VIBE MRI For Evaluating The Normal and Abnormal Gastrointestinal Tract in Fetuses

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fm — 11/9/07
Inaoka et al. Wo m e n ’s I m a g i n g • C l i n i c a l O b s e r v a t i o n s
MRI of Fetal
Gastrointestinal Tract

VIBE MRI for Evaluating the


Normal and Abnormal
W O M E N ’S
IMAGING Gastrointestinal Tract in Fetuses
Tsutomu Inaoka1 OBJECTIVE. The great potential of MRI for assessing gastrointestinal abnormalities in fe-
Hiroyuki Sugimori1 tuses has been described. T1-weighted images may add additional information to T2-weighted
Yoshihito Sasaki2 images in diagnosing fetal gastrointestinal abnormalities. The objective of this study was to as-
Koji Takahashi1 sess the performance of a 3D volumetric interpolated breath-hold sequence (VIBE) in evaluat-
Kazuo Sengoku2 ing the normal and abnormal fetal gastrointestinal tract.
CONCLUSION. VIBE provides high-quality T1-weighted and 3D MR colonography
Nobuhisa Takada1
images for the evaluation of the normal and abnormal gastrointestinal tract in fetuses, and 3D
American Journal of Roentgenology 2007.189:W303-W308.

Tamio Aburano1
MR colonography provides excellent delineation of the meconium.
Inaoka T, Sugimori H, Sasaki Y, et al.
renatal diagnosis of fetal gas- additional information to T2-weighted images

P trointestinal tract malformations,


including bowel dilatation, polyhy-
dramnios, hyperechoic bowel, and
in diagnosing fetal gastrointestinal abnormali-
ties because meconium is more apparent on
T1-weighted than on T2-weighted images [5].
ascites, is commonly made with sonographic Three-dimensional MR images generated
findings. However, these findings are not spe- from T1-weighted images, which were ob-
cific and may relate to transient normal variants tained using 2D or 3D fast gradient-echo MR
[1–3]. In addition, sonography has some disad- sequences, are useful for 3D understanding in
vantages, such as operator dependence, low im- the diagnosis and monitoring of fetal gas-
age contrast, and a small field of view [1–3]. trointestinal tract malformations [4, 7]. For
Therefore, it is occasionally challenging for ob- conventional T1-weighted sequences, a 4-mm
stetric sonographers to assess fetal gastrointes- or greater section thickness is required to per-
tinal abnormalities when accurate recognition form imaging through the fetus during a lim-
of the bowel condition is required to determine ited acquisition time [2–7]. However, addi-
fetal and neonatal management [1, 2]. tional thin sections of 3 mm or less are needed
Keywords: fetus, gastrointestinal tract, meconium, MR The usefulness of fast MRI, including sin- to better characterize abnormal findings and to
colonography, MRI, obstetrics, pediatrics, volume gle-shot fast spin-echo sequences, for evaluat- make 3D MR images of sufficient quality be-
interpolated breath-hold imaging, women’s imaging
ing fetal abdominal disorders has been re- cause a mean diameter of the intestine in fe-
DOI:10.2214/AJR.07.2063 ported with increasing frequency. The great tuses after 20 weeks’ gestation is 3 mm or
potential of MRI for the assessment of the fetal greater [4, 6, 7]. Conventional sequences are
Received February 17, 2007; accepted after revision gastrointestinal tract has been described; in di- still limited in temporal resolution for obtain-
June 24, 2007. agnosing abnormal cases, it is important to as- ing T1-weighted images of such thin sections
1Department
sess whether meconium is present in the fetal with adequate anatomic coverage for evaluat-
of Radiology, Asahikawa Medical College,
2-1-1-1 Midorigaoka-Higashi, Asahikawa City, Hokkaido, bowel [2–5]. MRI is more sensitive than ing fetal gastrointestinal abnormalities.
078-8510, Japan. Address correspondence to T. Inaoka sonography for detecting the presence of Recently, a 3D volumetric interpolated
(tinaoka@asahikawa-med.ac.jp). meconium [2]. The location and amounts of breath-hold sequence (VIBE), which is a
2Department
meconium in the fetal bowel depend on gesta- modified fast 3D gradient-echo sequence,
of Obstetrics and Gynecology, Asahikawa
Medical College, Asahikawa City, Hokkaido, Japan.
tional age; however, the accumulation of has been applied to T1-weighted images in
meconium may steadily advance from the anal clinical body MRI [8–10]. This sequence
WEB canal in a normal fetus after 20 weeks’ gestation may provide isotropic or nearly isotropic
This is a Web exclusive article. [2–6]. Meconium exhibits an intermediate or resolution in three dimensions while pre-
AJR 2007; 189:W303–W308
low signal intensity on T2-weighted images serving wide anatomic coverage in a short
and a high signal intensity on T1-weighted im- acquisition time [8–10]. Motion artifacts are
0361–803X/07/1896–W303
ages because of its high protein and mineral also reduced by the rapid data acquisition
© American Roentgen Ray Society content [2–4]. T1-weighted images may add [10]. Therefore, 3D MR images of high qual-

