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Sandrasegaran et al.
Pancreatic MRI
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Gastrointestinal Imaging
Review
Kumaresan Sandrasegaran1
Chen Lin
Fatih M. Akisik
Mark Tann
Sandrasegaran K, Lin C, Akisik FM, Tann M
42
is necessary to obtain the following sequences: T1-weighted gradient-echo; T2-weighted axial and coronal sequences, usually turbo spin-echo (TSE) or a variant of TSE; 2D
and 3D MRCP; and T1-weighted 3D gradientecho before and after gadolinium. S-MRCP
is a useful optional sequence. Tables 1 and 2
give the MRI parameters for these sequences on 1.5- and 3-T scanners, respectively. For
most patients, it is possible to complete the
core sequences and S-MRCP within 20 minutes. In the following sections, we discuss different methods of performing these sequences, while being as vendor-neutral as possible.
Patient Preparation
In our practice, patients fast for 4 hours
before the MRI examination so that the
gallbladder is distended and it is possible to
adequately assess the exocrine response to
secretin. Negative oral contrast is useful to
reduce the signal from overlying stomach
and duodenum. Pineapple and blueberry
juice have been used as oral contrast agents
[13]. The manganese content of these juices results in increased signal on T1-weighted images and reduced signal on T2-weighted images. We prefer the use of 300 mL of
proprietary silicone-coated superparamagnetic iron oxide particle suspension (ferumoxsil, GastroMark, Mallinckrodt Medical) (Fig. 1) taken orally a few minutes
before the MRI examination.
Pancreatic MRI
TABLE 1: Parameters for Pancreatic Imaging on 1.5-T MRI Scanner
Parameter
3D SPGR Dixon
T2 2D SSFSE
T2 2D STIR
Axial
Axial
Axial
Coronal
Coronal
Coronal
Coronal
Axial
TR/TE (msec)
1,100/90
1,100/90
2,000/755
2,500/691
2,000/756
5.17/2.52
Flip angle ()
10
13050
180
130
180
Variable
12
ST/SG (mm)
3.4/
4.0/4.0
4.0/4.0
40
1/
40
3.0/
290
475
250
476
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Plane of
acquisition
NEX
RBW (Hz/pixel)
Phase direction
Echo-train length
Matrix
Field of view (mm)
Respiration
3D SPGR FS
300
372
300
300
Right to left
Right to left
Right to left
Anterior to posterior
160
33
192
320
189
256
256 120
256 192
256 180
256 192
256 256
384 346
256 256
256 144
400
360
360
360
290
350
290
360
Breath-hold
Breath-hold
Breath-hold
Fat saturation
No
No
Inversion recovery
Breath-hold Breath-hold
Navigator
Breath-hold
Breath-hold
Fat sat
Fat sat
Fat sat
Fat sat
Concatenation
Parallel imaging
No
No
No
No
No
0:12
0:44
0:58
0:31
0:18
3:55
0.03 (9:58)
0:18 (3:28)
No
NoteThese are guidelines for use on a Magnetom Avanto 1.5-T MRI scanner (Siemens Healthcare). The names of the sequences and parameter values may vary with other
scanners. Where parallel imaging is used, the number given is the acceleration factor. Parallel imaging is typically performed with GRAPPA (generalized autocalibrating
partially parallel acquisition). The scan time given in parentheses is the total scan time for performing the secretin-enhanced MRCP series and the three gadoliniumenhanced series. 3D SPGR Dixon = 3D nonfat-saturated spoiled gradient-echo sequence for chemical shift imaging, SSFSE = half single-shot fast spin-echo sequence, 3D
SPGR FS = fat-saturated 3D spoiled gradient-echo T1-weighted sequence for contrast-enhanced imaging, ST/SG = slice thickness and slice gap (2D MRCP and secretin
MRCP slabs are single slabs of 40-mm thickness; 3D sequences do not have slice gap), NEX = number of excitations, RBW = receiver bandwidth, FOV = field of view,
Navigator = navigator-monitored respiratory triggering, Fat sat = spectral selective fat saturation, Concatenation = number of interleaved acquisitions or number of
breath-holds.
