AJR 2000; 175:91-97
© American Roentgen Ray Society
Selective Intraarterial Contrast-Enhanced CT of Pancreaticoduodenal Tumors
Early Clinical Experience in Evaluating Blood Supply and Detectability
Hiroyoshi Furukawa1,
Ryoko Iwata1,
Noriyuki Moriyama1 and
Tomoo Kosuge2
1
Department of Diagnostic Radiology, National Cancer Center Hospital, 5-1-1,
Tsukiji, Chuo-ku, Tokyo, 104, Japan.
2
Department of Surgery, National Cancer Center Hospital, Chuo-ku, Tokyo, 104,
Japan.
Received August 11, 1999;
accepted after revision December 10, 1999.
Supported in part by a grant-in-aid for cancer research from the Japanese
Ministry of Health and Welfare.
Address correspondence to H. Furukawa.
Abstract
OBJECTIVE. The purpose of this study was to compare CT with
selective intraarterial contrast enhancement with IV contrast-enhanced CT for
diagnostic usefulness in the detection of tumors in the pancreaticoduodenal
region.
SUBJECTS AND METHODS. intraarterial contrast-enhanced CT was
performed in 36 patients with tumors of the pancreaticoduodenal region.
Feeding arteries of the tumors and distribution of hyperattenuating areas on
intraarterial contrast-enhanced CT were analyzed with various routes of
contrast material injections. The intraarterial contrast-enhanced CT scans
were compared with the IV contrast-enhanced CT scans.
RESULTS. In all 29 patients with standard vascular anatomy, the
right cephalic portion of the pancreatic head was enhanced on CT during common
hepatic or gastroduodenal arteriography and the left caudal portion was
enhanced on CT during superior mesenteric arteriography. The enhanced areas
were complementary to each other in the whole pancreatic head, including the
tumor. Tumor conspicuity from the surrounding pancreatic tissue on
intraarterial contrast-enhanced CT was not superior to that on IV
contrast-enhanced CT in all but four patients with cystic tumors. After
intraarterial contrast-enhanced CT, three patients with tumors less invasive
than pancreatic ductal carcinoma underwent local resection of their
lesions.
CONCLUSION. Intraarterial contrast-enhanced CT for
pancreaticoduodenal tumors has potential technical problems and is not
valuable in improving the detectability of tumors other than cystic lesions
because the enhancement of the wall and septa of the tumor is emphasized.
However, the feeding artery of the tumor and its surrounding tissue were
clearly depicted.
Introduction
An understanding of arterial blood flow in neoplasms is important for
radiologic interpretation, cancer research, and selection of therapeutic
strategies. The hemodynamics of pancreaticoduodenal tumors has been
radiologically investigated using angiography
[1,2,3],
dynamic CT
[4,5,6],
dynamic MR imaging [7], Doppler
and contrast-enhanced sonography
[8,
9], and combined techniques
such as CT during arteriography
[10] and sonographic
angiography [11]. Angiography
has been a standard method for investigating vascular anatomy and tumor
resectability [3].
Pancreatic adenocarcinoma, which is the most common neoplasm of the
pancreaticoduodenal region, is a scirrhous, infiltrating lesion similar to
other adenocarcinomas of the gastrointestinal tract. The angiographic
abnormalities that are caused by the tumor reflect the infiltrating nature of
the tumor. The salient angiographic abnormality is arterial encasement in or
around the pancreas; therefore, an accurate evaluation of the arterial blood
supply to this region has been difficult.
Helical CT with selective intraarterial contrast enhancement can show the
blood distribution of a particular artery injected with contrast material on
transaxial images. Although the effectiveness of this technique for evaluating
the detectability and vascularity of hepatic tumors has been reported
[12,13,14],
it has rarely been applied to tumors of the pancreaticoduodenal region
[10]. We evaluated tumor
enhancement of the pancreaticoduodenal region by intraarterial
contrast-enhanced CT with selective catheterization into the peripancreatic
artery and compared intraarterial contrast-enhanced CT scans with conventional
IV contrast-enhanced CT scans.
