DOI:10.2214/AJR.05.0875
AJR 2006; 187:W365-W374
© American Roentgen Ray Society
MRI of Adenocarcinoma of the Pancreas
Frank H. Miller1,
Nancy J. Rini1 and
Ana L. Keppke1
1 All authors: Department of Radiology, Northwestern Memorial Hospital,
Northwestern University, The Feinberg School of Medicine, 676 N. St. Clair,
Ste. 800, Chicago, IL 60611.
Received May 23, 2005;
accepted after revision July 12, 2005.
Address correspondence to F. H. Miller
(fmiller{at}northwestern.edu).
WEB
This is a Web exclusive article.
Abstract
OBJECTIVE. CT is the established imaging technique for evaluation of
pancreatic adenocarcinoma. MRI, however, can play a major role in this
disease. The objective of this study is to illustrate the strengths of MRI for
evaluating pancreatic adenocarcinoma.
CONCLUSION. The superior soft-tissue contrast of MRI compared with
CT is useful in the detection and characterization of non-contour-deforming
pancreatic masses. MRI compared with CT may be more sensitive in the detection
of distant disease, better for defining appropriate surgical candidates, and
better for characterizing small liver metastases and peritoneal and omental
metastases.
Keywords: adenocarcinoma • cancer • MRI • pancreas • pancreatic neoplasms
Introduction
Pancreatic ductal adenocarcinoma is the fourth leading cause of cancer
death. Most cases are advanced and unresectable at the time of diagnosis.
Pancreatic carcinoma commonly metastasizes to the lymph nodes, liver, and
peritoneum. The indications for surgical resection vary throughout medical
centers. Contraindications to surgical resection include liver and peritoneal
metastases, distant lymph node metastases, arterial encasement, and greater
than 50% encasement of major venous structures
[1].
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Fig. 1A —49-year-old man with small non-contour-deforming pancreatic
mass caused by adenocarcinoma. Axial contrast-enhanced MDCT image shows
atrophy of pancreatic tail and pancreatic duct dilation (arrow).
Discrete mass is difficult to identify.
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CT is the established imaging technique for the evaluation of pancreatic
adenocarcinoma. MRI, however, can play a major role in this disease. The
superior soft-tissue contrast of MRI compared with CT is useful in the
evaluation of subtle non-contour-deforming pancreatic masses. MRI compared
with CT may be more sensitive in the detection of distant disease, better for
defining appropriate surgical candidates, and better for characterizing small
liver metastases and peritoneal and omental metastases. Recent advances in
abdominal MRI allow fast acquisition of multiple sequences free of artifacts.
Our routine MRI protocol is detailed in
Appendix 1. This pictorial
essay illustrates the strengths of MRI for evaluating pancreatic
adenocarcinoma.
APPENDIX I: Pancreatic MRI Protocol
Sequence |
Acquisition Time (seconds) |
| 1. Axial HASTE T2-weighted sequence |
30 |
| 2. Coronal HASTE T2-weighted sequence |
30 |
| 3. Axial in- and opposed-phase T1-weighted GRE sequence |
18 |
| 4. Axial unenhanced fat-saturated T1-weighted GRE sequence |
18 |
| 5. Coronal unenhanced fat-saturated T1-weighted GRE sequence |
18 |
| 6. Axial T1-weighted fat-saturated Gd-enhanced GRE at 15—20 seconds
(fluoro-preparation timed sequence) and at 45 seconds |
18 x 2 = 36 |
| 7. Coronal T1-weighted fat-saturated Gd-enhanced GRE at 90 seconds |
18 |
| 8. Axial T1-weighted fat-saturated Gd-enhanced GRE at 120 seconds |
18 |
| 9. Optional RARE MRCP |
3 x 6 = 18 |
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Note—GRE = gradient-recalled echo, Gd = gadolinium, MRCP = MR
cholangiopancreatography
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Fig. 1B —49-year-old man with small non-contour-deforming pancreatic
mass caused by adenocarcinoma. Axial T2-weighted HASTE MR image (5-mm slice
thickness) shows pancreatic ductal dilation (arrow) with associated
atrophy of pancreatic tail. Duct dilation is easily seen on T2-weighted images
and may be better seen than on MDCT.
