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Purpose: To describe the magnetic resonance imaging Key Words: pancreas, MR; pancreas, neoplasm; liver, MR;
spectrum of appearances of liver metastases from pancre- liver, neoplasm; MR contrast agents
atic ductal adenocarcinoma. J. Magn. Reson. Imaging 2003;18:181–188.
© 2003 Wiley-Liss, Inc.
Materials and Methods: We retrospectively evaluated the
MRI exams performed between July 1996 and August 2001
in all patients who had liver metastases from pancreatic
adenocarcinoma and histopathologic diagnosis from either DUCTAL ADENOCARCINOMA of the pancreas repre-
the primary pancreatic tumor, liver metastases, or both. sents 95% of malignant pancreatic tumors and is the
Sixteen patients were included in the study. All MR studies fourth most common cause of cancer death in the
were performed at 1.5 T with a standard protocol including United States (1). The prognosis of pancreatic adeno-
T1- and T2-weighted images and serial post-gadolinium carcinoma is very poor with a 5-year survival rate of 5%
spoiled gradient echo (SGE) images. Location, size, num- (1). Upon initial investigation, 65% of the patients have
ber, signal characteristics on T1- and T2-weighted images,
advanced local disease or hematogeneous metastases,
and pattern of enhancement on serial gadolinium-en-
with the liver being the most common site of distant
hanced SGE images were assessed.
metastases (2). On computed tomography (CT) and
Results: The diameter of metastases ranged from a few magnetic resonance imaging (MRI), pancreatic adeno-
millimetres to 4 cm, and 12 patients (75%) had only lesions carcinoma is considered a hypovascular lesion since it
of 1.5 cm or less. Capsular-based liver metastases were
enhances to a lesser extent than the normal pancreatic
found in 13 patients (81%) and three patients had only
capsular-based lesions with a diameter under 1.5 cm. Hy-
tissue on the arterial phase (1–3). It is generally believed
pervascular lesions were found in six patients (38%) and that metastases have the same angiographic character-
hypovascular lesions in 10 patients (62%). Perilesional en- istics as the primary tumor (4), and therefore liver
hancement was present in 10 patients (62%), with six pa- metastases from pancreatic adenocarcinoma are con-
tients (38%) having ring perilesional enhancement and sidered hypovascular (4,5). To our knowledge, hyper-
eight patients (50%) having wedge-shaped perilesional en- vascular liver metastases from pancreatic adenocarci-
hancement. noma have been only occasionally reported (4,6).
Conclusion: On MR imaging, hepatic metastases from Although both tumor vascularity and a high histologic
pancreatic adenocarcinoma show a range of enhancement grade have been related to a more aggressive tumoral
patterns. Hypervascular metastases are not rare. Capsular behavior and a poorer prognosis in pancreatic adeno-
based distribution, small diameter, and perilesional en- carcinoma, the relationship between these two factors
hancement are common features. This retrospective study is still poorly understood (2,7,8). MRI is very sensitive in
describes the MR imaging spectrum of appearances of liver analyzing the pattern of enhancement. Administration
metastases from pancreatic adenocarcinoma in patients
of an extracellular space contrast agent such as gado-
with histopathologic confirmation of the diagnosis.
linium chelate can provide estimates of the physiologic
properties of tumor microvessels such as perfusion,
diffusion, and distribution of contrast material within
the interstitial space (9). Moreover, the degree of vascu-
larization of a liver tumor is assessed on the arterial
phase of enhancement (10,11). To our knowledge, nei-
1
Department of Radiology, University of North Carolina at Chapel Hill, ther the spectrum of appearances of liver metastases
Chapel Hill, North Carolina.
2
Department of Pathology, University of North Carolina at Chapel Hill,
from pancreatic adenocarcinoma on MRI nor the fre-
Chapel Hill, North Carolina. quency of hypervascular liver metastases have been
*Address reprint requests to: R.C.S., Department of Radiology, Univer- described. Therefore, we performed this retrospective
sity of North Carolina at Chapel Hill, CB# 7510, Chapel Hill, North study to describe the MRI spectrum of appearances of
Carolina 27599-7510. E-mail: richsem@med.unc.edu
Received November 8, 2002; Accepted April 8, 2003.
liver metastases from pancreatic adenocarcinoma in
DOI 10.1002/jmri.10337 patients with histopathologic confirmation of the diag-
Published online in Wiley InterScience (www.interscience.wiley.com). nosis.
© 2003 Wiley-Liss, Inc. 181
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182 Danet et al.
