{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T10:22:33Z","timestamp":1789640553153,"version":"4.0.0"},"reference-count":63,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,6,23]],"date-time":"2025-06-23T00:00:00Z","timestamp":1750636800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Pregnancies complicated by fetal growth restriction are associated with specific bacterial abundances and elevation of proinflammatory cytokines. The aim of the study was to simultaneously analyze the relation between the gut and placenta microbiome and cytokine profile in pregnant women with fetuses appropriate (AGA) and small for gestational age (SGA).<\/jats:p><\/jats:sec><jats:sec><jats:title>Material and methods<\/jats:title><jats:p>Women with singleton pregnancies at or beyond 32 weeks of gestation were recruited. 11 delivered SGA newborns (study group) and 11 AGA newborns (control group). Samples of maternal venous blood, stool and placenta were collected perinatally.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>In SGA group lower Chao index in placental samples collected from maternal side, while higher Chao index in placental samples collected from fetal side were observed. Taxonomic analysis identified four significantly less abundant genera in samples collected from maternal side. No taxa remained significant after correction in samples from fetal side, but several taxa showed trends of differing abundance. <jats:italic>Veillonella<\/jats:italic> showed a trend toward higher abundance in stool samples in SGA group, while other taxa were significant only at a lower threshold. Metabolite analysis revealed that hexanoic acid was significantly elevated compound in the stool of women from the SGA group. <jats:italic>Proteobacteria<\/jats:italic> unclassified and <jats:italic>Halomonadaceae<\/jats:italic> correlated with stool metabolites, while IL-6 and TNF-\u03b1 correlated with specific bacterial groups.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>Specific changes in the gut microbiome and metabolome as well as placenta microbiome of women with SGA have been observed, with additional associations with inflammatory cytokine levels, suggesting a potential role of these factors in SGA development and highlighting the need for further research.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fcimb.2025.1596588","type":"journal-article","created":{"date-parts":[[2025,6,23]],"date-time":"2025-06-23T04:13:22Z","timestamp":1750652002000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Maternal and placental microbiome and immune crosstalk in pregnancies with small-for-gestational-age fetuses \u2013 a pilot case-control study"],"prefix":"10.3389","volume":"15","author":[{"given":"Katarzyna","family":"Kosi\u0144ska-Kaczy\u0144ska","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominika","family":"Krawczyk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martyna","family":"Bednorz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katarzyna","family":"Chaberek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agnieszka","family":"Czapska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Magdalena","family":"Zgliczy\u0144ska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Krzysztof","family":"Goryca","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Magdalena","family":"Pi\u0105tkowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aneta","family":"Ba\u0142abas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pawe\u0142","family":"Czarnowski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalia","family":"\u017beber-Lubecka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,6,23]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"237ra265","DOI":"10.1126\/scitranslmed.3008599","article-title":"The placenta harbors a unique microbiome","volume":"6","author":"Aagaard","year":"2014","journal-title":"Sci. Transl. Med."},{"key":"B2","doi-asserted-by":"publisher","first-page":"98","DOI":"10.12891\/ceog3295.2017","article-title":"Pro-inflammatory and anti-inflammatory cytokine profiles in fetal growth restriction","volume":"44","author":"Al-Azemi","year":"2017","journal-title":"Clin. Exp. Obstet Gynecol."