3D SPGR Dixon
T2 2D SSFSE
MRCP 3D
MRCP Secretin
3D SPGR FS
Axial
Axial
Coronal
Coronal
Coronal
Axial
TR/TE (msec)
2,000/96
2,000/97
4,500/622
2,400/719
4,500/746
4.19/1.47
Flip angle ()
150
150
160
Variable
180
ST/SG (mm)
4.0/
5/5.2
4/4.4
40/
1.2/
40/
2.6/
NEX
RBW (Hz/pixel)
500 or 780
780
780
383
318
161
350
Phase direction
Anterior to posterior
Anterior to posterior
Right to left
Right to left
Right to left
Right to left
Anterior to posterior
Echo-train length
Matrix
Field of view (mm)
Respiration
Fat saturation
168
256
307
101
288
320 224
320 224
320 256
384 306
380 380
384 306
308 210
400
380
350
300
380
300
400
Breath-hold
Breath-hold
Navigator
Breath-hold
Navigator
Breath-hold
Breath-hold
No
SPAIR
No
Fat sat
SPAIR
Fat sat
SPAIR
Concatenation
Parallel imaging
0:16
1.08
1:50
0:36
3:54
0.04 (9.56)
0:19 (3:19)
NoteThese are guidelines for use on Magnetom Verio 3-T MRI scanner (Siemens Healthcare). The names of sequences and parameter values may vary with other
scanners. Where parallel imaging is used, the number given is the acceleration factor. Parallel imaging is typically performed with GRAPPA (generalized autocalibrating
partially parallel acquisition). The scan time given in parentheses is the total scan time for performing the secretin-enhanced MRCP series and the three gadoliniumenhanced series. 3D SPGR Dixon = 3D nonfat-saturated spoiled gradient-echo sequence for chemical shift imaging, SSFSE = half single-shot fast spin-echo sequence, 3D
SPGR FS = fat-saturated 3D spoiled gradient-echo T1-weighted sequence for contrast-enhanced imaging, ST/SG = slice thickness and slice gap (2D MRCP and secretin
MRCP slabs are single slabs of 40-mm thickness; 3D sequences do not have slice gap), NEX = number of excitations, RBW = receiver bandwidth, FOV = field of view,
Navigator = navigator-monitored respiratory triggering, SPAIR = spectral adiabatic inversion recovery, Fat sat = spectral selective fat saturation, Concatenation =
number of interleaved acquisitions or number of breath-holds.
43
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Sandrasegaran et al.
Fig. 163-year-old woman with known branch-type intraductal papillary mucinous neoplasm.
A, Coronal T2-weighted turbo spin-echo 2D slab image from examination performed at outside institution
without oral contrast shows stomach contents (arrowhead) are bright and overlie body and tail of pancreas,
obscuring main duct. There is 2.5-cm cystic mass (solid arrow) in pancreatic body. There is also N/2 ghosting
of stomach (dashed arrows) projected over right hepatic lobe. This artifact is due to filling of k-space over two
respiratory cycles. Ghost signal is shifted by one half length of field of view (FOV) in phase-encoding direction
(or FOV/4 if parallel imaging with acceleration factor of 2 is used). It is less likely to occur with variable flip-angle
techniques.
B, Single-shot fast spin-echo image from examination performed at our institution with negative oral contrast
administration shows good visualization of cystic mass (arrow) and main pancreatic duct.
