{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T22:25:35Z","timestamp":1785363935548,"version":"3.55.0"},"reference-count":54,"publisher":"Georg Thieme Verlag KG","issue":"12","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Am J Perinatol"],"published-print":{"date-parts":[[2023,9]]},"abstract":"<jats:p>\n            Objective\u2003Shallow placental implantation (SPI) features placental maldistribution of extravillous trophoblasts and includes excessive amount of extravillous trophoblasts, chorionic microcysts in the membranes and chorionic disc, and decidual clusters of multinucleate trophoblasts. The histological lesions were previously and individually reported in association with various clinical and placental abnormalities. This retrospective statistical analysis of a large placental database from high-risk pregnancy statistically compares placentas with and without a composite group of features of SPI.<\/jats:p><jats:p>\n            Study Design\u2003Twenty-four independent abnormal clinical and 44 other than SPI placental phenotypes were compared between 4,930 placentas without (group 1) and 1,283 placentas with one or more histological features of SPI (composite SPI group; group 2). Placentas were received for pathology examination at a discretion of obstetricians. Placental lesion terminology was consistent with the Amsterdam criteria, with addition of other lesions described more recently.<\/jats:p><jats:p>\n            Results\u2003Cases of group 2 featured statistically and significantly (p\u2009&lt;\u20090.001after Bonferroni's correction) more common than group 1 on the following measures: gestational hypertension, preeclampsia, oligohydramnios, polyhydramnios, abnormal Dopplers, induction of labor, cesarean section, perinatal mortality, fetal growth restriction, stay in neonatal intensive care unit (NICU), congenital malformation, deep meconium penetration, intravillous hemorrhage, villous infarction, membrane laminar necrosis, fetal blood erythroblastosis, decidual arteriopathy (hypertrophic and atherosis), chronic hypoxic injury (uterine and postuterine), intervillous thrombus, segmental and global fetal vascular malperfusion, various umbilical cord abnormalities, and basal plate myometrial fibers.<\/jats:p><jats:p>\n            Conclusion\u2003SPI placentas were statistically and significantly associated with 48% abnormal independent clinical and 51% independent abnormal placental phenotypes such as acute and chronic hypoxic lesions, fetal vascular malperfusion, umbilical cord abnormalities, and basal plate myometrial fibers among others. Therefore, SPI should be regarded as a category of placental lesions related to maternal vascular malperfusion and the \u201cGreat Obstetrical Syndromes.\u201d<\/jats:p><jats:p>\n            Key Points\n          <\/jats:p>","DOI":"10.1055\/s-0041-1735554","type":"journal-article","created":{"date-parts":[[2021,9,29]],"date-time":"2021-09-29T22:41:14Z","timestamp":1632955274000},"page":"1328-1335","source":"Crossref","is-referenced-by-count":14,"title":["Shallow Placentation: A Distinct Category of Placental Lesions"],"prefix":"10.1055","volume":"40","author":[{"given":"Jerzy","family":"Stanek","sequence":"additional","affiliation":[{"name":"Division of Pathology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"194","published-online":{"date-parts":[[2021,9,29]]},"reference":[{"issue":"03","key":"ref1","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.ajog.2010.08.009","article-title":"The \u201cGreat Obstetrical Syndromes\u201d are associated with disorders of deep placentation","volume":"204","author":"I Brosens","year":"2011","journal-title":"Am J Obstet Gynecol"},{"issue":"08","key":"ref2","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1034\/j.1600-0412.2003.00220.x","article-title":"Quantitative analysis of trophoblast invasion in preeclampsia","volume":"82","author":"T Naicker","year":"2003","journal-title":"Acta Obstet Gynecol Scand"},{"issue":"04","key":"ref3","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1309\/AJCPOZ73MPSPYFEZ","article-title":"Chorionic disk extravillous trophoblasts in placental diagnosis","volume":"136","author":"J Stanek","year":"2011","journal-title":"Am J Clin Pathol"},{"issue":"02","key":"ref4","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1177\/1093526618803759","article-title":"Histological features of shallow placental implantation unify early onset and late onset preeclampsia","volume":"22","author":"J Stanek","year":"2019","journal-title":"Pediatr Dev Pathol"},{"issue":"06","key":"ref5","doi-asserted-by":"crossref","first-page":"493.e1\u2013e8","DOI":"10.1016\/j.ajog.2012.03.025","article-title":"Clustering of maternal\/fetal clinical conditions and outcomes and placental lesions","volume":"206","author":"J Stanek","year":"2012","journal-title":"Am J Obstet