Subjects and Methods
Between January 1997 and December 1998 at our institution, of 52
consecutive patients with pancreaticoduodenal diseases who underwent
angiography, 36 underwent intraarterial contrast-enhanced CT (24 men and 12
women; age range, 32-79 years; mean, 64 years) for pancreaticoduodenal tumors.
All 36 patients were candidates for surgical treatment. The other 16 patients
did not undergo intraarterial contrast-enhanced CT because their diseases were
far advanced and required no further examination. The final diagnoses in the
36 patients were made by surgical resection and percutaneous or endoscopic
biopsy: pancreatic carcinoma in 21, intraductal papillary adenoma in four,
ampullary carcinoma in three, intrapancreatic bile duct carcinoma in two,
duodenal carcinoma in two, nonfunctioning islet cell tumor in two, carcinoid
tumor of the ampulla in one, and leiomyosarcoma of the duodenum in one. The
locations of the 27 pancreatic tumors were head in 22 patients and body and
tail in five.
IV contrast-enhanced CT was performed and the tumors were confirmed in all
36 patients before intraarterial contrast-enhanced CT. IV contrast-enhanced CT
was obtained with an X-Vigor scanner (Toshiba Medical Systems, Tokyo, Japan).
CT was performed with 5-mm collimation and 5 mm/sec table movement (scan time
per section, 1 sec; scan collimation, 5 mm; scan pitch, 1) with mechanical
injection of 150 ml of iohexol (Omnipaque; Daiichi, Tokyo, Japan) (300 mg
I/ml) into the antecubital vein at a rate of 2-3 ml/sec. CT scanning commenced
40-60 sec after the start of the injection of contrast material. Transaxial
images from the helical CT scan were reconstructed with 2-5 mm overlapping
intervals.
Patients underwent intraarterial contrast-enhanced CT at the time of
conventional preoperative angiography. Informed consent was obtained from all
36 patients before the procedure. In the angiography suite, celiac and
superior mesenteric arteriography were performed to visualize the
peripancreatic artery anatomy. A 5-French catheter system (Serecon catheter;
Clinical Supply, Gifu, Japan) was used via the right transfemoral approach.
After confirming the branching pattern of the celiac and superior mesenteric
arteries, helical CT during the injection of the contrast material into the
celiac artery, the superior mesenteric artery, and their branches was
performed according to the tumor location to evaluate the perfusion areas.
Among the 36 patients, major anatomic anomalies of the peripancreatic
artery were shown in seven patients (19%), the common hepatic artery arising
from the superior mesenteric artery in five, and the right hepatic artery
arising from the superior mesenteric artery in two. In cases with the common
hepatic artery arising from the superior mesenteric artery, CT during the
injection of the contrast material into the hepatomesenteric trunk (the common
axis of the common hepatic artery and the superior mesenteric artery) was
routinely performed. In cases with the right hepatic artery arising from the
superior mesenteric artery, CT was performed during the injection of the
contrast material into the superior mesenteric trunk and during injection into
the celiac artery.
A total of 76 injections for intraarterial contrast-enhanced CT were
performed; one to three procedures of intraarterial contrast-enhanced CT were
performed in each patient (average, 2.1). All studies were performed with an
IVR-CT system (Toshiba Medical Systems), which comprised a digital subtraction
angiography system (KXO-80C/DFP-2000A; Toshiba Medical Systems) and a helical
CT scanner (X-Vision; Toshiba Medical Systems). This equipment is capable of
performing digital subtraction angiography and CT with the patient in one
position. The helical CT was obtained with a 1:1 pitch, 5-mm collimation,
2-5-mm reconstruction, 120 kVp, and 250 mAs. Scanning was started 5-10 sec
after the commencement of injection of ioversol (Optiray; Mallinckrodt
Medical, Montreal, Canada) (350 mg I/ml) diluted with saline (1:2 ratio) at a
rate of 1-3 ml/sec for a total volume of 20-60 ml (40 ml in most cases) using
a power injector (Autoenhance A-50; Nemoto Kyorindo, Tokyo, Japan). For
thinner arteries, such as the branches of the gastroduodenal artery, the
contrast material was manually injected. We confirmed the absence of reflux
into the arteries of this condition on previous conventional arteriography or
on test CT. A vasodilator was not injected through the catheter.
