Peter Reimer, MD #{149} Sanjay Saini, MD Thomas J. Brady, MD #{149} Mark S. Cohen,
Techniques Echo-Planar
could
ference
Index
be identified
in signal
atitis,
terms:
by their
C
intensity.
Magnetic
resonance
#{149} Magnetic
enhancement
770.291
(1).
The
two
principal
#{149} Peter
R. Mueller,
any
to gross
reasons
physiologic
and
the lack
trast
agent
many])
for
motion
of a suitable
this
second(2,3)
bowel
and
various Erlangen,
MR
con-
because
noise ratio abdominal restricted
and
low
liver
(14).
Since
these
MR
improved
nan MR images can variety of strategies
enhancement
bowel
contrast
with
on
aqueous
the
MGH-NMR
Massachusetts
General
RSNA,
1992
a section
was
(Signa;
GE Medical
with
Systems,
Center Hospital
and
Division and
Harvard
of Gastrointestinal Medical
Radiology, School,
32 Fruit
Department St. Boston,
[TR]
size
of 128
and
images
a 10-mm
in eight x 256
pa-
was
used
of 40 cm. These patients bowel lumen enhanceTIW
axial
of 10 mm
gap
section
times
T2W
fat-sup-
(15) were
obtained
thickness gap. pulse
(TIs)
and
Multisection sequences
selected
a invenwith
to approxi-
the null points of fat (TI = 100 msec), and pancreas (TI = 380 msec), and (TI = 800 msec) were used for TIW
oc) and
=
(14,16,17).
with
For
a TE
T2W
(26, 50, and “high-resolution” were
100
obtained
ac-
a multisection
SE pulse sequence was used. these SE images were acquired gle excitation pulse (TR = ) of TEs These
were pulse
of 26 msec
images,
Data for after a sinat a variety
msec) (14,16,17). echo-planar
with
“standard-resolution”
METHODS
performed
thickness
intersection
(64 x 128) (8,10,1 1).
imaging
(T1W) se-
time
imaging. Data for these images quired after a single excitation
ages
of
previ-
Ti-weighted with a pulse
(repetition
A matrix
mate liver spleen
(TR
or its
details
a matrix
im-
size
of
128 x 128, which, for a 40 x 20-cm field of view, yielded an in-plane resolution of 1.6 x 3.1 mm (14,16,17), and provided betten anatomical resolution than did the
Imaging
MR
Received June 27, 1991; revision requested July 24; revision Supported in part by grant CA Pol 48279 from the National development fund, and by the Society of Computed Body Deutsche Forschungsgemeinschaft (grant no. Re 758/1-2). (
with a 5-mm
echo-planar
described
To examine
182:175-179
features,
time [TE] msec], four excitaT2-weighted (T2W) SE images two excitations) were ob-
inversion
a i.5-T
MR
Mil-
resolution, was
, From
of 250/20
with
a
Insta-
the conof the Signa
described
axial images
5-mm intersection sion recovery (IR)
with acquisi-
The alter
technical
been
Echo-planar
agent.
AND
have
The
echo-planar
(14).
pressed
echo-pla-
an
system
size.
at a field of view did not undergo ment.
imaging
be obtained for image
bore
tients.
ana-
tion, we compared different echoplanar techniques for MR imaging of the pancreas. In addition, we exammed the potential utility of bowel lumen
comfort
its patient
tamed
or to dynamic
of conventional
imager,
and
motion studies of the bowel (8,11). Technical advances provide anatomic resolution and S/N values in echo-planar images comparable with those
did not capability
msec/echo tions) and (2,500/50-100,
signal-to-
(S/N) (7,10-13). Reports applications have been to the
scan modification ventional imaging
quence
imaging
of suboptimal
resolution
(Instascan).
Conventional spin-echo (SE)
Mass) have been developed to overcome motion artifacts in MR imaging of the abdomen and chest (5-9). Diagnostic application of echo-planar imaging techniques has been limited, tomic
to provide
capability
ousby
techniques such as Instascan (Advanced NMR Systems, Wilmington,
however,
modified
imaging
this
fast (TurboGer-
echo-planar
waukee)
imaging
(4).
