{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T13:18:06Z","timestamp":1793452686420,"version":"4.5.0"},"reference-count":57,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2009,3,1]],"date-time":"2009-03-01T00:00:00Z","timestamp":1235865600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2009,3,1]],"date-time":"2009-03-01T00:00:00Z","timestamp":1235865600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2013,7,16]],"date-time":"2013-07-16T00:00:00Z","timestamp":1373932800000},"content-version":"vor","delay-in-days":1598,"URL":"http:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"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":[[2009,3]]},"DOI":"10.1016\/j.placenta.2008.11.003","type":"journal-article","created":{"date-parts":[[2008,12,10]],"date-time":"2008-12-10T10:09:59Z","timestamp":1228903799000},"page":"43-48","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":455,"special_numbering":"S","title":["Placental Endoplasmic Reticulum Stress and Oxidative Stress in the Pathophysiology of Unexplained Intrauterine Growth Restriction and Early Onset Preeclampsia"],"prefix":"10.1016","volume":"30","author":[{"given":"G.J.","family":"Burton","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H.-W.","family":"Yung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"T.","family":"Cindrova-Davies","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D.S.","family":"Charnock-Jones","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.placenta.2008.11.003_bib1","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.ajog.2005.07.049","article-title":"Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia","volume":"195","author":"Ness","year":"2006","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib2","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1111\/j.1471-0528.1977.tb12676.x","article-title":"Fetal growth retardation and the arteries of the placental bed","volume":"84","author":"Brosens","year":"1977","journal-title":"Br J Obstet Gynaecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib3","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1111\/j.1471-0528.1981.tb02222.x","article-title":"Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation","volume":"88","author":"Gerretsen","year":"1981","journal-title":"Br J Obstet Gynaecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib4","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1111\/j.1471-0528.1994.tb13182.x","article-title":"A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies","volume":"101","author":"Meekins","year":"1994","journal-title":"Br J Obstet Gynaecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib5","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1053\/plac.2002.0850","article-title":"The human placental bed revisited","volume":"23","author":"Lyall","year":"2002","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2008.11.003_bib6","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1111\/j.1471-0528.1986.tb07830.x","article-title":"Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants","volume":"93","author":"Khong","year":"1986","journal-title":"Br J Obstet Gynaecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib7","first-page":"43","article-title":"The morphology of human uteroplacental vasculature","volume":"38","author":"Harris","year":"1966","journal-title":"Contrib Embryol"},{"key":"10.1016\/j.placenta.2008.11.003_bib8","first-page":"153","article-title":"The form and functions of the uterine blood vessels in the rhesus monkey","volume":"36","author":"Bartelmez","year":"1957","journal-title":"Contrib Embryol"},{"key":"10.1016\/j.placenta.2008.11.003_bib9","doi-asserted-by":"crossref","first-page":"1416","DOI":"10.1067\/mob.2002.127305","article-title":"The myometrial junctional zone spiral arteries in normal and abnormal pregnancies","volume":"187","author":"Brosens","year":"2002","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib10","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1017\/S0965539503001049","article-title":"Hypoxia-reoxygenation: a potential source of placental oxidative stress in normal pregnancy and preeclampsia","volume":"14","author":"Burton","year":"2003","journal-title":"Fetal Mat Med Rev"},{"key":"10.1016\/j.placenta.2008.11.003_bib11","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1016\/S0002-9440(10)61778-6","article-title":"In vitro ischemia\u2013reperfusion injury in term human placenta as a model for oxidative stress in pathological pregnancies","volume":"159","author":"Hung","year":"2001","journal-title":"Am J Pathol"},{"key":"10.1016\/j.placenta.2008.11.003_bib12","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1111\/j.1471-0528.1964.tb04270.x","article-title":"A study of the spiral arteries of the decidua basalis in normotensive and hypertensive pregnancies","volume":"71","author":"Brosens","year":"1964","journal-title":"J