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Original Research |
1 Department of Radiodiagnosis, Postgraduate Institute of Medical Education and
Research, PGIMER, Sector 12, Chandigarh, India 160012.
2 Department of General Surgery, Postgraduate Institute of Medical Education and
Research, PGIMER, Chandigarh, India 160012.
3 Department of Histopathology, Postgraduate Institute of Medical Education and
Research, PGIMER, Chandigarh, India 160012.
Received August 26, 2004;
accepted after revision February 7, 2005.
Address correspondence to N. Kalra
(navkal2004{at}yahoo.com).
Abstract
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SUBJECTS AND METHODS. Twenty-seven consecutive patients with suspected gallbladder carcinoma on clinical examination and routine sonography were prospectively analyzed with dual-phase MDCT. Of these patients, only 20 who underwent a laparotomy for extended cholecystectomy or a palliative surgery were included in the study. Three-dimensional volume-rendered reconstruction was used for evaluation of the vascular invasion and anatomy. The staging and resectability as determined on CT were compared with preoperative findings.
RESULTS. On the basis of the CT findings, eight tumors were resectable and 12 were unresectable. On surgery, 11 tumors were found to be resectable and the remaining were unresectable. Overstaging by CT occurred in three patients due to overassessment of duodenal infiltration. CT had a sensitivity of 72.7%, a specificity of 100%, and an accuracy of 85% for determining resectability of gallbladder carcinoma. For the diagnosis of hepatic and vascular invasion by the tumor, there was 100% correlation between CT and surgery. Vascular variations were found in six of the 11 patients who underwent radical cholecystectomy.
CONCLUSION. Dual-phase MDCT with 3D reconstruction is a comprehensive imaging technique for staging gallbladder carcinoma and determining the vascular road map before surgery.
Keywords: cancer • gallbladder • MDCT
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Most gallbladder carcinomas present when the disease is at an advanced stage. As a result, the prognosis for gallbladder carcinoma remains poor, with the curative resection rate ranging only between 10-30% [4-6]. As surgery is the only definitive cure, it is important to diagnose this disease at an early stage and also determine its extent accurately.
Advanced gallbladder carcinoma is managed with curative resection, which includes resection of segments IVb and V or even an extended right hepatectomy [7]. For confined gallbladder carcinoma, some surgeons recommend simple cholecystectomy and others consider extended cholecystectomy (wedge resection of the gallbladder fossa including a 3- to 5-cm margin of a normal liver and a cystic, pericholedochal, gastrohepatic, pancreaticoduodenal, and paraaortic lymphadenectomy) to be a curative resection [8-10]. The 5-year survival rate after a curative resection is more than 50% [11-13] compared with only 5% after a noncurative resection [12].
To achieve a high resection rate for gallbladder carcinoma, a precise preoperative evaluation of tumor extension is essential [14]. The development of a preoperative road map of hepatic arterial and venous anatomy further helps the surgeon plan the surgical strategy before oncologic hepatic surgery [15].
MDCT with 3D reconstruction has been used for preoperative evaluation of hepatic and pancreatic neoplasms [16-18]. Yoshimitsu et al. [19] first described the role of MDCT in the evaluation of the local spread of gallbladder carcinoma. To our knowledge, the role of MDCT with 3D reconstruction has not been evaluated for gallbladder carcinoma. In this study, we prospectively evaluated the utility of MDCT as a comprehensive technique for assessing the resectability of gallbladder carcinoma and providing a vascular road map for preoperative surgical planning.
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CT Technique
Dual-phase MDCT was performed in all patients on an MDCT scanner
(LightSpeed QX/i Plus, GE Healthcare). The patients did not eat or drink for
4-6 hr. Water (1.5-2 L) was used as an oral contrast. Initial 10-mm
contiguous, noncontrast axial sections of the upper abdomen were obtained. One
hundred fifty milliliters of nonionic iodinated contrast (300 mg I/mL) was
then injected at a rate of 5 mL/sec through a 16-gauge IV cannula using a
pressure injector.
