Placenta and Fetal Growth Restriction

SALAFIA, CAROLYN M.; CHARLES, ADRIAN K.; MAAS, ELIZABETH M.

doi:10.1097/00003081-200606000-00007

Cited by 235Pregnancy and preeclampsia studiesBirth, Development, and HealthReproductive System and Pregnancy

Placenta and Fetal Growth Restriction

SALAFIA, CAROLYN M., CHARLES, ADRIAN K., MAAS, ELIZABETH M.·2006·Clinical Obstetrics and Gynecology

DOI 10.1097/00003081-200606000-00007

Open this paper in CoChat — free account

Abstract

The placenta, as the vector for all maternal-fetal oxygen and nutrient exchange, is a principal influence on birthweight. Placental weight summarizes laterally expanding growth of the chorionic disc, and villous arborization yielding the nutrient exchange surface. These different growth dimensions alter fetoplacental weight ratio and ponderal index, and thus may modify placental functional efficiency. The placenta may show a range of histopathologies, some of which are also associated with fetal growth restriction. Different fetal intrinsic abilities to compensate for gross and histo-pathology may clarify the imperfect relationships between fetal growth and both intrauterine pathology, and the long-term health risks associated with poor fetal growth.

Integrity signals

Registry

Crossref · 10.1097/00003081-200606000-00007

Cites

103 of 103 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Hypertensive pregnancy disorders, compromised fetal growth, and fetal death often stem from placental dysfunction-either due to insufficient initial placentation or diminishing placental function with increasing gestational age.
“In particular, hypertensive pregnancy disorders, compromised fetal growth, and fetal death often stem from placental dysfunction—either due to insufficient initial placentation or diminishing placental function with increasing gestational age14,15.”
From Multi-centre deep learning for placenta segmentation in obstetric ultrasound with multi-observer and cross-country generalization (2023) · cites this paper as [15]
Placental volume as early as 11 to 13 weeks' gestation correlates with birth weight at term.
“The placental volume as early as 11 to 13 weeks’ gestation has long been known to correlate with birth weight at term [39].”
From Deep Learning Strategies for Ultrasound in Pregnancy (2020) · cites this paper as [39]
Placental insufficiency is associated with adverse pregnancy outcomes like fetal growth restriction (FGR), caused by insufficient transport of nutrients and oxygen through the placenta.
“Placental insufficiency is associated with adverse pregnancy outcomes like fetal growth restriction (FGR), caused by insufficient transport of nutrients and oxygen through the placenta [38].”
From Deep Learning Strategies for Ultrasound in Pregnancy (2020) · cites this paper as [38]
Birth weight is dependent on gestational age at delivery, maternal characteristics, and placental volume, vasculature and function.
“Birth weight is dependent upon numerous factors including gestational age at the time of delivery [1]; maternal characteristics [1–3]; and placental volume, vasculature and function [4].”
From Volume and vascularity: Using ultrasound to unlock the secrets of the first trimester placenta (2019) · cites this paper as [4]

