DOI:10.2214/AJR.07.2131
AJR 2007; 189:1044-1050
© American Roentgen Ray Society
New Concepts in Staging and Treatment of Locally Advanced Pancreatic Head Cancer
Chandana G. Lall1,
Thomas J. Howard2,
Arunan Skandarajah1,
John M. DeWitt3,
Alex M. Aisen1 and
Kumaresan Sandrasegaran1
1 Department of Radiology, Indiana University Medical Center, UH 0279, 550 N
University Blvd., Indianapolis, IN 46202.
2 Department of Surgery, Indiana University Medical Center, Indianapolis,
IN.
3 Department of Medicine, Indiana University Medical Center, Indianapolis,
IN.
Received February 27, 2007;
accepted after revision June 6, 2007.
Address correspondence to K. Sandrasegaran.
CME
This article is available for CME credit. See
www.arrs.org
for more information.
Abstract
OBJECTIVE. The objective of this article is to discuss the CT
findings that guide surgeons in deciding the feasibility of tumor excision in
patients with locally advanced pancreatic head cancers.
CONCLUSION. Vascular resection as an adjunct to
pancreaticoduodenectomy is increasingly used in pancreatic head cancer. As a
result, the imaging criteria to determine which patients are candidates for
potentially curative resection are evolving.
Keywords: borderline resectability • neoadjuvant therapy • pancreatic cancer • pancreaticoduodenectomy • portal vein • superior mesenteric vein
Introduction
Pancreatic carcinoma is the second most common malignancy of the
gastrointestinal tract and the fifth most common malignancy in adults. The
only potentially curative treatment is complete surgical resection, which is
limited to those patients without metastatic disease and in whom the entire
tumor can be resected with negative surgical margins (R0 resection). This
ideal surgical outcome should be contrasted with resection containing
microscopically (R1) or macroscopically (R2) positive surgical margins. In
many patients with potentially curable disease, the only obstacle to achieving
a completely negative surgical margin is involvement of the portal or superior
mesenteric vein.
In the past, pancreaticoduodenectomy (Whipple procedure) was avoided in
these patients because venous resection was perceived to be technically
difficult and had a poor long-term survival rate
[1]. With advances in surgical
techniques, venous resection and reconstruction are increasingly performed
[1–7],
with a morbidity and mortality similar to pancreaticoduodenectomy without
vascular reconstruction [1,
2,
6]. Traditionally, arterial
invasion has been deemed to be inoperable in patients with pancreatic head
cancer because of the high morbidity of arterial reconstruction and the
concomitant presence of extensive celiac or mesenteric neural invasion
[8]. However, in carefully
selected cases, early arterial invasion is considered resectable
[9].
Several radiologic reports have examined the accuracy of CT or MRI in
determining the presence of vascular invasion
[10–16].
It is now necessary to show on preoperative staging CT studies not only the
presence but also the site and extent of venous and arterial invasion. To our
knowledge, there is no literature on the additional radiologic information
that should be given to the surgeon performing vascular reconstruction in this
setting. In this article, we discuss our experience of the CT findings that
predict unresectability or resectability with vascular reconstruction of
pancreatic head cancer. Before reviewing the pretreatment CT staging, we
discuss new concepts in surgical and oncologic treatment of locally invasive
nonmetastatic pancreatic cancer.
Pancreaticoduodenectomy (Whipple Procedure)
Pancreaticoduodenectomy is the only potentially curative treatment for
carcinoma of the head of the pancreas. Survival rate, after resection, is
about 12–20% at 5 years compared with less than 1% for those who do not
qualify for this surgery
[17–19].
However, only 15–20% of patients present with potentially resectable
tumors [9]. Pylorus-preserving
pancreaticoduodenectomy consists of radical resection of the pancreatic head,
duodenum, regional lymph nodes, gallbladder, and distal common bile duct
(Fig. 1). Contiguous invasion
of the duodenum, stomach, right colon, or regional lymph nodes is not a
contraindication to surgery
[20]. One of the key
requirements for a successful surgery is a negative retroperitoneal
soft-tissue margin. The retroperitoneal margin is the tissue to the right of
the first 3–4 cm of the superior mesenteric artery
[9]. Resection with a positive
margin (R1 or R2) results in a median survival of 8–12 months that is
not significantly different from those who undergo palliative therapy
[21,
22].