AJR:189, December 2007 W303


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Inaoka et al.

TABLE 1: Normal Gastrointestinal Tract Features Having High Signal Intensity in Fetuses 19 Weeks 4 Days’ to 40 Weeks
5 Days’ Gestational Age
Small Intestine Colon
Fetal Age and Imaging Type Stomach Duodenum Proximal Distal Ascending Transverse Descending Sigmoid Rectum
Overall (n = 28)
T2-weighteda 28 (100) 28 (100) 23 (82.1) 19 (67.9) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
T1-weightedb 0 (0) 0 (0) 11 (39.3) 15 (53.6) 26 (92.9) 28 (100) 28 (100) 28 (100) 28 (100)
MR colonographyc 0 (0) 0 (0) 9 (32.1) 12 (42.9) 26 (92.9) 28 (100) 28 (100) 28 (100) 28 (100)
< 32 weeks’ gestation (n = 12)
T2-weighteda 12 (100) 12 (100) 7 (58.3) 6 (50) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
T1-weightedb 0 (0) 0 (0) 5 (41.7) 8 (66.7) 12 (100) 12 (100) 12 (100) 12 (100) 12 (100)
MR colonographyc 0 (0) 0 (0) 3 (25) 5 (41.7) 12 (100) 12 (100) 12 (100) 12 (100) 12 (100)
≥ 32 weeks’ gestation (n = 16)
T2-weighteda 16 (100) 16 (100) 16 (100) 13 (81.3) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
T1-weightedb 0 (0) 0 (0) 6 (37.5) 7 (43.8) 14 (87.5) 16 (100) 16 (100) 16 (100) 16 (100)
MR colonographyc 0 (0) 0 (0) 6 (37.5) 7 (43.8) 14 (87.5) 16 (100) 16 (100) 16 (100) 16 (100)
Note—Data are number (%) of patients.
a HASTE.
American Journal of Roentgenology 2007.189:W303-W308.

b Three-dimensional volumetric interpolated breath-hold fast gradient-echo.


c Three-dimensional.

