Hostname: page-component-7d684dbfc8-jcwnr Total loading time: 0 Render date: 2023-09-27T09:56:36.319Z Has data issue: false Feature Flags: { "corePageComponentGetUserInfoFromSharedSession": true, "coreDisableEcommerce": false, "coreDisableSocialShare": false, "coreDisableEcommerceForArticlePurchase": false, "coreDisableEcommerceForBookPurchase": false, "coreDisableEcommerceForElementPurchase": false, "coreUseNewShare": true, "useRatesEcommerce": true } hasContentIssue false


Published online by Cambridge University Press:  01 August 2008

Department of Obstetrics and Gynaecology, Wayne State University, Detroit, Michigan, United States of America.
Department of Obstetrics and Gynaecology, Wayne State University, Detroit, Michigan, United States of America.
Giancarlo Mari, Professor of Obstetrics and Gynaecology, Department of Obstetrics and Gynaecology, Wayne State University, 3990 John R. Box 163, Detroit, Michigan 48201, United States of America.


Despite a plethora of publications existing in the literature, there is still confusion about the definition and management of intrauterine growth-restricted fetuses. Fetal growth restriction (FGR) is defined by the American College of Obstetricians and Gynecologists as estimated fetal weight (EFW) less than that expected for gestational age. Clinically this is applied when the EFW is less than the 10th percentile because perinatal morbidity and mortality is increased in low-birth weight infants. Other investigators have proposed and used a variety of fetal definitions: a fetus with an estimated weight < 2SD (standard deviation) from the mean, the 3rd 5th or 15th percentile and an abdominal circumference 2 SD below the mean. Because of the different definitions, it is understandable why different information has been obtained in growth restricted fetuses and why different management schemes have been proposed. A second source of confusion in FGR lies in the fundamental misunderstanding that all growth restricted fetuses are the same, and all will progress to cardiovascular failure following a similar time frame. We believe that in FGR, 2 concepts are important: the first is to detect those growth restricted fetuses at risk for adverse perinatal outcome; the second is to optimize the timing of delivery for these fetuses.

Research Article
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)



