DOI:10.2214/AJR.04.1374
AJR 2007; 189:W13-W19
© American Roentgen Ray Society
CT Angiography for Delineation of Celiac and Superior Mesenteric Artery Variants in Patients Undergoing Hepatobiliary and Pancreatic Surgery
Corinne B. Winston1,
Nancy A. Lee2,
William R. Jarnagin3,
Jerrold Teitcher1,
Ronald P. DeMatteo3,
Yuman Fong3 and
Leslie H. Blumgart3
1 Department of Radiology, Memorial Sloan-Kettering Cancer Center, 160 E 53rd
St., 8th Fl., New York, NY 10022.
2 Department of Radiology, Thomas Jefferson University Hospital, Philadelphia,
PA 19107.
3 Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York,
NY
Received August 31, 2004;
accepted after revision September 13, 2005.
Address correspondence to C. B. Winston.
WEB
This is a Web exclusive article.
Abstract
OBJECTIVE. The objective of our study was to determine the frequency
of different arterial variants identified at abdominal CT angiography (CTA)
performed before pancreatic and hepatobiliary surgery.
CONCLUSION. Variant hepatic and celiac arterial anatomy is common.
CTA can be used to identify common and uncommon variants that are important
for the surgical management of patients with pancreatic and hepatobiliary
neoplasms.
Keywords: arteriography • CT angiography • hepatobiliary imaging • pancreas • superior mesenteric artery
Introduction
MDCT allows the rapid acquisition of high-resolution images through the
hepatic and mesenteric arteries during the phase of maximal contrast
enhancement. The role of CT angiography (CTA) in determining tumor
resectability in patients with pancreatic and hepatobiliary malignancy has
been described [1,
2]. An important additional
role of CTA for evaluating patients with pancreatic and hepatobiliary
malignancy is the delineation of variant arterial anatomy. Variant arterial
anatomy is common, occurring in more than half of the population
[3]. Visualization of the
surgical field can often be limited in patients with pancreatic and
hepatobiliary malignancy, especially if there has been prior surgery, if there
is local inflammation such as that accompanying a biliary stent, or if the
patient is obese. Preoperative knowledge of variant anatomy can assist in
selection of treatment options and in surgical planning, facilitate surgical
dissection, and help avoid iatrogenic injury. The purpose of this study was to
determine the frequency of different arterial variants identified at abdominal
CTA performed in a large series of patients before major pancreatic or
hepatobiliary surgery.
Materials and Methods
Patient Population
A CTA database from August 2001 to February 2003 included 394 consecutive
CT angiograms in 371 patients, all of whom were under consideration for
surgical resection for a suspected pancreatic or hepatobiliary neoplasm. Each
patient was included only once in the study. CTA was performed to determine
tumor resectability and to aid surgical planning. Our institutional review
board approved this retrospective report review, and patient informed consent
was not required.
CTA
All CT examinations were performed on a 4-MDCT scanner (LightSpeed QX/i, GE
Healthcare). Water was administered to all patients as a nonopaque oral
contrast agent. CTA was performed after the IV administration of 140 mL of
nonionic contrast material (iohexol [Omnipaque, Nycomed]) with a power
injector through an 18-gauge catheter at a rate of 4 mL/s when possible
(n = 325 patients, 88%). If limited venous access precluded this
injection rate, a slower injection rate was used. A 10-mL timing bolus was
used to determine peak enhancement of the upper abdominal aorta; 1.25-mm
images were acquired with a 1-mm overlap (table speed, 7.5 mm per 0.8-second
rotation; pitch, HS) at the point of maximal arterial enhancement.
For patients with suspected hypervascular lesions, including hepatocellular
carcinoma and neuroendocrine carcinoma, CTA was performed as part of a
triphasic examination with 2.5-mm slices acquired at a 1.25-mm interval in the
early arterial phase and 5-mm slices obtained during the same breath-hold in
the late arterial phase. For patients with suspected pancreatic lesions,
3.75-mm-slice images acquired with a 2-mm overlap were obtained in the late
arterial phase (table speed, 11.25 mm per 0.8-second rotation; pitch, HQ) in
the same breath-hold as the angiographic images; 5-mm-slice images acquired at
a 2.5-mm interval through the abdomen were obtained at 70 seconds after the
start of the injection (table speed, 11.25 mm per 0.8-second rotation; pitch,
HQ).
