Advanced MR I mag ing of

t h e P a n c re a s
Danielle V. Hill, MD, Temel Tirkes, MD*

KEYWORDS

MRI
MRCP
T1 mapping
Extracellular volume
Diffusion-weighted imaging

Quantitative imaging

KEY POINTS

T2-weighted imaging is useful for assessing fluid components of lesions or collections and provides
guidance for MR cholangiopancreatography (MRCP) acquisition.

MRCP sequences provide detailed images of the pancreatic duct and can be further augmented
with secretin to improve visualization and grade the exocrine function of the pancreas.

T1-weighted images are useful in assessing the pancreatic parenchyma, detecting areas of hem-
orrhage, and characterizing the enhancement pattern of neoplasms after gadolinium
administration.

Advanced imaging techniques, such as T1 mapping, diffusion-weighted imaging, elastography,
and extracellular volume quantification, show promise for adding diagnostic value and further
data quantification.

INTRODUCTION few breath-holds, improving patient experience

and decreasing motion artifact. As a result, MR
MR imaging of the pancreas is a powerful tool to has increasingly been used to evaluate the
diagnose and characterize a range of anomalous pancreas.5 By using the current advanced capa-
and pathologic conditions such as variant ductal bilities of MR in conjunction with other imaging
anatomy, inflammatory conditions such as chronic modalities, the radiologist is best equipped to di-
pancreatitis (CP), neoplasms, and ductal injuries. agnose a wide spectrum of pancreatic pathologic
Because of the high functional reserve of the conditions. In this review article, the authors
pancreas, early pathologic changes can be subtle, explore current MR imaging techniques.
making diagnosis challenging.1,2 In addition, inter-
rogating the pancreas with endoscopic retrograde
pancreatography (ERCP) or via tissue sampling MR SEQUENCES FOR PANCREAS IMAGING
carries complication risks, such as ERCP-
A comprehensive MR examination should demon-
induced pancreatitis. As a result, MR and MR chol-
strate detailed anatomy of the pancreatic duct and
angiopancreatography (MRCP) play major
the biliary tree, detect and characterize paren-
noninvasive roles in identifying pancreatic patho-
chymal disease, delineate extension of neoplastic
logic condition with diagnostic power equivalent
or inflammatory processes, and provide evaluation
to ERCP.1 Ductal detail can be enhanced by
of the vascular anatomy. To do so, the following
administration of secretin, thus improving the
sequences may be used:
diagnostic capabilities of MRCP.3,4 Technical in-
novations have continued to improve, now with
T1-weighted gradient-echo
most sequences being performed in a single or a
T2-weighted axial and coronal sequences
mri.theclinics.com

Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 550 North University
Boulevard, Suite UH0663, Indianapolis, IN 46202, USA
* Corresponding author.
E-mail address: atirkes@iupui.edu

Magn Reson Imaging Clin N Am 28 (2020) 353–367

https://doi.org/10.1016/j.mric.2020.03.003
1064-9689/20/Ó 2020 Elsevier Inc. All rights reserved.
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354 Hill & Tirkes

Turbo spin-echo (TSE) or a variant of TSE compensate for the potential decreased soft tis-

Two-dimensional (2D) and 3-dimensional (3D) sue contrast.6–10 Tables 1 and 2 define the MR im-
MRCP aging parameters for these sequences on 1.5-T

T1-weighted 3D gradient-echo before and af- and 3.0-T scanners, respectively. Pancreatic path-
ter gadolinium (Gd) ologic conditions can be subtle in the early stages,

(optional) Secretin-enhanced MR cholangio- for example, the loss of ductal compliance or sub-
pancreatography (S-MRCP) tle alterations in enhancement patterns that can be
seen in early CP.1 These parenchymal alterations,
Currently, it is possible to complete these core such as atrophy, loss of proteinaceous water con-
sequences within 30 minutes. Pancreatic imaging tent, and fibrotic changes, can be detected using
can adequately be performed with 1.5-T scanners, advanced MR techniques, which include T1 signal
although 3.0 T is preferable for improved signal-to- intensity ratio (SIR), T1 mapping, diffusion-
noise ratio (SNR) if techniques such as parallel im- weighted imaging (DWI), elastography, and extra-
aging and reconstruction algorithms are used to cellular volume (ECV) quantification.

