{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,11]],"date-time":"2026-06-11T10:21:14Z","timestamp":1781173274694,"version":"3.54.1"},"reference-count":46,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2024,6,3]],"date-time":"2024-06-03T00:00:00Z","timestamp":1717372800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"German Research Foundation","award":["512648189"],"award-info":[{"award-number":["512648189"]}]},{"name":"Open Access Publication Fund of the Th\u00fcringer Universit\u00e4ts- und Landesbibliothek Jena","award":["512648189"],"award-info":[{"award-number":["512648189"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Background: Schistosome egg deposition in pregnant women may affect the placenta of infected mothers and cause placental schistosomiasis (PS). Histopathological examination of placental tissue is an inadequate detection method due to low sensitivity. So far, there has not been any systematic review on PS. Methods: We conducted a systematic literature search on PubMed, EMBASE, and Medline and included all publications that reported microscopically confirmed cases of PS, as well as the relevant secondary literature found in the citations of the primarily included publications. Results: Out of 113 abstracts screened we found a total of 8 publications describing PS with a total of 92 cases describing egg deposition of dead and\/or viable eggs and worms of S. haematobium and S. mansoni in placental tissue. One cross-sectional study investigating the prevalence of PS and its association with adverse birth outcomes, found 22% of placentas to be infested using a maceration technique but only &lt;1% using histologic examination. Additionally, no direct link to deleterious pregnancy outcomes could be shown. Conclusions: PS is a highly unattended and underdiagnosed condition in endemic populations, due to a lack of awareness as well as low sensitivity of histopathological examinations. However, PS may play an important role in mediating or reinforcing adverse birth outcomes (ABO) such as fetal growth restriction (FGR) in maternal schistosomiasis, possibly by placental inflammation.<\/jats:p>","DOI":"10.3390\/pathogens13060470","type":"journal-article","created":{"date-parts":[[2024,6,3]],"date-time":"2024-06-03T08:19:42Z","timestamp":1717402782000},"page":"470","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Human Placental Schistosomiasis\u2014A Systematic Review of the Literature"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0009-0008-1604-9710","authenticated-orcid":false,"given":"Jacob","family":"Gerstenberg","sequence":"first","affiliation":[{"name":"Institute for Tropical Medicine, Eberhard-Karls University T\u00fcbingen, 72074 T\u00fcbingen, Germany"},{"name":"Centre de Recherches M\u00e9dicales de Lambar\u00e9n\u00e9, Lambar\u00e9n\u00e9 242, Gabon"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sasmita","family":"Mishra","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Heidekreis Klinikum, 29664 Walsrode, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martha","family":"Holtfreter","sequence":"additional","affiliation":[{"name":"Tropical Medicine Unit, Department of Gastroenterology, Hepatology and Infectious Diseases, Faculty of Medicine, Heinrich-Heine-University, Moorenstr. 5, 40225 Duesseldorf, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1930-2944","authenticated-orcid":false,"given":"Joachim","family":"Richter","sequence":"additional","affiliation":[{"name":"Institute of International Health, Global Health Center, Charit\u00e9 University Medicine, 13353 Berlin, Germany"},{"name":"Swiss Tropical and Public Health Institute, 4123 Allschwil, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Saskia Dede","family":"Davi","sequence":"additional","affiliation":[{"name":"Center for Tropical Medicine, Bernhard Nocht Institute for Tropical Medicine & I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20359 Hamburg, Germany"},{"name":"German Centre for Infection Research (DZIF), Partner Site Hamburg-Luebeck-Borstel, 20359 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4025-2320","authenticated-orcid":false,"given":"Dearie Glory","family":"Okwu","sequence":"additional","affiliation":[{"name":"Centre de Recherches M\u00e9dicales de Lambar\u00e9n\u00e9, Lambar\u00e9n\u00e9 242, Gabon"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Ramharter","sequence":"additional","affiliation":[{"name":"Center for Tropical Medicine, Bernhard Nocht Institute for Tropical Medicine & I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20359 Hamburg, Germany"},{"name":"German Centre for Infection Research (DZIF), Partner Site Hamburg-Luebeck-Borstel, 20359 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2012-6327","authenticated-orcid":false,"given":"Johannes","family":"Mischlinger","sequence":"additional","affiliation":[{"name":"Center for Tropical Medicine, Bernhard Nocht Institute for Tropical Medicine & I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20359 Hamburg, Germany"},{"name":"German Centre for Infection Research (DZIF), Partner Site Hamburg-Luebeck-Borstel, 20359 Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4678-2469","authenticated-orcid":false,"given":"Benjamin T.","family":"Schleenvoigt","sequence":"additional","affiliation":[{"name":"Institute of Infectious Diseases and Infection Control, Jena University Hospital, Friedrich-Schiller-University, 07747 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,6,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Hotez, P.J., Alvarado, M., Bas\u00e1\u00f1ez, M.G., Bolliger, I., Bourne, R., Boussinesq, M., Brooker, S.J., Brown, A.S., Buckle, G., and Budke, C.M. (2014). The Global Burden of Disease Study 2010: Interpretation and Implications for the Neglected Tropical Diseases. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0002865"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"59","DOI":"10.2471\/BLT.17.198879","article-title":"Praziquantel for the Treatment of Schistosomiasis during Human Pregnancy","volume":"96","author":"Friedman","year":"2018","journal-title":"Bull. World Health Organ."},{"key":"ref_3","unstructured":"World Health Organization (WHO) (2015). Female Genital Schistosomiasis: A Pocket Atlas for Clinical Health-Care Professionals, WHO\/HTM\/NTD\/2015.4."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1080\/pdp.21.4.401.432","article-title":"The Placenta in Hematogenous Infections","volume":"21","author":"Bittencourt","year":"2002","journal-title":"Pediatr. Pathol. Mol. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1186\/s13071-021-04642-4","article-title":"Prevalence of schistosomiasis and its association with anemia among pregnant women: A systematic review and meta-analysis","volume":"14","author":"Adam","year":"2021","journal-title":"Parasites Vectors"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e193","DOI":"10.1016\/S1473-3099(17)30490-5","article-title":"Schistosomiasis in the first 1000 days","volume":"18","author":"Freer","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.pt.2007.02.006","article-title":"Schistosomiasis and Pregnancy","volume":"23","author":"Friedman","year":"2007","journal-title":"Trends Parasitol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"f3443","DOI":"10.1136\/bmj.f3443","article-title":"Anaemia, prenatal iron use, and risk of adverse pregnancy outcomes: Systematic review and meta-analysis","volume":"346","author":"Haider","year":"2013","journal-title":"BMJ"},{"key":"ref_9","first-page":"76","article-title":"Placental Bilharziasis","volume":"3","author":"Sutherland","year":"1965","journal-title":"S. Afr. J. Obstet. Gynaecol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1002\/j.1879-3479.1972.tb00812.x","article-title":"Placental Bilharziasis","volume":"10","author":"Renaud","year":"1972","journal-title":"Int. J. Gynecol. Obstet."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Holtfreter, M.C., Neubauer, H., Groten, T., El-Adawy, H., Pastuschek, J., Richter, J., H\u00e4ussinger, D., Pletz, M.W., and Schleenvoigt, B.T. (2017). Improvement of a tissue maceration technique for the determination of placental involvement in schistosomiasis. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005551"},{"key":"ref_12","first-page":"60","article-title":"Methodological quality and synthesis of case series and case reports","volume":"23","author":"Murad","year":"2018","journal-title":"Evid. Based Med."},{"key":"ref_13","first-page":"149","article-title":"A bilharziose na Africa oriental portuguesa e sua importancia na etiolog\u00eda dos carcinomas primitivos do f\u00edgado dos ind\u00edgenas","volume":"5","author":"Prates","year":"1948","journal-title":"An. Inst. Med. Trop."