AJR 2005; 184:993-998
© American Roentgen Ray Society
Supplemental Value of MRI in Fetal Abdominal Disease Detected on Prenatal Sonography: Preliminary Experience
Brook J. Hill1,2,
Bonnie N. Joe1,
Aliya Qayyum1,
Benjamin M. Yeh1,
Ruth Goldstein1 and
Fergus V. Coakley1
1 Department of Radiology, University of California San Francisco, 505 Parnassus
Ave., Box 0628, M-372, San Francisco, CA, 94143–0628.
2 Present address: Division of Health Sciences and Technology, Harvard Medical
School–Massachusetts Institute of Technology, 260 Longwood Ave., Rm.
213, Boston, MA 02115.
Received March 19, 2004;
accepted after revision June 8, 2004.
Address correspondence to B. N. Joe
(Bonnie.Joe{at}radiology.ucsf.edu).
Abstract
OBJECTIVE. Our aim was to determine the supplemental value of MRI in
fetal abdominal disease detected on prenatal sonography.
CONCLUSION. Our preliminary results suggest the primary supplemental
value of MRI relative to sonography in fetal abdominal disease lies in
improved tissue characterization rather than in improved anatomic
characterization.
Introduction
Fetal abdominal disease encompasses a wide array of conditions that can
arise from nearly every structure in the abdominal cavity. The prognosis and
treatment of these diseases are equally variable. Management options include
corrective fetal surgery (e.g., bladder outlet obstruction), postnatal
resection and chemotherapy (e.g., neuroblastoma), and surveillance (e.g.,
small ovarian cysts)
[1–3].
Accordingly, accurate diagnosis is crucial for optimal treatment planning and
parental counseling; prenatal sonography is the primary technique for the
detection and characterization of these anomalies
[4]. Prenatal MRI is
increasingly recognized as a useful supplement to sonography in difficult or
complex cases of fetal disease, particularly in neurologic abnormities
[5,
6]. However, only a small
number of studies have reported on the role of MRI in fetal abdominal disease
[7–10],
and these publications have not systematically examined the supplemental value
of MRI relative to sonography in this setting. Therefore, we undertook this
study to determine the supplemental value of MRI in fetal abdominal disease
detected on prenatal sonography.
Materials and Methods
Subjects
This was a retrospective single-institution study approved by our Committee
on Human Research. Informed consent was not required. We identified all
fetuses referred for MRI for abnormalities seen or suspected on detailed
prenatal sonography between 1996 and 2003 (we did not include the fetuses of
pregnant women who were referred for MRI for primarily obstetric conditions,
such as placenta accreta). The study group consisted of 422 fetuses in 334
women (250 singleton pregnancies, 80 twin pregnancies, and 4 triplet
pregnancies). The mean maternal age was 30 years (range, 14–48 years).
The mean gestational age was 25 weeks (range, 18–39 weeks). The
indications for MRI were neurologic disorders (n = 258), thoracic
abnormalities (n = 49), abdominal disease (n = 8), or other
conditions (n = 19). For purposes of classification, sacrococcygeal
teratoma and congenital diaphragmatic hernia were considered neurologic and
thoracic abnormalities, respectively. All available clinical, radiologic, and
histopathologic records, both prenatal and postnatal, of those cases referred
for further evaluation of abdominal disease detected on prenatal sonography
were reviewed to determine the final diagnosis and clinical outcome. All
pertinent data were recorded. Three of the fetuses with abdominal disease were
included in prior reports
[11–13].
Sonography and MRI Techniques
Sonography was performed with state-of-the-art equipment (Sequoia, Acuson)
and 4.0-8.0–MHz sector or curved-array multifrequency electronically
focused transducers. The examinations were combined gray-scale and color
Doppler studies. All sonography studies were reviewed and reported by one of
four attending radiologists with extensive experience in prenatal sonography.
MRI was performed with a 1.5-T superconducting magnet (Signa, GE Healthcare)
and a four-element phased-array surface coil provided by the manufacturer.
T1-weighted MR images were obtained by using a breath-hold spoiled
gradient-echo sequence (TR range/TE, 100–140/4.2; 70–90° flip
angle; 256 x 160–256 matrix; 1 signal acquired). T2-weighted
images were obtained using a single-shot rapid-acquisition with relaxation
enhancement sequence (TR/TE range, infinite/100–120; 256 x
160–256 matrix). A variable bandwidth was used for all sequences.