Molecular basis of the effects of shear stress on vascular endothelial cells
Li, Y.-S. J., Haga, J. H., & Chien, S. (2005) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2004.09.030 · Cited by 904 · see citing works
Fetal umbilical artery flow velocity waveforms and placental resistance: pathological correlation
Giles, W. B., Trudinger, B., & Baird, P. J. (1985) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1985.tb01045.x · Cited by 730 · see citing works
Fetal growth retardation and the arteries of the placental bed
Brosens, I., Dixon, H. G., & Robertson, W. B. (1977) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1977.tb12676.x · Cited by 430 · see citing works
MORPHOLOGICAL CHANGES OF THE SPIRAL ARTERIES IN THE PLACENTAE BED IN RELATION TO PRE‐ECLAMPSIA AND FETAL GROWTH RETARDATION
Gerretsen, G., Huisjes, H. J., & Elema, J. D. (1981) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1981.tb02222.x · Cited by 370 · see citing works
Maternal placental vasculopathy and infection: Two distinct subgroups among patients with preterm labor and preterm ruptured membranes
Arias, F., Rodriquez, L., Rayne, S. C., & Kraus, F. T. (1993) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(93)90499-9 · Cited by 365 · see citing works
Human Cytomegalovirus Infection of Placental Cytotrophoblasts In Vitro and In Utero: Implications for Transmission and Pathogenesis
Fisher, S. J., Genbačev, O., Maidji, E., & Pereira, L. (2000) · Journal of Virology · doi:10.1128/jvi.74.15.6808-6820.2000 · Cited by 353 · see citing works
Inhibition of Insulin Sensitivity by Free Fatty Acids Requires Activation of Multiple Serine Kinases in 3T3-L1 Adipocytes
Gao, Z., Zhang, X., Zuberi, A. R., Hwang, D. H., Quon, M. J., Lefevre, M., & Ye, J. (2004) · Molecular Endocrinology · doi:10.1210/me.2003-0383 · Cited by 335 · see citing works
Intrauterine growth restriction in infants of less than thirty-two weeks' gestation: Associated placental pathologic features
Salafia, C. M., MINIOR, V. K., Pezzullo, J. C., Popek, E. J., Rosenkrantz, T. S., & Vintzileos, A. M. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)91325-4 · Cited by 308 · see citing works
Self-citation
Uteroplacental vascular pathology
Robertson, W. B., Brosens, I. A., & Dixon, G. (1975) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/0028-2243(75)90130-6 · Cited by 290 · see citing works
AN ULTRASTRUCTURAL STUDY OF UTERO‐PLACENTAL SPIRAL ARTERIES IN HYPERTENSIVE AND NORMOTENSIVE PREGNANCY AND FETAL GROWTH RETARDATION
SHEPPARD, B. L., & Bonnar, J. (1981) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1981.tb01268.x · Cited by 288 · see citing works
Role of Inflammatory Mediators in Angiogenesis
Naldini, A., & Carraro, F. (2005) · Current Drug Targets - Inflammation & Allergy · doi:10.2174/1568010053622830 · Cited by 287 · see citing works
Stereological Investigation of Placental Morphology in Pregnancies Complicated by Pre-eclampsia with and without Intrauterine Growth Restriction
Mayhew, T. M., Ohadike, C., Baker, P. N., Crocker, I. P., Mitchell, C. A., & Ong, S. S. (2003) · Placenta · doi:10.1053/plac.2002.0900 · Cited by 278 · see citing works
Placental pathologic features of preterm preeclampsia
Salafia, C. M., Pezzullo, J. C., López-Zeno, J., Simmens, S. J., MINIOR, V. K., & Vintzileos, A. M. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)91333-5 · Cited by 254 · see citing works
Self-citation
Fetal thrombotic vasculopathy: The clinical significance of extensive avascular villi
Redline, R. W., & Pappin, A. (1995) · Human Pathology · doi:10.1016/0046-8177(95)90118-3 · Cited by 240 · see citing works
ON THE PATHOGENESIS OF PLACENTAL INFARCTS IN PRE‐ECLAMPSIA
Brosens, I. A., & Renaer, M. (1972) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1972.tb12922.x · Cited by 214 · see citing works
Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats
MacLennan, N. K., James, S. J., Melnyk, S., Piroozi, A., Jernigan, S., Hsu, J. L., Janke, S. M., Pham, T. D., & Lane, R. H. (2004) · Physiological Genomics · doi:10.1152/physiolgenomics.00042.2004 · Cited by 209 · see citing works
Fetal umbilical cord oxygen values and birth to placental weight ratio in relation to size at birth
Lackman, F., Capewell, V., Gagnon, R. J., & Richardson, B. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.116686 · Cited by 192 · see citing works