In recent years, FLASH [Siemens,
imager
ogy,
MD
Pancreas’
artifacts
MATERIALS
1992;
PhD
magnetic resonance (MR) imaging has been of limvalue in examining the pancreas
are phase-encoding
MR Radiology
MD,
ONVENTIONAL
ited
dif-
(MR), conresonance (MR), echo planar #{149} Magnetic resonance (MR), pulse sequences #{149} Magnetic resonance (MR), tissue characterization #{149} Pancreas, MR, 770.1214 Pancreas, neoplasms, 770.321, 770.34 #{149} Pancretrast
F. Hahn,
PhD
for High-Resolution MR Imaging ofthe
Recent technical advances in echoplanar magnetic resonance (MR) imaging prompted an investigation of these new techniques in pancreatic MR imaging and evaluation of bowel lumen enhancement with an aqueous bowel contrast agent. In 42 subjects (36 healthy, six with pancreatic disease), various Ti-weighted inversionrecovery and T2-weighted spin-echo fat-suppressed pulse sequences were assessed with an echo-planar technique implemented with a modified clinical MR imager. Single-excitation imaging (echo time, 26 msec) provided a higher (P < .05) signal-tonoise ratio than did conventional spin-echo and all other echo-planar techniques. In i3 (72%) of i8 healthy subjects who did not undergo administration of the contrast agent, the entire pancreas was distinguished from adjoining bowel. In all 18 subjects who underwent contrast-enhanced imaging, a significantly greater (P < .05) intraluminal signal intensity was apparent with all echoplanar pulse sequences and the entire pancreas was identified. In six patients with pancreatic disease, be-
sions
#{149} Peter
images used
the utility with
even
the “mosaic” with
the
images
in previous
T2W
reports
of echo-planar higher
anatomic
method SE pulse
(14,16,17) sequence
of RadiolMA
02114.
received August 8; accepted August 16. Institutes of Health, by the MGH-NMR Tomography. P.R. supported by the Address reprint requests to 5.5.
Abbreviations: C/N = contrast-to-noise IR = inversion recovery, SE = spin echo, signal-to-noise ratio, TE = echo time, TI version time, TR = repetition time, TIW weighted, T2W = T2-weighted.
ratio, S/N =
in-
=
TI-
=
175
Figure 1.
Echo-planar and conventional MR images of the pancreas with no bowel lumen enhancement. (a) T2W high-resolution (single excitation, oo/26) SE image (top) and maximum-resolution (two excitations, 6,000/26) SE image (bottom) in a fasting subject. The pancreas is visualized because signal from netnoperitoneal fat is suppressed. The pancreas has a higher S/N on the single-excitation image, while anatomic resolution is better tional T1W (250/20)
on the two-excitation image. Note (top) and T2W (2,500/50) (bottom)
to achieve a 128 x 256 data matrix and an in-plane resolution of 1.6 x 1.6 mm. This “maximum-resolution”
quired
technique
separate
two
doubled
the breath-hold
seconds.
TR, which
between
the
tions,
ne-
excitations,
which
time from 6 to 12
represents
the
time
two radio-frequency excitaset at 6 seconds to minimize TI
was
effects (14,16,17). SE T2W maximum-nesolution images were also obtained with TEs of 26, 50, and 100 msec. All images were acquired with a constant 62.5% k-space coverage to provide a TEminimum of 26 msec (TEminimum at 100% k-space
coverage
tiab survey
is 73 msec)
examination
high-resolution 26)
image
men
(14).
with
single-excitation covered
during
the
a 6-second
mi-
An
a 21-section T2W
entire
upper
breath
(c/
We
then restricted the pancreas
the cephabocaudal range for subsequent acquisitions.