Sequence acquisition times were all less than 30 sec. The section thickness
was 4–6 mm (6- mm thickness used for T1-weighted sequences), and the
intersection gap was 0–1 mm. The field of view, number of sections,
section thickness, and intersection gap were optimized for each patient by the
supervising radiologist. In suspected congenital hemochromatosis, a
T2*-weighted gradient-echo sequence (TR/TE, 130/20; 20° flip
angle) of the fetal liver and an in- and out-of-phase T1-weighted
gradient-echo sequence (40/2.1 and 4.2; 70° flip angle) of the maternal
liver were also performed.
MR Image Interpretation and Assessment of Supplemental Value
All MRI studies were reported by one of two attending radiologists who were
experienced in prenatal abdominal MRI. Clinical and previous imaging results,
including sonography findings, were available during the interpretation of MRI
studies. MRI was considered to have supplemental value if the diagnosis
recorded in the MRI report more closely corresponded to the final diagnosis
than to that recorded in the sonography report. The supplemental value of MRI
findings was further classified into tissue or anatomic characterization; the
former was defined as MRI signal changes that indicated a histopathologic
diagnosis for a mass or diseased organ but were independent of lesion or
disease location, whereas the latter was defined as structural findings
related to lesion location that indicated a particular diagnosis.
Results
Eight (1.9%) of 422 fetuses that underwent MRI were referred for evaluation
of abdominal disease. Final individual diagnoses were established for six of
these eight fetuses, which consisted of subdiaphragmatic sequestration, cecal
atresia with proximal bowel dilatation, congenital hemochromatosis, mesenteric
lymphangioma, exophytic hepatic hemangioma, and ectopic ureter with distal
dilatation. Two other fetuses were lost to follow-up. The sonography findings,
MRI findings, final diagnoses, and supplemental value of MRI are detailed for
all eight cases in Table 1.
MRI was of supplemental value relative to sonography because of improved
tissue characterization in three of the six cases with established diagnoses,
specifically, in the fetuses with congenital hemochromatosis, subdiaphragmatic
sequestration, and cecal atresia with proximal bowel dilatation. In the case
of congenital hemochromatosis, MRI showed diffusely low T2* signal
intensity of the fetal liver relative to the maternal liver and fetal spleen
(Fig. 1). There was no evidence
of potentially confounding diffuse fatty infiltration of the maternal liver on
in- and out-of-phase gradient-echo imaging. The liver echotexture was
unremarkable on the prenatal sonography. On the basis of MRI findings, in
combination with a maternal history of two prior pregnancies with congenital
hemochromatosis, labor was induced at 31 weeks' gestation. The diagnosis of
congenital hemochromatosis was confirmed postnatally, and medical therapy for
severe neonatal hepatic failure was initiated. Neonatal liver function
gradually normalized, and hepatic transplantation was not required. The child
is now 5 years old with normal hepatic function. In the case of
subdiaphragmatic sequestration, sonography detected a mass in the left upper
quadrant, and the differential diagnosis included both subdiaphragmatic
sequestration and neuroblastoma. MRI showed a left upper quadrant mass of
uniformly hyperintense T2 signal intensity (Figs.
2A and
2B), favoring the diagnosis of
sequestration over neuroblastoma. The parents were appropriately reassured,
and the diagnosis was confirmed by postnatal resection. In the case of cecal
atresia with proximal bowel dilatation (Figs.
3A,
3B, and
3C), sonography detected a
nonspecific hypoechoic mass in the center of the fetal abdomen. MRI showed an
intraperitoneal mass of high T1 and low T2 signal intensity, consistent with
meconium. The presence of meconium was considered indicative of a
gastrointestinal anomaly, as confirmed at postnatal surgery.
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Fig. 1. —31-week fetus with congenital hemochromatosis. Coronal
T2*-weighted MR image (TR/TE, 130/20; 20° flip angle) shows
that fetal liver (black arrow) is of diffusely low T2*
signal relative to maternal liver (white arrow), highly suggestive of
congenital hemochromatosis. Diagnosis was confirmed postnatally.
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Fig. 2A. —28-week fetus with subdiaphragmatic sequestration. Coronal
T2-weighted single-shot fast spin-echo MR image (TR/TE, infinite/96) shows
2.7-cm left subdiaphragmatic mass (arrow) of high T2 signal.