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Fig. 1 —Diagram shows pylorus-preserving pancreaticoduodenectomy
(classic Whipple procedure is shown in inset). This procedure entails radical
dissection of pancreatic head, adjacent nodes, gallbladder, common bile duct,
and most or all of duodenum followed by gastrojejunostomy or
duodenojejunostomy, pancreaticojejunostomy, and hepaticojejunostomy.
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Fig. 2 —Diagram shows sites of venous invasion that may be
potentially resectable; v = vein, vv = veins. Most common anatomic
configuration of portal vein is shown. Early invasion of venous segment marked
in purple is potentially resectable, with subsequent vein reconstruction.
Invasion of superior mesenteric vein proximal (away from liver) to its jejunal
tributaries is not resectable due to difficulty with vascular control in this
area and potential for bowel infarction.
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Fig. 3A —62-year-old man with locally advanced pancreatic cancer.
Intraoperative photograph before tumor resection shows portal vein confluence
(arrowhead) involved by tumor (arrows) arising from superior
aspect of pancreatic head.
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Fig. 3B —62-year-old man with locally advanced pancreatic cancer.
Intraoperative photograph after tumor resection shows portal and superior
mesenteric veins reconstructed over segment marked by sutures
(arrows).
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Venous reconstruction performed at the time of pancreaticoduodenectomy
increases the operative time, transfusion requirements, and total hospital
length of stay but has been shown to have no significant impact on
perioperative morbidity, mortality, or the incidence of positive histologic
margins [1]. Survival of
patients after such surgery is similar to patients with pancreatic cancer who
undergo pancreaticoduodenectomy without the need for venous reconstruction
[1,
2,
6]. It is possible to resect
and reconstruct the superior mesenteric, splenic, and portal veins during
pancreaticoduodenectomy for cancer of the pancreatic head as long as flow
remains in the vessel and adequate distal (portal vein) and proximal (superior
mesenteric vein) tumor-free margins can be obtained.
In addition, the resected segment of vessel should be downstream (toward
the liver) from the entry of the jejunal vein tributaries draining the small
bowel (Fig. 2). Resection of a
venous segment may be followed by end-to-end anastomosis or interposition of a
vascular conduit (Fig. 3A,
3B). In most cases, the right
and middle colic veins (gastrocolic trunk) or the inferior mesenteric vein may
be sacrificed without major sequelae because of the extensive collateral flow
of colonic veins. However, as a general rule, it is usually not wise to resect
both the gastrocolic trunk (containing the right colic vein) and the inferior
mesenteric vein (left colic vein) at the same time. Current contraindications
to surgery include occlusion of the superior mesenteric or portal vein or
vascular encasement (> 180° arc of tumor contact) of the superior
mesenteric, celiac, or hepatic arteries
[1,
7,
23]. In our experience,
long-segment (typically at least 2 cm) circumferential tumor involvement of
the superior mesenteric or portal vein is a relative contraindication to
vascular reconstruction.
Neoadjuvant Chemoradiotherapy
Preoperative chemoradiotherapy is sometimes used to treat potentially
positive margins—that is, downstage from an R1 margin to R0, and to
provide early treatment of micrometastatic disease, which often exists in
locally advanced tumors. Chemoradiotherapy also allows a period of time,
usually 6 weeks to 3 months, to gauge the aggressiveness of the cancer and
exclude from surgery patients who have unresponsive and rampant disease.
Neoadjuvant chemoradiotherapy may be given to a carefully selected group of
patients with a pancreatic head cancer of borderline resectability
[9]. Baseline CT in such
patients may show any of the following: tumor abutting the superior mesenteric
artery over a segment of less than 180°, periarterial fat stranding around
the superior mesenteric artery, or short-segment abutment (< 180° of
circumferential contact) or encasement (> 180°) of the common hepatic
artery at the origin of the gastroduodenal artery
[9].
