|Year : 2017 | Volume
| Issue : 3 | Page : 862-869
Staging of cholangiocarcinoma by multidetector computed tomography
Elsayed E Elsayed1, Mohammed M Houseni2, Rasha Ab Ali Abd Elwahab MSc 2
1 Department of Radiology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Radiology, National Liver Institute, Menoufia University, Menoufia, Egypt
|Date of Submission||29-Mar-2016|
|Date of Acceptance||26-Jun-2016|
|Date of Web Publication||15-Nov-2017|
Rasha Ab Ali Abd Elwahab
Department of Radiology, National Liver Institute, Shebin Elkom, Menoufia, 32511
Source of Support: None, Conflict of Interest: None
The aim of this article is to describe the role of multidetector computed tomography (MDCT) in the staging of cholangiocarcinoma using surgery as the reference standard.
Cholangiocarcinoma is associated with a dismal prognosis; however, curative resection may offer a chance of cure. Various factors should be considered in the staging of cholangiocarcinoma. These factors include the extent of bile duct involvement, vascular invasion, lymph node metastasis, peritoneal seeding, and distant metastases. Using high-quality volume data from MDCT and adequate postprocessing images, radiologists can provide various types of information that is imperative for curative resection of cholangiocarcinoma.
Patients and methods
This study included 50 patients (23 men and 27 women) who had finally been diagnosed with cholangiocarcinoma. Informed consent was signed by the patients. All patients were subjected to a proper assessment of history, clinical examination as well as routine laboratory investigations. Triphasic abdominal MDCT was performed using postprocessing techniques including multiplanar reformation, maximum intensity projection, and minimum intensity projection.
Twenty-one patients had intrahepatic cholangiocarcinoma, 27 patients had perihilar cholangiocarcinoma, one patient had extrahepatic distal cholangiocarcinoma, and one patient had mixed (intrahepatic and perihilar) cholangiocarcinoma. The tumor was resectable in 13 patients, where 10 patients were consistent with preoperative MDCT findings and three patients were inconsistent.
MDCT images provide important information on the preoperative evaluation and staging of cholangiocarcinoma with reference to the surgical procedures and findings.
Keywords: distal cholangiocarcinoma, intrahepatic cholangiocarcinoma, multidetector computed tomography, perihilar cholangiocarcinoma
|How to cite this article:|
Elsayed EE, Houseni MM, Ali Abd Elwahab RA. Staging of cholangiocarcinoma by multidetector computed tomography. Menoufia Med J 2017;30:862-9
|How to cite this URL:|
Elsayed EE, Houseni MM, Ali Abd Elwahab RA. Staging of cholangiocarcinoma by multidetector computed tomography. Menoufia Med J [serial online] 2017 [cited 2019 Nov 12];30:862-9. Available from: http://www.mmj.eg.net/text.asp?2017/30/3/862/218254
| Introduction|| |
Cholangiocarcinoma is an adenocarcinoma that arises from the intrahepatic and extrahepatic bile duct epithelium. It is a relatively common liver cancer, the second most prevalent liver cancer after hepatocellular carcinoma . Cholangiocarcinoma is mainly a tumor of the elderly, with peak prevalence during the seventh decade of life and a slight male predilection .
Cholangiocarcinoma may arise at any portion of the bile duct epithelium, from the terminal ductules (canals of Hering) to the ampulla of Vater, as well as the peribiliary glands. Cholangiocarcinoma is subdivided into intrahepatic, perihilar (Klatskin tumor), or extrahepatic on the basis of its site of origin. Cholangiocarcinoma tend to grow slowly and to infiltrate duct walls, dissecting along tissue planes .
Several methods have been proposed to evaluate tumor extension. The Bismuth–Corlette classification has been used to define the longitudinal tumor extension in hilar cholangiocarcinoma. Lateral tumor extension can be defined by the TNM staging provided by the American Joint Committee Cancer staging system. Resectability of the tumor can be evaluated by the Blumgart T-staging system combined with the American Joint Committee Cancer staging system .
The most important staging issue is whether the tumor can be removed surgically or whether it is too advanced or invasive for surgical treatment. Tumors may extend locally into the liver, porta hepatis structures, and regional lymph nodes of the celiac and pancreaticoduodenal chains .