Figure 1. Hypovascular liver metastases from pancreatic ductal adenocarcinoma in a 67-year-old female patient. Precontrast
T2-weighted HASTE image (a), T1-weighted SGE images (b), postcontrast arterial dominant phase (c), and interstitial phase (d)
images. On T2-weighted images the lesions are of minimal high signal intensity (a) and of low signal intensity on T1-weighted
images (b). Negligible enhancement of the lesion is demonstrated on early and late postcontrast images (c,d). Transient
moderately intense circumferential perilesional enhancement is identified on the arterial dominant phase. Perilesional enhance-
ment is demonstrated as enhancement beyond the lesion margins on the arterial dominant phase (c) when compared to the
precontrast T1-weighted images (b).
Figure 2. Hypervascular liver metastases from pancreatic carcinoma in a 61-year-old male patient. Precontrast T2-weighted
HASTE image (a), T1-weighted SGE image (b), postcontrast arterial dominant phase (c), and interstitial phase (d). On T2-
weighted images the lesions are almost isointense to the liver parenchyma and of low signal intensity on T1-weighted images.
Early enhancement is either homogeneous (arrow, c) or peripheral ring (arrowhead, c) and there is progression to isointensity on
delayed images (d). An adenocarcinoma of the tail of the pancreas is demonstrated on postcontrast images (curved arrow c,d).
ized as follows: 1) a faint ring of enhancement in five patients. In addition, lesions under 1.5 cm in diam-
patients, and 2) negligible enhancement identified in eter (four patients) also showed homogeneous en-
five patients. In this latter group, a peripheral ring of hancement. On the portal venous phase or the inter-
enhancement was identified on the portal phase in stitial phase, the hypervascular lesions showed either
four patients. On the interstitial phase, eight of the a persistent nonenhanced central core (five patients),
10 patients with hypovascular metastases showed progression to complete isointense (three patients), or
either an isointense homogeneous enhancement (one hyperintense homogeneity (four patients) relative to
patient) or a persistent nonenhancing central core the liver parenchyma. In three patients, both pat-
(seven patients). In one patient, the two types of cen- terns of progression were observed. In two patients,
tripetal progression were encountered, and in the last peripheral washout was identified on the interstitial
patient negligible enhancement was identified in all phase. Pronounced late enhancement was identified
phases of enhancement. A hypervascular pattern of in seven patients (six patients with hypervascular
enhancement was encountered in six patients (23 metastases and one patient with hypovascular me-
lesions) on the arterial dominant phase (Fig. 2). Pe- tastases). No patient possessed both hypervascular
ripheral ring of enhancement was identified in all and hypovascular metastases.
15222586, 2003, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jmri.10337 by CochraneItalia, Wiley Online Library on [10/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Liver Metastases From Pancreatic Adenocarcinoma 185
Figure 3. Wedge-shaped perilesional enhancement in a 59-year-old male patient. Precontrast T2-weighted HASTE image
(a),T1-weighted SGE images (b), postcontrast arterial dominant phase (c), and interstitial phase (d). Wedge-shaped early
perilesional enhancement associated with a metastatic lesion is clearly depicted on immediate post-gadolinium image (c) that
fades rapidly (d).
Table 1.
Enhancement Patterns of Liver Metastases From Adenocarcinoma of the Pancreas
Patients
Vascularity Arterial phase Portal venous and interstitial phase
N ⫽ 16
Hypervascular, 6 patients Intense homogeneous Hyperintense homogeneous 1
Isointense/hyperintense homogeneity 3
Intense peripheral rim Incomplete central progression or 6
progression to isointense/hyperintense
homogeneity
Peripheral washout 2
Hypovascular, 10 patients Faint peripheral rim Centripetal progression with lack of 5
central enhancement and/or
progression to isointense/hyperintense
homogeneity
Negligible Ring enhancement with centripetal 4
progression with lack of central
enhancement and/or progression to
isointense/hyperintense homogeneity
Negligible 1
low angiogenetic activity in pancreatic adenocarcinoma the cases in two series in the pathology literature (8,15).
may be responsible for the small size of the metastatic The relatively large number of patients with hypervas-
lesions (13,15). The small size of the liver metastases cular liver metastases in our study may be related to
may also relate to the aggressiveness of their malig- the presence of a hypervascular type of pancreatic ad-
nancy such that patients do not live long enough to enocarcinoma. However, complex series of interactions
develop large metastases. between the tumor and the host microenvironment
In our study, capsular based hepatic metastases have been described that influence the degree of vascu-
were noteworthy and were identified in a large number larization of primary tumor and metastases. We believe
of the patients (88%), while 18% (3) showed capsular- this may be the major contribution to explain the dif-
based metastases exclusively. The capsular-based dis- ference in vascularization between the primary tumor
tribution may be related to dissemination of pancreatic and the metastatic lesions (19,20). The native liver pro-
adenocarcinoma through direct seeding of the perito- vides a richly vascularized environment with its dual
neal cavity and serous coat of the liver. Alternatively, blood supply and sinusoidal architecture. This ana-
since pancreatic carcinoma shows a penchant for inva- tomic feature together with angiogenetic factors gener-
sion of the adjacent vascular structures, subcapsular ated by both host and metastatic tumor cells (21) may
metastases may reflect the hematogeneous spread of work in concert to render metastases hypervascular.