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Fig. 2B. —28-week fetus with subdiaphragmatic sequestration. Sagittal
T2-weighted MR image shows mass (black arrow) above normal left
kidney (white arrow). Fetal stomach (S) is filled with fluid. MRI
diagnosis of subdiaphragmatic sequestration was confirmed at neonatal
surgery.
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Fig. 3B. —23-week fetus with cecal atresia. Coronal T1-weighted spoiled
gradient-echo MR image (TR/TE, 140/4.2; 70° flip angle) shows
intraabdominal mass (horizontal white arrow) containing
high-T1-signal-intensity material closely associated with tubular structure
(vertical white arrow) containing similar material.
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Fig. 3C. —23-week fetus with cecal atresia. Coronal T2-weighted single-shot
fast spin-echo MR image (infinite/96) shows that same mass (arrow)
contains material of low T2 signal intensity, consistent with meconium. Note
normal bladder (B). Diagnosis of gastrointestinal anomaly was suggested
on basis of MRI findings, and cecal atresia was confirmed at surgery.
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MRI was noncontributory in the fetus with mesenteric lymphangioma and
simply confirmed the sonography findings of a multicystic abdominal mass
(Figs. 4A and
4B). MRI provided inferior
anatomic characterization in the fetuses with exophytic hepatic hemangioma and
ectopic ureter with distal dilatation. In the fetus with an exophytic hepatic
hemangioma, sonography showed a right upper quadrant mass with feeding vessels
emanating from the liver, suggestive of a hepatic origin. MRI showed a
nonspecific mass in the right upper quadrant, with no features to suggest the
organ of origin or the tissue diagnosis (Figs.
5A,
5B,
5C, and
5D). Postnatal resection
revealed a large cavernous hemangioma arising from the liver. In the case of
an ectopic ureter with distal dilatation, both sonography and MRI showed a
rightsided multicystic dysplastic kidney and two fluid-filled midline
structures arising from the fetal pelvis. The anteriorly located fluid-filled
structure in the pelvis was identified on sonography as the bladder, and the
proffered differential diagnosis for the posteriorly located structure
included a dilated ureter or seminal vesicle cyst. On MRI, the posteriorly
located fluid-filled structure was considered to be the bladder and the
anterior structure was considered to be an urachal diverticulum (Figs.
6A and
6B); the possibility of
underlying posterior urethral valves was also suggested in view of the size of
the apparent bladder. At postnatal surgery, the anteriorly located
fluid-filled structure was found to be the bladder, whereas the posteriorly
located structure was found to be a massively dilated distal ureter.
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Fig. 4A. —20-week fetus with cystic abdominal mass. Axial T2-weighted
single-shot fast spin-echo MR image (TR/TE, infinite/96) shows 5.5-cm
multilocular cystic mass (asterisk) in fetal abdomen and normal
kidneys (arrows).
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Fig. 4B. —20-week fetus with cystic abdominal mass. Sagittal T2-weighted MR
image shows mass (asterisk), which was presumed to be mesenteric
cyst. Follow-up imaging after birth failed to show mass, and no intervention
was performed.
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Fig. 5C. —30-week fetus with exophytic hepatic hemangioma. Coronal T1-weighted
spoiled gradient-echo MR image (TR/TE, 140/4.2; 70° flip angle) shows
large homogenous mass (asterisk) of moderate signal intensity in left
upper quadrant.
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Fig. 5D. —30-week fetus with exophytic hepatic hemangioma. Coronal T2-weighted
single-shot fast spin-echo MR image (infinite/96) shows heterogeneity within
mass (asterisk), which appears to be adjacent to liver but is not
clearly of hepatic origin.
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Fig. 6A. —Fetus with dilated ectopic ureter. Sagittal gray-scale sonogram
obtained at 29 weeks' gestation shows two fluid-filled masses in abdomen and
pelvis. Smaller structure (arrow) was correctly identified as fetal
bladder, and larger structure (asterisk) was thought to represent
either dilated ureter or seminal vesicle cyst.
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Fig. 6B. —Fetus with dilated ectopic ureter. Sagittal T2-weighted single-shot
fast spin-echo MR image (TR/TE, infinite/96) obtained at 30 weeks' gestation
shows two cystic fluid-filled masses in fetal pelvis. Anterior structure
(arrow) was thought to be urachal diverticulum, whereas posterior
structure (asterisk) was thought to represent bladder. At surgery,
anterior mass was found to be bladder, and posterior mass was dilated distal
ureter.