Imaging plays a role in the noninvasive diagnosis, characterization of cholangiocarcinoma, confirmation of diagnosis, pretherapeutic staging, assessment of resectability, and screening of high-risk patients for early detection .
Ultrasonography (US) is the initial screening imaging modality for evaluating biliary dilatation in patients with jaundice because it is inexpensive and widely available. Color Doppler US is useful in differentiating vessels from dilated ducts and can provide information on the status of vessels. Other imaging modalities are generally relied upon for further evaluation .
Computed tomography (CT) scanning plays an important role in the diagnosis of cholangiocarcinoma. With the emergence of multidetector scanners, CT has become the noninvasive diagnostic test of choice for detailed evaluation and staging of cholangiocarcinoma. It can show bile duct dilatation, tumor mass, bile duct wall thickening, or intraductal tissue in exophytic, infiltrative, and polypoid cholangiocarcinoma by a simple evaluation of the relationship of the tumor with vessels and surrounding organs . Multidetector computed tomography (MDCT) may challenge the role of MRI in the diagnosis of cholangiocarcinoma because of its high spatial resolution .
Although abdominal imaging can be useful in the diagnosis of cholangiocarcinoma, direct imaging of the bile ducts by endoscopic retrograde cholangiopancreatography or percutaneous transhepatic cholangiography may be utilized. Magnetic resonance cholangiopancreatography is a noninvasive alternative to endoscopic retrograde cholangiopancreatography and percutaneous transhepatic cholangiography .
Although surgery offers the only chance of a cure, the majority of these tumors, because of their poor prognosis and advanced stage at the time of diagnosis, are managed with nonsurgical treatment such as endoscopic or percutaneous placement of biliary endoprosthesis for palliation of jaundice. Biliary bypass surgery is considered for palliation in patients in whom stent placement fails or is not possible. Liver transplantation, although not performed routinely for cholangiocarcinoma, can increase survival time in selected patients in whom resection is not feasible because of locally advanced disease .
| Patients and Methods|| |
This study was carried out on 50 patients (23 men and 27 women) with a final diagnosis of cholangiocarcinoma; their mean age was 57.44 years, ranging between 40 and 83 years. The patients were referred to the CT unit in National Liver Institute, Menoufia University, in the period between January 2012 and January 2015.
Cholangiocarcinoma was diagnosed on the basis of clinical, laboratory (elevated tumor markers), and imaging studies (including US, triphasic CT), and confirmed by a postoperative pathological study. They were referred for the MDCT study of the hepatobiliary system to confirm the level of obstruction and for tumor staging.
All patients were subjected to the following:
- Clinical evaluation: identification data: age, sex, and weight
- Complete assessment of history
- Laboratory and serological examinations including serum bilirubin, liver enzymes (aspartate transaminase and alanine transaminase), prothrombin time, prothrombin concentration, alkaline phosphatase, γ-glutamyl transferase, and renal profiles that included blood urea and serum creatinine level, carbohydrate antigen 19–9, and carcinoembryonic antigen were performed
- Imaging investigations: US with colored Doppler and triphasic MDCT of the abdomen and pelvis.
A written consent was signed by all patients or their relatives before the procedure. The study was approved by the Research Ethics Committee of National Liver Institute and the Research Ethics Committee of the Faculty of Medicine, Menoufia University.
The patient was provided a brief explanation of the procedure. A low-residue diet was prescribed 24 h before the procedure and the patient was instructed to come to the CT unit after fasting for at least 4 h. The patient was asked to drink 800–1000 ml of water at least 90 min before the examination to distend the gastrointestinal tract. Reassurance and a brief explanation of the procedure were provided to the patient.
All patients were examined in the supine position and they were instructed not to move during the examination. They were asked to suspend breathing during the scanning time. Anteroposterior scout view was used to set the scanning area from the diaphragm to the level below the symphysis pubis.
A precontrast scan of the upper abdomen in the craniocaudal direction during breath hold was performed to screen the gall bladder and detect any bile duct stones. Then, a triphasic study was carried out for all the patients. This included an arterial, portal–venous, and delayed phase at around 20–25, 60, and 180 s after the initiation of intravenous contrast, respectively. The injection was administered using an automatic power injector through a wide-pore peripheral venous access cannula; in most cases, this was the antecubital fossa vein (1.5–2 ml/kg patient's body weight of 300–350 mg of iodine/ml). Injection flow rate was set to 4–5 ml/s. Most of the patients who were administered the intravenous contrast had normal serum creatinine.
