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ORIGINAL RESEARCH |
From the Departments of Radiology and Obstetrics and Gynecology, Beth Israel Deaconess Medical Center, Boston; and the Departments of Radiology and Neurosurgery, Children’s Hospital, Boston, Massachusetts.
Address reprint requests to: Deborah Levine, MD, Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston, MA 02215, E-mail: dlevine{at}caregroup.harvard.edu
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Abstract |
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Methods: Between May 1, 1996, and March 26, 1999, 83 women with 90 fetuses (including seven sets of live twins) had 91 ultrasonographic and MRI examinations of the fetal CNS. Eight women were studied twice, one for two different indications. If referrals came from outside our institution, a confirmatory sonogram was obtained. Indications for examination were ventriculomegaly (n = 25), suspected neural tube defect (n = 16), arachnoid cyst (n = 12), large cisterna magna (n = 11), and miscellaneous indications (n = 20).
Results: Magnetic resonance imaging findings led to changed diagnoses in 26 (40%) of 66 fetuses with abnormal confirmatory sonograms. Magnetic resonance imaging findings not found by ultrasound included partial or complete agenesis of the corpus callosum (n = 11), porencephaly (n = 6), hemorrhage (n = 5), tethered cord (n = 3), cortical gyral abnormality (n = 2), cortical cleft (n = 2), midbrain abnormality (n = 2), and partial or complete agenesis of the septi pellucidi (n = 3), as well as holoprosencephaly, cerebellar hypoplasia, subependymal and cortical tubers, vascular malformation, and vermian cysts (one case each). Abnormalities better delineated by MRI than ultrasound included three cephaloceles, a dural arteriovenous malformation, one distal sacral neural tube defect, and the mass effect of three arachnoid cysts. That information was used to alter patient counseling and at times management.
Conclusion: When a CNS anomaly is detected by sonography or suspected on ultrasound, MRI findings might lead to altered diagnosis and patient counseling.
Central nervous system (CNS) abnormalities affect approximately 6000 neonates each year in the United States.1 Sonography is the standard approach for evaluating those anomalies prenatally. However, the success of sonographic evaluation of the fetal CNS is hindered by the nonspecific appearance of some anomalies and technical factors that make viewing the brain near the transducer difficult and viewing the posterior fossa difficult late in gestation, and subtle parenchymal abnormalities frequently cannot be visualized sonographically. Because of those limitations, magnetic resonance imaging (MRI) has been suggested as a useful adjunct in cases in which sonographic findings are nonspecific.2,3
Early studies of MRI to evaluate fetal morphology were limited by fetal motion.4 The half-Fourier acquisition single-shot turbo spin-echo sequence is a fast MRI technique used to depict fetal anatomy.3,5–7 Half-Fourier acquisition single-shot turbo spin-echo imaging can produce T2-weighted images in 430 milliseconds, effectively eliminating artifact from maternal and fetal motion.7 Several studies addressed the ability of MRI to provide additional information in cases of suspected CNS abnormalities on ultrasound.2,8,9 However, no large studies in the obstetric literature have evaluated systematically the types of anomalies for which MRI findings are most likely to influence care. This study was done to identify types of fetal CNS anomalies detected sonographically for which MRI is likely to lead to changes in patient counseling or management.
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Materials and Methods |
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We assessed degree of ventriculomegaly using the sonographic measurement of the maximum width of the atrium of the lateral ventricle. Ventriculomegaly was considered mild when this measurement was 10–15 mm, moderate when it was at least 15 mm but there was still more than 3 mm of cortical mantle, and severe when there was no more than 3 mm of visible cortical mantle.
After screening for contraindications, we performed MRI examinations with a 1.5-T superconductive system (Siemens Vision, Erlangen, Germany), using the Half-Fourier acquisition single-shot turbo spin-echo technique described previously.3 Contiguous slices were used early in our series. Later, acquisitions were interleaved with an interslice gap equal to that of the slice thickness, to minimize inadvertent radiofrequency excitation of adjacent sections. When hemorrhage was suspected, T1-weighted imaging was done using a fast low-angle shot technique.
Magnetic resonance images were reviewed at the time of acquisition by one of the authors (DL or TM), who knew the sonographic diagnoses. Magnetic resonance images were reviewed subsequently by a second author (PDB). An attempt was made to review all films prospectively and before delivery. However, early in the series the reviews of two cases were not complete until after delivery. Images of fetal anatomy also were evaluated for defects outside the CNS.
Women and their referring physicians were informed of the results of confirmatory sonography and MRI, with the caveat that the prenatal MRI was experimental and of unproved accuracy in terms of diagnosis of CNS anomalies. Referring physicians were asked how the additional information provided by MRI changed management or counseling. Because patient management is affected by many variables, the influence on counseling was used as an outcome, unless a clear management change occurred.
