{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T03:39:18Z","timestamp":1785296358282,"version":"3.55.0"},"reference-count":39,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2017,12,1]],"date-time":"2017-12-01T00:00:00Z","timestamp":1512086400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2017,12,1]],"date-time":"2017-12-01T00:00:00Z","timestamp":1512086400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2017,10,13]],"date-time":"2017-10-13T00:00:00Z","timestamp":1507852800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"name":"Friedrich-Bauer-Foundation","award":["02\/17"],"award-info":[{"award-number":["02\/17"]}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["DFG Fr1245\/9-1"],"award-info":[{"award-number":["DFG Fr1245\/9-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Placenta"],"published-print":{"date-parts":[[2017,12]]},"DOI":"10.1016\/j.placenta.2017.10.004","type":"journal-article","created":{"date-parts":[[2017,10,14]],"date-time":"2017-10-14T17:01:53Z","timestamp":1508000513000},"page":"47-53","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":10,"special_numbering":"C","title":["Syncytial nuclei accumulate at the villous surface in IUGR while proliferation is unchanged"],"prefix":"10.1016","volume":"60","author":[{"given":"E.","family":"Haeussner","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C.","family":"Schmitz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D.","family":"Grynspan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"F.","family":"Edler von Koch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H.-G.","family":"Frank","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.placenta.2017.10.004_bib1","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1016\/j.bpobgyn.2009.05.003","article-title":"Aetiology and pathogenesis of IUGR","volume":"23","author":"Sankaran","year":"2009","journal-title":"Best. Pract. Res. Clin. Obstet. Gynecol."},{"key":"10.1016\/j.placenta.2017.10.004_bib2","series-title":"Fetal Therapy. Scientific Basis and Critical Appraisal of Clinical Benefits","article-title":"Intrauterine growth restriction: placental basis and implications for clinical practice","author":"Kingdom","year":"2013"},{"key":"10.1016\/j.placenta.2017.10.004_bib3","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1016\/j.jgyn.2013.09.013","article-title":"Pr\u00e9valence, facteurs de risque et morbi-mortalit\u00e9 materno-f\u0153tale des troubles de la croissance f\u0153tale","volume":"42","author":"Gaudineau","year":"2013","journal-title":"J.\u00a0Gynecol. Obstet. Biol. Reprod. Paris."},{"key":"10.1016\/j.placenta.2017.10.004_bib4","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1152\/physrev.00029.2015","article-title":"Placental origins of chronic disease","volume":"96","author":"Burton","year":"2016","journal-title":"Physiol. Rev."},{"key":"10.1016\/j.placenta.2017.10.004_bib5","doi-asserted-by":"crossref","first-page":"696","DOI":"10.1016\/j.placenta.2014.06.375","article-title":"Placental pathology in early intrauterine growth restriction associated with maternal hypertension","volume":"35","author":"Veerbeek","year":"2014","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib6","doi-asserted-by":"crossref","first-page":"24004","DOI":"10.1038\/srep24004","article-title":"Novel 3D light microscopic analysis of IUGR placentas points to a morphological correlate of compensated ischemic placental disease in humans","volume":"6","author":"Haeussner","year":"2016","journal-title":"Sci. Rep."},{"key":"10.1016\/j.placenta.2017.10.004_bib7","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1203\/00006450-199311000-00019","article-title":"Amino acid (system A) transporter activity in microvillous membrane vesicles from the placentas of appropriate and small for gestational age babies","volume":"34","author":"Mahendran","year":"1993","journal-title":"Pediatr. Res."},{"key":"10.1016\/j.placenta.2017.10.004_bib8","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1203\/00006450-199808000-00016","article-title":"Intrauterine growth restriction is associated with a reduced activity of placental taurine transporters","volume":"44","author":"Norberg","year":"1998","journal-title":"Pediatr. Res."