{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T03:38:19Z","timestamp":1783049899237,"version":"3.54.6"},"reference-count":50,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2025,5,14]],"date-time":"2025-05-14T00:00:00Z","timestamp":1747180800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R21AI111242"],"award-info":[{"award-number":["R21AI111242"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01AI050240"],"award-info":[{"award-number":["R01AI050240"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01AI168923"],"award-info":[{"award-number":["R01AI168923"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,7,30]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Placental malaria is characterized by the accumulation of Plasmodium falciparum-infected erythrocytes and maternal inflammation in the intervillous spaces of the placenta. These features are associated with placental damage and fetal compromise. However, understanding of the mechanisms that lead to poor pregnancy outcome and interventions targeting excessive host responses to placental malaria are still lacking. The syncytiotrophoblast, a cell of fetal origin, is known to be responsive to malaria-infected erythrocytes as well as the malaria toxin, hemozoin, but its susceptibility to oxidative stress and how this might contribute to placental damage and dysfunction has not yet been directly investigated.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>The characteristics and key drivers of the syncytiotrophoblast response to oxidative stress were investigated using ex vivo human placental tissues and primary trophoblasts isolated from healthy pregnant women. Primary syncytiotrophoblast was exposed to hemozoin and tumor necrosis factor, a critical inflammatory cytokine, to model conditions found in human placental malaria.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>The data show remarkable lipid peroxidation in human placental samples from a malaria endemic setting and evidence of a modulated antioxidant response at the transcriptional level. Likewise, primary human syncytiotrophoblast exposed to hemozoin, tumor necrosis factor, and tumor necrosis factor combined with hemozoin in vitro exhibited increased markers of an antioxidative response, and, with hemozoin alone, oxidation of lipids and DNA.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>These results suggest that oxidative stress in syncytiotrophoblast is promoted by both hemozoin exposure and maternal inflammatory responses to placental malaria, and contribute to an increased understanding of placental dysfunction and compromise in this infection.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/infdis\/jiaf243","type":"journal-article","created":{"date-parts":[[2025,5,8]],"date-time":"2025-05-08T07:41:41Z","timestamp":1746690101000},"page":"e174-e185","source":"Crossref","is-referenced-by-count":5,"title":["Placental Malaria Induces Oxidative Stress in Human Syncytiotrophoblast"],"prefix":"10.1093","volume":"232","author":[{"given":"Demba","family":"Sarr","sequence":"first","affiliation":[{"name":"1Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia , Athens, Georgia ,","place":["USA"]},{"name":"Center for Tropical and Emering Global Diseases, University of Georgia , Athens, Georgia ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4909-0759","authenticated-orcid":false,"given":"Alicer K","family":"Andrew","sequence":"additional","affiliation":[{"name":"1Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia , Athens, Georgia ,","place":["USA"]},{"name":"Center for Tropical and Emering Global Diseases, University of Georgia , Athens, Georgia ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9905-9795","authenticated-orcid":false,"given":"Ashish K","family":"Shukla","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Immunology, College of Veterinary Medicine, University of Florida , Gainesville, Florida ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7834-6859","authenticated-orcid":false,"given":"Stephen","family":"Mwalimu","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Immunology, College of Veterinary Medicine, University of Florida , Gainesville, Florida ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5031-3270","authenticated-orcid":false,"given":"Julie