T1-Weighted Sequences
T1-weighted sequences are useful for assessing hemorrhage, such as within inflammatory collections in acute pancreatitis (Fig. 2),
and pancreatic fat. Estimation of pancreatic
fat is currently not considered part of routine
MRI assessment. However, studies in animals
and humans have shown that fatty pancreas
is associated with increased severity of acute
pancreatitis or higher incidence of postoperative complications [46]. Thus, accurate assessment of pancreatic fat content may be
useful. Traditionally, 2D gradient-echo sequences with two TEs have been used. This
sequence yields images in which water and
fat protons have the same or opposing phases
(Fig. 2). Fat content may be estimated by assessing the signal drop-off on opposed-phase
T2-Weighted Sequences
Multishot fast spin-echo (TSE) and single-shot fast spin-echo (SSFSE) sequences
are the most commonly used T2-weighted
sequences for pancreatic (and liver) imaging. We use both of these sequences. An alternative technique is balanced steady-state
free precession. Respiratory-gated TSE has
been shown to be superior to breath-hold
TSE and respiratory-gated SSFSE in detecting solid liver lesions, such as metastases [11,
12]. SSFSE sequences have a long echo-train
length, which reduces the contrast-to-noise
ratio (CNR) of solid liver lesions (which have
short T2) because of magnetization transfer
effect and T2-filtering produced by multiple 180 refocusing pulses [12, 13]. On the
other hand, the image quality of SSFSE sequence is superior to TSE sequences. SSFSE
sequences are used to obtain T2-weighted
sequences, with a TE of about 100 milliseconds, and MRCP, with a TE of about 600
milliseconds (Tables 1 and 2). Fat is bright
on these sequences, and fat suppression may
be required. In addition, T2-weighted sequences are too long to be acquired within
one breath-hold. They may be concatenated
Fig. 233-year-old woman with acute pancreatitis with sudden drop in hematocrit.
A, Axial T2-weighted image shows large fluid collection (arrow) with low-signal material (arrowhead) in dependent aspect.
B and C, Axial T1-weighted in-phase (B) and opposed-phase (C) images show high signal (arrowhead) in dependent aspect of cyst (arrow) indicating blood. Patient was
diagnosed with hemorrhagic pseudocyst. Angiography (not shown) did not reveal pseudoaneurysm. In addition, there is reduced liver signal (dashed arrow) on opposedphase image compared with in-phase image, indicating hepatic steatosis.
44
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Pancreatic MRI
Fig. 359-year-old man with postprandial pain who
underwent mesenteric CT angiography.
A, Axial CT image shows mild reduced density
and irregular outline of pancreatic head (arrow),
considered worrisome for pancreatic neoplasm.
B and C, In-phase (B) and opposed-phase (C) images
from 3D T1-weighted MRI show signal loss on
opposed-phase in anterior aspect of pancreatic head
(arrows).
D, Using in- and opposed-phase images, it is possible
to derive fat-only or water-only images. On fat-only
image, pancreatic head shows focal increased signal
(arrow). Appearances are consistent with fatty
infiltration of pancreatic head, simulating tumor.
Fat Suppression
Two different approaches are traditionally used for fat suppression. Chemical shift
fat suppression is based on the difference of
resonance frequency between fat and water.
Before the main sequence, a spectrally selective radiofrequency pulse tuned to the fat frequency is applied, followed by spoiler gradient pulses. The frequency of precession of fat
protons is dependent on the magnetic field.
Therefore, this technique is adversely affected by magnetic field inhomogeneity. Another
approach is inversion recovery (IR) fat suppression, such as STIR, which is based on the
A
AJR:195, July 2010
B
45
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Sandrasegaran et al.
Fig. 541-year-old man with chronic pancreatitis
who underwent 3-T MRI.
A and B, Line diagrams show conventional inversion
recovery (A) and spectral adiabatic inversion
recovery (SPAIR) (B) sequences. Gray lines show
signal from fat and dashed lines, signal from water.
There is reduced water signal in conventional
inversion recovery sequence compared with SPAIR.
C and D, Comparison of axial images from
conventional inversion recovery (C) and SPAIR (D).
Susceptibility artifact from bowel gas, seen as dark
band in anterior abdomen on inversion recovery
image (arrowheads), is not evident on SPAIR
sequence.
46
90
90
Water
Water
Fat
Fat
180
180
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Pancreatic MRI
Fig. 971-year-old man with multiple cystic pancreatic lesions seen for follow-up.
