Placental biomarkers of fetal-originated diseases
DOI:
https://doi.org/10.54844/prm.2024.0466Keywords:
placenta, adverse environment, fetal growth restriction, fetal-originated diseases, biomarkersAbstract
Fetal-originated diseases refer to birth defects of offspring and multiple chronic diseases in adulthood caused by abnormal embryonic development. However, due to the vulnerability of the fetus/ neonate and technical limitations, it is very difficult to carry out effective development assessment and early warning of long-term diseases in the early stages of life. It is known that the placenta is the unique link between the mother and the fetus, and its role in the occurrence and progression of fetal-originated diseases cannot be ignored. Studies have found that a variety of adverse environmental factors (such as nanoparticle exposure) cannot pass through the placental barrier, but can lead to fetal dysplasia and multi-organ development programming changes by affecting placental development, and ultimately mediate the occurrence of fetal-originated diseases. Meanwhile, some environmental factors that can pass through the placental barrier can cause placenta-fetal co-exposure, resulting in similar signaling pathways and epigenetic changes. The placenta originates from the fetus and the mother, and its development is accompanied by changes in indicators that can be objectively and quantitatively detected. These factors can be used as a biomarker to assess maternal exposure, and placental function, and to predict the developmental status and long-term disease susceptibility of offspring. To date, researchers have discovered a variety of potential placental biomarkers, and show promising application prospects. This paper reviews the recent research on placenta-related mechanisms leading to fetal-originated diseases and placental biomarkers, to provide the theoretical and experimental basis for early warning, prevention, and treatment of fetal-originated diseases.
References
Uauy R, Kain J, Corvalan C. How can the Developmental Origins of Health and Disease (DOHaD) hypothesis contribute to improving health in developing countries? Am J Clin Nutr 2011;94:1759.
Hedderson MM, Ferrara A, Avalos LA, et al. The Kaiser Permanente Northern California research program on genes, environment, and health (RPGEH) pregnancy cohort:study design, methodology and baseline characteristics. BMC Pregnancy Childbirth 2016;16:381.
Fleming TP, Sun C, Denisenko O, et al. Environmental Exposures around Conception:Developmental Pathways Leading to Lifetime Disease Risk. Int J Environ Res Public Health 2021;18:9380.
Drwal E, Rak A, Gregoraszczuk EL. Review:Polycyclic aromatic hydrocarbons (PAHs)-Action on placental function and health risks in future life of newborns. Toxicology 2019;411:133–142.
Morales-Rubio RA, Alvarado-Cruz I, Manzano-León N, et al. In utero exposure to ultrafine particles promotes placental stress-induced programming of renin-angiotensin system-related elements in the offspring results in altered blood pressure in adult mice. Part Fibre Toxicol 2019;16:7.
Ghosh R, Causey K, Burkart K, Wozniak S, Cohen A, Brauer M. Ambient and household PM2.5 pollution and adverse perinatal outcomes:A meta-regression and analysis of attributable global burden for 204 countries and territories. PLoS Med 2021;18:e1003718.
Arias A, Schander JA, Bariani MV, et al. Dexamethasone-induced intrauterine growth restriction modulates expression of placental vascular growth factors and fetal and placental growth. Mol Hum Reprod 2021;27:gaab006.
Bar-Lev MR, Maayan-Metzger A, Matok I, Heyman Z, Sivan E, Kuint J. Short-term outcomes in low birth weight infants following antenatal exposure to betamethasone versus dexamethasone. Obstet Gynecol 2004;104:484–488.
Xiong YW, Zhu HL, Nan Y, et al. Maternal cadmium exposure during late pregnancy causes fetal growth restriction via inhibiting placental progesterone synthesis. Ecotoxicol Environ Saf 2020;187:109879.
Zhu HL, Shi XT, Xu XF, et al. Environmental cadmium exposure induces fetal growth restriction via triggering PERK-regulated mitophagy in placental trophoblasts. Environ Int 2021;147:106319.
Liu L, Liu F, Kou H, et al. Prenatal nicotine exposure induced a hypothalamic-pituitary-adrenal axis-associated neuroendocrine metabolic programmed alteration in intrauterine growth retardation offspring rats. Toxicol Lett 2012;214:307–313.
Feng JH, Yan YE, Liang G, et al. Maternal and fetal metabonomic alterations in prenatal nicotine exposure-induced rat intrauterine growth retardation. Mol Cell Endocrinol 2014;394(1–2):59–69. DOI:10.1016/j.mce.2014.06.016]
Connor S, Tan KY, Pestell CF, Fitzpatrick JP. The Demographic and Neurocognitive Profile of Clients Diagnosed With Fetal Alcohol Spectrum Disorder in PATCHES Paediatrics Clinics Across Western Australia and the Northern Territory. Alcohol Clin Exp Res 2020;44:1284–1291.
He Z, Zhang J, Chen G, et al. H19/let-7 axis mediates caffeine exposure during pregnancy induced adrenal dysfunction and its multi-generation inheritance. Sci Total Environ 2021;792:148440.
Jafari A, Naghshi S, Shahinfar H, et al. Relationship between maternal caffeine and coffee intake and pregnancy loss:A grading of recommendations assessment, development, and evaluation-assessed, dose-response meta-analysis of observational studies. Front Nutr 2022;9:886224.
Janardhan N, Roy PG, Vyas AK. Impact of maternal substance use on offspring's cardiovascular health. Toxicol Appl Pharmacol 2022;450:116164.