},{"key":"B3","volume-title":"rCCA nutrimouse case study|mixOmics","year":""},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.7754\/Clin.Lab.2022.211244","article-title":"Firmicutes\/bacteroidetes ratio in the gut microbiota and IL-1\u03b2, IL-6, IL-8, TLR2, TLR4, TLR5 gene expressions in type 2 diabetes","volume":"68","author":"Bahar-Tokman","year":"2022","journal-title":"Clin. Lab."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1099","DOI":"10.1046\/j.1600-0412.2003.00259.x","article-title":"Inflammatory cytokines in intrauterine growth retardation","volume":"82","author":"Bartha","year":"2003","journal-title":"Acta Obstet Gynecol Scand."},{"key":"B6","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: A practical and powerful approach to multiple testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Society: Ser. B (Methodological)."},{"key":"B7","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1093\/pcmedi\/pbz008","article-title":"Gut microbiota metabolite regulation of host defenses at mucosal surfaces: implication in precision medicine","volume":"2","author":"Bilotta","year":"2019","journal-title":"Precis Clin. Med."},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1038\/s41390-025-04075-0","article-title":"Short-chain fatty acids-a key link between the gut microbiome and T-lymphocytes in neonates","author":"Bui","year":"2025","journal-title":"Pediatr. Res"},{"key":"B9","doi-asserted-by":"publisher","first-page":"513","DOI":"10.1136\/gutjnl-2019-319101","article-title":"Gut dysbiosis induces the development of pre-eclampsia through bacterial translocation","volume":"69","author":"Chen","year":"2020","journal-title":"Gut"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms7120583","article-title":"The th17\/treg cell balance: A gut microbiota-modulated story","volume":"7","author":"Cheng","year":"2019","journal-title":"Microorganisms"},{"key":"B11","doi-asserted-by":"publisher","first-page":"851","DOI":"10.1038\/s41564-018-0202-y","article-title":"Recognizing the reagent microbiome","volume":"3","author":"de Goffau","year":"2018","journal-title":"Nat. Microbiology."},{"key":"B12","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1038\/s41586-019-1451-5","article-title":"Human placenta has no microbiome but can contain potential pathogens","volume":"572","author":"de Goffau","year":"2019","journal-title":"Nature"},{"key":"B13","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1136\/gutjnl-2013-306423","article-title":"Faecal metabolite profiling identifies medium-chain fatty acids as discriminating compounds in IBD","volume":"64","author":"De Preter","year":"2015","journal-title":"Gut"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.664371","article-title":"Upregulated IL-32 expression and reduced gut short chain fatty acid caproic acid in people living with HIV with subclinical atherosclerosis","volume":"12","author":"El-Far","year":"2021","journal-title":"Front. Immunol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1007\/s10815-015-0614-z","article-title":"Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit","volume":"33","author":"Franasiak","year":"2016","journal-title":"J. Assist Reprod. Genet."},{"key":"B16","doi-asserted-by":"publisher","first-page":"103354","DOI":"10.1016\/j.retram.2022.103354","article-title":"The fecal microbiota of gravidas with fetal growth restriction newborns characterized by metagenomic sequencing","volume":"71","author":"He","year":"2023","journal-title":"Curr. Res. Transl. Med."},{"key":"B17","doi-asserted-by":"publisher","first-page":"828","DOI":"10.1007\/s43032-020-00374-5","article-title":"Intrauterine growth restriction is associated with unique features of the reproductive microbiome","volume":"28","author":"Hu","year":"2021","journal-title":"Reprod. Sci."},{"key":"B18","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.ejogrb.2023.08.013","article-title":"Systematic review and meta-analysis of maternal and fetal outcomes among pregnant women with bacterial vaginosis","volume":"289","author":"Kenfack-Zanguim","year":"2023","journal-title":"Eur. J. Obstet Gynecol Reprod. Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1038\/s41423-023-00987-1","article-title":"Complex regulatory effects of gut microbial short-chain fatty acids on immune tolerance and autoimmunity","volume":"20","author":"Kim","year":"2023","journal-title":"Cell. Mol. Immunol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1038\/s41575-023-00864-2","article-title":"The maternal gut microbiome in pregnancy: implications for the developing immune system","volume":"21","author":"Koren","year":"2024","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fnut.2022.1092846","article-title":"Characteristics of the gut microbiome in esports players compared with those in physical education students and professional athletes","volume":"9","author":"Kulecka","year":"2022","journal-title":"Front. Nutr."