ity can be available because of the resultant tuses with a normal gastrointestinal tract ranged ium-based contrast material was used. The preg-
minimization of partial volume averaging ef- from 19 weeks 4 days to 40 weeks 5 days (mean, 30 nant patients were instructed to walk for 10 minutes
fects and motion artifacts [8, 10]. We at- weeks 5 days). These fetuses had other abnormali- before the MR examination.
tempted to obtain thin-section T1-weighted ties: CNS abnormalities (n = 10), urogenital abnor-
images through the fetus using VIBE and to malities (n = 7), musculoskeletal abnormalities MR Image Processing and Evaluation
generate 3D MR colonography images of the (n = 6), and hydrops fetalis (n = 1). Four of those We generated 3D MR colonography images
fetus from the VIBE data sets. The purpose fetuses had normal findings. The remaining seven from the VIBE data sets using a volume-render-
of this study was to assess the performance fetuses were confirmed as having gastrointestinal ing algorithm at a computer workstation (Aquar-
of VIBE in evaluating the normal and abnor- abnormalities, which included duodenal atresia ius, version 3.2, Elk Corporation). T2-weighted
mal fetal gastrointestinal tract. (n = 3), congenital diaphragmatic hernia (n = 2), images, T1-weighted images, and 3D MR
gastroschisis (n = 1), and ileal atresia with meco- colonography images were simultaneously as-
Materials and Methods nium peritonitis (n = 1). sessed on an image viewer. In the fetuses with a
Subjects normal gastrointestinal tract, signal characteris-
Between June 2004 and September 2006, 45 MRI Protocol tics of the stomach, the duodenum, the proximal
patients underwent fetal MRI after sonography in MRI was performed on a 1.5-T MR unit (Mag- small intestine, the distal small intestine, the as-
our institute. Fetal MRI was limited to cases in netom Sonata, Siemens Medical Solutions) using a cending colon, the transverse colon, the descend-
which complex anomalies were suspected at sec- phased-array body coil. In the fetal MR examina- ing colon, the sigmoid colon, and the rectum were
ond- or third-trimester fetal sonography screening tions, HASTE T2-weighted sequences (TR/TEeff, assessed. The small intestine was subdivided into
or in which the sonography results were equivocal 1,100/81; flip angle, 150°; field of view, 400 mm; the duodenum, the proximal small intestine, and
or undetermined. Before the examination, all sub- slice thickness, 5.0 mm; section gap, 1.0 mm; slice the distal small intestine because a distinction be-
jects were informed about the procedure and the number, 18; image matrix, 256; bandwidth, 476 tween the jejunum and the ileum was not feasible.
safety of the technique by obstetricians, and all Hz/pixel; turbo factor, 164; 1 signal acquisition; The identification of the respective intestine was
provided their informed consent. Of the 45 partic- scanning time, 20 seconds) were obtained through made on the basis of the anatomic location, the
ipants, 35 who fulfilled the following inclusion the fetus in the transverse, sagittal, and coronal continuity, and the presence or absence of haus-
criteria were enrolled in this retrospective study. planes. T1-weighted images were obtained through tra. The liver was used as a landmark of the ana-
The first criterion was that HASTE T2-weighted the fetus in the coronal plane using VIBE (TR/TE, tomic position in the fetal abdomen. Signal inten-
and VIBE T1-weighted images were both ob- 4.45/1.34; flip angle, 15°; field of view, 400 mm; sity (high or low) of the precise intestinal
tained through the fetus. The second criterion was slice thickness, 3 mm; section gap, 0–0.6 mm; num- segments was subjectively determined on both
that diagnoses were confirmed after delivery in ber of slices, 32–40; image matrix, 256 [interpola- T2- and T1-weighted images. Particularly on T1-
our institute. Although there was one twin preg- tion, 512]; bandwidth, 490 Hz/pixel; 1 signal acqui- weighted images, we compared the signal inten-
nancy, we examined only the indicated fetus. sition; scanning time, 24–28 seconds). Although sity with that of muscle because the T1-weighted
On the basis of the medical records of postnatal the images were basically obtained during a single signal in the small and large intestine is greater
diagnoses, 28 of the 35 fetuses had a normal gas- breath-hold, these were sometimes acquired during than that of muscle [4]. On 3D MR colonography
trointestinal tract. The gestational ages of the fe- quiet respiration. Neither sedatives nor IV gadolin- images, visualization of the intestine was judged

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MRI of Fetal Gastrointestinal Tract