M","family":"Moore","sequence":"additional","affiliation":[{"name":"1Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia , Athens, Georgia ,","place":["USA"]},{"name":"Center for Tropical and Emering Global Diseases, University of Georgia , Athens, Georgia ,","place":["USA"]},{"name":"Department of Infectious Diseases and Immunology, College of Veterinary Medicine, University of Florida , Gainesville, Florida ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,5,14]]},"reference":[{"key":"2025073007422247600_jiaf243-B1","doi-asserted-by":"crossref","DOI":"10.30875\/9789287076717","volume-title":"World malaria report 2024","author":"World Health Organization","year":"2024"},{"key":"2025073007422247600_jiaf243-B2","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1186\/s12916-023-02991-8","article-title":"Severe falciparum malaria in pregnancy in Southeast Asia: a multi-centre retrospective cohort study","volume":"21","author":"Saito","year":"2023","journal-title":"BMC Med"},{"key":"2025073007422247600_jiaf243-B3","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1126\/science.272.5267.1502","article-title":"Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta","volume":"272","author":"Fried","year":"1996","journal-title":"Science"},{"key":"2025073007422247600_jiaf243-B4","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/1475-2875-7-42","article-title":"Immunologic activation of human syncytiotrophoblast by Plasmodium falciparum","volume":"7","author":"Lucchi","year":"2008","journal-title":"Malar J"},{"key":"2025073007422247600_jiaf243-B5","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1016\/j.placenta.2011.05.003","article-title":"Natural hemozoin stimulates syncytiotrophoblast to secrete chemokines and recruit peripheral blood mononuclear cells","volume":"32","author":"Lucchi","year":"2011","journal-title":"Placenta"},{"key":"2025073007422247600_jiaf243-B6","first-page":"631","article-title":"Levels of macrophage inflammatory protein 1 alpha (MIP-1 alpha) and MIP-1 beta in intervillous blood plasma samples from women with placental malaria and human immunodeficiency virus infection","volume":"10","author":"Chaisavaneeyakorn","year":"2003","journal-title":"Clin Diagn Lab Immunol"},{"key":"2025073007422247600_jiaf243-B7","doi-asserted-by":"crossref","first-page":"1371","DOI":"10.1086\/344322","article-title":"Immunity to placental malaria. IV. Placental malaria is associated with up-regulation of macrophage migration inhibitory factor in intervillous blood","volume":"186","author":"Chaisavaneeyakorn","year":"2002","journal-title":"J Infect Dis"},{"key":"2025073007422247600_jiaf243-B8","doi-asserted-by":"crossref","first-page":"2759","DOI":"10.4049\/jimmunol.170.5.2759","article-title":"Host response to malaria during pregnancy: placental monocyte recruitment is associated with elevated beta chemokine expression","volume":"170","author":"Abrams","year":"2003","journal-title":"J Immunol"},{"key":"2025073007422247600_jiaf243-B9","doi-asserted-by":"crossref","first-page":"1074","DOI":"10.1086\/378500","article-title":"Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria","volume":"188","author":"Suguitan","year":"2003","journal-title":"J Infect Dis"},{"key":"2025073007422247600_jiaf243-B10","doi-asserted-by":"crossref","first-page":"2523","DOI":"10.4049\/jimmunol.160.5.2523","article-title":"Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes","volume":"160","author":"Fried","year":"1998","journal-title":"J Immunol"},{"key":"2025073007422247600_jiaf243-B11","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/S1473-3099(07)70022-1","article-title":"Malaria in pregnancy: pathogenesis and immunity","volume":"7","author":"Rogerson","year":"2007","journal-title":"Lancet Infect Dis"},{"key":"2025073007422247600_jiaf243-B12","doi-asserted-by":"crossref","first-page":"e31090","DOI":"10.1371\/journal.pone.0031090","article-title":"Maternal malaria induces a procoagulant and antifibrinolytic state that is embryotoxic but responsive to anticoagulant therapy","volume":"7","author":"Avery","year":"2012","journal-title":"PLoS One"},{"key":"2025073007422247600_jiaf243-B13","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.exppara.2012.04.005","article-title":"Plasmodium berghei: influence of infection on the oxidant and antioxidants levels in pregnant BALB\/c mice","volume":"131","author":"Sharma","year":"2012","journal-title":"Exp Parasitol"},{"key":"2025073007422247600_jiaf243-B14","doi-asserted-by":"crossref","first-page":"e32694","DOI":"10.1371\/journal.pone.0032694","article-title":"Role of oxidative stress and apoptosis in the placental pathology of Plasmodium berghei infected mice","volume":"7","author":"Sharma","year":"2012","journal-title":"PLoS One"},{"key":"2025073007422247600_jiaf243-B15","doi-asserted-by":"crossref","first-page":"29","DOI":"10.4049\/immunohorizons.1700002","article-title":"Oxidative stress: a potential therapeutic target in placental malaria","volume":"1","author":"Sarr","year":"2017","journal-title":"ImmunoHorizons"},{"key":"2025073007422247600_jiaf243-B16","doi-asserted-by":"crossref","first-page":"e0134633","DOI":"10.1371\/journal.pone.0134633","article-title":"Impact of placental Plasmodium falciparum malaria on the profile of some oxidative stress biomarkers in women living in Yaounde, Cameroon","volume":"10","author":"Megnekou","year":"2015","journal-title":"PLoS One"},{"key":"2025073007422247600_jiaf243-B17","doi-asserted-by":"crossref","first-page":"21","DOI":"10.4103\/tp.TP_18_20","article-title":"Impact of oxidative stress in response to malarial infection during pregnancy: complications, histological changes, and pregnancy outcomes","volume":"12","author":"Chandrashekhar","year":"2022","journal-title":"Trop Parasitol"},{"key":"2025073007422247600_jiaf243-B18","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1007\/s12291-009-0054-6","article-title":"Evaluation of oxidative stress and antioxidant status of pregnant women suffering from malaria in Cameroon","volume":"24","author":"Tiyong Ifoue","year":"2009","journal-title":"Indian J Clin Biochem"},{"key":"2025073007422247600_jiaf243-B19","doi-asserted-by":"crossref","first-page":"360438","DOI":"10.1155\/2014\/360438","article-title":"Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal","volume":"2014","author":"Ayala","year":"2014","journal-title":"Oxid Med Cell Longev"},{"key":"2025073007422247600_jiaf243-B20","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1128\/IAI.71.1.267-270.2003","article-title":"Placental tumor necrosis factor alpha but not gamma interferon is associated with placental malaria and low birth weight in Malawian women","volume":"71","author":"Rogerson","year":"2003","journal-title":"Infect Immun"},{"key":"2025073007422247600_jiaf243-B21","doi-asserted-by":"crossref","first-page":"119","DOI":"10.4269\/ajtmh.2009.80.119","article-title":"Human immunodeficiency virus co-infection increases placental parasite density and transplacental malaria transmission in western Kenya","volume":"80","author":"Perrault","year":"2009","journal-title":"Am J Trop Med Hyg"},{"key":"2025073007422247600_jiaf243-B22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0022-3476(70)80038-5","article-title":"Clinical assessment of gestational age in the newborn infant","volume":"77","author":"Dubowitz","year":"1970","journal-title":"J Pediatr"},{"key":"2025073007422247600_jiaf243-B23","doi-asserted-by":"crossref","first-page":"C968","DOI":"10.1152\/ajpcell.00154.2010","article-title":"Hypoxia downregulates p53 but induces apoptosis and enhances expression of BAD in cultures of human syncytiotrophoblasts","volume":"299","author":"Chen","year":"2010","journal-title":"Am J Physiol Cell Physiol"},{"key":"2025073007422247600_jiaf243-B24","doi-asserted-by":"crossref","first-page":"4868","DOI":"10.1128\/IAI.72.8.4868-4873.2004","article-title":"Elevated nitric oxide production in children with malarial anemia: hemozoin-induced nitric oxide synthase type 2 transcripts and nitric oxide in blood mononuclear cells","volume":"72","author":"Keller","year":"2004","journal-title":"Infect Immun"},{"key":"2025073007422247600_jiaf243-B25","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1186\/s13000-014-0221-9","article-title":"Different approaches for interpretation and reporting of immunohistochemistry analysis results in the bone tissue\u2014a review","volume":"9","author":"Fedchenko","year":"2014","journal-title":"Diagn Pathol"},{"key":"2025073007422247600_jiaf243-B26","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1016\/j.placenta.2015.04.007","article-title":"Differential