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Published online before print April 24, 2003, 10.1148/radiol.2273020535
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(Radiology 2003;227:839-843.)
© RSNA, 2003

Obstetric Imaging

Myelomeningocele: Prenatal Evaluation—Comparison between Transabdominal US and MR Imaging1

Oran S. Aaronson, MD, Marta Hernanz-Schulman, MD, Joseph P. Bruner, MD, George W. Reed, PhD and Noel B. Tulipan, MD

1 From the Departments of Neurosurgery (O.S.A., N.B.T.), Radiology (M.H.S.), and Obstetrics and Gynecology (J.P.B.), Vanderbilt University Medical Center, A-2219 Medical Center North, Nashville, TN 37232; and Division of Preventive and Behavioral Medicine, University of Massachusetts Medical School, Worcester (G.W.R.). Received May 6, 2002; revision requested June 21; final revision received September 27; accepted October 25. Supported by a grant from the Dana Foundation. Address correspondence to N.B.T. (e-mail: noel.tulipan@vanderbilt.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To compare transabdominal ultrasonography (US) with fetal magnetic resonance (MR) imaging in the prenatal evaluation of myelomeningocele lesion level.

MATERIALS AND METHODS: Prenatal US images, pre- and postnatal MR images, and postnatal spinal radiographs obtained in the first 100 fetuses who underwent intrauterine myelomeningocele repair were the basis for this study. Each image was used to assign a lesion level. The assigned levels were compared by means of the {kappa} statistic, as an index of agreement.

RESULTS: All fetuses underwent prenatal US. Sixty-one fetuses underwent prenatal MR imaging. Fifty fetuses underwent both postnatal spinal radiography and postnatal MR imaging, and an additional 34 fetuses underwent one postnatal study but not the other. When findings on prenatal US images were compared with those on postnatal radiographs, the findings agreed within one spinal level in 79% (55 of 70, {kappa} = 0.60) of cases. When findings on prenatal MR images were compared with those on postnatal radiographs, the findings agreed in 82% (31 of 38, {kappa} = 0.63) of cases. Findings on postnatal MR images and those on postnatal spinal radiographs agreed within one spinal level in 100% (50 of 50, {kappa} = 1.0) of cases.

CONCLUSION: Findings at prenatal MR imaging and prenatal US are equally accurate for the assignment of a lesion level in a fetus with myelomeningocele. Given that findings with both modalities will lead to misdiagnosis of the spinal level by two or more segments in at least 20% of cases, care should be exercised when neurologic outcome is predicted on the basis of these studies alone.

© RSNA, 2003

Index terms: Fetus, central nervous system, 856.8746 • Fetus, MR, 856.121412, 856.121416, 856.8746 • Fetus, surgery, 856.12986, 856.8746 • Fetus, US, 856.12986, 856.8746 • Pregnancy, US, 856.12986, 856.8746 • Spina bifida, 351.1452


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Transabdominal ultrasonography (US) has been the mainstay of prenatal imaging for more than 25 years. Recently, however, the development of faster imaging sequences has led to increasing use of magnetic resonance (MR) imaging in fetal evaluation. MR imaging offers the potential advantage of providing superior anatomic resolution, regardless of maternal body habitus or the way the fetus lies in the uterus. MR imaging provides an image display that is more intuitively comprehensible to the patient and to many consulting physicians. Despite the increasing use of prenatal MR imaging, to our knowledge, only a few published studies have been performed to compare the advantages and disadvantages of the two in a systematic fashion.

