{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,5]],"date-time":"2026-06-05T18:06:24Z","timestamp":1780682784838,"version":"3.54.1"},"reference-count":122,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2026,6,5]],"date-time":"2026-06-05T00:00:00Z","timestamp":1780617600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Placental examination is frequently performed following adverse fetal or neonatal neurologic outcomes to elucidate the cause or timing of injury. In practice, however, the placenta more often serves as a biologic archive of fetal stress, adaptation, and reduced physiologic reserve rather than a definitive record of injury. This review synthesizes current research linking placental pathology to perinatal brain injury, with emphasis on biological mechanisms and temporal interpretation. We examine how placental findings inform assessments of intrauterine stress, impaired placental or fetal perfusion, inflammation, and diminished placental reserve. Surrogate markers of fetal stress, including nucleated red blood cells and intrauterine meconium passage, provide contextual evidence regarding the duration and severity of intrauterine compromise but do not establish causality. Finally, we review acute circulatory disruption, chronic or intermittent impairment of fetal blood flow, umbilical cord-related pathology, and immune-mediated placental disorders that increase vulnerability to neurologic injury.<\/jats:p>","DOI":"10.3390\/jcm15114380","type":"journal-article","created":{"date-parts":[[2026,6,5]],"date-time":"2026-06-05T17:18:16Z","timestamp":1780679896000},"page":"4380","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Placental Evidence of Intrauterine Stress: Mechanisms, Timing, and Links to Perinatal Brain Injury"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0009-0000-9472-9617","authenticated-orcid":false,"given":"Charlotte F.","family":"Kim","sequence":"first","affiliation":[{"name":"Department of Pathology and Immunology, Baylor College of Medicine, Texas Children\u2019s Hospital, 6621 Fannin St., MC-1195, Houston, TX 77030, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2152-7998","authenticated-orcid":false,"given":"Chrystalle Katte","family":"Carreon","sequence":"additional","affiliation":[{"name":"Department of Pathology, Harvard Medical School, Boston Children\u2019s Hospital, Boston, MA 02115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,6,5]]},"reference":[{"key":"ref_1","first-page":"CD004661","article-title":"Magnesium Sulphate for Women at Risk of Preterm Birth for Neuroprotection of the Fetus","volume":"2024","author":"Shepherd","year":"2024","journal-title":"Cochrane Database Syst. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1159\/000538879","article-title":"Blood Lactate Levels During Therapeutic Hypothermia and Neurodevelopmental Outcome or Death at 18\u201324 Months of Age in Neonates with Moderate and Severe Hypoxic-Ischemic Encephalopathy","volume":"121","author":"Boerger","year":"2024","journal-title":"Neonatology"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1016\/j.cca.2015.08.021","article-title":"Neonatal Hypoxic Ischemic Encephalopathy-Related Biomarkers in Serum and Cerebrospinal Fluid","volume":"450","author":"Lv","year":"2015","journal-title":"Clin. Chim. Acta"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1038\/s41390-022-01994-0","article-title":"Combined Gfap, Nfl, Tau, and Uch-L1 Panel Increases Prediction of Outcomes in Neonatal Encephalopathy","volume":"93","author":"Yang","year":"2023","journal-title":"Pediatr. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.jpeds.2020.06.078","article-title":"Plasma and Cerebrospinal Fluid Candidate Biomarkers of Neonatal Encephalopathy Severity and Neurodevelopmental Outcomes","volume":"226","author":"Dietrick","year":"2020","journal-title":"J. Pediatr."