The subjects
were
instructed
to hold
to
their
breath for the duration of each acquisition (6 seconds for the single-excitation and 12 seconds for the two-excitation technique)
to minimize spatial misregistration tween the multisection acquisitions.
Figure normal ment. c/50)
be-
2.
Echo-planar
(36
was performed
with
a normal
The
portion
bile duct
two
with
pancreatitis, two with pancreatic carcinoma, and two with penipancreatic lymphoma). Eighteen subjects underwent imaging without any bowel preparation and 24
subjects
six patients 176
(18
with
with
#{149} Radiology
a normal
pancreatic
pancreas,
disease),
arrow)
as a high-signal-intensity
all
after
corn-
solution
All subjects had
at computed
in the
a normal
tomography
pathologic with either
informed
of the
can be identified
of a contrast
biopsy
consent
pan-
(CT).
conditions
study was approved ies Committee at our ten
convenimages.
structure.
oral administration as described below. healthy study group
creatic firmed
(b) Comparison on echo-planar
tail
mon
(small
secretions. S/N than
i
ages.
intrapancreatic
gastric a lower
enhanceexcitation, before
oral administration 2. The pancreatic
were
Pan-
con-
or surgery.
The
by the Human Studinstitution, and writwas
obtained
from
all subjects. Lumen
Enhancement 450
Westbury,
mL
of Readi-Cat
NY)
was
orally 15-30 minutes before cording to the manufacturer’s
in 42 sub-
pancreas,
of the
from adjoining on postcontrast im-
(E-Z-Em,
MR imaging
due to native pancreas has
can be clearly distinguished bowel (large arrow) only
In 24 subjects,
jects
MR images
(top) and after (bottom) of 450 mL of Readi-Cat
Bowel
Subjects
gastric antrum also shown. The
pancreas after bowel lumen T2W high-resolution (single SE images of normal pancreas
creas
abdo-
hold.
the hypenintense SE images are
Readi-Cat
2 is a dilute
2
administered
imaging acinstructions.
suspension
of bar-
ium that is commonly used in CT for bowel opacification. This preparation was chosen because of its tonicity (which distends the bowel), well-known administration methodology, safety, wide availability, and predictable signal intensity be-
havior. trast
The
high and
high
material signal
water
was intensity
SE echo-planar
enhance
the
of bowel
loops.
content
intended to bowel MR
images
2%
barium
intnaluminal The
of this
con-
to contribute lumen
on
and
thus
signal
IR
intensity content
of
Readi-Cat 2 renders it opaque at CT and is not a significant contributor to the MR signab intensity. No adverse reactions to the imaging
procedure
material
were
or to the
reported
oral
by any
contrast
subjects.
January1992
fenentiation
(binary
creatic
head,
addition,
images
tively
for
the
structures, and by
decision)
body,
were
Figure 3. Echo-planar MR images of pancreatic carcinoma after bowel lumen enhancement. Two adjacent T2W high-resolution (single excitation, c/50) SE images (10-mm sections with 5-mm gap). The cancinoma (arrow) can be identified as a highsignal-intensity area compared with the normal tissue in the pancreatic head (C/N, 13.8 ± 1.1). Atrophy with fatty replacement is seen in the body and tail of the pancreas. The pancreatic duct is dilated and visible as a high-signal-intensity structure.
by the noise
surrounding of interest
T2W SE (2,500/50,
Pancreatic S/N*
intensity
excitation) Echo-planar
MR
± 4.6
10.6
±
tail.