Table 1
Parameters for pancreatic imaging on 1.5-T MR imaging scanners

3D SPGR T2 2D T2 2D T2 2D MRCP MRCP 3D SPGR

DIXON SSFSE STIR SSFSE 2D Slab MRCP 3D Secretin FS
Plane of Axial Axial Axial Coronal Coronal Coronal Coronal Axial
acquisition
TR/TE (ms) 7.47/4.76 1100/90 2900/132 1100/90 2000/755 2500/691 2000/756 5.17/2.52
(in), 2.38 (TI 150)
(out)
Flip angle 10 130–50 180 130 180 Variable 1 12
(degree)
ST/SG 3.4/- 4.0/4.0 7 4.0/4.0 40 1/- 40 3.0/-
NEX 1 1 1 1 1 2 1 1
RBW 290 475 250 476 300 372 300 300
Phase A to P A to P A to P R to L R to L R to L R to L A to P
direction
Echo train 1 160 33 192 320 189 256 1
length
Matrix 256 256 256 256 256 384 256 256
 120  192  180  192  256  346  256  144
FOV 400 360 360 360 290 350 290 360
Respiration BH BH BH BH BH Navigator BH BH
Fat saturation No No IR No Fat sat Fat sat Fat sat Fat sat
Concatenation 1 3 4 3 8 1 1 1
Parallel 2 No No No No 3 No 2
imaging
Scan time 0:12 0:44 0:58 0:31 0:18 3:55 0.03 0:18
(min:s) (9:58) (3:28)
These are guidelines for use on a 1.5-T MR imager. The names of sequences and parameter values may vary with different
MR vendors.
Abbreviations: 3D SPGR DIXON, 3D nonfat-saturated spoiled gradient-echo sequence for chemical shift imaging; 3D
SPGR FS, fat-saturated 3D spoiled gradient-echo T1-weighted sequence for postcontrast; BH, breath-hold; Concatenation,
number of interleaved acquisitions or number of breath-holds; Fat sat, spectral selective fat saturation; FOV, field of view
in millimeters; Navigator, navigator monitored respiratory triggering (see text); NEX, number of excitations; PI, parallel
imaging, where PI is used; the number given is the acceleration factor. PI is typically performed with GRAPPA (GeneRal-
ized Auto-calibrating Partially Parallel Acquisition); Phase direction, A to P is anterior to posterior, R to L is right to left;
RBW, receiver bandwidth in Hertz/pixel; Scan time, scan time in minutes. The time given in parentheses is the total scan
times for performing the secretin-enhanced MRCP series and the 3 postGd series; Secretin, presecretion and postsecretion
MRCP as described in the text; SSFSE, half single-shot fast spin-echo sequence; ST/SG, slice thickness and slice gap in mil-
limeters. 2D MRCP and secretin MRCP slabs are single slabs of 40 mm thickness. 3D sequences do not have slice gap.

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 Advanced MR Imaging of the Pancreas 355

Table 2
Parameters for pancreatic imaging on 3.0 T MR imaging scanners

3D SPGR T2 2D T2 2D MRCP MRCP 3D SPGR

Parameter DIXON SSFSE SSFSE 2D Slab MRCP 3D Secretin FS
Plane of Axial Axial Coronal Coronal Coronal Coronal Axial
acquisition
TR/TE (ms) 5.45/2.45 2000/96 2000/97 4500/622 2400/719 4500/746 4.19/1.47
(in),
3.68
(out)
Flip angle 9 150 150 160 Variable 180 9
(degree)
ST/SG 4.0/— 5/5.2 4/4.4 40/— 1.2/— 40/— 2.6/—
NEX 1 1 1 1 2 1 1
RBW 500 780 780 383 318 161 350
or 780
Phase AP AP R to L R to L R to L R to L AP
direction
Echo train 1 168 256 307 101 288 1
length
Matrix 320 320 320 384 380 384 308
 224  224  256  306  380  306  210
Field of view 400 380 350 300 380 300 400
Respiration BH BH Navigator BH Navigator BH BH
Fat saturation No SPAIR No Fat Sat SPAIR Fat Sat SPAIR
Concatenation 1 4 1 8 1 1 1
Parallel 2 2 3 2 2 2 2
imaging
Scan time 0:16 1.08 1:50 0:36 3:54 0.04 (9.56) 0:19 (3:19)
(min:s)
These are guidelines for use on a 3.0 T MR imager. The names of sequences and parameter values may vary with different
MR vendors.
The time given in parentheses is the total scan times for performing the secretin-enhanced MRCP series and the 3 post-
Gd series; 2D MRCP and Secretin MRCP slabs are single slabs of 40 mm thickness. 3D sequences do not have slice gap.