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1350","DOI":"10.1016\/S0140-6736(13)61132-0","article-title":"Risk Factors for Congenital Anomaly in a Multiethnic Birth Cohort: An Analysis of the Born in Bradford Study","volume":"382","author":"Sheridan","year":"2013","journal-title":"Lancet"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1001\/jamapsychiatry.2016.3798","article-title":"Diagnostic Yield and Novel Candidate Genes by Exome Sequencing in 152 Consanguineous Families with Neurodevelopmental Disorders","volume":"74","author":"Reuter","year":"2017","journal-title":"JAMA Psychiatry"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"113917","DOI":"10.1016\/j.expneurol.2021.113917","article-title":"Placental Pathology: Pathways Leading to or Associated with Perinatal Brain Injury in Experimental Neurology, Special Issue: Placental Mediated Mechanisms of Perinatal Brain Injury","volume":"347","author":"Redline","year":"2022","journal-title":"Exp. Neurol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1016\/j.ajog.2023.06.014","article-title":"Placental Fetal Vascular Malperfusion, Neonatal neurologic Morbidity, and Infant Neurodevelopmental Outcomes: A Systematic Review and Meta-Analysis","volume":"229","author":"Spinillo","year":"2023","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Mastrangelo, H., Sacco, M.A., Gualtieri, S., Grimaldi, G., Monterossi, M.D., Neri, G., and Aquila, I. (2026). Placental Vascular Malperfusion, Perinatal Death and Neonatal Brain Injury: A Mechanism-Based Narrative Review with Medico-Legal Implications. J. Clin. Med., 15.","DOI":"10.3390\/jcm15072734"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.jpeds.2021.06.023","article-title":"Acute and Chronic Placental Abnormalities in a Multicenter Cohort of Newborn Infants with Hypoxic-Ischemic Encephalopathy","volume":"237","author":"Chalak","year":"2021","journal-title":"J. Pediatr."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"F211","DOI":"10.1136\/fn.84.3.F211","article-title":"Nucleated Red Blood Cells in the Fetus and Newborn","volume":"84","author":"Hermansen","year":"2001","journal-title":"Arch. Dis. Child. Fetal Neonatal Ed."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Dulay, A.T., Buhimschi, I.A., Zhao, G., Luo, G., Abdel-Razeq, S., Cackovic, M., Rosenberg, V.A., Pettker, C.M., Thung, S.F., and Bahtiyar, M.O. (2008). Nucleated Red Blood Cells Are a Direct Response to Mediators of Inflammation in Newborns with Early-Onset Neonatal Sepsis. Am. J. Obstet. Gynecol., 198.","DOI":"10.1016\/j.ajog.2008.01.040"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/S0020-7292(00)00259-9","article-title":"Nucleated Red Blood Cells as a Marker in Acute and Chronic Fetal Asphyxia","volume":"71","author":"Sahin","year":"2000","journal-title":"Int. J. Gynecol. Obstet."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/S0002-9378(12)90891-1","article-title":"Fetal Plasma Erythropoietin in Pregnancies Complicated by Maternal Diabetes Mellitus","volume":"168","author":"Salvesen","year":"1993","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/S0022-3476(05)81662-2","article-title":"Nucleated Erythrocytes in Healthy Infants and in Infants of Diabetic Mothers","volume":"116","author":"Green","year":"1990","journal-title":"J. Pediatr."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.blre.2012.12.003","article-title":"Regulation of Erythropoiesis by Hypoxia-Inducible Factors","volume":"27","author":"Haase","year":"2013","journal-title":"Blood Rev."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.1016\/j.ajog.2004.12.076","article-title":"Fetal \u201cNonreassuring Status\u201d Is Associated with Elevation of Nucleated Red Blood Cell Counts and Interleukin-6","volume":"192","author":"Ferber","year":"2005","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1097\/01.AOG.0000195066.43243.56","article-title":"Neonatal Nucleated Red Blood Cells and the Prediction of Cerebral White Matter Injury in Preterm Infants","volume":"107","author":"Silva","year":"2006","journal-title":"Obstet. Gynecol."},{"key":"ref_20","first-page":"371","article-title":"Placenta Pathology Questions to the Perinatologist","volume":"14","author":"Benirschke","year":"1994","journal-title":"J. Perinatol."