Gynecol"},{"issue":"04","key":"ref6","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1007\/s00428-009-0841-8","article-title":"Acute and chronic placental membrane hypoxic lesions","volume":"455","author":"J Stanek","year":"2009","journal-title":"Virchows Arch"},{"issue":"01","key":"ref7","doi-asserted-by":"crossref","first-page":"13","DOI":"10.17116\/patol201678113-18","article-title":"Histological hanges in the placenta and vascularization of its villi in early- and late-onset preeclampsia [in Russian]","volume":"78","author":"A I Shchegolev","year":"2016","journal-title":"Arkh Patol"},{"issue":"05","key":"ref8","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1111\/jog.13276","article-title":"Decidual arteriolopathy with or without associated hypertension modifies the underlying histomorphology in placentas from diabetic mothers","volume":"43","author":"J Stanek","year":"2017","journal-title":"J Obstet Gynaecol Res"},{"issue":"06","key":"ref9","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1177\/1093526619852869","article-title":"Patterns of placental injury in congenital anomalies in second half of pregnancy","volume":"22","author":"J Stanek","year":"2019","journal-title":"Pediatr Dev Pathol"},{"issue":"08","key":"ref10","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1016\/S0143-4004(97)90000-X","article-title":"Oxygen and placental villous development: origins of fetal hypoxia","volume":"18","author":"J C Kingdom","year":"1997","journal-title":"Placenta"},{"issue":"06","key":"ref11","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1007\/s00428-016-1921-1","article-title":"Association of coexisting morphological umbilical cord abnormality and clinical cord compromise with hypoxic and thrombotic placental histology","volume":"468","author":"J Stanek","year":"2016","journal-title":"Virchows Arch"},{"issue":"04","key":"ref12","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1161\/HYPERTENSIONAHA.107.107607","article-title":"Placental origins of preeclampsia: challenging the current hypothesis","volume":"51","author":"B Huppertz","year":"2008","journal-title":"Hypertension"},{"issue":"06","key":"ref13","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1007\/s00404-020-05546-x","article-title":"Placental pathology in pregnancies complicated by fetal growth restriction: recurrence vs. new onset","volume":"301","author":"M Levy","year":"2020","journal-title":"Arch Gynecol Obstet"},{"issue":"02","key":"ref14","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1097\/AOG.0000000000001843","article-title":"Pathologically diagnosed placenta accrete and hemorrhagic morbidity in a subsequent pregnancy","volume":"129","author":"C Roeca","year":"2017","journal-title":"Obstet Gynecol"},{"issue":"13","key":"ref15","doi-asserted-by":"crossref","first-page":"2140","DOI":"10.1111\/1471-0528.13579","article-title":"Does the presence of placental basal plate myometrial fibres increase the risk of subsequent morbidly adherent placenta: a case-control study","volume":"123","author":"E S Miller","year":"2016","journal-title":"BJOG"},{"issue":"05","key":"ref16","doi-asserted-by":"crossref","first-page":"706","DOI":"10.5858\/arpa.2011-0645-RA","article-title":"Hypoxic patterns of placental injury: a review","volume":"137","author":"J Stanek","year":"2013","journal-title":"Arch Pathol Lab Med"},{"issue":"04","key":"ref17","doi-asserted-by":"crossref","first-page":"266","DOI":"10.2350\/06-10-0174.1","article-title":"Occult placenta accreta: the missing link in the diagnosis of abnormal placentation","volume":"10","author":"J Stanek","year":"2007","journal-title":"Pediatr Dev Pathol"},{"issue":"05","key":"ref18","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1309\/M9BF-6JHH-VF2U-2B8T","article-title":"Myometrial fibers in the placental basal plate can confirm but do not necessarily indicate clinical placenta accreta","volume":"116","author":"T Y Khong","year":"2001","journal-title":"Am J Clin Pathol"},{"issue":"07","key":"ref19","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1016\/j.placenta.2008.04.008","article-title":"Pathophysiology of placenta creta: the role of decidua and extravillous trophoblast","volume":"29","author":"P Tantbirojn","year":"2008","journal-title":"Placenta"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"4230451","DOI":"10.1155\/2020\/4230451","article-title":"Placenta creta: A spectrum of lesions associated with shallow placental implantation","volume":"2020","author":"J Stanek","year":"2020","journal-title":"Obstet Gynecol Int"},{"issue":"03","key":"ref21","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1016\/0029-7844(95)00426-2","article-title":"Placental basal plate myometrial fibers: clinical correlations of abnormally deep trophoblast invasion","volume":"87","author":"D M Sherer","year":"1996","journal-title":"Obstet