PREPARATION be performed with a single breath-hold. Therefore,

efforts to minimize respiratory motion are neces-
Patient preparation is important, and fasting for at sary for optimal results. Techniques used during
least 4 hours before the examination is recommen- free breathing include the use of respiratory trig-
ded to ensure distention of the gallbladder. Admin- gering, respiratory monitoring with navigator pulse
istering a negative oral contrast agent is helpful to (Fig. 2), and rotatory k-space sampling.
reduce fluid signal from the adjacent stomach and
duodenum, which can obscure MRCP images. T2-WEIGHTED IMAGING
This is particularly necessary for adequate assess-
ment of exocrine response if secretin is used. The normal pancreatic parenchyma exhibits rela-
Pineapple or blueberry juice can be used as an tively low to intermediate signal on T2-weighted
oral contrast agent because the manganese con- images. These sequences are helpful in distin-
tent of these juices results in signal reduction on guishing fluid from solid tissue and to characterize
T2-weighted images.11–13 Comparison of MRCP cystic pancreatic lesions and evaluate pancreatic
sequences without and then with negative oral duct and peripancreatic inflammatory collections
contrast can be seen in Fig. 1. Motion artifact (Fig. 3). Because of the high signal from pancreatic
can markedly limit the yield of pancreatic MR im- fluid, the pancreatic duct is usually well delineated
aging, especially detailed ductal views obtained on T2 images, which can then be used to guide the
on MRCP sequences, which are often too long to acquisition of the MRCP series.14

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356 Hill & Tirkes

Fig. 1. A 65-year-old patient with a history of intraductal papillary mucinous neoplasm, status post Whipple oper-
ation. (A) Coronal MRCP image with hyperintense signal from fluid within the stomach (asterisk), which obscures
the body and tail of the pancreas as well as the cystic lesion (black arrow). (B) Same patient reexamined after
ingesting a negative contrast agent, thus nullifying the signal from the stomach. Repeat study shows good visu-
alization of the cystic mass and the main pancreatic duct (arrow). (From Tirkes T, Menias CO, Sandrasegaran K. MR
imaging techniques for pancreas. Radiol Clin North Am 2012;50(3):382; with permission.)

FAT SUPPRESSION time, generally 150 to 170 milliseconds for 1.5 T.

IR techniques usually have more homogenous fat
Chemical shift fat suppression and inversion- suppression and better contrast-to-noise ratio
recovery (IR) fat suppression are 2 approaches (CNR), but tend to have lower-spatial resolution
traditionally used to suppress fat. Chemical shift or longer acquisition times. Spectral Adiabatic
fat suppression exploits the difference of reso- Inversion Recovery (SPAIR) is an IR fat-
nance frequency between fat and water. IR fat suppression technique whereby the inversion
suppression, such as short tau inversion recovery pulse is spectrally selective and only affects the
(STIR), relies on the difference in T1 relaxation fat protons. Compared with conventional IR,
times between fat and water. The fat signal is SPAIR generally has better SNR and reduced sus-
selectively suppressed by using an inversion ceptibility artifact, notably at 3.0 T.15

Fig. 2. Navigator monitoring of respiratory motion. (A) First, a coronal 2D, low-resolution gradient-echo image
with small flip angle is acquired. (B) The respiratory motion of the right hemidiaphragm is traced in real time with
subsequent synchronization of the data with the patient’s respiratory cycle. Initially, the range of motion is deter-
mined, and then on subsequent respirations, data acquisition is triggered when the diaphragm is stationary (ar-
rows). (From Tirkes T, Menias CO, Sandrasegaran K. MR imaging techniques for pancreas. Radiol Clin North Am
2012;50(3):385; with permission.)

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 Advanced MR Imaging of the Pancreas 357

Fig. 3. (A) T2-weighted axial image of a patient after a motor vehicle collision showing a fluid collection trans-
ecting the tail of the pancreas (arrow). (B) Maximum intensity projection MRCP image depicting the pancreatic
duct (arrow) communicating with the fluid collection in this patient with a transected pancreas.

Two-point Dixon method is an alternative tech- MR CHOLANGIOPANCREATOGRAPHY

nique that relies on the phase shifts created by IMAGING
the differences in fat-water resonance frequency
to separate water from fat. A fast spin echo (FSE) MRCP is a noninvasive technique for evaluating
T2-weighted 2-point Dixon sequence can reduce the pancreatic ducts with similar diagnostic accu-
overall scan time by generating both T2 and fat- racy to ERCP.18 It relies on acquisition of heavily
suppressed T2-weighted images during a single T2-weighted images to provide noninvasive
acquisition. A study aimed at quantifying pancre- detailed evaluation of the pancreaticobiliary ductal
atic steatosis and fibrosis with histologic analysis system.1 For example, MRCP has traditionally
found a moderate correlation of MR fat fractions been used to diagnose and grade severity of CP
using the T2*-corrected Dixon technique.16 Pre- by comparing ductal imaging with the Cambridge
liminary testing of flexible FSE triple-echo Dixon classification developed for ERCP grading
technique shows promise in combining the effi- (Fig. 4). Although this has proved to have similar
ciency of FSE and reliable separation of fat and efficacy to ERCP, further diagnostic criteria are
water in Dixon imaging.17 necessary to include the parenchymal changes