},{"key":"ref_21","first-page":"485","article-title":"Neonatal Nucleated Red Blood Cell and Lymphocyte Counts in Fetal Brain Injury","volume":"91","author":"Phelan","year":"1998","journal-title":"Obstet. Gynecol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1016\/S0002-9378(96)80010-X","article-title":"Nucleated Red Blood Cells: An Update on the Marker for Fetal Asphyxia","volume":"175","author":"Korst","year":"1996","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1080\/14767050701232596","article-title":"Nucleated Red Blood Cell and Platelet Counts in Asphyxiated Neonates Sufficient to Result in Permanent Neurologic Impairment","volume":"20","author":"Phelan","year":"2007","journal-title":"J. Matern.-Fetal Neonatal Med."},{"key":"ref_24","first-page":"242","article-title":"Nucleated Red Blood Cell Counts in Growth-Restricted Neonates with Absent or Reversed-End-Diastolic Umbilical Artery Velocity","volume":"29","author":"Hendrik","year":"2002","journal-title":"Clin. Exp. Obstet. Gynecol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1038\/sj.jp.7211437","article-title":"Umbilical Cord Nucleated Red Blood Cell Counts: Normal Values and the Effect of Labor","volume":"26","author":"McCarthy","year":"2006","journal-title":"J. Perinatol."},{"key":"ref_26","first-page":"711","article-title":"Neonatal Outcome in Meconium Stained Amniotic Fluid-One Year Experience","volume":"60","author":"Mehmood","year":"2010","journal-title":"J. Pak. Med. Assoc."},{"key":"ref_27","first-page":"329","article-title":"Meconium: A 1990s Perspective on an Old Obstetric Hazard","volume":"83","author":"Nathan","year":"1994","journal-title":"Obstet. Gynecol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1097\/01.ogx.0000149659.89530.c2","article-title":"Meconium Passage in Utero: Mechanisms, Consequences, and Management","volume":"60","author":"Ahanya","year":"2005","journal-title":"Obstet. Gynecol. Surv."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1111\/j.1447-0756.2012.01896.x","article-title":"Hepcidin and Erythropoietin Measurements in the Cord Blood of Neonates with Meconium-Stained Amniotic Fluid","volume":"39","author":"Tavil","year":"2013","journal-title":"J. Obstet. Gynaecol. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/S0002-9378(00)20815-6","article-title":"Fetal Erythropoietin Levels in Pregnancies Complicated by Meconium Passage: Does Meconium Suggest Fetal Hypoxia?","volume":"183","author":"Jazayeri","year":"2000","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1016\/0002-9378(95)91481-1","article-title":"Markers of Acute and Chronic Asphyxia in Infants with Meconium-Stained Amniotic Fluid","volume":"172","author":"Richey","year":"1995","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1203\/pdr.0b013e31802d8a81","article-title":"Elevated Plasma Corticotrophin Release Factor Levels and in Utero Meconium Passage","volume":"61","author":"Lakshmanan","year":"2007","journal-title":"Pediatr. Res."},{"key":"ref_33","first-page":"459","article-title":"Dating the Time Interval from Meconiuim Passage to Birth","volume":"66","author":"Miller","year":"1985","journal-title":"Obstet. Gynecol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/0028-2243(91)90222-7","article-title":"Vasoconstrictive Effect of Bile Acids on Isolated Human Placental Chorionic Veins","volume":"42","author":"Cruz","year":"1991","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/S0301-2115(99)00099-8","article-title":"Vasoconstrictive Activity of Meconium Stained Amniotic Fluid in the Human Placental Vasculature","volume":"87","author":"Holcberg","year":"1999","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.humpath.2003.12.002","article-title":"Myocytes of Chorionic Vessels from Placentas with Meconium-Associated Vascular Necrosis Exhibit Apoptotic Markers","volume":"35","author":"King","year":"2004","journal-title":"Hum. Pathol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/S0301-2115(01)00543-7","article-title":"Vasoconstrictive Activity of Oxytocin in Meconium Impregnated Human Placentas","volume":"101","author":"Holcberg","year":"2002","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"315","DOI":"10.2350\/15-06-1660-OA.1","article-title":"Meconium-Associated Umbilical Vascular Myonecrosis: Correlations with Adverse Outcome and Placental Pathology","volume":"19","author":"Cimic","year":"2016","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_39","first-page":"760","article-title":"Meconium-Induced Umbilical Cord Vascular Necrosis and Ulceration: A Potential Link Between