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Obstetric Imaging |
1 From the Departments of Radiology (D.L., T.S.M.) and Obstetrics and Gynecology (D.L., G.W.), Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215; Department of Radiology, Children’s Hospital, Boston, Mass (R.R.R.); and Department of Radiology, Lucille Salter Packard Children’s Hospital at Stanford, Palo Alto, Calif (P.D.B.). Received July 10, 2002; revision requested August 23; final revision received April 27, 2003; accepted May 5. Supported by a National Institutes of Health grant, National Institute of Neurologic Disorders and Stroke, NS 37945. Address correspondence to D.L. (e-mail: dlevine@caregroup.harvard.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: The authors compared images from 242 ultrasonographic (US) studies and 242 MR imaging studies of the CNS in 214 fetuses. Reference standards of postnatal physical examination, imaging, surgical, and autopsy findings were available in 171 (79.9%) fetuses. Referring physicians were surveyed on how MR imaging findings changed patient counseling or case management. Outcomes were compared with respect to GA. Statistical tests used were the Fisher exact test, Student t test, and analysis of variance.
RESULTS: Confirmatory US findings were normal in 69 fetuses. MR imaging findings changed diagnosis in 46 of 145 (31.7%) fetuses with abnormal US findings. The mean GA of 72 of 145 fetuses with changes in maternal counseling (25.9 weeks) was significantly greater than that in 73 of 145 fetuses without changes in maternal counseling (22.6 weeks, P < .01). The mean GA of the 46 fetuses with changes in diagnosis (26.3 weeks) was significantly greater than that of the 99 fetuses with no major change in diagnosis (23.3 weeks, P < .01). There were 27 of 145 changes in case management, with no significant difference in mean GA of fetuses with and those without changes in case management. In fetuses with abnormal US findings, MR images were used to decide to terminate the pregnancy (n = 13; mean GA, 20.1 weeks), continue the pregnancy (n = 4; mean GA, 19.2 weeks), direct the mode and/or location of delivery (n = 5; mean GA, 30.5 weeks), and direct perinatal care (n = 5; mean GA, 30.2 weeks).
CONCLUSION: When a CNS anomaly is detected or suspected at US, MR imaging may demonstrate additional findings that can alter diagnosis and case management. Changes in management are GA dependent.
© RSNA, 2003
Index terms: Fetus, abnormalities, 856.874 • Fetus, central nervous system, 856.874 • Fetus, MR, 856.121416 • Fetus, US, 856.1298 • Magnetic resonance (MR), rapid imaging, 856.121416
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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If the confirmatory US findings differed from those of the referral diagnosis, then the confirmatory US findings were used for data analysis. In one case, the patient refused to undergo confirmatory US, so the referral diagnosis was used. The results of confirmatory US were discussed with each patient. Each patient was informed that she could withdraw from the MR imaging portion of the study after confirmatory US was performed.
One hundred ninety-two women with 214 fetuses underwent 242 MR examinations of the fetal CNS (Table 1). The results in the first 90 fetuses were reported previously (3,6). Two additional women underwent confirmatory US and then declined MR imaging: one because of normal US findings, the other because of fetal demise. These women were not included in the study population.
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Data obtained by the radiologist at the time of US included referral diagnosis and/or indication for US and/or MR imaging, history of prior US during the index pregnancy, gestational age according to the last menstrual period, chromosomal analysis results (which at times were not available until later in pregnancy), gestational age according to US biometric measurements and ventricular size as measured at the level of the ventricular atrium, and diagnosis of CNS abnormalities at US.
Gestational age was calculated according to the date of the last menstrual period, unless first-trimester US had been performed by the patient’s obstetrician for recalculation. If the date of the last menstrual period was unknown and first-trimester US was not performed, then US biometric measurements obtained from the earliest US study during the pregnancy were used for data analysis.
The degree of ventriculomegaly was assessed by using US measurement of the atrium of the lateral ventricles as follows: mild ventriculomegaly, 10–14 mm; moderate ventriculomegaly, at least 15 mm with more than 3 mm of brain parenchyma (cortical mantle) surrounding the ventricles; and severe ventriculomegaly, at least 15 mm with up to 3 mm of visible cortical mantle. Degree of ventriculomegaly was graded by two authors (D.L., T.M.) separately at a time remote from initial US. Differences of opinion were decided by means of consensus.