tumor via the hepatic artery that reaches the surface of On precontrast images, liver metastases with a diam-
the organ and ends in its fibrous coat in stellate plex- eter greater than 1.5 cm were generally identified.The
uses (16). most common appearance was that of moderately high
Generally, it has been considered that the vascularity signal intensity on T2-weighted images and a moder-
of the metastases is similar to the vascularity of the ately low signal intensity on T1-weighted images. These
primary focus (4,5). From the radiological point of view, signal characteristics have been commonly described
pancreatic ductal adenocarcinoma is considered a hy- for liver metastases in general (10,22). Metastases with
povascular tumor since, on the arterial phase, it en- a diameter less than 1.5 cm were inconsistently shown
hances to a lesser extent pancreatic tissue uninvolved on noncontrast images. On the arterial phase, hyper-
by tumor (1,8). This feature was present in all patients vascular metastases showed greater enhancement rel-
in our study. Thus, metastases from pancreatic adeno- ative to the liver parenchyma with the most common
carcinoma have been generally considered as hypovas- appearance being that of a peripheral rim of enhance-
cular (4,17). However, in 38% of the cases in our study, ment. As previously observed, less than 1.5 cm metas-
the vascularity of the liver metastases did not correlate tases often showed homogeneous enhancement (23).
with the enhancement of the primary tumor, as these Peripheral washout, considered as a specific sign of
metastases showed a hypervascular pattern of en- metastases and reflecting rapid arterio-venous transit
hancement. Angiographic studies have demonstrated in the periphery of the metastasis (24), was identified in
irregular and tortuous small vessels in up to 75% of the only two patients with hypervascular metastases. Hy-
cases of pancreatic adenocarcinoma (18). Endothelial povascular lesions showed either a faint peripheral ring
immunohistochemical staining measurements of an- or negligible enhancement on the arterial phase. Re-
giogenetic activity have shown relatively low microves- gardless of the vascularity of the metastases, 94% of the
sel density (MVD) counts for ductal adenocarcinoma of patients in our study demonstrated incomplete centrip-
the pancreas in comparison with other neoplasms such etal progression with persistence of a nonenhanced
as bladder or gastric carcinoma (15). However, a hyper- core on delayed images. Centripetal progression of en-
vascular subgroup of pancreatic adenocarcinoma with hancement on delayed images is a relatively common
high MVD counts has been described in up to 45% of feature of liver metastases and is suggestive of slow flow
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Liver Metastases From Pancreatic Adenocarcinoma 187
or slow passage of contrast material into the extracel- One important limitation in our study is the small
lular space in the central aspect of the tumor. The lack number of patients, which reflects both the single in-
of total central enhancement may be related to necro- stitution accrual and the limited number of concurrent
sis, fibrosis, compression of central vessels (25), or slow histopathologic examinations. On the basis of these
centripetal flow. Pronounced late enhancement was ob- initial observations, it would be of interest to study a
served in metastases in 44% of the patients in our larger population in order to correlate the metastatic
study. Adenocarcinoma of the pancreas has a high con- pattern of enhancement on MR images, tumoral MVD,
tent of desmoplastic or fibrous tissue (1) that may con- and patient outcome.
tribute to the prolonged enhancement on delayed im- In conclusion, a variable pattern of enhancement of
ages. Perilesional enhancement on dynamic contrast metastases from pancreatic adenocarcinoma can be
enhanced MR images has been observed in hepatic demonstrated by MRI. Although adenocarcinoma of the
metastases most commonly from colorectal carcinoma. pancreas from the radiological point of view is consid-
Semelka et al (26) showed that intense perilesional en- ered a hypovascular tumor, hypervascular liver metas-
hancement on early gadolinium SGE images correlates tases are common and are found in 38% of the patients.
with peritumoral desmoplastic reaction, inflammatory In our study, hepatic metastases from pancreatic car-
cell infiltration, and vascular proliferation. In our cinoma generally presented as small and multiple he-
study, perilesional enhancement was present in 63% of patic lesions. We observed that a capsular based distri-
the patients and the wedge-shaped pattern was the bution is common, underscoring the fact that careful
most common. We believe the wedge-shaped pattern of attention should be paid to this location when staging
enhancement is related to a vascular imbalance be- pancreatic adenocarcinoma. Perilesional enhancement
tween the arterial and the portal supply with resultant is also a common feature of these metastases with a
wedge-shaped pattern most commonly observed.
increased hepatic arterial enhancement. However, the
precise underlying pathophysiologic cause remains un-
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