TABLE 2: Fetuses with Gastrointestinal Abnormalities


Patient No. Gestational Age Diagnosis T1-Weighted VIBE and 3D MR Colonography Findings
1 28 wk 6 d Gastroschisis No intestinal complications (volvulus, atresia, perforation)
2 29 wk 5 d Duodenal atresia No other intestinal complications
3 30 wk 2 d Ileal atresia, meconium peritonitis Ileal atresia
4 33 wk 0 d Left diaphragmatic hernia Colon involved, liver not involved
5 34 wk 0 d Duodenal atresia No other intestinal complications
6 34 wk 2 d Duodenal atresia No other intestinal complications
7 37 wk 5 d Left diaphragmatic hernia Colon involved, liver not involved
Note—VIBE = volumetric interpolated breath-hold.
American Journal of Roentgenology 2007.189:W303-W308.

A B C
Fig. 1—MR images of fetus at 35 weeks 4 days’ gestation show normal gastrointestinal tract. St = stomach, pSm = proximal small intestine, dSm = distal small intestine,
As = ascending colon, Tr = transverse colon, Ds = descending colon, Sg = sigmoid colon, R = rectum, L = liver, B = urinary bladder.
A, Coronal T2-weighted image shows high signal intensity from stomach to small intestine but low signal intensity from transverse colon to sigmoid colon.
B, Coronal 3D T1-weighted gradient-echo image shows low signal intensity in stomach and high signal intensity from distal small intestine to colon and rectum. Proximal
small intestine shows higher signal intensity than liver does.
C, Volume-rendered image in anteroposterior view visualizes through distal small intestine to rectum and also shows liver.

to be satisfactory when its signal intensity was Results Discussion


distinguished from that of background and when In all 28 normal and seven abnormal cases, In fetal MRI, signal intensity of the gas-
the continuity of the intestine was confirmed. HASTE T2-weighted imaging, VIBE T1- trointestinal tract is basically determined by
We divided the fetuses with a normal gas- weighted imaging, and 3D MR colonography the location and amounts of swallowed am-
trointestinal tract into two age groups of less than were performed. A summary of the normal niotic fluid and meconium [2–4, 6]. Meco-
32 weeks’ gestation (n = 12) and 32 weeks’ or findings is presented in Table 1; abnormal nium is formed from secretions of the liver
more gestation (n = 16) on the basis of a previous findings are listed in Table 2. In the three and intestinal glands, desquamated intestinal
report [2]. Whether there was herniation, obstruc- cases of duodenal atresia, VIBE imaging and epithelium, and some amniotic fluid after 13
tion, dilatation, or narrowing of intestine in the fe- 3D MR colonography did not add to the diag- weeks and slowly migrates from the small
tal gastrointestinal abnormalities was qualita- nosis. In the two diaphragmatic hernias and intestine to the colon and rectum [4]. There-
tively assessed. The diagnosis of herniation was one gastroschisis case, VIBE imaging and 3D fore, signal intensity of the intestine greatly
made when the intestine was seen outside the ab- MR colonography clearly showed colon in- varies depending on gestational age. Ac-
domen, whereas the diagnosis of obstruction was volvement in the defect but did not provide cording to previous reports [2–4], signal in-
made when the intestine was constricted with a additional information. In the case of ileal tensity of the stomach through the proximal
resultant dilatation of the bowel proximal to the atresia with meconium peritonitis, the ileal small intestine is hyperintense on T2-
site of obstruction. atresia was confirmed (Figs. 1–3). weighted images after 26–27 weeks’ gesta-

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Inaoka et al.

hyperintense in more than half of cases be-


fore 32 weeks’ gestation; thereafter, it re-
mains hyperintense in almost 40% of cases
[3]. The visualization of the proximal small
intestine on T1-weighted images is limited
[2–4]. In our results, the percentages of the
respective intestine segments showing a high
signal intensity on HASTE T2-weighted and
VIBE T1-weighted images were equal or su-
perior to the previously published data; how-
ever, the percentage of the proximal small
intestine having a high T1 signal was much
higher than in previous reports. The rate of
the distal small intestine showing a high sig-
nal intensity on HASTE T2-weighted im-
ages in fetuses at 32 weeks’ gestation or
longer was higher than that in fetuses at less
than 32 weeks’ gestation. The rate of the
proximal small intestine showing a high sig-
nal intensity on T1-weighted images in fe-
American Journal of Roentgenology 2007.189:W303-W308.

