Maternal plasma syndecan-1: a biomarker for fetal growth restriction

References

• Lees CC, Romero R, Stampalija T, et al. Clinical opinion: the diagnosis and management of suspected fetal growth restriction: an evidence-based approach. Am J Obstet Gynecol. 2022;226(3):366–378.
   PubMed Web of Science ®Google Scholar
• Baschat AA, Galan HL, Lee W, et al. The role of the fetal biophysical profile in the management of fetal growth restriction. Am J Obstet Gynecol. 2022;226(4):475–486.
   PubMed Web of Science ®Google Scholar
• Deter RL, Lee W, Yeo L, et al. Individualized growth assessment: conceptual framework and practical implementation for the evaluation of fetal growth and neonatal growth outcome. Am J Obstet Gynecol. 2018;218(2s):S656–s678.
   PubMed Web of Science ®Google Scholar
• Pacora P, Romero R, Jung E, et al. Reduced fetal growth velocity precedes antepartum fetal death. Ultrasound Obstet Gynecol. 2021;57(6):942–952.
   PubMed Web of Science ®Google Scholar
• Lees C, Marlow N, Arabin B, et al. Perinatal morbidity and mortality in early-onset fetal growth restriction: cohort outcomes of the trial of randomized umbilical and fetal flow in Europe (TRUFFLE). Ultrasound Obstet Gynecol. 2013;42(4):400–408.
   PubMed Web of Science ®Google Scholar
• Gardosi J, Francis A. Adverse pregnancy outcome and association with small for gestational age birthweight by customized and population-based percentiles. Am J Obstet Gynecol. 2009;201(1):28.e1-8–28.e8.
   PubMed Web of Science ®Google Scholar
• Walker D-M, Marlow N, Upstone L, et al. The growth restriction intervention trial: long-term outcomes in a randomized trial of timing of delivery in fetal growth restriction. Am J Obstet Gynecol. 2011;204(1):34.e1-9–34.e9.
   PubMed Web of Science ®Google Scholar
• Barker DJP, Osmond C, Forsén TJ, et al. Trajectories of growth among children who have coronary events as adults. N Engl J Med. 2005;353(17):1802–1809.
   PubMed Web of Science ®Google Scholar
• Kajantie E, Osmond C, Barker DJP, et al. Size at birth as a predictor of mortality in adulthood: a follow-up of 350 000 person-years. Int J Epidemiol. 2005;34(3):655–663.
   PubMed Web of Science ®Google Scholar
• Skilton MR, Evans N, Griffiths KA, et al. Aortic wall thickness in newborns with intrauterine growth restriction. Lancet. 2005;365(9469):1484–1486.
   PubMed Web of Science ®Google Scholar
• Crispi F, Miranda J, Gratacós E. Long-term cardiovascular consequences of fetal growth restriction: biology, clinical implications, and opportunities for prevention of adult disease. Am J Obstet Gynecol. 2018;218(2s):S869–s879.
   PubMed Web of Science ®Google Scholar
• Gluckman PD, Hanson MA, Cooper C, et al. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359(1):61–73.
   PubMed Web of Science ®Google Scholar
• Deter RL, Lee W, Kingdom J, et al. Second trimester growth velocities: assessment of fetal growth potential in SGA singletons. J Matern Fetal Neonatal Med. 2019;32(6):939–946.
   PubMed Web of Science ®Google Scholar
• Platz E, Newman R. Diagnosis of IUGR: traditional biometry. Semin Perinatol. 2008;32(3):140–147.
   PubMed Web of Science ®Google Scholar
• Grantz KL, Kim S, Grobman WA, et al. Fetal growth velocity: the NICHD fetal growth studies. Am J Obstet Gynecol. 2018;219(3):285.e1-285–e36.