},{"issue":"A","key":"10.1016\/j.placenta.2017.10.004_bib9","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1053\/plac.2002.0790","article-title":"Regulation of placental transfer: the Na(+)\/H(+) exchanger\u2013a review","volume":"23","author":"Sibley","year":"2002","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib10","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1016\/j.bbamem.2016.03.028","article-title":"Computational modelling of placental amino acid transfer as an integrated system","volume":"1858","author":"Panitchob","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"10.1016\/j.placenta.2017.10.004_bib11","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1055\/s-0042-107078","article-title":"Maternal serum lipid, estradiol, and progesterone levels in pregnancy, and the impact of placental and hepatic pathologies","volume":"76","author":"Pecks","year":"2016","journal-title":"Geburtshilfe Frauenheilkd"},{"key":"10.1016\/j.placenta.2017.10.004_bib12","series-title":"Pathology of the Human Placenta","author":"Benirschke","year":"2012"},{"key":"10.1016\/j.placenta.2017.10.004_bib13","series-title":"Fetal and Neonatal Physiology","first-page":"101","article-title":"Placental development","volume":"vol. 1","author":"Frank","year":"2016"},{"key":"10.1016\/j.placenta.2017.10.004_bib14","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.placenta.2014.01.011","article-title":"Turnover of human villous trophoblast in normal pregnancy: what do we know and what do we need to know?","volume":"35","author":"Mayhew","year":"2014","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib15","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1530\/REP-15-0544","article-title":"Studies of the dynamics of nuclear clustering in human syncytiotrophoblast","volume":"151","author":"Calvert","year":"2016","journal-title":"Reproduction"},{"key":"10.1016\/j.placenta.2017.10.004_bib16","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1177\/107155769800500607","article-title":"Cellular proliferation in the placenta in normal human pregnancy and pregnancy complicated by intrauterine growth restriction","volume":"5","author":"Smith","year":"1998","journal-title":"J.\u00a0Soc. Gynecol. Investig."},{"key":"10.1016\/j.placenta.2017.10.004_bib17","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/S0143-4004(05)80642-3","article-title":"Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms","volume":"17","author":"Macara","year":"1996","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib18","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/j.acthis.2013.10.007","article-title":"Immunolocalization of cell cycle proteins (p57, p27, cyclin D3, PCNA and Ki67) in intrauterine growth retardation (IUGR) and normal human term placentas","volume":"116","author":"Unek","year":"2013","journal-title":"Acta Histochem."},{"key":"10.1016\/j.placenta.2017.10.004_bib19","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.1016\/j.placenta.2015.10.003","article-title":"Does 2D-Histologic identification of villous types of human placentas at birth enable sensitive and reliable interpretation of 3D structure?","volume":"36","author":"Haeussner","year":"2015","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib20","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1016\/j.neuron.2013.02.036","article-title":"Autism-associated neuroligin-3 mutations commonly disrupt tonic endocannabinoid signaling","volume":"78","author":"F\u00f6ldy","year":"2013","journal-title":"Neuron"},{"key":"10.1016\/j.placenta.2017.10.004_bib21","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1038\/4611149a","article-title":"Neural circuits: putting neurons on the map","volume":"461","author":"Eisenstein","year":"2009","journal-title":"Nature"},{"key":"10.1016\/j.placenta.2017.10.004_bib22","doi-asserted-by":"crossref","first-page":"6192","DOI":"10.1038\/srep06192","article-title":"Novel 3D microscopic analysis of human placental villous trees reveals unexpected significance of branching angles","volume":"4","author":"Haeussner","year":"2014","journal-title":"Sci. Rep."},{"key":"10.1016\/j.placenta.2017.10.004_bib23","series-title":"R: a Language and Environment for Statistical Computing","author":"R Core Team","year":"2013"},{"key":"10.1016\/j.placenta.2017.10.004_bib24","doi-asserted-by":"crossref","first-page":"1669","DOI":"10.1126\/science.277.5332.1669","article-title":"Regulation of human placental development by oxygen tension","volume":"277","author":"Genbacev","year":"1997","journal-title":"Science"},{"key":"10.1016\/j.placenta.2017.10.004_bib25","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1007\/978-1-4615-4711-2_20","article-title":"Oxygen and placental vascular development","volume":"474","author":"Kingdom","year":"1999","journal-title":"Adv. Exp. Med. Biol."