Fig. 4. A 47-year-old patient with chronic abdominal pain. (A) Coronal thick-slab MRCP image shows effacement
of the main pancreatic duct in the region of the body (short arrow). There is evidence of pancreas divisum as the
main pancreatic (dorsal) duct (long arrow) drains into the duodenum at the minor papilla. (B) This image was
obtained in the same patient following injection of secretin. There is complete visualization of the main pancre-
atic duct (short arrow), which appears unremarkable. The ventral duct, which was not visible before secretin
(long arrow), is also visible.

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358 Hill & Tirkes

that occur early in the course of CP, thus providing to the segment of duodenum the secreted fluid ex-
opportunity for earlier intervention. A large multi- tends to (ie, grade 1 equates to fluid in the
institutional study is underway aimed at producing duodenal bulb and grade 4 when fluid is seen
a radiologic-based scoring system to serve as a reaching the fourth segment of the duodenum).4,24
biomarker for pancreatic fibrosis and possibly to
grade efficacy of therapeutic agents on the pro- Three-Dimensional MR
gression or reversal of disease.19 Cholangiopancreatography
3D TSE sequence can produce high-spatial reso-
Secretin-Enhanced–MR lution MRCP images with thin sections, which
Cholangiopancreatography can be useful for detecting small stones, evalu-
ating the intrahepatic ducts, and imaging ductal
The addition of secretin during MRCP can improve side branches.25,26 A 3D TSE sequence can be
visualization of the pancreatic duct and is particu- performed either during free breathing and using
larly helpful in evaluating congenital anomalies motion reduction techniques or as a series of
(Fig. 5), in evaluating cystic pancreatic tumors, breath-holds. The disadvantage of free breathing
and in assessing acute pancreatitis (AP) and is the relatively long acquisition time and need
CP.4,18,20–22 Administration of secretin for for uniform, regular breathing cycles. Another op-
example, ChiRhoStim; ChiRhoClin Inc, Burtons- tion for producing 3D MRCP images is the use of
ville, MD, USA; Secrelux, Sanochemia results in a TSE sequence with the addition of a 90 flip-
secretion of pancreatic fluid from acinar cells and back pulse known as a fast recovery fast spin-
simultaneous increased tone of the sphincter of echo, DRIVE, or RESTORE. The advantage of
Oddi. As a result, there is increased dilatation these sequences is their ability to reduce repetition
and visualization of the pancreatic duct that im- time (TR) while maintaining SNR and is done by
proves the diagnostic yield of MRCP.3,4 This effect refocusing of the residual transverse magnetiza-
can result in distention of the duct by 1 mm or tion after a long echo train, which is then flipped
more and usually peaks after 3 to 5 minutes along the z-axis by a 90 fast-recovery pulse,
following injection.23 Lack of main duct distensi- thereby accelerating the relaxation of the longitu-
bility can be thought of as a surrogate for noncom- dinal magnetization.25,27
pliance secondary to periductal fibrosis seen with
CP.24 The degree to which the pancreas is able to FLIP ANGLE MODULATION
respond to secretin can also be used to estimate
loss of pancreatic function, be it from an inflamma- Traditional 3D MRCP used a constant flip angle to
tory process or after pancreatoduodenectomy.4 generate images, which at 1.5 T does not generate
Exocrine response of the pancreas is routinely significant energy deposition. With the increasing
evaluated semiquantitatively by assessing use of 3-T scanners, however, this technique gen-
duodenal filling with grade 1 to 4 corresponding erates a high amount of radiofrequency (RF)

Fig. 5. (A) Secretin-enhanced MRCP with abnormal looping configuration of the pancreatic duct with concurrent
narrowing of the lumen of the descending duodenum (arrow). (B) T1-weighted contrast-enhanced, fat-
suppressed, image demonstrates enhancing pancreatic parenchyma surrounding the descending duodenum
compatible with annular pancreas (arrow).

