Imaging in Intrauterine Growth Retardation

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The term intrauterine growth restriction has largely replaced the term intrauterine growth retardation (IUGR). The definition of IUGR is a problematic one because we do not know the inherent growth potential of the fetus. The most common definition used is fetal weight below the 10th percentile for gestational age. The preferred method for evaluating intrauterine growth retardation (intrauterine growth restriction; IUGR) is ultrasonographic examination ^{[1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13]}  (see the images below).

In most cases of fetal growth restriction, the transcerebellar diameter appears to be spared and can be used as an unbiased measure of gestational age. The transcerebellar diameter in millimeters is equal to gestational age in weeks to 22 weeks of gestation. With this definition, IUGR and “small for gestational age” are synonymous terms.

Intrauterine growth restriction has a prevalence of 10% for all pregnancies. However, the figure varies in different patient populations, with rates of 3-5% for healthy mothers and 25% or higher for some high-risk groups, such as hypertensive mothers. Growth-restricted pregnancies are often complicated by a high rate of antepartum and intrapartum fetal distress and the need for cesarean delivery. Infants who are small for their gestational dates are predisposed to low APGAR scores, low cord pH, intraventricular hemorrhage, necrotizing enterocolitis, hypoglycemia, hypocalcemia, and polycythemia.

Melchiorre et al found that there is a significant relationship between first-trimester uterine artery Doppler resistance indices (RI) and the subsequent delivery of neonates who are small for gestational age (SGA) or have intrauterine growth restriction (IUGR). They found, however, that the sensitivity of first-trimester uterine artery Doppler is greater for SGA with preeclampsia than it is for IUGR alone and noted that this difference could be the result of different underlying placental abnormalities that are detected variably on first-trimester uterine artery Doppler evaluation. ^[2]

Scifres et al found that oligohydramnios (amniotic fluid index < 5) and abnormal umbilical artery Dopplers (absent or reverse end-diastolic flow) had modest predictive value for perinatal mortality. ^[14] The authors evaluated whether maternal demographic and ultrasound parameters predict perinatal mortality (in utero death or neonatal death within the first 28 days of life) in preterm IUGR (delivery gestational age < 35 weeks and birth weight < 10th percentile for gestation). Two hundred thirty singleton pregnancies with preterm IUGR meeting the study inclusion criteria were identified.

In a prospective study (2005-2007) by Bastek et al of 93 women with severe preeclampsia and ultrasound 3 weeks or less before delivery, current ultrasound practice was noted to have moderately good positive and negative predictive values and a high specificity for the diagnosis of IUGR in women with severe preeclampsia. However, according to the authors, the poor sensitivity (56.7%) and low positive likelihood ratio (8.9) indicate that additional modalities are needed to improve the usefulness of ultrasound in detecting IUGR in severe preeclampsia. ^[3]

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Doppler study of the umbilical artery can be done anywhere along the length of the umbilical artery. One should try to obtain as vertical view as possible on the umbilical artery. Blood in the main uterine arteries flows in a direction opposite that in the iliac arteries. The typical waveform shows a deep notch in relation to the closure of the aortic valve. The notch that is present before pregnancy gradually disappears during pregnancy, and diastolic flow increases with advancing gestation (ie, the vessel resistance decreases). ^{[1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13]}

See the ultrasound images below.

Fetal weight below the 10th percentile has negative predictive value of 99%, a sensitivity of 89%, and a specificity of 88% for the detection of IUGR. ^[15] An elevated HC-to-AC ratio has a negative predictive value of 98%, a sensitivity of 82%, and a specificity of 94% for the detection of IUGR. Decreased weight with decreased amniotic fluid and the presence of hypertension are good predictors of IUGR.

The triplex mode is used for the evaluation of the umbilical venous blood flow. This mode includes color Doppler sonography of the umbilical vein, pulsed Doppler velocimetry, and real-time sonography to measure the diameter of the umbilical vein. ^{[4, 5, 6, 7]}

Several clinical and sonographic parameters can be used in combination to establish the diagnosis of intrauterine growth retardation (intrauterine growth restriction; IUGR) with greater certainty. The key parameters for diagnosing IUGR are the following:

Estimated fetal weight

Volume of amniotic fluid

Mother’s blood pressure status

The sonographic criteria for IUGR include the following:

An elevated ratio of femoral length to abdominal circumference (AC)

An elevated ratio of head circumference (HC) to AC

Unexplained oligohydramnios

The AC measurement is the best single measurement to assess fetal growth because, in growth curtailment, the liver is virtually always affected. Hadlock charts can be used to calculate the fetal weight from the AC. ^[16] Most ultrasonography machines also use the Hadlock method of calculating fetal weight. The literature describes at least 47 formulas for the estimation of fetal weight. Using the Shepard formula (AC and biparietal diameter [BPD]), one can come within 5% of the true fetal weight and within 10% of the fetal weight 80% of the time. However, 20% of the time, the estimation of the fetal weight may be discrepant by more than 10%.