Re-
the
lu-
measuring
bowel wall. Regions within individual disease were used contrast-to-
(ri
17.3
of the
enhancement was
test
SE (TE, 26 msec) SE (TE, 50 msec) SE (TE, 100 msec) ane expressed
as mean
lumen
with
protocol
well
tolerated
Analysis
the
with-
signal Fisher
experienced dominal MR were analyzed
182
visible
by
analyzed
independently (P.R.,
S.S.,
in the interpretation and CT images. qualitatively
#{149} Number
i
P.R.M.)
of abThe images for clean dif-
signal
Overall
enhancement.
tomic
appeared
signal
interfaces,
with sunno visible the singleAna-
however,
with
had
a CT scan-bike
image
quality
subjects, in fat sup-
apparent
in the
The intrapancreatic common bile duct
was
substruc-
be identified
com-
and distinguished from adbowel with each imaging (Fig 1). This ease in identifiis best explained by intrinsic secretions that appeared hy-
an abnormal
intensity
pancreas.-
relative
to that
of nor-
mal pancreas (Fig 3). Tumor tissue and areas of pancreatitis demonstrated higher signal intensity than pancreas. The also identified
changes
common
bile
diseased by means
such duct,
of
as a di-
dilated
pan-
creatic duct, mesenteric stranding, pancreatic contour deformity. Quantitative With
high-intenwater con-
ture, and portions of the pancreatic duct could be identified as a highsignal-intensity structure in eight (22%) of 36 healthy subjects. In 13 (72%) of 18 subjects without bowel lumen enhancement, the entire could
of
intraluminab and
lated
pancreas-In
in 32 (89%) of 36 healthy as a high-signal-intensity
pletely joining technique cation bowel
and
In both groups (without bowel lumen enhancement), rounding bowel produced motion artifacts with either or two-excitation technique.
morphologic
Analysis
usually (high
images
especially
pancreas
radiologists
and lumen
these
pression
jects
was
distention
did normal areas were
a normal
larger subjects. segment of the
± I standand
bowel
conspicu-
because
and
with
of bowel
varied somewhat among with reduced efficiency
tissue.
patients.
were
tent),
18.1 ± 5.4 12.2 ± 3.4 6.2 ± 2.7
deviation for normal pancreatic t Highest S/N (P < .05)
with
bowel
Preliminary studies in six patients with pancreatic disease and bowel enhancement demonstrated that diseased areas or lesions were seen readily on the basis of their different
analyzed
appearance.
T2W
of surrounding
lumen
the
of back-
(18).
suppression) sity bowel
29.4 ± 96t 18.5 ± 6.4 8.3 ± 3.0
ity
Bowel
improved
deviation
pancreas
Image
< .05).
sharper on single-excitation images than on two-excitation images when the longer breath holds for two-excitation images could not be sustained.
all cases, the echo-planar technique produced diagnostic-quality images free of motion artifacts. With bow-intensity retropenitoneal fat (due to fat
± 7.7
(P
enhancement
signal intensity
Analysis
Subjects
2.9 ± 1.5 13.2 ± 4.5
significant
[mean mean signal =
noise).
Qualitative
36)
=
penintense on IR and SE echo-planar MR images. In the other five subjects, the pancreatic tail could not be distinguished clearly from collapsed or airfilled adjacent bowel. In all subjects with bowel lumen enhancement, the entire pancreas (head, body, and tail) was identified (Fig 2). The difference between the bowel-enhanced and bowel-unenhanced study groups was statistically
Subjects
4.0
TIW
Two-excitation
Volume
-
of lesion
Statistical
one
JR (TI, 100 msec) IR (TI, 380 msec) IR (TI, 800 msec) Single-excitation T2W SE (TE, 26 msec) SE (TE, 50 msec) SE (TE, 100 msec)
overall
13.5
6.8 ± 2.8
Single-excitation
three
over
without
of pancreas]/standard
ground
pancreatic placed
signal intensity of the of interest ( > 25 pixels) patients with pancreatic to calculate lesion-pancreas noise ratio (C/N) (C/N
rank
one
T2W SE (2,500/100,
Images
of back-
RESULTS
excitation)
by
signal
exact test. Variations in S/N among diffenent imaging methods were evaluated with the nonpanametnic Wilcoxon signed
tations)
Image
loops
= 8) four exci-
T1W SE (250/20,
all
de=
MR (n
Conventional
The
the were
of bowel
intensity
Analysis S/N
Imaging Technique and Sequence
Values
(S/N
noise). Intraluminal bowel signal was measured in small bowel
Visibility
*
lumen,
standard
deviation
gions
out
Table 1 Quantitative of Pancreatic
measure-
on bowel
divided
loops
men
duct
was provided of the pan-
intensity
intensity/standard
-
pancreatic
S/N
of background
ground intensity
qualita-
lumen in the region S/N values were cal-
pancreas
respectively, viation
bowel tail.