Since April 1997, our institution (Vanderbilt University Medical Center) has offered intrauterine myelomeningocele repair as an alternative to conventional postnatal therapy (1). Early prenatal surgical results indicate that the procedure reduces shunt-dependent hydrocephalus and the hindbrain herniation associated with the Chiari type II malformation, both of which usually accompany this disease (2,3). As part of the screening process that precedes this procedure, all candidates undergo transabdominal US. More recently, prospective candidates have also undergone fetal MR imaging (4). The purpose of our study was to compare transabdominal US with fetal MR imaging in the prenatal evaluation of myelomeningocele lesion level.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Pregnant patients who had a fetus with myelomeningocele diagnosed at US were referred to our institution and evaluated for intrauterine surgery according to a protocol approved by the institutional committee for the protection of human subjects. This protocol included both repeat US and MR imaging before surgery. Informed consent was obtained from each participant according to the guidelines of the institutional committee. The only inclusion criteria for study participation were the absence of other major fetal anomalies, a normal fetal karyotype, and the parents’ ability to fully comprehend the potential risks and benefits of the available care options. Repair was performed when the fetus was between 21.1 and 29.4 weeks of estimated gestational age, with a method described previously (1). Prenatal US images, pre- and postnatal MR images, and postnatal spinal radiographs obtained in the first 100 fetuses who underwent intrauterine myelomeningocele repair at our institution were the basis for this study. All prenatal imaging studies were performed within 48 hours before surgery.

US Imaging
All patients underwent repeat transabdominal US at our institution to confirm the diagnosis of myelomeningocele and to rule out other anomalies. This study was performed (Toshiba 270; Toshiba, Tustin, Calif) with a 5-MHz curvilinear transducer. All US images were interpreted and the lesion levels were assigned by one investigator (J.P.B.). The lesion level was assigned by scanning the fetal spine in a transverse plane. Each vertebra was sequentially examined, and the most cephalic vertebra with evidence of laminar separation was used to identify the lesion level. For purposes of establishing a frame of reference, the insertion of the most caudal rib was assigned the level of T12. In some cases, especially with a low lesion situated near the sacral curve, the iliac crests were assigned a vertebral level of L5, and the first anomalous lamina was located relative to this level. The lower level of the lesion was not determined, and lesion size was not measured (Fig 1).



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  		Figure 1. Prenatal transabdominal US images of a fetus at an estimated gestational age of 22 weeks. The spine is seen in the transverse plane. Left: Image shows intact laminae at the level of the distal abdominal aorta (arrow). Center: Image demonstrates the beginning of posterior element separation (curved arrows) and the myelomeningocele sac (straight arrow), below the aortic bifurcation. Right: Image shows wide-open posterior elements (curved arrows) and the myelomeningocele sac (straight arrow) at the level of the iliac crests at L5. Therefore, the most cephalic level of the dysraphic defect is at L4, as seen in the center image.

 
MR Imaging and Radiography
Prenatal MR images were obtained with a 1.5-T unit (Signa LX; GE Medical Systems, Milwaukee, Wis) and a quadrature phased-array flexible body coil. After an initial three-plane gradient-echo localizer sequence, a single-shot fast spin-echo T2-weighted sequence was used: 5-mm section thickness, acquisition matrix of 256 (frequency) x 128 (phase), 100% phase oversampling, 25-cm field of view, 19 sections, and 25-second acquisition time. Transverse, sagittal, and coronal images were obtained through the dysraphic defect in the fetal spine. The rapid acquisition time of the single-shot sequence allowed adequate visualization of fetal anatomy in most patients (Fig 2). Fetal sedation or paralysis was not used in any patient.



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  		Figure 2. Prenatal sagittal fast spin-echo MR image (1,200/120 [repetition time msec/echo time msec]) obtained in a fetus at an estimated gestational age of 24 weeks. The dysraphic defect (arrow) begins at L3.

 
Postnatal MR imaging was performed at the patients’ home institutions. Although the overall methods varied, sagittal T1-weighted spinal images were available in all studies; therefore, levels were based on this view. Digitized copies of the T1-weighted spinal MR images were used for the purposes of this study. The most cephalic level of bone abnormality at the myelomeningocele site was used as the lesion level. Lesions below L5 were labeled as sacral (Fig 3).