   Web of Science ®Google Scholar
• Chatzakis C, Papaioannou G-K, Eleftheriades M, et al. Perinatal outcome of appropriate-weight fetuses with decelerating growth. J Matern Fetal Neonatal Med. 2021;34(20):3362–3369.
   PubMed Web of Science ®Google Scholar
• McCowan LM, Figueras F, Anderson NH. Evidence-based national guidelines for the management of suspected fetal growth restriction: comparison, consensus, and controversy. Am J Obstet Gynecol. 2018;218(2s):S855–s868.
   PubMedGoogle Scholar
• Hiersch L, Melamed N. Fetal growth velocity and body proportion in the assessment of growth. Am J Obstet Gynecol. 2018;218(2s):S700–S711.e1.
   PubMedGoogle Scholar
• Unterscheider J, Daly S, Geary MP, et al. Optimizing the definition of intrauterine growth restriction: the multicenter prospective Porto study. Am J Obstet Gynecol. 2013;208(4):290.e1-6–290.e6.
   PubMed Web of Science ®Google Scholar
• Figueras F, Gratacós E. Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther. 2014;36(2):86–98.
   PubMed Web of Science ®Google Scholar
• Ananth CV, Vintzileos AM. Distinguishing pathological from constitutional small for gestational age births in population-based studies. Early Hum Dev. 2009;85(10):653–658.
   PubMed Web of Science ®Google Scholar
• Gordijn SJ, Beune IM, Thilaganathan B, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48(3):333–339.
   PubMed Web of Science ®Google Scholar
• Lees CC, Stampalija T, Baschat A, et al. ISUOG practice guidelines: diagnosis and management of small-for-gestational-age fetus and fetal growth restriction. Ultrasound Obstet Gynecol. 2020;56(2):298–312.
   PubMed Web of Science ®Google Scholar
• Fleischer A, Schulman H, Farmakides G, et al. Umbilical artery velocity waveforms and intrauterine growth retardation. Am J Obstet Gynecol. 1985;151(4):502–505.
   PubMed Web of Science ®Google Scholar
• Brosens I, Pijnenborg R, Vercruysse L, et al. The “great obstetrical syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol. 2011;204(3):193–201.
   PubMed Web of Science ®Google Scholar
• Trudinger BJ, Giles WB, Cook CM. Flow velocity waveforms in the maternal uteroplacental and fetal umbilical placental circulations. Am J Obstet Gynecol. 1985;152(2):155–163.
   PubMed Web of Science ®Google Scholar
• Alfirevic Z, Stampalija T, Gyte GM. Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database Syst Rev. 2013;2013(11):CD007529.
   PubMedGoogle Scholar
• Baschat AA, Cosmi E, Bilardo CM, et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol. 2007;109(2 Pt 1):253–261.
   PubMed Web of Science ®Google Scholar
• Ferrazzi E, Bozzo M, Rigano S, et al. Temporal sequence of abnormal Doppler changes in the peripheral and central circulatory systems of the severely growth-restricted fetus. Ultrasound Obstet Gynecol. 2002;19(2):140–146.
   PubMed Web of Science ®Google Scholar
• Tarbell JM, Cancel LM. The glycocalyx and its significance in human medicine. J Intern Med. 2016;280(1):97–113.
   PubMed Web of Science ®Google Scholar
• Reitsma S, Slaaf DW, Vink H, et al. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch. 2007;454(3):345–359.
   PubMed Web of Science ®Google Scholar
• Pillinger NL, Kam P. Endothelial glycocalyx: basic science and clinical implications. Anaesth Intensive Care. 2017;45(3):295–307.
   PubMed Web of Science ®Google Scholar
• Mertens G, Cassiman JJ, Van den Berghe H, et al. Cell surface heparan sulfate proteoglycans from human vascular endothelial cells. Core protein characterization and antithrombin III binding properties. J Biol Chem. 1992;267(28):20435–20443.
   PubMed Web of Science ®Google Scholar
• Bernfield M, Götte M, Park PW, et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 1999;68:729–777.