},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2023.1190910","article-title":"Diarrheal-associated gut dysbiosis in cancer and inflammatory bowel disease patients is exacerbated by Clostridioides difficile infection","volume":"13","author":"Kulecka","year":"2023","journal-title":"Front. Cell Infect. Microbiol."},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2022.911852","article-title":"The composition of placental microbiota and its association with adverse pregnancy outcomes","volume":"13","author":"La","year":"2022","journal-title":"Front. Microbiol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1186\/s40168-018-0529-x","article-title":"Detecting eukaryotic microbiota with single-cell sensitivity in human tissue","volume":"6","author":"Lager","year":"2018","journal-title":"Microbiome"},{"key":"B25","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1002\/uog.22134","article-title":"ISUOG Practice Guidelines: diagnosis and management of small-for-gestational-age fetus and fetal growth restriction","volume":"56","author":"Lees","year":"2020","journal-title":"Ultrasound Obstet Gynecol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1186\/s40168-018-0575-4","article-title":"Lack of detection of a human placenta microbiome in samples from preterm and term deliveries","volume":"6","author":"Leiby","year":"2018","journal-title":"Microbiome"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0036297","article-title":"Medium chain fatty acids are selective peroxisome proliferator activated receptor (PPAR) gamma activators and pan-PPAR partial agonists","volume":"7","author":"Liberato","year":"2012","journal-title":"PloS One"},{"key":"B28","doi-asserted-by":"publisher","first-page":"386","DOI":"10.1007\/s00018-022-04379-y","article-title":"Maternal gut microbiota Bifidobacterium promotes placental morphogenesis, nutrient transport and fetal growth in mice","volume":"79","author":"Lopez-Tello","year":"2022","journal-title":"Cell Mol. Life Sci."},{"key":"B29","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1111\/j.1600-0897.2011.01089.x","article-title":"Short-chain fatty acids induce pro-inflammatory cytokine production alone and in combination with toll-like receptor ligands","volume":"67","author":"Mirmonsef","year":"2012","journal-title":"Am. J. Reprod. Immunol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"684","DOI":"10.1016\/j.ajog.2016.09.075","article-title":"Evidence that the endometrial microbiota has an effect on implantation success or failure","volume":"215","author":"Moreno","year":"2016","journal-title":"Am. J. Obstet Gynecol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"2324","DOI":"10.1007\/s43032-022-01153-0","article-title":"Preterm prelabor rupture of membranes linked to vaginal bacteriome of pregnant females in the early second trimester: a case-cohort design","volume":"30","author":"Mu","year":"2023","journal-title":"Reprod. Sci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s44342-024-00001-8","article-title":"Gut metagenomic analysis of gastric cancer patients reveals Akkermansia, Gammaproteobacteria, and Veillonella microbiota as potential non-invasive biomarkers","volume":"22","author":"Nath","year":"2024","journal-title":"Genomics Informatics."},{"key":"B33","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1002\/uog.2018.52.issue-1","article-title":"Fetal Medicine Foundation fetal and neonatal population weight charts","volume":"52","author":"Nicolaides","year":"2018","journal-title":"Ultrasound Obstet Gynecol."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2024.1445300","article-title":"Vaginal microbiota of pregnant women with Ureaplasma urealyticum and Mycoplasma hominis infections","volume":"14","author":"Oh","year":"2024","journal-title":"Front. Cell Infect. Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"5","DOI":"10.21149\/8133","article-title":"High relative abundance of firmicutes and increased TNF-\u03b1 levels correlate with obesity in children","volume":"60","author":"Orbe-Orihuela","year":"2018","journal-title":"Salud Publica Mex."