signal
of the
In
duct.
evaluation of the
from
ments
the
bile
Quantitative measurement
pan-
of anatomic
including
creas and small of the pancreatic
L.
assessed
identification
common
culated
of the
and tail from bowel.
Image
varying
TE,
or
Analysis differences
sue signal intensity related cay were seen on SE images. barly, variation of TI produced
in tisto T2 deSimiTi-
related effects on IR images. Table 1 summarizes the S/N of the pancreas for the three conventional pulse sequences and the nine echo-planar imaging techniques. The single-excitation SE sequence with a TE of 26 msec
provided
the
highest
(P
< .05)
pancreatic S/N. Within each given set of T2W sequences, increase in TE resulted in decreased S/N (Table 1). The high-resolution single-excitation technique showed significantly higher S/N than did the maximum-resolution two-excitation technique (P < .05). On T1W images, the short TI (100 msec) and long TI (800 msec) IR sequences had a significantly (P < .05)
higher with
than
did
a TI of 380
S/N
msec
the sequence (which
was
Radiolosrv
#{149} 177
chosen to minimize or eliminate signab from pancreas and liver). Table 2 summarizes quantitative measurements of bowel lumen enhancement. Intraluminab signal intensity, which was high with all of the pulse sequences evaluated, was significantly higher (P < .05) after oral administration of the bowel contrast agent. The single-excitation T2W SE technique demonstrated a significantly higher S/N (P < .05) than did the two-excitation T2W SE technique. Fluid-filled bowel appeared hyperintense on T1W IR images because the TI used was short compared with the long Ti of the aqueous intrabuminab bowel content.
Table 2 Bowel Lumen
Enhancement
Imaging Technique
and
Unenhanced
Sequence
S/N
Single-excitation
S/N
(n = 18)*
Enhancementt
TIW
IR (TI, 100 msec) IR (TI, 380 msec) IR (TI, 800 msec) Single-excitation
3.9
± 2.0 2.5 ± 1.2 1.5 ± 0.7
47.3 36.5 23.9
± 7.9
7.0 ± 3.1 4.8 ± 2.1 3.3 ± 1.2
55.1 52.3 50.1
± 7.7
4.8
33.4 25.8 24.9
12.1 14.6 15.9
± 7.5 ± 5.7
T2W
SE (TE, 26 msec) SE (TE, 50 msec) SE (TE, 100 msec) Two-excitation T2W
.
Enhanced
18)
(n =
SE (TE, 26 msec) SE (TE, 50 msec) SE (TE, 100 msec)
± 2.7 2.6 ± 1.0 1.7 ± 0.5
Note-Values are expressed as mean ± 1 standard * SI was increased significantly in the postcontrast t Enhancement is expressed as the factor by which
7.9
11.0
±
10.9
± 10.8
16.5
± 5.7
7.0 9.9 14.7
± 2.6 ± 2.6
deviation. group with all pulse sequences the intraluminal S/N increased.
studied
(P < .05).
DISCUSSION In the
current
study,
of echo-planar
the
normal
Signal
the
potential
MR
imaging
pancreas
was
evaluated.
enhancement
of
intensity
to depict
bowel lumen and different echo-planar imaging techniques were used. Echo-planar images are generally bebieved to be limited by a low S/N (8,11,14). Our study demonstrates, however, that abdominal MR imaging with echo-planar techniques provides excellent S/N, probably because motion noise is suppressed by the short acquisition time. study, pancreas
Therefore, S/N actually
in this ex-
ceeded the S/N of our conventional T2W images (Table 1) or those in the literature (19,20). Echo-planar MR imaging provided pancreatic images free of motion artifacts (Fig 1) and thus provided images of improved diagnostic quality. A section thickness of 10 mm and a gap of 5 mm yielded images with an acceptable trade-off of anatomic coverage and S/N. Singleexcitation T2W images, each obtained in 40 msec, showed the overall best performance
organ
in sharp
delineation
of
margins.
