Applied Radiology

Dr. Berggruen received her medical degree from Loyola Stritch School of Medicine, Maywood, IL, in 1998. She is a fourth-year resident at the University of Arizona Health Sciences Center, Tucson, AZ. Next year she will begin an MRI Body fellowship at Northwestern Memorial Hospital, Chicago, IL.

Ultrasound (US) is the screening method of choice for prenatal imaging; however, there are cases in which US is equivocal. In those cases, ultrafast prenatal magnetic resonance imaging (MRI) is an important complementary means of investigation. Prenatal MRI is helpful at improving the anatomic definition, clarifying the diagnosis, and identifying associated abnormalities. This information facilitates family counseling for prenatal and perinatal management.

Ultrasound (US) continues to be the screening method of choice for prenatal imaging because of its widespread availability, real-time capability, low cost, and safety. The quality of the examination is dependent on the equipment and skill of the examiner. In most cases, the findings on US are decisive. There are cases, however, in which the findings are equivocal or diagnostic information is insufficient, including pregnancies complicated by maternal obesity, oligohydramnios, or an unusual fetal lie. In such cases, the availability of another imaging technique, such as magnetic resonance imaging (MRI), may prove beneficial.

Until recently, T2-weighted MRI acquisition times of several minutes made it necessary to sedate the fetus directly through the umbilical cord or sedate the mother. The development of ultrafast T2-weighted MRI makes it possible to obtain images of good quality, enhancing fetal anatomic evaluation without sedation. Prenatal MRI is helpful in improving the anatomic definition, clarifying the diagnosis, and identifying other associated abnormalities, particularly before fetal surgical intervention.

Techniques

MRI gradient systems with higher slew rates and gradient amplitude have allowed newer pulse sequences, including single-shot half-Fourier T2-weighted images and echo planar imaging. Single-shot fast-spin echo (or HASTE [half-Fourier acquisition single-shot turbo-spin echo]) images were the first type of sequence to obtain high quality T2-weighted spin-echo images in a single breath-holding period. Single-shot fast-spin echo sequences achieve relatively motion-free breath-hold images in the pelvis or abdomen with T2-weighted tissue contrast similar to conventional fast-spin echo images. Obtaining planes that represent anatomic cross sections relative to the fetus facilitates examination of the fetus with HASTE imaging. ¹ Gadolinium is not used in fetal MRI as it crosses the placenta and is not cleared from fetal circulation. The effect of gadolinium on the fetus is not known. ²

Fetal brain

In a study by Laveaucoupet et al, ³ the usefulness of fetal MRI in ischemic brain injury was demonstrated in seven cases of fetal brain ischemia that was suspected on US and confirmed by fetal MRI. The abnormalities suspected on US included ventricular dilatation (n = 3), microcephaly (n = 1), twin pregnancy with in utero death of a twin and suspected cerebral lesion in surviving twin (n = 3). MRI diagnosed hydranencephaly (n = 1), multicystic encephalomalacia (n = 2) (figure 1), unilateral capsular ischemia (n = 1), porencephaly (n = 2) (figure 2), and corpus callosum and cerebral atrophy (n = 1). US and MR images were compared with pathologic findings or postnatal imaging. In comparison to US, visualization of fetal brain anomalies was superior with MRI, which provided a more precise diagnosis. These seven cases demonstrated that MRI could be an important complementary means of investigation when pathology is suspected during prenatal US.

Many pathologic conditions throughout gestation may compromise materno-fetal circulation and lead to hemorrhagic or ischemic injuries in the fetal brain. In the second trimester, the fetal brain responds to trauma by liquefaction of destroyed parenchyma resulting in cavities: multicystic encephalomalacia, porencephaly, and hydranencephaly are terms that describe patterns of cavitation. The more mature brain reacts to an insult by astrocytic proliferation or gliosis. ³

MRI allows visualization of the entire fetal brain, which sometimes is not possible by US, especially in fetuses with ventricular dilatation. MRI provides better soft-tissue contrast than US, and therefore evaluates extension of lesions into the cerebral parenchyma. However, MRI may not detect subtle ischemic lesions such as gliosis, microcalcifications, and microthrombi associated with isolated ventricular dilatation. ³