},{"key":"B36","doi-asserted-by":"publisher","first-page":"11200","DOI":"10.1038\/s41598-017-11514-4","article-title":"Microbial communities in placentas from term normal pregnancy exhibit spatially variable profiles","volume":"7","author":"Parnell","year":"2017","journal-title":"Sci. Rep."},{"key":"B37","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1186\/s12866-022-02457-6","article-title":"Maternal microbiota-derived metabolic profile in fetal murine intestine, brain and placenta","volume":"22","author":"Pessa-Morikawa","year":"2022","journal-title":"BMC Microbiol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"734865","DOI":"10.1155\/2012\/734865","article-title":"Intrauterine growth restriction: cytokine profiles of trophoblast antigen-stimulated maternal lymphocytes","volume":"2012","author":"Raghupathy","year":"2012","journal-title":"Clin. Dev. Immunol."},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.00973","article-title":"An overview on fecal branched short-chain fatty acids along human life and as related with body mass index: associated dietary and anthropometric factors","volume":"11","author":"Rios-Covian","year":"2020","journal-title":"Front. Microbiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"4148","DOI":"10.3390\/nu15194148","article-title":"Pro-inflammatory diet is correlated with high veillonella rogosae, gut inflammation and clinical relapse of inflammatory bowel disease","volume":"15","author":"Rocha","year":"2023","journal-title":"Nutrients"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.3390\/cancers16010104","article-title":"Commensal fecal microbiota profiles associated with initial stages of intestinal mucosa damage: A pilot study","volume":"16","author":"Ruiz-Saavedra","year":"2023","journal-title":"Cancers (Basel)."},{"key":"B42","doi-asserted-by":"publisher","first-page":"146.e141","DOI":"10.1016\/j.ajog.2019.04.036","article-title":"Visualization of microbes by 16S in situ hybridization in term and preterm placentas without intraamniotic infection","volume":"221","author":"Seferovic","year":"2019","journal-title":"Am. J. Obstet Gynecol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"1030","DOI":"10.1080\/15592294.2019.1629234","article-title":"Maternal dyslipidemia during early pregnancy and epigenetic ageing of the placenta","volume":"14","author":"Shrestha","year":"2019","journal-title":"Epigenetics"},{"key":"B44","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1126\/science.1241165","article-title":"The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis","volume":"341","author":"Smith","year":"2013","journal-title":"Science"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.3390\/ijms24086922","article-title":"Comparative analysis of the placental microbiome in pregnancies with late fetal growth restriction versus physiological pregnancies","volume":"24","author":"Stupak","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"9986187","DOI":"10.1155\/2024\/9986187","article-title":"Potential association of gut microbial metabolism and circulating mRNA based on multiomics sequencing analysis in fetal growth restriction","volume":"2024","author":"Tang","year":"2024","journal-title":"Mediators Inflamm."},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.1128\/spectrum.00076-23","article-title":"Alterations in the gut microbiome and metabolisms in pregnancies with fetal growth restriction","volume":"11","author":"Tao","year":"2023","journal-title":"Microbiol Spectr."},{"key":"B48","doi-asserted-by":"publisher","first-page":"267.e261","DOI":"10.1016\/j.ajog.2018.10.018","article-title":"Does the human placenta delivered at term have a microbiota? Results of cultivation, quantitative real-time PCR, 16S rRNA gene sequencing, and metagenomics","volume":"220","author":"Theis","year":"2019","journal-title":"Am. J. Obstet Gynecol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1186\/s12884-022-04635-w","article-title":"Characteristics of the gut microbiota in pregnant women with fetal growth restriction","volume":"22","author":"Tu","year":"2022","journal-title":"BMC Pregnancy Childbirth."},{"key":"B50","doi-asserted-by":"publisher","first-page":"1057","DOI":"10.1097\/CM9.0000000000000734","article-title":"Gut microbiota dysbiosis in preeclampsia patients in the second and third trimesters","volume":"133","author":"Wang","year":"2020","journal-title":"Chin Med. J. (Engl)."