Placental inflammation
Redline, R. W. (2004) · Seminars in Neonatology · doi:10.1016/j.siny.2003.09.005 · Cited by 185 · see citing works
Fetal growth is directly related to maternal anthropometry and placental volume
Thame, M. M., Osmond, C., Bennett, F. I., Wilks, R., & Forrester, T. (2004) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601909 · Cited by 182 · see citing works
Placental pathologic findings in preterm birth
Salafia, C. M., Vogel, C., Vintzileos, A., et al. (1991) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(91)90443-u · Cited by 181 · see citing works
Self-citation
Placental pathology of absent and reversed end-diastolic flow in growth-restricted fetuses
Salafia, C., Pezzullo, J. C., MINIOR, V. K., & Divon, M. Y. (1997) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(97)00473-0 · Cited by 162 · see citing works
Self-citation
INFECTION AND PRETERM BIRTH
Andrews, W. W., Hauth, J. C., & Goldenberg, R. L. (2000) · American Journal of Perinatology · doi:10.1055/s-2000-13448 · Cited by 159 · see citing works
Intrauterine Growth Restriction in Humans Is Associated with Abnormalities in Placental Insulin-Like Growth Factor Signaling
Laviola, L., Perrini, S., Belsanti, G., Natalicchio, A., Montrone, C., Leonardini, A., Vimercati, A., Scioscia, M., Selvaggi, L. E., GIORGINO, R., et al. (2004) · Endocrinology · doi:10.1210/en.2004-1332 · Cited by 151 · see citing works
Placental Pathology of Idiopathic Intrauterine Growth Retardation at Term
Salafia, C., Vintzileos, A. M., Silberman, L., Bantham, K., & Vogel, C. (1992) · American Journal of Perinatology · doi:10.1055/s-2007-999316 · Cited by 150 · see citing works
Self-citation
Nutritionally Mediated Placental Growth Restriction in the Growing Adolescent: Consequences for the Fetus1
Wallace, J. M., Aitken, R. P., Milne, J. S., & Hay, W. W. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.104.030965 · Cited by 149 · cited 1× · see citing works
“Thus, the investigators concluded that, in the model, it is the small size of the placenta per se rather than alterations in its nutrient metabolism or transfer capacity that is the major limitation to fetal growth.(5) Recent work has also clarified the potential signals that operate this causal chain.”
Background
Sequelae of chorioamnionitis
Hagberg, H., Wennerholm, U., & Sävman, K. (2002) · Current Opinion in Infectious Diseases · doi:10.1097/00001432-200206000-00014 · Cited by 148 · see citing works
The correlation between sampling site and gene expression in the term human placenta
Wyatt, S. M., Kraus, F. T., Roh, C., Elchalal, U., Nelson, D. M., & Sadovsky, Y. (2004) · Placenta · doi:10.1016/j.placenta.2004.07.003 · Cited by 144 · see citing works
Placental Growth from the First to the Second Trimester of Pregnancy in SGA-foetuses and Pre-eclamptic Pregnancies Compared to Normal Foetuses
Hafner, E., Metzenbauer, M., Höfinger, D., Münkel, M., Gassner, R., Schuchter, K., Dillinger‐Paller, B., & Philipp, K. (2003) · Placenta · doi:10.1053/plac.2002.0918 · Cited by 127 · see citing works
Dysfunction of the endothelial nitric oxide signalling pathway in diabetes and hyperglycaemia
Sobrevía, L., & Mann, G. E. (1997) · Experimental Physiology · doi:10.1113/expphysiol.1997.sp004038 · Cited by 126 · see citing works
Bias in Studies of Preterm and Postterm Delivery Due to Ultrasound Assessment of Gestational Age
Henriksen, T. B., Wilcox, A. J., Hedegaard, M. S., & Secher, N. J. (1995) · Epidemiology · doi:10.1097/00001648-199509000-00012 · Cited by 122 · see citing works
Chorioamnionitis: A Risk Factor for Fetal and Neonatal Morbidity
Bracci, R., & Buonocore, G. (2003) · Neonatology · doi:10.1159/000067956 · Cited by 116 · see citing works
Influence of pre-eclampsia on fetal growth
Xiao, R., Sorensen, T. K., Williams, W., & Luthy, D. A. (2003) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/jmf.13.3.157.162 · Cited by 115 · see citing works
Fibrinoid and Trophoblastic Necrosis With Massive Chronic Intervillositis: An Extreme Variant of Villitis of Unknown Etiology
Labarrere, C. A., & Müllen, E. (1987) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1987.tb00162.x · Cited by 114 · see citing works
Impaired Vascular Growth in Late Adolescence After Intrauterine Growth Restriction