the Placenta and Poor Pregnancy Outcome","volume":"79","author":"Altshuler","year":"1992","journal-title":"Obstet. Gynecol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1177\/088307388900400214","article-title":"Meconium-Induced Vasocontraction: A Potential Cause of Cerebral and Other Fetal Hypoperfusion and of Poor Pregnancy Outcome","volume":"4","author":"Altshuler","year":"1989","journal-title":"J. Child Neurol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"S527","DOI":"10.1016\/j.ajog.2020.12.871","article-title":"It\u2019s Not All in the Fluid: Occult Meconium-Associated Myonecrosis","volume":"224","author":"Matthews","year":"2021","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.ogrm.2016.05.001","article-title":"Meconium Stained Amniotic Fluid","volume":"26","author":"Argyridis","year":"2016","journal-title":"Obstet. Gynaecol. Reprod. Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1159\/000081359","article-title":"Prognostic Value of Change in Amniotic Fluid Color During Labor","volume":"20","author":"Locatelli","year":"2005","journal-title":"Fetal Diagn. Ther."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1080\/jmf.11.1.54.59","article-title":"The Effect of Meconium on Perinatal Outcome: A Prospective Analysis","volume":"11","author":"Sheiner","year":"2002","journal-title":"J. Matern.-Fetal Neonatal Med."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/S0140-6736(98)85013-7","article-title":"Effect of Interleukin 8 in Meconium on In-Vitro Neutrophil Chemotaxis","volume":"352","author":"Pelikan","year":"1998","journal-title":"Lancet"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1016\/S0344-0338(96)80029-X","article-title":"Inflammation of the Lungs, Umbilical Cord and Placenta Associated with Meconium Passage in Utero","volume":"192","author":"Burgess","year":"1996","journal-title":"Pathol. Res. Pract."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"B157","DOI":"10.1016\/S0020-7292(00)83236-1","article-title":"Meconium-Stained Amniotic Fluid Exhibits Chemotactic Activity for Polymorphonuclear Leukocytes in Vitro","volume":"70","author":"Yamada","year":"2000","journal-title":"Int. J. Gynecol. Obstet."},{"key":"ref_48","unstructured":"Benirschke, K. (1996). The Use of the Placenta in the Understanding of Perinatal Injury. Risk Manag. Tech. Perinat. Neonatal Pract., 325\u2013345."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.5858\/2000-124-1785-PLAWCP","article-title":"Placental Lesions Associated with Cerebral Palsy and Neurologic Impairment Following Term Birth","volume":"124","author":"Redline","year":"2000","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1097\/00005072-199407000-00013","article-title":"The Correlation of Prenatal Brain Damage with Placental Pathology","volume":"53","author":"Grafe","year":"1994","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Baergen, R. (2005). Manual of Benirschke and Kaufmann\u2019s Pathology of the Human Placenta, Springer.","DOI":"10.1007\/b138589"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1097\/AOG.0b013e318193beaf","article-title":"Intrapartum Umbilical Cord Rupture","volume":"113","author":"Walker","year":"2009","journal-title":"Obstet. Gynecol."},{"key":"ref_53","unstructured":"Benirschke, K., Kaufmann, P., and Baergen, R.N. (2006). Pathology of the Human Placenta, Springer. [5th ed.]."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1159\/000082429","article-title":"Brain Damage to the Survivor within 30 Min of Co-Twin Demise in Monochorionic Twins","volume":"20","author":"Kars","year":"2005","journal-title":"Fetal Diagn. Ther."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.placenta.2020.07.020","article-title":"Risk Factors for Spontaneous Hematoma of the Umbilical Cord: A Case-Control Study","volume":"99","author":"Thibouw","year":"2020","journal-title":"Placenta"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.jpeds.2018.06.005","article-title":"The Placenta in Neonatal Encephalopathy: A Case\u2013Control Study","volume":"202","author":"Vik","year":"2018","journal-title":"J. Pediatr."