A and B, Coronal images of free-breathing 3D MRCP performed at 3-T MRI using constant flip angle (single-shot
fast spin-echo [SSFSE]) (A) and variable refocusing flip angles (sampling perfection with application optimized
contrasts using different flip-angle evolutions [SPACE]) (B). Both sequences show side-branch intraductal
papillary mucinous neoplasm (arrowheads). SPACE sequence suggests irregularity of main pancreatic duct
(arrow) that was not evident on conventional SSFSE sequence. Specific absorption rate of SPACE sequence
was 52% lower than that of conventional SSFSE sequence.
Motion Suppression
Techniques of motion suppression during
free breathing include the use of respiratory
triggering, respiratory monitoring with navigator pulse, and rotatory k-space sampling. Most
T2-weighted SSFSE and 3D MRCP sequences
are too long to be performed within a breathhold and require respiratory triggering. Traditionally, this has been performed using pneumatic bellows placed around the lower chest to
detect respiratory motion. The use of 2D navigator pulses is a more recent development. The
most commonly used navigator technique is
2D PACE (prospective acquisition correction
encoding) (Fig. 6). This technique is further
discussed under the section on MRCP.
Rotatory filling of k-space allows inherent motion correction capabilities. With these
techniques, named PROPELLER (periodically rotated overlapping parallel lines with enhancement reconstruction) or BLADE (Siemens Healthcare), the entire k-space is covered
by multiple rectangular regions shaped like
blades rotated around the center [18, 19]. Each
blade consists of a small number of phase-encoding lines that can be filled with a multiple
echo acquisition after a single excitation. Any
in-plane motion that occurs between the acquisitions of the two blades can be determined by
comparing the k-space data in the overlapping
part of two blades and may be corrected. After repeating the process for all the blades, the
full k-space can be created from motion-corrected blades to reconstruct an image with re-
47
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Sandrasegaran et al.
Fig. 112D MRCP in 67-year-old woman with intraductal papillary mucinous neoplasm (IPMN).
A, Positioning of 40-mm MRCP slabs is performed on axial single-shot fast spin-echo sequence. In our practice, six coronal oblique slabs are used to ensure that entire
pancreaticobiliary ductal system is included. C and B indicate slabs.
B, 2D MRCP coronal image, corresponding to slab B on image A, shows that cystic lesion in downstream body (arrowhead) communicates with main duct. Duct in
pancreatic tail (solid arrow) is not well visualized on this image. Note divisum anatomy (dashed arrow).
C, 2D MRCP coronal image, corresponding to slab C on image A, does not optimally show main ductal communication of IPMN in pancreatic body (arrowhead) but shows
cystic masses in pancreatic tail (arrow). Dashed arrow indicates divisum anatomy.
Fig. 1274-year-old woman with intraductal
papillary mucinous neoplasm.
A and B, Coronal image from 2D MRCP (A) and
coronal maximum-intensity-projection image from
3D MRCP (B) show that duct in pancreatic tail
(arrowhead) and posterior branch of right hepatic
duct (arrow) are better visualized on 3D sequence.
We perform both 2D and 3D MRCP because 2D may
have better image quality in patients with irregular or
rapid respiratory cycles.
(GE Healthcare). Variable refocusing flip-angle techniques can maintain higher signal intensity in a long echo-train to produce higher
SNR [22]. The SAR may be reduced by about
70% at 3 T by using a varying flip angle [23].
