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DOI:10.2214/AJR.07.2348
AJR 2008; 190:74-80
© American Roentgen Ray Society

Original Research

Accuracy of Preoperative T-Staging of Gallbladder Carcinoma Using MDCT

Soo Jin Kim1, Jeong Min Lee1, Jae Young Lee1, Jin Young Choi1,2, Se Hyung Kim1, Joon Koo Han1 and Byung Ihn Choi1

1 Department of Radiology and Institute of Radiation Medicine, Seoul National University Hospital, 28, Yeongeon-dong, Jongno-gu, Seoul 110-744, Korea.
2 Present address: Department of Diagnostic Radiology, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, Korea.

Received March 31, 2007; accepted after revision July 30, 2007.

 
Address correspondence to J. M. Lee (leejm{at}radcom.snu.ac.kr).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The objective of our study was to evaluate the performance of MDCT in the preoperative T-staging of gallbladder cancer and to determine whether adding multiplanar reconstruction (MPR) images to axial images can improve the accuracy of MDCT for the T-staging of gallbladder cancer.

MATERIALS AND METHODS. Two abdominal radiologists retrospectively reviewed by consensus axial images of portal phase MDCT scans of 118 patients who had pathologically confirmed gallbladder cancers; they then reviewed the axial and MPR images from 53 of the 118 patients who had undergone MPR imaging. Local disease spread was evaluated according to the TNM system, and the results were compared with the pathologic findings using the McNemar test. The MDCT performance to differentiate each T-stage was evaluated using Fisher's exact test.

RESULTS. The sensitivities of the ability to differentiate the ≤ T1 versus ≥ T2 lesions, ≤ T2 versus ≥ T3 lesions, and ≤ T3 versus T4 lesions were 79.3%, 92.7%, and 100%, respectively; the specificities were 98.8%, 86%, and 100%, respectively (p < 0.0001). The overall accuracy for the T-stage was 83.9%. In the 53 patients with MPR images, the combined reading of the axial and MPR images increased the diagnostic accuracy compared with axial image reading only from 71.7% to 84.9%, a statistically significant degree (p = 0.0233).

CONCLUSION. MDCT provided 83.9% accuracy in the diagnosis of the local extent of gallbladder carcinomas, thereby showing acceptable sensitivity and specificity. The addition of MPR images to the axial CT data increased the accuracy.

Keywords: biliary system • gallbladder carcinoma • MDCT • T-stage


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Carcinoma of the gallbladder is the most common biliary tree malignancy and is the fifth most common malignancy of the alimentary tract [1]. As imaging techniques have developed, the preoperative diagnosis of gallbladder carcinoma has improved. However, the prognosis for gallbladder carcinoma remains poor because most gallbladder carcinomas present when the disease is at an advanced stage and the curative resection rate ranges only between 10% and 30% [2-4]. Because surgery is the only definitive curative therapy and the extent of surgery is determined by the extent of local tumor spread, it is important to diagnose this disease at an early stage and to accurately determine its extent [5]. For this purpose, several imaging techniques, such as CT, MRI, and endoscopic sonography, are currently being used, with CT being the most commonly used imaging study. Regarding evaluation of the local spread of gallbladder carcinoma, Yoshimitsu et al. [6] first described the role of helical CT and Naveen et al. [5] described the use of dual-phase MDCT with 3D reconstruction for staging and assessing the resectability of gallbladder carcinoma. However, in these studies, there were either only a small number of patients with early stage gallbladder cancer or only advanced stage carcinoma was included.