Gynecol"},{"issue":"12","key":"ref22","doi-asserted-by":"crossref","first-page":"1483","DOI":"10.1038\/modpathol.3800210","article-title":"Implantation site intermediate trophoblasts in placenta cretas","volume":"17","author":"K R Kim","year":"2004","journal-title":"Mod Pathol"},{"issue":"04","key":"ref23","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1016\/0143-4004(87)90067-1","article-title":"Placenta creta and placenta praevia creta","volume":"8","author":"T Y Khong","year":"1987","journal-title":"Placenta"},{"issue":"07","key":"ref24","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":"T Y Khong","year":"2016","journal-title":"Arch Pathol Lab Med"},{"issue":"01","key":"ref25","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1007\/s10024-004-8092-9","article-title":"Laminar necrosis of placental membranes: a histologic sign of uteroplacental hypoxia","volume":"8","author":"J Stanek","year":"2005","journal-title":"Pediatr Dev Pathol"},{"issue":"05","key":"ref26","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/j.placenta.2011.02.002","article-title":"Placental fetal thrombotic vasculopathy in severe congenital anomalies prompting EXIT procedure","volume":"32","author":"J Stanek","year":"2011","journal-title":"Placenta"},{"issue":"03","key":"ref27","doi-asserted-by":"crossref","first-page":"192","DOI":"10.2350\/06-06-0110.1","article-title":"Microscopic chorionic pseudocysts in placental membranes: a histologic lesion of in utero hypoxia","volume":"10","author":"J Stanek","year":"2007","journal-title":"Pediatr Dev Pathol"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.placenta.2019.07.011","article-title":"Segmental villous mineralization: a placental feature of fetal vascular malperfusion","volume":"86","author":"J Stanek","year":"2019","journal-title":"Placenta"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.placenta.2019.02.001","article-title":"CD34 immunostain increases the sensitivity of placental diagnosis of fetal vascular malperfusion in stillbirth","volume":"77","author":"J Stanek","year":"2019","journal-title":"Placenta"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"9","DOI":"10.4236\/ojog.2013.39A002","article-title":"Periarterial stem villous edema is associated with hypercoiled umbilical cord and stem obliterative endarteritis","volume":"3","author":"J Stanek","year":"2013","journal-title":"OJOG"},{"issue":"02","key":"ref31","doi-asserted-by":"crossref","first-page":"125","DOI":"10.3109\/00313020903494052","article-title":"Membrane microscopic chorionic pseudocysts are associated with increased amount of placental extravillous trophoblasts","volume":"42","author":"J Stanek","year":"2010","journal-title":"Pathology"},{"issue":"01","key":"ref32","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1111\/j.1469-7580.2008.01036.x","article-title":"Oxygen as modulator of trophoblast invasion","volume":"215","author":"B Huppertz","year":"2009","journal-title":"J Anat"},{"issue":"03","key":"ref33","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.gendis.2018.04.005","article-title":"The metabolic role of LncZBTB39-1:2 in the trophoblast mobility of preeclampsia","volume":"5","author":"Y Liu","year":"2018","journal-title":"Genes Dis"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.jri.2015.06.002","article-title":"PreImplantation Factor (PIF*) endogenously prevents preeclampsia: Promotes trophoblast invasion and reduces oxidative stress","volume":"114","author":"E R Barnea","year":"2016","journal-title":"J Reprod Immunol"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"S115","DOI":"10.1016\/j.ajog.2015.08.042","article-title":"Why is placentation abnormal in preeclampsia?","volume":"213","author":"S J Fisher","year":"2015","journal-title":"Am J Obstet Gynecol"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.placenta.2019.08.077","article-title":"Reduced ELABELA expression attenuates trophoblast invasion through the PI3K\/AKT\/mTOR pathway in early onset preeclampsia","volume":"87","author":"L Wang","year":"2019","journal-title":"Placenta"},{"key":"ref37","first-page":"31130","article-title":"Decidualization resistance in the origin of preeclampsia","author":"T Garrido-G\u00f3mez","year":"2020","journal-title":"Am J Obster Gynecol"},{"issue":"06","key":"ref38","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1515\/jpm-2018-0055","article-title":"The frequency and type of placental histologic lesions in term pregnancies with normal outcome","volume":"46","author":"R Romero","year":"2018","journal-title":"J Perinat Med"},{"issue":"01","key":"ref39","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1007\/s00428-011-1061-6","article-title":"Relationship between placental morphology and histological findings in an unselected population near term","volume":"459","author":"S Pathak","year":"2011","journal-title":"Virchows