{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,28]],"date-time":"2026-01-28T13:13:06Z","timestamp":1769605986157,"version":"3.49.0"},"reference-count":42,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2024,8,10]],"date-time":"2024-08-10T00:00:00Z","timestamp":1723248000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"FAPESP","award":["2023\/04391-6"],"award-info":[{"award-number":["2023\/04391-6"]}]},{"name":"FAPESP","award":["88887.973643\/2025-00"],"award-info":[{"award-number":["88887.973643\/2025-00"]}]},{"name":"CAPES","award":["2023\/04391-6"],"award-info":[{"award-number":["2023\/04391-6"]}]},{"name":"CAPES","award":["88887.973643\/2025-00"],"award-info":[{"award-number":["88887.973643\/2025-00"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["TropicalMed"],"abstract":"<jats:p>Schistosomiasis is a neglected tropical disease that affects developing countries worldwide and is caused by several species of parasites from the Schistosoma genus. Chronic infection is characterized by the formation of granulomas around the parasite eggs, the leading cause of pathology. The hepatosplenic clinical form is one of the most common, but urogenital schistosomiasis is another relevant clinical presentation responsible for infertility in men and women. Inflammatory response, anatomical deformations, and endocrine\/biochemical changes are involved in the development of infertility. Schistosome parasites can synthesize catechol estrogen-like molecules and affect the sexual hormone balance in their host. Here, we review many aspects of the pathology of urogenital schistosomiasis, specifically infertility, and point to the biochemical and endocrinal elements that must be investigated in the future.<\/jats:p>","DOI":"10.3390\/tropicalmed9080177","type":"journal-article","created":{"date-parts":[[2024,8,12]],"date-time":"2024-08-12T05:19:38Z","timestamp":1723439978000},"page":"177","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Insights into the State of the Art of Urogenital Schistosomiasis with a Focus on Infertility"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0887-1372","authenticated-orcid":false,"given":"Rafaella P.","family":"Marques","sequence":"first","affiliation":[{"name":"Disciplina de Parasitologia, Departamento de Microbiologia, Imunologia e Parasitologia, Escola Paulista de Medicina, Universidade Federal de S\u00e3o Paulo, S\u00e3o Paulo 04023-062, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4423-7371","authenticated-orcid":false,"given":"Waqas","family":"Ahmad","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences, University of Veterinary and Animal Sciences (UVAS), KBCMA Campus, Narowal 51800, Pakistan"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9157-5541","authenticated-orcid":false,"given":"Raquel","family":"Soares","sequence":"additional","affiliation":[{"name":"Department of Biomedicine, Faculty of Medicine, University of Porto, 4200-450 Porto, Portugal"},{"name":"i3S\u2014Instituto de Investiga\u00e7\u00e3o e Inova\u00e7\u00e3o em Sa\u00fade, Universidade do Porto, 4200-135 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8535-0901","authenticated-orcid":false,"given":"Katia C.","family":"Oliveira","sequence":"additional","affiliation":[{"name":"Disciplina de Parasitologia, Departamento de Microbiologia, Imunologia e Parasitologia, Escola Paulista de Medicina, Universidade Federal de S\u00e3o Paulo, S\u00e3o Paulo 04023-062, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0466-8465","authenticated-orcid":false,"given":"Monica C.","family":"Botelho","sequence":"additional","affiliation":[{"name":"i3S\u2014Instituto de Investiga\u00e7\u00e3o e Inova\u00e7\u00e3o em Sa\u00fade, Universidade do Porto, 4200-135 Porto, Portugal"},{"name":"Department of Health Promotion and Chronic Diseases, INSA\u2014National Institute of Health Dr. Ricardo Jorge, 4000-055 Porto, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2024,8,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"549","DOI":"10.4269\/ajtmh.2009.08-0498","article-title":"Case Report: Cervical Schistosomiasis as a Risk Factor of Cervical Uterine Dysplasia in a Traveler","volume":"81","author":"Consigny","year":"2009","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_2","first-page":"28","article-title":"Schistosomiasis: Health Effects on Women","volume":"3","author":"Nour","year":"2010","journal-title":"Rev. Obstet. Gynecol."},{"key":"ref_3","first-page":"563","article-title":"Primary Infertility Associated with Schistosoma mansoni: A Case Report from the Jos Plateau, North Central Nigeria","volume":"12","author":"Adisa","year":"2012","journal-title":"Afr. Health Sci."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Montresor, A., Mwinzi, P., Mupfasoni, D., and Garba, A. (2022). Reduction in DALYs Lost Due to Soil-Transmitted Helminthiases and Schistosomiasis from 2000 to 2019 Is Parallel to the Increase in Coverage of the Global Control Programs. PLoS Negl. Trop. Dis., 16.","DOI":"10.1371\/journal.pntd.0010575"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"267","DOI":"10.4161\/viru.2.4.16734","article-title":"Targeting Molecular Signaling Pathways of Schistosoma haematobium Infection in Bladder Cancer","volume":"2","author":"Botelho","year":"2011","journal-title":"Virulence"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"73","DOI":"10.4269\/ajtmh.23-0751","article-title":"Predicting Schistosomiasis Intensity in Africa: A Machine Learning Approach to Evaluate the Progress of WHO Roadmap 2030","volume":"111","author":"Chen","year":"2024","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1007\/s00436-014-4250-9","article-title":"Prostate Adenocarcinoma Associated with Prostatic Infection Due to Schistosoma haematobium. Case Report and Systematic Review","volume":"114","author":"Figueiredo","year":"2015","journal-title":"Parasitol. Res."