With the marked development of CT technology, MDCT, which provides high spatial resolution, is now widely used. Several previous studies have shown that MDCT improves the diagnostic accuracy of the staging workup in patients with gastric cancer or colon cancer [7, 8]. To our knowledge, until now there have been no published reports regarding the performance of MDCT in the preoperative evaluation of the local spread of gallbladder carcinomas, including those in patients with early stage cancers. The purposes of this study were to assess the diagnostic performance of MDCT in the T-staging of gallbladder cancer and to evaluate whether the combined interpretation of axial and multiplanar reconstruction (MPR) images improved the diagnostic accuracy compared with axial images only.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Population
A computerized search of our hospital's pathology database for the 4-year period from 2003 to 2006, revealed that 166 patients underwent surgery or biopsy and were pathologically confirmed to have gallbladder cancer. Among these patents, 48 were excluded from the study for two reasons: an MDCT study had not been performed (n = 42), or a pathologic diagnosis had not been obtained within 6 weeks of the CT examination (n = 6). A total of 118 patients (68 women and 50 men; age range, 41-94 years; mean age, 65 years) had undergone MDCT before surgery or biopsy, and MPR images were available for 53 of these patients. The mean interval between the time of CT and pathologic confirmation was 11.34 ± 9.35 (SD) days.

On histopathologic examination, 29 (24.6%) lesions were staged as pT1 (7 pTis, 13 pT1a, 9 pT1b), 39 (33.1%) as pT2, 39 (33.1%) as pT3, and 11 (9.3%) as pT4. Among 53 patients with MPR images, 11 (20.8%) lesions were staged as pT1 (3 pTis, 4 pT1a, 4 pT1b), 18 (34.0%) as pT2, 19 (35.8%) as pT3, and 5 (9.4%) as pT4. One hundred ten of these 118 patients underwent surgery: laparoscopic cholecystectomy (n = 15), open cholecystectomy (n = 35), cholecystectomy and partial hepatectomy (n = 42), and extended radical cholecystectomy (n = 18). In the other eight patients with evident T4 lesions on imaging studies including sonography, CT, and MRI, the diagnosis of gallbladder cancer was established by multiple core needle biopsies of the primary gallbladder lesion as well as of tumors extending into the liver and into two or more adjacent organs.

MDCT Protocol
Patients fasted for at least 8 hours before the examination; no oral contrast medium or water was given to the patients. CT examinations were performed with a Brilliance 64 (Philips Medical Systems) (n = 14), Sensation 16 (Siemens Medical Solutions) (n = 30), LightSpeed Ultra scanner (GE Healthcare) (n = 40), or MX8000 4-MDCT scanner (Philips Medical Systems) (n = 34). Each patient received 120 mL of a nonionic contrast material (iopromide, Ultravist 370, Bayer HealthCare) through an 18-gauge angiographic catheter inserted into a forearm vein. CT scans were routinely obtained with the patient in a supine position during full inspiration. The contrast material was injected at a rate of 3 mL/s with an automatic power injector. MDCT was performed with an MDCT scanner using the following parameters: detector collimation, 0.75~2.5 mm; table pitch, 1-1.5; kVp, 120; mAs, 170-220; slice thickness, 2.5-5 mm; and reconstruction intervals, 1.25-5 mm. After an initial unenhanced scan of the upper abdomen was obtained, MDCT scans were obtained at 65~75 seconds (portal venous phase) after initiation of the contrast injection.

In 53 patients, to obtain MPR images, 1- to 1.25-mm-thick axial images were reconstructed with 30% overlapping. The MPR images along the long axis and the short axis of the gallbladder were arbitrarily created using a dedicated workstation (Leonardo, Siemens Medical Solutions) by two experienced radiology technicians with at least 5 years of 3D reconstruction experience.

Image Analysis
The CT scans acquired in the 118 patients were reviewed in consensus by two abdominal radiologists with 13 and 15 years of experience. Although the reviewers knew that all patients had confirmed gallbladder carcinomas, they were unaware of the tumor location and size. All CT scans were reviewed on a PACS workstation (m-view, Marotech). During analysis of the CT features, cases of each T-stage were randomly intermixed.

