{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,8]],"date-time":"2026-02-08T11:14:28Z","timestamp":1770549268909,"version":"3.49.0"},"reference-count":37,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2024,7,12]],"date-time":"2024-07-12T00:00:00Z","timestamp":1720742400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the Program to Support the Improvement of the Production Conditions of the SNI and SNCA Members","award":["PRO-SNI 2022"],"award-info":[{"award-number":["PRO-SNI 2022"]}]},{"name":"the Program to Support the Improvement of the Production Conditions of the SNI and SNCA Members","award":["237086\/2021"],"award-info":[{"award-number":["237086\/2021"]}]},{"name":"the Universidad de Guadalajara","award":["PRO-SNI 2022"],"award-info":[{"award-number":["PRO-SNI 2022"]}]},{"name":"the Universidad de Guadalajara","award":["237086\/2021"],"award-info":[{"award-number":["237086\/2021"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Toxoplasma gondii (T. gondii) is the causal agent of toxoplasmosis. It may produce severe damage in immunocompromised individuals, as well as congenital infection and intrauterine growth restriction (IUGR). Previous reports have associated interleukin IL-33 with miscarriage, fetal damage, and premature delivery due to infections with various microorganisms. However, IL-33 has not been associated with congenital toxoplasmosis. The sST2 receptor has been reported in patients who have had recurrent miscarriages. On the other hand, IL-1\u03b2 was not found in acute Toxoplasma infection. Our aim was to analyze the associations between the serum levels of IL-33 and IL-1\u03b2 in IUGR and toxoplasmosis during pregnancy. Eighty-four serum samples from pregnant women who had undergone 26 weeks of gestation were grouped as follows: with anti-Toxoplasma antibodies, without anti-Toxoplasma antibodies, IUGR, and the control group. IgG and IgM anti-T. gondii antibodies, as well as IL-33, ST2, and IL-1\u03b2, were determined using an ELISA assay. Statistical analyses were performed using the Pearson and Chi-square correlation coefficients, as well as the risk factors and Odds Ratios (ORs), with a confidence interval of 95% (CI 95). The results showed that 15\/84 (17.8%) of cases were positive for IgG anti-Toxoplasma antibodies and 2\/84 (2.38%) of cases were positive for IgM. A statistically significant difference was found between IUGR and IL-33 (p &lt; 0.001), as well as between ST2 and IUGR (p &lt; 0.001). In conclusion, IUGR was significantly associated with IL-33 and ST2 positivity based on the overall IUGR grade. No significant association was found between IUGR and the presence of anti-Toxoplasma antibodies. There was no association between IL-1\u03b2 and IUGR. More research is needed to strengthen the utility of IL-33 and ST2 as biomarkers of IUGR.<\/jats:p>","DOI":"10.3390\/microorganisms12071420","type":"journal-article","created":{"date-parts":[[2024,7,12]],"date-time":"2024-07-12T14:04:35Z","timestamp":1720793075000},"page":"1420","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Interleukins IL33\/ST2 and IL1-\u03b2 in Intrauterine Growth Restriction and Seropositivity of Anti-Toxoplasma gondii Antibodies"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0009-0008-7474-4252","authenticated-orcid":false,"given":"Karen","family":"Franco-De Le\u00f3n","sequence":"first","affiliation":[{"name":"Departamento de Microbiolog\u00eda y Patolog\u00eda, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara 44340, Jalisco, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9522-7499","authenticated-orcid":false,"given":"Eva Elizabeth","family":"Camarena","sequence":"additional","affiliation":[{"name":"Departamento de Ginecolog\u00eda y Obstetricia, Hospital Civil Juan I. Menchaca, Guadalajara 44340, Jalisco, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ana Laura","family":"Pereira-Su\u00e1rez","sequence":"additional","affiliation":[{"name":"Departamento de Microbiolog\u00eda y Patolog\u00eda, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara 44340, Jalisco, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-1168-3845","authenticated-orcid":false,"given":"Ernesto","family":"Barrios-Prieto","sequence":"additional","affiliation":[{"name":"Unidad de Medicina Materno Fetal, Hospital Civil Juan I. Menchaca, Guadalajara 44340, Jalisco, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andrea","family":"Soto-Venegas","sequence":"additional","affiliation":[{"name":"Unidad de Medicina Materno Fetal, Hospital Civil Juan I. Menchaca, Guadalajara 44340, Jalisco, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zamira Helena","family":"Hern\u00e1ndez-Nazara","sequence":"additional","affiliation":[{"name":"Instituto de Investigaci\u00f3n en Enfermedades Cr\u00f3nico Degenerativas, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara 44340, Jalisco, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-1376-5155","authenticated-orcid":false,"given":"Yithzel Guadalupe","family":"Luna Rojas","sequence":"additional","affiliation":[{"name":"Departamento de Ginecolog\u00eda y Obstetricia, Hospital Civil Juan I. Menchaca, Guadalajara 44340, Jalisco, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5581-4322","authenticated-orcid":false,"given":"Mar\u00eda de la Luz","family":"Galv\u00e1n-Ram\u00edrez","sequence":"additional","affiliation":[{"name":"Departamento de Microbiolog\u00eda y Patolog\u00eda, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara 44340, Jalisco, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,7,12]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.jogoh.2017.12.003","article-title":"An updated literature review on maternal-fetal and reproductive disorders of Toxoplasma gondii infection","volume":"47","author":"Fallahi","year":"2018","journal-title":"J. Gynecol. Obstet. Hum. Reprod."