Brodszki, J., Länne, T., Maršál, K., & Ley, D. (2005) · Circulation · doi:10.1161/circulationaha.104.490326 · Cited by 113 · see citing works
Histomorphology of the Placenta and the Placental Bed of Growth Restricted Foetuses and Correlation with the Doppler Velocimetries of the Uterine and Umbilical Arteries
Madazlı, R., Somunkiran, A., Calay, Z., et al. (2003) · Placenta · doi:10.1053/plac.2002.0945 · Cited by 112 · see citing works
Placental pathology at term associated with elevated midtrimester maternal serum α-fetoprotein concentration
Salafia, C. M., Silberman, L., Herrera, N. E., & Mahoney, M. J. (1988) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(88)90220-7 · Cited by 110 · see citing works
Self-citation
Maternal factors that determine neonatal size and body fat
Catalano, P. M., & Kirwan, J. P. (2001) · Current Diabetes Reports · doi:10.1007/s11892-001-0013-y · Cited by 102 · see citing works
Expression analyses of human endogenous retroviruses (HERVs): tissue-specific and developmental stage-dependent expression of HERVs.
Okahara, G., Matsubara, S., Oda, T., Sugimoto, J., Jinno, Y., & Kanaya, F. (2004) · Genomics · doi:10.1016/j.ygeno.2004.09.004 · Cited by 96 · see citing works
Chorioamnionitis and Labor
Edwards, R. K. (2005) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/j.ogc.2004.12.002 · Cited by 94 · see citing works
The Very Low Birthweight Infant: Maternal Complications Leading to Preterm Birth, Placental Lesions, and Intrauterine Growth
Salafia, C., Ernst, L. M., Pezzullo, J. C., Wolf, E. J., Rosenkrantz, T. S., & Vintzileos, A. M. (1995) · American Journal of Perinatology · doi:10.1055/s-2007-994417 · Cited by 93 · see citing works
Self-citation
Fetal hypertension and abnormal Doppler velocimetry in an ovine model of intrauterine growth restriction
Galan, H. L., Anthony, R. V., Rigano, S., Parker, T. A., de Vrijer, B., Ferrazzi, E. M., Wilkening, R. B., & Regnault, T. R. H. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.05.088 · Cited by 93 · see citing works
Correlation between prenatal velocity waveforms in the aortic isthmus and neurodevelopmental outcome between the ages of 2 and 4 years
Fouron, J., Gosselin, J., Amiel‐Tison, C., et al. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.110696 · Cited by 89 · see citing works
Computerized microscope morphometry of umbilical vessels from pregnancies with intrauterine growth retardation and abnormal umbilical artery doppler
Bruch, J.-F., Sibony, O., Bénali, K., et al. (1997) · Human Pathology · doi:10.1016/s0046-8177(97)90251-3 · Cited by 88 · see citing works
Pregnancy hypertension, placental evidences of low uteroplacental blood flow, and spontaneous premature delivery
Naeye, R. L. (1989) · Human Pathology · doi:10.1016/0046-8177(89)90008-7 · Cited by 88 · see citing works
Histologic chorioamnionitis is associated with fetal growth restriction in term and preterm infants
Williams, M. C., O’Brien, W. F., Nelson, R. N., & Spellacy, W. N. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2000.108866 · Cited by 85 · see citing works
Short-term exposure of high glucose concentration induces generation of reactive oxygen species in endothelial cells: implication for the oxidative stress associated with postprandial hyperglycemia
Yano, M., Hasegawa, G., Ishii, M., Yamasaki, M., Fukui, M., Nakamura, N., & Yoshikawa, T. (2004) · Redox Report · doi:10.1179/135100004225004779 · Cited by 85 · see citing works
Patterns of placental injury. Correlations with gestational age, placental weight, and clinical diagnoses.
Redline, R. W., & Patterson, P. H. (1994) · PubMed · Cited by 84 · see citing works
Plasma cellular fibronectin as a measure of endothelial involvement in preeclampsia and intrauterine growth retardation
Friedman, S. A., de Groot, C. J. M., Taylor, R. N., et al. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(94)70295-0 · Cited by 84 · see citing works
Placental hstology and fetal blood flow in intrauterine growth retardation
Laurini, R., Laurin, J., & Maršál, K. (1994) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349409006268 · Cited by 83 · see citing works
The effects of maternal vascular pressure on the dimensions of the placental capillaries
Karimu, A. L., & Burton, G. J. (1994) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1994.tb13011.x · Cited by 82 · see citing works