According to the TNM classification and related radiologic literature regarding the CT staging of gallbladder cancer [5, 6, 9, 10], we defined the CT criteria for each T-stage (Table 1). The criteria of CT findings for each T category were as follows: T1, polypoid lesions without focal thickening of the gallbladder wall; T2, nodular or sessile lesions associated with focal thickening of the gallbladder wall at what was considered to be attachment sites and with the presence of an apparently smooth fat plane separating the adjacent organs [6]; T3, tumor perforates the serosa (visceral peritoneum) and directly invades the liver or one other adjacent organ or structure (such as the stomach; duodenum; colon; or pancreas, omentum, or extrahepatic bile ducts); and T4, tumor invades main portal vein or hepatic artery or invades multiple extrahepatic organs or structures [9]. In addition to the previously reported CT criteria of T-staging of gallbladder cancer [5, 6], we added some additional criteria regarding T1 and T2 lesions on the basis of our previous experience using radiologic-pathologic correlation. Nodular or flat lesions with mucosal enhancement or focal thickening of the inner enhancing layer of the gallbladder wall with clear, low-attenuated outer wall were regarded as T1 lesions. Regarding T2 lesions, we included the findings of diffuse thickening of the gallbladder wall with heterogeneous enhancement or two-layered enhancement (composed of strong, thick inner-layer enhancement and weak enhancement of the outer layer) and focal wall thickening with outer surface dimpling at the tumor base as criteria for identifying these lesions.


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  		TABLE 1: Suggested Revised CT Criteria for T-Stage of Gallbladder Cancer

 


Figure 1
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  		Fig. 1A —51-year-old woman with stage pT1a lesion of gallbladder, which was diagnosed on CT as stage T1. Axial CT scan shows well-enhancing nodular lesion (arrow). There is no wall thickening around nodular lesion in gallbladder.

 


Figure 2
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  		Fig. 1B —51-year-old woman with stage pT1a lesion of gallbladder, which was diagnosed on CT as stage T1. Photomicrograph of histopathologic specimen reveals tumor to be confined to mucosal layer (pT1a). (H and E)

 


Figure 3
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  		Fig. 2A —55-year-old woman with stage pT1b lesion of gallbladder, which was diagnosed on CT as stage T1. Axial CT scan shows nodular lesion with smooth thickening and enhancement of gallbladder wall (arrows).

 


Figure 4
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  		Fig. 2B —55-year-old woman with stage pT1b lesion of gallbladder, which was diagnosed on CT as stage T1. Photomicrograph of histopathologic specimen shows tumor to be confined to muscular layer (pT1b) (arrowheads). (H and E, x40)

 
In the first review session, two reviewers evaluated the axial images for the extent of local spread of disease in terms of the TNM system using the radiologic criteria determined by consensus [9, 10]. To assess the usefulness of the MPR images for predicting the local spread of the gallbladder cancer, after an interval of 4 weeks from the first review session, the reviewers were asked to interpret the CT data of the axial and MPR images of the 53 patients with MPR images.

Statistical Analysis
The diagnostic performance of the MDCT images in terms of differentiating T1 from ≥ T2, ≤ T2 from ≥ T3, and ≤ T3 from T4 for both interpretation sessions was evaluated using the Fisher's exact test (GraphPad InStat, version 3.0, Graph-Pad Software). Differences in the accuracy of the T-staging in the axial only and the combined MPR images were assessed using the McNemar test in the MedCalc statistical software, version 6.15.000 (MedCalc Software). Sensitivities and specificities were presented as 95% CIs. Statistical significance was inferred at a confidence level of 0.05.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Axial Only Data Set in the First Interpretation Session
The overall accuracy of MDCT for T-staging of gallbladder cancer was 83.9% (99 of 118 patients) (Figs. 1A, 1B and 2A, 2B and Table 2). Over- and understaging occurred in 11 (9.3%) and in eight (6.8%) of 118 patients, respectively. Among the 11 overstaged patients, six pT1 (2 pTis, 2 pT1a, 2 pT1b) lesions were misinterpreted as T2 lesions, and five pT2 lesions were misinterpreted as T3 lesions (Fig. 3A, 3B, 3C). Among the eight understaged patients, one pT2 lesion was misinterpreted as a T1 lesion, and seven pT3 lesions were misinterpreted as T2 lesions (Fig. 4A, 4B, 4C).