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Fig. 1C —49-year-old man with small non-contour-deforming pancreatic
mass caused by adenocarcinoma. Axial venous-phase gadolinium-enhanced
T1-weighted fat-suppressed gradient-recalled echo MR image shows 1.8-cm
hypointense mass (arrowhead) in pancreatic body, consistent with
pancreatic carcinoma. Pancreatic duct dilation (long arrow) and
pancreatic atrophy upstream from mass are seen. Ill-defined soft tissue
(short arrows) surrounding celiac artery was proven to be
malignant.
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Fig. 2B —31-year-old man with suspected pancreatic mass on MDCT. Axial
T1-weighted in-phase gradient-recalled echo MR image shows prominent
pancreatic head (arrow) with normal signal intensity.
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Non-Contour-Deforming Pancreatic Mass
The normal pancreas shows high signal intensity on unenhanced T1-weighted
fat-suppressed sequences because of the presence of acinar proteins. It also
shows homogeneous intense enhancement on the early arterial phase and becomes
isointense to the liver on more delayed enhanced sequences
[2]. Conversely, pancreatic
adenocarcinoma is hypointense to the normal pancreas on T1-weighted
fat-suppressed sequences, shows decreased enhancement on the arterial phase,
and shows progressive enhancement on delayed sequences. These MRI features are
related to the fibrotic nature of the tumor. The arterial phase of imaging
yields the greatest conspicuity of pancreatic carcinoma, which appears
hypointense compared with the adjacent normal pancreas
[3].
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Fig. 2C —31-year-old man with suspected pancreatic mass on MDCT. Axial
T1-weighted opposed-phase gradient-recalled echo MR image shows signal dropout
in pancreatic head (arrow) because of fatty infiltration without
evidence of underlying mass.
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Fig. 2D —31-year-old man with suspected pancreatic mass on MDCT. Axial
arterial-phase gadolinium-enhanced T1-weighted fat-suppressed
gradient-recalled echo MR image shows normal homogeneous enhancement of head
of pancreas (arrow) without mass.
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Fig. 3A —60-year-old man with mass in uncinate process of pancreas
that proved to be pancreatic adenocarcinoma. Patient had elevated creatinine
and could not receive iodinated contrast material on CT. Coronal T2-weighted
RARE MR cholangiopancreatography image shows dilation of common bile duct
(short arrow) and pancreatic duct (long arrow) with abrupt
termination at confluence of ducts (arrowhead). This double duct sign
is highly suspicious for malignancy.
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Fig. 3B —60-year-old man with mass in uncinate process of pancreas
that proved to be pancreatic adenocarcinoma. Patient had elevated creatinine
and could not receive iodinated contrast material on CT. Axial late
arterial-phase gadolinium-enhanced T1-weighted fat-suppressed
gradient-recalled echo MR image shows 2.5-cm hypointense mass (short
arrow) in head of pancreas responsible for double duct sign seen on MR
cholangiopancreatography. Fat plane between superior mesenteric artery and
pancreatic mass (long arrow) is obscured, suggesting vascular
invasion.
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Small pancreatic masses may not deform the pancreatic contour and may be
difficult to detect even on thin-section arterial and venous MDCT. The
excellent contrast resolution of MRI facilitates detection of a small tumor,
which may appear as a hypointense mass within the enhancing pancreas on
gadolinium-enhanced fat-suppressed images. Important secondary signs may be
present to suggest that an underlying pancreatic mass exists. Focal pancreatic
atrophy or pancreatic duct dilation may be seen on CT because of an underlying
downstream pancreatic mass not well seen on CT, for which MRI may be helpful
(Figs. 1A,
1B, and
1C).
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Fig. 4A —55-year-old man with pancreatic adenocarcinoma and suspected
liver metastases shown by MRI but inconspicuous on MDCT. Axial venous-phase
contrast-enhanced MDCT image shows hypodense mass (arrow) in
pancreatic head. Note homogeneous liver enhancement, without evidence of
metastases.