Scanning was performed using a pitch of 1.5:1, a scanning time of 0.5 sec/rotation, table speed of 7.5 mm/rotation, 250-300 mAs, and 120 kVp. Using a bolus-triggered technique (Smart Prepare Protocol, GE Healthcare) by placing the cursor in the aorta at L1/L2 level and setting the threshold at 50 H, hepatic artery phase images were obtained in a craniocaudal direction. Portal venous phase images were obtained in a caudocranial direction with a scan delay of 40 sec after initiation of contrast injection. Images were acquired in both phases in a single breath-hold with a slice thickness of 2.5 mm and a reconstruction interval of 1.25 mm. The rest of the abdomen and pelvis were then scanned in the axial mode by taking 10-mm-thick sections.
Image Processing
The axial images were processed on an Advantage Windows 4.0 workstation (GE
Healthcare) by one radiologist. Three-dimensional volume-rendered images were
obtained for both the hepatic arterial and portal venous phases. The average
image processing time was 30 min.
Image Analysis
The axial and volume-rendered images were prospectively evaluated on the
Advantage Windows workstation with the consensus of three radiologists. The
morphology of the tumor, vascularity, locoregional spread, and distant spread
were studied. The resectability of the tumor was also determined. The criteria
for nonresectability were as follows
[20]: involvement of main
portal vein or hepatic artery; involvement of the portal vein or hepatic
artery branches of both lobes of the liver; simultaneous involvement of the
ipsilateral hepatic artery and contralateral portal vein; simultaneous
invasion in both lobes of the liver at the level of confluence of segmental
bile ducts to form the hepatic ducts; contiguous involvement of more than two
segments each in both lobes of the liver; contiguous extensive infiltration of
the colon, duodenum, or pancreas; the presence of hepatic metastases; and the
presence of peritoneal metastases.
Regional lymph node metastasis was not a criterion for nonresectability [14]. Vascular anatomy and invasion was assessed on both axial and 3D volume-rendered images. Hepatic arterial, portal venous, and hepatic venous variations were recorded. The criterion for vascular invasion was irregularity of the vessel wall or the presence of a tumor on both sides of the vessel. Loss of fat planes between adjacent organs such as the duodenum, colon, pancreas, and bile ducts was considered a sign of infiltration of these organs by the tumor.
Surgery
All patients included in the study underwent laparotomy within 4 weeks of
the CT examination. Nine patients underwent only palliative procedures such as
hepaticojejunostomy or gastrojejunostomy. Radical cholecystectomy
(cholecystectomy with IVb and V segmentectomy) was performed in 11 patients.
Preoperative sonography was performed in all patients who underwent resection.
The surgical and CT findings were compared, with surgery used as the standard
of reference.
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Locoregional spread—Contiguous hepatic infiltration was found in 14 patients. Involvement of segments IVb and V was seen in all patients. The hepatic infiltration was less than 2 cm in five patients and more than 2 cm in nine patients.
Infiltration of the duodenum was seen in 11 patients and hepatic flexure was seen in two patients. Bile duct invasion was seen in 10 patients along with intrahepatic biliary duct dilatation.
Lymphadenopathy was seen in 10 patients. A size larger than 1 cm was used as a criterion for lymph node metastases. Two of these patients had hilar lymphadenopathy. In five patients, peripancreatic and celiac lymphadenopathy were seen. Four patients had paraaortic lymphadenopathy, including one patient who also had celiac lymphadenopathy. However, paraaortic lymph node involvement was regarded as a distant metastasis.
Vascular invasion and vascular variations—Vascular invasion was seen in four patients on both axial and volume-rendered images. This was seen in the form of left portal vein involvement, main portal vein involvement, right portal vein and right hepatic artery involvement, and right hepatic artery involvement (one patient each, respectively) (Figs. 1A and 1B).
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Distant metastases—Peritoneal deposits were seen in one patient. In another patient, distant hepatic metastases and lung metastases were seen. Four patients had paraaortic lymphadenopathy.