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 Advanced MR Imaging of the Pancreas 359

energy. Flip-angle modulation techniques Furthermore, the normal hyperintense signal of

generate 3D TSE sequences using variable flip an- the pancreas on unenhanced T1 images can be
gles (VFA), thus significantly reducing the specific used to delineate nonpancreatic tissue, such as
absorption rate, perhaps as much as 70%.28 In some pancreatic neoplasms, and can be espe-
addition, variable flip-angle techniques can main- cially helpful for pancreatic adenocarcinoma
tain higher signal intensity (SI) in a long echo train, (PDAC), whereby the tumor is typically hypoin-
thus producing higher SNR.29 Example techniques tense to normal pancreas on T1-weighted fat-
include SPACE (Sampling Perfection with Applica- suppressed sequences33 (Fig. 6). However, a
tion optimized Contrasts using different flip angle known mimic of pancreatic tumors includes
Evolutions), XETA (Extended Echo Train Acquisi- confined areas of inflammation, such as in
tion), and CUBE (not an acronym). mass-forming CP, which can also result in hypo-
intense SI on T1-weighted images.34,35 Although
the clinical background for both entities can be
T1-WEIGHTED IMAGING similar, features including the duct-penetrating
sign and concurrent collateral duct dilatation are
The pancreatic parenchyma has a shorter T1
usually indicators of mass-forming pancreatitis,
relaxation time compared with other intraabdomi-
best assessed on S-MRCP.35–37
nal organs because of protein-rich acinar cells.30
As a result, the normal pancreas is relatively
hyperintense on unenhanced T1-weighted im- CONTRAST-ENHANCED T1-WEIGHTED
ages. Decreased T1 signal is indicative of loss IMAGING
of acinar cells, which are replaced with fibrosis,
especially in CP.31 The degree of signal loss can Gd increases the T1 SI of normal pancreatic
be assessed by comparing the brightness of the parenchyma, aiding in the detection of pancre-
pancreas on unenhanced T1-weighted images atic lesions. For example, pancreatic neuroendo-
with a reference organ, such as the spleen or par- crine tumors are typically hypointense compared
aspinal muscles. The SI can be further quantified with normal pancreas on unenhanced fat-
by calculating the SIR, which is found by dividing suppressed T1-weighted images but show
the average SI of the pancreas with the reference hypervascular enhancement during the arterial
organ of choice (spleen or paraspinal muscle); phase38 (Fig. 7A, B). Enhancement of the normal
SIR 5 SIPancreas/SIReference.1 A decreased SIR be- pancreatic parenchyma can increase visualiza-
tween the pancreas and muscle was found to tion of PDAC, which usually demonstrates
correlate with increased parenchymal fibrosis in decreased enhancement on arterial phase with
patients who underwent pancreatectomy.30 progressive enhancement on delayed phases.38
Another study found a significant difference in Therefore, acquisition of Gd-enhanced se-
SNR between pancreas and spleen comparing quences is advisable unless contraindicated (ie,
normal and low pancreatic fluid bicarbonate severe allergy, pregnancy, and end-stage renal
groups. There was also a significant correlation dysfunction). A 3D fat-suppressed spoiled
between pancreatic fluid bicarbonate fluid level gradient echo is the sequence of choice for
and SIR of pancreas compared with spleen.32 pre-Gd and post-Gd series. A few common

Fig. 6. (A) Unenhanced T1-weighted image of the pancreas demonstrating the difference between the normal
hyperintense signal of the pancreatic head and the ovoid hypointense signal of a PDAC (arrow). (B) Axial T2-
weighted image demonstrates the mass with abrupt cutoff and upstream dilatation of the main pancreatic
duct (arrow).

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360 Hill & Tirkes

Fig. 7. (A) Axial unenhanced, T1-weighted, fat-suppressed, image demonstrating a mass in the tail of the
pancreas (arrow in A–D). (B) Axial contrast-enhanced T1-weighted, fat-suppressed, image showing arterial-
phase enhancement consistent with a pancreatic neuroendocrine tumor. (C) DWI and (D) ADC map through
the tail of the pancreas showing restricted diffusion.

examples include volume interpolated breath- instructions, and the arterial phase is initiated
hold fast gradient echo, live acquisition with vol- 8 seconds later. A quality arterial phase should
ume acceleration, and T1-weighted high-resolu- demonstrate contrast predominantly in the aorta
tion isotropic volume examination. The entire and superior mesenteric artery with some
pancreas and liver are typically included and contrast seen in the portal vein. No contrast
imaged in multiple phases (arterial, venous, and should be seen in the hepatic veins. Clear in-
delayed) after injecting Gd through a power structions and coaching on breath-holds from
injector at 2 mL/s followed by a 20-mL saline the technologist are necessary to reduce motion
flush. Acquisition can usually be performed in a artifact.
20-s breath-hold providing 2 to 5 mm contiguous
slices through the upper abdomen. Timing of the DYNAMIC CONTRAST-ENHANCED MR
bolus can be performed using fixed time delays IMAGING
such as 25, 60, and 180 seconds, respectively,
or with bolus tracking. Fixed time delays may Dynamic contrast-enhanced MR imaging re-
be adequate in patients without cardiovascular quires a rapid sequence of images with high
comorbidities.39 However, bolus tracking gives temporal resolution to analyze the dynamic up-
a more reliable arterial phase in patients with take and subsequent washout of a contrast
comorbidities, such as hypertension or agent. It is frequently used for abdominal appli-
cirrhosis.40 At the authors’ institution, a bolus cations to demonstrate the changes in tissue SI
tracking sequence is used to monitor the distal over time after contrast administration and can
aorta at the diaphragmatic hiatus. Once contrast help differentiate lesions with differing perfusion
appears, the patient is given breathing characteristics or measure pancreatic blood