Definitive diagnostic procedures were postnatal imaging (MRI: n = 15; ultrasound: n = 23; angiography: n = 1; and plain film radiography: n = 4), surgery (n = 15), postnatal physical examination (n = 11), and autopsy (n = 7). Prenatal MRI findings were taken as definitive diagnoses in 16 cases in which postnatal imaging, surgery, or autopsy findings were not available, two cases in which ultrasonography was done postnatally but MRI findings were not expected to be found sonographically, and in four ongoing pregnancies. When abnormalities were present postnatally but not diagnosed by prenatal imaging, two radiologists and a pediatric neurosurgeon decided, by consensus, whether the disparity represented a prenatal-imaging false-negative finding.
Abnormalities on ultrasound and magnetic resonance images and definitive diagnoses were coded with the use of the classification of congenital cerebral, cerebellar, and spinal malformations described by van der Knaap and Valk.10 The sonographic, prenatal MRI, and definitive diagnoses were compared. Any changes in findings or diagnosis were specified. A change in diagnosis was graded as a major change (new finding unsuspected on ultrasound or a change in diagnosis of anomaly), a minor change (slightly different diagnosis without a change in classification of anomaly), or no change.
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Sixty-six fetuses had abnormal findings on confirmatory sonograms. MRI showed two minor and 35 major additional findings in 26 fetuses (Tables 1
and 2; Figures 1–5). In 38 (57.6%) of 66 cases involving abnormal confirmatory sonograms, MRI yielded additional information that clearly changed counseling. Confirmatory sonogram and MRI findings were given to referring clinicians simultaneously, so there were many cases in which more confident diagnoses were made by MRI; however, those MRI findings were not considered to have instigated changes in counseling unless MRI clearly added information beyond that available with ultrasound, other than images of normal structures that were assumed to be present sonographically.
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There was one case of a potential MRI misdiagnosis. A 22-week fetus had an enlarged cisterna magna and an MRI diagnosis of agenesis of the corpus callosum. The corpus callosum was not examined directly at the time of brain cutting. Slides showed at least a portion of the corpus callosum, but it was difficult to tell whether the fibers were running in a normal direction.
Defects outside the CNS that were visualized on ultrasound and MRI included (one fetus each) unilateral hydroureteronephrosis; ureteropelvic junction obstruction; omphalocele and cleft lip; omphalocele, rocker-bottom feet, clenched fists, and pleural effusion; absent stomach; bilateral club feet; scoliosis; and two-vessel cord. Anomalies outside the CNS seen on MRI but not on ultrasound included pelvic kidneys (two fetuses). Anomalies that were visualized better on MRI than ultrasound included situs ambiguous, midline heart, and right-sided stomach in the fetus of the obese woman in whom the fetal chest and abdomen were not visualized adequately sonographically; and cloacal malformation in a fetus with oligohydramnios. Magnetic resonance imaging did not characterize adequately three cardiac abnormalities that were visualized sonographically: a ventricular septal defect in a fetus with tetrology of Fallot, a small aorta in a fetus with aortic stenosis, and a cardiac rhabdomyoma. Magnetic resonance imaging did not visualize adequately the umbilical vein in a fetus with persistent right umbilical vein. Findings missed on ultrasound and MRI included a small cleft palate without cleft lip in a fetus with agenesis of the corpus callosum; truncus arteriosus, ventriculoseptal defect, hypertelorism, low-set ears, and thymic agenesis in a 16 week fetus with DiGeorge syndrome; scoliosis with dural ectasia in a fetus with an arachnoid cyst; and situs inversus totalis and a small ventriculoseptal defect and hypoplastic sacrum in a fetus with severe scoliosis. Findings outside the CNS did not lead to altered management in any case.
In one case, the postnatal sonogram showed a grade 1 germinal matrix hemorrhage at birth, which we believed was a recent event and therefore was not considered missed by prenatal imaging. The infant had a normal head ultrasound at 7 months of age. One fetus had a small choroid plexus papilloma, diagnosed 16 months after birth. In that case, the degree of ventriculomegaly in utero (which did not decrease postoperatively) was not believed to be caused by the choroid plexus papilloma.
There were seven chromosomal abnormalities, including three trisomy 21, one trisomy 18, one translocation of chromosome 20, one translocation of chromosome 22, and one 7p duplication.
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Isolated mild ventriculomegaly is considered present when the transverse atrial measurement is 10–15 mm,13 and this form of ventriculomegaly is associated with other anomalies, neuronal and somatic, in 70–85% of cases. Several studies have shown that anomalies occurring in conjunction with enlarged ventricles (rather than degree of ventricular dilatation) account for most morbidity and mortality.13,14 Therefore, the sonographic finding of fetal ventriculomegaly prompts a careful search for other CNS anomalies and anomalies outside the CNS. False-negative rates for detecting associated anomalies in experienced prenatal diagnostic centers are 10–25%.13,15 In some of those cases, undetected anomalies (such as migrational disorders) were too subtle for detection by sonography before birth. In other cases, anomalies might have been identified if there had not been technical limitations.16 In two of 11 cases of sonographic isolated mild ventriculomegaly, other anomalies were found by MRI. In our series, we found that ultrasound permitted identification of a slightly irregular contour of ventricles in cases of porencephaly but MRI showed the amount of cortical destruction better (Figure 4).