Cestonaro C, Menozzi L, Terranova C. Infants of Mothers with Cocaine Use:Review of Clinical and Medico-Legal Aspects. Children (Basel) 2022;9(1):67. [PMID:35053692 DOI:10.3390/children9010067]
Velez ML, Jordan C, Jansson LM. Reconceptualizing non-pharmacologic approaches to Neonatal Abstinence Syndrome (NAS) and Neonatal Opioid Withdrawal Syndrome (NOWS):A theoretical and evidence-based approach. Part II:The clinical application of nonpharmacologic care for NAS/NOWS. Neurotoxicol Teratol 2021;88:107032.
Albano GD, La Spina C, Pitingaro W, et al. Intrauterine and Neonatal Exposure to Opioids:Toxicological, Clinical, and Medico-Legal Issues. Toxics 2023;11:62.
Hawkins SJ, Crompton LA, Sood A, et al. Nanoparticle-induced neuronal toxicity across placental barriers is mediated by autophagy and dependent on astrocytes. Nat Nanotechnol 2018;13:427–433.
Choi H, Rauh V, Garfinkel R, Tu Y, Perera FP. Prenatal exposure to airborne polycyclic aromatic hydrocarbons and risk of intrauterine growth restriction. Environ Health Perspect 2008;116:658–665.
Perera FP, Rauh V, Tsai WY, et al. Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population. Environ Health Perspect 2003;111:201–205.
Li R, Wang X, Wang B, et al. Gestational 1-nitropyrene exposure causes fetal growth restriction through disturbing placental vascularity and proliferation. Chemosphere 2018;213:252–258.
Yingya Zhao, Qi Song, Wenzhen Ge, et al. Associations between in utero exposure to polybrominated diphenyl ethers, pathophysiological state of fetal growth and placental DNA methylation changes. Environ Int 2019;133:105255.
Jin Y, Li J, Deng X, et al. Association between fetal growth restriction and maternal exposure to polybrominated diphenyl ethers. Ecotoxicol Environ Saf 2020;198:110623.
Yu Z, Han Y, Shen R, et al. Gestational di-(2-ethylhexyl) phthalate exposure causes fetal intrauterine growth restriction through disturbing placental thyroid hormone receptor signaling. Toxicol Lett 2018;294:1–10.
Guo C, Yang Y, Shi MX, et al. Critical time window of fenvalerate-induced fetal intrauterine growth restriction in mice. Ecotoxicol Environ Saf 2019;172:186–193.
Wang B, Liu JJ, Wang Y, et al. Maternal Fenvalerate Exposure Induces Fetal Intrauterine Growth Restriction Through Disrupting Placental Thyroid Hormone Receptor Signaling. Toxicol Sci 2017;157:377–386.
Sabra S, Malmqvist E, Saborit A, Gratacos E, Gomez Roig MD. Heavy metals exposure levels and their correlation with different clinical forms of fetal growth restriction. PLoS One 2017;12:e0185645.
Camsari C, Folger JK, McGee D, et al. Effects of Periconception Cadmium and Mercury Co-Administration to Mice on Indices of Chronic Diseases in Male Offspring at Maturity. Environ Health Perspect 2017;125:643–650.
Müller JE, Meyer N, Santamaria CG, et al. Bisphenol A exposure during early pregnancy impairs uterine spiral artery remodeling and provokes intrauterine growth restriction in mice. Sci Rep 2018;8:9196.
Nava-Castro KE, Ramírez-Nieto R, Méndez-García LA, et al. Environmental Pollution as a Risk Factor in Testicular Tumour Development:Focus on the Interaction between Bisphenol A and the Associated Immune Response. Int J Environ Res Public Health 2019;16:4113.
Levario-Carrillo M, Amato D, Ostrosky-Wegman P, González-Horta C, Corona Y, Sanin LH. Relation between pesticide exposure and intrauterine growth retardation. Chemosphere 2004;55:1421–1427.
Zhao Y, Chen L, Li LX, et al. Gender-specific relationship between prenatal exposure to phthalates and intrauterine growth restriction. Pediatr Res 2014;76:401–408.
Milnerowicz-Nabzdyk E, Bizon A. How does tobacco smoke influence the morphometry of the fetus and the umbilical cord?-Research on pregnant women with intrauterine growth restriction exposed to tobacco smoke. Reprod Toxicol 2015;58:79–84.
Onoda A, Takeda K, Umezawa M. Pretreatment with N-acetyl cysteine suppresses chronic reactive astrogliosis following maternal nanoparticle exposure during gestational period. Nanotoxicology 2017;11:1012–1025.
Carter RC, Wainwright H, Molteno CD, et al. Alcohol, Methamphetamine, and Marijuana Exposure Have Distinct Effects on the Human Placenta. Alcohol Clin Exp Res 2016;40:753–764.
Singh M, Varukolu S, Chauhan A, et al. Paracetamol exposure and asthma:What does the evidence say? An overview of systematic reviews. Pediatr Pulmonol 2021;56:3189–3199.
Ryan L, Ehrlich S, Finnegan L. Cocaine abuse in pregnancy:effects on the fetus and newborn. Neurotoxicol Teratol 1987;9:295–299.
Xiao D, Huang X, Xu Z, Yang S, Zhang L. Prenatal cocaine exposure differentially causes vascular dysfunction in adult offspring. Hypertension 2009;53:937–943.
Pacheco ALD, de Melo IS, de Souza FMA, et al. Maternal crack cocaine use in rats leads to depressive- and anxiety-like behavior, memory impairment, and increased seizure susceptibility in the offspring. Eur Neuropsychopharmacol 2021;44:34–50.
de Castro A, Jones HE, Johnson RE, Gray TR, Shakleya DM, Huestis MA. Maternal methadone dose, placental methadone concentrations, and neonatal outcomes. Clin Chem 2011;57:449–458.