roles of inflammation and apoptosis in initiation of mid-gestational abortion in malaria-infected C57BL\/6 and A\/J mice","volume":"36","author":"Sarr","year":"2015","journal-title":"Placenta"},{"key":"2025073007422247600_jiaf243-B27","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1038\/nprot.2008.73","article-title":"Analyzing real-time PCR data by the comparative C(T) method","volume":"3","author":"Schmittgen","year":"2008","journal-title":"Nat Protoc"},{"key":"2025073007422247600_jiaf243-B28","doi-asserted-by":"crossref","first-page":"682668","DOI":"10.3389\/fimmu.2021.682668","article-title":"Myeloperoxidase and other markers of neutrophil activation associate with malaria and malaria\/HIV coinfection in the human placenta","volume":"12","author":"Sarr","year":"2021","journal-title":"Front Immunol"},{"key":"2025073007422247600_jiaf243-B29","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":"2025073007422247600_jiaf243-B30","doi-asserted-by":"publisher","DOI":"10.1038\/s41573-025-01145-0","article-title":"Thirty years of NRF2: advances and therapeutic challenges [published online ahead of print 4 March 2025]","author":"Zhang","journal-title":"Nat Rev Drug Discov"},{"key":"2025073007422247600_jiaf243-B31","doi-asserted-by":"crossref","first-page":"e202302276","DOI":"10.26508\/lsa.202302276","article-title":"Targeting circulating labile heme as a defense strategy against malaria","volume":"7","author":"Ramos","year":"2024","journal-title":"Life Sci Alliance"},{"key":"2025073007422247600_jiaf243-B32","doi-asserted-by":"crossref","first-page":"10.15226\/sojmid\/4\/2\/00154","DOI":"10.15226\/sojmid\/4\/3\/00154","article-title":"Iron supplementation alters heme and heme oxygenase 1 (HO-1) levels in pregnant women in Ghana","volume":"4","author":"Salifu","year":"2016","journal-title":"SOJ Microbiol Infect Dis"},{"key":"2025073007422247600_jiaf243-B33","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1146\/annurev.pharmtox.010909.105600","article-title":"Mechanisms of cell protection by heme oxygenase-1","volume":"50","author":"Gozzelino","year":"2010","journal-title":"Annu Rev Pharmacol Toxicol"},{"key":"2025073007422247600_jiaf243-B34","doi-asserted-by":"crossref","first-page":"1693","DOI":"10.1016\/j.bbadis.2014.06.010","article-title":"Elevated risk of type 2 diabetes for development of Alzheimer disease: a key role for oxidative stress in brain","volume":"1842","author":"Butterfield","year":"2014","journal-title":"Biochim Biophys Acta"},{"key":"2025073007422247600_jiaf243-B35","doi-asserted-by":"crossref","first-page":"24840","DOI":"10.1074\/jbc.M000835200","article-title":"Thioredoxin facilitates the induction of heme oxygenase-1 in response to inflammatory mediators","volume":"275","author":"Wiesel","year":"2000","journal-title":"J Biol Chem"},{"key":"2025073007422247600_jiaf243-B36","doi-asserted-by":"crossref","first-page":"1348","DOI":"10.1038\/s12276-023-01019-8","article-title":"TXNIP: a key protein in the cellular stress response pathway and a potential therapeutic target","volume":"55","author":"Choi","year":"2023","journal-title":"Exp Mol Med"},{"key":"2025073007422247600_jiaf243-B37","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/S1995-7645(11)60076-X","article-title":"Asymptomatic malaria parasitemia does not induce additional oxidative stress in pregnant women of south east Nigeria","volume":"4","author":"Nwagha","year":"2011","journal-title":"Asian Pac J Trop Med"},{"key":"2025073007422247600_jiaf243-B38","first-page":"138","article-title":"Effect of malaria infection on biomarker of lipid peroxidation (malondialdehyde) and lipid profile in pregnant women","volume":"17","author":"Balogun","year":"2022","journal-title":"Sci World J"},{"key":"2025073007422247600_jiaf243-B39","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/0009-8981(82)90360-6","article-title":"Superoxide dismutase in extracellular fluids","volume":"126","author":"Marklund","year":"1982","journal-title":"Clin Chim Acta"},{"key":"2025073007422247600_jiaf243-B40","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/j.placenta.2010.02.007","article-title":"Effects of labor on placental expression of superoxide dismutases in