All intraarterial contrast-enhanced CT and angiographic images were
analyzed by two experienced radiologists; discrepancies were resolved by
consensus. The medical history, laboratory data, and IV contrast-enhanced CT
scans were available to the reviewers at the time of image analysis. The
evaluation was focused on the distribution and correlation of the
hyperattenuating areas in the pancreaticoduodenal region and the degree of
enhancement of the tumor injected with contrast material from the artery in
which a catheter tip was inserted. These intraarterial contrast-enhanced CT
scans were compared with the IV contrast-enhanced CT scans and superiority of
the tumor conspicuity was evaluated. If the tumor was supplied by more than
one artery on intraarterial contrast-enhanced CT, these intraarterial
contrast-enhanced CT scans were combined for the evaluation.
Results
In all 29 patients with normal vascular anatomy and two with the right
hepatic artery arising from the superior mesenteric artery, the right cephalic
side of the pancreatic head, including the ampulla of Vater, was enhanced on
CT during the injection of the contrast material from the celiac artery side
(Figs.
1A,1B,1C
and
2A,2B,2C).
In contrast, the left caudal side of the pancreatic head was enhanced on CT
during the injection of the contrast material from the superior mesenteric
artery side (Figs.
1A,1B,1C
and
2A,2B,2C).
These areas were complementary to each other in the whole pancreatic head
parenchyma. In five patients with a tumor in the hepatomesenteric trunk, the
whole pancreatic head was enhanced by injection of the contrast material into
the hepatomesenteric trunk alone (Fig.
3A,3B,3C).
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Fig. 1A. —Pancreatic adenocarcinoma in 52-year-old woman. IV contrast-enhanced
CT scan shows hypoattenuating area in pancreatic head (arrowheads).
Note superior tumor conspicuity from surrounding pancreatic tissue.
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Fig. 1B. —Pancreatic adenocarcinoma in 52-year-old woman. CT during common
hepatic arteriography at same level as A shows marked enhancement on
right side of pancreas and duodenum. Note faint enhancement on right side of
tumor (arrow). Volume and injection rate of contrast material were 50
ml and 2 ml/sec, respectively.
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Fig. 1C. —Pancreatic adenocarcinoma in 52-year-old woman. CT scan obtained
during superior mesenteric arteriography at same level as A and
B shows faint enhancement on left side of tumor (arrow) and
marked enhancement of jejunum. Volume and injection rate of contrast material
were 50 ml and 1.5 ml/sec, respectively. Both enhanced areas in B and
C are complementary to each other in whole pancreaticoduodenal region
including tumor.
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Fig. 2B. —Ampullary carcinoma in 58-year-old man. CT scan obtained during
gastroduodenal arteriography at same level as A shows enhancement in
right superior side of tumor and in duodenum. Volume and injection rate of
contrast material were 30 ml and 1.5 ml/sec, respectively.
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Fig. 2C. —Ampullary carcinoma in 58-year-old man. CT scan obtained during
superior mesenteric arteriography at same level as A and B shows
enhancement in left inferior side of tumor and in jejunum. Volume and
injection rate of contrast material were 60 ml and 3 ml/sec, respectively.
Both enhanced areas in B and C are complementary to each other
in whole pancreaticoduodenal region including tumor.
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Fig. 3A. —Pancreatic adenocarcinoma in 74-year-old man. On arteriography,
common hepatic artery arises from superior hepatic artery. Volume and
injection rate of contrast material were 30 ml and 4 ml/sec, respectively.
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Fig. 3B. —Pancreatic adenocarcinoma in 74-year-old man. IV contrast-enhanced
CT scan shows tumor as hypoattenuated area in pancreatic head
(arrow). Note superior tumor conspicuity from surrounding pancreatic
tissue.
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Fig. 3C. —Pancreatic adenocarcinoma in 74-year-old man. CT scan obtained
during hepatomesenteric arteriography at same level as A shows marked
enhancement in whole pancreatic head, in which tumor appears as hypoattenuated
area (arrow). Volume and injection rate of contrast material were 60
ml and 3 ml/sec, respectively.