Hulse GK, Milne E, English DR, Holman CD. The relationship between maternal use of heroin and methadone and infant birth weight. Addiction 1997;92(11):1571–1579.
Fishman B, Daniel S, Koren G, Lunenfeld E, Levy A. Pregnancy outcome following opioid exposure:A cohort study. PLoS One 2019;14:e0219061.
Straub HL, Mou J, Drennan KJ, Pflugeisen BM. Maternal Marijuana Exposure and Birth Weight:An Observational Study Surrounding Recreational Marijuana Legalization. Am J Perinatol 2021;38:65–75.
Smid MC, Metz TD, McMillin GA, et al. Prenatal Nicotine or Cannabis Exposure and Offspring Neurobehavioral Outcomes. Obstet Gynecol 2022;139:21–30.
Paul SE, Hatoum AS, Fine JD, et al. Associations Between Prenatal Cannabis Exposure and Childhood Outcomes:Results From the ABCD Study. JAMA Psychiatry 2021;78:64–76.
Doi M, Nakama N, Sumi T, Usui N, Shimada S. Prenatal methamphetamine exposure causes dysfunction in glucose metabolism and low birthweight. Front Endocrinol (Lausanne) 2022;13:1023984.
Dong N, Zhu J, Han W, et al. Maternal methamphetamine exposure causes cognitive impairment and alteration of neurodevelopment-related genes in adult offspring mice. Neuropharmacology 2018;140:25–34.
Sanjari Moghaddam H, Mobarak Abadi M, Dolatshahi M, et al. Effects of Prenatal Methamphetamine Exposure on the Developing Human Brain:A Systematic Review of Neuroimaging Studies. ACS Chem Neurosci 2021;12:2729–2748.
Lu X, Mao T, Dai Y, et al. Azithromycin exposure during pregnancy disturbs the fetal development and its characteristic of multi-organ toxicity. Life Sci 2023;329:121985. [PMID:37516432 DOI:10.1016/j.lfs.2023.121985]
Flory T Muanda, Odile Sheehy, Anick Bérard. Use of antibiotics during pregnancy and risk of spontaneous abortion. CMAJ 2017;189:E625–E633.
Voormolen DN, de Wit L, van Rijn BB, et al. Neonatal Hypoglycemia Following Diet-Controlled and Insulin-Treated Gestational Diabetes Mellitus. Diabetes Care 2018;41:1385–1390.
Fraser A, Nelson SM, Macdonald-Wallis C, Sattar N, Lawlor DA. Hypertensive disorders of pregnancy and cardiometabolic health in adolescent offspring. Hypertension 2013;62:614–620.
Zheng W, Zhang X, Feng Y, et al. Association of Corpus Callosum Development With Fetal Growth Restriction and Maternal Preeclampsia or Gestational Hypertension. JAMA Netw Open 2022;5:e2226696.
Ayano G, Betts K, Tait R, Dachew BA, Alati R. Maternal depressive and anxiety symptoms and the risk of attention deficit hyperactivity disorder symptoms in offspring aged 17:Findings from the Raine Study. J Affect Disord 2021;284:149–156.
Zhu Q, Yang X, Zhang Y, Shan C, Shi Z. Role of the Gut Microbiota in the Increased Infant Body Mass Index Induced by Gestational Diabetes Mellitus. mSystems 2022;7:e0046522.
Chu AHY, Godfrey KM. Gestational Diabetes Mellitus and Developmental Programming. Ann Nutr Metab 2020;76 Suppl 3:4-15.
Furse S, Koulman A, Ozanne SE, Poston L, White SL, Meek CL. Altered Lipid Metabolism in Obese Women With Gestational Diabetes and Associations With Offspring Adiposity. J Clin Endocrinol Metab 2022;107:e2825-e2832.
Kim C, Harrall KK, Glueck DH, Needham BL, Dabelea D. Gestational diabetes mellitus, epigenetic age and offspring metabolism. Diabet Med 2022;39:e14925.
Yu Y, Arah OA, Liew Z, et al. Maternal diabetes during pregnancy and early onset of cardiovascular disease in offspring:population based cohort study with 40 years of follow-up. BMJ 2019;367:l6398.
Yamamoto JM, Benham JL, Dewey D, et al. Neurocognitive and behavioural outcomes in offspring exposed to maternal pre-existing diabetes:a systematic review and meta-analysis. Diabetologia 2019;62:1561-1574.
Smith CA. Effects of maternal under nutrition upon the newborn infant in Holland (1944-1945). J Pediatr 1947;30:229-243.
Sarli PM, Manousopoulou A, Efthymiou E, et al. Liver Proteome Profile of Growth Restricted and Appropriately Grown Newborn Wistar Rats Associated With Maternal Undernutrition. Front Endocrinol (Lausanne) 2021;12:684220.
Zouridis A, Manousopoulou A, Potiris A, et al. Impact of Maternal Food Restriction on Heart Proteome in Appropriately Grown and Growth-Restricted Wistar-Rat Offspring. Nutrients 2021;13:466.
Potiris A, Manousopoulou A, Zouridis A, et al. The Effect of Prenatal Food Restriction on Brain Proteome in Appropriately Grown and Growth Restricted Male Wistar Rats. Front Neurosci 2021;15:665354.