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Fig. 4B —55-year-old man with pancreatic adenocarcinoma and suspected
liver metastases shown by MRI but inconspicuous on MDCT. Axial arterial-phase
gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image
performed 3 days after MDCT shows several ring-enhancing liver lesions
(short white arrows) suggestive of liver metastases. These lesions
were not bright on T2-weighted images, suggesting bile lakes or abscesses.
Patient was afebrile. These lesions were inconspicuous on MDCT. There is
susceptibility artifact because of biliary stent (arrowhead) with
adjacent dilated pancreatic duct en face (long arrow). Note poorly
defined hypointense mass (black arrow) in pancreatic head.
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Fig. 4C —55-year-old man with pancreatic adenocarcinoma and suspected
liver metastases shown by MRI but inconspicuous on MDCT. Axial venous-phase
gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image
confirms the ring-enhancing lesions (arrows).
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Prominent Pancreatic Head on CT
A prominent pancreatic head may be seen on contrast-enhanced CT and may be
difficult to distinguish from a mass. MRI may help to detect or exclude
neoplasm in patients with indeterminate pancreatic enlargement. Focal fat of
the pancreas can occasionally present as a mass on CT or sonography and
potentially be confused with a tumor. On MRI, fatty abnormalities may show
increased signal on T1-weighted images, decreased signal intensity with fat
suppression, and phase cancellation on opposed-phase images. These typical MRI
features allow noninvasive characterization of fatty abnormalities and
distinguish them from cancer (Figs.
2A,
2B,
2C, and
2D).
Double Duct Sign
T2-weighted sequences and MR cholangiopancreatography (MRCP) are valuable
for assessing the pancreaticobiliary ducts. Dilation of the common bile duct
and the pancreatic duct (double duct sign) may result from either benign or
malignant causes, but is most commonly associated with cancer (Figs.
3A and
3B). Duct dilation may be
smooth or beaded with an abrupt or gradual transition in caliber. Karasawa et
al. [4] found the pancreatic
duct to be smooth or beaded with malignancy and more irregularly dilated when
associated with chronic pancreatitis. MRCP is valuable in characterizing the
obstruction and its location and causes, including stones or masses.
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Fig. 5B —55-year-old man with metastatic pancreatic adenocarcinoma.
Axial unenhanced T1-weighted fat-suppressed gradient-recalled echo MR image
shows multiple hypointense liver masses (arrows).
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Fig. 5C —55-year-old man with metastatic pancreatic adenocarcinoma.
Axial arterial-phase gadolinium-enhanced T1-weighted fat-suppressed
gradient-recalled echo MR image shows ring-enhancing lesions (white
arrows) and wedge-shaped perilesional enhancement (black arrows)
of metastases.
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Fig. 6 —57-year-old woman with newly diagnosed pancreatic carcinoma
and peritoneal metastases. Axial venous-phase gadolinium-enhanced T1-weighted
fat-suppressed gradient-recalled echo MR image shows right-sided peritoneal
implant (black arrow). Hypointense pancreatic mass (open
arrow) and pseudocyst (short white arrow) are seen. Mass in left
adrenal gland (long arrow) does not have imaging characteristics of
adenoma on other imaging sequences and may represent metastasis or lipid-poor
adenoma.
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Fig. 7A —53-year-old man with pancreatic carcinoma metastatic to liver
and greater omentum. Axial unenhanced T1-weighted fat-suppressed
gradient-recalled echo MR image shows low-signal-intensity lesions
(arrows) in liver, consistent with metastases.
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Fig. 7B —53-year-old man with pancreatic carcinoma metastatic to liver
and greater omentum. Axial gadolinium-enhanced T1-weighted fat-suppressed
gradient-recalled echo MR image shows enhancement along left side of greater
omentum (arrow), consistent with metastases. Hypointense liver
metastases (arrowheads) are also identified.
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Fig. 8A —36-year-old man with clinical history of pancreatitis was
subsequently proven to have pancreatic carcinoma with axillary lymph node
metastases. Axial arterial-phase contrast-enhanced MDCT image shows prominence
of pancreatic tail (arrow), mild peripancreatic fat stranding, and
multiple retroperitoneal lymph nodes (arrowheads).