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 Advanced MR Imaging of the Pancreas 361

flow. Other MR perfusion techniques include dy-

namic susceptibility contrast and arterial spin
labeling. Both techniques are used in neuroradi-
ology, but few sources are found discussing their
use in pancreatic imaging.41–43

T1 MAPPING
Many studies have shown that pancreatic fibrosis
causes T1 relaxation time to increase, thus
decreasing the normal T1 hyperintense signal of
the pancreas. T1 mapping is a quantitative MR
imaging technique allowing measurement of
tissue-specific T1 relaxation time. Once limited in
abdominal application because of long scan times
inherent in spin-echo imaging, newer protocols
using 3D VFA gradient echo and parallel imaging
techniques can produce parametric maps of T1
relaxation time in a single breath-hold. An advan-
tage of new T1 mapping techniques is its
decreased acquisition time compared with other
techniques, such as DWI or S-MRCP.
Pancreatic parenchyma has a median T1 of
654 milliseconds at 1.5 T and a median T1 of
717 milliseconds at 3.0 T.44 Quantification of the
data allows for ready comparison across longitudi-
nal time points as well as population-derived
norms, offering the potential benefit of using quan-
titative MR imaging as a biomarker for a spectrum Fig. 8. T1 relaxometry provides quantitative evalua-
of diseases. For example, comparing T1 relaxation tion of the pancreas. (A) Axial grayscale T1 map ob-
time of pancreatic tissue in normal controls and in tained at 1.5 T has round region-of-interest
patients with mild CP, a statistically significant in- measurements of the pancreas. The mean T1 in the
crease of T1 relaxation time was found in the pancreatic head measures 278 milliseconds, and the
group with mild CP (Fig. 8). Sensitivity of 80% mean T1 in the tail measures 271 milliseconds. (B)
Axial T1 map in a color-scale format. The intensity of
and 69% specificity for mild CP was found using
the pancreatic signal can be visually assessed by color
a T1 relaxation time cutoff of 900 milliseconds at of the scale. K, kidneys; L, liver; S, stomach.
3 T.45 However, more studies are required to reach
a consensus on what the normal T1 of abdominal
organs should be and the amount of signal change
necessary to diagnose clinically significant patho- delay times and are fitted using the relaxation
logic condition.1 model.48 MOLLI is a commercially available
There are multiple T1 mapping pulse sequence sequence originally developed for myocardial im-
products or prototypes under development by aging and uses a modified variation of inversion
manufacturers, although there is no consensus recovery snapshot. The acquisitions following the
yet on which sequence is ideal for abdominal im- inversion RF are segmented and synchronized us-
aging. That said, a recent study compared 4 ing ECG signal with the data acquisition only
different pulse sequences: VFA, modified look- occurring during diastole.49 SASHA is also similar
locker inversion recovery (MOLLI), a prototype to inversion recovery snapshot; however, it uses
inversion recovery snapshot, and a prototype a saturation RF instead of an inversion RF pulse.50
saturation recovery single-shot acquisition The study found MOLLI, SASHA, and inversion
(SASHA).46 VFA pulse sequence quantifies T1 by recovery snapshot had the highest precision,
acquiring voxel signals at steady state by using whereas VFA has relatively less, although still sub-
multiple flip angles.47 Inversion recovery snapshot stantial, precision. Because MOLLI and SASHA
relies on the relaxation of longitudinal magnetiza- were designed for myocardial imaging, they pro-
tion after an inversion RF pulse is applied. With vide a single image per breath-hold, whereas
this sequence, after the inversion RF pulse, a se- inversion recovery snapshot can acquire 3 images.
ries of quick acquisitions are collected at different In either case, this is potentially problematic