Hagstrom H, Simon TG, Roelstraete B, Stephansson O, Soderling J, Ludvigsson JF. Maternal obesity increases the risk and severity of NAFLD in offspring. J Hepatol 2021;75:1042-1048.
Liu X, Li X, Xia B, et al. High-fiber diet mitigates maternal obesity-induced cognitive and social dysfunction in the offspring via gut-brain axis. Cell Metab 2021;33:923-938 e926.
Davenport BN, Wilson RL, Jones HN. Interventions for placental insufficiency and fetal growth restriction. Placenta 2022;125:4-9.
Eriksson JG, Kajantie E, Thornburg KL, Osmond C, Barker DJ. Mother's body size and placental size predict coronary heart disease in men. Eur Heart J 2011;32:2297-2303.
Hu C, Wu Z, Huang Z, Hao X, Wang S, Deng J. et al. Nox2 impairs VEGF-A-induced angiogenesis in placenta via mitochondrial ROS-STAT3 pathway. Redox Biol 2021;45:102051.
McIntyre KR, Hayward CE, Sibley CP, Greenwood SL, Dilworth MR. Evidence of adaptation of maternofetal transport of glutamine relative to placental size in normal mice, and in those with fetal growth restriction. J Physiol 2019;597:4975-4990.
Janzen C, Lei MY, Cho J, Sullivan P, Shin BC, Devaskar SU. Placental glucose transporter 3 (GLUT3) is up-regulated in human pregnancies complicated by late-onset intrauterine growth restriction. Placenta 2013;34:1072-1078.
Xu P, Wu Z, Xi Y, Wang L. Epigenetic regulation of placental glucose transporters mediates maternal cadmium-induced fetal growth restriction. Toxicology 2016;372:34-41.
Jansson T, Castillo-Castrejon M, Gupta MB, Powell TL, Rosario FJ. Down-regulation of placental Cdc42 and Rac1 links mTORC2 inhibition to decreased trophoblast amino acid transport in human intrauterine growth restriction. Clin Sci (Lond) 2020;134:53-70.
Chen YY, Rosario FJ, Shehab MA, Powell TL, Gupta MB, Jansson T. Increased ubiquitination and reduced plasma membrane trafficking of placental amino acid transporter SNAT-2 in human IUGR. Clin Sci (Lond) 2015;129:1131-1141.
Paolini CL, Marconi AM, Ronzoni S, et al. Placental transport of leucine, phenylalanine, glycine, and proline in intrauterine growth-restricted pregnancies. J Clin Endocrinol Metab 2001;86:5427-5432.
Johansson M, Karlsson L, Wennergren M, Jansson T, Powell TL. Activity and protein expression of Na+/K+ ATPase are reduced in microvillous syncytiotrophoblast plasma membranes isolated from pregnancies complicated by intrauterine growth restriction. J Clin Endocrinol Metab 2003;88:2831-2837.
Chassen SS, Ferchaud-Roucher V, Gupta MB, Jansson T, Powell TL. Alterations in placental long chain polyunsaturated fatty acid metabolism in human intrauterine growth restriction. Clin Sci (Lond) 2018;132:595-607.
Assumpcao RP, Mucci DB, Fonseca FCP, et al. Fatty acid profile of maternal and fetal erythrocytes and placental expression of fatty acid transport proteins in normal and intrauterine growth restriction pregnancies. Prostaglandins Leukot Essent Fatty Acids 2017;125:24-31.
Loubiere LS, Vasilopoulou E, Bulmer JN, et al. Expression of thyroid hormone transporters in the human placenta and changes associated with intrauterine growth restriction. Placenta 2010;31:295-304.
Chan SY, Franklyn JA, Pemberton HN, et al. Monocarboxylate transporter 8 expression in the human placenta:the effects of severe intrauterine growth restriction. J Endocrinol 2006;189:465-471.
Vasilopoulou E, Loubiere LS, Martin-Santos A, et al. Differential triiodothyronine responsiveness and transport by human cytotrophoblasts from normal and growth-restricted pregnancies. J Clin Endocrinol Metab 2010;95:4762-4770.
Settle P, Sibley CP, Doughty IM, et al. Placental lactate transporter activity and expression in intrauterine growth restriction. J Soc Gynecol Investig 2006;13:357-363.
Harrison DJ, Creeth HDJ, Tyson HR, et al. Placental endocrine insufficiency programs anxiety, deficits in cognition and atypical social behaviour in offspring. Hum Mol Genet 2021;30:1863-1880.
Whitehead CL, McNamara H, Walker SP, et al. Identifying late-onset fetal growth restriction by measuring circulating placental RNA in the maternal blood at 28 weeks' gestation. Am J Obstet Gynecol 2016;214:521 e521-521 e528.
Whitehead CL, Walker SP, Mendis S, Lappas M, Tong S. Quantifying mRNA coding growth genes in the maternal circulation to detect fetal growth restriction. Am J Obstet Gynecol 2013;209:133 e131-139.
Vacher CM, Lacaille H, O'Reilly JJ, et al. Placental endocrine function shapes cerebellar development and social behavior. Nat Neurosci 2021;24:1392-1401.
Sato K. Placenta-derived hypo-serotonin situations in the developing forebrain cause autism. Med Hypotheses 2013;80:368-372.
Ranzil S, Ellery S, Walker DW, et al. Disrupted placental serotonin synthetic pathway and increased placental serotonin:Potential implications in the pathogenesis of human fetal growth restriction. Placenta 2019;84:74-83.