Resectability—Eight patients were found to be resectable and 12 patients were unresectable on MDCT. The reasons for nonresectability were duodenal infiltration in six patients, duodenal infiltration and paraaortic lymph nodes in two patients, and duodenal and colonic infiltration in one patient. Three patients had more than two reasons for being labeled as unresectable (duodenal and main portal vein involvement with peritoneal deposits, duodenal and colonic infiltration with paraaortic lymph nodes, and paraaortic lymph nodes with hepatic and lung metastases, respectively).
Surgical Findings
Of the 20 patients with gallbladder carcinoma, 11 (55%) were found to be
resectable on surgery. Table 1
shows the comparison of CT and surgical findings. There was 100% correlation
in the diagnosis of hepatic, colonic, and bile duct infiltration by the tumor.
On surgery, discordant findings were found regarding infiltration of the
duodenum, lymphadenopathy, and peritoneal metastases. Three patients were
overstaged on CT due to duodenal infiltration and had been labeled as
unresectable (Fig. 2). They
were resectable on surgery. In two of these adhesions were present but sleeve
resection could be performed. In one of them, the duodenum was normal at
surgery. Thus, the accuracy of diagnosing involvement of the duodenum on the
basis of the loss of fat planes was 85%. Cystic duct, pericholedochal, or
hilar lymph nodes (N1 level nodes) were seen at surgery in eight patients. In
six of these patients, no lymph nodes were detected on CT. CT detected only
hilar nodes in two patients. Six patients had peripancreatic, periduodenal,
periportal, celiac or superior mesenteric lymph nodes (N2 level nodes) at
surgery. CT detected lymph nodes in five of these patients. In one patient,
peripancreatic lymph nodes were not detected on CT. The resectability of the
tumors was not affected in any of these cases as regional lymph node
metastases was not a criterion for nonresectability. Paraaortic lymph nodes
were seen in all four patients who had these nodes on CT. Peritoneal
metastases were found in three patients on laparotomy. CT did not reveal two
of these, but these two patients had been labeled as unresectable on CT due to
extensive duodenal and colonic infiltration in one and the presence of
paraaortic lymphadenopathy with duodenal infiltration in the other.
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Vascular invasion was confirmed on surgery in four patients. All six hepatic arterial variations were confirmed on surgery. Of the nine patients who revealed vascular variations on CT, radical cholecystectomy was performed in six patients. Four of these had arterial variations (accessory left hepatic artery from the LGA [two patients], replaced right hepatic artery from the SMA [one patient], and accessory left and right hepatic arteries [one patient]), one had both portal venous (trifurcation) and hepatic venous variation (accessory right hepatic vein), and one had only hepatic venous variation (accessory right hepatic vein). The venous variations were confirmed on preoperative sonography.
Histopathologic Findings
All of the gallbladder tumors were adenocarcinomas except one that was a
poorly differentiated carcinoma with focal squamoid differentiation.
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Complete preoperative evaluation remains the key factor for successful surgery in all hepatobiliary malignancies, including gallbladder carcinoma. Accurate evaluation of the segmental anatomy and development of a road map of the arterial and the venous structures are essential prerequisites for planning a radical cholecystectomy. MDCT has revolutionized vascular imaging with CT angiography, giving the same information as conventional angiography noninvasively. CT angiography is now increasingly used for staging and vascular evaluation in cases of hepatic and pancreatic cancers [16-18] but its utility in gallbladder carcinoma has not been reported, to our knowledge. The present study highlights the role of dual-phase MDCT with 3D reconstruction in the determination of resectability and charting of vascular anatomy for patients with gallbladder carcinoma.