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362 Hill & Tirkes

because the pancreas may shift in location with These values are then calculated by the following
each breath-hold. VFA, on the other hand, can formula:
generate fast 3D acquisition of 64 slices in a single
ð1  hematocritÞ  DR1pancreas
breath-hold. However, VFA is inherently sensitive ECVpancreas 5
to pulsatile flow within the aorta. Ultimately, the DR1 blood
study concluded more refinement of these pulse
where DR1pancreas and DR1blood are defined as
sequences is necessary to provide the high preci-
the change of 1/T1 relaxation rate in pancreas and
sion and large spatial coverage needed during 1
blood pool relaxivity before and after contrast
breath-hold optimal for abdominal imaging.44
administration; T1 is a time constant describing
the longitudinal relaxation rate; and its reciprocal
DIFFUSION-WEIGHTED IMAGING (1/T1) is referred to as R1. The change in R1
(DR1) is defined as: DR1 5 (R1postcontrast) –
DWI is used to identify areas where there is
(R1precontrast). DR1 is proportional to Gd con-
reduced mobility of water molecules. With the
centration when both tissues are in equilibrium;
development of “ultrafast” echoplanar and paral-
DR1pancreas/DR1blood 5 [Gd]pancreas/[Gd]blood.
lel imaging in combination with improvements in
Because the Gd chelates are extracellular agents,
high-density surface coils and respiratory navi-
the ratio of contrast agent concentrations between
gation, the role of DW imaging in the body has
the pancreas and blood equals the ratio of ECV
expanded.51,52 In the pancreas, this can aid in
between the tissues: [Gd]pancreas/[Gd]blood 5-
diagnosing tumors (Fig. 7C, D) and inflammation.
ECVpancreas/ECVblood. The ECV of the blood is
A study found patients with AP had significantly
defined as the fraction of the blood volume, which
lower apparent diffusion coefficient (ADC) values
is not composed of blood cells (ie, the fraction of
compared with normal pancreatic paren-
plasma). The plasma volume is simply calculated
chyma.53 DWI is a spin-echo T2-weighted
as ECVblood 5 [1 – hematocrit].59
sequence that uses a pair of gradients applied
The pancreas has a reported median ECV of
before and after a 180 refocusing RF pulse to
0.28 on 1.5 T (interquartile range [IQR]: 0.21–
measure the diffusivity of tissue. Restriction of
0.33), and median ECV of 0.25 (IQR 0.19–0.28)
water molecules produces imaging with high SI
on 3.0 T.44 A study by Tirkes and colleagues,59
on the DW images and low signal on the ADC
investigating patients with and without known
maps. The phase shift caused by the initial
pancreatic disease, reported that an ECV greater
gradient is canceled by the second gradient,
than 0.27 demonstrated 92% sensitivity and 77%
and thus, there is no significant loss of
specificity for the diagnosis of CP when using a
signal.54,55 When water molecules move freely,
3.0-T scanner (Fig. 9). By combining ECV and
the movement between the first and second
T1, this study achieved 85% sensitivity and 92%
gradient results in decreased signal on DWI.
specificity for diagnosing mild CP (area under the
Practically, this results in high SI on both the
curve: 0.94).59 Although T1 relaxation times differ
DW images and the ADC maps, although the
signal decreases at higher b values.

EXTRACELLULAR VOLUME IMAGING

ECV imaging is a quantitative MR radiomics tool
that calculates increased extracellular matrix sec-
ondary to tissue fibrosis, namely, collagen56,57 and
proteoglycan content.58 Although changes to the
extracellular matrix can be seen in a variety of
intraabdominal pathologic conditions, in the
pancreas, it can be used as a marker for CP.45,59
Using Gd as an extracellular contrast agent, the
ECV dichotomizes pancreatic tissue into intracel-
lular and extracellular/interstitial spaces. ECV frac-
tions can then be depicted as pixels on an image
called ECV map. To do so, tissue and blood Fig. 9. ECV imaging of the CP. ECV imaging technique
plasma concentrations of Gd are compared by us- uses T1 maps obtained before and after MR contrast
ing the T1 relaxation times obtained from the enhancement. This axial color map image depicts
pancreas and the aortic lumen (blood pool) in calculated ECV fraction. B, body; H, head; T, tail of
unenhanced and postcontrast equilibrium phases. the pancreas.