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  		Figure 3. Postnatal sagittal T2-weighted MR image (3,600/113) in the newborn who is depicted prenatally in Figure 2 demonstrates the dysraphic defect (arrow) beginning at L4. The tethered neural placode is seen one level below, at L5. Image quality of this image was better than that of the T1-weighted image (not shown).

 
Postnatal radiographs were evaluated either as film hard copies or as digitized images. Levels were assigned by using the anteroposterior view to identify the most cephalic open posterior dysraphic elements (Fig 4).



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  		Figure 4. Postnatal anteroposterior spinal radiograph of the same patient as in Figures 2 and 3 demonstrates spinal dysraphia beginning at L4. Note the laminar separation (arrows) at this level.

 
The pre- and postnatal MR images and postnatal spinal radiographs were interpreted by one radiologist (M.H.S.), who was blinded to the lesion level assigned at US. Pre- and postnatal MR images and postnatal radiographs were not viewed at the same session to avoid bias. As a measurement of intraobserver variability, spinal radiographs from an earlier study (5) in 26 fetuses who underwent intrauterine myelomeningocele repair were reevaluated approximately 2 years later for the current study. The radiologist was blinded to the results of the initial interpretation (5). The images in the second reading (the current study) were digitized; therefore, they could be magnified and their contrast and brightness manipulated to optimize visualization of the spine through variable overlying bowel contents. We thought that the second reading was probably the more accurate one, and the second reading was used for subsequent comparative analysis.

Statistical Analysis
The lesion levels assigned on the basis of the imaging modalities were compared as follows. Each of the four possible studies—prenatal US, pre- and postnatal MR imaging, and postnatal spinal radiography—was used to assign a lesion level. As in previous studies (5–7), the postnatal spinal radiograph was used as the reference standard in the current study. Images obtained with these modalities were then compared to assess agreement. The {kappa} statistic was used as a measurement of agreement (8).

The {kappa} statistic is an index of agreement, with 1.0 indicating perfect reproducibility or concordance and 0 indicating no reproducibility or concordance. The {kappa} statistic is estimated as the difference between the observed agreement (PO) and the expected agreement (Pe) divided by 1 minus the expected agreement: (PO - Pe)/(1 - Pe). Expected agreement is defined as the agreement with the assumption of independence of the two measurement tools, or no concordance. A {kappa} value of 0–0.4 indicates marginal agreement; 0.41–0.75, good agreement; and 0.76–1.00, excellent agreement (9). We defined "agreement" as a match within one level. For example, a measurement of L4 with one tool and of L5 with another tool would be considered agreement. Ninety-five percent CIs were estimated for {kappa}.

The difference in levels was computed between measurement tools, and a mean difference was estimated along with 95% CIs to test for any bias (ie, more or less severe measurement of levels). Paired differences were tested by using a signed rank test. Analyses were performed (Stata, version 7.0; Stata, College Station, Tex) with formulas from Fleiss (10).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
One hundred consecutive fetuses underwent intrauterine myelomeningocele repair. Each of these fetuses was examined and assigned a lesion level on the basis of findings at transabdominal US. Only 61 fetuses underwent prenatal MR imaging because this modality became available at our institution 18 months after inception of the protocol for this study. One patient was excluded from the prenatal MR imaging analysis because only transverse images were available. Therefore, it was not possible to accurately assign a lesion level in that patient. Therefore, a lesion level was assigned in 60 fetuses on the basis of prenatal MR imaging findings.

The lesion level was definitively assigned in 70 fetuses on the basis of findings at postnatal spinal radiography. In 50 of these fetuses, postnatal MR imaging was also performed. An additional 14 fetuses underwent only postnatal MR imaging. Thus, postnatal MR imaging was performed in 64 fetuses. A lesion level was assigned in 60 of these fetuses on the basis of the postnatal MR imaging findings. In four fetuses, the lesion level could not be assigned because of image degradation from motion artifact. The remaining fetuses either had no postnatal spinal images, or none could be obtained after repeated calls to the patient and local physician.