},{"key":"ref_14","first-page":"113","article-title":"Placental Schistosomiasis","volume":"3","author":"Bittencourt","year":"1969","journal-title":"Gaz. M\u00e9dica Bahia"},{"key":"ref_15","first-page":"273","article-title":"Placentite esquistosom\u00f3tica","volume":"85","author":"Viggiano","year":"1978","journal-title":"J. Bras. Ginecol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"571","DOI":"10.4269\/ajtmh.1980.29.571","article-title":"Placental Involvement in Schistosomiasis Mansoni\u2014Report of Four Cases","volume":"29","author":"Bittencourt","year":"1980","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_17","first-page":"788","article-title":"Schistosoma mansoni eggs in the placenta: An unusual finding","volume":"5","author":"Peres","year":"1994","journal-title":"Rev. Hosp. S\u00e4o Paulo Esc. Paul. Med"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1007\/s15010-014-0684-3","article-title":"Placental Schistosoma haematobium infection in a German returnee from Malawi","volume":"42","author":"Schleenvoigt","year":"2014","journal-title":"Infection"},{"key":"ref_19","unstructured":"Fujinami, A., and Nakamura, H. (1911). On the prophylaxis of schistosomiasis and some investigations on infection with this disease. Chugi- Iji Shimpo, 753."},{"key":"ref_20","first-page":"20","article-title":"Beitr\u00e4ge zur Frage der kongenitalen Invasion von Schistosoma japonicum","volume":"4","author":"Narabayashi","year":"1914","journal-title":"Verhandl. Jap. Path. Gesellsch."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"256","DOI":"10.2307\/3271662","article-title":"Development in Prenatal Infestation of Belascaris","volume":"13","author":"Augustine","year":"1927","journal-title":"J. Parasitol."},{"key":"ref_22","unstructured":"Rodrigues, M.A. (1968, January 9). Placental bilharziasis\u2014A preliminary report. Proceedings of the Abstracts of the 7th International Congress of International Academy of Pathology, Milano, Italy."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Franz, R., Hahn, A., Hagen, R.M., Rohde, H., Eberhardt, K.A., Ehrhardt, S., Baum, J., Claussen, L., Feldt, T., and Hinz, R. (2023). Screening for Resistant Bacteria, Antimicrobial Resistance Genes, Sexually Transmitted Infections and Schistosoma spp. in Tissue Samples from Predominantly Vaginally Delivered Placentae in Ivory Coast and Ghana. Pathogens, 12.","DOI":"10.3390\/pathogens12080999"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/0001-706X(92)90066-7","article-title":"Schistosoma Haematobium Infection in Pregnancy","volume":"50","author":"Siegrist","year":"1992","journal-title":"Acta Trop."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/S0001-706X(00)00129-7","article-title":"Investigation of association between female genital tract diseases and Schistosomiasis japonica infection","volume":"77","author":"Qunhua","year":"2000","journal-title":"Acta Trop."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.ijpara.2016.11.001","article-title":"Urogenital schistosomiasis during pregnancy is associated with low birth weight delivery: Analysis of a prospective cohort of pregnant women and their offspring in Gabon","volume":"47","author":"Honkpehedji","year":"2017","journal-title":"Int. J. Parasitol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1111\/tmi.13591","article-title":"Association of low birth weight and polyparasitic infection during pregnancy in Lambar\u00e9n\u00e9, Gabon","volume":"26","author":"Adegbite","year":"2021","journal-title":"Trop. Med. Int. Health"},{"key":"ref_28","first-page":"575","article-title":"Transplacental Transfer of Schistosomal Antigens and Antibodies","volume":"22","author":"Romia","year":"1992","journal-title":"J. Egypt. Soc. Parasitol."},{"key":"ref_29","first-page":"773","article-title":"Transmission of Circulating Schistosomal Antigens from Infected Mothers to Their Newborns","volume":"27","author":"Hassan","year":"1997","journal-title":"J. Egypt. Soc. Parasitol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"647","DOI":"10.4269\/ajtmh.2003.68.647","article-title":"Placental and oral delivery of Schistosoma mansoni antigen from infected mothers to their newborns and children","volume":"68","author":"Attallah","year":"2003","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1128\/IAI.01149-12","article-title":"Schistosome egg antigens elicit a proinflammatory response by trophoblast cells of the human placenta","volume":"81","author":"McDonald","year":"2013","journal-title":"Infect. Immun."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1128\/IAI.01072-10","article-title":"Maternal schistosomiasis japonica is associated with maternal, placental, and fetal inflammation","volume":"79","author":"Kurtis","year":"2011","journal-title":"Infect. Immun."