Axial CT source images were displayed with liver window settings and all axial CT image data were sent through a local area network to a freestanding available picture archiving and communication system workstation. Multiplanar reformation (MPR) images provided axial, orthogonal coronal, sagittal, or oblique planes. Three-dimensional rendering of the arterial-phase and portal–venous-phase imaging was used to construct detailed vascular maps of the hepatic artery and the portal/hepatic veins, respectively.
CT cholangiographic images were created by MPR and thin-slab minimum intensity projection (MinIP) techniques; MPR uses oblique projection of 0.6 mm thickness in contiguous planes throughout the biliary tract and the MinIP technique uses variable slab thickness according to bile duct dilatation in coronal oblique planes throughout the biliary tract.
A retrospective interpretation of MDCT images of the workstation was performed independently by two radiologists. Differences in assessments were resolved by consensus. With MDCT, tumor characteristics were noted on imaging and morphologically classified using the Liver Cancer Study Group of Japan criteria and staged using the TNM classification.
| Results|| |
Our 50 patients were classified by MDCT into four groups according to the level of lesion: group I: intrahepatic level (21 cases), group II: perihilar level (27 cases), group III: extrahepatic level (one case), and group IV: mixed intrahepatic and perihilar (one case) [Table 1].
|Table 1: Levels of lesion in the studied 50 patients with cholangiocarcinoma|
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The patterns of tumor growth of the cases studied were classified according to the level of lesion by MDCT as follows: Intrahepatic cholangiocarcinoma into a mass-forming lesion in 10/21 (47%) patients, infiltrating lesion in 1/21 (4.8%) patients, multicentric lesion in 8/21 (38.1%) patients, and combined hepatocellular carcinoma (HCC)–cholangiocarcinoma in 2/21 (9.5%) patients; perihilar cholangiocarcinoma into a mass-forming lesion in 12/27 (44.4%) patients and infiltrating lesion in 15/27 (55.6%) patients; and extrahepatic distal infiltrating cholangiocarcinoma in 1/1 (100%) patient and finally mixed perihilar (polypoid lesion) and intrahepatic (mass-forming lesion) cholangiocarcinoma in 1/1 (100%) patient [Table 2].
|Table 2: Multidetector computed tomography classification of the pattern of tumor growth of the studied cases|
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MDCT showed that according to hilar obstruction on the basis of the Bismuth classification, no patient had type I obstruction; 4/27 (14.8%) patients had type II obstruction; 7/27 (25.9%) patients had type IIIa obstruction; 6/27 (22.2%) patients had type IIIb obstruction; and 10/27 (37%) patients had type IV obstruction [Table 3].
Vascular involvement of the studied cases by the MDCT study showed that portal vein involvement was detected in 19/50 (38%) patients, hepatic artery involvement was detected in 12/50 (24%) patients, hepatic vein involvement was detected in 5/50 (10%) patients, and retrohepatic inferior vena cava (IVC) involvement was detected in 3/50 (6%) patients [Table 4].
|Table 4: Hepatic vessels' involvement in the tumor on multidetector computed tomography angiography|
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MDCT showed the following: T1 in 4/50 (8%) cases; T2 in 6/50 (12%) cases; T3 in 31/50 (62%) cases; T4 in 9/50 (18%) cases; N0 in 30/50 (60%) cases; N1 in 20/50 (40%) cases; M0 in 45/50 (90%) cases; and M1 in 5/50 (10%) cases [Table 5].