The oral administration
of a high-
bowel contrast agent improved the distinction of pancreas from adjoining bowel (Fig 2) and enhanced intraluminab S/N by an average factor of 10-15 (Table 2). Long T2 aqueous gastrointestinal contrast media may well serve as bowel enhancement agents in echo-planar imaging. Increased signal in the bowel lumen signal-intensity
contributes
image
noise
because
the
image
acquisition
nar
image
acquisition
is extremely
short
bowel (21).
time, compared
moves
dur-
Echo-pla-
however, with
all
gross physiologic motion. High signal intensity in intrabuminal bowel is therefore achieved without cost to 178
#{149} Radioboirv
hancement values are tional MR
tensity
liminary
retropenitoneum
and
high-
is feasible. Pancreatic S/N similar to those in convenimaging. Thus, in this pre-
study,
signal-intensity bowel is qualitatively similar to that on CT scans. Studies to investigate the capability of aqueous bowel contrast agents to enhance the entire bowel are currently under way. Quantitative data demonstrated that the single-excitation T2W echoplanar imaging technique with a TE of 26 msec had a significantly (P < .05) higher pancreatic S/N than achieved with two-excitation T2W or single-excitation T1W echo-planar techniques or conventional SE techniques. Multisection two-excitation techniques require a breath hold of about 12 seconds, making them more susceptible to spatial misregistration. There is, however, a trade-off between anatomic resolution and S/N. When the matrix size is increased from 128 x 128 to 256 x 128, the S/N is expected to decrease as a result of the twofold reduction in voxel vobume. Although the expected decrease in S/N is only 21/2, our experimental data demonstrate somewhat lower
are available to the detection
S/N,
pancreas
presumably
as a consequence
of
abdominal tions and
motion between excitathe decrease in TR (from to 6 seconds). Since high S/N and
C/N
are
both
important
ing, single-excitation preferable for routine pancreas. It appears lect
to a conventional
ing
overall image quality. The contrast pattern on fat-suppressed echo-pbanar MR images with a low-signal-in-
images
at a variety
in MR
techniques imaging necessary of TEs:
of focal
imag-
seem of the to cob-
pancreatic
prerequisites
this technique characterization
lesions.
These
le-
might be detected and identified on the basis of their difference in signab behavior and good tissue contrast (Fig 3), as has previously been demonstrated with hepatic MR imaging sions
(9). IR techniques from
nulbing
normal
the
pancreatic
be advantageous (22), despite their
signal
tissue
for lesion
might
detection
limited S/N, belesions have different null therefore appear hypenintense with this TI (22). A prospective controlled study comparing CT performed with bowel opacification and high-resolution echo-planar MR imaging performed with bowel en-
cause points
focal and
hancement is currently in progress. In summary, our study illustrates that trast
pancreatic imaging material-enhanced
tion
echo-planar
allows
and oc
all of the to apply and
imaging
reliable
of the
surrounding
improve
con-
is feasible,
differentiation
from
may
with oral high-resolu-
bowel,
the diagnosis
of
pancreatic disease. High S/N, elimination of motion artifacts, and intrabuminal bowel signal enhancement are critical
steps
in
developing
strategy
for abdominal
imaging.
#{149}
an
overall
echo-planar
Short
TE images yield higher S/N but limited C/N, whereas long TE images have improved C/N at the cost of neduced S/N. We have demonstrated that echoplanar imaging of the pancreas with adequate bowel lumen signal en-
Acknowledgment: PhD, for his statistical
We thank analysis.
Elkan
Halpern,
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