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The presence of a cisterna magna of more than 10 mm raises the possibility of an anomaly in the spectrum of Dandy Walker malformation to Dandy Walker variant, cerebellar hypoplasia, or an arachnoid cyst. However, the enlarged cisterna magna also might be a normal variant. Megacisterna magna must be differentiated from abnormal causes of cisterna magna enlargement. In Dandy-Walker variant, a portion of the cerebellar vermis is absent. In cerebellar hypoplasia, the cerebellar diameter is reduced. In arachnoid cyst, the cerebellar structures are present, but displaced. In megacisterna magna, the cisterna magna is enlarged but cerebellar structures are in their normal positions. Sonography of normal posterior fossa anatomy might be difficult because of shadowing from the fetal skull, particularly in the third trimester. Extreme inclination of the scan plane through the posterior fossa can result in falsely increased cisterna magna measurements. Magnetic resonance imaging was helpful in that it permitted reassurance of women who were referred for diagnoses of posterior fossa abnormality and who had normal confirmatory sonograms, because the cerebellum was shown better in all cases by MRI. The acquisition plane can be optimized to show the cerebellar vermis and to allow measurement of the cisterna magna.
We evaluated ten fetuses with myelomeningocele. Although the spinal defects and Chiari malformation were visualized well with MRI, the additional information did not lead to changes in management, with the exception of one case, in which MRI showed a low sacral neural tube defect that was visualized poorly sonographically. In the future, it is likely that MRI will play a role in fetal surgery for neural tube defects.19
Magnetic resonance imaging was helpful in delineating intracranial anatomy in five fetuses with cephaloceles. In one case, MRI showed that there was minimal cortical tissue in the cephalocele, and the woman decided to continue the pregnancy. In another case, MRI showed the extent of the cephalocele and unformed brain stem better. Those findings were important for counseling before delivery. In a third case, a portion of the ventricle extended into the cephalocele, a condition with worse prognosis than that of a cephalocele without ventricular involvement.
Unlike Resta et al,20 we found that migrational abnormalities such as polymicrogyria can be visualized with prenatal MRI. In our study, there were two cases of cortical gyral abnormalities, and in both cases the abnormalities were shown only by MRI.
The death of one monozygotic twin might be an indication for fetal MRI. Pathology studies have shown that cavitary white-matter lesions and cerebral atrophy develop 2 or more weeks after acute necrosis in the live twin. Therefore, MRI and ultrasound findings would be negative until at least 2 weeks after the death of a twin. We studied three cases of single surviving twins. In one woman, the surviving twin appeared normal by ultrasound and MRI, and the pregnancy was ongoing. In two cases, ventriculomegaly was present, but no intracranial lesions were seen sonographically. One fetus had ventriculomegaly increasing over 5 days with multiple regions of cortical necrosis seen histologically (the study was performed 1 week after MRI). The second fetus had encephalomalacia, cortical hemorrhage, and porencephaly. Those findings regarding surviving twins are consistent with reports that some twins do well after the death of a cotwin21 and that it is difficult to prevent damage after acute fetal death, because by the time imaging findings are obtained, the damage is done. Magnetic resonance imaging does permit diagnosis of encephalomalacia prenatally, with increased sensitivity compared with ultrasound, which has important implications in counseling and management in cases of death of a twin.
One limitation of our study was that autopsies or postnatal MRI was not performed in all cases. Fetal autopsies were not done in all terminated pregnancies. Many second-trimester dilation and evacuations resulted in fetal maceration. In a few cases, parents decided against autopsies.
In the live-born and well neonates, it was difficult to justify the expense and the risk associated with sedation of confirmatory MRI. That problem is exemplified in two cases involving incidental findings, namely an enlarged subtemporal vein and a subependymal hemorrhage. Both infants had normal sonograms at birth. The prenatal MRI findings were diagnostic in each case, so it was reasonable to consider the prenatal MRI findings as a definitive diagnosis. We are unsure of the significance of those findings in utero. This leads to counseling difficulty. However, in the case of the two fetuses in our series with incidental findings, the women were counseled about the uncertain clinical significance of the findings and both sets of parents were satisfied with their understanding of the incidental findings. The third pregnancy with an incidental finding is ongoing.
This study did not take into account the increased diagnostic confidence that MRI provides when the anatomy is normal or when no abnormality is seen in addition to sonographic findings. An example is a normal corpus callosum seen by MRI in a fetus with mild ventriculomegaly. Although the increased confidence allows for improved counseling, confidence is difficult to quantify.
Magnetic resonance imaging was least helpful in patients whose confirmatory sonograms were normal and in cases of sonographically obvious myelomeningocele. Magnetic resonance imaging was most helpful in obese women whose anatomy was difficult to visualize sonographically and in women with fetuses with ventriculomegaly, enlarged cisterna magna, and arachnoid cysts.
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Footnotes |
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Received April 9, 1999. Received in revised form May 24, 1999. Accepted June 17, 1999.
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2. Sonigo PC, Rypens FF, Carteret M, Delezoide AL, Brunelle FO. MR imaging of fetal cerebral anomalies. Pediatr Radiol 1998;28:212–22.[Medline]
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