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On intraarterial contrast-enhanced CT, the tumors were revealed as
hypoattenuating areas compared with the surrounding pancreatic tissue in all
21 patients with pancreatic ductal carcinoma (Figs.
1A,1B,1C
and
3A,3B,3C),
two patients with bile duct carcinoma, and two patients with duodenal
carcinoma. The peripheral area of the tumor was slightly enhanced in all
patients (Figs.
1A,1B,1C
and
3A,3B,3C).
In 15 (13 with normal vascular anatomy and two with the right hepatic artery
arising from the superior mesenteric artery) of the 25 patients, the tumor was
complementarily enhanced by the injection of the contrast material into the
celiac artery and the superior mesenteric artery (Fig.
1A,1B,1C).
In six patients (five with normal vascular anatomy and one with the right
hepatic artery from the superior mesenteric artery), the tumor was enhanced by
the injection of the contrast material into the celiac artery alone in four
and the superior mesenteric artery alone in two. In the remaining four
patients with a tumor in the hepatomesenteric trunk, the tumor was enhanced by
the injection of contrast material into the hepatomesenteric trunk (Fig.
3A,3B,3C).
The attenuation difference between the tumor and its surrounding pancreatic
parenchyma on intraarterial contrast-enhanced CT was equal or inferior to that
on IV contrast-enhanced CT in all 25 cases (Figs.
1A,1B,1C
and
3A,3B,3C).
All three patients with ampullary carcinoma were shown to have a mass
protruding into the duodenal lumen on intraarterial contrast-enhanced CT (Fig.
2A,2B,2C).
The findings were almost the same as those of IV contrast-enhanced CT. In
these patients, most of the tumor was enhanced on CT during the injection of
the contrast material into the common hepatic artery or the gastroduodenal
artery. On CT during superior mesenteric arteriography, only a small dorsal
part of the tumor was enhanced.
Two patients with islet cell tumor and one each of ampullary carcinoid and
duodenal leiomyosarcoma were shown to have an isoattenuating or
hyperattenuating area compared with that of the surrounding pancreatic
parenchyma on intraarterial contrast-enhanced CT (Fig.
4A,4B,4C,4D,4E).
These four patients had normal vascular anatomy. In both patients with islet
cell tumors, the tumor was complementarily enhanced by the injection of the
contrast material into the celiac artery and the superior mesenteric artery
(Fig.
4A,4B,4C,4D,4E).
Each patient with ampullary carcinoid and duodenal leiomyosarcoma was shown to
have a hyperattenuated area on CT during the injection of the contrast
material into the gastroduodenal artery and the superior mesenteric artery,
respectively. The attenuation difference between the tumor and its surrounding
pancreatic parenchyma on intraarterial contrast-enhanced CT was almost equal
to that on IV contrast-enhanced CT in all four patients (Fig.
4A,4B,4C,4D,4E).
According to these findings on intraarterial contrast-enhanced CT, in three of
the four patients with a hyperattenuating tumor that was less invasive than
pancreatic ductal carcinoma based on their imaging characteristics or
pre-existing pathologic data, local resection of the tumor was performed to
divide the feeding arteries and preserve the normal pancreatic parenchyma and
the duodenum.
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Fig. 4A. —Islet cell tumor of the pancreas in 45-year-old man. Superior
mesenteric arteriogram shows marked tumor stain (arrows). Volume and
injection rate of contrast material were 25 ml and 3 ml/sec, respectively.
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Fig. 4B. —Islet cell tumor of the pancreas in 45-year-old man. Celiac
arteriogram also shows faint tumor stain (arrow). Volume and
injection rate of contrast material were 20 ml and 4 ml/sec, respectively.
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Fig. 4D. —Islet cell tumor of the pancreas in 45-year-old man. CT scan
obtained during superior mesenteric arteriography shows enhancement in large
left-sided pancreatic tumor (arrow) and pancreatic body. Volume and
injection rate of contrast material were 40 ml and 2 ml/sec, respectively.