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Fig. 1 —Classic hepatic arterial anatomy in 58-year-old man with
metastatic colon cancer to liver. Volume-rendered 3D image created from axial
contrast-enhanced CT data reveals classic branching arterial anatomy. Celiac
axis (short solid arrow) trifurcates into splenic artery, common
hepatic artery (long solid arrow), and left gastric artery. Common
hepatic artery gives rise to gastroduodenal artery (open arrowhead)
and proper hepatic artery (solid arrowhead). Right hepatic artery
(long open arrow) and left hepatic artery (short open arrow)
originate from proper hepatic artery.
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Fig. 2A —Replaced right hepatic artery in 69-year-old woman.
Volume-rendered 3D image created from axial contrast-enhanced CT data reveals
right hepatic artery (small open arrow) originating from superior
mesenteric artery (SMA) (large solid arrow). Right hepatic artery
courses posterior to stent (large open arrow) located within common
bile duct. Note left hepatic artery (small solid arrow) originating
from left gastric artery.
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Fig. 2B —Replaced right hepatic artery in 69-year-old woman. Thin-slab
maximum-intensity-projection axial image reveals right hepatic artery
(small solid arrow) originating from SMA (small open arrow).
Right hepatic artery courses through portacaval space, between portal vein
(large open arrow) and inferior vena cava (large solid
arrow).
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Data Collection
During routine interpretation of the CTA examinations, the attending
radiologist prospectively assessed for the presence of variant celiac axis and
hepatic arterial anatomy. All radiologists interpreting these examinations
were attending oncologic imagers experienced in using CT for preoperative
planning. The official reports of the CTA examinations were reviewed to
identify whether variant hepatic arterial or variant celiac axis anatomy was
present. The reports were also reviewed to determine if a study was considered
of limited or if it was of diagnostic quality. For patients in whom a variant
was identified, the specific type of variant was recorded according to
Michels' criteria [3]. For
those patients in whom no mention of the arterial anatomy was reported
(n = 24), one attending radiologist retrospectively reviewed the
scans to assess the vascular anatomy. All studies were evaluated in the cine
mode on PACS. Three-dimensional reconstructions were created by the attending
radiologist at the time of interpretation of the CT scan based on the
discretion of the radiologist interpreting that examination.
Results
All studies were considered of diagnostic quality, although the examination
was considered somewhat limited due to respiratory motion in one patient. One
hundred eighty-eight (51%) of the 371 patients had classic arterial anatomy
identified at CTA (Fig. 1). One
hundred sixty-two (44%) patients had a single arterial variant identified, and
21 (6%) patients had more than one arterial variant seen.
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Fig. 3A —Replaced left hepatic artery originating from left gastric
artery in 73-year-old woman. Volume-rendered 3D image created from axial
contrast-enhanced CT data reveals replaced left hepatic artery (small
arrow) originating from left gastric artery (arrowhead). Common
hepatic artery (large arrow) arises from celiac axis.
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Fig. 3B —Replaced left hepatic artery originating from left gastric
artery in 73-year-old woman. Thin-slab axial maximum-intensity-projection
image reveals replaced left hepatic artery (arrow) coursing through
fissure for ligamentum venosum to perfuse left hepatic lobe.
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The most common variant identified was a replaced right hepatic artery
originating from the superior mesenteric artery (SMA), which was seen in 54
(15%) patients (Figs. 2A and
2B). The second most common
variant was a replaced left hepatic artery originating from the left gastric
artery, seen in 30 (8%) patients (Figs.
3A and
3B). Variations in the origin
of the common hepatic artery were seen in 12 (3%) patients. In six (2%)
patients, the common hepatic artery originated from the SMA
(Fig. 4A), and in six (2%)
patients, the common hepatic artery originated from the abdominal aorta
(Fig. 4B). A "double
hepatic artery," as described by Fasel et al.
[4] and Covey et al.
[5], refers to one or both
hepatic arteries originating from the celiac axis or the aorta. This was seen
in 15 (4%) of the patients in our study population. The right hepatic artery
originated from the celiac axis in 13 (4%) patients (Figs.
5A and
5B) and from the aorta in one
(< 1%) patient (Fig. 5C).
The left hepatic artery originated from the celiac axis in one (< 1%)
patient (Fig. 5D). Accessory
hepatic arteries were identified in 16 (4%) patients. The frequencies of the
different types of arterial variants identified are reported in
Table 1.
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Fig. 4A —Variation in origin of common hepatic artery. Common hepatic
artery originates from superior mesenteric artery (SMA) in 62-year-old man.