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Vargas-Montes, M., Cardona, N., Moncada, D.M., Molina, D.A., Zhang, Y., and G\u00f3mez-Mar\u00edn, J.E. (2019). Enzyme-Linked Aptamer Assay (ELAA) for Detection of Toxoplasma ROP18 Protein in Human Serum. Front. Cell. Infect. Microbiol., 13.","DOI":"10.3389\/fcimb.2019.00386"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1093\/jpids\/piu077","article-title":"Congenital Toxoplasmosis","volume":"1","author":"McAuley","year":"2014","journal-title":"Pediatr. Infect. Dis. Soc."},{"key":"ref_4","unstructured":"Galv\u00e1n-Ram\u00edrez, M.L., and Mondrag\u00f3n-Flores, R. (2017). Toxoplasmosis Humana, ECORFAN. Available online: https:\/\/www.ecorfan.org\/libros\/BOOK_TOXOPLASMOSIS.pdf."},{"key":"ref_5","first-page":"336","article-title":"Co-operation of interleukin-1 beta and tumour necrosis factor-alpha in the activation of human umbilical vein endothelial cells to inhibit Toxoplasma gondii replication","volume":"79","author":"Dimier","year":"1993","journal-title":"Inmunology"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Yang, F., Zheng, Q., and Jin, L. (2019). Dynamic Function and Composition Changes of Immune Cells During Normal and Pathological Pregnancy at the Maternal-Fetal Interface. Front. Immunol., 10.","DOI":"10.3389\/fimmu.2019.02317"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"19420","DOI":"10.1074\/jbc.M901744200","article-title":"Interleukin-33 is biologically active independently of caspase-1 cleavage","volume":"284","author":"Lamacchia","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1111\/j.1600-065X.2008.00624.x","article-title":"IL-1, IL-18, and IL-33 families of cytokines","volume":"223","author":"Arend","year":"2008","journal-title":"Immunol. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/S0716-8640(12)70335-8","article-title":"Visi\u00f3n panor\u00e1mica del sistema inmune","volume":"23","author":"Toche","year":"2012","journal-title":"Rev. M\u00e9dica Cl\u00ednica Las. Condes"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1111\/aji.12303","article-title":"Fetal sex-based differences in maternal hormones, angiogenic factors, and immune mediators during pregnancy and the postpartum period","volume":"73","author":"Enninga","year":"2015","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_11","unstructured":"Murphy, K., and Casey, W. (2017). Din\u00e1mica integrada de la inmunidad innata y adaptativa. Inmunolog\u00eda de Janeway 9th Edition Ciudad de M\u00e9xico: Manual moderno, World Press."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"155283","DOI":"10.1016\/j.cyto.2020.155283","article-title":"Macrophage migration inhibitory factor (MIF) and pregnancy may impact the balance of intestinal cytokines and the development of intestinal pathology caused by Toxoplasma gondii infection","volume":"2","author":"Marcon","year":"2020","journal-title":"Cytokine"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1080\/09513590.2018.1528220","article-title":"Association of IL-10, IL-18, and IL-33 genetic polymorphisms with recurrent pregnancy loss risk in Iranian women","volume":"35","author":"Soheilyfar","year":"2019","journal-title":"Gynecol. Endocrinol. Off. J. Int. Soc. Gynecol. Endocrinol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e12836","DOI":"10.1111\/aji.12836","article-title":"IL-33\/ST2 axis affects the polarization and efferocytosis of decidual macrophages in early pregnancy","volume":"79","author":"Sheng","year":"2018","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.jri.2012.06.003","article-title":"Maternal serum interleukin-33 and soluble ST2 across early pregnancy, and their association with miscarriage","volume":"95","author":"Tuohey","year":"2012","journal-title":"J. Reprod. Immunol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"106931","DOI":"10.1016\/j.actatropica.2023.106931","article-title":"Upregulation of IL-33, CCL2, and CXCL16 levels in Brazilian pregnant women infected by Toxoplasma gondii","volume":"243","author":"Santos","year":"2023","journal-title":"Acta Trop."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Yang, X., Tian, Y., Zheng, L., Luu, T., and Kwak-Kim, J. (2022). The Update Immune-Regulatory Role of Pro- and Anti-Inflammatory Cytokines in Recurrent Pregnancy Losses. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24010132"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1007\/s00109-018-01737-x","article-title":"NLRP7 Is increased in human idiopathic fetal growth restriction and plays a critical role in trophoblast differentiation","volume":"97","author":"Reynaud","year":"2019","journal-title":"J. Mol. Med."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e439","DOI":"10.1111\/apa.12339","article-title":"Perinatal systemic inflammatory responses of growth-restricted preterm newborns","volume":"102","author":"McElrath","year":"2013","journal-title":"Acta Paediatr."