   PubMed Web of Science ®Google Scholar
• Villalba N, Baby S, Yuan SY. The endothelial glycocalyx as a Double-Edged sword in microvascular homeostasis and pathogenesis. Front Cell Dev Biol. 2021;9:711003.
   PubMed Web of Science ®Google Scholar
• Bode L, Murch S, Freeze HH. Heparan sulfate plays a central role in a dynamic in vitro model of protein-losing enteropathy. J Biol Chem. 2006;281(12):7809–7815.
   PubMed Web of Science ®Google Scholar
• Bode L, Eklund EA, Murch S, et al. Heparan sulfate depletion amplifies TNF-alpha-induced protein leakage in an in vitro model of protein-losing enteropathy. Am J Physiol Gastrointest Liver Physiol. 2005;288(5):G1015–23.
   PubMed Web of Science ®Google Scholar
• Szabo S, Xu Y, Romero R, et al. Changes of placental syndecan-1 expression in preeclampsia and HELLP syndrome. Virchows Arch. 2013;463(3):445–458.
   PubMed Web of Science ®Google Scholar
• Crescimanno C, Marzioni D, Paradinas FJ, et al. Expression pattern alterations of syndecans and glypican-1 in normal and pathological trophoblast. J Pathol. 1999;189(4):600–608.
   PubMed Web of Science ®Google Scholar
• Lorenzi T, Turi A, Crescimanno C, et al. Syndecan expressions in the human amnion and chorionic plate. Eur J Histochem. 2010;54(4):e42.
   PubMed Web of Science ®Google Scholar
• Jokimaa V, Inki P, Kujari H, et al. Expression of syndecan-1 in human placenta and decidua. Placenta. 1998;19(2-3):157–163.
   PubMed Web of Science ®Google Scholar
• Moore KH, Murphy HA, Chapman H, et al. Syncytialization alters the extracellular matrix and barrier function of placental trophoblasts. Am J Physiol Cell Physiol. 2021;321(4):C694–C703.
   PubMed Web of Science ®Google Scholar
• Couchman JR. Syndecans: proteoglycan regulators of cell-surface microdomains? Nat Rev Mol Cell Biol. 2003;4(12):926–937.
   PubMed Web of Science ®Google Scholar
• Yoneda A, Couchman JR. Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans. Matrix Biol. 2003;22(1):25–33.
   PubMed Web of Science ®Google Scholar
• Hahn RG, Patel V, Dull RO. Human glycocalyx shedding: systematic review and critical appraisal. Acta Anaesthesiol Scand. 2021;65(5):590–606.
   PubMed Web of Science ®Google Scholar
• Dogné S, Flamion B, Caron N. Endothelial glycocalyx as a shield against diabetic vascular complications: involvement of hyaluronan and hyaluronidases. Arterioscler Thromb Vasc Biol. 2018;38(7):1427–1439.
   PubMed Web of Science ®Google Scholar
• Yanagishita M, Hascall VC. Cell surface heparan sulfate proteoglycans. J Biol Chem. 1992;267(14):9451–9454.
   PubMed Web of Science ®Google Scholar
• Kim CW, Goldberger OA, Gallo RL, et al. Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. Mol Biol Cell. 1994;5(7):797–805.
   PubMed Web of Science ®Google Scholar
• Rehm M, Bruegger D, Christ F, et al. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation. 2007;116(17):1896–1906.
   PubMed Web of Science ®Google Scholar
• Ushiyama A, Kataoka H, Iijima T. Glycocalyx and its involvement in clinical pathophysiologies. J Intensive Care. 2016;4(1):59.
   PubMedGoogle Scholar
• Johansson PI, Stensballe J, Rasmussen LS, et al. A high admission syndecan-1 level, a marker of endothelial glycocalyx degradation, is associated with inflammation, protein C depletion, fibrinolysis, and increased mortality in trauma patients. Ann Surg. 2011;254(2):194–200.