Volume-rendered 3D image created from axial contrast-enhanced CT data reveals
common hepatic artery (small open arrow) originates from SMA
(large solid arrow). Gastroduodenal artery (large open
arrow) originates from common hepatic artery. Note accessory left hepatic
artery (small solid arrow) originating from left gastric artery.
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Fig. 4B —Variation in origin of common hepatic artery. Common hepatic
artery originates directly from aorta in 68-year-old woman who also has
trifurcation of common hepatic artery. Volume-rendered 3D image created from
axial contrast-enhanced CT data reveals common hepatic artery (small open
arrow) originates directly from abdominal aorta. Common hepatic artery
trifurcates into right hepatic artery (large solid arrow), left
hepatic artery (small solid arrow), and gastroduodenal artery
(large open arrow).
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Fig. 5A —Double hepatic artery. Double hepatic artery in 62-year-old
woman. Right hepatic artery originates from celiac axis. Steep oblique
volume-rendered 3D image created from axial contrast-enhanced CT data image
viewed from below reveals right hepatic artery (thick arrow)
originates from celiac axis (arrowhead). Right hepatic artery extends
posterior to stent (thin arrow) that is located within common bile
duct.
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Fig. 5B —Double hepatic artery. Double hepatic artery in 62-year-old
woman. Right hepatic artery originates from celiac axis. Volume-rendered 3D
image created from axial contrast-enhanced CT data reveals right hepatic
artery (small arrow) originates from celiac axis (arrowhead)
proximal to origin of common hepatic artery (large arrow).
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Fig. 5C —Double hepatic artery. Double hepatic artery in 71-year-old
woman. Right hepatic artery originates from aorta. Thick-slab
maximum-intensity-projection image obtained from axial contrast-enhanced CT
data reveals right hepatic artery (long arrow) originates directly
from abdominal aorta, parallel to origin of superior mesenteric artery (SMA)
(short arrow). Arrowhead indicates celiac axis.
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Fig. 5D —Double hepatic artery. Double hepatic artery in 77-year-old
woman. Left hepatic artery originates from celiac axis. Volume-rendered 3D
image created from axial contrast-enhanced CT data reveals origin (small
open arrow) of left hepatic artery (large open arrow) directly
from celiac axis. Common hepatic artery (large solid arrow)
originates from celiac axis. Origin of SMA (small solid arrow) is
obscured by splenic artery.
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Discussion
CTA is often performed in patients with pancreatic and hepatobiliary
neoplasms to determine tumor resectability. In addition to evaluating for
vascular involvement by tumor, it is also important for the radiologist to
assess for the presence of variant arterial anatomy. Variant hepatic and
celiac arterial anatomy have been reported in 55% of patients on the basis of
initial cadaveric dissections by Michels
[3]. In 1969, Redman and Reuter
[6] reported "most of the
variations" seen in roughly 50% of the population "have little
surgical significance." Since that time, however, there are new surgical
and interventional treatment options for patients with resectable and
unresectable disease. The presence of different arterial variants may alter
patient management. Therefore, having an awareness of the CTA appearance of
these variants and an appreciation of their clinical significance is of great
importance.
MDCT enables the rapid acquisition of thin-slice high-resolution images of
the abdominal arteries during the phase of maximal contrast enhancement. The
volumetric acquisition of data allows 3D reconstructions to be created,
providing the surgeon with a 3D model of the patient's arterial anatomy
[7]. A major benefit of CTA
over conventional arteriography is that the relationship of arteries to the
adjacent organs and the biliary tree is displayed so that the course of an
aberrant vessel is clearly delineated. This can be of great value because
direct visualization of the surgical field is often limited in patients with
pancreatic and hepatobiliary malignancy, especially if there has been prior
surgery, if there is local inflammation such as that accompanying a biliary
stent, or if the patient is obese. Preoperative knowledge of variant arterial
anatomy may obviate extensive dissection to identify the vessels and may avert
vascular damage. The mortality rate associated with liver resection ranges
from 3% to 5%, with hemorrhage a leading cause of perioperative mortality
[8,
9].
MDCT angiography has a reported accuracy of 97–98% compared with
conventional angiography for detecting arterial variants
[2,
10]. The role of CTA in the
preoperative evaluation of patients with hepatic
[2,
11] and pancreatic
[1] neoplasms has been
described. However, for those studies, the authors evaluated a relatively
small number of patients. To the best of our knowledge, this report is the
first describing the ability of CTA to delineate the broad range of clinically
significant different arterial variants encountered in a large surgical
population.