Oligohydramnios is an indicator of IUGR. Amniotic fluid of less than 5 cm, as measured in the 4 quadrants, is suggestive of oligohydramnios. Other causes of oligohydramnios include death in utero, renal agenesis, and premature rupture of membranes.

The rationale for performing a Doppler study in the diagnosis of IUGR is that many cases of growth restriction are thought to be associated with small vessel disease in the fetoplacental or uteroplacental circulation. Numerous Doppler criteria have been proposed for diagnosing IUGR. These involve at least 3 of the following waveform indices:

Systolic/diastolic (S/D) ratio

Pulsatility index (PI)

Resistive index (RI)

Spectral waveform of the umbilical, uterine, and fetal internal carotid arteries and the fetal descending thoracic aorta

Spectral waveform of the ductus venosus and inferior vena cava

Abnormal findings on Doppler waveforms include the following:

Highest uterine artery PI – lowest uterine artery PI greater than 1.1

Persistence of protodiastolic notch, unilateral or bilateral, after 23 weeks is suggestive of IUGR or preeclampsia.

RI greater than 0.55 with bilateral notches

RI greater than 0.65 with a unilateral notch

RI greater than 0.70 with or without notches

RI greater than 90th percentile for a given gestational age regardless of notches

An S/D ratio of greater than 3 after 30 weeks of gestation is abnormal.

The reversal of flow in ductus venosus is suggestive of a fetus with severely compromised IUGR and reflects fetal metabolic acidemia.

Umbilical venous blood flow, both absolute flow (in mm/min) and corrected blood flow (in mL/min/kg) are reduced in IUGR. Presence of pulsations in umbilical vein waveform between 8 and 12 weeks is normal, and its persistence is abnormal. The presence of umbilical vein pulsations is associated with an increased risk of an adverse perinatal outcome.

Grivell RM, Wong L, Bhatia V. Regimens of fetal surveillance for impaired fetal growth. Cochrane Database Syst Rev. 2009 Jan 21. CD007113. [Medline].

Melchiorre K, Leslie K, Prefumo F, Bhide A, Thilaganathan B. First-trimester uterine artery Doppler indices in the prediction of small-for-gestational age pregnancy and intrauterine growth restriction. Ultrasound Obstet Gynecol. 2009 May. 33(5):524-9. [Medline].

Bastek JA, Pare E, Wang E, Elovitz MA, Srinivas SK. Limitations of ultrasound in diagnosing intrauterine growth restriction in severe preeclampsia. J Matern Fetal Neonatal Med. 2009 Jun 29. 1-6. [Medline].

Kurjak A, Azumendi G, Andonotopo W. Three- and four-dimensional ultrasonography for the structural and functional evaluation of the fetal face. Am J Obstet Gynecol. 2006 Sep 29.

Jasovic-Siveska EI, Jasovic VI. Real-time ultrasound in the detection of intrauterine growth retardation in preeclampsia. Bratisl Lek Listy. 2008. 109(9):405-11. [Medline].

Palma-Dias RS, Fonseca MM, Brietzke E, Fritsch A, Schlatter D, Maurmann CB, et al. Screening for placental insufficiency by transvaginal uterine artery Doppler at 22-24 weeks of gestation. Fetal Diagn Ther. 2008. 24(4):462-9. [Medline].

Phupong V, Dejthevaporn T. Predicting risks of preeclampsia and small for gestational age infant by uterine artery Doppler. Hypertens Pregnancy. 2008. 27(4):387-95. [Medline].

Lazebnik N, Lazebnik RS. Doppler Evaluation in intrauterine growth-restricted fetuses. In: Dogra VS, Rubens DJ, eds. Philadelphia, Pa: Hanley & Belfus; 2003:67-74.

Paspulati RM, Bhatt S, Nour S. Sonographic evaluation of first-trimester bleeding. Radiol Clin North Am. 2004 Mar. 42(2):297-314. [Medline].

Giuliano N, Annunziata ML, Tagliaferri S, Esposito FG, Imperato OC, Campanile M, et al. IUGR management: new perspectives. J Pregnancy. 2014. 2014:620976. [Medline].

Bhimarao, Nagaraju RM, Bhat V, Gowda PV. Efficacy of Transcerebellar Diameter/Abdominal Circumference Versus Head Circumference/Abdominal Circumference in Predicting Asymmetric Intrauterine Growth Retardation. J Clin Diagn Res. 2015 Oct. 9 (10):TC01-5. [Medline].

Osmanski BF, Lecarpentier E, Montaldo G, Tsatsaris V, Chavatte-Palmer P, Tanter M. Discriminative imaging of maternal and fetal blood flow within the placenta using ultrafast ultrasound. Sci Rep. 2015 Sep 16. 5:13394. [Medline].

Cruz-Martinez R, Tenorio V, Padilla N, Crispi F, Figueras F, Gratacos E. Risk of ultrasound-detected neonatal brain abnormalities in intrauterine growth-restricted fetuses born between 28 and 34 weeks’ gestation: relationship with gestational age at birth and fetal Doppler parameters. Ultrasound Obstet Gynecol. 2015 Oct. 46 (4):452-9. [Medline].

Scifres CM, Stamilio D, Macones GA, Odibo AO. Predicting perinatal mortality in preterm intrauterine growth restriction. Am J Perinatol. 2009 Nov. 26(10):723-8. [Medline].

Proctor LK, Toal M, Keating S, Chitayat D, Okun N, Windrim RC, et al. Placental size and the prediction of severe early-onset intrauterine growth restriction in women with low pregnancy-associated plasma protein-A. Ultrasound Obstet Gynecol. 2009 Sep. 34(3):274-82. [Medline].

Hadlock FP, Harrist RB, Carpenter RJ. Sonographic estimation of fetal weight. The value of femur length in addition to head and abdomen measurements. Radiology. 1984 Feb. 150(2):535-40. [Medline].

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Bewley S, Cooper D, Campbell S. Doppler investigation of uteroplacental blood flow resistance in the second trimester: a screening study for pre-eclampsia and intrauterine growth retardation. Br J Obstet Gynaecol. 1991 Sep. 98(9):871-9. [Medline].

Bower S, Vyas S, Campbell S, Nicolaides KH. Color Doppler imaging of the uterine artery in pregnancy: normal ranges of impedance to blood flow, mean velocity and volume of flow. Ultrasound Obstet Gynecol. 1992 Jul 1. 2(4):261-5. [Medline].

Doubilet PM, Benson CB. Sonographic evaluation of intrauterine growth retardation. AJR Am J Roentgenol. 1995 Mar. 164(3):709-17. [Medline].

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Shepard MJ, Richards VA, Berkowitz FL. An evaluation of two equations for predicting fetal weight by ultrasound. Am J Obstet Gynecol. 1982. 142:47.

Vikram S Dogra, MD Professor of Diagnostic Radiology, Urology, and Biomedical Engineering, University of Rochester School of Medicine; Director, Division of Ultrasound, Associate Chair of Education and Research, Department of Imaging Sciences, University of Rochester Medical Center

Vikram S Dogra, MD is a member of the following medical societies: American College of Radiology, Association of Program Directors in Radiology, Society of Radiologists in Ultrasound, American Institute of Ultrasound in Medicine, American Roentgen Ray Society, Radiological Society of North America, Society of Abdominal Radiology

Disclosure: Nothing to disclose.

Shweta Bhatt, MD Associate Professor, Department of Imaging Sciences, University of Rochester Medical Center

Shweta Bhatt, MD is a member of the following medical societies: Radiological Society of North America

Disclosure: Nothing to disclose.

Bernard D Coombs, MB, ChB, PhD Consulting Staff, Department of Specialist Rehabilitation Services, Hutt Valley District Health Board, New Zealand

Disclosure: Nothing to disclose.

Karen L Reuter, MD, FACR Professor, Department of Radiology, Lahey Clinic Medical Center

Karen L Reuter, MD, FACR is a member of the following medical societies: American Association for Women Radiologists, American College of Radiology, American Institute of Ultrasound in Medicine, American Roentgen Ray Society, Radiological Society of North America

Disclosure: Nothing to disclose.

Eugene C Lin, MD Attending Radiologist, Teaching Coordinator for Cardiac Imaging, Radiology Residency Program, Virginia Mason Medical Center; Clinical Assistant Professor of Radiology, University of Washington School of Medicine

Eugene C Lin, MD is a member of the following medical societies: American College of Nuclear Medicine, American College of Radiology, Radiological Society of North America, Society of Nuclear Medicine and Molecular Imaging

Disclosure: Nothing to disclose.

Imaging in Intrauterine Growth Retardation

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