   PubMed Web of Science ®Google Scholar
• Gonzalez Rodriguez E, Ostrowski SR, Cardenas JC, et al. Syndecan-1: a quantitative marker for the endotheliopathy of trauma. J Am Coll Surg. 2017;225(3):419–427.
   PubMed Web of Science ®Google Scholar
• Nelson A, Berkestedt I, Schmidtchen A, et al. Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma. Shock. 2008;30(6):623–627.
   PubMed Web of Science ®Google Scholar
• Suzuki K, Okada H, Sumi K, et al. Serum syndecan-1 reflects organ dysfunction in critically ill patients. Sci Rep. 2021;11(1):8864.
   PubMed Web of Science ®Google Scholar
• Puskarich MA, Cornelius DC, Tharp J, et al. Plasma syndecan-1 levels identify a cohort of patients with severe sepsis at high risk for intubation after large-volume intravenous fluid resuscitation. J Crit Care. 2016;36:125–129.
   PubMed Web of Science ®Google Scholar
• Piotti A, Novelli D, Meessen JMTA, et al. Endothelial damage in septic shock patients as evidenced by circulating syndecan-1, sphingosine-1-phosphate and soluble VE-cadherin: a substudy of ALBIOS. Crit Care. 2021;25(1):113.
   PubMed Web of Science ®Google Scholar
• Padberg J-S, Wiesinger A, di Marco GS, et al. Damage of the endothelial glycocalyx in chronic kidney disease. Atherosclerosis. 2014;234(2):335–343.
   PubMed Web of Science ®Google Scholar
• Chen X, Geng X, Jin S, et al. The association of syndecan-1, hypercoagulable state and thrombosis and in patients with nephrotic syndrome. Clin Appl Thromb Hemost. 2021;27:10760296211010256.
   Web of Science ®Google Scholar
• Kitagawa Y, Kawamura I, Suzuki K, et al. Serum syndecan-1 concentration in hospitalized patients with heart failure may predict readmission-free survival. PLoS One. 2021;16(12):e0260350.
   PubMed Web of Science ®Google Scholar
• Miranda CH, de Carvalho Borges M, Schmidt A, et al. Evaluation of the endothelial glycocalyx damage in patients with acute coronary syndrome. Atherosclerosis. 2016;247:184–188.
   PubMed Web of Science ®Google Scholar
• Bell JD, Rhind SG, Di Battista AP, et al. Biomarkers of glycocalyx injury are associated with delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage: a case series supporting a new hypothesis. Neurocrit Care. 2017;26(3):339–347.
   PubMed Web of Science ®Google Scholar
• Oravecz O, Balogh A, Romero R, et al. Proteoglycans: systems-Level insight into their expression in healthy and diseased placentas. IJMS. 2022;23(10):5798.
   Google Scholar
• Heyer-Chauhan N, Ovbude IJ, Hills AA, et al. Placental syndecan-1 and sulphated glycosaminoglycans are decreased in preeclampsia. J Perinat Med. 2014;42(3):329–338.
   PubMed Web of Science ®Google Scholar
• Inki P, Jalkanen M. Regulation of cell morphology and growth by syndecan-1: altered expression in malignancy. Cytoskeleton. 1996;3:305–324.
   Google Scholar
• Baston-Buest DM, Altergot-Ahmad O, Pour SJ, et al. Syndecan-1 acts as an important regulator of CXCL1 expression and cellular interaction of human endometrial stromal and trophoblast cells. Mediators Inflamm. 2017. 2017;2017:8379256.
   PubMed Web of Science ®Google Scholar
• Hofmann-Kiefer KF, Knabl J, Martinoff N, et al. Increased serum concentrations of circulating glycocalyx components in HELLP syndrome compared to healthy pregnancy: an observational study. Reprod Sci. 2013;20(3):318–325.