Obstet Gynaecol Br Cwlth"},{"key":"10.1016\/j.placenta.2008.11.003_bib13","doi-asserted-by":"crossref","first-page":"948","DOI":"10.1111\/j.1471-0528.1976.tb00781.x","article-title":"The ultrastructure of the arterial supply of the human placenta in pregnancy complicated by fetal growth retardation","volume":"83","author":"Sheppard","year":"1976","journal-title":"Br J Obstet Gynaecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib14","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1016\/j.ajog.2005.10.813","article-title":"Preeclampsia, gestational hypertension and intrauterine growth restriction, related or independent conditions?","volume":"194","author":"Villar","year":"2006","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib15","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.placenta.2006.02.011","article-title":"The placenta in pre-eclampsia and intrauterine growth restriction: studies on exchange surface areas, diffusion distances and villous membrane diffusive conductances","volume":"28","author":"Mayhew","year":"2007","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2008.11.003_bib16","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1016\/S0143-4004(98)90018-2","article-title":"Placental mitochondria as a source of oxidative stress in pre-eclampsia","volume":"19","author":"Wang","year":"1998","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2008.11.003_bib17","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1161\/01.RES.0000024411.22110.AA","article-title":"Hypoxia\/reoxygenation: a potent inducer of apoptotic changes in the human placenta and possible etiological factor in preeclampsia","volume":"90","author":"Hung","year":"2002","journal-title":"Circ Res"},{"key":"10.1016\/j.placenta.2008.11.003_bib18","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1038\/sj.cdd.4401593","article-title":"A novel Mtd splice isoform is responsible for trophoblast cell death in pre-eclampsia","volume":"12","author":"Soleymanlou","year":"2005","journal-title":"Cell Death Differ"},{"key":"10.1016\/j.placenta.2008.11.003_bib19","doi-asserted-by":"crossref","first-page":"2656","DOI":"10.1172\/JCI26373","article-title":"Endoplasmic reticulum stress: cell life and death decisions","volume":"115","author":"Xu","year":"2005","journal-title":"J Clin Invest"},{"key":"10.1016\/j.placenta.2008.11.003_bib20","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/j.biocel.2005.09.018","article-title":"Coordination of ER and oxidative stress signaling: the PERK\/Nrf2 signaling pathway","volume":"38","author":"Cullinan","year":"2006","journal-title":"Int J Biochem Cell Biol"},{"key":"10.1016\/j.placenta.2008.11.003_bib21","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1111\/j.1742-4658.2007.05639.x","article-title":"ER stress and diseases","volume":"274","author":"Yoshida","year":"2007","journal-title":"FEBS J"},{"key":"10.1016\/j.placenta.2008.11.003_bib22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1471-4159.2004.02703.x","article-title":"Cerebral ischemia and the unfolded protein response","volume":"91","author":"DeGracia","year":"2004","journal-title":"J Neurochem"},{"key":"10.1016\/j.placenta.2008.11.003_bib23","doi-asserted-by":"crossref","first-page":"1511","DOI":"10.2353\/ajpath.2007.061035","volume":"170","author":"Cindrova-Davies","year":"2007","journal-title":"Am J Pathol"},{"key":"10.1016\/j.placenta.2008.11.003_bib24","doi-asserted-by":"crossref","first-page":"451","DOI":"10.2353\/ajpath.2008.071193","article-title":"Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction","volume":"173","author":"Yung","year":"2008","journal-title":"Am J Pathol"},{"key":"10.1016\/j.placenta.2008.11.003_bib25","doi-asserted-by":"crossref","first-page":"8505","DOI":"10.1073\/pnas.96.15.8505","article-title":"Mammalian unfolded protein response inhibits cyclin D1 translation and cell-cycle progression","volume":"96","author":"Brewer","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.placenta.2008.11.003_bib26","first-page":"A.99","article-title":"Stereological evidence for reduced cytotrophoblast proliferation in severe IUGR","volume":"29","author":"Widdows","year":"2008","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2008.11.003_bib27","doi-asserted-by":"crossref","first-page":"32124","DOI":"10.1074\/jbc.M302847200","article-title":"Protein kinase B alpha\/Akt1 regulates placental development and fetal growth","volume":"278","author":"Yang","year":"2003","journal-title":"J Biol Chem"},{"key":"10.1016\/j.placenta.2008.11.003_bib28","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1067\/mob.2001.112906","article-title":"Increased placental apoptosis in pregnancies complicated by preeclampsia","volume":"184","author":"Leung","year":"2001","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib29","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1016\/S0002-9378(97)70081-4","article-title":"Increased placental apoptosis in intrauterine growth restriction","volume":"177","author":"Smith","year":"1997","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib30","first-page":"271","article-title":"Placental apoptosis in preeclampsia","volume":"96","author":"Allaire","year":"2000","journal-title":"Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib31","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1067\/mob.2002.119176","article-title":"Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation","volume":"186","author":"Ishihara","year":"2002","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib32","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.placenta.2004.11.007","article-title":"Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction","volume":"27","author":"Goswami","year":"2006","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2008.11.003_bib33","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1053\/plac.2000.0560","article-title":"Placental debris, oxidative stress and pre-eclampsia","volume":"21","author":"Redman","year":"2000","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2008.11.003_bib34","series-title":"Free radicals in biology and medicine","author":"Halliwell","year":"1999"},{"key":"10.1016\/j.placenta.2008.11.003_bib35","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1016\/S0002-9378(96)70410-6","article-title":"Hyperuricemia and xanthine oxidase in preeclampsia, revisited","volume":"174","author":"Many","year":"1996","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib36","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1083\/jcb.200311055","article-title":"Oxidative protein folding in eukaryotes: mechanisms and consequences","volume":"164","author":"Tu","year":"2004","journal-title":"J Cell Biol"},{"key":"10.1016\/j.placenta.2008.11.003_bib37","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1038\/nature07203","article-title":"From endoplasmic-reticulum stress to the inflammatory response","volume":"454","author":"Zhang","year":"2008","journal-title":"Nature"},{"key":"10.1016\/j.placenta.2008.11.003_bib38","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1016\/S0002-9440(10)63192-6","article-title":"Secretion of tumour necrosis factor-a from human placental tissues induced by hypoxia-reoxygenation causes endothelial cell activation in vitro: a potential mediator of the inflammatory response in preeclampsia","volume":"164","author":"Hung","year":"2004","journal-title":"Am J Pathol"},{"key":"10.1016\/j.placenta.2008.11.003_bib39","doi-asserted-by":"crossref","first-page":"400","DOI":"10.2353\/ajpath.2006.060161","article-title":"Trophoblastic oxidative stress and the release of cell-free feto-placental DNA","volume":"169","author":"Tjoa","year":"2006","journal-title":"Am J Pathol"},{"issue":"Suppl. A","key":"10.1016\/j.placenta.2008.11.003_bib40","doi-asserted-by":"crossref","first-page":"S55","DOI":"10.1016\/j.placenta.2008.11.020","article-title":"Pre-eclampsia; from placental oxidative stress to maternal endothelial dysfunction","volume":"23","author":"Cindrova-Davies","year":"2009","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2008.11.003_bib41","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1046\/j.1525-1373.1999.d01-139.x","article-title":"Oxidative stress in the pathogenesis of preeclampsia","volume":"222","author":"Hubel","year":"1999","journal-title":"Proc Soc Exp Biol Med"},{"key":"10.1016\/j.placenta.2008.11.003_bib42","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1007\/s00418-004-0677-x","article-title":"Oxidative stress in the placenta","volume":"122","author":"Myatt","year":"2004","journal-title":"Histochem Cell Biol"},{"key":"10.1016\/j.placenta.2008.11.003_bib43","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1016\/S0140-6736(99)80002-6","article-title":"Is oxidative stress the link in the two-stage model of pre-eclampsia?","volume":"354","author":"Roberts","year":"1999","journal-title":"Lancet"},{"key":"10.1016\/j.placenta.2008.11.003_bib44","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.1126\/science.1111726","article-title":"Latest advances in understanding preeclampsia","volume":"308","author":"Redman","year":"2005","journal-title":"Science"},{"key":"10.1016\/j.placenta.2008.11.003_bib45","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1007\/s00428-003-0903-2","article-title":"Levels of oxidative stress and redox-related molecules in the placenta in preeclampsia and fetal growth restriction","volume":"444","author":"Takagi","year":"2004","journal-title":"Virchows Arch"},{"key":"10.1016\/j.placenta.2008.11.003_bib46","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.2353\/ajpath.2007.070528","article-title":"Oxidative stress, gene expression, and protein changes induced in the human placenta during