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1016\/j.humpath.2004.02.014","article-title":"Placental Fetal Thrombotic Vasculopathy Is Associated with Neonatal Encephalopathy","volume":"35","author":"McDonald","year":"2004","journal-title":"Hum. Pathol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1016\/j.ajog.2004.07.030","article-title":"Severe Fetal Placental Vascular Lesions in Term Infants with Neurologic Impairment","volume":"192","author":"Redline","year":"2005","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1038\/s41372-019-0334-9","article-title":"Placental Findings among Newborns with Hypoxic Ischemic Encephalopathy","volume":"39","author":"Bingham","year":"2019","journal-title":"J. Perinatol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.jpeds.2021.11.062","article-title":"Placental Findings in Infants with Hypoxic-Ischemic Encephalopathy: The Importance of the Comparison Group","volume":"242","author":"Bingham","year":"2022","journal-title":"J. Pediatr."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.jpeds.2017.11.061","article-title":"Placental Pathology in Neonatal Stroke: A Retrospective Case-Control Study","volume":"195","author":"Boyd","year":"2018","journal-title":"J. Pediatr."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"(2021). Fetal Growth Restriction: Acog Practice Bulletin, Number 227. Obstet. Gynecol., 137, e16\u2013e28.","DOI":"10.1097\/AOG.0000000000004251"},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"(2021). Antepartum Fetal Surveillance: Acog Practice Bulletin, Number 229. Obstet. Gynecol., 137, e116\u2013e127.","DOI":"10.1097\/AOG.0000000000004410"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Pardo, N., Kingdom, J., Nevo, O., Pardo, A., and Melamed, N. (2026). Umbilical Artery Doppler Deterioration, Time to Delivery, and Risk of Fetal Death in Early-Onset Severe Fetal Growth Restriction Progressing to Absent or Reversed End-Diastolic Flow. Am. J. Obstet. Gynecol., in press.","DOI":"10.1016\/j.ajog.2026.03.003"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"2517763","DOI":"10.1080\/14767058.2025.2517763","article-title":"Umbilical Cord Coiling Index in Predicting Neonatal Outcomes: A Single-Center Cross-Sectional Study from Vietnam","volume":"38","author":"Nguyen","year":"2025","journal-title":"J. Matern. Fetal Neonatal Med."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1542\/peds.67.5.618","article-title":"Short Umbilical Cord: Its Origin and Relevance","volume":"67","author":"Miller","year":"1981","journal-title":"Pediatrics"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1016\/0002-9378(66)90777-0","article-title":"The Umbilical Cord Complications of True Knots, Nuchal Coils, and Cords around the Body. Report from the Collaborative Study of Cerebral Palsy","volume":"94","author":"Spellacy","year":"1966","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1007\/s100240010135","article-title":"Morbidity, Mortality, and Placental Pathology in Excessively Long Umbilical Cords: Retrospective Study","volume":"4","author":"Baergen","year":"2001","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1016\/j.placenta.2015.02.007","article-title":"Placental Lesions Associated with Oligohydramnios in Fetal Growth Restricted (Fgr) Pregnancies","volume":"36","author":"Spinillo","year":"2015","journal-title":"Placenta"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1007\/s100240010103","article-title":"Abnormal Umbilical Cord Coiling Is Associated with Adverse Perinatal Outcomes","volume":"3","author":"Machin","year":"2000","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.placenta.2013.04.002","article-title":"Gross Patterns of Umbilical Cord Coiling: Correlations with Placental Histology and Stillbirth","volume":"34","author":"Ernst","year":"2013","journal-title":"Placenta"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1177\/10935266231195166","article-title":"Gross and Histologic Placental Abnormalities Associated with Neonatal Hypoxic-Ischemic Encephalopathy","volume":"27","author":"Kim","year":"2024","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1016\/j.humpath.2004.08.003","article-title":"Clinical and Pathological Umbilical Cord Abnormalities in Fetal Thrombotic Vasculopathy","volume":"35","author":"Redline","year":"2004","journal-title":"Hum. Pathol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"14","DOI":"10.2350\/05-05-0051.1","article-title":"Umbilical