   PubMed Web of Science ®Google Scholar
• Greeley ET, Rochelson B, Krantz DA, et al. Evaluation of syndecan-1 as a novel biomarker for adverse pregnancy outcomes. Reprod Sci. 2020;27(1):355–363.
   PubMed Web of Science ®Google Scholar
• Garcha D, Walker SP, MacDonald TM, et al. Circulating syndecan-1 is reduced in pregnancies with poor fetal growth and its secretion regulated by matrix metalloproteinases and the mitochondria. Sci Rep. 2021;11(1):16595.
   PubMed Web of Science ®Google Scholar
• 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(1):2411.
   PubMed Web of Science ®Google Scholar
• Hadlock FP, Harrist RB, Sharman RS, et al. Estimation of fetal weight with the use of head, body, and femur measurements–a prospective study. Am J Obstet Gynecol. 1985;151(3):333–337.
   PubMed Web of Science ®Google Scholar
• Alexander GR, Himes JH, Kaufman RB, et al. A United States national reference for fetal growth. Obstet Gynecol. 1996;87(2):163–168.
   PubMed Web of Science ®Google Scholar
• ACOG Committee on Obstetric Practice. ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Obstet Gynecol. 2002;99(1):159–167.
   PubMed Web of Science ®Google Scholar
• Arduini D, Rizzo G. Normal values of pulsatility index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. J Perinat Med. 1990;18(3):165–172.
   PubMed Web of Science ®Google Scholar
• Trudinger BJ, Cook CM, Giles WB, et al. Fetal umbilical artery velocity waveforms and subsequent neonatal outcome. Br J Obstet Gynaecol. 1991;98(4):378–384.
   PubMedGoogle Scholar
• Kurmanavicius J, Florio I, Wisser J, et al. Reference resistance indices of the umbilical, fetal middle cerebral and uterine arteries at 24-42 weeks of gestation. Ultrasound Obstet Gynecol. 1997;10(2):112–120.
   PubMed Web of Science ®Google Scholar
• Baston-Büst DM, Götte M, Janni W, et al. Syndecan-1 knock-down in decidualized human endometrial stromal cells leads to significant changes in cytokine and angiogenic factor expression patterns. Reprod Biol Endocrinol. 2010;8:133.
   PubMed Web of Science ®Google Scholar
• Ferretti C, Bruni L, Dangles-Marie V, et al. Molecular circuits shared by placental and cancer cells, and their implications in the proliferative, invasive and migratory capacities of trophoblasts. Hum Reprod Update. 2007;13(2):121–141.
   PubMed Web of Science ®Google Scholar
• Larrain J, et al. Syndecan-1 expression is down-regulated during myoblast terminal differentiation. Modulation by growth factors and retinoic acid. J Biol Chem. 1997;272(29):18418–18424.
   PubMed Web of Science ®Google Scholar
• Bonneh-Barkay D, Shlissel M, Berman B, et al. Identification of glypican as a dual modulator of the biological activity of fibroblast growth factors. J Biol Chem. 1997;272(19):12415–12421.
   PubMed Web of Science ®Google Scholar
• Bernfield M, Sanderson RD. Syndecan, a developmentally regulated cell surface proteoglycan that binds extracellular matrix and growth factors. Philos Trans R Soc Lond B Biol Sci. 1990;327(1239):171–186.
   PubMed Web of Science ®Google Scholar
• Gandley RE, Althouse A, Jeyabalan A, et al. Low soluble syndecan-1 precedes preeclampsia. PLoS One. 2016;11(6):e0157608.
   PubMed Web of Science ®Google Scholar
• Jokimaa VI, Kujari HP, Ekholm EM, et al. Placental expression of syndecan 1 is diminished in preeclampsia. Am J Obstet Gynecol. 2000;183(6):1495–1498.