In a study by Wagenvoort et al, ⁴ MR images were reviewed to determine if MRI could give additional information in prenatal diagnosis of congenital anomalies in cases in which US analysis was not conclusive. In this study, in which MR images were reviewed with US knowledge, MRI supplied additional information in 10 of 19 cases referred due to equivocal findings of brain anomalies on US. MRI was provided a confirmative diagnosis for six patients (31.6%). One exam was false negative; MRI did not show periventricular leukomalacia (PVL) or hemorrhage while vaginal US did suggest PVL. In 5 of 10 cases referred for ventriculomegaly, MRI discovered other anomalies (figure 3).

Sonography of posterior fossa anatomy may be difficult because of fetal skull shadowing or engaging of the fetal head in the third trimester of pregnancy. In three patients referred for cerebellar anomalies, a correct diagnosis was made with fetal MRI. ⁴ In a study by Quinn et al, ⁵ MRI excluded a suspected Dandy-Walker malformation in a fetus with agenesis of the corpus callosum, a difficult diagnosis to make accurately by US. In contrast to US, MRI allowed for the correct identification of posterior fossa anatomy in third-trimester fetuses. ⁶ Evaluation of the posterior fossa on US often depends on a single angled axial view through the cerebellar hemispheres and region of the cisterna magna. The cisterna magna may appear artificially enlarged or the shape of the hemispheres may appear abnormal. MRI markedly improves visualization of the posterior fossa because direct coronal, sagittal, and axial images can be obtained, thereby confirming anatomy of the vermis and fourth ventricle. MRI usually can identify the typical findings of a Chiari malformation. ²

Holoprosencephaly is a malformation of the prosencephalon with failure of normal midline cleavage and incomplete midfacial development. MRI is most helpful in trying to distinguish a mild or lobar form of holoprosencephaly from other forms of ventriculomegaly and hydranencephaly, which is a severe failure of brain formation, secondary to ischemic event. ^7,8 In a study evaluating central nervous system (CNS) anomalies by Ohgiya et al, ⁶ US findings were suggestive of, but not definitive, for anencephaly. MRI was helpful in defining a large amount of angiomatous stroma and absence of normal calvaria. The information about the CNS deformity was helpful to the parents considering a pregnancy termination.

Normal gyral patterns, ventricular size, and patterns of neuronal migration have all been documented by MRI. ⁹ Sulcal development is a marker of cortical maturation and fetal maturity. In a MRI study of 93 fetuses, Levine and Barnes ¹⁰ found that sulcation appeared in the order predicted by anatomic studies, but with a lag of up to 8 weeks (mean 1.9 weeks). The first to form is the interhemispheric fissure, present in all normal fetuses studied at 14 weeks. The Sylvian fissure becomes grooved by 16 weeks. Beginning at approximately 29 weeks in utero, myelination progresses cephalad from the spinal cord and is not complete until about the second year of life. ^11,12 Myelination accounts for signal intensity differences between the different regions of the brain. In a study by Lan et al, ¹³ evaluation of 25 normal fetuses showed that only two layers could be discerned after 29 weeks: an inner hyperintense layer (the white matter) and an outer hypointense layer (the gray matter). The corpus callosum is fully formed by 20 weeks. The basal ganglia and thalami are best seen after 26 weeks.

In a review of 128 fetuses referred for non-CNS indications, no fetus was found with an atrial diameter exceeding 10 mm on MRI. ¹⁴ The 10-mm rule, described on a sonographic axial view of the fetal atrium, is therefore the measurement used as the upper limit of normal on MRI. The cavum septum pellucidum is seen in all normal fetuses. ¹⁴

Previously, abnormalities of neuronal migration were believed to be rare; however, with MRI, they are seen in up to 20% of cases of CNS anomalies. In one report, MRI was able to visualize areas of neuronal heterotopias in 54% of fetuses with a definite diagnosis of migrational disorder. MRI demonstrated 80% of lissencephaly, 73% of polymicrogyria, and 100% of schizencephaly prenatally. ⁷