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Fig. 8B —36-year-old man with clinical history of pancreatitis was
subsequently proven to have pancreatic carcinoma with axillary lymph node
metastases. Axial unenhanced T1-weighted fat-suppressed gradient-recalled echo
MR image shows subtle enlargement of pancreatic tail (arrow) and
multiple small lymph nodes (arrowheads) along celiac artery.
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Liver Metastases
The detection of liver metastases is critical for properly staging
pancreatic carcinoma, as this finding deems the patient unresectable.
Thin-collimation CT detects liver lesions smaller than 1 cm, which are often
difficult to characterize (Figs.
4A,
4B, and
4C). MRI may further delineate
these lesions as cysts, hemangiomas, or metastases, which significantly
influences patient workup and prognosis. Danet et al.
[5] described liver metastases
as minimally hypointense on T1-weighted images and isointense to moderately
hyperintense on T2-weighted images. These authors found that although the
primary tumor is generally hypovascular, a spectrum is seen of
hypovascular-to-hypervascular liver metastases with ring- or wedge-shaped
perilesional enhancement after IV gadolinium (Figs.
5A,
5B, and
5C). Reticuloendothelial
system-specific contrast agents (ferumoxides) and hepatocyte-selective
contrast agents (mangafodipir trisodium) may increase the conspicuity of liver
metastases through selective enhancement of the normal liver, although we do
not routinely use these agents
[6].
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Fig. 8C —36-year-old man with clinical history of pancreatitis was
subsequently proven to have pancreatic carcinoma with axillary lymph node
metastases. Axial venous-phase gadolinium-enhanced T1-weighted fat-suppressed
gradient-recalled echo MR image shows pancreatic tail mass (arrow),
which proved to be pancreatic carcinoma, more conspicuously than MDCT.
Multiple retroperitoneal lymph nodes (arrowheads) are also identified
around celiac artery.
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Fig. 9A —59-year-old man with unexplained acute recurrent pancreatitis
on MDCT examinations performed 2 years apart. The patient subsequently proved
to have pancreatic carcinoma. Axial arterial-phase contrast-enhanced MDCT
image from 2002 shows nonenhancing, ill-defined pancreatic body (white
arrow) with moderate peripancreatic fat stranding and fluid
(arrowheads), which is consistent with pancreatitis. Normal
enhancement in pancreatic tail is seen (black arrow).
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Fig. 9B —59-year-old man with unexplained acute recurrent pancreatitis
on MDCT examinations performed 2 years apart. The patient subsequently proved
to have pancreatic carcinoma. Axial arterial-phase contrast-enhanced MDCT
image from 2004 shows poorly defined, nonenhancing pancreatic body and tail
suggestive of necrosis (white arrow). There were findings suggestive
of pancreatic mass (black arrow).
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Peritoneal and Omental Metastases
Detection of extrapancreatic disease is critical because it prevents the
patient from undergoing unnecessary surgery. The peritoneum is often involved
in metastatic pancreatic carcinoma, and MRI may be more sensitive than CT for
detecting peritoneal enhancement and implants. Low et al.
[7] found MRI to be superior to
CT in detection of upper abdominal peritoneal metastases and implants smaller
than 1 cm, which are best seen in the presence of ascites (Figs.
6,
7A, and
7B).
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Fig. 9C —59-year-old man with unexplained acute recurrent pancreatitis
on MDCT examinations performed 2 years apart. The patient subsequently proved
to have pancreatic carcinoma. Axial T2-weighted HASTE MR image performed 3
weeks after MDCT (B) shows pancreatic duct dilation and atrophy of
pancreatic tail (arrow).
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Fig. 9D —59-year-old man with unexplained acute recurrent pancreatitis
on MDCT examinations performed 2 years apart. The patient subsequently proved
to have pancreatic carcinoma. Axial unenhanced T1-weighted fat-suppressed
gradient-recalled echo MR image at lower level than C shows mass
(arrow) in body of pancreas. Bowel (arrowhead) is seen
adjacent to pancreatic mass.