MR Imaging
After screening for contraindications, patients underwent prenatal MR imaging. No patients were excluded because of contraindications to MR imaging. MR examinations were performed with a 1.5-T superconducting system (Vision; Siemens, Erlangen, Germany) by using a four-element phased-array coil and/or body coil. The minimum rise time was 600 msec (for a 25-mT peak gradient amplitude). Patients were positioned supine and feet first into the gantry to minimize claustrophobia. Scout images were obtained in three planes, and fetal CNS images were obtained by using the half-Fourier single-shot RARE technique in the fetal sagittal, coronal, and transverse planes. In the 1st year of the study, imaging parameters included echo spacing of 4.2 msec, echo time of 60 msec, echo train length of 72, one signal acquired, 5-mm section thickness, 26 x 35-cm field of view, 128 x 256 matrix, 19-second sequence duration, and a section acquisition of 420 msec with no intersection gap.
In subsequent years, the typical sequence included 4-mm section thickness interleaved with an intersection gap equal to the section thickness. This was done to minimize inadvertent radiofrequency excitation of adjacent sections. Thin sections (2.8–3.5 mm) were used with a flip angle of 150° for evaluation of fetuses with early gestational age or for delineation of small structures when needed. The smallest field of view was used to allow for visualization of fetal anatomy without aliasing artifact from wraparound of the maternal anatomy. Matrix size was at times increased to 196 x 256 or 256 x 512. The whole-body specific absorption rate was kept under 3.0 W/kg.
A representative image from each sequence was used as a scout to align the subsequent acquisition. In the second and subsequent years of the study in cases in which hemorrhage was suspected, T1-weighted MR imaging was performed by using a fast low-angle shot technique with a repetition time (msec)/echo time (msec) of 126/4, flip angle of 80°, field of view of 24 x 32 cm, acquisition matrix of 96 x 256, section thickness of 5 mm, and one signal acquired for an acquisition time of 12 seconds. The T1-weighted images were obtained with maternal breath hold. The total examination time for each study was approximately 20 minutes. MR images were of diagnostic quality for the fetal brain in each of the 214 fetuses studied.
MR Image Review
MR images were reviewed at the time of acquisition by the radiologist who performed confirmatory US to ensure that MR images were of diagnostic quality and to give a preliminary interpretation of the findings. MR images were reviewed subsequently by a radiologist with experience in pediatric neuroradiology (P.D.B., with 22 years of experience; or R.R.R., with 10 years of experience) with knowledge of the US diagnosis, who gave his interpretation of the MR imaging findings. Preliminary diagnoses and those assigned subsequently by a pediatric neuroradiologist were compared by one author (D.L.). If the two diagnoses differed, then the images were reviewed again by two authors (D.L. and P.D.B. or D.L. and R.R.R.), and a final diagnosis was assigned. An attempt was made for the pediatric neuroradiologist to review all images prospectively, prior to delivery.
Physician Survey
The patients and their referring physicians were informed of the results of confirmatory US and MR imaging with the caveat that prenatal MR imaging was investigative and of unproven accuracy for the diagnosis of CNS anomalies. In general, however, despite unproven accuracy, the physician accepted the MR imaging findings and used them to counsel the patient. The patients also tended to accept the MR imaging findings. The referring physician was asked how the additional information provided by MR imaging changed case management or patient counseling. Since case management is affected by many variables that could not be selected easily from US and MR imaging findings, the influence on patient counseling was used as an outcome, unless a clear change in case management occurred. Since confirmatory US and MR imaging findings were given to referring clinicians simultaneously, there were many cases in which a more confident diagnosis was assigned by using MR imaging; however, these were not considered to have changed counseling unless the MR images clearly demonstrated findings beyond those available with US, other than demonstrating normal structures, which were assumed to be present at US. In two cases, the final prenatal diagnosis based on MR imaging findings (after review by a pediatric neuroradiologist) was not available until after delivery because of the short interval between MR imaging and delivery. In these cases, the referring clinician was questioned as to what potential effect the MR imaging results would have had on patient counseling.
Reference Standards
Diagnostic procedures for the 214 fetuses in the study included autopsy (n = 24), surgery (n = 25), and postnatal imaging without surgery or autopsy (n = 81). Thirty-seven fetuses with normal prenatal CNS findings underwent physical examination only for follow-up, as did four fetuses with abnormal CNS findings. Details of postnatal follow-up are given in Table 2. Modalities used for postnatal imaging were MR imaging (n = 54), US of the head (n = 47) and spine (n = 5), CT (n = 5), radiography of the spine (n = 21), and angiography (n = 2). Twenty-six fetuses underwent two types of postnatal imaging, and one fetus underwent three types of postnatal imaging.