In a study by Enomoto et al, ¹⁵ 121 fetuses were imaged to determine the predictive value of prenatal MRI for evaluation of fetal brain anomaly and other pathology. The degree of cortical convolution and ventricular size were used as landmarks to assess the fetal brains of different gestational age, together with the degree of myelination and presence of parenchymal signal abnormality in the group of late gestation. The subjects were divided into 99 with normal findings and 22 with abnormalities. In normal subjects, the ventricles ceased to dilate after 25 weeks. The convolutional development increased after 30 weeks and a primitive form of the cerebral surface was detected at 32 weeks. The myelination started in the brain stem and internal capsules between 22 and 25 weeks. The abnormalities found included anencephaly, holoprosencephaly, Chiari malformation, ventriculomegaly, cephalocele, Dandy-Walker syndrome, and hypogenesis of the corpus callosum. Five autopsy cases and 17 postnatal imaging cases confirmed the abnormalities. Focal encephalomalacia, abnormal configuration of the ventricles, heterotopia, and callosal and posterior fossa anomalies were delineated clearly on MRI.

Neck masses

In a study of 3 cases, fetal MRI was instrumental in evaluating the anatomic extent of giant neck masses with potential airway obstruction. ⁵ In contrast to US, anatomic details about location and impingement of the fetal airway and neck vessels by lesions that rivaled the fetus in volume were better seen with MRI. Cervical teratoma could be differentiated from cystic hygroma on MRI. In each case, fetal MRI helped in the prenatal assessment of the mass before cesarean delivery using an ex-utero intrapartum therapy (EXIT) procedure to establish an airway. Compared with US exams in which only a small part of the lesion may be present in the acoustic window, the whole lesion and its anatomic relations could be reviewed on MRI.

Lungs

Lungs show moderately high signal intensity on T2-weighted images. ⁴ Congenital diaphragmatic hernia (CDH) is the most common fetal chest mass, usually occurring on the left side. US differentiation of bowel loops from other chest masses is sometimes difficult. The US determination of liver herniation is not always possible because it relies on indirect signs. ⁶ Evaluating liver position on US may be difficult, as the echo texture of the liver and lung is similar. Estimations of the residual lung area are not always possible by US. With MRI, it can be easy to depict the herniated bowel and the position of the liver and to distinguish meconium-filled bowel from normal lung because of the difference in signal intensity. On T1-weighted images, meconium-filled bowel is very high in signal intensity, making the position of bowel above or below the diaphragm easy to evaluate. ²

In a study by Quinn et al, ⁵ fetal surgery candidates undergoing evaluation for a congenital anomaly that was potentially a correctable lesion were selected for MRI. The diagnoses included: CDH (n = 14) and lung masses (n = 4). The results of the US exam were known at the time of the MRI study on the same day. All diagnoses were confirmed after delivery by radiographic imaging, operation, or autopsy. With CDH, MRI demonstrated liver herniation into the chest in 11 of 14 cases. The information included the amount and location of bowel, stomach, and liver herniated into the fetal thorax. The degree of liver herniation was substantial in six cases, in which a third or more of the fetal liver was intrathoracic. MRI was able to identify bilateral CDH in one fetus. In four cases, US findings had not been definitive. In two cases of CDH detected by MRI, the primary diagnosis by US was congenital cystic adematoid malformation (CCAM) based on the presence of nonperistaltic bowel in the chest that may appear as a multicystic lesion similar to a CCAM on US.

Despite advances in sonography and color Doppler imaging, the prenatal diagnosis of anomalies such as CDH is difficult and has been missed in 41% of cases in one recent retrospective study. ¹⁶ The mortality in CDH relates to the degree of pulmonary hypoplasia and associated pulmonary hypertension and has been estimated to be as high as 58%. Differentiating between chest masses, such as CCAM and bronchopulmonary sequestration (BPS), by US can be difficult. Fetal MRI provided more anatomic detail than US regarding extent and location of the chest masses that included BPS (n = 2), and CCAM (n = 2). In many cases, the lobe of the lung involved with the lesion could be identified. ⁵