Arch"},{"issue":"01","key":"ref40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0378-3782(01)00114-1","article-title":"Placental lesion multiplicity: risk factor for IUGR and neonatal cranial ultrasound abnormalities","volume":"62","author":"R M Viscardi","year":"2001","journal-title":"Early Hum Dev"},{"issue":"01","key":"ref41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2350\/10-02-0795-OA.1","article-title":"Placental membrane and placental disc microscopic chorionic cysts share similar clinicopathologic associations","volume":"14","author":"J Stanek","year":"2011","journal-title":"Pediatr Dev Pathol"},{"issue":"02","key":"ref42","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.humpath.2011.03.012","article-title":"Sensitivity and specificity of finding of multinucleate trophoblastic giant cells in decidua in placentas from high-risk pregnancies","volume":"43","author":"J Stanek","year":"2012","journal-title":"Hum Pathol"},{"issue":"04","key":"ref43","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1111\/aogs.12350","article-title":"Clinicoplacental phenotypes vary with gestational age: an analysis by classical and clustering methods","volume":"93","author":"J Stanek","year":"2014","journal-title":"Acta Obstet Gynecol Scand"},{"issue":"03","key":"ref44","doi-asserted-by":"crossref","first-page":"234.e1","DOI":"10.1016\/j.ajog.2013.10.015","article-title":"Comparison of placental pathology in preterm, late-preterm, near-term, and term births","volume":"210","author":"J Stanek","year":"2014","journal-title":"Am J Obstet Gynecol"},{"key":"ref45","first-page":"285","volume-title":"Laminar necrosis, membrane chorionic microcysts, and chorion nodosum","author":"J Stanek","year":"2019"},{"issue":"03","key":"ref46","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":"R W Redline","year":"2004","journal-title":"Pediatr Dev Pathol"},{"issue":"06","key":"ref47","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1016\/0046-8177(95)90162-0","article-title":"Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast","volume":"26","author":"R W Redline","year":"1995","journal-title":"Hum Pathol"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.placenta.2016.04.012","article-title":"Clustering and classical analysis of clinical and placental phenotypes in fetal growth restriction and constitutional fetal smallness","volume":"42","author":"J Stanek","year":"2016","journal-title":"Placenta"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.placenta.2016.02.013","article-title":"Macroscopic and histological characteristics of retained placenta: a prospectively collected case-control study","volume":"41","author":"M Endler","year":"2016","journal-title":"Placenta"},{"issue":"12","key":"ref50","doi-asserted-by":"crossref","first-page":"2382","DOI":"10.1038\/s41379-020-0569-1","article-title":"Classification and reporting guidelines for the pathology diagnosis of placenta accreta spectrum (PAS) disorders: recommendations from an expert panel","volume":"33","author":"J L Hecht","year":"2020","journal-title":"Mod Pathol"},{"issue":"01","key":"ref51","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1097\/00004347-199601000-00005","article-title":"Placenta accreta: mild cases diagnosed by placental examination","volume":"15","author":"S M Jacques","year":"1996","journal-title":"In J Gynecol Pathol"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.placenta.2018.08.003","article-title":"Chorion laeve accreta - Another manifestation of morbid adherence","volume":"74","author":"T Y Khong","year":"2018","journal-title":"Placenta"},{"issue":"01","key":"ref53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.placenta.2007.05.010","article-title":"Taking tissue samples from the placenta: an illustration of principles and strategies","volume":"29","author":"T M Mayhew","year":"2008","journal-title":"Placenta"},{"key":"ref54","doi-asserted-by":"crossref","DOI":"10.1007\/b138589","volume-title":"Manual of Benirschke and Kaufmann's Pathology of the Human Placenta","author":"R N Baergen","year":"2005"}],"container-title":["American Journal of Perinatology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.thieme-connect.de\/products\/ejournals\/pdf\/10.1055\/s-0041-1735554.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,25]],"date-time":"2023-08-25T23:25:26Z","timestamp":1693005926000},"score":1,"resource":{"primary":{"URL":"http:\/\/www.thieme-connect.de\/DOI\/DOI?10.1055\/s-0041-1735554"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,29]]},"references-count":54,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2023,8,25]]},"published-print":{"date-parts":[[2023,9]]}},"URL":"https:\/\/doi.org\/10.1055\/s-0041-1735554","archive":["Portico","CLOCKSS"],"relation":{},"ISSN":["0735-1631","1098-8785"],"issn-type":[{"value":"0735-1631","type":"print"},{"value":"1098-8785","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,29]]}}}