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  		TABLE 2: Diagnostic Accuracy of MDCT Images in T-Staging of Gallbladder Cancer

 

Figure 5
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  		Fig. 3A —72-year-old man with stage pT1 gallbladder cancer, which was overstaged as T2. Axial CT scan shows focal wall thickening and nodular lesion (black arrow) in body of gallbladder. Tumor was overstaged as T2 by observers because enhancement of thickened gallbladder wall was considered to represent tumor involvement of whole layer of gallbladder wall (white arrow).

 

Figure 6
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  		Fig. 3B —72-year-old man with stage pT1 gallbladder cancer, which was overstaged as T2. Endoscopic sonogram definitely shows preserved hypoechoic muscle layer (arrowheads) that suggests T1 lesion.

 

Figure 7
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  		Fig. 3C —72-year-old man with stage pT1 gallbladder cancer, which was overstaged as T2. Photomicrograph of histopathologic specimen reveals tumoral extension (arrowheads) through Rokitansky-Aschoff sinuses (asterisk). Involvement of Rokitansky-Aschoff sinuses indicates T1 lesion. However, tumor involvement of Rokitansky-Aschoff sinuses, which is invaginated into muscular layer, may mimic T2 lesion. (H and E, x40)

 

Figure 8
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  		Fig. 4A —57-year-old man with stage pT3 gallbladder cancer that was understaged as T2 on axial CT images. Axial CT scan shows nodular lesion (arrow) in body of gallbladder and subtle hyperattenuation of adjacent pericholecystic fat (arrowheads). Observers considered lesion to be cholecystitis accompanying cancer because of weak enhancement of pericholecystic fat.

 

Figure 9
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  		Fig. 4B —57-year-old man with stage pT3 gallbladder cancer that was understaged as T2 on axial CT images. Oblique coronal CT scan shows pericholecystic fat infiltration and pericholecystic vessel involvement (arrowheads).

 

Figure 10
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  		Fig. 4C —57-year-old man with stage pT3 gallbladder cancer that was understaged as T2 on axial CT images. Cut surface of gross specimen of gallbladder reveals pericholecystic fat invasion (arrowheads).

 

Axial Only and Combined Axial and MPR Data Sets in the Second Interpretation Session
Of the 53 patients for whom MPR images were available, T-staging was correctly diagnosed in 38 (71.7%) using axial-only data sets and in 45 (84.9%) using axial and MPR combined data sets. The overall accuracy for T-staging improved when MPR images were added to axial images (Fig. 5A, 5B, 5C); these differences were statistically significant (p = 0.0233). Specifically, the diagnostic performance of the axial-only images and of the combined axial and MPR data sets in terms of differentiating T1 from ≥ T2, ≤ T2 from ≥ T3, and ≤ T3 from T4, are shown in Table 3. In particular, in terms of differentiating ≤ T2 from ≥ T3, the combined axial and MPR data sets showed statistically significantly greater accuracy (p = 0.0412).


Figure 11
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  		Fig. 5A —54-year-old woman with stage pT3 gallbladder cancer. These images show value of multiplanar reformation (MPR) images in evaluation of T-staging. Axial CT scan shows eccentric wall thickening (arrow) and papillary lesion (asterisk) in fundus of gallbladder. Fat plane between liver and gallbladder seems to be preserved on this axial plane (arrowheads). This lesion was interpreted as T2 on axial CT image.

 

Figure 12
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  		Fig. 5B —54-year-old woman with stage pT3 gallbladder cancer. These images show value of multiplanar reformation (MPR) images in evaluation of T-staging. However, oblique coronal MPR image shows focal liver invasion of gallbladder cancer into adjacent liver (arrowheads). Asterisk indicates papillary lesion.