Radiation therapy is given as a fractionated external beam course, and
chemotherapy involves the use of a combination or single-agent treatment with
gemcitabine or 5-fluorouracil
[24].
Staging of Pancreatic Cancer
CT
In most institutions, CT is the primary technique for staging of suspected
pancreatic cancer. For optimum evaluation, isotropic imaging of the abdomen
should be performed using a rapid IV injection of iodinated contrast material,
ideally at a rate of at least 4 mL/s. At least two contrast-enhanced
acquisitions, in the late arterial and venous phases, are useful. Depending on
the rate of injection and the speed of the CT scanner, the late arterial phase
occurs between 35 and 50 seconds after commencement of injection, and the
venous phase occurs between 65 and 80 seconds. Neutral enteral contrast
material such as water or 0.1% barium sulfate suspension (VoLumen, E-Z-EM) is
helpful because such contrast agents allow better identification of the
duodenal wall compared with positive enteral contrast material and result in
artifact-free reformations. VoLumen has been proven to distend the small bowel
better than water [25],
probably because it contains sorbitol, which reduces absorption of water in
the small bowel, and gum, which maintains the viscosity. VoLumen may be
preferable when duodenal distention is important, such as identifying and
staging periampullary tumors.
Coronal and sagittal reformations in both the arterial and venous phases
increase the sensitivity for determining local invasion
[26].
Maximum-intensity-projection images are helpful in identifying variant
vascular anatomy. Some studies have reported that curved reformations may be
helpful in staging pancreatic cancer
[13,
15]. In our practice, curved
reformations are not routinely used because of the long time required to
produce such reformations.
The additional value of PET, after highquality MDCT, in confirming or
excluding local tumor invasion is limited
[27]. Thus, PET is not used
routinely in preoperative staging of pancreatic cancer. A recent study
suggested that combined PET/CT may be cost-effective before a Whipple
procedure [28] for detecting
unsuspected distant metastases. This finding needs to be validated by
prospective multicenter trials. PET has been used for determining response to
definitive chemotherapy in patents with unresectable pancreatic cancer
[29,
30]. The usefulness of PET/CT
in assessing the response to neoadjuvant therapy (i.e., chemotherapy or
radiation therapy given before definitive surgery) is not known.
MRI
Dynamic gadolinium sequences using 3D gradient-echo (FAME [fast acquisition
with multiphase efgre {enhanced fast gradient echo}, GE Healthcare] or VIBE
[volumetric interpolated breath-hold examination, Siemens Medical Solutions])
are among the most useful MRI sequences for staging pancreatic cancer. These
sequences have better signal-to-noise ratio, allow thinner contiguous slices
(2 mm), and have more homogeneous fat saturation compared with 2D
gradient-echo sequences [31,
32]. The contrast resolution
of MRI is superior to that of CT
[33]; however, the spatial
resolution of MRI is lower than that currently available on MDCT. In addition,
isotropic CT gives highquality multiplanar images, which used to be an
advantage of MRI. In general, CT is preferred over MRI for staging pancreatic
cancer. MRI is used if there is a contraindication to CT or for problem
solving—for example, characterizing small, low-density liver lesions
seen on CT. In our experience, MRI has an important role in staging cystic
pancreatic tumors because internal septations and mural nodules, which have
prognostic value, are easier to visualize on MRI than on CT.
Endoscopic Sonography
Endoscopic sonography is useful in the diagnosis and staging of pancreatic
cancer. Fine-needle aspiration cytology under endoscopic sonography guidance
has a positive predictive value in the range of 92–97% but a negative
predictive value of only 40–50%
[34–36].
Endoscopic sonography was considered superior to nonhelical or single-detector
CT in detecting small (< 2 cm) primary pancreatic cancers
[37–39],
although this difference is not significant compared with MDCT
[40–42].