   PubMed Web of Science ®Google Scholar
• Chui A, Murthi P, Brennecke SP, et al. The expression of placental proteoglycans in pre-eclampsia. Gynecol Obstet Invest. 2012;73(4):277–284.
   PubMed Web of Science ®Google Scholar
• Ogawa M, Yanoma S, Nagashima Y, et al. Paradoxical discrepancy between the serum level and the placental intensity of PP5/TFPI-2 in preeclampsia and/or intrauterine growth restriction: possible interaction and correlation with glypican-3 hold the key. Placenta. 2007;28(2-3):224–232.
   PubMed Web of Science ®Google Scholar
• Chui A, Zainuddin N, Rajaraman G, et al. Placental syndecan expression is altered in human idiopathic fetal growth restriction. Am J Pathol. 2012;180(2):693–702.
   PubMed Web of Science ®Google Scholar
• Than NG, Vaisbuch E, Kim CJ, et al. Early-onset preeclampsia and HELLP syndrome: an overview. In Preedy VR, editors. Handbook of growth and growth monitoring in health and disease. Cham: Springer, 2012. p. 1867–1891.
   Google Scholar
• Ness RB, Roberts JM. Heterogeneous causes constituting the single syndrome of preeclampsia: a hypothesis and its implications. Am J Obstet Gynecol. 1996;175(5):1365–1370.
   PubMed Web of Science ®Google Scholar
• von Dadelszen P, Magee LA, Roberts JM. Subclassification of preeclampsia. Hypertens Pregnancy. 2003;22(2):143–148.
   PubMed Web of Science ®Google Scholar
• Kornacki J, Wirstlein P, Wender-Ozegowska E. Serum levels of soluble FMS-like tyrosine kinase 1 and endothelial glycocalyx components in early- and late-onset preeclampsia. J Matern Fetal Neonatal Med. 2022;35(25):7466–7470.
   PubMed Web of Science ®Google Scholar
• Alici Davutoğlu E, Akkaya Firat A, Ozel A, et al. Evaluation of maternal serum hypoxia inducible factor-1α, progranulin and syndecan-1 levels in pregnancies with early- and late-onset preeclampsia. J Matern Fetal Neonatal Med. 2018;31(15):1976–1982.
   PubMed Web of Science ®Google Scholar
• Kuessel L, Husslein H, Montanari E, et al. Dynamics of soluble syndecan-1 in maternal serum during and after pregnancies complicated by preeclampsia: a nested case control study. Clin Chem Lab Med. 2019;58(1):50–58.
   PubMed Web of Science ®Google Scholar
• Riquelme G, Vallejos C, de Gregorio N, et al. Lipid rafts and cytoskeletal proteins in placental microvilli membranes from preeclamptic and IUGR pregnancies. J Membr Biol. 2011;241(3):127–140.
   PubMed Web of Science ®Google Scholar
• Schmedt A, Götte M, Heinig J, et al. Evaluation of placental syndecan-1 expression in early pregnancy as a predictive fetal factor for pregnancy outcome. Prenat Diagn. 2012;32(2):131–137.
   PubMed Web of Science ®Google Scholar
• Thompson RS, Trudinger BJ. Doppler waveform pulsatility index and resistance, pressure and flow in the umbilical placental circulation: an investigation using a mathematical model. Ultrasound Med Biol. 1990;16(5):449–458.
   PubMed Web of Science ®Google Scholar
• Giles WB, Trudinger BJ, Baird PJ. Fetal umbilical artery flow velocity waveforms and placental resistance: pathological correlation. Br J Obstet Gynaecol. 1985;92(1):31–38.
   PubMedGoogle Scholar
• Spinillo A, Gardella B, Bariselli S, et al. Placental histopathological correlates of umbilical artery Doppler velocimetry in pregnancies complicated by fetal growth restriction. Prenat Diagn. 2012;32(13):1263–1272.