1ACOG Practice Bulletin, Intrauterine Growth Restriction. Number 12. Washington, DC: American College of Obstetricians and Gynecologists 2000.Google Scholar
2Garite, TJ, Clark, R, Thorp, JA. Intrauterine growth restriction increases morbidity and mortality among premature neonates. Am J Obstet Gynecol 2004; 191: 481–87.CrossRefGoogle ScholarPubMed
3Manning, FA. Intrauterine growth retardation. In: Manning, FA, (ed). Fetal Medicine: Principles and practice. Norwalk, CT: Appleton and Lange 1995.Google Scholar
4Barker, DJ, Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986; 1: 1077–81.CrossRefGoogle ScholarPubMed
5Breart, G, Rabarison, Y, Plouin, PF, Sureau, C, Rumeau-Roquette, C. Rosk of fetal growth retardation as a result of maternal hypertension: preparation to a trial on antihypertensive drugs. Dev Pharmacol Ther 1982; 4: 116–23.CrossRefGoogle Scholar
6McIntyre, DD, Bloom, SL, Casey, BM, Leveno, KJ. Birth weight in relation to morbidity and mortality among newborn infants. N Eng J Med 1999; 340: 1234–238.CrossRefGoogle Scholar
7Usher, R, McLean, F. Intrauterine growth of live-born Caucasian infants at sea level: standards obtained from measurements in 7 dimensions of infants born between 25 and 44 weeks of gestation. J Pediatr 1969; 74: 901–10.CrossRefGoogle ScholarPubMed
8Seeds, JW, Peng, T. Impaired growth and risk of fetal death: is the tenth percentile the appropriate standard? Am J Obstet Gynecol 1998; 178: 658–69.CrossRefGoogle ScholarPubMed
9Padoan, A, Rigano, S, Ferrazzi, E, Beaty, BL, Battaglia, FC, Galan, HL. Differences in fat and lean mass proportions in normal and growth-restricted fetuses. Am J Obstet Gynecol 2004; 191: 1459–464.CrossRefGoogle ScholarPubMed
10Mari, G, Deter, RL. Middle cerebral artery flow velocity waveforms in normal and small-for-gestational-age fetuses. Am J Obstet Gynecol 1992; 166: 1262–270.CrossRefGoogle ScholarPubMed
11Trudinger, BJ, Giles, WB, Cook, CM, Bombardieri, J, Collins, L. Fetal umbilical artery flow velocity waveforms and placental resistance: clinical significance. Br J Obstet Gynaecol 1985; 92: 2330.CrossRefGoogle ScholarPubMed
12Manning, FA, Platt, LD, Sipos, L. Antepartum fetal evaluation: development of a fetal biophysical profile. Am J Obstet Gynecol. 1980; 136: 787–95.CrossRefGoogle ScholarPubMed
13Dawes, GS, Redman, CW, Smith, JH. Improvements in the registration and analysis of fetal heart rate records at the bedside. Br J Obstet Gynaecol 1985; 92: 317–25.CrossRefGoogle ScholarPubMed
14Walkinshaw, S, Cameron, H, MacPhail, S, Robson, S. The prediction of fetal compromise and acidosis by biophysical profile scoring in the small for gestational age fetus. J Perinat Med 1992; 20: 227–32.CrossRefGoogle ScholarPubMed
15Manning, FA, Snijders, R, Harman, CR, Nicolaides, K, Menticoglou, S, Morrison, I. Fetal biophysical profile score. VI. Correlation with antepartum umbilical venous fetal pH. Am J Obstet Gynecol 1993; 169: 755–63.CrossRefGoogle ScholarPubMed
16Vintzileos, AM, Gaffney, SE, Salinger, LM, Kontopoulos, VG, Campbell, WA, Nochimson, DJ. The relationships among the fetal biophysical profile, umbilical cord pH, and Apgar scores. Am J Obstet Gynecol 1987; 157: 627–31.CrossRefGoogle ScholarPubMed
17Baschat, 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: 571–77.CrossRefGoogle ScholarPubMed
18Soothill, PW, Ajayi, RA, Campbell, S, Ross, EM, Candy, DC, Snijders, RM et al. Relationship between fetal acidaemia at cordocentesis and subsequent neurodevelopment. Ultrasound Obstet.Gynecol 1992; 2: 8083.CrossRefGoogle Scholar
19Kaur, S, Hanif, F, Drennan, K, Chada, R, Kruger, M, Mari, G. Biophysical profile in the management of intrauterine growth-restricted fetuses with birth weights less than 1000 grams. Am J Obstet Gynecol 2007: 197: S181.CrossRefGoogle Scholar
20Lalor, JG, Fawole, B, Alfirevic, Z, Devane, D. Biophysical profile for fetal assessment in high risk pregnancies. Cochrane Database of Systematic Reviews 2008, Issue 1. Art No: CD000038. DOI: 10.1002/14651858.CD000038.pub2.CrossRefGoogle Scholar
21Mari, G, Wasserstrum, N. Flow velocity waveforms of the fetal circulation preceding fetal death in a case of lupus anticoagulant. Am J Obstet Gynecol 1991; 164: 776–78.CrossRefGoogle Scholar
22Arduini, D, Rizzo, G, Romanini, C. Changes of pulsatility index from fetal vessels preceding the onset of late decelerations in growth-retarded fetuses. Obstet Gynecol. 1992; 79: 605–10.Google ScholarPubMed
23Hecher, K, Bilardo, CM, Stigter, RH, Ville, Y, Hackeloer, BJ, Kok, HJ et al. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol 2001; 18: 564–70.CrossRefGoogle ScholarPubMed
24Baschat, 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: 571–77.CrossRefGoogle ScholarPubMed
25Ferrazzi, E, Bozzo, M, Rigano, S, Bellotti, M, Morabito, A, Pardi, G 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: 140–46.CrossRefGoogle ScholarPubMed
26Cosmi, E, Ambrosini, G, D'Antona, D, Saccardi, C, Mari, G. Doppler, cardiotocography, and biopgysical profile changes in growth restricted fetuses. Obstet Gynecol 2005; 106: 1240–245.CrossRefGoogle ScholarPubMed
27Mari, G, Deter, RL, Hanif, F, Treadwell, M, Kruger, M. Sequence of cardiovascular changes occurring in severe IUGR fetuses – part II. Ultrasound Obstet Gynecol 2006; 28: 390.CrossRefGoogle Scholar
28Hanif, F, Mari, G, Drennan, K, Kruger, M. Sequence of cardiovascular changes occurring in severe IUGR fetuses in pregnancies complicated by pre-eclampsia and in pregnancies without this complication. Ultrasound Obstet Gynecol 2007; 30: 444–45.CrossRefGoogle Scholar
29Baschat, AA, Cosmi, E, Bilardo, CM, Wolf, H, Berg, C, Rigano, S et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol 2007: 109: 253–61.CrossRefGoogle ScholarPubMed
30Mari, G, Hanif, F, Treadwell, MC, Kruger, M. Gestational age at delivery and Doppler waveforms in very preterm IUGR fetuses as predictors of perinatal mortality. J Ultrasound Med 2007; 26: 555–59.CrossRefGoogle ScholarPubMed
31Krebs, C, Macara, LM, Leiser, R, Bowman, AW, Greer, IA, Kingdom, JCP. Intrauterine growth restriction with absent end-diastolic flow velocity in the umbilical artery is associated with maldevelopment of the placental terminal villous tree. Am J Obstet Gynecol 1996; 175: 1534–542.CrossRefGoogle ScholarPubMed
32Picconi, JL, Hanif, F, Drennan, K, Mari, G. The transitional phase of ductus venosus reversed flow in severely premature IUGR fetuses. Am J Perinatol 2008; 25: 199204.CrossRefGoogle ScholarPubMed
33Hanif, F, Drennan, K, Picconi, J, Mari, G. Ductus venosus reversed flow and arterial cord pH in fetuses delivered at <30 weeks and weighing <750 grams. Am J Obstet Gynecol 2007: 197: S208.CrossRefGoogle Scholar
34Mari, G, Hanif, F, Kruger, M, Cosmi, E, Santolaya-Forgas, J, Treadwell, MC. Middle cerebral artery peak systolic velocity: a new Doppler parameter in the assessment of growth-restricted fetuses. Ultrasound Obstet Gynecol 2007; 29: 310–16.CrossRefGoogle ScholarPubMed
35Hanif, F, Drennan, K, Mari, G. Variables affecting the middle cerebral artery peak systolic velocity in anaemic and IUGR fetuses. Am J Perinatol 2007; 24: 501505.CrossRefGoogle Scholar
36Greisen, G. Autoregulation of cerebral blood flow in newborn babies. Early Hum Dev 2005: 81: 423–28.CrossRefGoogle ScholarPubMed
37Mari, G, Hanif, F, Drennan, F, Kruger, M. Staging of intrauterine growth-restricted fetuses. J Ultrasound Med 2007; 26: 1469–477.CrossRefGoogle ScholarPubMed