For detection of peripancreatic lymph node metastasis in pancreatic cancer,
endoscopic sonography is superior to CT. Morphologic features such as absence
of an echogenic center and a rounded rather than ovoid outline suggest
malignant invasion, even in normal-sized nodes. However, due to the limited
field of view of endoscopic sonography, CT is better at detecting paraaortic
and mesenteric nodes. In assessing vascular invasion, MDCT has a slightly
higher accuracy (83–89%) compared with endoscopic sonography
(68–76%) [41,
42]. However, endoscopic
sonography may better detect portal vein invasion, whereas CT may be better at
discerning superior mesenteric vein invasion
[43]. The absence of an
echogenic rim of venous wall over at least 5 mm, irregular tumor–vessel
interface, vessel encasement, or occlusion indicate invasion on endoscopic
sonography [40].
Endoscopic sonography allows identification and, if necessary, biopsy, of
some left hepatic lobe masses. Examination of the entire right lobe of the
liver is not possible with endoscopic sonography. CT is superior to endoscopic
sonography in assessing for both liver and omental metastases. Overall, CT and
endoscopic sonography are complementary in staging pancreatic cancer, although
both techniques may fail to identify small peritoneal metastases.
CT Findings Suggesting a Tumor Is Amenable to Vascular Reconstruction
A tumor in the cranial aspect of the head of the pancreas with
noncircumferential apposition to the portal venous confluence is usually
resectable with venous reconstruction (Fig.
4A,
4B). Noncircumferential
invasion of the superior mesenteric vein, proximal (toward the liver) to its
jejunal branches, usually indicates resectability with vein reconstruction.
Coronal and sagittal reformations are superior to axial images in determining
the vertical distance of venous involvement
(Fig. 5).
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Fig. 4A —58-year-old man with pancreatic cancer. Noncircumferential
distal superior mesenteric vein involvement is potentially resectable with
vein reconstruction. Coronal CT reformation images show invasion of proximal
portal vein (straight arrow, A) by tumor in superior head of
pancreas (arrowhead, A). Superior mesenteric vein was not
involved at level of its most distal jejunal tributary (arrow,
B). Hepatic artery (arrowhead, B), superior mesenteric
artery (dashed arrow, A), and splenic vein (curved
arrow, A) were clear of tumor. Whipple procedure with portal vein
reconstruction was performed.
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Fig. 4B —58-year-old man with pancreatic cancer. Noncircumferential
distal superior mesenteric vein involvement is potentially resectable with
vein reconstruction. Coronal CT reformation images show invasion of proximal
portal vein (straight arrow, A) by tumor in superior head of
pancreas (arrowhead, A). Superior mesenteric vein was not
involved at level of its most distal jejunal tributary (arrow,
B). Hepatic artery (arrowhead, B), superior mesenteric
artery (dashed arrow, A), and splenic vein (curved
arrow, A) were clear of tumor. Whipple procedure with portal vein
reconstruction was performed.
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Fig. 5 —83-year-old man with resectable pancreatic cancer. This case
shows value of coronal reformation in determining length of venous invasion.
Coronal reformation image shows that tumor abuts portal confluence over 1-cm
segment (double arrow). Vertical length of involvement was easier to
determine on coronal reformation images than on axial images (not shown).
Superior mesenteric vein was involved above insertion of first jejunal branch
(black arrow). Note anomalous venous anatomy with inferior mesenteric
vein (white arrow) joining superior mesenteric vein and biliary
(arrowhead) and pancreatic stents. Whipple procedure with vein
reconstruction was performed.
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Follow-up CT may be used to assess response to neoadjuvant
chemoradiotherapy when baseline CT shows the tumor abutting (< 180° of
circumferential contact) a short segment, typically less than 2 cm, of the
superior mesenteric or hepatic artery. CT scans are usually obtained at 4- to
6-week intervals. The principal evidence of potential resectability is the
disappearance of soft tissue abutting the arteries. Persistent periarterial
stranding does not preclude surgery because this finding may be the result of
radiation therapy [44].