Findings with prenatal US and pre- and postnatal MR images were compared with those with postnatal spinal radiographs (Table 1). Note that the number at the top of each column represents the number of cases in which both the particular study and a postnatal spinal radiograph were available for a given patient. Good, but not excellent, agreement was seen when prenatal US images ({kappa} = 0.60) and prenatal MR images ({kappa} = 0.63) were compared with postnatal radiographs; agreement rates of approximately 80% were observed. Expected agreement rates, however, were approximately 50%, with an assumption of independence. A comparison of postnatal MR images with postnatal radiographs showed excellent agreement, with an agreement rate of 100% versus an expected agreement rate of approximately 53% ({kappa} = 1.0). There was a statistically significant (P < .001) bias toward underestimation of the lesion level in the comparison of the prenatal US images with the postnatal radiographs; US tended to indicate a higher, more cephalic level than did radiography in the majority of cases. This bias is graphically demonstrated in Figure 5.


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  		TABLE 1. Comparison of Prenatal US and MR Images and Postnatal MR Images with Postnatal Radiographs

 


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  		Figure 5. Graph illustrates the tendency for a lesion to be assigned a higher, more cephalic level at prenatal US than that assigned at postnatal spinal radiography. {bullet} = lesions assigned identical levels with both modalities, {circ} = lesions assigned different levels.

 
Results from a comparison between duplicate readings of the same postnatal spinal radiographs as a measurement of intraobserver variability are shown in Table 2. This comparison showed that the criterion for excellent agreement was met, with an observed agreement of approximately 92% versus an expected agreement of approximately 66% ({kappa} = 0.78). Agreement was again defined as concordance within one spinal level. The two duplicate readings that differed by more than one spinal level were attributed to the poor quality of the initial image, which was improved with digitization in the second reading.


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  		TABLE 2. Comparison between Duplicate Readings of the Same Postnatal Spinal Radiographs

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
The anatomic level of the myelomeningocele has traditionally been used to place disease in fetuses with myelomeningocele into stratified categories. Lesion level is correlated with both leg function and shunt-dependent hydrocephalus (5–7,11). In the past, lesion level was determined prenatally with transabdominal US, but more recently, prenatal MR imaging and three-dimensional US are also used, usually as adjunctive procedures (4,12).

Until now, the accuracy of the prenatal level determination has been of minor importance because prenatal decision making was confined to the question of whether to terminate the pregnancy. If termination was declined, the only other option was conventional postnatal closure. In these circumstances, the majority of such fetuses underwent repair at birth, regardless of the lesion level, and 80%–90% of fetuses required insertion of a shunt. Recently, however, that situation has changed substantially with the introduction of a third option, intrauterine myelomeningocele repair. In other research, we found that lesion level is an important determinant of outcome after intrauterine myelomeningocele repair, especially with regard to shunt-dependent hydrocephalus (unpublished data). Accurate determination of the lesion level is critical to the proper counseling of prospective parents of an affected fetus.

The accuracy of a diagnostic test is generally determined by comparing it with a reference standard or benchmark. In the neurosurgery literature (5–7), postnatal spinal radiographs are considered a benchmark for determining the level of a myelomeningocele lesion. Data in the current study suggest that lesion level is accurately assigned by using either postnatal spinal radiographs or postnatal MR images. Results with prenatal images, however, are substantially less reliable. The prenatal US images and prenatal MR images were within one level of the reference standard about 80% of the time; there is a possibility (~20%) that either imaging modality will lead to assignment of the wrong lesion level by two or more segments.

Results of previous studies of US in the diagnosis of myelomeningocele agree with this percentage possibility. Kollias et al (13) found US to be accurate within one spinal level 80% (22 of 28) of the time. In the article by Coniglio et al (11), 30% (five of 15) of their prenatal images differed from postnatal radiographs by two levels or more.