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Richardson, M.L., Fu, C.L., Pennington, L.F., Honeycutt, J.D., Odegaard, J.L., Hsieh, Y.J., Hammam, O., Conti, S.L., and Hsieh, M.H. (2014). A New Mouse Model for Female Genital Schistosomiasis. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0002825"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1016\/j.fertnstert.2009.12.050","article-title":"The First Community-Based Report on the Effect of Genital Schistosoma haematobium Infection on Female Fertility","volume":"94","author":"Kjetland","year":"2010","journal-title":"Fertil. Steril."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1593","DOI":"10.1017\/S0031182009990552","article-title":"A Wake up Call for Urinary Schistosomiasis: Reconciling Research Effort with Public Health Importance","volume":"136","author":"Rollinson","year":"2009","journal-title":"Parasitology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/j.socscimed.2003.09.018","article-title":"The Social Context of Reproductive Health in an Egyptian Hamlet: A Pilot Study to Identify Female Genital Schistosomiasis","volume":"58","author":"Talaat","year":"2004","journal-title":"Soc. Sci. Med."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Hotez, P.J., Fenwick, A., and Kjetland, E.F. (2009). Africa\u2019s 32 Cents Solution for HIV\/AIDS. PLoS Negl. Trop. Dis., 3.","DOI":"10.1371\/journal.pntd.0000430"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2075.e7","DOI":"10.1016\/j.fertnstert.2009.05.043","article-title":"Genital Schistosomiasis as a Cause of Female Sterility and Acute Abdomen","volume":"93","author":"Schanz","year":"2010","journal-title":"Fertil. Steril."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1111\/j.1708-8305.2010.00476.x","article-title":"Fluke Infertility: The Late Cost of a Quick Swim","volume":"18","author":"Bailey","year":"2011","journal-title":"J. Travel Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1097\/AOG.0000000000000025","article-title":"Helminth Infections: A New Global Women\u2019s Health Agenda","volume":"123","author":"Hotez","year":"2014","journal-title":"Obstet. Gynecol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Mbabazi, P.S., Andan, O., Fitzgerald, D.W., Chitsulo, L., Engels, D., and Downs, J.A. (2011). Examining the Relationship between Urogenital Schistosomiasis and Hiv Infection. PLoS Negl. Trop. Dis., 5.","DOI":"10.1371\/journal.pntd.0001396"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Odaibo, A.B., Komolafe, A.K., Olajumoke, T.O., Diyan, K.D., Aluko, D.A., Alagbe, O.A., Ajagbe, O.A., and Olarinloye, D.B. (2024). Endemic Status of Urogenital Schistosomiasis and the Efficacy of a Single-Dose Praziquantel Treatment in Unmapped Rural Farming Communities in Oyo East Local Government Area, Oyo State, Nigeria. PLoS Negl. Trop. Dis., 18.","DOI":"10.1371\/journal.pntd.0012101"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Lamberti, O., Kayuni, S., Kumwenda, D., Ngwira, B., Singh, V., Moktali, V., Dhanani, N., Wessels, E., Van Lieshout, L., and Fleming, F.M. (2024). Female Genital Schistosomiasis Burden and Risk Factors in Two Endemic Areas in Malawi Nested in the Morbidity Operational Research for Bilharziasis Implementation Decisions (MORBID) Cross-Sectional Study. PLoS Negl. Trop. Dis., 18.","DOI":"10.1371\/journal.pntd.0012102"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1893","DOI":"10.1007\/s00467-023-06260-x","article-title":"Pediatric Urogenital Schistosomiasis Diagnosed in France","volume":"39","author":"Percheron","year":"2024","journal-title":"Pediatr. Nephrol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"e366","DOI":"10.1016\/S2666-5247(23)00377-4","article-title":"Diagnostic Tests for Human Schistosoma mansoni and Schistosoma haematobium Infection: A Systematic Review and Meta-Analysis","volume":"5","author":"Vaillant","year":"2024","journal-title":"Lancet Microbe"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1185","DOI":"10.1007\/s15010-023-02060-5","article-title":"Diagnosis and Management of Complicated Urogenital Schistosomiasis: A Systematic Review of the Literature","volume":"51","author":"Manciulli","year":"2023","journal-title":"Infection"},{"key":"ref_22","first-page":"634264","article-title":"Genital Schistosomiasis Leading to Ectopic Pregnancy and Subfertility: A Case for Parasitic Evaluation of Gynecologic Patients in Schistosomiasis Endemic Areas","volume":"2013","author":"Odoi","year":"2013","journal-title":"Case Rep. Obstet. Gynecol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1016\/j.pt.2015.03.005","article-title":"The Role of Estrogens and Estrogen Receptor Signaling Pathways in Cancer and Infertility: The Case of Schistosomes","volume":"31","author":"Botelho","year":"2015","journal-title":"Trends Parasitol."