labor","volume":"171","author":"Cindrova-Davies","year":"2007","journal-title":"Am J Pathol"},{"key":"10.1016\/j.placenta.2008.11.003_bib47","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1053\/plac.2000.0554","article-title":"Decreased expression of thioredoxin and glutaredoxin in placentae from pregnancies with pre-eclampsia and intrauterine growth restriction","volume":"21","author":"Sahlin","year":"2000","journal-title":"Placenta"},{"issue":"45","key":"10.1016\/j.placenta.2008.11.003_bib48","first-page":"e1","article-title":"Increased expression of N-myc downstream-regulated gene 1 (NDRG1) in placentas from pregnancies complicated by intrauterine growth restriction or preeclampsia","volume":"196","author":"Choi","year":"2007","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib49","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1186\/1471-2164-6-111","article-title":"Hypoxia-activated genes from early placenta are elevated in preeclampsia, but not in intra-uterine growth retardation","volume":"6","author":"Vaiman","year":"2005","journal-title":"BMC Genomics"},{"key":"10.1016\/j.placenta.2008.11.003_bib50","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1203\/01.PDR.0000181381.82856.23","article-title":"Placental phenotypes of intrauterine growth","volume":"58","author":"Sibley","year":"2005","journal-title":"Ped Res"},{"key":"10.1016\/j.placenta.2008.11.003_bib51","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1016\/j.placenta.2008.07.001","article-title":"Placental system A amino acid transport is reduced in pregnancies with small for gestational age (SGA) infants but not in preeclampsia with SGA infants","volume":"29","author":"Shibata","year":"2008","journal-title":"Placenta"},{"key":"10.1016\/j.placenta.2008.11.003_bib52","doi-asserted-by":"crossref","first-page":"4895","DOI":"10.1210\/jc.2004-1955","article-title":"Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: relationship to circulating placental growth factor","volume":"90","author":"Shibata","year":"2005","journal-title":"J Clin Endocrinol Metab"},{"key":"10.1016\/j.placenta.2008.11.003_bib53","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1080\/14767050701832833","article-title":"The maternal plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated in SGA and the magnitude of the increase relates to Doppler abnormalities in the maternal and fetal circulation","volume":"21","author":"Chaiworapongsa","year":"2008","journal-title":"J Matern Fetal Neonatal Med"},{"key":"10.1016\/j.placenta.2008.11.003_bib54","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1001\/jama.293.1.77","article-title":"Urinary placental growth factor and risk of preeclampsia","volume":"293","author":"Levine","year":"2005","journal-title":"JAMA"},{"key":"10.1016\/j.placenta.2008.11.003_bib55","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1067\/mob.2003.27","article-title":"Cell-free fetal DNA in the plasma of pregnant women with severe fetal growth restriction","volume":"188","author":"Sekizawa","year":"2003","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.placenta.2008.11.003_bib56","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1093\/molehr\/gal064","article-title":"Relationships between maternal plasma leptin, placental leptin mRNA and protein in normal pregnancy, pre-eclampsia and intrauterine growth restriction without pre-eclampsia","volume":"12","author":"Laivuori","year":"2006","journal-title":"Mol Hum Reprod"},{"key":"10.1016\/j.placenta.2008.11.003_bib57","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1111\/j.1471-0528.2002.01045.x","article-title":"Does endothelial cell activation occur with intrauterine growth restriction?","volume":"109","author":"Johnson","year":"2002","journal-title":"BJOG"}],"container-title":["Placenta"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0143400408003755?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0143400408003755?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,26]],"date-time":"2025-09-26T17:40:28Z","timestamp":1758908428000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0143400408003755"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,3]]},"references-count":57,"alternative-id":["S0143400408003755"],"URL":"https:\/\/doi.org\/10.1016\/j.placenta.2008.11.003","relation":{},"ISSN":["0143-4004"],"issn-type":[{"value":"0143-4004","type":"print"}],"subject":[],"published":{"date-parts":[[2009,3]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Placental Endoplasmic Reticulum Stress and Oxidative Stress in the Pathophysiology of Unexplained Intrauterine Growth Restriction and Early Onset Preeclampsia","name":"articletitle","label":"Article Title"},{"value":"Placenta","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.placenta.2008.11.003","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2009 IFPA and Elsevier Ltd.","name":"copyright","label":"Copyright"}]}}