},{"key":"B51","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1136\/gutjnl-2018-317836","article-title":"Alterations of gut microbiome in autoimmune hepatitis","volume":"69","author":"Wei","year":"2020","journal-title":"Gut"},{"key":"B52","doi-asserted-by":"publisher","first-page":"7025","DOI":"10.1080\/14767058.2021.1936487","article-title":"Investigating the origin of the fetal gut and placenta microbiome in twins","volume":"35","author":"Williams","year":"2022","journal-title":"J. Matern Fetal Neonatal Med."},{"key":"B53","doi-asserted-by":"publisher","first-page":"9905","DOI":"10.1038\/s41598-019-46173-0","article-title":"Does the endometrial cavity have a molecular microbial signature","volume":"9","author":"Winters","year":"2019","journal-title":"Sci. Rep."},{"key":"B54","doi-asserted-by":"publisher","first-page":"728","DOI":"10.1186\/s12884-024-06930-0","article-title":"Alterations in maternal-fetal gut and amniotic fluid microbiota associated with fetal growth restriction","volume":"24","author":"Xiao","year":"2024","journal-title":"BMC Pregnancy Childbirth."},{"key":"B55","doi-asserted-by":"publisher","first-page":"525","DOI":"10.1093\/toxsci\/kfi300","article-title":"Effect of N-acetylcysteine on lipopolysaccharide-induced intra-uterine fetal death and intra-uterine growth retardation in mice","volume":"88","author":"Xu","year":"2005","journal-title":"Toxicol. Sci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1038\/s41522-023-00383-7","article-title":"Ecological change of the gut microbiota during pregnancy and progression to dyslipidemia","volume":"9","author":"Yang","year":"2023","journal-title":"NPJ Biofilms Microbiomes."},{"key":"B57","doi-asserted-by":"publisher","first-page":"103455","DOI":"10.1016\/j.jri.2021.103455","article-title":"The evidence for placental microbiome and its composition in healthy pregnancies: A systematic review","volume":"149","author":"Zakis","year":"2022","journal-title":"J. Reprod. Immunol."},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0302270","article-title":"Cervical microbiota dysbiosis associated with high-risk Human Papillomavirus infection","volume":"19","author":"Zeber-Lubecka","year":"2024","journal-title":"PloS One"},{"key":"B59","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2024.1279132","article-title":"Breast cancer but not the menopausal status is associated with small changes of the gut microbiota","volume":"14","author":"Zeber-Lubecka","year":"2024","journal-title":"Front. Oncol."},{"key":"B60","doi-asserted-by":"publisher","first-page":"6416","DOI":"10.3748\/wjg.v25.i43.6416","article-title":"Altered profiles of fecal metabolites correlate with visceral hypersensitivity and may contribute to symptom severity of diarrhea-predominant irritable bowel syndrome","volume":"25","author":"Zhang","year":"2019","journal-title":"World J. Gastroenterol."},{"key":"B61","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0082713","article-title":"Folic acid protects against lipopolysaccharide-induced preterm delivery and intrauterine growth restriction through its anti-inflammatory effect in mice","volume":"8","author":"Zhao","year":"2013","journal-title":"PloS One"},{"key":"B62","doi-asserted-by":"publisher","first-page":"20662","DOI":"10.1002\/jcp.v234.11","article-title":"Exosomal microRNA-155-5p from PDLSCs regulated Th17\/Treg balance by targeting sirtuin-1 in chronic periodontitis","volume":"234","author":"Zheng","year":"2019","journal-title":"J. Cell Physiol."},{"key":"B63","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1186\/s13059-022-02655-5","article-title":"LinDA: linear models for differential abundance analysis of microbiome compositional data","volume":"23","author":"Zhou","year":"2022","journal-title":"Genome Biol."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2025.1596588\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,6,23]],"date-time":"2025-06-23T04:13:24Z","timestamp":1750652004000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2025.1596588\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6,23]]},"references-count":63,"alternative-id":["10.3389\/fcimb.2025.1596588"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2025.1596588","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,23]]},"article-number":"1596588"}}