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Outcomes
Abnormalities seen at US and MR imaging and the definitive diagnoses were coded by using the classification of congenital cerebral, cerebellar, and spinal malformations as described by van der Knaap and Valk (7). The diagnoses assigned at the time of US and prenatal MR imaging and the final diagnoses were compared by one author (D.L.). Changes in diagnosis were graded as 1, a major change (a new finding unsuspected at US or a change in diagnosis of the anomaly); 2, a minor change (a slightly different diagnosis without a change in the classification of the anomaly); and 3, no change. In cases in which more than one MR examination was performed, the most abnormal MR imaging results were used for data analysis, as compared with US findings obtained within 2 days of MR imaging. If both MR examinations yielded similar findings, then the earliest MR examination findings were used for data analysis.
Changes in case management were grouped by type of decision: (a) termination of the pregnancy, (b) continuation of the pregnancy, (c) direction of the mode and/or location of delivery (eg, delivery at a tertiary care site or delivery by means of cesarean section because of risk of bleeding), and (d) direction of perinatal care (eg, not monitoring the fetus during delivery or not placing the neonate on life support).
Statistical Analysis
The effect of MR imaging on changes in diagnosis, patient counseling, and case management was assessed with respect to gestational age. Statistical methods used were the Fisher exact text for comparison of proportions of fetuses older than and younger than 24 weeks of gestational age with respect to change in maternal counseling, diagnosis, and case management (Instat software; GraphPad, San Diego, Calif); the Student t test for comparison of mean gestational age in groups of fetuses with and those without changes in maternal counseling, diagnosis, and case management (Instat software); and analysis of variance for comparison of gestational ages with respect to type of change in case management (Minitab Statistical Software; Minitab, State College, Pa). A P value of less than .05 was considered to indicate a statistically significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Confirmatory US
In 159 fetuses with MR imaging findings that indicated presence of an anomaly, confirmatory US findings differed from the referral diagnosis in 51 of 144 (35.4%) cases (14 patients initially underwent US at our institution and thus did not undergo confirmatory US, and one patient declined confirmatory US and underwent MR imaging only). Confirmatory US findings were normal in 18 patients, including those with fetuses that received referral diagnoses of enlarged posterior fossa (n = 7), ventriculomegaly (n = 6), neural tube defect (n = 3), and arachnoid cysts (n = 2). New findings at confirmatory US included suspected or definite agenesis of the corpus callosum (n = 12), cerebellar hypoplasia (n = 8), spinal meningomyelocele (n = 5), meningocele (n = 2), hemorrhage (n = 2), and Dandy-Walker variant (n = 2); one case each of scoliosis without neural tube defect, ventriculomegaly, arachnoid cyst, hemangioma, hydranencephaly, and megacisterna magna; and four cases of a combination of two of the previous findings. In each case, MR imaging findings substantiated the diagnosis assigned on the basis of confirmatory US findings (although additional findings were also seen, as discussed later).
MR Imaging
There were 69 fetuses with a normal CNS at US without other US findings to suggest CNS anomaly. Most of these patients were referred for screening (n = 32, Table 3) or had co-twins with anomalous fetuses (n = 19). The remainder had referral diagnoses of enlarged cisterna magna and/or Dandy-Walker variant (n = 7), ventriculomegaly (n = 5), arachnoid cysts (n = 2), and neural tube defects (n = 4). Sixty-six of these 69 fetuses had normal MR imaging findings of the CNS. One fetus had an incidental finding of an enlarged supratentorial vein, one had a subependymal hemorrhage (Fig 1), and fetus had a focal thoracic diastematomyelia without a tethered cord.
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In the 145 cases in which there was a CNS abnormality at confirmatory US or at initial US at our institution or in which US showed normal CNS findings but a CNS anomaly was strongly suspected on the basis of extra-CNS findings of cardiac rhabdomyomas, spinal abnormalities, or exstrophy, MR imaging provided additional information in 72 of 145 (49.6%) cases that led to a change in either diagnosis or patient counseling. There were 46 of 145 (31.7%) cases in which MR imaging demonstrated a major new finding (excluding two cases of a tethered cord, which were not visualized at US but were expected because of cloacal malformation and diastematomyelia; Tables 4, 5). In the two patients in whom the final diagnosis based on MR images was not available until after delivery, the MR imaging findings led to a change in diagnosis (and thus would have led to a change in counseling) but were not of the type that would have led to a change in case management.