tuses at less than 32 weeks’ gestation is


higher than that in fetuses at 32 weeks’ ges-
A B tation or longer.
The VIBE sequence, which is a modified
3D fast gradient-echo sequence, uses a sym-
metric echo in the read direction, partial in-
plane Fourier sampling in the phase-encoding
direction, and asymmetric echo sampling and
sinc interpolation along the partition direction
[8–11]. This sequence has the ability to pro-
vide thinner sections, higher signal-to-noise
ratio, higher image contrast, and a shorter ac-
quisition time than conventional sequences
while preserving adequate anatomic coverage
[8–11]. In fetal MRI, rapid data acquisition is
important because it may reduce motion arti-
facts of both mothers and fetuses. Indeed,
VIBE enabled us to obtain 32–40 sections of
3-mm section thickness through the fetuses
with a short acquisition time, and it provided
high-quality T1-weighted imaging and 3D
MR colonography of the fetuses.
Several investigators have suggested that
3D MR images were useful in surgical simu-
lation and treatment planning before birth [7,
12–14]. Rotation of 3D MR colonography
C D images on an image viewer aids in under-
Fig. 2—MR images of fetus with congenital diaphragmatic hernia at 37 weeks 5 days’ gestation. R = rectum, standing the anatomic position of the intestine
L = liver. and the relation between the intestine and the
A and B, Coronal T2-weighted (A) and 3D T1-weighted gradient-echo (B) images show herniated intestine in left liver. We have actually presented 3D MR
thoracic space. Extent of colon into left thoracic space (arrows) is clearly visualized.
C and D, Volume-rendered images in anteroposterior (C) and posteroanterior (D) views show anatomic relationship colonography images, with their excellent de-
between herniated colon and liver. Colon beyond diaphragm (arrows, C), is clearly shown. Liver has normal shape. lineation of the meconium, at family counsel-
Small intestine is not visualized. ing and at conferences with neonatologists
and pediatric surgeons. In our results, T1-
weighted and 3D MR colonography images
tion, whereas that of the distal small intes- signal intensity from the sigmoid colon to of sufficient quality were generated from the
tine through the colon is intermediate to low the rectum is always bright after 23 weeks’ same VIBE data sets. The percentages of the
signal intensity. On T1-weighted images, gestation [2, 3]. The distal small intestine is recognition of the proximal and distal small

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MRI of Fetal Gastrointestinal Tract

Fig. 3—MR images of fetus with gastroschisis at 28 weeks 6 days’ gestation. Sm = small intestine, As = ascending
colon, Tr = transverse colon, Ds = descending colon, R = rectum, L = liver, St = stomach.
A, Sagittal T2-weighted image shows extraabdominal bowel (arrows) has low signal intensity.
B, Coronal 3D T1-weighted gradient-echo image shows absence of colon in abdominal cavity.
C and D, Sagittal multiplanar reformatted (MPR) T1-weighted images show eviscerated bowel has high signal
intensity, which is consistent with normal colon. Small intestine appears normal. When coronal image sections
cannot show abnormal findings, MPR images are useful for evaluation.
E–H, Volume-rendered images in anteroposterior (E), oblique left-to-right (F), left-to-right (G), and right-to-left (H) views
show condition of eviscerated bowel segments of gastroschisis. No volvulus or bowel atresia is seen. Site of abdominal wall
defect is predictable because intestine becomes constricted just at defect site (arrows). Small intestine is not visualized.

C
American Journal of Roentgenology 2007.189:W303-W308.

A B D

E F H

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Inaoka et al.

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W308 AJR:189, December 2007

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