 

Figure 13
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  		Fig. 5C —54-year-old woman with stage pT3 gallbladder cancer. These images show value of multiplanar reformation (MPR) images in evaluation of T-staging. Cut surface of gross specimen reveals pT3 lesion (arrowheads).

 

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  		TABLE 3: Comparison of Diagnostic Performancea

 

Over- and understaging on axial-only images occurred in five (9.4%) of 53 patients and in three (5.7%) of 53 patients, respectively. However, on combined data sets, six (11.3%) of 53 patients were overstaged, and understaging was not observed. Among these, five patients were commonly overstaged on axial-only and combined data sets; three pT1 (2 pTis, 1 pT1a) lesions were misinterpreted as T2 lesions, and two pT2 lesions were misinterpreted as T3 lesions. In addition, on combined data sets, one pT1b lesion was misinterpreted as a T2 lesion. In three understaged patients on axial-only images, one pT2 lesion was interpreted as T1, and two pT3 lesions were interpreted as T2 lesions.


Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Accurate evaluation of the local extent of a gallbladder lesion is of pivotal importance in determining the optimal therapeutic strategy. The surgical approaches are determined by the extent of the primary tumor, and the prognosis of gallbladder cancer differs according to the T-staging [6, 11, 12]. Therefore, accurate preoperative T-staging of gallbladder cancer is crucial, and radiologists must be able to preoperatively differentiate T1 lesions from T2 lesions and T2 lesions from more advanced lesions [6].

In our study, the accuracy rate of MDCT in the T-staging of gallbladder cancer (83.9%) was comparable to that in other studies in which helical CT was used [6]. However, considering that our study included many patients with early gallbladder cancer (a total of 68 pT1 and pT2 lesions), absolute comparison with other studies cannot be made. More specifically, the study of Yoshimitsu et al. [6] showed that only one of three patients with T1 gallbladder cancer was correctly diagnosed on CT, which resulted in poor sensitivity (33%) for accurate T1 staging. In contrast, in our data, 23 of 29 pT1 lesions were correctly diagnosed, thereby resulting in relatively high sensitivity (79.3%). Improvement in these results can be expected with the continuing technical development of MDCT [13]. Because of the improved spatial resolution of MDCT compared with that of helical CT, in the diseased or thickened gallbladder wall several findings can help to distinguish the involved layer thereby allowing determination of the accurate T-stage.

Considering the improved spatial resolution of MDCT and the pathologic criteria for T-staging, we used new CT criteria for distinguishing T1 from T2 lesions. Given that T2 lesions indicate tumoral involvement of the perimuscular connective tissue layer, the diagnostic criteria suggesting T2 lesions included a nodular lesion with the area of the tumor base dimpled suggesting involvement of perimuscular connective tissue layer; a flat lesion with two-layered enhancement or heterogeneous enhancement of the thickened gallbladder wall, suggesting muscle layer involvement or perimuscular connective tissue involvement, respectively; and no pericholecystic vessel involvement. Using these criteria, the accuracies of MDCT in terms of differentiating T1 from ≥ T2 and ≤ T2 from ≥ T3, were 94.1% and 89.8%, respectively (Table 2). In previous studies of gallbladder cancer diagnosed on helical CT, the authors applied morphologic criteria based on previously reported pathologic observations [11, 14, 15] that most T1 lesions are polypoid with thin stalks and are typically 2 cm or less in diameter, whereas T2 lesions tend to be nodular or sessile with focal thickening of the adjacent gallbladder wall. Distinguishing T1 lesions from T2 lesions on helical CT using these criteria, however, has been discouraged perhaps because of the limited spatial resolution achievable with the helical CT technique [6].