   PubMed Web of Science ®Google Scholar
• Parra-Saavedra M, Crovetto F, Triunfo S, et al. Placental findings in late-onset SGA births without Doppler signs of placental insufficiency. Placenta. 2013;34(12):1136–1141.
   PubMed Web of Science ®Google Scholar
• Baschat AA, Gembruch U, Harman CR. The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens. Ultrasound Obstet Gynecol. 2001;18(6):571–577.
   PubMed Web of Science ®Google Scholar
• Karsdorp VH, van Vugt JM, van Geijn HP, et al. Clinical significance of absent or reversed end diastolic velocity waveforms in umbilical artery. Lancet. 1994;344(8938):1664–1668.
   PubMed Web of Science ®Google Scholar
• Bilardo CM, Nicolaides KH, Campbell S. Doppler measurements of fetal and uteroplacental circulations: relationship with umbilical venous blood gases measured at cordocentesis. Am J Obstet Gynecol. 1990;162(1):115–120.
   PubMed Web of Science ®Google Scholar
• Yoon BH, Romero R, Roh CR, et al. Relationship between the fetal biophysical profile score, umbilical artery Doppler velocimetry, and fetal blood acid-base status determined by cordocentesis. Am J Obstet Gynecol. 1993;169(6):1586–1594.
   PubMed Web of Science ®Google Scholar
• Nicolaides KH, Bilardo CM, Soothill PW, et al. Absence of end diastolic frequencies in umbilical artery: a sign of fetal hypoxia and acidosis. BMJ. 1988;297(6655):1026–1027.
   PubMed Web of Science ®Google Scholar
• Hecher K, Campbell S, Doyle P, et al. Assessment of fetal compromise by Doppler ultrasound investigation of the fetal circulation. Arterial, intracardiac, and venous blood flow velocity studies. Circulation. 1995;91(1):129–138.
   PubMed Web of Science ®Google Scholar
• Labarrere CA, Althabe OH. Inadequate maternal vascular response to placentation in pregnancies complicated by preeclampsia and by small-for-gestational-age infants. Br J Obstet Gynaecol. 1987;94(11):1113–1116.
   PubMedGoogle Scholar
• Mifsud W, Sebire NJ. Placental pathology in early-onset and late-onset fetal growth restriction. Fetal Diagn Ther. 2014;36(2):117–128.
   PubMed Web of Science ®Google Scholar
• Burton GJ, Jauniaux E. Pathophysiology of placental-derived fetal growth restriction. Am J Obstet Gynecol. 2018;218(2s):S745–s761.
   PubMedGoogle Scholar
• Macara L, Kingdom JC, Kaufmann P, et al. Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms. Placenta. 1996;17(1):37–48.
   PubMed Web of Science ®Google Scholar
• Jackson MR, Walsh AJ, Morrow RJ, et al. Reduced placental villous tree elaboration in small-for-gestational-age pregnancies: relationship with umbilical artery Doppler waveforms. Am J Obstet Gynecol. 1995;172(2 Pt 1):518–525.
   PubMed Web of Science ®Google Scholar
• Hitschold T, Weiss E, Beck T, et al. Low target birth weight or growth retardation? Umbilical Doppler flow velocity waveforms and histometric analysis of fetoplacental vascular tree. Am J Obstet Gynecol. 1993;168(4):1260–1264.
   PubMed Web of Science ®Google Scholar
• Jauniaux E, Jurkovic D, Campbell S, et al. Investigation of placental circulations by color Doppler ultrasonography. Am J Obstet Gynecol. 1991;164(2):486–488.
   PubMed Web of Science ®Google Scholar
• Olofsson P, Laurini RN, Marsál K. A high uterine artery pulsatility index reflects a defective development of placental bed spiral arteries in pregnancies complicated by hypertension and fetal growth retardation. Eur J Obstet Gynecol Reprod Biol. 1993;49(3):161–168.