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Discussion
In general, fetal MRI is considered a valuable complement to prenatal
sonography. The most common indications for fetal MRI are the evaluation of
suspected brain or spinal anomalies such as callosal agenesis or
myelomeningocele. The next most common is the evaluation of fetal thoracic
abnormalities, including congenital diaphragmatic hernia. Fetal abdominal
disease is an uncommon indication for fetal MRI (1.9% of cases in this
study).
This study shows both the usefulness and limitations of MRI in the prenatal
evaluation of fetal abdominal disease. MRI was particularly helpful in
providing tissue characterization when sonography was nonspecific. MRI helped
confirm the diagnosis of congenital hemochromatosis through the finding of
reduced hepatic T2* signal intensity in one case, distinguished a
subdiaphragmatic sequestration from a neuroblastoma by virtue of its high T2
signal intensity in another case, and identified a dilated loop of bowel
immediately proximal to a cecal atresia because of the characteristic high T1
and low T2 signal intensity of meconium in a third case. Conversely, MRI
proved inferior in relation to sonography in anatomic characterization in two
cases: In one case, MRI could not differentiate which of two fluid-filled
structures in the pelvis was the bladder, and in another case, MR images
showed a large abdominal mass but could not identify the liver to be the organ
of origin. The improved anatomic localization on sonography in these cases
probably relates to the superior real-time capability and spatial resolution
of sonography. However, these limitations of MRI relative to sonography may be
only temporary because MRI technology continues to improve with development of
faster pulse sequences and higher- field-strength magnets.
The cases presented in this study are unusual. For example, cecal atresia
with proximal bowel dilatation diagnosed prenatally on MRI is not described in
the literature. Only one other case of subdiaphragmatic sequestration
evaluated on prenatal MRI has been reported
[14], and MRI in that case
also showed a well-circumscribed subdiaphragmatic mass superior to and
separate from the kidney that was of marked T2 signal hyperintensity, favoring
the diagnosis of subdiaphragmatic sequestration over neuroblastoma. Only two
other cases of hepatic hemangioma evaluated on prenatal MRI have been reported
[15,
16]. In both cases, MRI showed
a heterogeneous tumor closely associated with the liver. The unusual mix of
diagnoses in our series probably reflects two factors. First, our institution
serves as a tertiary referral center for complex fetal anomalies so that
obscure and rare diagnoses are to be expected. Second, the increasing use of
screening sonography may have altered the range of fetal abdominal
abnormalities that are encountered. This has practical implications for all
radiologists involved in prenatal imaging. For example, the fetus with
presumed mesenteric lymphangioma in our series would never have been diagnosed
in the absence of prenatal sonography because the lesion had resolved by the
time neonatal imaging was performed.
Our study has several limitations. First, this was a retrospective study
involving a relatively small number of cases with fetal abdominal
abnormalities (eight fetuses with abdominal disease out of 422 cases
undergoing MRI). Such small numbers presumably reflect the rarity of fetal
abdominal disease, the adequacy of sonographic evaluation in most cases, and
our strict definition of abdominal disease that excluded sacrococcygeal
teratoma, myelomeningocele, and congenital diaphragmatic hernia (we considered
such conditions to be primarily neurologic or thoracic). Second, MRI was
performed only in problematic cases in which sonography was inconclusive or in
which additional information was desired. This referral mechanism introduces a
large selection bias, although this is the customary practice in selecting
patients for fetal MRI at our institution and elsewhere. Finally, the study
was not blinded or randomized and was based on retrospective review of patient
records and reports. Nonetheless, this methodology allowed us to assess the
real-life supplemental value of MRI as performed in the clinical setting.
Given the tailored nature of each study, it would have been impractical to ask
independent reviewers to interpret the MR images without clinical information.
Indeed, because the mix of images and sequences was so specific to each case
and suspected diagnosis, the structure of interest would have been immediately
apparent to any blinded reviewer.
In conclusion, fetal abdominal disease is a rare indication for MRI; our
preliminary results suggest the primary supplemental value of MRI relative to
sonography lies in improved tissue characterization rather than in improved
anatomic characterization.
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Abstract
Introduction