With regard to the effect of gestational age on changes in counseling and diagnosis (excluding those fetuses with normal confirmatory US findings), the mean gestational age of 72 of 145 fetuses with changes in maternal counseling (25.9 weeks ± 0.78) was significantly older than those without changes in maternal counseling (73 of 145 fetuses; mean gestational age, 22.6 weeks ± 0.58; P < .01). Similarly, the mean gestational age of the 46 of 145 fetuses with changes in diagnosis (mean gestational age, 26.3 weeks ± 0.95) was significantly older than that of the 99 of 145 fetuses with no major change in diagnosis (23.3 weeks ± 0.57, P < .01). The proportion of fetuses at a gestational age of younger than 24 weeks with changes in maternal counseling (35 of 83, 42.2%) was significantly different than the proportion at a gestational age of 24 weeks and older with changes in maternal counseling (38 of 62, 61.3%; P < .05). Similarly, the proportion at a gestational age of younger than 24 weeks with major changes in diagnosis (19 of 83, 22.9%) was significantly different than the proportion at a gestational age of 24 weeks and older with major changes in diagnosis (27 of 62, 43.5%; P < .05).
Changes in management occurred in 27 of 145 cases of abnormal confirmatory or initial US findings at our institution or cases in which a CNS anomaly was strongly suspected on the basis of extra-CNS findings. There was no significant difference in the mean gestational age of 27 of 145 fetuses with changes in care (23.8 weeks ± 6.3) compared with that of 118 of 145 fetuses without changes in care (24.4 weeks ± 5.4, P = .17). There was no significant difference in the proportion of fetuses with changes in care at younger than 24 weeks (18 of 83, 21.7%) compared with those fetuses 24 weeks and older (nine of 62, 14.5%; P = .29). MR images were used to decide to terminate the pregnancy (n = 13; mean gestational age, 20.1 weeks ± 3.5), to continue the pregnancy (n = 4; mean gestational age, 19.2 weeks ± 2.5), to direct the mode and/or location of delivery (n = 5; mean gestational age, 30.5 weeks ± 7.7), and to direct perinatal care (n = 5; mean gestational age, 30.2 weeks ± 5.6). There was a significant difference in the gestational age of fetuses with changes in care after MR imaging among the four aforementioned groups (P < .01) (Fig 6).
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There were three false-negative MR imaging findings. In one case of a neural tube defect that was visualized with US and MR imaging, hypoplasia of the rostrum of the corpus callosum and a subtle cortical gyral abnormality were not diagnosed at prenatal US or MR imaging. One small arachnoid cyst was not visible on prenatal MR or postnatal US images but was clearly present at prenatal US. In one monochorionic diamniotic pair of twins with the demise of one twin, the living twin had mild ventriculomegaly that increased to moderate ventriculomegaly over 5 days, at which time MR imaging was performed. At the time of autopsy of the twin that subsequently died (1 week after MR imaging), multiple small regions of cortical necrosis were present that were not visualized at MR imaging. Although this brain destruction was an evolving process, it was considered a false-negative finding.
There were three potential false-negative MR imaging findings that were deemed to be postnatal developments rather than diagnoses missed in utero. In one case, postnatal US demonstrated a grade 1 germinal matrix hemorrhage at birth. This was believed to be a recent event. The infant had normal US findings of the head at 7 months of age. Another infant born preterm had choroid plexus, intraventricular, subarachnoid, and subependymal hemorrhages that were believed to have formed postnatally. The third infant had a small choroid plexus papilloma diagnosed at 16 months of age (after documentation of normal US findings of the head on day 3 after birth). In this case, the degree of ventriculomegaly in utero was not believed to be caused by the choroid plexus papilloma.
There were 11 chromosomal abnormalities, including four cases of trisomy 21, three cases of trisomy 18, one case of trisomy 13, one translocation present in the father of the neonate, one 22q chromosomal deletion, and one unbalanced translocation.
Twenty-five patients with 28 fetuses (three sets of twins) underwent two MR examinations. MR imaging results were similar between examinations in eight healthy fetuses (referred for screening protocols) and 10 abnormal fetuses—three with arachnoid cysts (one of which also had partial agenesis of the septi pellucidi), two with mild ventriculomegaly, and one each with anencephaly, encephalocele, Dandy-Walker malformation, cloacal exstrophy, and congenital stippled epiphyses. MR imaging findings that were different between the two examinations in 10 other fetuses are detailed in Table 6.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Important findings in the current study that were previously unreported include the effect of gestational age on the impact of MR imaging findings. We found that while third-trimester fetuses were more likely to have changes in diagnosis and maternal counseling, there was no significant difference in the proportion of younger versus older fetuses with changes in case management. The changes in management that occurred prior to 24 weeks of gestational age were typically decisions regarding the continuation or termination of pregnancy. Changes in management that occurred after 24 weeks were changes in the location of delivery (community hospital vs tertiary care hospital), mode of delivery (cesarian section or vaginal delivery), and decisions regarding provision of only supportive care in the perinatal period (as opposed to monitoring a fetus during delivery and placing the neonate on life support).