Placental histomorphometry and morphometric diffusing capacity of the villous membrane in pregnancies complicated by maternal iron-deficiency anemia
Reshetnikova, O. S., Burton, G. J., & Васильевна, Т. О. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)90330-5 · Cited by 82 · see citing works
Relationships among Doppler-derived umbilical artery absolute velocities, cardiac function, and placental volume blood flow and resistance in fetal sheep
Acharya, G., Erkinaro, T. M., Mäkikallio, K., Lappalainen, T., & Rasanen, J. P. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00523.2003 · Cited by 82 · see citing works
Association of severe placental insufficiency and systemic venous pressure rise in the fetus with increased neonatal cardiac troponin T levels
Mäkikallio, K., Vuolteenaho, O. J., Jouppila, P. I., & Rasanen, J. P. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2000.106753 · Cited by 76 · see citing works
Intralobular Differences in Antioxidant Enzyme Expression and Activity Reflect the Pattern of Maternal Arterial Bloodflow Within the Human Placenta
Hempstock, J., Bao, Y.-P., Bar-Issac, M., et al. (2003) · Placenta · doi:10.1053/plac.2002.0955 · Cited by 73 · see citing works
Are Placental Lakes of any Clinical Significance?
Thompson, M. O., Vines, S. K., Aquilina, J., Wathen, N. C., & Harrington, K. (2002) · Placenta · doi:10.1053/plac.2002.0837 · Cited by 71 · see citing works
Preterm Delivery: Correlations of Fetal Growth and Placental Pathology
Salafia, C. M., Vogel, C., Bantham, K., Vintzileos, A. M., Pezzullo, J. C., & Silberman, L. (1992) · American Journal of Perinatology · doi:10.1055/s-2007-999318 · Cited by 69 · see citing works
Self-citation
Recurrent reproductive failure due to severe placental villitis of unknown etiology.
Russell, P., Atkinson, K., & Krishnan, L. (1980) · PubMed · Cited by 69 · see citing works
Histomorphometry of the human placenta in pre-eclampsia associated with severe intrauterine growth retardation
Teasdale, F. (1987) · Placenta · doi:10.1016/0143-4004(87)90015-4 · Cited by 68 · see citing works
Chronic villitis of unknown aetiology and intrauterine growth-retarded infants of normal and low ponderal index
Althabe, O., & Labarrere, C. A. (1985) · Placenta · doi:10.1016/s0143-4004(85)80047-3 · Cited by 68 · see citing works
The thick heterogeneous (jellylike) placenta: a strong predictor of adverse pregnancy outcome
Raio, L., Ghezzi, F., Cromi, A., Nelle, M., Dürig, P., & Schneider, H. (2004) · Prenatal Diagnosis · doi:10.1002/pd.828 · Cited by 68 · see citing works
Leptin: A Potential Marker of Placental Insufficiency
Lepercq, J. A., Guerre-Millo, M., André, J., Caüzac, M., & Mouzon, S. H. (2003) · Gynecologic and Obstetric Investigation · doi:10.1159/000071529 · Cited by 66 · see citing works
A proinflammatory cytokine response is present in the fetal placental vasculature in placental insufficiency
Wang, X., Athayde, N., & Trudinger, B. (2003) · American Journal of Obstetrics and Gynecology · doi:10.1067/s0002-9378(03)00652-5 · Cited by 62 · see citing works
Placental Cellular Immune Response in Women Infected with Human Parvovirus B19 during Pregnancy
Jordan, J. A., Huff, D. S., & DeLoia, J. A. (2001) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.8.2.288-292.2001 · Cited by 60 · see citing works
Maternal insulin-like growth factor-I levels (IGF-I) reflect placental mass and neonatal fat mass
Clapp, J. F., Schmidt, S., Paranjape, A., et al. (2004) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2003.09.061 · Cited by 59 · see citing works
Mechanisms, organisms and markers of infection in pregnancy
Garland, S. M., Chuileannáin, F. N., Satzke, C., & Robins-Browne, R. M. (2002) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(02)00018-9 · Cited by 58 · see citing works
Role of cytokines and other inflammatory mediators
Winkler, M. H. (2003) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1016/s1470-0328(03)00062-4 · Cited by 56 · see citing works
Placental morphology in relation to umbilical artery blood velocity waveforms
Nordenvall, M., Ullberg, U., Laurin, J., Lingman, G., Sandstedt, B., & Ulmsten, U. (1991) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/0028-2243(91)90115-2 · Cited by 55 · see citing works
Effects of Maternal Iron Restriction on Placental Vascularization in the Rat