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Fig. 4E. —Islet cell tumor of the pancreas in 45-year-old man. CT scan
obtained during celiac arteriography shows enhancement in small right-sided
pancreatic tumor (arrow) and pancreatic head and tail. Volume and
injection rate of contrast material were 40 ml and 2 ml/sec, respectively.
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In all four patients with intraductal papillary adenoma, each tumor was
shown as a multilocular cystic lesion with a hyperattenuated wall and septa
(Fig.
5A,5B,5C,5D,5E).
The wall and septa were complementarily enhanced by the injection of the
contrast material into the celiac artery and the superior mesenteric artery in
two patients. In the other two patients, these were shown as lesions with a
hyperattenuated wall and septa on CT during the injection of the contrast
material into the gastroduodenal artery and dorsal pancreatic artery alone,
respectively. Intraarterial contrast-enhanced CT showed these septal
structures better than IV contrast-enhanced CT in all four patients (Fig.
5A,5B,5C,5D,5E).
The mural nodule was not shown, nor was it similar to the macroscopic
appearance of the resected specimen.
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Fig. 5A. —Intraductal papillary adenoma in 69-year-old man. Celiac arteriogram
shows no remarkable or abnormal findings. Volume and injection rate of
contrast material were 20 ml and 4 ml/sec, respectively. GD = gastroduodenal
artery, DP = dorsal pancreatic artery.
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Fig. 5C. —Intraductal papillary adenoma in 69-year-old man. CT scan obtained
during celiac arteriography at same level as B shows marked enhancement
in whole pancreatic head. Volume and injection rate of contrast material were
50 ml and 2.5 ml/sec, respectively.
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Fig. 5D. —Intraductal papillary adenoma in 69-year-old man. CT scan obtained
during gastroduodenal arteriography at same level as B shows enhanced
area in right side of pancreas and duodenum. Volume and injection rate of
contrast material were 20 ml and 1 ml/sec, respectively. Cystic tumor is not
enhanced.
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Fig. 5E. —Intraductal papillary adenoma in 69-year-old man. CT scan obtained
during dorsal pancreatic arteriography shows marked enhancement in cystic
tumor. Volume and injection rate of contrast material were 10 ml and 0.5
ml/sec, respectively. Note conspicuity of wall and septa of tumor.
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Discussion
Several authors have analyzed the vessels of the pancreaticoduodenal region
by arteriography or autopsy
[15,16,17].
However, it is difficult to clarify the distribution area of each vessel using
these techniques. Intraarterial contrast-enhanced CT can show the blood
distribution of a particular artery injected with contrast material on
transaxial images. With intraarterial contrast-enhanced CT of each
peripancreatic artery, the path and zones supplied can be further elucidated.
Such elucidation is achieved even in hypovascular tumors of this region.
In the patients with normal vascular anatomy, the right cephalic side of
the pancreatic head, including the ampulla of Vater, was enhanced on
intraarterial contrast-enhanced CT from the celiac artery side. In contrast,
the left caudal side of the pancreatic head was enhanced on intraarterial
contrast-enhanced CT from the superior mesenteric artery side. These areas
were complementary to each other in the whole pancreatic head parenchyma. This
means that the pancreatic head can be clinically separated into the right
superior and the left posterior segments by the arterial blood supply.
Although unusual opacification induced by high-pressure injection might be a
potential pitfall, each artery was catheterized and injected without reflux,
then helical CT was performed so that the anatomy of the enhanced area could
be evaluated by transaxial images under quasiphysiologic conditions. Detailed
analysis could not be performed for the blood supply to the body and tail of
the pancreas because of the small number of patients.
If simultaneous celiac and superior mesenteric arteriography are performed
by placing two catheters, one in each artery, or if a balloon catheter has
been used in either artery, the whole pancreaticoduodenal arcade may appear
similar to that of a patient with a tumor in the hepatomesenteric trunk
[18,
19]. However, we did not use
these methods because they are too complicated and invasive for routine
preoperative evaluation.
We thought that intraarterial contrast-enhanced CT would prove superior to
IV contrast-enhanced CT for the detection of hypovascular tumors of this
region because of the more intensive enhancement in normal pancreatic
parenchyma, which means that the tumor should be demarcated more easily.