A study comparing traditional constant flipangle 3D MRCP with variable refocused flipangle MRCP in healthy volunteers imaged on a
3-T MR scanner found significantly better image quality of intrahepatic bile ducts with the
latter sequence [22] (Fig. 9). The superiority of
image quality with the variable refocused flipangle technique has also been found in healthy
subjects scanned at 1.5 T [24], where energy
deposition is not a major consideration. This
finding may be due to the shorter echo spacing, and thus less image blurring, that is possible with variable refocusing flip angles. The
advantages and disadvantages of flip-angle
modulation techniques over constant flip-angle
techniques are shown in Table 3 [25].
imaging, balanced steady-state free precession sequences (SSFP), such as FIESTA (fast
imaging employing steady-state acquisition),
trueFISP (fast imaging with steady-state precession) or balanced FFE (fast-field echo) may
be used. Balanced SSFP sequences have high
SNR. Contrast in these sequences is determined by a ratio of T2/T1. By keeping the TR
and TE very short, T1 remains constant, and
the principal component of image contrast is
48
Disadvantages
NoteFlip-angle modulation techniques include sampling perfection with application optimized contrasts
using different flip-angle evolutions. Variable flip-angle techniques may fill the entire k-space partition in a
respiratory cycle. Constant flip-angle 3D techniques may fill the k-space partition in two breathing cycles. If
the diaphragmatic positions in the two cycles are different, N/2 ghosting artifacts may occur [25] (Fig. 1).
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Pancreatic MRI
Fig. 1348-year-old woman with abdominal pain.
AD, MRCP images at 0 (A), 3 (B), 7 (C), and 10 (D)
minutes after IV secretin injection. Patient has
reverse divisum with ventral duct (arrowhead, B)
entering minor papilla. Diagnosis is easier to make on
postsecretin images. Reverse divisum may result in
isolated ventral chronic pancreatitis. Note progress
filling of duodenum (solid arrows, BD) and proximal
small bowel loops (dashed arrow, D) with high-signal
fluid.
MRCP
MRCP refers to the acquisition of heavily T2-weighted images, with variants of TSE
sequences. These sequences consist of a single 90 pulse followed by multiple constant
refocusing pulses. The refocusing pulses typically have been 180 pulses, although pulses
of 130 to 160 are often used to reduce energy deposition, especially at 3-T MRI. Very
long echo-trains may be required to acquire
all data in a slice within a single TR. However, long echo pulses cause some blurring of
the images. The commonly used sequences
use partial Fourier technique, in which between 50% and 60% of the k-space is filled
by data. The remainder of the k-space is filled
by extrapolation using the symmetry of the kspace. Sequences that acquire the entire data
set within one TR and use partial Fourier
technique are called SSFSE or HASTE; 2D
MRCP has long been performed using coronal SSFSE slabs. We prefer to acquire 40mm slabs in multiple coronal oblique planes
3D MRCP
The 3D TSE sequence can produce highspatial-resolution MRCP images (Fig. 12).
Thin sections without a slice gap allow better assessment of small stones, side branches of the main pancreatic duct, and intrahepatic bile ducts [28, 29]. Three-dimensional
TSE MRCP may be performed as a series of
breath-holds or during free breathing. We
acquire 12 mm, contiguous slices during
free breathing and use the navigator-echo
technique to reduce motion effects. The
main disadvantage of this technique is the
relatively long acquisition time. In addition,
navigator-based triggering requires uniform
and regular breathing cycles for optimal image quality. If the patient has rapid or irregular breathing, the image quality may be impaired. An alternative method of producing
3D MRCP images is to use a TSE sequence
with a 90 flip-back pulse. This sequence is
called FRFSE (fast recovery fast spin-echo),
DRIVE, or RESTORE. The unique feature
of this sequence is that after a long echotrain, the residual transverse magnetization
49
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Sandrasegaran et al.
our practice, we use secretin even in patients
with mild acute pancreatitis but avoid its use
in severe pancreatitis. The major drawbacks
of S-MRCP are the 10 minutes of acquisition
time and the cost of secretin (estimated to be
$300 per adult dose).
Contrast-Enhanced Sequences
If the only indication for the MRI examination is evaluation of choledocholithiasis,
contrast enhancement may not be necessary.
For most other indications, the acquisition of
gadolinium-enhanced sequences is advisable.
The sequence of choice for unenhanced and
gadolinium-enhanced series is 3D fat-suppressed spoiled gradient-echo. This sequence
has many names, such as VIBE (volume interpolated breath-hold F-GRE), LAVA (liver acquisition with volume acceleration) and
THRIVE (T1-weighted high-resolution isotropic volume examination), and allows the
acquisition of 2- to 5-mm contiguous slices
within a 20-second breath-hold.