CT Findings Suggesting a Tumor Is Not Amenable to Vascular Reconstruction
Circumferential involvement of a superior mesenteric vein–portal vein
segment more than 2 cm long, thrombus in the vein, or invasion of the
transverse mesocolon indicate unresectability, and vein reconstruction is not
usually attempted in such cases (Fig.
6). Circumferential involvement of a short segment, typically less
than 2 cm, of the superior mesenteric vein close to the portal confluence is
considered borderline resectable. The main concern for operating on these
patients is that the tumor will be closely applied to the retroperitoneal
margin. However, some patients with this finding on baseline CT may be
considered for radical resection if they have good imaging results and tumor
marker response to neoadjuvant therapy.
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Fig. 6 —58-year-old man with unresectable pancreatic cancer. Coronal
slab maximum-intensity-projection image shows cancer arising in head of
pancreas (arrowhead) encircling and constricting portal vein (P).
Even though length of involvement (double arrow) was short, surgery
was not contemplated in view of likelihood of positive margins. Advanced
venous invasion is usually not resectable for cure.
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Fig. 7 —65-year-old man with unresectable pancreatic cancer.
Inferiorly positioned pancreatic head and uncinate process cancers are usually
unresectable if they locally invade superior mesenteric vein or transverse
mesocolon. Axial CT image shows small inferior pancreatic head–uncinate
process tumor (solid black arrow) applied over 90° arc to
superior mesenteric vein (black arrowhead). Note jejunal branch
(dashed arrow) entering superior mesenteric vein at this level.
Despite CT findings, surgery was attempted, but adequate vascular control of
superior mesenteric vein could not be performed safely. Palliative surgery was
performed. In addition, transverse mesocolon was invaded. This finding was not
called preoperatively, but, in retrospect, there was wispiness of mesocolic
fat (white arrow). Note proximity of fine veins (white
arrowheads) in mesocolon.
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Tumors in the uncinate process are generally too low to resect if the
superior mesenteric vein is also involved
[45]
(Fig. 7). Invasion of the
transverse mesocolon is difficult to appreciate on CT, and coronal or sagittal
reformations are helpful (Figs.
7 and
8). Such invasion precludes
curative surgery because adequate control of the venous tributaries making up
the superior mesenteric vein is virtually impossible in this area.
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Fig. 8 —72-year-old man with unresectable pancreatic cancer. Invasion
of transverse mesocolon signals unresectability. Coronal reformation image
shows barely visible tumor abutting superior mesenteric vein over 1.5-cm
segment (double arrow). This finding per se was not considered
contraindication to pancreaticoduodenectomy. However, there was soft tissue in
transverse mesocolon (arrowhead), which was suspected to be invasive
cancer and proven on subsequent diagnostic laparoscopy. Patient did not have
curative resection. Tumor is closely abutting and probably invades third part
of duodenum (white arrow). Duodenal invasion does not preclude
pancreaticoduodenectomy because almost all of duodenum is removed at
surgery.
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Celiac, hepatic, or superior mesenteric arterial occlusion and
circumferential invasion remain contraindications to curative surgery.
Invasion of the gastroduodenal artery per se is not a contraindication to
surgery because this vessel is ligated at its origin from the common hepatic
artery and resected during pancreaticoduodenectomy (Fig.
9A,
9B). Systemic metastatic
disease to the liver, bone marrow, lung, or peritoneal surface is a
contraindication to resection.
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Fig. 9A —69-year-old woman with pancreatic cancer. Invasion or
occlusion of gastroduodenal artery is not contraindication to surgery. Axial
CT image shows constriction of gastroduodenal artery (white
arrowhead) by tumor (white arrow). Superior mesenteric vein
(black arrow) was free of tumor. Note common bile duct stent
(black arrowhead).
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Fig. 9B —69-year-old woman with pancreatic cancer. Invasion or
occlusion of gastroduodenal artery is not contraindication to surgery.
Endoscopic color Doppler sonogram (reproduced here in gray-scale) obtained
before common bile duct (CBD) stent insertion showed dilated CBD and encased
but patent gastroduodenal artery (GDA). Common hepatic artery (not shown) was
uninvolved by tumor. Echogenic fat (arrowhead) was seen between tumor
(TU) and superior mesenteric vein (SMV), indicating this vessel was free of
tumor.