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Ferrari, D., Polettini, J., de Moraes, L.L., de Campos, L.A., da Silva, M.G., Saeki, E.K., and Morceli, G. (2020). Profile of pro-inflammatory cytokines in colostrum of nursing mothers at the extremes of reproductive age. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0231882"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1093\/intimm\/dxy004","article-title":"Host immune responses to Toxoplasma gondii","volume":"30","author":"Sasai","year":"2018","journal-title":"Int. Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.jacr.2021.02.017","article-title":"ACR Appropriateness Criteria Second and third trimester screening for fetal anormaly","volume":"18","author":"Sussman","year":"2021","journal-title":"J. Am. Coll. Radiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.jacr.2019.02.009","article-title":"Growth Disturbances\u2014Risk of Fetal Growth Restriction","volume":"16","author":"Shipp","year":"2019","journal-title":"J. Am. Coll. Radiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1016\/j.ajog.2021.11.1357","article-title":"Clinical Opinion: The diagnosis and management of suspected fetal growth restriction: An evidence-based approach","volume":"226","author":"Lees","year":"2022","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/s00436-023-08068-y","article-title":"Impact of chronic toxoplasmosis in pregnancy: Association between maternal seropositivity for Toxoplasma gondii IgG antibodies and fetal growth restriction","volume":"123","author":"Martinez","year":"2023","journal-title":"Parasitol. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"S745","DOI":"10.1016\/j.ajog.2017.11.577","article-title":"Pathophysiology of placental-derived fetal growth restriction","volume":"218","author":"Burton","year":"2018","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"20971","DOI":"10.1038\/s41598-021-00430-3","article-title":"NF-\u03baB regulation in maternal immunity during normal and IUGR pregnancies","volume":"11","author":"Ariyakumar","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Granne, I., Southcombe, J.H., Snider, J.V., Tannetta, D.S., Child, T., Redman, C.W., and Sargent, I.L. (2011). ST2 and IL-33 in pregnancy and pre-eclampsia. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0024463"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2153034","DOI":"10.1080\/14767058.2022.2153034","article-title":"Soluble suppression of tumorigenicity-2 in pregnancy with a small-for-gestational-age fetus and with preeclampsia","volume":"36","author":"Kanninen","year":"2023","journal-title":"J. Matern.-Fetal Neonatal Med."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Zhao, L., Fu, J., Ding, F., Liu, J., Li, L., and Song, Q. (2022). IL-33 and Soluble ST2 Are Associated With Recurrent Spontaneous Abortion in Early Pregnancy. Front. Physiol., 12.","DOI":"10.3389\/fphys.2021.789829"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Silva, Z.M., Toledo, D.N.M., Pio, S., Machado, B.A.A., Dos Santos, P.V., H\u00f3, F.G., Medina, Y.N., Cordeiro, P.H.M., Perucci, L.O., and Pinto, K.M.C. (2024). Neuroserpin, IL-33 and IL-17A as potential markers of mild symptoms of depressive syndrome in Toxoplasma gondii-infected pregnant women. Front. Immunol., 15.","DOI":"10.3389\/fimmu.2024.1394456"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1111\/j.1447-0756.2012.02012.x","article-title":"Significance of maternal screening for toxoplasmosis, rubella, cytomegalovirus and herpes simplex virus infection in cases of fetal growth restriction","volume":"39","author":"Yamamoto","year":"2013","journal-title":"J. Obstet. Gynaecol. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"114","DOI":"10.3345\/kjp.2018.61.4.114","article-title":"TORCH (toxoplasmosis, rubella, cytomegalovirus, and herpes simplex virus) screening of small for gestational age and intrauterine growth restricted neonates: Efficacy study in a single institute in Korea","volume":"61","author":"Chung","year":"2018","journal-title":"Korean J. Pediatr."},{"key":"ref_34","first-page":"333","article-title":"Incidence of anti-Toxoplasma antibodies in women with high-risk pregnancy and habitual abortions","volume":"4","year":"1995","journal-title":"Rev. Soc. Bras. Med. Tropical."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1177\/1933719113492204","article-title":"The interplay of the interleukin 1 system in pregnancy and labor","volume":"21","author":"Heng","year":"2014","journal-title":"Reprod. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1007\/s40291-022-00611-4","article-title":"Epigenetics Beyond Fetal Growth Restriction: A Comprehensive Overview","volume":"26","author":"Salmeri","year":"2022","journal-title":"Mol. Diagn. Ther."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1146\/annurev-micro-090817-062741","article-title":"The Epigenome, Cell Cycle, and Development in Toxoplasma","volume":"8","author":"Kim","year":"2018","journal-title":"Annu. Rev. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/7\/1420\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:15:57Z","timestamp":1760109357000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/7\/1420"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,12]]},"references-count":37,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2024,7]]}},"alternative-id":["microorganisms12071420"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms12071420","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,12]]}}}