Cord Stricture and Overcoiling Are Common Causes of Fetal Demise","volume":"9","author":"Peng","year":"2006","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1111\/j.1471-0528.1995.tb10850.x","article-title":"The Mortality and Morbidity Associated with Umbilical Cord Prolapse","volume":"102","author":"Murphy","year":"1995","journal-title":"BJOG Int. J. Obstet. Gynaecol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"247","DOI":"10.2147\/IJWH.S285860","article-title":"Current Perspectives of Prenatal Sonographic Diagnosis and Clinical Management Challenges of Complex Umbilical Cord Entanglement","volume":"13","author":"Sherer","year":"2021","journal-title":"Int. J. Women\u2019s Health"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1097\/01.AOG.0000165322.42051.0f","article-title":"Nuchal Cords in Term and Postterm Deliveries: Do We Need to Know?","volume":"106","author":"Burkhardt","year":"2005","journal-title":"Obstet. Gynecol."},{"key":"ref_78","first-page":"262","article-title":"Obstetrically Important Lesions of the Umbilical Cord","volume":"39","author":"Benirschke","year":"1994","journal-title":"J. Reprod. Med."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1053\/sper.2002.29860","article-title":"Umbilical Cord Accidents: Human Studies","volume":"26","author":"Collins","year":"2002","journal-title":"Semin. Perinatol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1007\/s00404-019-05178-w","article-title":"Adverse Pregnancy Outcomes and Multiple Nuchal Cord Loops","volume":"300","author":"Schreiber","year":"2019","journal-title":"Arch. Gynecol. Obs."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.ijgo.2013.02.012","article-title":"True Umbilical Cord Knot and Obstetric Outcome","volume":"122","author":"Georgiadis","year":"2013","journal-title":"Int. J. Gynecol. Obstet."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1097\/01.ogx.0000208802.20908.c6","article-title":"Umbilical Cord Prolapse","volume":"61","author":"Lin","year":"2006","journal-title":"Obstet. Gynecol. Surv."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"698","DOI":"10.5858\/arpa.2015-0225-CC","article-title":"Sampling and Definitions of Placental Lesions: Amsterdam Placental Workshop Group Consensus Statement","volume":"140","author":"Khong","year":"2016","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/S0002-9378(16)38991-8","article-title":"Vasa Previa","volume":"63","year":"1952","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"100876","DOI":"10.1016\/j.ajogmf.2023.100876","article-title":"Impact of Marginal Cord Insertion on Perinatal Outcomes: A Systematic Review and Meta-Analysis","volume":"5","author":"Siargkas","year":"2023","journal-title":"Am. J. Obstet. Gynecol. MFM"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.placenta.2020.03.008","article-title":"Wharton\u2019s Jelly Area and Its Association with Placental Morphometry and Pathology","volume":"94","author":"Debebe","year":"2020","journal-title":"Placenta"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"721","DOI":"10.3109\/14767058.2015.1015984","article-title":"Hypoxic Ischemic Encephalopathy in Newborns Linked to Placental and Umbilical Cord Abnormalities","volume":"29","author":"Nasiell","year":"2016","journal-title":"J. Matern. Fetal Neonatal Med."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1080\/15513815.2022.2142490","article-title":"Recurrent Second Trimester Fetal Demise Caused by Hypercoiled Umbilical Cords","volume":"42","author":"Slack","year":"2022","journal-title":"Fetal Pediatr. Pathol."