cavlek, T.; Boda, D.; Craina, M.; et al. A decreasing trend in Toxoplasma gondii seroprevalence among pregnant women in Romania—Results of a large scale study. Exp. Ther. Med. 2020, 20, 3536–3540. [Google Scholar] [CrossRef]
- Gorun, F.; Motoi, S.; Malita, D.; Navolan, D.B.; Nemescu, D.; Olariu, T.R.; Craina, M.; Vilibic-Cavlek, T.; Ciohat, I.; Boda, D.; et al. Cytomegalovirus seroprevalence in pregnant women in the western region of Romania: A large—Scale study. Exp. Ther. Med. 2020, 20, 2439–2443. [Google Scholar] [CrossRef]
- Gorun, F.; Malita, D.; Ciohat, I.; Vilibic-Cavlek, T.; Feier, H.; Tabain, I.; Craina, M.; Cretu, O.; Navolan, D. Prevalence of Rubella antibodies among fertile women in the west of Romania, 18 Years after the implementation of immunization. Vaccines 2021, 9, 104. [Google Scholar] [CrossRef]
- Abu-Madi, M.A.; Behnke, J.M.; Dabritz, H.A. Toxoplasma gondii seropositivity and co-infection with TORCH pathogens in High-Risk Patients from Qatar. Am. J. Trop. Med. Hyg. 2010, 82, 626–633. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ahmed, A. Immunopathology of CMV Co-Infection: Review. MOJ Immunol. 2014, 1, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Gras, L.; Gilbert, R.E.; Wallon, M.; Peyron, F.; Cortina-Borja, M. 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, 541–548. [Google Scholar] [CrossRef]
- Araujo, P.R.; Ferreira, A.W. Avidity of IgG antibodies against excreted/secreted antigens of Toxoplasma gondii: Immunological marker for acute recent toxoplasmosis. Rev. Soc. Bras. Med. Trop. 2008, 41, 142–147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akyar, I. Seroprevalence and coinfections of Toxoplasma gondii in childbearing age women in Turkey. Iran. J. Public Health 2011, 40, 63–67. [Google Scholar] [PubMed]
- Vilibic-Cavlek, T.; Ljubin-Sternak, S.; Ban, M.; Kolaric, B.; Sviben, M.; Mlinaric-Galinovic, G. Seroprevalence of TORCH infections in women of childbearing age in Croatia. J. Matern. Fetal. Neonatal. Med. 2011, 24, 280–283. [Google Scholar] [CrossRef] [PubMed]
- Alvarado-Esquivel, C.; Campillo-Ruiz, F.; Liesenfeld, O. Seroepidemiology of Infection With Toxoplasma Gondii in Migrant Agricultural Workers Living in Poverty in Durango, Mexico. Parasites Vectors 2013, 36, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Rivera, E.M.; Lavayén, S.N.; Sánchez, P.; Martins, C.M.A.; Gomez, E.; Rodriguez, J.P.; Arias, M.E.; Silva, A.P.; Angel, S.O. Toxoplasma gondii seropositivity associated to peri-urban living places in pregnant women in a rural area of Buenos Aires province, Argentina. Parasite Epidemiol. Control 2019, 7, e00121. [Google Scholar] [CrossRef]
- Cannon, M.; Schmid, D.; Hyde, T. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev. Med. Virol. 2010, 20, 202–213. [Google Scholar] [CrossRef]