Li D, Gao R, Qin L, Yue H, Sang N. New Insights into Prenatal NO2 Exposure and Behavioral Abnormalities in Male Offspring:Disturbed Serotonin Metabolism and Delayed Oligodendrocyte Development. Environ Sci Technol 2022;56:11536-11546.
Noorlander CW, Ververs FF, Nikkels PG, van Echteld CJ, Visser GH, Smidt MP. Modulation of serotonin transporter function during fetal development causes dilated heart cardiomyopathy and lifelong behavioral abnormalities. PLoS One 2008;3:e2782.
Wu YM, Luo HW, Kou H, et al. Prenatal caffeine exposure induced a lower level of fetal blood leptin mainly via placental mechanism. Toxicol Appl Pharmacol 2015;289:109-116.
Allbrand M, Eklund D, Cao Y, Nilsson K, Lodefalk M. Gene expression of leptin, leptin receptor isoforms and inflammatory cytokines in placentas of obese women- Associations to birth weight and fetal sex. Placenta 2022;117:64-71.
Visan V, Balan RA, Costea CF, et al. Morphological and histopathological changes in placentas of pregnancies with intrauterine growth restriction. Rom J Morphol Embryol 2020;61:477-483.
Wang T, Chen M, Yan YE, Xiao FQ, Pan XL, Wang H. Growth retardation of fetal rats exposed to nicotine in utero:possible involvement of CYP1A1, CYP2E1, and P-glycoprotein. Environ Toxicol 2009;24:33-42.
Ge C, Xu D, Yu P, et al. P-gp expression inhibition mediates placental glucocorticoid barrier opening and fetal weight loss. BMC Med 2021;19:311.
Marsit CJ, Maccani MA, Padbury JF, Lester BM. Placental 11-beta hydroxysteroid dehydrogenase methylation is associated with newborn growth and a measure of neurobehavioral outcome. PLoS One 2012;7:e33794.
Saegusa H, Nakagawa Y, Liu YJ, Ohzeki T. Influence of placental 11beta-hydroxysteroid dehydrogenase (11beta-HSD) inhibition on glucose metabolism and 11beta-HSD regulation in adult offspring of rats. Metabolism 1999;48:1584-1588.
Welberg LA, Seckl JR, Holmes MC. Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. Eur J Neurosci 2000;12:1047-1054.
Kratimenos P, Penn AA. Placental programming of neuropsychiatric disease. Pediatr Res 2019;86:157-164.
Behura SK, Kelleher AM, Spencer TE. Evidence for functional interactions between the placenta and brain in pregnant mice. FASEB J 2019;33:4261-4272.
Redline RW. Severe fetal placental vascular lesions in term infants with neurologic impairment. Am J Obstet Gynecol 2005;192:452-457.
Redline RW, O'Riordan MA. Placental lesions associated with cerebral palsy and neurologic impairment following term birth. Arch Pathol Lab Med 2000;124:1785-1791.
Whitehead E, Dodds L, Joseph KS, et al. Relation of pregnancy and neonatal factors to subsequent development of childhood epilepsy:a population-based cohort study. Pediatrics 2006;117:1298-1306.
Ruiz-Palacios M, Prieto-Sanchez MT, Ruiz-Alcaraz AJ, et al. Insulin Treatment May Alter Fatty Acid Carriers in Placentas from Gestational Diabetes Subjects. Int J Mol Sci 2017;18:1203.
Xu P, Guo H, Wang H, et al. Downregulations of placental fatty acid transporters during cadmium-induced fetal growth restriction. Toxicology 2019;423:112-122.
Goeden N, Velasquez J, Arnold KA, et al. Maternal Inflammation Disrupts Fetal Neurodevelopment via Increased Placental Output of Serotonin to the Fetal Brain. J Neurosci 2016;36:6041-6049.
Camm EJ, Botting KJ, Sferruzzi-Perri AN. Near to One's Heart:The Intimate Relationship Between the Placenta and Fetal Heart. Front Physiol 2018;9:629.
Barker DJ, Thornburg KL, Osmond C, Kajantie E, Eriksson JG. The surface area of the placenta and hypertension in the offspring in later life. Int J Dev Biol 2010;54:525-530.
Barker DJ, Gelow J, Thornburg K, Osmond C, Kajantie E, Eriksson JG. The early origins of chronic heart failure:impaired placental growth and initiation of insulin resistance in childhood. Eur J Heart Fail 2010;12:819-825.
Martyn CN, Barker DJ, Osmond C. Mothers' pelvic size, fetal growth, and death from stroke and coronary heart disease in men in the UK. Lancet 1996;348:1264-1268.
Burton GJ, Jauniaux E. Pathophysiology of placental-derived fetal growth restriction. Am J Obstet Gynecol 2018;218:S745-S761.
Linask KK, Han M, Bravo-Valenzuela NJ. Changes in vitelline and utero-placental hemodynamics:implications for cardiovascular development. Front Physiol 2014;5:390.
Maslen CL. Recent Advances in Placenta-Heart Interactions. Front Physiol 2018;9:735.
Linask KK. The heart-placenta axis in the first month of pregnancy:induction and prevention of cardiovascular birth defects. J Pregnancy 2013;2013:320413.
Kaufmann P, Mayhew TM, Charnock-Jones DS. Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta 2004;25:114-126.
Courtney JA, Cnota JF, Jones HN. The Role of Abnormal Placentation in Congenital Heart Disease;Cause, Correlate, or Consequence? Front Physiol 2018;9:1045.
Wilson RL, Yuan V, Courtney JA, Tipler A, Cnota JF, Jones HN. Analysis of commonly expressed genes between first trimester fetal heart and placenta cell types in the context of congenital heart disease. Sci Rep 2022;12:10756.