Similarly, because of the more pronounced tumor enhancement, hypervascular
tumors should be more readily visualized. However, the attenuation difference
between the tumor and surrounding organs on intraarterial contrast-enhanced CT
was not superior to that on IV contrast-enhanced CT for several reasons. Any
type of peripancreatic tumor has an arterial blood supply from the celiac
artery, the superior mesenteric artery, or both. Even pancreatic ductal
carcinoma, bile duct carcinoma, and duodenal carcinoma have a blood supply,
although they are thought to be hypovascular tumors. Because the contrast
material was directly and mechanically injected on intraarterial
contrast-enhanced CT, the enhancement of the tumor was emphasized over IV
contrast-enhanced CT. Moreover, intraarterial contrast-enhanced CT was usually
performed after conventional arteriography in which some amount of contrast
material had already been injected. Once the contrast material has moved into
the fibrous tissue that accompanies pancreatic and bile duct adenocarcinoma,
it remains there for approximately 5-15 min
[20,
21]. Therefore, the
attenuation difference between the tumor and the surrounding pancreatic
parenchyma on intraarterial contrast-enhanced CT was inferior to that on IV
contrast-enhanced CT. Ahlström et al.
[10] also compared
intraarterial contrast-enhanced CT with angiography for localizing endocrine
tumors and found that intraarterial contrast-enhanced CT offered no
improvement of the detectability. Our results suggest that intraarterial
contrast-enhanced CT is not valuable in improving the detectability of
pancreaticoduodenal tumors, although a statistical comparison of IV
contrast-enhanced CT and intraarterial contrast-enhanced CT was impossible
because of the small number of patients and selection bias in our study. Our
results are different from the evaluation of CT during arteriography and
arterial portography for liver tumors
[12,
13].
In contrast to the results in the solid tumors, intraarterial
contrast-enhanced CT revealed the wall and septa of the cystic lesions, such
as intraductal papillary tumors, better than IV contrast-enhanced CT. As
mentioned, the contrast material was directly and mechanically injected on
intraarterial contrast-enhanced CT, and the attenuation difference between
these structures and the surrounding fluid was emphasized better than on IV
contrast-enhanced CT. Because all the cystic lesions in this series were
benign, the mural nodules, which are an important landmark for differentiating
whether the cystic tumor is malignant or benign
[22], did not appear on the
resected specimens. We suppose that, when present, mural nodules may be shown
on intraarterial contrast-enhanced CT better than on IV contrast-enhanced
CT.
Recently, regional arterial infusion of protease inhibitor and antibiotics
in acute necrotizing pancreatitis has been performed and the effectiveness in
reducing mortality and preventing the development of pancreatic infection has
been reported [23]. Similarly,
intraarterial chemotherapy has been attempted to improve the survival rate of
advanced pancreatic carcinoma
[24]. To perform these
transarterial infusion therapies effectively, evaluation of the perfusion area
via the inserted catheter is necessary. The results in this study may suggest
an optimal approach for infusion of these therapeutic drugs.
Although superiority of the detectability of the pancreatic tumor was not
shown, intraarterial contrast-enhanced CT showed filling of the vascular bed
supplied by the artery injected. According to the findings on intraarterial
contrast-enhanced CT, local resection was performed in the patients with less
invasive tumors to divide the feeding arteries and preserve the normal tissue.
Surgically, several types of limited resection of the pancreas have been
attempted for chronic pancreatitis and tumors with low invasiveness to
preserve the physiologic condition of the pancreas
[25,
26]. Intraarterial
contrast-enhanced CT may be useful for surgical planning of limited resection
of this region.
Although our study is preliminary and limited by the small number of
patients and selection bias, intraarterial contrast-enhanced CT of
pancreaticoduodenal tumors was not valuable for improving the detectability of
tumors other than cystic lesions. However, the feeding artery of the tumor and
the surrounding tissue were clearly shown. These results will be useful for
limited resection and transarterial infusion therapy of this region.
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Abstract
Introduction