},{"key":"10.1016\/j.placenta.2017.10.004_bib26","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.placenta.2007.11.002","article-title":"Effects of oxygen on cell turnover and expression of regulators of apoptosis in human placental trophoblast","volume":"29","author":"Heazell","year":"2008","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib27","first-page":"151","article-title":"Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: molecular evidence for \u201cplacental hyperoxia\u201d in intrauterine growth restriction","volume":"79","author":"Khaliq","year":"1999","journal-title":"Lab. Invest"},{"issue":"A","key":"10.1016\/j.placenta.2017.10.004_bib28","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1053\/plac.1999.0522","article-title":"Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia","volume":"21","author":"Caniggia","year":"2000","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1053\/plac.2002.0878","article-title":"The 'reference trap' revisited: examples of the dangers in using ratios to describe fetoplacental angiogenesis and trophoblast turnover","volume":"24","author":"Mayhew","year":"2003","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib30","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1016\/j.placenta.2008.08.017","article-title":"Quantitative 3D micro-CT imaging of the human feto-placental vasculature in intrauterine growth restriction","volume":"29","author":"Langheinrich","year":"2008","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib31","doi-asserted-by":"crossref","first-page":"4114","DOI":"10.1038\/s41598-017-04379-0","article-title":"Whole organ vascular casting and microCT examination of the human placental vascular tree reveals novel alterations associated with pregnancy disease","volume":"7","author":"Junaid","year":"2017","journal-title":"Sci. Rep."},{"key":"10.1016\/j.placenta.2017.10.004_bib32","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.ajpath.2013.03.016","article-title":"Syncytial knots (Tenney-Parker changes) in the human placenta: evidence of loss of transcriptional activity and oxidative damage","volume":"183","author":"Fogarty","year":"2013","journal-title":"Am. J. Pathol."},{"key":"10.1016\/j.placenta.2017.10.004_bib33","first-page":"144","article-title":"Uber \u201cProliferationsknoten\u201d und \u201cSyncytialbr\u00fccken\u201d der menschlichen Plazenta","volume":"150","author":"K\u00fcstermann","year":"1981","journal-title":"Anat. Anz"},{"key":"10.1016\/j.placenta.2017.10.004_bib34","first-page":"13","article-title":"Intervillous connections in the mature human placenta: instances of syncytial fusion or section artifacts?","volume":"145","author":"Burton","year":"1986","journal-title":"J.\u00a0Anat."},{"key":"10.1016\/j.placenta.2017.10.004_bib35","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/0143-4004(87)90046-4","article-title":"Interpretation of syncytial sprouts and bridges in the human placenta","volume":"8","author":"Cantle","year":"1987","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2017.10.004_bib36","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1111\/j.1471-0528.1965.tb01469.x","article-title":"The siginificance of villous syncytial knots in the human placenta","volume":"72","author":"Fox","year":"1965","journal-title":"J.\u00a0Obstet. Gynaecol. Br. Commonw."},{"key":"10.1016\/j.placenta.2017.10.004_bib37","first-page":"1687","article-title":"Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in\u00a0vitro","volume":"79","author":"Huppertz","year":"1999","journal-title":"Lab. Invest"},{"key":"10.1016\/j.placenta.2017.10.004_bib38","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.ajog.2005.07.039","article-title":"Apoptosis and its role in the trophoblast","volume":"195","author":"Huppertz","year":"2006","journal-title":"Am. J. Obstet. Gynecol."},{"key":"10.1016\/j.placenta.2017.10.004_bib39","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/j.placenta.2016.04.001","article-title":"Mitochondrial - endoplasmic reticulum interactions in the trophoblast: stress and senescence","volume":"52","author":"Burton","year":"2017","journal-title":"Placenta"}],"container-title":["Placenta"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0143400417311451?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0143400417311451?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,26]],"date-time":"2025-09-26T17:56:00Z","timestamp":1758909360000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0143400417311451"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,12]]},"references-count":39,"alternative-id":["S0143400417311451"],"URL":"https:\/\/doi.org\/10.1016\/j.placenta.2017.10.004","relation":{},"ISSN":["0143-4004"],"issn-type":[{"value":"0143-4004","type":"print"}],"subject":[],"published":{"date-parts":[[2017,12]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Syncytial nuclei accumulate at the villous surface in IUGR while proliferation is unchanged","name":"articletitle","label":"Article Title"},{"value":"Placenta","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.placenta.2017.10.004","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2017 The Authors. Published by Elsevier Ltd.","name":"copyright","label":"Copyright"}]}}