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1093\/infdis\/jit446","article-title":"Schistosomiasis japonica during pregnancy is associated with elevated endotoxin levels in maternal and placental compartments","volume":"209","author":"McDonald","year":"2014","journal-title":"J. Infect. Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"321","DOI":"10.4269\/ajtmh.2011.10-0397","article-title":"Short report: Human schistosomiasis is associated with endotoxemia and toll-like receptor 2- and 4-bearing B cells","volume":"84","author":"Onguru","year":"2011","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5721","DOI":"10.4049\/jimmunol.164.11.5721","article-title":"Gestational Age-Dependent Expression of IL-10 and Its Receptor in Human Placental Tissues and Isolated Cytotrophoblasts","volume":"164","author":"Hanna","year":"2000","journal-title":"J. Immunol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1034\/j.1600-0897.2002.1o057.x","article-title":"Spontaneous secretion of interleukin-4, interleukin-10 and interferon-\u03b3 by first trimester decidual mononuclear cells","volume":"47","author":"Ekerfelt","year":"2002","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1038\/ni.3131","article-title":"Immune mechanisms at the maternal-fetal interface: Perspectives and challenges","volume":"16","author":"PrabhuDas","year":"2015","journal-title":"Nat. Immunol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1987","DOI":"10.1086\/315135","article-title":"Malaria and pregnancy: Placental cytokine expression and its relationship to intrauterine growth retardation","volume":"180","author":"Moormann","year":"1999","journal-title":"J. Infect. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Abioye, A.I., McDonald, E.A., Park, S., Joshi, A., Kurtis, J.D., Wu, H., Pond-Tor, S., Sharma, S., Ernerudh, J., and Baltazar, P. (2019). Maternal, placental and cord blood cytokines and the risk of adverse birth outcomes among pregnant women infected with schistosoma japonicum in the Philippines. PLoS Negl. Trop. Dis., 13.","DOI":"10.1371\/journal.pntd.0007371"},{"key":"ref_40","unstructured":"World Health Organization (WHO) (2002). Report of the WHO Informal Consultation on the use of Praziquantel during Pregnancy\/Lactation and Albendazole\/Mebendazole in Children under 24 Months."},{"key":"ref_41","unstructured":"World Health Organization (WHO) (2022). WHO Guideline on Control and Elimination of Human Schistosomiasis."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1086\/649924","article-title":"Effects of deworming during pregnancy on maternal and perinatal outcomes in entebbe, Uganda: A randomized controlled Trial","volume":"50","author":"Ndibazza","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/S1473-3099(15)00345-X","article-title":"A randomized double blind placebo controlled trial assessing the efficacy and safety of praziquantel for the treatment of human schistosomiasis during pregnancy","volume":"16","author":"Olveda","year":"2016","journal-title":"Lancet Infect. Dis."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Honkpehedji, Y.J., Adegnika, A.A., Dejon-Agobe, J.C., Zinsou, J.F., Mba, R.B., Gerstenberg, J., Rakotozandrindrainy, R., Rakotoarivelo, R.A., Rasamoelina, T., and Sicuri, E. (2020). Prospective, observational study to assess the performance of CAA measurement as a diagnostic tool for the detection of Schistosoma haematobium infections in pregnant women and their child in Lambar\u00e9n\u00e9, Gabon: Study protocol of the freeBILy clinical trial. BMC Infect. Dis., 20.","DOI":"10.1186\/s12879-020-05445-1"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1186\/s40001-023-01202-7","article-title":"Investigation on birth weight outcomes in schistosomiasis and praziquantel research: A correspondence","volume":"28","author":"Holtfreter","year":"2023","journal-title":"Eur. J. Med. Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"n71","DOI":"10.1136\/bmj.n71","article-title":"The PRISMA 2020 statement: An updated guideline for reporting systematic reviews","volume":"372","author":"Page","year":"2021","journal-title":"BMJ"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/6\/470\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:52:57Z","timestamp":1760107977000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/6\/470"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,3]]},"references-count":46,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2024,6]]}},"alternative-id":["pathogens13060470"],"URL":"https:\/\/doi.org\/10.3390\/pathogens13060470","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,3]]}}}