Pulmonary hypoplasia is a condition that causes high mortality and morbidity in neonates. The prenatal diagnosis of pulmonary hypoplasia assists with the postnatal care. In a study by Kuwashima et al, ¹⁷ the diagnostic capabilities of fetal MRI in pulmonary hypoplasia were evaluated. Subjects included 23 fetuses. A diagnosis of pulmonary hypoplasia was made on the basis of perinatal physical, surgical, and/or autopsy findings. With regard to pulmonary hypoplasia, the subjects were divided into three groups--1a: infants with pulmonary hypoplasia and perinatal death (n = 8), including 5 who underwent autopsy; 1b: infants with pulmonary hypoplasia and longer survival over the neonatal period (n = 2); and 2: infants without pulmonary hypoplasia (n = 13). On MRI, all fetuses in groups 1a and 1b showed low signal intensity of the lung, obscured pulmonary vessels, and a small thorax. All fetuses in group 2, except for one fetus at 24 weeks gestation, showed homogeneously high signal intensity in the lung and well-defined pulmonary vessels.

In another study, Shinmoto et al ¹⁸ investigated normal fetal lung growth and correlated the estimated lung volume with clinical outcome in 90 fetuses (58 with normal lungs and 32 with suspected pulmonary hypoplasia) who underwent MRI including volumetric lung measurement. The gestational age ranged from 21 to 38 weeks. The lung volume was calculated by multiplying total lung area and slice thickness. The measured fetal lung volumes were correlated with gestational age and other parameters of fetal size such as crown-rump length (CRL). The calculated percentages of lung volume were well correlated with neonatal respiratory condition and Apgar scores. The volumetric measurement of fetal lung was valuable in that the relative fetal lung volume was correlated with neonatal respiratory conditions.

Abdomen/pelvis

Fetal renal anomalies often are associated with oligohydramnios, a condition that makes fetal US difficult. MRI is not greatly affected by decreased amniotic fluid. ² A study by Caire et al ¹⁹ was designed to evaluate the usefulness of MRI in suspected congenital fetal genitourinary anomalies. ¹⁶ Assessments were made of amniotic fluid; location, size and presence of kidneys; bladder appearance; and evaluation of the perineum. MRI findings were compared with US and neonatal diagnosis. MRI changed the diagnosis in 4 of 15 cases. Oligohydramnios or anhydramnios was present in 8 of 15 cases; this did not hinder MRI visualization of genitourinary anomalies. Visualization of bladder and kidneys was possible after 18 weeks. MRI also provided better anatomic detail of the perineum. ¹⁹

Multicystic dysplastic kidney (MCDK) may be confused with hydronephrosis on US. MRI, confirming the absence of normal renal parenchyma and renal pelvis, can diagnose MCDK. ¹⁴ Although primary hepatic tumors are uncommon, hamartomas, hemangoendotheliomas, and hepatoblastomas do occur in the fetus. MRI helps differentiate these masses based on morphology. In addition, MRI can be used to differentiate abdominal masses and other cystic structures, such as mesenteric cysts, lymphangiomas, and ovarian cysts, from dilated loops of bowel. ² With huge abdominal masses, such as mesenteric cyst and lymphangioma, MRI clarified the diagnosis in 14 of 31 (45%) patients who underwent fetal treatment after US and MRI. ⁵

Twin pregnancy

When assessing twin anomalies by US, the problems of multiple fetuses in the field, fetal lie, and aberrant anatomy can create diagnostic confusion. MRI allowed anatomic refinement of the US diagnosis of twin-twin transfusion syndrome. The placental anatomy and cord insertion sites were delineated for preoperative planning for cord legation or placental vessel laser ablation. ⁵

Safety

To date, no known harmful effects to the developing fetus have been documented using clinical MR scanners. One long-term study evaluated 20 children who had undergone fetal MRI after 21 weeks gestation. After 3 years, there was no demonstrable increase in occurrence of disease or disabilities. ²⁰ In 1991, the safety committee of the Society for Magnetic Resonance Imaging issued guidelines for patient safety. ²¹ The guidelines recommended that patients be informed that there has been no indication that the use of clinical MRI during pregnancy has produced deleterious effects; however, safety has not been proven to date. ²

Conclusion

As further improvements in MRI technology yield faster scan times and higher resolution, the applications for fetal imaging will increase. Presently, MRI is an adjunct to good prenatal US. It can provide significant additional information that can affect prenatal counseling, prenatal intervention, and delivery planning.