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Variant Vascular Anatomy
Variant anatomy of arteries and veins is important in considering
resectability. Venous anatomic variants that may make vein reconstruction
difficult or impossible include multiple jejunal branches that insert high on
the superior mesenteric vein near the portal vein confluence. Arterial
anatomic variants that may make resection impossible include a low takeoff of
the common hepatic artery from the celiac axis with an aberrant course
inferior in relation to the portal vein (Fig.
10A,
10B) or a completely replaced
hepatic artery from the superior mesenteric artery coursing through the
retroperitoneal soft-tissue margin. In this respect it is important to
differentiate a replaced hepatic artery from an accessory artery. A replaced
artery has an anomalous origin and supplies all or most of the arterial flow
to a liver lobe. An accessory artery also has an anomalous origin but supplies
a hepatic lobe that also receives substantial arterial input from the common
hepatic artery. This determination is usually easily possible on a highquality
arterial phase CT scan.
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Fig. 10A —76-year-old woman with small tumor in head of pancreas.
Variant anatomy makes otherwise resectable cancer unresectable. Axial
(A) and coronal (B) reformation images of small tumor (black
arrows) in head of pancreas show that cancer was unresectable for cure
because common hepatic artery (black arrowheads) had very low course,
inferior in relation to portal vein (white arrow, B) and was
encased by tumor. Note biliary stent (white arrowheads).
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Fig. 10B —76-year-old woman with small tumor in head of pancreas.
Variant anatomy makes otherwise resectable cancer unresectable. Axial
(A) and coronal (B) reformation images of small tumor (black
arrows) in head of pancreas show that cancer was unresectable for cure
because common hepatic artery (black arrowheads) had very low course,
inferior in relation to portal vein (white arrow, B) and was
encased by tumor. Note biliary stent (white arrowheads).
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Fig. 11A —59-year-old man with pancreatic cancer. Variant anatomy may
make an otherwise unresectable cancer potentially resectable. A is most
superior and C is most inferior of these images. Axial CT image shows
mass arising from neck of pancreas (solid arrow) and invading distal
celiac (arrowhead) and splenic (dashed arrow) arteries.
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Fig. 11B —59-year-old man with pancreatic cancer. Variant anatomy may
make an otherwise unresectable cancer potentially resectable. A is most
superior and C is most inferior of these images. Axial CT image shows
hepatic artery (white arrow) branching almost immediately from celiac
trunk and not involved by tumor (black arrow).
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Fig. 11C —59-year-old man with pancreatic cancer. Variant anatomy may
make an otherwise unresectable cancer potentially resectable. A is most
superior and C is most inferior of these images. Axial CT image shows
replaced right hepatic artery (arrowhead) from superior mesenteric
artery (dashed arrow) also clear of tumor. Because hepatic arterial
supply was spared despite celiac artery involvement, curative resection was
attempted but abandoned because of unexpected peritoneal metastases.
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On the other hand, variant anatomy may make resection more likely. Such
anatomic variants include the hepatic artery arising separately from the aorta
with the celiac artery only supplying splenic and gastroduodenal arteries
(Fig. 11A,
11B,
11C) or accessory right and
left hepatic arteries arising from the superior mesenteric and left gastric
arteries, respectively. Accessory hepatic arteries may be sacrificed during
resection if there is adequate collateral flow to the liver.
Conclusions
As surgical techniques for the treatment of pancreatic head cancer evolve,
the criteria used in preoperative determination of resectability also need to
be revised. Noncircumferential involvement of the superior mesenteric vein
downstream (toward the liver) from its jejunal branches is no longer
considered unresectable for cure. Multiphasic isotropic CT of the abdomen and
use of reformations help in determining the exact site and extent of venous
invasion. The radiologist needs to identify variant vascular anatomy that may
increase or decrease the chances of successful surgical resection.
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Abstract
Introduction