},{"key":"ref_89","first-page":"409","article-title":"Non-Coiled Umbilical Blood Vessels: A New Marker for the Fetus at Risk","volume":"81","author":"Strong","year":"1993","journal-title":"Obstet. Gynecol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.ejogrb.2006.01.018","article-title":"The Umbilical Coiling Index in Complicated Pregnancy","volume":"130","author":"Franx","year":"2007","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1352","DOI":"10.5858\/2000-124-1352-RUCTLT","article-title":"Recurrent Umbilical Cord Torsion Leading to Fetal Death in 3 Subsequent Pregnancies: A Case Report and Review of the Literature","volume":"124","author":"Bakotic","year":"2000","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_92","first-page":"450","article-title":"Umbilical Cord Length and Intrapartum Complications","volume":"57","author":"Rayburn","year":"1981","journal-title":"Obstet. Gynecol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1016\/S0143-4004(83)80045-9","article-title":"Standards for Measuring Umbilical Cord Length","volume":"4","author":"Mills","year":"1983","journal-title":"Placenta"},{"key":"ref_94","first-page":"429","article-title":"Placental Pathology Casebook. Long Umbilical Cord with Torsion and Diffuse Chorionic Surface Vein Thrombosis: Multiple Associated Congenital Abnormalities Including Destructive Encephalopathy","volume":"15","author":"Stanley","year":"1995","journal-title":"J. Perinatol."},{"key":"ref_95","unstructured":"American Registry of Pathology (2021). Atlas of Placental Pathology, American Registry of Pathology."},{"key":"ref_96","first-page":"113","article-title":"Developmental Abnormalities Resulting in Short Umbilical Cord","volume":"29","author":"Drut","year":"1993","journal-title":"Birth Defects Orig. Artic. Ser."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1097\/01.AOG.0000102706.84063.C7","article-title":"Risk Factors and Outcomes Associated with a Short Umbilical Cord","volume":"103","author":"Krakowiak","year":"2004","journal-title":"Obstet. Gynecol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1007\/s13224-012-0194-0","article-title":"Study of Length of Umbilical Cord and Fetal Outcome: A Study of 1,000 Deliveries","volume":"62","author":"Balkawade","year":"2012","journal-title":"J. Obstet. Gynaecol. India"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/S0002-9378(88)80084-X","article-title":"Antenatal Origin of Neurologic Damage in Newborn Infants. I: Preterm Infants","volume":"159","author":"Bejar","year":"1988","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1016\/S0046-8177(99)90136-3","article-title":"Fetal Thrombotic Vasculopathy in the Placenta: Cerebral Thrombi and Infarcts, Coagulopathies, and Cerebral Palsy","volume":"30","author":"Kraus","year":"1999","journal-title":"Hum. Pathol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"37","DOI":"10.3109\/15513818809022278","article-title":"Thrombosis of the Umbilical Cord: Analysis of 52 Cases and Literature Review","volume":"8","author":"Heifetz","year":"1988","journal-title":"Fetal Pediatr. Pathol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"8167276","DOI":"10.1155\/2017\/8167276","article-title":"Amniotic Fluid Infection in Preterm Pregnancies with Intact Membranes","volume":"2017","author":"Myntti","year":"2017","journal-title":"Dis. Markers"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"1276","DOI":"10.1136\/adc.62.12.1276","article-title":"Tight Nuchal Cord and Neonatal Hypovolaemic Shock","volume":"62","author":"Vanhaesebrouck","year":"1987","journal-title":"Arch. Dis. Child."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.siny.2006.02.011","article-title":"Inflammatory Responses in the Placenta and Umbilical Cord","volume":"11","author":"Redline","year":"2006","journal-title":"Semin. Fetal Neonatal Med."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1203\/00006450-200006000-00007","article-title":"The Relationship between Placental and Other Perinatal Risk Factors for Neurologic Impairment in Very Low Birth Weight Children","volume":"47","author":"Redline","year":"2000","journal-title":"Pediatr. Res."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1007\/s10024-003-8083-2","article-title":"Maternal Vascular Underperfusion: Nosology and Reproducibility of Placental Reaction Patterns","volume":"7","author":"Redline","year":"2004","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1111\/j.1469-8749.1997.tb07373.x","article-title":"Ischaemic Cerebral Injury, Intrauterine Growth Retardation, and Placental Infarction","volume":"39","author":"Burke","year":"1997","journal-title":"Dev. Med. Child Neurol."