Lewis, R. M., Doherty, C., James, L. A., Burton, G. J., & Hales, C. N. (2001) · Placenta · doi:10.1053/plac.2001.0679 · Cited by 55 · see citing works
Role of cytokines and other inflammatory mediators
Winkler, M. H. (2003) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1046/j.1471-0528.2003.00062.x · Cited by 55 · see citing works
Chronic villitis of unknown aetiology in recurrent intrauterine fetal growth retardation
Labarrere, C. A., & Althabe, O. (1987) · Placenta · doi:10.1016/0143-4004(87)90019-1 · Cited by 52 · see citing works
Lateral Placental Growth Occurs by Trophoblast Cell Invasion of Decidual Veins
Craven, C. M., Zhao, L., & Ward, K. (2000) · Placenta · doi:10.1053/plac.1999.0449 · Cited by 51 · see citing works
Trophoblast alterations in the placental bed in relation to physiological changes in spiral arteries
Gerretsen, G., Huisjes, H. J., HARDONKf, M. J., et al. (1983) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1983.tb06743.x · Cited by 51 · see citing works
Placental Composition and Surface Area but not Vascularization are Altered by Maternal Protein Restriction in the Rat
Doherty, C., Lewis, R. M., Sharkey, A., & Burton, G. J. (2002) · Placenta · doi:10.1053/plac.2002.0858 · Cited by 50 · see citing works
Differential Expression of the Coxsackievirus and Adenovirus Receptor Regulates Adenovirus Infection of the Placenta1
Koi, H., Zhang, J., Makrigiannakis, A., et al. (2001) · Biology of Reproduction · doi:10.1095/biolreprod64.3.1001 · Cited by 49 · see citing works
Foetal Growth Restriction in Children with Prothrombotic Risk Factors
von Kries, R., Junker, R., Oberle, D., et al. (2001) · Thrombosis and Haemostasis · doi:10.1055/s-0037-1616526 · Cited by 48 · see citing works
Apoptotic Activity in Villous Trophoblast Cells During B19 Infection Correlates with Clinical Outcome: Assessment by the Caspase-related M30 CytoDeath Antibody
Jordan, J. A., & Butchko, A. R. (2002) · Placenta · doi:10.1053/plac.2002.0843 · Cited by 47 · see citing works
Prospective Evaluation of Uterine Artery Flow Velocity Waveforms at 12–14 and 22–24 Weeks of Gestation in Relation to Pregnancy Outcome and Birth Weight
Carbillon, L., Uzan, M., Largillière, C., et al. (2004) · Fetal Diagnosis and Therapy · doi:10.1159/000077971 · Cited by 47 · see citing works
Placental blood flow measured by simultaneous multigate spectral Doppler imaging in pregnancies complicated by placental vascular abnormalities
Yagel, S., Anteby, E. Y., Shen, O., et al. (1999) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.1999.14040262.x · Cited by 45 · see citing works
Haemorrhagic endovasculitis of the placenta: a review with clinical correlation
Sander, C. H., Kinnane, L., Stevens, N. G., et al. (1986) · Placenta · doi:10.1016/s0143-4004(86)80141-2 · Cited by 44 · see citing works
The Longitudinal Variation in Uterine Artery Blood Flow Pattern in Relation to Birth Weight
Prefumo, F., Güven, M., Ganapathy, R., et al. (2004) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000118310.51730.2d · Cited by 44 · see citing works
Cytotoxic antibody against trophoblast and lymphocytes present in pregnancy with intra-uterine fetal growth retardation and its relation to anti-phospholipid antibody
Hasegawa, I., Takakuwa, K., Adachi, S., et al. (1990) · Journal of Reproductive Immunology · doi:10.1016/0165-0378(90)90031-z · Cited by 43 · see citing works
Suboptimal neurodevelopment in very preterm infants is related to fetal cardiovascular compromise in placental insufficiency
Kaukola, T., Rasanen, J. P., Herva, R., et al. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.12.005 · Cited by 38 · see citing works
Histologic Examination of the Placenta in the Growth-Retarded Fetus
Rayburn, W. F., Sander, C. H., & Compton, A. A. (1989) · American Journal of Perinatology · doi:10.1055/s-2007-999546 · Cited by 37 · see citing works
Choosing the best estimate of gestational age from routinely collected population‐based perinatal data
Blair, E. M., Liu, Y., & Cosgrove, P. (2004) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2004.00562.x · Cited by 36 · see citing works
Significance of changes in fetal perfusion pressure to factors controlling angiogenesis in the human term placenta
Karimu, A. L., & Burton, G. J. (1994) · Reproduction · doi:10.1530/jrf.0.1020447 · Cited by 35 · see citing works
Chorionic villous haemorrhage is associated with retroplacental haemorrhage