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Fig. 9E —59-year-old man with unexplained acute recurrent pancreatitis
on MDCT examinations performed 2 years apart. The patient subsequently proved
to have pancreatic carcinoma. Axial gadolinium-enhanced T1-weighted
fat-suppressed gradient-recalled echo MR image shows hypointense mass
(arrow) suspicious for tumor in body of pancreas. Endoscopic
sonography with biopsy showed adenocarcinoma. Bowel (arrowhead) is
seen adjacent to pancreatic mass.
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Pancreatitis Mimicking Pancreatic Cancer
Patients with pancreatic carcinoma often develop chronic pancreatitis
related to duct obstruction by the pancreatic mass. Chronic pancreatitis may
be difficult to differentiate from cancer because of similar imaging features.
These include hypointensity on unenhanced T1-weighted fat-suppressed images
and delayed enhancement on dynamic gadolinium-enhanced T1-weighted
fat-suppressed sequences [8].
Pancreatitis without an appropriate clinical history should prompt further
investigation for an underlying mass. The characteristics of the pancreatic
duct dilation may suggest chronic pancreatitis or pancreatic carcinoma as the
cause. Karasawa et al. [4]
found that the ratio of duct to gland was larger in carcinoma compared with
chronic pancreatitis. Pancreatic carcinoma can also present with gland
enlargement, abnormal enhancement, and peripancreatic stranding, mimicking
acute pancreatitis (Figs. 8A,
8B,
8C,
9A,
9B,
9C,
9D, and
9E). Additional findings, such
as retroperitoneal lymphadenopathy, may suggest an underlying malignancy.
Lymph Node Metastases
Pancreatic carcinoma commonly metastasizes to the peripancreatic and porta
hepatis lymph nodes. Size criteria are of limited use because microscopic
disease may be present in normal-size lymph nodes. Pathologically enlarged
lymph nodes (i.e., larger than 1 cm in short-axis diameter) determined by
imaging criteria should raise suspicion for disease involvement and prompt
further evaluation (Figs. 10A
and 10B).
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Fig. 10A —55-year-old man with metastatic pancreatic carcinoma. Axial
T2-weighted HASTE MR image shows multiple periaortic lymph nodes (white
arrows) and hyperintense metastasis (black arrow) in liver and
paraspinal muscles (arrowhead).
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Fig. 10B —55-year-old man with metastatic pancreatic carcinoma. Axial
gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image
shows multiple, ring-enhancing, periaortic lymph nodes (short
arrows). Ring-enhancing liver metastasis (arrowhead) and
multiple enhancing foci (long arrows) in paraspinal muscles caused by
metastases are seen.
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Vascular Invasion
Encasement of the celiac, superior mesenteric, or hepatic artery is a
contraindication to surgical resection. Limited involvement of the portal vein
or superior mesenteric vein by tumor may be treated with a surgical bypass.
However, extensive involvement of major venous structures by tumor is a
surgical contraindication [1].
In a patient with a history of pancreatic carcinoma, obliteration of the fat
planes surrounding the superior mesenteric artery is highly suggestive of
tumor encasement (Figs. 11A,
11B, and
11C). CT or MR angiography is
usually not necessary, but could be performed in inconclusive cases.
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Fig. 11A —49-year-old man with locally advanced pancreatic carcinoma.
Axial gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR
image shows abnormal enhancing soft tissue (arrows) surrounding
celiac artery, which is suspicious for vascular encasement.
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Fig. 11B —49-year-old man with locally advanced pancreatic carcinoma.
Coronal gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo
MR image shows abnormal soft tissue (arrow) surrounding origin of
celiac and superior mesenteric arteries. This tissue was positive for
malignancy by fine-needle aspiration.
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Conclusion
MRI may significantly impact therapy and prognosis in patients with
pancreatic cancer. Although CT is the established imaging technique for
evaluation of pancreatic carcinoma, the superior contrast resolution of MRI
may better detect and characterize non-contour-deforming lesions of the
pancreas, small liver metastases, and peritoneal disease. Specific indications
for MRI include suboptimal CT results and inability to administer iodinated
contrast material because of renal insufficiency or contrast allergy.
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Abstract
Introduction