},{"key":"ref_24","first-page":"308","article-title":"Evaluation and Treatment of Infertility","volume":"91","author":"Lindsay","year":"2015","journal-title":"Am. Fam. Physician"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1725","DOI":"10.1093\/oxfordjournals.humrep.a136163","article-title":"Schistosomiasis: An Unusual Cause of Tubal Infertility","volume":"10","author":"Balasch","year":"1995","journal-title":"Hum. Reprod."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e13165","DOI":"10.1111\/and.13165","article-title":"Schistosomiasis (Bilharziasis) and Male Infertility","volume":"51","author":"Altenburg","year":"2019","journal-title":"Andrologia"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/S0001-706X(96)00025-3","article-title":"Schistosomiasis in Women: Manifestations in the Upper Reproductive Tract","volume":"62","author":"Kjetland","year":"1996","journal-title":"Acta Trop."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/S0169-4758(99)01497-0","article-title":"Schistosomiasis of the Female Genital Tract: Public Health Aspects","volume":"15","author":"Poggensee","year":"1999","journal-title":"Parasitol. Today"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Kini, S., Dayoub, N., Raja, A., Pickering, S., and Thong, J. (2009). Schistosomiasis-Induced Male Infertility. BMJ Case Rep., 2009.","DOI":"10.1136\/bcr.01.2009.1481"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/0020-7292(82)90072-8","article-title":"Pelvic Schistosomiasis and Infertility","volume":"20","year":"1982","journal-title":"Int. J. Gynecol. Obstet."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"369","DOI":"10.3109\/01485018008987008","article-title":"Bilharziasis and Azoospermia","volume":"5","author":"Girgis","year":"1980","journal-title":"Arch. Androl."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.molmed.2012.12.007","article-title":"Estrogen Synthesis and Signaling Pathways during Aging: From Periphery to Brain","volume":"19","author":"Cui","year":"2013","journal-title":"Trends Mol. Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.mce.2009.03.026","article-title":"Mechanisms of Estrogen Signaling and Gene Expression via GPR30","volume":"308","author":"Prossnitz","year":"2009","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.cellimm.2015.01.018","article-title":"Estrogen Receptors Regulate Innate Immune Cells and Signaling Pathways","volume":"294","author":"Kovats","year":"2015","journal-title":"Cell. Immunol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.steroids.2014.06.012","article-title":"Estrogen Receptors Alpha (ER\u03b1) and Beta (ER\u03b2): Subtype-Selective Ligands and Clinical Potential","volume":"90","author":"Paterni","year":"2014","journal-title":"Steroids"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Santos, J., Gouveia, M.J., Vale, N., De Lurdes Delgado, M., Gon\u00e7alves, A., Da Silva, J.M.T., Oliveira, C., Xavier, P., Gomes, P., and Santos, L.L. (2014). Urinary Estrogen Metabolites and Self-Reported Infertility in Women Infected with Schistosoma haematobium. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0096774"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1210\/me.2004-0486","article-title":"Mechanisms of Estrogen Receptor Signaling: Convergence of Genomic and Nongenomic Actions on Target Genes","volume":"19","year":"2005","journal-title":"Mol. Endocrinol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1152\/physrev.00026.2006","article-title":"Estrogen Receptors: How Do They Signal and What Are Their Targets","volume":"87","author":"Heldring","year":"2007","journal-title":"Physiol. Rev."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"329","DOI":"10.11613\/BM.2014.035","article-title":"The Many Faces of Estrogen Signaling","volume":"24","author":"Ostanek","year":"2014","journal-title":"Biochem. Medica"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"135","DOI":"10.2174\/1570180813666160720165057","article-title":"Estrogen Catechol Detection as Biomarkers in Schistosomiasis Induced Cancer and Infertility Graphical Abstract HHS Public Access","volume":"14","author":"Botelho","year":"2017","journal-title":"Lett. Drug Des. Discov."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Cardoso, R., Lacerda, P.C., Costa, P.P., Machado, A., Carvalho, A., Bordalo, A., Fernandes, R., Soares, R., Richter, J., and Alves, H. (2017). Estrogen Metabolism-Associated CYP2D6 and IL6-174g\/c Polymorphisms in Schistosoma haematobium Infection. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18122560"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1122","DOI":"10.2174\/1871530319666190529121204","article-title":"Imbalance of Steroid Hormones in Hamsters Infected with Schistosoma mansoni","volume":"19","author":"Oliveira","year":"2019","journal-title":"Endocr. Metab. Immune Disord.-Drug Targets"}],"container-title":["Tropical Medicine and Infectious Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2414-6366\/9\/8\/177\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:34:30Z","timestamp":1760110470000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2414-6366\/9\/8\/177"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,10]]},"references-count":42,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2024,8]]}},"alternative-id":["tropicalmed9080177"],"URL":"https:\/\/doi.org\/10.3390\/tropicalmed9080177","relation":{},"ISSN":["2414-6366"],"issn-type":[{"value":"2414-6366","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,10]]}}}