Mooney, E. E., Shunnar, A. A., O'Regan, M. E., & Gillan, J. (1994) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1994.tb13041.x · Cited by 34 · see citing works
Distribution of Varicella‐Zoster Virus DNA and Gene Products in Tissues of a First‐Trimester Varicella‐Infected Fetus
Nikkels, A., Delbecque, K., Pierard, G., et al. (2005) · The Journal of Infectious Diseases · doi:10.1086/426942 · Cited by 33 · see citing works
Deficiency of Blocking Factors in Intrauterine Growth Retardation and Its Relationship With Chronic Villitis
Labarrere, C. A., ALTHABE, O. H., CALETTI, E., et al. (1986) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1986.tb00003.x · Cited by 31 · see citing works
Oligohydramnios: Antepartum fetal urine production and intrapartum fetal distress
Groome, L. J., Owen, J., Neely, C. L., et al. (1991) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(91)90474-6 · Cited by 28 · see citing works
Ultrastructural abnormalities of placental villi in placentae from pregnancies complicated by intrauterine fetal growth retardation: Their relationship to decidual spiral arterial lesions
SHEPPARD, B. L., & Bonnar, J. (1980) · Placenta · doi:10.1016/s0143-4004(80)80023-3 · Cited by 27 · see citing works
Human Cytomegalovirus-Induced Upregulation of Intercellular Cell Adhesion Molecule-1 on Villous Syncytiotrophoblasts
Chan, G. C. T., Stinski, M. F., & Guilbert, L. J. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.104.028118 · Cited by 26 · see citing works
Association of Umbilical Placental Vascular Disease With Fetal Acute Inflammatory Cytokine Responses
Trudinger, B., Wang, J., Athayde, N., et al. (2002) · Journal of the Society for Gynecologic Investigation · doi:10.1177/107155760200900306 · Cited by 26 · see citing works
Endothelial cell expression of adhesion molecules is induced by fetal plasma from pregnancies with umbilical placental vascular disease
Wang, X., Athayde, N., & Trudinger, B. (2002) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2002.01240.x · Cited by 24 · see citing works
Fetal plasma stimulates endothelial cell production of cytokines and the family of suppressor of cytokine signaling in umbilical placental vascular disease
Wang, X., Athayde, N., & Trudinger, B. (2003) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2003.152 · Cited by 23 · see citing works
Placental vascular disease and toll-like receptor 4 gene expression
Wang, X., Athayde, N., & Trudinger, B. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.09.009 · Cited by 22 · see citing works
Microvascular endothelial cell activation is present in the umbilical placental microcirculation in fetal placental vascular disease
Wang, X., Athayde, N., & Trudinger, B. (2004) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2003.09.021 · Cited by 20 · see citing works
Gross pathology of the placenta in intrauterine growth retardation.
Bjøro, K. (1981) · PubMed · Cited by 20 · see citing works
Intrauterine Growth Retardation of Unknown Etiology: II. Serum Complement and Circulating Immune Complexes in Maternal Sera and Their Relationship With Parity and Chronic Villitis
Labarrere, C. A., & ALTHABE, O. H. (1986) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1986.tb00050.x · Cited by 18 · see citing works
Association of umbilical placental vascular disease with fetal acute inflammatory cytokine responses
Trudinger, B. (2002) · Journal of the Society for Gynecologic Investigation · doi:10.1016/s1071-5576(02)00147-8 · Cited by 18 · see citing works
Perinatal outcome in women with severe pregnancy complications and multiple thrombophilias
Kupferminc, M. J., Rimon, E., Ascher-Landsberg, J., et al. (2004) · Journal of Perinatal Medicine · doi:10.1515/jpm.2004.042 · Cited by 17 · see citing works
INFARCTIONS AND INTERVILLOUS THROMBOSIS IN PLACENTA, AND THEIR ASSOCIATION WITH INTRAUTERINE GROWTH RETARDATION
Rolschau, J. (1978) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.1978.57.s72.22 · Cited by 14 · see citing works
The critical role of perinatal pathology
Jeffrey, I. (2003) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1016/s1470-0328(03)00064-8 · Cited by 8 · see citing works
The critical role of perinatal pathology
Jeffrey, I. (2003) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1046/j.1471-0528.2003.00064.x · Cited by 4 · see citing works