Woolford SJ, Curtis EM, D'Angelo S, et al. Placental volume at 11 weeks is associated with offspring bone mass at birth and in later childhood:Findings from the Southampton Women's Survey. Placenta 2020;99:101-107.
Holroyd CR, Osmond C, Barker DJ, et al. Placental Size Is Associated Differentially With Postnatal Bone Size and Density. J Bone Miner Res 2016;31:1855-1864.
Holroyd CR, Harvey NC, Crozier SR, et al. Placental size at 19 weeks predicts offspring bone mass at birth:findings from the Southampton Women's Survey. Placenta 2012;33:623-629.
Li SH, Yin HB, Ren MR, et al. TRPV5 and TRPV6 are expressed in placenta and bone tissues during pregnancy in mice. Biotech Histochem 2019;94:244-251.
Strimbu K, Tavel JA. What are biomarkers? Curr Opin HIV AIDS 2010;5:463-466.
Napso T, Zhao X, Lligona MI, et al. Placental secretome characterization identifies candidates for pregnancy complications. Commun Biol 2021;4:701.
Zamarian AC, Araujo Junior E, Daher S, Rolo LC, Moron AF, Nardozza LM. Evaluation of biochemical markers combined with uterine artery Doppler parameters in fetuses with growth restriction:a case-control study. Arch Gynecol Obstet 2016;294:715-723.
Yu N, Cui H, Chen X, Chang Y. First trimester maternal serum analytes and second trimester uterine artery Doppler in the prediction of preeclampsia and fetal growth restriction. Taiwan J Obstet Gynecol 2017;56:358-361.
Chafetz I, Kuhnreich I, Sammar M, et al. First-trimester placental protein 13 screening for preeclampsia and intrauterine growth restriction. Am J Obstet Gynecol 2007;197:35 e31-37.
Lo YM, Corbetta N, Chamberlain PF, et al. Presence of fetal DNA in maternal plasma and serum. Lancet 1997;350:485-487.
Poon LL, Leung TN, Lau TK, Lo YM. Presence of fetal RNA in maternal plasma. Clin Chem 2000;46:1832-1834.
Tsui NB, Chim SS, Chiu RW, et al. Systematic micro-array based identification of placental mRNA in maternal plasma:towards non-invasive prenatal gene expression profiling. J Med Genet 2004;41:461-467.
Go AT, van Vugt JM, Oudejans CB. Non-invasive aneuploidy detection using free fetal DNA and RNA in maternal plasma:recent progress and future possibilities. Hum Reprod Update 2011;17:372-382.
Chim SS, Shing TK, Hung EC, et al. Detection and characterization of placental microRNAs in maternal plasma. Clin Chem 2008;54:482-490.
Jelena M, Sopic M, Joksic I, et al. Placenta-specific plasma miR518b is a potential biomarker for preeclampsia. Clin Biochem 2020;79:28-33.
Vlahos A, Mansell T, Saffery R, Novakovic B. Human placental methylome in the interplay of adverse placental health, environmental exposure, and pregnancy outcome. PLoS Genet 2019;15:e1008236.
Ravaei A, Emanuele M, Nazzaro G, Fadiga L, Rubini M. Placental DNA methylation profile as predicting marker for autism spectrum disorder (ASD). Mol Med 2023;29:8.
Schroeder DI, Schmidt RJ, Crary-Dooley FK, et al. Placental methylome analysis from a prospective autism study. Mol Autism 2016;7:51.
Zhu Y, Mordaunt CE, Yasui DH, et al. Placental DNA methylation levels at CYP2E1 and IRS2 are associated with child outcome in a prospective autism study. Hum Mol Genet 2019;28:2659-2674.
Radhakrishna U, Albayrak S, Zafra R, et al. Placental epigenetics for evaluation of fetal congenital heart defects:Ventricular Septal Defect (VSD). PLoS One 2019;14:e0200229.
Paauw ND, Lely AT, Joles JA, et al. H3K27 acetylation and gene expression analysis reveals differences in placental chromatin activity in fetal growth restriction. Clin Epigenetics 2018;10:85.
Pedroso MA, Palmer KR, Hodges RJ, Costa FDS, Rolnik DL. Uterine Artery Doppler in Screening for Preeclampsia and Fetal Growth Restriction. Rev Bras Ginecol Obstet 2018;40:287-293.
Bakalis S, Peeva G, Gonzalez R, Poon LC, Nicolaides KH. Prediction of small-for-gestational-age neonates:screening by biophysical and biochemical markers at 30-34 weeks. Ultrasound Obstet Gynecol 2015;46:446-451.
Dieste-Perez P, Saviron-Cornudella R, Tajada-Duaso M, et al. Personalized Model to Predict Small for Gestational Age at Delivery Using Fetal Biometrics, Maternal Characteristics, and Pregnancy Biomarkers:A Retrospective Cohort Study of Births Assisted at a Spanish Hospital. J Pers Med 2022;12:762.
Kienast C, Moya W, Rodriguez O, Jijon A, Geipel A. Predictive value of angiogenic factors, clinical risk factors and uterine artery Doppler for pre-eclampsia and fetal growth restriction in second and third trimester pregnancies in an Ecuadorian population. J Matern Fetal Neonatal Med 2016;29:537-543.
Kwiatkowski S, Bednarek-Jedrzejek M, Ksel J, et al. sFlt-1/PlGF and Doppler ultrasound parameters in SGA pregnancies with confirmed neonatal birth weight below 10th percentile. Pregnancy Hypertens 2018;14:79-85.
Garcia-Manau P, Mendoza M, Bonacina E, et al. Soluble fms-like tyrosine kinase to placental growth factor ratio in different stages of early-onset fetal growth restriction and small for gestational age. Acta Obstet Gynecol Scand 2021;100:119-128.
Chen W, Wei Q, Liang Q, Song S, Li J. Diagnostic capacity of sFlt-1/PlGF ratio in fetal growth restriction:A systematic review and meta-analysis. Placenta 2022;127:37-42.
Cowans NJ, Spencer K. First-trimester ADAM12 and PAPP-A as markers for intrauterine fetal growth restriction through their roles in the insulin-like growth factor system. Prenat Diagn 2007;27:264-271.
Stepan H, Kramer T, Faber R. Maternal plasma concentrations of soluble endoglin in pregnancies with intrauterine growth restriction. J Clin Endocrinol Metab 2007;92:2831-2834.
Asvold BO, Vatten LJ, Romundstad PR, Jenum PA, Karumanchi SA, Eskild A. Angiogenic factors in maternal circulation and the risk of severe fetal growth restriction. Am J Epidemiol 2011;173:630-639.
Nanjo S, Minami S, Mizoguchi M, et al. Levels of serum-circulating angiogenic factors within 1 week prior to delivery are closely related to conditions of pregnant women with pre-eclampsia, gestational hypertension, and/or fetal growth restriction. J Obstet Gynaecol Res 2017;43:1805-1814.
Li Y, Liu J. MicroRNA-206 predicts raised fetal growth retardation risk through the interaction with vascular endothelial growth factor in pregnancies. Medicine (Baltimore) 2020;99:e18897.
Tang Y, Ye W, Liu X, Lv Y, Yao C, Wei J. VEGF and sFLT-1 in serum of PIH patients and effects on the foetus. Exp Ther Med 2019;17:2123-2128.
Bourque DK, Avila L, Penaherrera M, von Dadelszen P, Robinson WP. Decreased placental methylation at the H19/IGF2 imprinting control region is associated with normotensive intrauterine growth restriction but not preeclampsia. Placenta 2010;31:197-202.
Qiu Q, Bell M, Lu X, et al. Significance of IGFBP-4 in the development of fetal growth restriction. J Clin Endocrinol Metab 2012;97:E1429-1439.
Pang WW, Tsui MH, Sahota D, et al. A strategy for identifying circulating placental RNA markers for fetal growth assessment. Prenat Diagn 2009;29:495-504.
Kaitu'u-Lino TJ, MacDonald TM, Cannon P, et al. Circulating SPINT1 is a biomarker of pregnancies with poor placental function and fetal growth restriction. Nat Commun 2020;11:2411.
Kaitu'u-Lino TJ, Tong S, Walker SP, et al. Maternal circulating SPINT1 is reduced in small-for-gestational age pregnancies at 26 weeks:Growing up in Singapore towards health outcomes (GUSTO) cohort study. Placenta 2021;110:24-28.
Murphy CN, Cluver CA, Walker SP, et al. Circulating SPINT1 Is Reduced in a Preeclamptic Cohort with Co-Existing Fetal Growth Restriction. J Clin Med 2022;11:901.
MacDonald TM, Walker SP, Hiscock R, Cannon P, Harper A, Murray E. et al. Circulating Delta-like homolog 1 (DLK1) at 36 weeks is correlated with birthweight and is of placental origin. Placenta 2020;91:24-30.
Krauss T, Emons G, Kuhn W, Augustin HG. Predictive value of routine circulating soluble endothelial cell adhesion molecule measurements during pregnancy. Clin Chem 2002;48:1418-1425.
Schneuer FJ, Nassar N, Khambalia AZ, et al. First trimester screening of maternal placental protein 13 for predicting preeclampsia and small for gestational age:in-house study and systematic review. Placenta 2012;33:735-740.
Spencer K, Yu CK, Cowans NJ, Otigbah C, Nicolaides KH. Prediction of pregnancy complications by first-trimester maternal serum PAPP-A and free beta-hCG and with second-trimester uterine artery Doppler. Prenat Diagn 2005;25:949-953.
Gundu S, Kulkarni M, Gupte S, Gupte A, Gambhir M, Gambhir P. Correlation of first-trimester serum levels of pregnancy-associated plasma protein A with small-for-gestational-age neonates and preterm births. Int J Gynaecol Obstet 2016;133:159-163.
Canini S, Prefumo F, Pastorino D, et al. Association between birth weight and first-trimester free beta-human chorionic gonadotropin and pregnancy-associated plasma protein A. Fertil Steril 2008;89:174-178.
Crovetto F, Crispi F, Scazzocchio E, et al. First-trimester screening for early and late small-for-gestational-age neonates using maternal serum biochemistry, blood pressure and uterine artery Doppler. Ultrasound Obstet Gynecol 2014;43:34-40.
Erez O, Romero R, Espinoza J, et al. The change in concentrations of angiogenic and anti-angiogenic factors in maternal plasma between the first and second trimesters in risk assessment for the subsequent development of preeclampsia and small-for-gestational age. J Matern Fetal Neonatal Med 2008;21:279-287.
Regnault TR, Orbus RJ, de Vrijer B, et al. Placental expression of VEGF, PlGF and their receptors in a model of placental insufficiency-intrauterine growth restriction (PI-IUGR). Placenta 2002;23:132-144.