- Vilibic-Cavlek, T.; Kolaric, B.; Beader, N.; Vrtar, I.; Tabain, I.; Mlinaric-Galinovic, G. Seroepidemiology of cytomegalovirus infections in Croatia. Wien. Klin. Wochenschr. 2016, 129, 129–135. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jones, J.L.; Kruszon-Moran, D.; Rivera, H.N.; Price, C.; Wilkins, P.P. Toxoplasma gondii seroprevalence in the United States 2009-2010 and comparison with the past two decades. Am. J. Trop. Med. Hyg. 2014, 90, 1135–1139. [Google Scholar] [CrossRef] [PubMed]
- Pereboom, M.T.; Manniën, J.; Spelten, E.R.; Schellevis, F.G.; Hutton, E.K. Observational study to assess pregnant women’s knowledge and behaviour to prevent toxoplasmosis, listeriosis and cytomegalovirus. BMC Pregnancy Childbirth 2013, 13, 98. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ross, D.S.; Jones, J.L.; Lynch, M.F. Toxoplasmosis, cytomegalovirus, listeriosis, and preconception Care. Matern. Child Health J. 2006, 10, 187–191. [Google Scholar] [CrossRef] [Green Version]
Group 1 n/Total (%) | Group 2 n/Total (%) | ||
---|---|---|---|
Area of residence | Urban | 1054/1461 (72.1%) | 3570/5500(64.9%) |
Rural | 407/1461 (27.9%) | 1930/5500(35.1%) | |
Age of participants | 14–43 years | 14–45 years | |
Year of birth | 1966–1994 | 1970–2004 |
Toxoplasma gondii | CMV | Rubella Virus | ||||
---|---|---|---|---|---|---|
Group | IgG+ n/% (95%CI) | IgM+ n/% (95%CI) | IgG+ n/% (95%CI) | IgM+ n/% (95%CI) | IgG+ n/% (95%CI) | IgM+ n/% (95%CI) |
1 (2008–2010) n = 1461 | 639/43.7%) (41.2–46.3%) | 12/0.8% (0.5–1.4%) | 1384/94.7% (93.5–95.8%) | 5/0.3% (0.1–0.8%) | 1375/94.1% (92.8–95.2%) | 7/0.5% (0.2–1%) |
2 (2015–2018) n = 5500 | 2132/38.8% (37.5–40.1%) | 58/1.1% (0.8–1.4%) | 5012/91.1% (90.3–91.9%) | 16/0.3% (0.2–0.5%) | 5032/91.5% (90.7–92.2%) | 15/0.3% (0.2–0.4%) |
p value | p = 0.0006 | p = 0.55 | p < 0.0001 | p = 0.78 | p = 0.0009 | p = 0.19 |
Odds ratio (95%CI) | 0.81 (0.72–0.91) | 1.28 (0.68–2.46) | 0.57 (0.99–0.72) | 0.84 (0.32–2.12) | 0.67 (0.47–0.85) | 0.56 (0.24–1.48) |
Group 1 n/% (95% CI) | Group 2 n/% (95%CI) | p Value OR (95%CI) | |
---|---|---|---|
Toxoplasma gondii | 11/0.8% (0.4–1.3) | 56/1.0% (0.8–1.3) | p = 0.45 1.35 (0.72–2.51) |
CMV | 4/0.3% (0.1–0.7) | 16/0.3% (0.2–0.5) | p > 0.99 1.06 (0.36–2.93) |
Rubella virus | 7/0.5% (0.2–1.0) | 15/0.3% (0.2–0.4) | p = 0.19 0.56 (0.24–1.48) |
Group 1 (2008–2010) | Group 2 (2015–2018) | Group 1 vs. Group 2 | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Overall n/Total % (95%CI) | Urban n/Total % (95%CI) | Rural n/Total % (95%CI) | p Value OR (95%CI) | Overall n/Total % (95%CI) | Urban n/Total % (95%CI) | Rural n/Total % (95%CI) | p Value OR (95%CI) | Overall p Value OR (95%CI) | Urban p Value OR (95%CI) | Rural p Value OR (95%CI) | |
T. gondii + CMV + | 605/1461 41.4% (38.9–44.0) | 405/1054 38.4% (35.5–41.4) | 200/407 49.1% (44.3–54.0) | p = 0.0002 1.54 (1.23–1.94) | 1986/3570 36.1% (34.8–37.4) | 1134/3570 31.8% (30.3–33.3) | 852/1930 44.1% (41.9–46.4) | p < 0.0001 1.69 (1.51–1.90) | 0.0002 0.79 (0.71–0.89) | <0.0001 0.74 (0.64–0.85) | 0.07 0.81 (0.65–1.01) |