Flagged first, then by citations

Sorted by citations

Consensus definition of fetal growth restriction: a Delphi procedure: Consensus definition of FGR
Gordijn, S. J., Beune, I. M., Thilaganathan, B., Papageorghiou, A., Baschat, A. A., Baker, P. N., Silver, R. M., Wynia, K., & Ganzevoort, W. (2016) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.15884 · Cited by 1,638 · see citing works
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
Early Life Exposure to Per- and Polyfluoroalkyl Substances (PFAS) and Latent Health Outcomes: A Review Including the Placenta as a Target Tissue and Possible Driver of Peri- and Postnatal Effects
Blake, B. E., & Fenton, S. E. (2020) · Toxicology · doi:10.1016/j.tox.2020.152565 · Cited by 499 · see citing works
The placenta in fetal growth restriction: What is going wrong?
Sun, C., Groom, K. M., Oyston, C., Chamley, L. W., Clark, A. R., & James, J. L. (2020) · Placenta · doi:10.1016/j.placenta.2020.05.003 · Cited by 253 · see citing works
Placental weight in singleton pregnancies with and without assisted reproductive technology: a population study of 536 567 pregnancies
Haavaldsen, C., Tanbo, T., & Eskild, A. (2012) · Human Reproduction · doi:10.1093/humrep/der428 · Cited by 120 · see citing works
First-trimester placental ultrasound and maternal serum markers as predictors of small-for-gestational-age infants
Schwartz, N., Sammel, M. D., Leite, R., & Parry, S. (2014) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2014.02.033 · Cited by 80 · see citing works
Macrosomia has its roots in early placental development
Schwartz, N., Quant, H. S., Sammel, M. D., & Parry, S. (2014) · Placenta · doi:10.1016/j.placenta.2014.06.373 · Cited by 35 · see citing works
Deep Learning Strategies for Ultrasound in Pregnancy
Diniz, P. H. B., Yin, Y., & Collins, S. (2020) · EMJ Reproductive Health · doi:10.33590/emjreprohealth/20-00100 · Cited by 32 · see citing works
Volume and vascularity: Using ultrasound to unlock the secrets of the first trimester placenta
Mathewlynn, S., & Collins, S. L. (2019) · Placenta · doi:10.1016/j.placenta.2019.06.379 · Cited by 30 · see citing works
Gross placental measures and childhood growth
Baptiste-Roberts, K., Salafia, C. M., Nicholson, W. K., Duggan, A., Wang, N.-Y., & Brancati, F. L. (2009) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050802415728 · Cited by 30 · see citing works
Self-citation
Multi-centre deep learning for placenta segmentation in obstetric ultrasound with multi-observer and cross-country generalization
Andreasen, L. A., Feragen, A., Christensen, A. N., Thybo, J. K., Svendsen, M. B. S., Zepf, K., Lekadir, K., & Tolsgaard, M. G. (2023) · Scientific Reports · doi:10.1038/s41598-023-29105-x · Cited by 28 · see citing works
“In particular, hypertensive pregnancy disorders, compromised fetal growth, and fetal death often stem from placental dysfunction— either due to insufficient initial placentation or diminishing placental function with increasing gestational age 14,15 .”

Production of NO and Oxidative Destruction of Proteins in the Placenta during Normal Pregnancy and Placental Insufficiency
Ивановна, К. И. (2003) · Bulletin of Experimental Biology and Medicine · doi:10.1023/b:bebm.0000010954.15992.68 · Cited by 5 · see citing works
Cotyledonary‐like placenta associated with severe intrauterine growth restriction
Kita, N., Ohira, S., Ashida, T., et al. (2003) · Journal of obstetrics and gynaecology research · doi:10.1046/j.1341-8076.2003.00123.x · Cited by 1 · see citing works
Effects of Diabetes and Hypertension on Placenta
Khatoon, F., Alshammari, R. F., Alturki, A., et al. (2022) · Journal of Advances in Medical and Pharmaceutical Sciences · doi:10.9734/jamps/2022/v24i10581
Placental Gene Expression Profile in Intrauterine Growth Restriction Due to Placental Insufficiency
Sitras, V., Paulssen, R. H., Leirvik, J., Vårtun, Å., & Acharya, G. (2009) · Reproductive Sciences · doi:10.1177/1933719109334256 · Cited by 50 · see citing works
An Animal Model of Placental Insufficiency-Induced Intrauterine Growth Restriction
Barry, J. S., Rozance, P. J., & Anthony, R. V. (2008) · Seminars in Perinatology · doi:10.1053/j.semperi.2007.11.004 · Cited by 90 · see citing works

Authors: SALAFIA, C. M., CHARLES, A. K., & MAAS, E. M.
Affiliations: Columbia University (US)
ORCID: SALAFIA, CAROLYN M.
CHARLES, ADRIAN K.
Venue: Clinical Obstetrics and Gynecology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2006-06
Volume: 49
Issue: 2
Pages: 236-256
ISSN: 0009-9201 (ISSN-L)
DOI: 10.1097/00003081-200606000-00007
OpenAlex: W2063634025
Cited by: 235
References: 103
Citations by year: 2026: 5 · 2025: 9 · 2024: 17 · 2023: 12 · 2022: 7 · 2021: 13 · 2020: 19 · 2019: 7 · 2018: 18 · 2017: 22 · 2016: 13 · 2015: 14 · 2014: 23 · 2013: 10 · 2012: 13
FWCI: 0.84
Type: journal article
Language: en
Open access: closed
Locations: Clinical Obstetrics & Gynecology (publishedVersion)
PubMed (publishedVersion)
UWA Profiles and Research Repository (UWA) (submittedVersion)
Topics: Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Keywords: placenta, fetal growth restriction, birth weight, placental weight, ponderal index, placental pathology, long-term health risks
MeSH terms: Birth Weight, Fetal Growth Retardation, Fetus, Gestational Age, Humans, Placenta

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Placenta and Fetal Growth Restriction

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks