Advances in fetal imaging.

Review Article

567

Advances in Fetal Imaging Richard A. Barth, MD1

1 Department of Radiology, Lucile Packard Children’s Hospital,

Stanford University School of Medicine, Stanford, California Am J Perinatol 2014;31:567–576.

Abstract

Keywords

► ► ► ►

fetal imaging fetal MRI 3D US

While ultrasound (US) has been a part of prenatal care for almost 40 years, technical progress over the last two decades has resulted in improved image quality and detection rate of congenital anomalies. The past 15 years have also seen the expansion of three-dimensional (3D) US, providing enhancements over with 2D US, and more realistic images of babies to parents and providers. Fetal magnetic resonance imaging (MRI) was first performed over 30 years ago, and has undergone major technical improvement over the past 15 to 20 years. Fetal MRI complements US by providing better visualization in the fetus when US is limited such as in oligohydramnios or severe maternal obesity. It offers a larger field of view and better tissue contrast than US and is not limited by shadowing from osseous structures. However, MRI has a limited resolution compared with US, is less readily available, and more expensive. While indications for fetal MRI have been clearly established for some abnormalities, such as neurological anomalies, other indications especially for fetal body imaging are not as clearly defined. In this article, we discuss recent developments in fetal MRI and 3D US and their common and newest indications.

Fetal Lungs Ultrasound (US) is the primary screening method for detecting chest anomalies, such as diaphragmatic hernias and bronchopulmonary malformations (BPM), largely due to its ability to detect mediastinal shift.1 In the case of congenital diaphragmatic hernia (CDH), the severity of the anomaly needs to be established to anticipate prenatal and postnatal management and to provide accurate parental counseling. The main factors for prognosis of outcome are residual lung volumes and herniated organs. At the time of the anatomyscreening US scan, bowel and liver have relatively similar echogenicity to the fetal lung and the severity of the CDH may be difficult to evaluate by US alone. Moreover, a small diaphragmatic hernia that does not produce mediastinal shift or a rare bilateral diaphragmatic hernia may be missed.2 Fetal magnetic resonance imaging (MRI) provides higher tissue contrast and allows for delineation and quantification of the herniated organs, particularly solid organs such as the liver or kidneys. MRI also provides visualization of the hernia sac,

received January 13, 2014 accepted after revision January 23, 2014 published online May 2, 2014

Address for correspondence Erika Rubesova, MD, Department of Radiology, Lucile Packard Children’s Hospital, Stanford University School of Medicine, 725 Welch Road, Room 1681, Stanford, CA 943055913 (e-mail: [email protected]).

if present, which is associated with better outcome.3,4 T1-weighted images better assess the liver location, volume of herniated liver, and meconium filled bowel in the chest (►Fig. 1).5 Postnatal morbidity and survival in isolated CDH is largely dependent on the severity of pulmonary hypoplasia and degree of pulmonary hypertension. Fetal MRI has been shown to be superior to US for quantification of residual lung volumes in the case of diaphragmatic hernia. Several methods have been described to measure lung volumes.6,7 The most commonly used is the measure of lung volumes obtained by tracing the region of interest (ROI) around the residual lung on each slide (preferably in the axial plane). The sum of the ROI from each slice, multiplied by the slice thickness gives the total lung volume. Many publications provide normative data of lung volumes as a function of gestational age, but values vary widely between studies.8 The multi-institutional study by Rypens et al6 included the largest number of patients and is the primary reference for most investigators and clinicians, but demonstrated a broad range

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DOI http://dx.doi.org/ 10.1055/s-0034-1371712. ISSN 0735-1631.

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Erika Rubesova, MD1

Advances in Fetal Imaging

Rubesova, Barth

Fig. 1 Coronal T2-weighted SSFSE image (A) of a fetus at 34 weeks of gestational age with diaphragmatic hernia. The coronal T1-weighted GRE image (B) demonstrates presence of meconium-filled bowel (most likely colon) in the hernia. (C) A sagittal T2-weighted SSFSE image of the same fetus shows that the left kidney is herniated in the chest (arrow). GRE, gradient recalled echo; SSFSE, single shot fast spin echo.

of normal fetal lung volume values at each gestational age. Measurement of lung volumes in fetuses with CDH may overlap with measured lung volumes in normal fetuses. To correct for the large variation of normal lung volume measurements, some have suggested using an internal reference for assessing the size of the lungs. These include “percent predicted lung volume (PPLV),” calculated by measuring the residual lung volume divided by the predicted lung volume.7 The authors have reported cut off points for the PPLV that predict postnatal survival or death in case of CDH. Another approach to assessing outcomes prediction for fetuses with CDH is based on the ratio of the measured or observed fetal lung volume to the expected fetal lung volume based on the Rypens normative data. The latter correlates better with postnatal outcome than the measured fetal lung volume alone.9,10 Liver herniation is another important predictor of survival CDH.11–13 Liver herniation as a predictor of need for extracorporeal membrane oxygenation support is less certain.13–15 US can also be used to predict outcome by assessing lung volume in fetuses with CDH. One of the best-validated US methods is the lung-to-head ratio.16 Pulmonary hypertension is also associated with adverse outcome in neonates with CDH. Doppler of the pulmonary arteries and correlation with pulsatile index and peak early diastolic reverse flow in the fetus has been suggested to assist in predicting severity of pulmonary hypertension. Another predictor of pulmonary hypertension is the modified McGoon index. It was originally described in adults but adapted to fetuses, and is obtained by combined diameters of hilar pulmonary arteries divided by the width of the descending aorta at the level of the diaphragm.17 Both US and MRI play a role in the evaluation and followup of congenital BPM. These lesions represent a spectrum of anomalies including congenital pulmonary airway malformation (CPAM), bronchopulmonary sequestration, and congenital lung overinflation (CLO) with or without bronchial atresia.18 While these lesions are easily visualized by US in the second trimester and early third trimester of pregnancy, American Journal of Perinatology

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they are less conspicuous in the late third trimester of pregnancy due to the normal changes in fetal lung, becoming similar in echogenicity to the BPM with advancing gestational age. BPM may decrease in absolute size or relative size to the fetus with advancing gestational age and mediastinal shift may become less apparent.19 US is useful for performing regular hydrops checks and to calculate the CPAM volume ratio, obtained by dividing the lesion volume by the fetal head circumference, and which predicts the risk of hydrops.19 Fetal MRI has been shown to yield useful additional information in the setting of thoracic anomalies.20 Fetal MRI may better delineate the lesion and characterize the type of BPM. Heterogeneous lesions containing cysts are more likely to represent a CPAM or hybrid lesion, whereas homogeneous lesions are more likely to represent CLO.21 A BPM associated with a systemic arterial feeder is characteristic of sequestration or hybrid mass. Appropriate characterization of these lesions assists in prenatal counseling and delivery planning as the management and postnatal outcome is variable. For instance, sequestration and CPAM are more likely to undergo surgical resection at some point in time, but CLO is frequently managed conservatively.22 Nevertheless, the postnatal management of asymptomatic BPM’s remains controversial.23

Fetal Mediastinum The combination of polyhydramnios and small stomach are the most frequent indirect signs of esophageal atresia on fetal US. However, direct visualization of the atresia remains challenging. In some circumstances, an intermittently fluid filled esophageal pouch can be seen in the proximal mediastinum (►Fig. 2).24 In the presence of a small stomach and polyhydramnios but no clear evidence of the atresia, it is important to consider the possibility of neurologic abnormalities, which may lead to lack of fetal deglutition. Fetal MRI is therefore recommended. In some instances, the esophageal atresia can be seen on fetal MRI as well as a fistula between the trachea and the distal esophagus. Real-time imaging in sagittal view on MRI is helpful to demonstrate normal fetal


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Fig. 2 (A) Fetus with polyhydramnios, on ultrasound, and small stomach. (B) Sagittal fluid sensitive magnetic resonance image of the same fetus at 29 weeks of gestational age shows an esophageal pouch in the upper mediastinum consistent with esophageal atresia.

swallowing and the filling of the esophageal pouch.25 Given a larger field of view than US and the lack of shadowing from fetal bones, MRI usually better delineates airways and abnormalities associated with them. In cases of suspected fetal airway compromise or obstruction, the level and the cause of obstruction can be established. This is essential for delivery planning, including ex-utero intrapartum treatment in severe cases, to safely establish an airway while the patient is maintained on placental circulation.26,27

Fetal Gastrointestinal System At the anatomy US scan (18–22 weeks gestational age), normal bowel usually appears as heterogeneous tissue; individual loops, if not dilated, are difficult to identify. The most common abnormalities of bowel seen on US at that gestational age are echogenic bowel and dilated bowel loops. Echogenic bowel is defined as a bowel with an echogenicity equal to the adjacent bone.28 It is a recognized soft marker for chromosomal abnormalities, but has also been described in fetuses with cystic fibrosis, viral infections, and in-utero growth restriction, with a rate of associated abnormalities reported to be about 30%.29 Echogenic bowel, without associated bowel dilatation, may resolve over the course of the pregnancy. In cases of isolated echogenic bowel, the indications for and value of fetal MRI have not been established. Fetal MRI may play a role in evaluation if the echogenic bowel is associated with other findings, or may help to confirm microcolon in cases of echogenic bowel associated with meconium ileus secondary to cystic fibrosis or in the setting dilated bowel on US.30 Bowel dilatation may be detected by screening US. US is the modality of choice for diagnosis of duodenal atresia, which presents with the pathognomonic “double bubble” sign. Fetal MRI is usually not considered unless there is suspicion for associated congenital anomalies. Advantages of US include real-time evaluation of peristalsis and detection of bowel wall thickening. Absence of peristalsis and bowel wall thickening

may be indicative of vascular injury to the fetal bowel.31 Jejunal, ileal, and colonic atresia may be the result of an ischemic event in utero, and can present on US as multiple loops of dilated bowel. Localization of the obstruction by US alone remains a challenge. Fetal MRI can provide complementary information given the larger field of view and better tissue contrast, but also by the unique appearance of meconium on T1-weighted sequences.32 Meconium is rich in amino acids, bile salts, dry residual of swallowed amniotic fluid, and desquamated cells which gives meconium a high signal intensity. Meconium is seen in the small bowel and colon beginning at 18 weeks gestation. With progression of pregnancy and onset of fetal bowel peristalsis, meconium accumulates first in the rectum and progressively in the more proximal colon.33,34 The fetal rectum is consistently the largest area of the fetal bowel through the pregnancy.35 This is an essential sign to assess on fetal MRI; identification of a high T1 signal in the rectum should be the starting point for evaluation of the bowel.33 Absence of high signal at the level of the rectum on T1-weighted images should raise concern for microcolon, or pathology that interferes with meconium formation or meconium accumulation in the rectum. Presence of microcolon helps to differentiate proximal from distal obstruction. Microcolon is usually associated with distal obstruction such as distal ileal atresia or colonic atresia (►Fig. 3). Understanding formation of meconium and its distribution at different gestational ages in the fetus is essential for understanding the location and type of bowel obstruction.32 Fluid sensitive sequences are also importance in the diagnosis of bowel obstruction as they allow the evaluation of the content of the dilated bowel such as amniotic fluid in proximal atresia, a mixture of fluid with meconium or blood in more distal atresia or urine with meconium in anal atresia with urorectal fistula.36 Congenital abdominal cysts are a common indication for referral for fetal MRI. Both prenatal US and fetal MRI may each play a role in establishing the diagnosis and anatomic relationships of these lesions. Fetal MRI is usually performed when the American Journal of Perinatology

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Fig. 3 Coronal T2-weighted SSFSE image of a fetus at 32 weeks of gestational age with dilated fluid-filled loops of small bowel (A) and sagittal T1weighted GRE image of the same fetus shows an abnormally small rectum consistent with microcolon. (B) Jejunal and ileal atresias were confirmed postnatally. GRE, gradient recalled echo.

cyst is of unclear origin or may result in mass effect on adjacent anatomic structures. In female fetuses, the most common etiology is ovarian cyst. Most studies comparing US to coronal fetal MRI concur that US is sufficient for diagnosis of ovarian cysts.37 If the diagnosis is unclear, fetal MRI helps to define the origin of the cyst, define anatomic extension and adjacent structure compression, and may assist in prenatal planning for postnatal management.38 This is especially the case for cystic lymphatic malformations where the lesion may compress adjacent structures such as the ureters (►Fig. 4). Fetal MRI may also be useful to define anatomical localization in intestinal duplication cysts, renal, and suprarenal cystic lesions.

Renal and Suprarenal Abnormalities US is the standard method to evaluate the fetal kidneys, adrenals, and bladder. The most common abnormality of

the fetal kidneys is renal pelvis dilation. Measurement of the pelvis, and assessment of the ureters and bladder are easily performed by US. Follow-up fetal and postnatal imaging studies are usually indicated. After 20 weeks gestational age, US also provides sufficient resolution to evaluate the corticomedullary differentiation and echogenicity of the kidneys.39 However, in cases of oligohydramnios or obesity in which sonographic evaluation of these structures may be limited, fetal MRI may provide information to inform prognosis and plan postnatal management.40 T2-weighted images are especially useful to demonstrate small subcortical cysts in cases of cystic obstructive dysplasia, which may not be seen on US (►Fig. 5).41 Fetal MRI provides better visualization of renal structural and positional abnormalities, and may provide adjuvant information in cases of hydronephrosis including the degree and extent of dilatation, and the relationship to an ureterocele when present. In the case of suspected bladder

Fig. 4 (A) Ultrasound image of lymphangioma (arrows) in the inguinal area of a fetus at 20 weeks gestational age and (B) fetal MRI of the same fetus at 22 weeks gestational age shows lymphangioma (arrow) extending in the retroperitoneum. MRI, magnetic resonance imaging. American Journal of Perinatology

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Fig. 5 (A) Ultrasound coronal image of a fetal kidney shows slightly increased echogenicity in the upper pole of the right kidney but no cystic changes. (B) Fetal MRI performed the same day shows cystic dysplasia of the upper pole in this duplex kidney (arrow). MRI, magnetic resonance imaging.

exstrophy, MRI may also further delineate associated abnormalities such as those found in cloacal anomalies and the OEIS complex (omphalocele, bladder exstrophy, imperforate anus, and spinal abnormalities).42,43 Bladder distension and wall thickening can be easily seen on US, but when associated with oligohydramnios, the etiology of the bladder outlet obstruction can be difficult to establish. Fetal MRI may be helpful to diagnose megacystis, microcolon, hypoperistalsis syndrome by demonstrating a microcolon on T1-weighted images.34 Over the last several years, fetal MRI has evolved as the image and modality of choice for evaluation of urogenital anomalies. For instance, differentiating between a persistent cloaca, urogenital sinus, and any other abnormality, such as teratoma or anterior myelomeningocele, may be challenging by US. In this setting, absence of normal meconium in the fetal rectum helps confirm the diagnosis of a cloaca. 44 Fetal MRI improves diagnostic accuracy by identifying structures such as the fetal rectum, bladder, dilated vagina, and uterus (►Fig. 6).

Abdominal Wall Anomalies The most common abdominal wall anomalies are omphalocele and gastroschisis. The omphalocele consists of a defect of abdominal wall closure and can be diagnosed as early as at 12 weeks when the bowel re-enters the fetal abdominal cavity in normal fetuses but not in fetuses with omphalocele. While US shows the herniation, the sac content and extent of other anomalies cannot always be established. Giant omphalocele, which has been defined variably, including a defect with more than 75% of liver herniated, is associated with fetal thoracic and lung volume compromise, and poorer outcomes.45,46 Fetal MRI allows for lung volume measurement and assessment of fetal chest shape, which may assist in appropriate prenatal counseling and preparations for postnatal management. Omphalocele has been described in association of multiple congenital abnormalities. Some diagnoses including trisomy 13, 18, and 21 and Beckwith–Wiedemann syndrome among others, require genetic testing. However, fetal MRI may enhance information provided by fetal US

Fig. 6 Single-shot sequences T2-weighted images in the coronal (A) and sagittal (B) planes and a sagittal T1-weighted LAVA image of a cloaca in a fetus at 33 weeks gestational age (C). The images demonstrate a bladder (arrowhead) and a fluid-filled vagina (arrow) with a septum. There is no normal meconium-filled rectum seen on the T1-weighted images. American Journal of Perinatology

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related to abnormalities associated with OEIS, pentalogy of Cantrell (omphalocele, ectopia cordis, diaphragmatic hernia, sternal cleft, and cardiac defect), and others.43,47 In rare cases of rupture of the omphalocele sac, differentiation from gastroschisis is difficult. Fetal MRI and three-dimensional (3D) US may be helpful to better characterize the defect.48 Gastroschisis represents a mesenchymal defect resulting in an abdominal wall defect usually to the right of the umbilical cord. US can routinely reveal lesion location, herniated abdominal contents, and absence of surrounding membrane, which differentiates it from omphalocele. Frequently, the herniated bowel wall appears echogenic and thickened which reflects the inflammatory changes in the bowel wall in contact with the amniotic fluid. Some degree of bowel dilatation and lack of peristalsis is often noted. The herniated bowel injury may be associated with atresia in postnatal life, and as a consequence, with a potential need for bowel resection and subsequent malabsorption.49 Gastroschisis with intra-abdominal bowel dilatation has been reported to be associated with poorer prognosis, thus the level and severity of intra-abdominal dilatation should be considered.50 In rare cases, the severe ischemia of the herniated bowel associated with a small abdominal defect may result in involution of the herniated bowel, intra-abdominal bowel dilatation and short gut syndrome postnatally.51 In approximately 6% of cases, the liver may be also herniated in gastroschisis, which can be difficult to differential from an omphalocele with a ruptured membrane. Fetal MRI may be helpful to evaluate complex cases of gastroschisis. 3D US also plays an important role in the evaluation of abdominal wall anomalies. It is a helpful tool for parental counseling to better illustrate the abdominal abnormality, and also helps localize the cord insertion (►Fig. 7).

Musculoskeletal System Evaluation of bones and soft tissues is part of the fetal screening in the first and second trimester. Femoral length

measurement is one of the parameters for evaluation of the fetal weight and growth. Any suspicion of skeletal dysplasia requires a comprehensive fetal bone skeletal survey to attempt to provide a diagnosis as outcomes are highly variable, in some cases associated with severe disability or perinatal death. The US bone survey should consist of detailed assessment of bone morphology and deformities, measurements, evaluation of the joints, and abnormal ossification centers. Fetal chest-to-abdominal circumference ratio of < 0.6 and/or femur length-to-abdominal circumference ratio of 0.16 or less is strongly suggestive of a perinatal lethal disorder, but there are exceptions.52 3D US has been shown to provide additional information to 2D US for the evaluation of skeletal dysplasia.53,54 Abnormalities of the extremities, such as clubfoot or polydactyly or facial dysmorphias, may be better appreciated on 3D images.54 Low-dose computed tomography (CT) imaging has been shown to be superior to US for diagnosis and classification of skeletal dysplasias. CT images can be processed into 3D reconstructions of the fetal skeleton and provide even better visualization. In a recent series by Victoria et al, US provided correct diagnosis of musculoskeletal dysplasia in 7/21 cases whereas CT was correct in 12/ 21 cases.55 The main limitation of CT use is ionizing radiation exposure to the fetus. With recent progress in dose reduction, images can now be obtained with low exposure to the fetus (3–5 mSv).55,56 In its guidelines for prenatal imaging, The American College of Radiology considers that exposure of less than 50 mSv does not pose a significant risk to the fetus.57 However it is important to remember that radiation exposure is acceptable in pregnancy only in cases where the CT scan provides information crucial for further management of the fetus. It must be used with extreme caution and only in centers with radiologists experienced in this technique. The role of fetal MRI for imaging of musculoskeletal anomalies is still under investigation. Previous studies on animal models have shown the ability of fetal MRI to evaluate skeletal maturation58 and more recently Nemec et al have

Fig. 7 (A) Axial ultrasound two-dimensional (2D) image of the abdomen of a fetus at 19 weeks gestational age with herniated bowel (arrow) consistent with gastroschisis. (B) The 3D image of the same fetus shows the defect to the right of the umbilical cord insertion. American Journal of Perinatology

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Cardiac Imaging US (fetal echocardiography) remains the gold standard for cardiac imaging. At this time there are only limited studies and case reports that suggest added value of fetal MRI, which has primarily been in characterizing associated airways abnormalities.60 MRI of the fetal heart is limited by technical challenges related to performing selective gating of the fetal heart without maternal cardiac interference. Moreover, the resolution of the images is not sufficient at this time to acquire adequately detailed images.61 With increased use of 3 Tesla (3T) fetal MRI and development of new gathering techniques, such as MRI-compatible monitoring of the fetal heart, cardiac fetal MRI may become a tool in the future for the evaluation of congenital cardiac anomalies.

Three-Dimensional Ultrasound 3D US has developed since the mid-1990s, and offers visualization of the fetus in orthogonal planes, parallel planes (tomographic display), 3D surface rendering, and 3D transparent display. 3D US has been shown to be superior to 2D US for the detection of facial abnormalities.62,63 The face may be difficult to evaluate by 2D US due to the fetal position and overall the 2D US detection rates of facial clefting have been reported to be as low as 21 to 30%.64,65 3D US has been shown to improve detection rates of fetal lip and palate abnormalities (►Fig. 8). Since palate clefting may be associated with other abnormalities, careful evaluation of the fetus, particularly of the fetal brain should be performed.66,67 With the availability of 3D US machines, new indications are being developed as complementary to 2D US including diagnosis of limb abnormalities, spinal abnormalities, and abdominal wall anomalies.48,53 First trimester 3D US is technically straightforward due to the large amount of amniotic fluid surrounding the fetus and is increas-

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ingly being used for early diagnosis of abnormalities such as spinal defects, conjoined twins, and some facial anomalies.68,69 With the exception of imaging of facial anomalies with 3D US where recommendations have been provided by the International 3D Focus Group,70 other applications of 3D US are limited to case reports or small studies. Larger systematic investigations are required to further evaluate advantages of 3D US for other specific indications.

Technical Development in Fetal MRI Imaging Compared with US, fetal MRI offers a larger field of view and better tissue contrast. The primary limitations of MRI compared with US include availability and cost. The other limitations of fetal MRI, such as length of the study, sensitivity to motion, and inability to generate real-time images, have been or are being overcome with development of ultrafast pulse sequences and parallel imaging, motion correction sequences, and other technical advances. Most fetal MRI protocols include single-shot T2-weighted images that acquire one slice at a time in very short time frames and steady state balanced sequences that are less sensitive to motion and offer motion sensitive signal, which allows visualization of most of fetal structures. T1-weighted images allow visualization of the meconium in the bowel, liver, and thyroid. The most frequently used sequences are dual echo and gradient recalled echo (GRE) acquisitions. In experienced hands, current sequences allow acquisition of images in a very short time. Images in any plane are obtained one by one in less than 2 seconds with the singleshot sequence whereas GRE sequence acquires the entire fetal body in any plane in less than 30 seconds. Diffusion imaging is based on the Brownian movement of molecules of water in different tissues. Molecules of water will move, for example, less freely in a hypercellular environment compared with their motion in free water. Diffusion imaging can therefore provide information on the intrinsic architecture and composition of a tissue. Diffusion imaging is part of the standard protocol in many institutions for imaging of the fetal brain for assessing parenchymal organization,

Fig. 8 Two three-dimensional ultrasound images of the fetal face shows normal fetal face (A) and a fetus with cleft lip (B).

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demonstrated similar findings in human fetuses.59 The value of fetal MRI for the diagnosis of skeletal dysplasia and other abnormalities over US or CT has still to be established.

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structural developmental abnormalities, and prolonged ischemic events.71 Diffusion imaging in other organs such as fetal lungs and kidneys remains experimental. Investigations of fetal lungs have shown changes in the apparent diffusion coefficient (ADC) with advancing gestational age,72 and in the lungs of fetuses with CDH compared with normal lungs.73 In the kidneys, the ADC values have been shown to slightly decrease with gestational age and may be abnormally decreased in pathologic situations.74 The number of published series is limited. Over the past years, real-time imaging with MRI has been largely developed in children and adults mainly for cardiac MRI imaging but also in musculoskeletal interventional imaging and gastrointestinal imaging. There is also increasing interest in the potential for in-utero applications, particularly for evaluation of fetal swallowing mechanism, neck masses, or for neurological evaluation.75 Real-time MRI may also be helpful to better delineate some structures of the fetal anatomy such as the palate or corpus callosum.76 The evolution of MRI application developments for fetal imaging is often limited by the lack of adequate signal and resolution, given the small size of fetal anatomic structures. This limitation is beginning to be addressed by the emerging utilization of 3T magnet platforms for fetal imaging. Its use was relatively limited to case reports because of concerns for safety and severity of artifacts, more pronounced at higher fields. While issues related to artifacts are still in process of ongoing improvement, the safety of 3T fetal MRI has been presented.70 Of note, imaging using 3T magnet platforms is common, and Food and Drug Administration (FDA) approved for brain imaging of premature neonates. Complications related to MRI in premature newborns have been noted due to hypothermia and respiratory support challenges, but no side effects related to the magnetic field have been reported.77 The energy deposition from MR radio frequency pulses occurs mainly in the form of heat. Specific absorption rate (SAR) is a measure of temperature increase from the protons placed in a magnetic field and undergoing an interaction with radiofrequency stimulation. It is a challenge to provide data on the degree of SAR deposition in vivo but all studies performed on pregnant patient models have concluded that the temperature rise remains within the defined limits. Finally, acoustic noise remains a problem with fetal imaging but seems not to be significantly different between 1.5 and 3T. 3T MRI compared with 1.5T MRI offers higher signal-to-noise ratio, which allows increased image quality, increased spatial or temporal resolution, and wider use of parallel imaging. It opens the door in research, to improve our understanding of human development, and in clinical practice, to improve our diagnosis of congenital abnormalities of the cardiac, musculoskeletal, or neurological systems.

References

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4

5

6 7

8

9

10

11

12

13

14

15

16

17

18

19

1 Colombani M, Rubesova E, Potier A, et al. Management of fetal

mediastinal shift: a practical approach [in French]. J Radiol 2011; 92(2):118–124


2 Lewis DA, Reickert C, Bowerman R, Hirschl RB. Prenatal ultraso-

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nography frequently fails to diagnose congenital diaphragmatic hernia. J Pediatr Surg 1997;32(2):352–356 Zamora IJ, Cass DL, Lee TC, et al. The presence of a hernia sac in congenital diaphragmatic hernia is associated with better fetal lung growth and outcomes. J Pediatr Surg 2013;48(6):1165–1171 Athanasiadis AP, Zafrakas M, Arnaoutoglou C, Karavida A, Papasozomenou P, Tarlatzis BC. Prenatal diagnosis of thoracic kidney in the 2nd trimester with delayed manifestation of associated diaphragmatic hernia. J Clin Ultrasound 2011;39(4):221–224 Ruano R, Lazar DA, Cass DL, et al. Fetal lung volume and quantification of liver herniation by magnetic resonance imaging in isolated congenital diaphragmatic hernia. Ultrasound Obstet Gynecol 2013 Rypens F, Metens T, Rocourt N, et al. Fetal lung volume: estimation at MR imaging-initial results. Radiology 2001;219(1):236–241 Barnewolt CE, Kunisaki SM, Fauza DO, Nemes LP, Estroff JA, Jennings RW. Percent predicted lung volumes as measured on fetal magnetic resonance imaging: a useful biometric parameter for risk stratification in congenital diaphragmatic hernia. J Pediatr Surg 2007;42(1):193–197 Deshmukh S, Rubesova E, Barth R. MR assessment of normal fetal lung volumes: a literature review. AJR Am J Roentgenol 2010; 194(2):W212-7 Victoria T, Bebbington MW, Danzer E, et al. Use of magnetic resonance imaging in prenatal prognosis of the fetus with isolated left congenital diaphragmatic hernia. Prenat Diagn 2012;32(8): 715–723 Gorincour G, Bouvenot J, Mourot MG, et al; Groupe Radiopédiatrique de Recherche en Imagerie Foetale (GRRIF). Prenatal prognosis of congenital diaphragmatic hernia using magnetic resonance imaging measurement of fetal lung volume. Ultrasound Obstet Gynecol 2005;26(7):738–744 Kitano Y, Nakagawa S, Kuroda T, et al. Liver position in fetal congenital diaphragmatic hernia retains a prognostic value in the era of lung-protective strategy. J Pediatr Surg 2005;40(12): 1827–1832 Walsh DS, Hubbard AM, Olutoye OO, et al. Assessment of fetal lung volumes and liver herniation with magnetic resonance imaging in congenital diaphragmatic hernia. Am J Obstet Gynecol 2000; 183(5):1067–1069 Hedrick HL, Danzer E, Merchant A, et al. Liver position and lung-tohead ratio for prediction of extracorporeal membrane oxygenation and survival in isolated left congenital diaphragmatic hernia. Am J Obstet Gynecol 2007;197(4):e1–e4 Kays DW, Islam S, Larson SD, Perkins J, Talbert JL. Long-term maturation of congenital diaphragmatic hernia treatment results: toward development of a severity-specific treatment algorithm. Ann Surg 2013;258(4):638–644, discussion 644–645 Jani J, Keller RL, Benachi A, et al; Antenatal-CDH-Registry Group. Prenatal prediction of survival in isolated left-sided diaphragmatic hernia. Ultrasound Obstet Gynecol 2006;27(1):18–22 Lipshutz GS, Albanese CT, Feldstein VA, et al. Prospective analysis of lung-to-head ratio predicts survival for patients with prenatally diagnosed congenital diaphragmatic hernia. J Pediatr Surg 1997; 32(11):1634–1636 Suda K, Bigras JL, Bohn D, Hornberger LK, McCrindle BW. Echocardiographic predictors of outcome in newborns with congenital diaphragmatic hernia. Pediatrics 2000;105(5):1106–1109 Achiron R, Hegesh J, Yagel S. Fetal lung lesions: a spectrum of disease. New classification based on pathogenesis, two-dimensional and color Doppler ultrasound. Ultrasound Obstet Gynecol 2004;24(2):107–114 Crombleholme TM, Coleman B, Hedrick H, et al. Cystic adenomatoid malformation volume ratio predicts outcome in prenatally diagnosed cystic adenomatoid malformation of the lung. J Pediatr Surg 2002;37(3):331–338


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Rubesova, Barth

20 Levine D, Barnewolt CE, Mehta TS, Trop I, Estroff J, Wong G. Fetal

43 Chen CP, Chang TY, Liu YP, et al. Prenatal 3-dimensional sono-

thoracic abnormalities: MR imaging. Radiology 2003;228(2): 379–388 Barth RA. Imaging of fetal chest masses. Pediatr Radiol 2012;42 (Suppl 1):S62–S73 Azizkhan RG, Crombleholme TM. Congenital cystic lung disease: contemporary antenatal and postnatal management. Pediatr Surg Int 2008;24(6):643–657 Rubesova E, Newman B, Dutta S, Gary EH, Rosenberg J, Barth R. Management of bronchopulmonary malformations: results of the SPR and ESPR survey. Paper presented at: 51st Annual Meeting of the Society for Pediatric Radiology; July 5–October 5, 2008; Scottsdale, AZ Solt I, Rotmensch S, Bronshtein M. The esophageal ’pouch sign’: a benign transient finding. Prenat Diagn 2010;30(9):845–848 Salomon LJ, Sonigo P, Ou P, Ville Y, Brunelle F. Real-time fetal magnetic resonance imaging for the dynamic visualization of the pouch in esophageal atresia. Ultrasound Obstet Gynecol 2009; 34(4):471–474 Mong A, Johnson AM, Kramer SS, et al. Congenital high airway obstruction syndrome: MR/US findings, effect on management, and outcome. Pediatr Radiol 2008;38(11):1171–1179 Bouchard S, Johnson MP, Flake AW, et al. The EXIT procedure: experience and outcome in 31 cases. J Pediatr Surg 2002;37(3): 418–426 Nyberg DA, Dubinsky T, Resta RG, Mahony BS, Hickok DE, Luthy DA. Echogenic fetal bowel during the second trimester: clinical importance. Radiology 1993;188(2):527–531 Mailath-Pokorny M, Klein K, Klebermass-Schrehof K, Hachemian N, Bettelheim D. Are fetuses with isolated echogenic bowel at higher risk for an adverse pregnancy outcome? Experiences from a tertiary referral center. Prenat Diagn 2012;32(13):1295–1299 Chan KL, Tang MH, Tse HY, Tang RY, Tam PK. Meconium peritonitis: prenatal diagnosis, postnatal management and outcome. Prenat Diagn 2005;25(8):676–682 Biyyam DR, Dighe M, Siebert JR. Antenatal diagnosis of intestinal malrotation on fetal MRI. Pediatr Radiol 2009;39(8):847–849 Rubesova E. Fetal bowel anomalies—US and MR assessment. Pediatr Radiol 2012;42(Suppl 1):S101–S106 Brugger PC, Prayer D. Fetal abdominal magnetic resonance imaging. Eur J Radiol 2006;57(2):278–293 Veyrac C, Couture A, Saguintaah M, Baud C. MRI of fetal GI tract abnormalities. Abdom Imaging 2004;29(4):411–420 Saguintaah M, Couture A, Veyrac C, Baud C, Quere MP. MRI of the fetal gastrointestinal tract. Pediatr Radiol 2002;32(6):395–404 Lubusky M, Prochazka M, Dhaifalah I, Horak D, Geierova M, Santavy J. Fetal enterolithiasis: prenatal sonographic and MRI diagnosis in two cases of urorectal septum malformation (URSM) sequence. Prenat Diagn 2006;26(4):345–349 Nemec U, Nemec SF, Bettelheim D, et al. Ovarian cysts on prenatal MRI. Eur J Radiol 2012;81(8):1937–1944 Gupta P, Sharma R, Kumar S, et al. Role of MRI in fetal abdominal cystic masses detected on prenatal sonography. Arch Gynecol Obstet 2010;281(3):519–526 Chaumoitre K, Brun M, Cassart M, et al. Differential diagnosis of fetal hyperechogenic cystic kidneys unrelated to renal tract anomalies: A multicenter study. Ultrasound Obstet Gynecol 2006;28(7): 911–917 Cassart M, Massez A, Metens T, et al. Complementary role of MRI after sonography in assessing bilateral urinary tract anomalies in the fetus. AJR Am J Roentgenol 2004;182(3):689–695 Cerwinka WH, Damien Grattan-Smith J, Kirsch AJ. Magnetic resonance urography in pediatric urology. J Pediatr Urol 2008;4(1): 74–82, quiz 82–83 Calvo-Garcia MA, Kline-Fath BM, Rubio EI, Merrow AC, Guimaraes CV, Lim FY. Fetal MRI of cloacal exstrophy. Pediatr Radiol 2013; 43(5):593–604

graphic and MRI findings in omphalocele-exstrophy-imperforate anus-spinal defects complex. J Clin Ultrasound 2008;36(5): 308–311 Chauvin NA, Epelman M, Victoria T, Johnson AM. Complex genitourinary abnormalities on fetal MRI: imaging findings and approach to diagnosis. AJR Am J Roentgenol 2012;199(2):W222-31 Biard JM, Wilson RD, Johnson MP, et al. Prenatally diagnosed giant omphaloceles: short- and long-term outcomes. Prenat Diagn 2004;24(6):434–439 Danzer E, Victoria T, Bebbington MW, et al. Fetal MRI-calculated total lung volumes in the prediction of short-term outcome in giant omphalocele: preliminary findings. Fetal Diagn Ther 2012; 31(4):248–253 McMahon CJ, Taylor MD, Cassady CI, Olutoye OO, Bezold LI. Diagnosis of pentalogy of cantrell in the fetus using magnetic resonance imaging and ultrasound. Pediatr Cardiol 2007;28(3): 172–175 Grigore M, Iliev G, Gafiteanu D, Cojocaru C. The fetal abdominal wall defects using 2D and 3D ultrasound. Pictorial essay. Med Ultrasound 2012;14(4):341–347 Kassa AM, Lilja HE. Predictors of postnatal outcome in neonates with gastroschisis. J Pediatr Surg 2011;46(11):2108–2114 Nick AM, Bruner JP, Moses R, Yang EY, Scott TA. Second-trimester intra-abdominal bowel dilation in fetuses with gastroschisis predicts neonatal bowel atresia. Ultrasound Obstet Gynecol 2006; 28(6):821–825 Anveden-Hertzberg L, Gauderer MW. Paraumbilical intestinal remnant, closed abdominal wall, and midgut loss in a neonate. J Pediatr Surg 1996;31(6):862–863 Krakow D, Lachman RS, Rimoin DL. Guidelines for the prenatal diagnosis of fetal skeletal dysplasias. Genet Med 2009;11(2): 127–133 Muscatello A, Mastrocola N, Di Nicola M, Patacchiola F, Carta G. Correlation between 3D ultrasound appearance and postnatal findings in bilateral malformations of the fetal hands. Fetal Diagn Ther 2012;31(2):138–140 Wu CJ, Huang KH, Liu JY. Prenatal 2D and 3D ultrasound diagnosis of radial ray defects. Int J Gynaecol Obstet 2011;113(2):158–159 Victoria T, Epelman M, Coleman BG, et al. Low-dose fetal CT in the prenatal evaluation of skeletal dysplasias and other severe skeletal abnormalities. AJR Am J Roentgenol 2013;200(5):989–1000 Macé G, Sonigo P, Cormier-Daire V, et al. Three-dimensional helical computed tomography in prenatal diagnosis of fetal skeletal dysplasia. Ultrasound Obstet Gynecol 2013;42(2):161–168 McCollough CH, Schueler BA, Atwell TD, et al. Radiation exposure and pregnancy: when should we be concerned? Radiographics 2007;27(4):909–917, discussion 917–918 Connolly SA, Jaramillo D, Hong JK, Shapiro F. Skeletal development in fetal pig specimens: MR imaging of femur with histologic comparison. Radiology 2004;233(2):505–514 Nemec SF, Nemec U, Brugger PC, Wadhawan I, Prayer D. Skeletal development on fetal magnetic resonance imaging. Top Magn Reson Imaging 2011;22(3):101–106 Sun HY, Boe J, Rubesova E, Barth RA, Tacy TA. Fetal MRI Correlates with Postnatal CT Angiogram Assessment of Pulmonary Anatomy in Tetralogy of Fallot with Absent Pulmonary Valve. Congenit Heart Dis 2013 Manganaro L, Savelli S, Di Maurizio M, et al. Potential role of fetal cardiac evaluation with magnetic resonance imaging: preliminary experience. Prenat Diagn 2008;28(2):148–156 Hata T, Yonehara T, Aoki S, Manabe A, Hata K, Miyazaki K. Threedimensional sonographic visualization of the fetal face. AJR Am J Roentgenol 1998;170(2):481–483 Merz E, Abramovicz J, Baba K, et al. 3D imaging of the fetal face recommendations from the International 3D Focus Group. Ultraschall Med 2012;33(2):175–182

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Sensitivity and specificity of routine antenatal screening for congenital anomalies by ultrasound: the Belgian Multicentric Study. Ultrasound Obstet Gynecol 1991;1(2):102–110 Crane JP, LeFevre ML, Winborn RC, et al; The RADIUS Study Group. A randomized trial of prenatal ultrasonographic screening: impact on the detection, management, and outcome of anomalous fetuses. Am J Obstet Gynecol 1994;171(2):392–399 Johnson DD, Pretorius DH, Budorick NE, et al. Fetal lip and primary palate: three-dimensional versus two-dimensional US. Radiology 2000;217(1):236–239 Chmait R, Pretorius D, Moore T, et al. Prenatal detection of associated anomalies in fetuses diagnosed with cleft lip with or without cleft palate in utero. Ultrasound Obstet Gynecol 2006;27(2):173–176 Pooh RK, Kurjak A. 3D/4D sonography moved prenatal diagnosis of fetal anomalies from the second to the first trimester of pregnancy. J Matern Fetal Neonatal Med 2012;25(5):433–455 Murphy A, Platt LD. First-trimester diagnosis of body stalk anomaly using 2- and 3-dimensional sonography. J Ultrasound Med 2011;30(12):1739–1743 Victoria T, Roberts T, Johnson A, et al. Fetal MRI—jumping from 1.5 to 3 tesla MRI: preliminary experience. Paper presented at: 55th Annual Meeting of the Society for Pediatric Radiology; April 16– 20, 2012; San Antonio, TX


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71 Kasprian G, Del Río M, Prayer D. Fetal diffusion imaging: pearls and

solutions. Top Magn Reson Imaging 2010;21(6):387–394 72 Manganaro L, Perrone A, Sassi S, et al. Diffusion-weighted MR

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imaging and apparent diffusion coefficient of the normal fetal lung: preliminary experience. Prenat Diagn 2008;28(8):745–748 Cannie M, Jani J, De Keyzer F, Roebben I, Dymarkowski S, Deprest J. Diffusion-weighted MRI in lungs of normal fetuses and those with congenital diaphragmatic hernia. Ultrasound Obstet Gynecol 2009;34(6):678–686 Chaumoitre K, Colavolpe N, Shojai R, Sarran A, D’ Ercole C, Panuel M. Diffusion-weighted magnetic resonance imaging with apparent diffusion coefficient (ADC) determination in normal and pathological fetal kidneys. Ultrasound Obstet Gynecol 2007; 29(1):22–31 Houshmand G, Hosseinzadeh K, Ozolek J. Prenatal magnetic resonance imaging (MRI) findings of a foregut duplication cyst of the tongue: value of real-time MRI evaluation of the fetal swallowing mechanism. J Ultrasound Med 2011;30(6):843–850 Levine D, Cavazos C, Kazan-Tannus JF, et al. Evaluation of real-time single-shot fast spin-echo MRI for visualization of the fetal midline corpus callosum and secondary palate. AJR Am J Roentgenol 2006; 187(6):1505–1511 Plaisier A, Raets MM, van der Starre C, et al. Safety of routine early MRI in preterm infants. Pediatr Radiol 2012;42(10):1205–1211


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