T. gondii – CMV – | 43/1461 2.9% (2.2–3.9) | 36/1054 3.4% (2.5–4.7) | 7/407 1.7% (0.8–3.5) | p = 0.11 0.49 (0.21–1.11) | 336/5500 6.1% (5.5–6.8) | 280/3570 7.8% (7.0–8.8) | 56/1930 2.9% (2.2–3.7) | p < 0.0001 0.35 (0.26–0.47) | <0.0001 2.14 (1.55–2.96) | <0.0001 2.40 (1.70–3.43) | 0.23 1.70 (0.81–3.83) |
T. gondii + Rubella + | 611/1461 41.8% (39.3–44.4) | 405/1054 38.4% (35.5–41.4) | 206/407 50.6% (45.8–55.4) | p < 0.0001 1.64 (1.30–2.06) | 1962/5500 35.7% (34.4–36.9) | 1149/3570 32.2% (30.7–33.7) | 813/1930 42.1% (39.9–44.3) | p < 0.0001 1.53 (1.36–1.71) | <0.0001 0.77 (0.68–0.86) | 0.0002 0.76 (0.66–0.87) | 0.002 0.71 (0.57–0.88) |
T. gondii – Rubella – | 58/1461 4.0% (3.1–5.1) | 39/1054 3.7% (2.7–5.0) | 19/407 4.7% (3.0–7.2) | p = 0.45 1.27 (0.73–2.25) | 292/5500 5.3% (4.7–5.9) | 201/3570 5.6% (4.9–6.4) | 91/1930 4.7% (3.9–5.8) | p = 0.16 0.82 (0.64–1.06) | 0.003 1.35 (1.01–1.80) | 0.01 1.55 (1.10–2.20) | >0.99 1.01 (0.61–1.69) |
CMV + Rubella + | 1299/1461 88.9% 87.2–90.4) | 936/1054 88.8% (86.8–90.6) | 363/407 89.2% (85.8–91.8) | p = 0.92 1.04 (0.72–1.48) | 4597/5500 83.6% (82.6–84.5) | 2925/3570 81.9% (80.6–83.2) | 1672/1930 86.6% (85.0–88.1) | p < 0.0001 1.42 (1.22–3.34) | <0.0001 0.63 (0.47–0.75) | <0.0001 0.57 (0.46–1.41) | 0.16 0.78 (0.56–1.1) |
CMV – Rubella – | 1/1461 0.1% NA | 1/1054 0.1% (NA) | 0/407 0.0% | NA | 53/5500 1.0% (07–1.3) | 41/3570 1.1%(0.8–1.6) | 12/1930 0.6% (0.4–1.1) | p = 0.06 0.53 (0.27–1.03) | <0.0001 14.57 (2.66–144.3) | 0.0003 12.23 2.24–124.9) | NA |
T. gondii + CMV + Rubella + | 578/1461 39.6% (37.1–42.1) | 384/1054 36.4% (33.6–39.4) | 194/407 47.7% (42.9–52.5) | p = 0.0001 1.58 (1.26–2.00) | 1824/5500 33.2% (31.9–34.4) | 1049/3570 29.4% (27.9–30.9) | 775/1930 40.2% (38.0–42.4) | p < 0.0001 1.61 (1.43–1.81) | <0.0001 0.75 (0.67–0.85) | <0.0001 0.72 (0.62–0.84) | 0.005 0.73 (0.59–0.91) |
T. gondii – CMV – Rubella – | 0 | 0 | 0 | NA | 39/5500 0.71% (0.5–1.00) | 31/3570 0.9% (0.6–1.2) | 8/3570 0.2% (0.1–0.4) | p = 0.0003 0.25 (0.12–0.55) | NA | NA | NA |
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Mocanu, A.G.; Gorun, F.; Ciohat, I.; Navolan, D.; Malita, D.; Vilibic-Cavlek, T.; Dahma, G.; Neamtu, R.; Popescu, D.; Cioca, A.; et al. Simultaneous Seroprevalence to Toxoplasma gondii, Cytomegalovirus and Rubella Virus in Childbearing Women from Western Romania. Medicina 2021, 57, 927. https://0-doi-org.brum.beds.ac.uk/10.3390/medicina57090927
Mocanu AG, Gorun F, Ciohat I, Navolan D, Malita D, Vilibic-Cavlek T, Dahma G, Neamtu R, Popescu D, Cioca A, et al. Simultaneous Seroprevalence to Toxoplasma gondii, Cytomegalovirus and Rubella Virus in Childbearing Women from Western Romania. Medicina. 2021; 57(9):927. https://0-doi-org.brum.beds.ac.uk/10.3390/medicina57090927
Chicago/Turabian StyleMocanu, Adelina Geanina, Florin Gorun, Ioana Ciohat, Dan Navolan, Daniel Malita, Tatjana Vilibic-Cavlek, George Dahma, Radu Neamtu, Daniela Popescu, Andreea Cioca, and et al. 2021. "Simultaneous Seroprevalence to Toxoplasma gondii, Cytomegalovirus and Rubella Virus in Childbearing Women from Western Romania" Medicina 57, no. 9: 927. https://0-doi-org.brum.beds.ac.uk/10.3390/medicina57090927