We identified classical arterial anatomy in 51% of the patients who
underwent CTA (Fig. 1). In
classic visceral anatomy, the celiac trunk originates from the abdominal aorta
and gives origin to the left gastric artery, the splenic artery, and the
common hepatic artery [12].
The common hepatic artery extends anteriorly and bifurcates into the
gastroduodenal artery and the proper hepatic artery. The proper hepatic artery
extends cephalad and runs to the left side of the common hepatic duct to
bifurcate into the right and left hepatic arteries, usually just below the
bifurcation of the common hepatic duct
[13].
Variant arterial anatomy was seen in 49% of the patients who underwent CTA.
This frequency is similar to the results of the cadaveric study by Michels
[3]. The most common variant
seen at CTA was a replaced right hepatic artery originating from the SMA,
identified in 15% of the patients. Identification of a replaced right hepatic
artery is critical when performing pancreaticoduodenectomy and for porta
hepatis dissection during hepatic resection. Whereas the right hepatic artery
usually courses anterior to the right portal vein, the replaced right hepatic
artery originates from the SMA, courses posterior to the main portal vein in
the portacaval space, and classically ascends posterolateral to the common
bile duct [13] (Figs.
2A and
2B). Palpation for the presence
of the artery can be unreliable when there is portal inflammation, enlarged
portal lymph nodes, or an existing biliary stent.
In a patient with cancer in the pancreatic head or uncinate process, a
replaced right hepatic artery may be involved by tumor, precluding the patient
from surgical resection. If the right hepatic artery is not involved,
particular care needs to be taken in this region so as not to inadvertently
injure such an artery during dissection. This is especially important because
patients with pancreatic head tumors are often jaundiced. Unlike the
nonjaundiced patient, in whom the portal blood flow can sustain viability of
the liver, the liver in the jaundiced patient is prone to hepatic necrosis if
the arterial blood flow is compromised
[14]. Therefore, the surgeon
may choose biliary drainage for the jaundiced patient with a replaced right
hepatic artery to relieve the jaundice before pancreaticoduodenectomy.
The second most common arterial variant identified at CTA was a replaced
left hepatic artery originating from the left gastric artery, seen in 8% of
the patients. This frequency is consistent with the findings reported by
Michels [3]. The replaced left
hepatic artery originates off the left gastric artery and courses to the right
through the lesser sac, through the fissure for the ligamentum venosum, and
into the umbilical fissure to perfuse the left hepatic lobe. Before left
hepatectomy is performed, this vessel must be identified and ligated.
Preoperative knowledge of this variant facilitates portal dissection because
the major arterial branch to the left liver does not need to be found in the
porta hepatis.
The "double hepatic artery" as described by Fasel et al.
[4] refers to a right or left
hepatic artery that originates from the celiac axis or aorta. We identified a
double hepatic artery in 4% of our patients, a result similar to that reported
by Covey et al. [5] (3.7%) as
seen at digital subtraction angiography. To the best of our knowledge, this
latter type of arterial variant has not been described in the CTA literature.
An anomalous location of the right hepatic artery that originates from the
celiac axis or aorta and extends posterior to the bile duct may result in
iatrogenic injury to such a vessel if that vessel is not seen by the
surgeon.
Accessory left and right hepatic arteries were identified in 4% and 1%,
respectively, of the patients in our study. An accessory left hepatic artery
usually originates from the left gastric artery and follows the same course
through the lesser sac as does the replaced left hepatic artery. This
accessory artery provides an additional source of arterial blood to the left
hepatic lobe (it is seen in addition to the "classic" left hepatic
artery) and may be sacrificed without compromising the arterial supply to the
left hepatic lobe. An accessory left hepatic artery needs to be occluded
separately when controlling the inflow to the left hepatic lobe because this
artery will not be occluded when the blood supply in the porta hepatis is
occluded. The course of an accessory right hepatic artery is similar to that
of a replaced right hepatic artery and is present in addition to the classic
right hepatic artery. As with the accessory left hepatic artery, the accessory
right hepatic artery provides additional blood supply to the respective
hepatic lobe and may be sacrificed without compromising the arterial supply to
the right lobe. Distinction between an accessory and a replaced artery is
therefore important. An awareness of an accessory right hepatic artery is also
important so that inadvertent injury to this artery does not result in
hemorrhage.
The common hepatic artery originated from the SMA in 2% as seen at CTA.
When pancreaticoduodenectomy is performed, it is important that the common
hepatic artery be preserved so the artery must be dissected to its origin from
the SMA. The anomalous course of the common hepatic artery is in proximity to
the pancreatic head and may be involved by tumor, making resection impossible.