In this study, MR imaging results allowed for diagnostic visualization of the brain in each of the 214 fetuses studied. In 86 cases, MR imaging findings led to a change in patient counseling. If the 69 fetuses that were deemed to be healthy at confirmatory US were excluded, then MR imaging led to a change in maternal counseling in 72 of 145 (49.6%) fetuses, a change in diagnosis in 46 of 145 (31.7%) fetuses, and a change in care in 27 of 145 (18.6%) fetuses with abnormal US findings.
One interesting finding in this study is the number of fetuses with callosal anomalies that were not diagnosed at US. In normal development, a rudimentary corpus callosum is present at 12 weeks. By 20 weeks, a prominent genu should be seen (22). Agenesis of the corpus callosum is typically diagnosed at US when the ventricles have an abnormal configuration. In fetuses with normal-sized ventricles, this abnormal configuration may be missed at US. In addition, in fetuses with encephalomalacia as a cause of abnormal corpus callosum, the ventricular contour may be normal. The direct visualization of all portions of the corpus callosum afforded by MR imaging should allow for more precise diagnosis of callosal abnormalities than is possible with US.
Twelve fetuses received a prenatal diagnosis of cortical dysplasia and/or cortical clefts. These disorders are typically too subtle to be visualized with US (4). Similarly, six fetuses had midbrain abnormalities that were seen at prenatal MR imaging and not at US. In our experience, this is another area that is difficult to evaluate with US.
A valuable finding in the present study is that confirmatory US findings led to a change in diagnosis in 35.4% of cases. This is important because if confirmatory US had not been performed, there would have been a perceived increase in the benefit of MR imaging, which led to a change in diagnosis in each of these cases.
A limitation of the present study is that MR images were reviewed with knowledge of the patient’s history and US findings. This could potentially bias our results. This was done to simulate the way examinations will be performed in the future. We believe that MR imaging will not replace US as a screening modality for fetal anomalies. Rather, fetuses with abnormal US findings will be sent for further evaluation with MR imaging. In addition, since MR images were obtained to best demonstrate the region of abnormality, it would be difficult to blind the reader to the area of interest. We do not believe that this is a severe limitation to the study, since so many findings were seen with MR imaging that were not suspected at US.
An additional limitation of our study is the reference standard. Since not all neonates underwent postnatal imaging or autopsy, not all anomalies were documented postnatally. Lack of a true reference standard for final diagnosis is a general problem in prenatal imaging research because pathologic findings are rarely available (23). However, findings of prenatal MR examinations were considered to be sufficiently diagnostic to require no further evaluation.
Another limitation is the changing nature of CNS anomalies over time, as shown in nine fetuses who underwent more than one MR examination. An additional example of a false-negative finding, possibly due to the timing of the examination, is the case of twin-twin transfusion syndrome after death of one of the twins, in which cortical defects were seen at the time of autopsy, which was performed 1 week after MR imaging. Since the brain lesions were changing over time (as evidenced by the history of rapid change in ventricular size of the then surviving twin), it is possible that MR imaging would have been able to depict the regions of porencephaly if it had been performed closer to the autopsy.
A final limitation of our study is the determination of the way the MR imaging results affected case management. While patient counseling can be altered by additional information, case management decisions are based on a variety of factors, including patient history, type of anomaly, patient and physician tendencies, and confidence in diagnosis.
In summary, limitations of current radiologic practice necessitate that decisions about the care of a pregnant patient and fetus must sometimes be made with inconclusive data regarding the specific cause or severity of a fetal CNS anomaly. Therapeutic choices often rely on a diagnosis assigned at US. Alternative imaging is important for decreasing ambiguity in the counseling of expectant parents when a questionable abnormality is visualized at US or when an abnormality is definite but the exact diagnosis is uncertain. US and MR imaging are complementary noninvasive imaging methods in the evaluation of high-risk pregnancy. When a CNS anomaly is detected at US, MR imaging may demonstrate additional findings that may alter patient counseling and case management. The types of changes in case management that occur as a result of findings on prenatal MR images are dependent on gestational age.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, D.L.; study concepts, D.L., P.D.B.; study design, D.L.; literature research, D.L.; clinical studies, all authors; data acquisition, D.L., T.S.M.; data analysis/interpretation, D.L.; statistical analysis, D.L.; manuscript preparation and definition of intellectual content, D.L.; manuscript editing, D.L., T.S.M., R.R.R., P.D.B.; manuscript revision/review, all authors; manuscript final version approval, D.L.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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