   PubMed Web of Science ®Google Scholar
• Brosens I, Puttemans P, Benagiano G. Placental bed research: I. The placental bed: from spiral arteries remodeling to the great obstetrical syndromes. Am J Obstet Gynecol. 2019;221(5):437–456.
   PubMed Web of Science ®Google Scholar
• Ferrazzi E, Bulfamante G, Mezzopane R, et al. Uterine Doppler velocimetry and placental hypoxic-ischemic lesion in pregnancies with fetal intrauterine growth restriction. Placenta. 1999;20(5-6):389–394.
   PubMed Web of Science ®Google Scholar
• Lin S, Shimizu I, Suehara N, et al. Uterine artery Doppler velocimetry in relation to trophoblast migration into the myometrium of the placental bed. Obstet Gynecol. 1995;85(5 Pt 1):760–765.
   PubMed Web of Science ®Google Scholar
• Romero R, Kingdom J, Deter R, et al. Fetal growth: evaluation and management. Am J Obstet Gynecol. 2018;218(2s):S608.
   PubMedGoogle Scholar
• Lees CC, Marlow N, van Wassenaer-Leemhuis A, et al. 2 Year neurodevelopmental and intermediate perinatal outcomes in infants with very preterm fetal growth restriction (TRUFFLE): a randomised trial. Lancet. 2015;385(9983):2162–2172.
   PubMed Web of Science ®Google Scholar
• Hecher K, Bilardo CM, Stigter RH, et al. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol. 2001;18(6):564–570.
   PubMed Web of Science ®Google Scholar
• Romero R, Tarca AL. Fetal size standards to diagnose a small- or a large-for-gestational-age fetus. Am J Obstet Gynecol. 2018;218(2s):S605–s607.
   PubMed Web of Science ®Google Scholar
• Gardosi J, Francis A, Turner S, et al. Customized growth charts: rationale, validation and clinical benefits. Am J Obstet Gynecol. 2018;218(2s):S609–s618.
   PubMed Web of Science ®Google Scholar
• Figueras F, Caradeux J, Crispi F, et al. Diagnosis and surveillance of late-onset fetal growth restriction. Am J Obstet Gynecol. 2018;218(2s):S790–S802.e1.
   PubMedGoogle Scholar
• Ciobanu A, Rouvali A, Syngelaki A, et al. Prediction of small for gestational age neonates: screening by maternal factors, fetal biometry, and biomarkers at 35-37 weeks’ gestation. Am J Obstet Gynecol. 2019;220(5):486.e1–486.e11.
   PubMed Web of Science ®Google Scholar
• Parra-Saavedra M, Simeone S, Triunfo S, et al. Correlation between histological signs of placental underperfusion and perinatal morbidity in late-onset small-for-gestational-age fetuses. Ultrasound Obstet Gynecol. 2015;45(2):149–155.
   PubMed Web of Science ®Google Scholar
• Lesmes C, Gallo DM, Gonzalez R, et al. Prediction of small-for-gestational-age neonates: screening by maternal serum biochemical markers at 19-24 weeks. Ultrasound Obstet Gynecol. 2015;46(3):341–349.
   PubMed Web of Science ®Google Scholar
• Poon LC, Lesmes C, Gallo DM, et al. Prediction of small-for-gestational-age neonates: screening by biophysical and biochemical markers at 19-24 weeks. Ultrasound Obstet Gynecol. 2015;46(4):437–445.
   PubMedGoogle Scholar
• Bakalis S, Peeva G, Gonzalez R, et al. Prediction of small-for-gestational-age neonates: screening by biophysical and biochemical markers at 30-34 weeks. Ultrasound Obstet Gynecol. 2015;46(4):446–451.
   PubMed Web of Science ®Google Scholar
• Gaccioli F, Aye ILMH, Sovio U, et al. Screening for fetal growth restriction using fetal biometry combined with maternal biomarkers. Am J Obstet Gynecol. 2018;218(2s):S725–s737.
   PubMedGoogle Scholar