One of the benefits that MDCT can provide is the ability to provide MPR images in any axis. Several studies have shown that adding MPR images to the axial images allows improved diagnostic performance of preoperative tumor staging in gastrointestinal tract malignancies [7, 8, 13, 16-19]. Our study also revealed that combining MPR images with axial images improved the accuracy of T-staging of MDCT with axial images (from 71.7% to 84.9%, p = 0.0233) and permitted differentiation of ≤ T2 lesions from more advanced stage ≥ T3 lesions (p = 0.0412). We believe that this improvement could be made with reduced partial volume effects, which are the drawback of axial images, especially in some transitional zones where the gallbladder axis is tangential to the scanning plane (Fig. 5A, 5B, 5C). Furthermore, because MPR shows an oblique coronal plane similar to the surgical plane, this can be helpful in planning the surgery.

On the other hand, the accuracy was lower in the combined axial and MPR data sets for axials alone than in the total group. This was because more difficult cases were included in the group with MPR images (53 lesions) compared with the total group. Histologically, more cases of flat and papillary tumors were included in the group with MPR images. Twenty-seven (50.9%) of 53 lesions were pathologically proven to be flat (n = 13) or papillary (n = 14) tumors. In our experience, it is difficult to diagnose the local spread of flat lesions, and papillary lesions were frequently overstaged because of their large size and strong enhancement. The relatively high incidence of flat or papillary lesions in the subgroup with MPR images might be the cause of the lower accuracy of the axial-only reading in these 53 patients on MPR images compared with that of the axial image reading in the total 118 patients.

In our study, there were 11 patients with overstaging on MDCT. Among them, seven (63.6%) had papillary growth-type lesions. Two (18.2%) had combined xanthogranulomatous inflammation. In the remaining two patients with pTis and pT1a (18.2%), respectively, pathologic specimens revealed tumor extension through the Rokitansky-Aschoff sinuses, which was invaginated into the muscle layer. Therefore, despite the tumors being confined to the mucosal layer, the exaggerated enhancement of the tumor and muscle layer complex mimicked a T2 lesion and led to overstaging (Fig. 3A, 3B, 3C). The literature suggests that concurrent inflammation around the tumor causes overstaging and that xanthogranulomatous cholecystitis can be found coincidently [6]. On the basis of our results, we believe that radiologists must be aware that lesions can be overstaged in the presence of concurrent inflammation or adenomyomatosis or when the mass shows papillary features.

Alternatively, in our study there were eight understaged lesions. Three (37.5%) of them revealed direct liver invasion less than 3 mm in depth in the gallbladder bed of segment IVb or V. In two of the eight lesions, the time intervals between CT acquisition and surgery were longer than average duration, 25 and 30 days, respectively. Two of these eight lesions had a reconstruction slice thickness of 5 mm, thus causing a partial volume averaging effect. The remaining lesion had subtle tumor infiltration into the muscle layer (Fig. 4A, 4B, 4C). Among the eight understaged lesions on axial-only readings, the three patients who had understaged lesions with focal liver invasion less than 3 mm in depth had MPR images available and when we reviewed the MPR images and axial images, we correctly diagnosed the local liver invasion (Fig. 5A, 5B, 5C).

The limitations of this study include its retrospective nature, consensus reading, and the use of four different MDCT scanners. In addition, there was a potential selection bias in the patient population toward those with less-advanced disease because most of the patients (93.2%, 110/118) we recruited had surgically confirmed lesions.

In conclusion, in our study, MDCT provided 83.9% accuracy in evaluating the T-staging of gallbladder carcinomas. The findings of the combined axial and MPR images allowed improved diagnostic accuracy compared with the results of axial imaging only.


Acknowledgments
 
The authors thank Dong Chul Kim and Hye Sil Seol of the Department of Pathology, Seoul National University Hospital, for providing the pathologic specimens and for their opinions regarding this study. We also thank Bonnie Hami for her editorial assistance in the preparation of this manuscript.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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A. Furlan, J. V. Ferris, K. Hosseinzadeh, and A. A. Borhani
Gallbladder Carcinoma Update: Multimodality Imaging Evaluation, Staging, and Treatment Options
Am. J. Roentgenol., November 1, 2008; 191(5): 1440 - 1447.
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