},{"key":"ref_108","first-page":"1091","article-title":"Placental Lesions Associated with Neurologic Impairment and Cerebral Palsy in Very Low-Birth-Weight Infants","volume":"122","author":"Redline","year":"1998","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1002\/uog.13415","article-title":"Correlation between Histological Signs of Placental Underperfusion and Perinatal Morbidity in Late-Onset Small-for-Gestational-Age Fetuses","volume":"45","author":"Simeone","year":"2015","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"2650","DOI":"10.4049\/jimmunol.1202698","article-title":"Human Chorionic Gonadotropin as a Central Regulator of Pregnancy Immune Tolerance","volume":"190","author":"Schumacher","year":"2013","journal-title":"J. Immunol."},{"key":"ref_111","doi-asserted-by":"crossref","unstructured":"Lentz, L.S., Stutz, A.J., Meyer, N., Schubert, K., Karkossa, I., von Bergen, M., Zenclussen, A.C., and Schumacher, A. (2022). Human Chorionic Gonadotropin Promotes Murine Treg Cells and Restricts Pregnancy-Harmful Proinflammatory Th17 Responses. Front. Immunol., 13.","DOI":"10.3389\/fimmu.2022.989247"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"S53","DOI":"10.1016\/j.ajog.2015.08.041","article-title":"Chronic Inflammation of the Placenta: Definition, Classification, Pathogenesis, and Clinical Significance","volume":"213","author":"Kim","year":"2015","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"7","DOI":"10.2350\/12-05-1195-OA.1","article-title":"Positive C4d Immunostaining of Placental Villous Syncytiotrophoblasts Supports Host-Versus-Graft Rejection in Villitis of Unknown Etiology","volume":"16","author":"Rudzinski","year":"2013","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"3919","DOI":"10.4049\/jimmunol.0803834","article-title":"Villitis of Unknown Etiology Is Associated with a Distinct Pattern of Chemokine up-Regulation in the Feto-Maternal and Placental Compartments: Implications for Conjoint Maternal Allograft Rejection and Maternal Anti-Fetal Graft-Versus-Host Disease","volume":"182","author":"Kim","year":"2009","journal-title":"J. Immunol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1111\/aji.12142","article-title":"Characterization of the Fetal Blood Transcriptome and Proteome in Maternal Anti-Fetal Rejection: Evidence of a Distinct and Novel Type of Human Fetal Systemic Inflammatory Response","volume":"70","author":"Lee","year":"2013","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/S0887-8994(98)00012-5","article-title":"Neonates with Electrically Confirmed Seizures and Possible Placental Associations","volume":"19","author":"Scher","year":"1998","journal-title":"Pediatr. Neurol."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"e841\u2013e849-849.e7","DOI":"10.1016\/j.ajog.2015.09.072","article-title":"Placental Pathology Is Associated with Severity Of neonatal Encephalopathy and Adverse Developmental Outcomes Following Hypothermia","volume":"213","author":"Mir","year":"2015","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1007\/s10024001-0195-y","article-title":"Maternal Floor Infarction and Massive Perivillous Fibrin Deposition: Histological Definitions, Association with Intrauterine Fetal Growth Restriction, and Risk of Recurrence","volume":"5","author":"Katzman","year":"2002","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1038\/sj.jp.7210685","article-title":"Maternal Floor Infarction of the Placenta: Association with Central Nervous System Injury and Adverse Neurodevelopmental Outcome","volume":"22","author":"Vaucher","year":"2002","journal-title":"J. Perinatol."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1016\/0002-9378(90)91100-Q","article-title":"The Association of Maternal Floor Infarction of the Placenta with Adverse Perinatal Outcome","volume":"163","author":"Andres","year":"1990","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1111\/aji.12143","article-title":"Maternal Floor Infarction\/Massive Perivillous Fibrin Deposition: A Manifestation of Maternal Antifetal Rejection?","volume":"70","author":"Romero","year":"2013","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1055\/s-2008-1078755","article-title":"Perinatal Cerebral Arterial Infarction Associated with a Placental Chorioangioma","volume":"25","author":"Das","year":"2008","journal-title":"Am. J. 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