Typically, gadolinium is injected at 2 mL/s
using a power injector and followed with a 20mL saline flush administered at the same rate.
It is usual to acquire the entire liver (and pancreas) in multiple phases. Timing of the scan
may be performed using fixed time delays, realtime bolus tracking, or a test bolus. Traditionally, empirical timing has been used with the arterial, venous, and delayed phases acquired 25,
60, and 180 seconds, respectively, after commencement of contrast infusion (Fig. 17).
Bolus tracking has been primarily used in
MR angiography but is used increasingly in
abdominal imaging. The delay from onset
of infusion to arrival of contrast material in
the distal aorta varies from 12 to 30 seconds,
with a mean of 1718 seconds [44, 45]. Thus,
50
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Pancreatic MRI
Fig. 1624-year-old woman with suspicion of pancreatic ductal disruption after motor vehicle accident.
A, Presecretin MRCP image shows probable ductal injury with focal segment of stenosis (solid arrow) and upstream duct dilation (dashed arrow).
B, After secretin, there is leakage of exocrine output into large collection (arrowhead).
C, ERCP image obtained on same day confirms ductal disruption (arrowhead). In our experience, secretin may be useful to show large ductal leakage postsurgically or
after blunt abdominal trauma. However, pressure within pancreatic duct after secretin may not be sufficient to show small leak, and potential leaks may be obscured by
surrounding collections. ERCP is superior to secretin MRCP for showing ductal leaks.
A
AJR:195, July 2010
nal dysfunction. When the estimated glomerular filtration rate (eGFR) is more than 60
mL/min/1.73 m2, we use the standard dose
of gadolinium (0.1 mmol/kg). With an eGFR
of 3060 mL/min/1.73 m2, we use a reduced
dose, typically one half of the standard dose.
We tend not to use gadolinium when the
eGFR is less than 30 mL/min/1.73 m2.
1.5- Versus 3-T MRI
In the previous sections, we have alluded
to sequences that tend to be more useful in
3-T MRI, such as variable flip-angle techniques for reducing SAR. The main advantage of scanning at 3 T is the higher SNR.
Parallel imaging is a technique used more
often in 3-T MRI than at 1.5 T. It allows the
production of images with adequate field of
view and spatial resolution using fewer kspace lines. This is possible because the spatial sensitivity information from independent
receiver coils may be used to overcome the
aliasing effect of acquiring a reduced number of phase encoding lines [47, 48]. As a
result, a shorter scanning time, often by a
factor of two, may be achieved. Other advan-
51
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Sandrasegaran et al.
1.5- and 3-T abdominal MRI suggest that 3
T does not offer substantial improvement in
image quality for unenhanced images [52
59]. However, the SNR of contrast-enhanced
images is thought to be superior at 3 T, compared with 1.5 T [60, 61]. It is probable that
future improvements in hardware and imaging sequences will make 3-T MRI the system
of choice for imaging the pancreas.
Conclusions
As a result of rapid technologic improvements, the current pancreatic MRI protocol
is very different from the one used a decade
ago. Most sequences can be performed in one
or a few breath-holds, and 3D sequences with
thin, contiguous slices offer good spatial resolution. Better fat and motion suppression allows improved contrast resolution and image
quality. The diagnostic potential of MRCP is
now almost as good as ERCP, eliminating the
need for most diagnostic ERCP studies.
Looking to the future, it is probable that increased functional assessment of the pancreas
will be performed. S-MRCP gives information on the exocrine function of the pancreas. Diffusion-weighted MRI, MRI perfusion,
and MR elastography are currently research
tools. In the future, they may become part of
the MR protocol for specific indications, such
as assessing the malignant potential of cystic
pancreatic tumor or evaluating the severity of
chronic pancreatitis. The future of pancreas
MRI appears to be exciting.
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