Even if this variant vessel is not involved, if not recognized, if may be
inadvertently injured during resection. This is particularly problematic in
the jaundiced patient.
In recent years, clinical data have shown hepatic artery infusional
chemotherapy to have efficacy as adjuvant to resection in controlling hepatic
disease [15]. The goal of
intraarterial chemotherapy is to provide uniform perfusion of the
chemotherapeutic agent throughout the liver. The catheter is surgically placed
via an arteriotomy in the gastroduodenal artery with the catheter tip inserted
up to—but not beyond—the junction of the gastroduodenal artery and
the common hepatic artery. Variant arterial anatomy does not necessarily
preclude a patient from placement of a pump. Recognition of a replaced or an
accessory artery is important so that the vessel can be ligated at the time of
catheter placement to allow uniform perfusion of the hepatic parenchyma. In
our institution, CTA has replaced direct catheter angiography in the
preoperative evaluation of patients before intraarterial pump
chemotherapy.
We assessed the main arteries surrounding the pancreatic head because these
are the vessels that are clinically relevant for pancreatic surgery.
Variations in the pancreaticoduodenal arcade, gastric arteries, and
gastroepiploic arteries are not usually significant for pancreatic and
hepatobiliary surgery. Variations of the portosplenic confluence are quite
rare and, therefore, not discussed in this article. Variations in the
branching of the intrahepatic portal venous system and the hepatic veins are
encountered more frequently. We are presently performing a large-scale
prospective study assessing the frequency of variant portal venous and hepatic
venous anatomy as seen at CT with surgical correlation.
A limitation of this study is that we do not have surgical or conventional
arteriographic confirmation of the accuracy of the CTA findings. However, the
overall prevalence of arterial variants in our study is concordant with that
described in the anatomy and conventional angiography literature
[3,
5]. A direct comparison of CTA
findings with conventional angiography findings is not be possible at our
institution because CTA has replaced invasive catheter angiography for
preoperative staging and for preoperative vascular mapping for placement of
intraarterial pump chemotherapy. We did not intend to assess the sensitivity
or specificity of CTA in detecting arterial variants, which have already been
reported, but rather to show that the broad range of common and uncommon
clinically significant arterial variants are visible using CTA. Although there
have been previous studies describing arterial variants, to the best of our
knowledge, those studies did not have large patient populations. Some of the
more uncommon variants that have surgical significance have not been described
at CTA. In addition, the importance of recognizing arterial variants in
preoperative planning for the resection of hepatic and pancreatic neoplasms
has not been systematically addressed. Most articles that focus on arterial
variants describe the clinical relevance of arterial variants in patients
undergoing hepatic transplantation.
Because CTA is becoming more widely used in the evaluation of patients with
hepatic and pancreatic neoplasms, recognition of both the CT appearance and
the clinical significance of these variants is essential for patient
management. The surgical relevance and clinical utility reported in this
article are based on a lifetime of experiences of the surgical coauthors of
this study, all of whom are experienced hepatobiliary surgeons. Whereas,
classically, interventional radiologists have been the radiologists who were
familiar with the conventional angiographic appearances of the liver and
pancreas, now CT radiologists must gain an awareness of the broad range of
arterial variants visible at CTA.
The images in this study were all obtained on a 4-MDCT unit and depict the
anatomy and variants of the major arteries. It is likely that use of 16- or
64-MDCT scanners would enable visualization of the smaller arteries. However,
it is the major arteries that are clinically significant. Not all institutions
(including academic institutions) have 16-MDCT scanners. Some arterial
variants can even be identified on standard 5-mm slices, such as a replaced
right hepatic artery coursing through the portacaval space. It is important to
recognize that valuable information can be obtained from a 4-MDCT scanner.
We did not describe the clinical significance of arterial variants in
patients undergoing liver transplantation because that is a separate topic and
has been discussed extensively by other authors.
In conclusion, variant celiac and hepatic arterial anatomy as seen at CTA
is common, occurring in 49% of our patient population. CTA can be used to
identify both the common and rare arterial variants. The role of CT in
patients with pancreatic and hepatobiliary malignancies has broadened from one
of staging to include vascular mapping, which is essential for surgical
planning. Preoperative knowledge of variant anatomy can assist in the
selection of treatment options, facilitate surgical dissection, and help avoid
iatrogenic injury.
Acknowledgments
We would like to express our tremendous gratitude to Lachlan Smith for much
valued computer expertise and assistance in database management. His efforts
are greatly appreciated.
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Abstract
Introduction