Sifakis S, Akolekar R, Kappou D, Mantas N, Nicolaides KH. Maternal serum placental growth hormone at 11-13 weeks' gestation in pregnancies delivering small for gestational age neonates. J Matern Fetal Neonatal Med 2012;25:1796-1799.
Cleaton MA, Dent CL, Howard M, et al. Fetus-derived DLK1 is required for maternal metabolic adaptations to pregnancy and is associated with fetal growth restriction. Nat Genet 2016;48:1473-1480.
Pham A, Mitanchez D, Forhan A, et al. Low Maternal DLK1 Levels at 26 Weeks Is Associated With Small for Gestational Age at Birth. Front Endocrinol (Lausanne) 2022;13:836731.
Ashraf UM, Hall DL, Rawls AZ, Alexander BT. Epigenetic processes during preeclampsia and effects on fetal development and chronic health. Clin Sci (Lond) 2021;135:2307-2327.
Stepan H, Galindo A, Hund M, et al. Clinical utility of sFlt-1 and PlGF in screening, prediction, diagnosis and monitoring of pre-eclampsia and fetal growth restriction. Ultrasound Obstet Gynecol 2023;61:168-180.
Guo Z, Yang F, Zhang J, et al. Whole-Genome Promoter Profiling of Plasma DNA Exhibits Diagnostic Value for Placenta-Origin Pregnancy Complications. Adv Sci (Weinh) 2020;7:1901819.
Bahado-Singh R, Vishweswaraiah S, Mishra NK, Guda C, Radhakrishna U. Placental DNA methylation changes in detection of tetralogy of Fallot. Ultrasound Obstet Gynecol 2020;55:768-775.
Liu J, Wu Y, Sun H, et al. Association between placental DNA methylation and fetal congenital heart disease. Mol Genet Genomics 2023;298:243-251.
Liu J, Wu Y, Sun H, et al. Placental DNA Methylation Abnormalities in Prenatal Conotruncal Heart Defects. Front Genet 2022;13:878063.
Zhu Y, Gomez JA, Laufer BI, Mordaunt CE, Mouat JS, Soto DC. et al. Placental methylome reveals a 22q13.33 brain regulatory gene locus associated with autism. Genome Biol 2022;23:46.
Bahado-Singh RO, Vishweswaraiah S, Aydas B, Radhakrishna U. Placental DNA methylation changes and the early prediction of autism in full-term newborns. PLoS One 2021;16:e0253340.
Appleton AA, Lester BM, Armstrong DA, Lesseur C, Marsit CJ. Examining the joint contribution of placental NR3C1 and HSD11B2 methylation for infant neurobehavior. Psychoneuroendocrinology 2015;52:32-42.
Ursini G, Di Carlo P, Mukherjee S, et al. Prioritization of potential causative genes for schizophrenia in placenta. Nat Commun 2023;14:2613.
Tehrani JM, Kennedy E, Tung PW, et al. Human placental microRNAs dysregulated by cadmium exposure predict neurobehavioral outcomes at birth. Pediatr Res 2023;93:1410-1418.
Howerton CL, Morgan CP, Fischer DB, Bale TL. O-GlcNAc transferase (OGT) as a placental biomarker of maternal stress and reprogramming of CNS gene transcription in development. Proc Natl Acad Sci U S A 2013;110:5169-5174.
Nugent BM, O'Donnell CM, Epperson CN, Bale TL. Placental H3K27me3 establishes female resilience to prenatal insults. Nat Commun 2018;9:2555.
Chhabra D, Sharma S, Kho AT, et al. Fetal lung and placental methylation is associated with in utero nicotine exposure. Epigenetics 2014;9:1473-1484.
Shorey-Kendrick LE, McEvoy CT, O'Sullivan SM, et al. Impact of vitamin C supplementation on placental DNA methylation changes related to maternal smoking:association with gene expression and respiratory outcomes. Clin Epigenetics 2021;13:177.
Arendt LH, Ramlau-Hansen CH, Wilcox AJ, Henriksen TB, Olsen J, Lindhard MS. Placental Weight and Male Genital Anomalies:A Nationwide Danish Cohort Study. Am J Epidemiol 2016;183:1122-1128.
Arrebola JP, Molina-Molina JM, Fernandez MF, et al. A novel biomarker for anti-androgenic activity in placenta reveals risks of urogenital malformations. Reproduction 2015;149:605-613.
Fernandez MF, Olmos B, Granada A, et al. Human exposure to endocrine-disrupting chemicals and prenatal risk factors for cryptorchidism and hypospadias:a nested case-control study. Environ Health Perspect 2007;115:8-14.
Green BB, Kappil M, Lambertini L, et al. Expression of imprinted genes in placenta is associated with infant neurobehavioral development. Epigenetics 2015;10:834-841.
Lesseur C, Armstrong DA, Murphy MA, et al. Sex-specific associations between placental leptin promoter DNA methylation and infant neurobehavior. Psychoneuroendocrinology 2014;40:1-9.
Redline RW, Minich N, Taylor HG, Hack M. Placental lesions as predictors of cerebral palsy and abnormal neurocognitive function at school age in extremely low birth weight infants (<1 kg). Pediatr Dev Pathol 2007;10:282-292.
Maccani MA, Padbury JF, Lester BM, Knopik VS, Marsit CJ. Placental miRNA expression profiles are associated with measures of infant neurobehavioral outcomes. Pediatr Res 2013;74:272-278.
Goodfellow LR, Cooper C, Harvey NC. Regulation of placental calcium transport and offspring bone health. Front Endocrinol (Lausanne) 2011;2:3.
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