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 Advanced MR Imaging of the Pancreas 363

between 1.5 T and 3 T, ECV fractions are similar in quantifying fat using Web-based calculators as
different magnet strengths. well as vendor software packages. Similarly, quan-
tifying fat within the pancreas can be performed;
MR ELASTOGRAPHY however, more data are needed to establish a
consensus on the normal range of pancreatic fat
Increased stiffness of the pancreas indicates fraction. A study performed on a large healthy
fibrosis and can be found in CP (Figs. 10 and 11) volunteer population in Europe reported the
as well as in pancreatic cancer.60 MR elastography normal pancreatic fat fraction as 4.4%.64 In the
(MRE) of the liver is a very useful tool in evaluating United States, the fat fraction in the general popu-
the degree of hepatic fibrosis; however, MRE of lation is reported to be between 8.3%45 and
the pancreas is still under development.61 A pilot 15%.65 There appears to be an association with
study of 20 healthy volunteers who underwent CP and a higher pancreatic fat fraction and higher
MRE examinations demonstrated promising and visceral adipose tissue.65 This topic is underinves-
reproducible stiffness measurements throughout tigated, and further research is needed to examine
the pancreas.62 In the study, an experimental the clinical consequences of pancreatic steatosis.
MRE driver that emitted lower-frequency vibra- Chemical shift imaging techniques depend on
tions in order to reach the deeper location of the the different resonance frequencies of water and
pancreas was used. Mean shear stiffness was fat protons. Two-point Dixon method is a practical
found to be (1.15  0.17) kPa at 40 Hz and technique with excellent image resolution routinely
(2.09  0.33) kPa at 60 Hz.62 Another pilot study used to obtain T1-weighted in-phase, out-of-
of healthy volunteers also showed highly repro- phase, water-only, and fat-only images as dis-
ducible pancreatic stiffness measurements with a cussed above. From these sequences, the
linear increase in stiffness with age.63 In both pre- pancreatic fat signal fraction (FSF) can be calcu-
liminary studies, 3D spin-echo echo planar imag- lated from measuring SI in localized regions of
ing sequence was used to obtain 3D wave interest:
information along with 3D spatial data.
FSF 5 SIfat/SIfat 1 SIwater
PANCREATIC FAT FRACTION
Alternatively, newer MR software can produce a
MR is superior at detecting fat deposition in tis- quantitative proton density fat fraction (PDFF) map
sues compared with computed tomography (CT) by using more complex, multiecho acquisition se-
and ultrasound. There are multiple tools for quences. T1 bias and T2* correction should be

Fig. 10. MRE of the pancreas in a normal healthy volunteer. MRE was performed at 40 Hz using a 3D echo planar
imaging sequence with slice thickness of 3 mm. Top row demonstrates magnitude images at the level of the tail,
body, and head of the pancreas. Bottom row shows corresponding stiffness maps (scale 0–8 kPa). The red outline
represents the region of interest drawn in different parts of the pancreas. The mean stiffness is 1.15 kPa (range
1.02–1.18 kPa). (Courtesy of S. Venkatesh, MD, Rochester, MN.)

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364 Hill & Tirkes

Fig. 11. MRE in CP. (A, B) T2-weighted images and (C) magnitude image in 3 patients with CP and (D–F) their cor-
responding level MRE stiffness maps. Note the dilated pancreatic duct (A and B), and the severe atrophy of the
pancreas (C). The mean pancreas stiffness is elevated in the first example; however, in the other 2 patients, the
mean stiffness is within normal limits and actually lower in the patient with severe pancreatic atrophy (C, F). (The
yellow dotted lines outline the pancreas). (Courtesy of S. Venkatesh, MD, Rochester, MN; and Y. Shi, MD, Shengj-
ing Hospital, Shenyang, China.)

used to ensure a reliable assessment of quantita- Restricted movement of water molecules demon-
tive fat.66,67 PDFF map shows promise as a strated on DWI may aid in detecting neoplastic
biomarker for estimating the probability of pancre- and inflammatory processes. FSF imaging can
atic cancer. In a study comparing PDFF map with quantify the degree of pancreatic steatosis, which
pancreatic index using CT, comparison of pancre- increases in patients with CP.
atic and splenic tissue with histologic results in pa-
tients with pancreatic cancer demonstrated PDFF
map was significantly higher along with higher his- DISCLOSURE
tologic fat fraction for the cancer group.68
Dr T. Tirkes is supported by National Cancer Insti-
SUMMARY tute and National Institute of Diabetes and Diges-
tive and Kidney Diseases of the National
Despite the challenges inherent in pancreatic im- Institutes of Health under award numbers
aging, multiple MR imaging tools can optimize 1R01DK116963 and U01DK108323 (Consortium
detail and increase diagnostic yield for a range for the Study of Chronic Pancreatitis, Diabetes,
of pancreatic pathologic condition and variant and Pancreatic Cancer). The content is solely the
anatomy. In addition to the traditional MR se- responsibility of the authors and does not neces-
quences, several emerging sequences, such as sarily represent the official views of the National In-
T1 mapping, ECV fraction, DWI, and recently, stitutes of Health.
pancreas MRE, show promise for earlier disease
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