preeclampsia","volume":"31","author":"Roland","year":"2010","journal-title":"Placenta"},{"key":"2025073007422247600_jiaf243-B41","doi-asserted-by":"crossref","first-page":"702","DOI":"10.4049\/jimmunol.1004117","article-title":"TNF mediates the sustained activation of nrf2 in human monocytes","volume":"187","author":"Rushworth","year":"2011","journal-title":"J Immunol"},{"key":"2025073007422247600_jiaf243-B42","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1186\/s12936-015-0888-8","article-title":"Nrf2-driven CD36 and HO-1 gene expression in circulating monocytes correlates with favourable clinical outcome in pregnancy-associated malaria","volume":"14","author":"Aubouy","year":"2015","journal-title":"Malar J"},{"key":"2025073007422247600_jiaf243-B43","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1186\/s12905-025-03682-7","article-title":"Silencing circRNA-ZFAND6 induces trophoblast apoptosis by activating the mitochondrial pathway through the miR-575\/SOD2 axis in unexplained recurrent spontaneous abortion","volume":"25","author":"Wang","year":"2025","journal-title":"BMC Womens Health"},{"key":"2025073007422247600_jiaf243-B44","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1016\/j.micinf.2010.07.001","article-title":"Innate inflammatory response to the malarial pigment hemozoin","volume":"12","author":"Shio","year":"2010","journal-title":"Microbes Infect"},{"key":"2025073007422247600_jiaf243-B45","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/978-1-61779-382-0_12","article-title":"Relation between mitochondrial membrane potential and ROS formation","volume":"810","author":"Suski","year":"2012","journal-title":"Methods Mol Biol"},{"key":"2025073007422247600_jiaf243-B46","doi-asserted-by":"crossref","first-page":"19566","DOI":"10.1038\/s41598-019-55588-8","article-title":"A novel murine model for assessing fetal and birth outcomes following transgestational maternal malaria infection","volume":"9","author":"Morffy Smith","year":"2019","journal-title":"Sci Rep"},{"key":"2025073007422247600_jiaf243-B47","doi-asserted-by":"crossref","first-page":"5392","DOI":"10.1073\/pnas.1218412110","article-title":"Protein complex directs hemoglobin-to-hemozoin formation in Plasmodium falciparum","volume":"110","author":"Chugh","year":"2013","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2025073007422247600_jiaf243-B48","doi-asserted-by":"crossref","first-page":"1006","DOI":"10.1097\/00000478-199808000-00011","article-title":"Massive chronic intervillositis of the placenta associated with malaria infection","volume":"22","author":"Ordi","year":"1998","journal-title":"Am J Surg Pathol"},{"key":"2025073007422247600_jiaf243-B49","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1038\/s42255-022-00591-z","article-title":"Guidelines for measuring reactive oxygen species and oxidative damage in cells and in vivo","volume":"4","author":"Murphy","year":"2022","journal-title":"Nat Metab"},{"key":"2025073007422247600_jiaf243-B50","doi-asserted-by":"crossref","first-page":"108","DOI":"10.3390\/nu15010108","article-title":"Influence of oxidative stress and inflammation on nutritional status and neural plasticity: new perspectives on post-stroke neurorehabilitative outcome","volume":"15","author":"Ciancarelli","year":"2022","journal-title":"Nutrients"}],"container-title":["The Journal of Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jid\/advance-article-pdf\/doi\/10.1093\/infdis\/jiaf243\/63144869\/jiaf243.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jid\/article-pdf\/232\/1\/e174\/63144869\/jiaf243.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jid\/article-pdf\/232\/1\/e174\/63144869\/jiaf243.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T11:42:32Z","timestamp":1753875752000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jid\/article\/232\/1\/e174\/8128682"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,14]]},"references-count":50,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,5,14]]},"published-print":{"date-parts":[[2025,7,30]]}},"URL":"https:\/\/doi.org\/10.1093\/infdis\/jiaf243","relation":{},"ISSN":["0022-1899","1537-6613"],"issn-type":[{"value":"0022-1899","type":"print"},{"value":"1537-6613","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,7,15]]},"published":{"date-parts":[[2025,5,14]]}}}