For purposes of prenatal counseling, especially if intrauterine myelomeningocele repair is an option, an error of plus or minus two levels could substantially affect a prospective parent’s decision to terminate a pregnancy or choose between intrauterine and conventional therapy. At present, therefore, caution should be exercised in the counseling of prospective parents regarding the prognosis of the fetus on the basis of analysis that relies heavily on lesion level as a reference. Furthermore, ways should be sought to improve the accuracy of prenatal imaging with both modalities.

The question remains whether MR imaging is equivalent, superior, or complementary to US for prenatal diagnosis of the abnormalities associated with myelomeningocele. For a newly applied diagnostic study to be accepted into general use, it must fulfill a number of requirements (14). First, it has to be safe and not expose the patient to unnecessary risks. Second, it has to be able to help diagnose the problem accurately (in this case, the level of the myelomeningocele lesion). Third, it should provide additional useful information that is not provided by the established study (in this case, US) and that might lead to substantial alterations in patient care. Finally, in the environment of financial awareness today, the test should be affordable.

The biologic effects of high-strength magnetic fields on the developing fetus have been reviewed previously (4). Although the potential exists for a teratogenic effect, study results suggest that MR imaging is not hazardous to the developing fetus (15–18). While results in the current study suggest that prenatal MR imaging with this protocol is roughly equivalent to US in the assignment of lesion level, it must also be remembered that myelomeningocele is invariably accompanied by abnormalities throughout the central nervous system. Hydrocephalus and Chiari type II malformation are common, and other abnormalities, such as agenesis of the corpus callosum, holoprosencephaly, cerebellar dysplasia, and defects in cellular migration, are often observed (19). Therefore, the optimal prenatal study should be capable of depicting these abnormalities and spinal anatomy.

Findings in two studies (20,21) suggest that MR imaging is superior to US for the prenatal depiction of these intracranial anomalies and may provide crucial additional prognostic information for parents trying to decide whether to proceed with intrauterine myelomeningocele repair or terminate the pregnancy. Whether the additional cost of MR imaging can be justified by its ability to depict such intracranial anomalies remains to be answered.

In summary, we have demonstrated that little difference exists between prenatal MR imaging and US in the assignment of a lesion level in a fetus with myelomeningocele. The additional anatomic information provided by MR imaging beyond that available with US might enhance patient counseling and affect the prenatal decision-making process, although those issues were not addressed in the current study. We believe it is reasonable to add fetal MR imaging to the diagnostic armamentarium available to parents of a fetus with myelomeningocele, in view of the additional anatomic information provided. It also appears likely that as the speed and resolution of MR imaging increase and the cost decreases, the advantages of MR imaging will become more apparent. Finally, caution should be exercised when findings at either prenatal US or prenatal MR imaging are used to provide prognostic counseling to parents of fetuses with myelomeningocele, since findings with either prenatal screening tool will lead to misdiagnosis of the lesion level in a substantial number of cases.


   FOOTNOTES
 
Author contributions: Guarantors of integrity of entire study, O.S.A., N.B.T.; study concepts, O.S.A., N.B.T., M.H.S.; study design, O.S.A., N.B.T., M.H.S., G.W.R.; literature research, O.S.A., N.B.T., M.H.S., J.P.B.; clinical studies, O.S.A., N.B.T., J.P.B.; data acquisition, O.S.A., N.B.T., M.H.S., J.P.B.; data analysis/interpretation, O.S.A., N.B.T., G.W.R.; statistical analysis, O.S.A., G.W.R.; manuscript preparation, all authors; manuscript definition of intellectual content, O.S.A., N.B.T.; manuscript editing, revision/review, and final version approval, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

  1. Tulipan N, Bruner JP. Myelomeningocele repair in utero: a report of three cases. Pediatr Neurosurg 1998; 28:177-180.[CrossRef][Medline]
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