The presence of vascular invasion, infiltration of contiguous organs, and hepatic and peritoneal metastases are the primary criteria for considering gallbladder carcinoma as unresectable [20]. In the present study, MDCT proved to be a reliable technique for the evaluation of vascular involvement. Vascular invasion was detected on MDCT in four of our patients and was confirmed on surgery in all of them. The volume-rendered images provided the surgeons with 3D data sets showing the relationship of the gallbladder carcinoma to the portal vein, hepatic artery proper, and the branches of these vessels. In addition, the 3D volume-rendered reconstructions were very useful for assessing the vascular anatomy for surgical planning. Vascular variation determination preoperatively is needed to provide a vascular road map before surgery. The anatomy of the hepatic veins helps surgeons determine the plane of resection for segmentectomy. The arterial variations affect the surgical planning and the hilar dissection. In this series, as many as six (55%) of the 11 patients who had resectable gallbladder carcinomas had vascular variations on CT that were confirmed on surgery and subsequent intraoperative sonography. In one patient who had an accessory left hepatic artery from the LGA, the 3D volume-rendered images did not show this vessel because it was small. Inability to detect small-caliber vessels on volume-rendered images has been reported in previous studies [16, 22].
Loss of fat planes between the tumor and the adjacent organs on CT has been used as a criterion for diagnosing infiltration by the tumor [23]. Using this criterion in the present study, three cases of gallbladder carcinoma were overstaged on CT. In these patients, CT results suggested duodenal infiltration but surgery did not confirm it. In two patients, duodenal adhesions were seen and sleeve resection was performed. In one patient the duodenum was normal. This mismatch between CT and surgical findings limited the sensitivity to 72.7%, specificity to 100%, and accuracy to 85% for determining resectability of gallbladder carcinoma. Kumaran et al. [20] reported an accuracy of 93.3% for assessing resectability of gallbladder carcinoma by dual-phase MDCT. However, both of these studies have small sample populations and the differences in accuracy are probably not significant.
CT is known to have limitations for the detection of peritoneal metastases. MDCT has a sensitivity of 85-93% for the detection of peritoneal metastases in contrast with previously reported values of 63-79% for conventional CT [24]. Laparoscopy still remains a reliable method for the evaluation of peritoneal disease [25, 26]. In the present study, CT could not detect peritoneal deposits in two of three patients. However, this did not affect the management because the tumor was unresectable in these two patients due to the presence of extensive duodenal and colonic infiltration in one and the presence of paraaortic lymph nodes with duodenal infiltration in the other.
Gallbladder carcinoma in the neck region frequently involves the common bile duct by intraductal extension through the cystic duct or by external invasion of the hepatoduodenal ligament [11]. Involvement of the common bile duct does not preclude resection of gallbladder carcinoma. Some surgeons routinely resect the extrahepatic bile duct in cases of radical dissection for gallbladder carcinoma [27]. In the present study, common bile duct infiltration was found in 10 patients on MDCT. The same findings were subsequently found in all of these patients on laparotomy.
Lymphatic spread in gallbladder carcinoma occurs from the gallbladder fossa through the hepatoduodenal ligament to nodal stations near the head of the pancreas [28]. The first lymph nodes to be involved in gallbladder carcinoma are the cystic or the pericholedochal lymph nodes (N1). This is followed by the involvement of the celiac, superior mesenteric (N2), and paraaortic lymph nodes (M). In this series, CT did not reveal nodes in six of eight patients with N1 level nodes and one of six patients with N2 level nodes. All of the paraaortic lymph nodes were detected on CT. All of the involved lymph nodes that were not detected on CT were smaller than 1 cm in size. Low sensitivities have been reported for the detection of positive nodes on CT (36% for N1 and 47% for N2) [29]. However, involvement of N1 or N2 nodal stations is not a criterion for nonresectability of gallbladder carcinoma and extensive surgery in these cases also improves the survival rate [14].
A limitation of our study was the small study group. Successful surgery in 11 (55%) of 20 patients seems to reflect a high rate of resection in gallbladder carcinoma. Larger prospective studies are needed to determine the actual resectability rate of gallbladder carcinoma.
In conclusion, dual-phase MDCT coupled with 3D volume-rendered reconstruction is a comprehensive preoperative imaging technique for gallbladder carcinoma. It helps to determine the resectability of gallbladder carcinoma and provides a vascular road map for radical cholecystectomy.
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