|Table 5: TNM staging of cholangiocarcinoma on multidetector computed tomography|
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Multidetector computed tomography diagnosis and staging
- Hilar (infiltrating) cholangiocarcinoma (Klatskin tumor, Bismuth grade IIIb), with vascular invasion, regional adenopathy, and pulmonary deposits. The initial imaging-based staging is T4N1M1. Blumgart T2. Nonresectable tumor [Figure 1]
- Hilar (mass-forming) cholangiocarcinoma (Klatskin tumor, Bismuth IIIb). The initial imaging-based staging is T3N0M0. Blumgart T1. Resectable tumor. Intraoperative findings were consistent with preoperative MDCT findings [Figure 2]
- Extrahepatic (infiltrating) cholangiocarcinoma. The initial imaging-based staging is T2N0M0. Resectable tumor. Intraoperatively, the tumor was seen extending proximally invading the liver parenchyma and distally invading the pancreatic head with regional adenopathy; common bile duct (CBD) resection, partial hepatectomy, Whipple procedure, and surgical biliary bypass were performed. Intraoperative findings were inconsistent with preoperative MDCT findings and the staging changed to T3N1M0 [Figure 3]
- Intrahepatic (multicentric) cholangiocarcinoma with IVC encasement. The initial imaging-based staging is T3N0M0. Nonresectable tumor [Figure 4]
- Intrahepatic (mass-forming) cholangiocarcinoma. This is associated with metastatic adenopathies and pulmonary deposits. The initial imaging-based staging is T3N1M1. Nonresectable tumor [Figure 5].
|Figure 1: Axial contrast-enhanced computed tomography (CT) images at arterial (a), portal–venous (b), and delayed (c) phases showed an ill-defined hilar lesion (arrow) reflecting mild intrahepatic biliary radicle dilatation. The lesion shows contrast retention at the delayed phase. Axial contrast-enhanced CT image (d) at the portal–venous phase showing porta hepatis necrotic lymph node. Axial CT image (lung window) (e) shows basal pulmonary nodules. Coronal maximum intensity projection and (g) shows CBD stent (white arrow). Left hepatic artery encasement (red arrow). CT portography (h) shows amputated left portal vein. CT arteriography.|
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|Figure 2: Axial images at arterial (a), portal–venous, (b) and delayed (c) phases, respectively, showed an ill-defined hilar mass (arrow) reflecting mildly dilated intrahepatic biliary radicles, more on the left side. The lesion shows contrast retention in the delayed phase. Coronal multiplanar reformation (e) image shows a pigtail drain (arrows) seen extending from the right hepatic duct along CBD to the duodenum computed tomography (CT) portography and (f) shows no invasion/displacement of the portal vein or its branches. CT arteriography (g) shows no invasion/displacement of the hepatic artery or its branches arrow ill defined hilar mass. Intraoperative images (h and i).|
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|Figure 3: Axial images at arterial (a) and portal–venous (b) phases showed dilated common bile duct with evidence of mural wall thickening and strong enhancement notably observed distally (white arrow). This is associated with bilobar mild intrahepatic biliary radicle dilatation. Multidetector computed tomography cholangiography (c) using coronal oblique minimum intensity projection shows the extension of the lesion beyond the wall of the common bile duct (arrows). Dilatation of the intrahepatic bile ducts was more clearly visualized.|
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|Figure 4: Axial images at arterial (a), portal–venous, (b) and delayed (c) phases showed a focal lesion observed at segments I, II, IV, and VIII. The lesion shows progressive contrast retention at the delayed phase. Axial image at the arterial phase (d) shows smaller similar lesions at the left lobe (segments II and IV) (arrows). Coronal maximum intensity projection (e) image shows encasement of inferior vena cava by the previously described focal lesion (arrow). Computed tomography (CT) portography (f and g) shows displacement, but not invasion, of the left portal vein (arrow). CT arteriography.|
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|Figure 5: Axial images at arterial (a), portal–venous, (b) and delayed (c) phases showed a focal lesion observed at segment VII. The lesion shows progressive contrast retention at the delayed phase. This is associated with smaller similar lesions (arrows) beside it. Axial computed tomography (CT) (d) image (lung window) shows two basal pulmonary nodules (arrows). Axial images at the portal–venous phase (e) show multiple enlarged porta hepatis, paraaortic, and pericaval lymph nodes (arrows). Coronal multiplanar reformation image at the portal–venous phase.|
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| Discussion|| |
Cholangiocarcinoma is the most common biliary malignancy and the second most common hepatic malignancy after HCC .
The site of cholangiocarcinoma determines the presenting symptoms. Tumors originating from a large bile duct are in a critical location and are discovered early. Conversely, tumors originating from small bile ducts do not cause significant biliary obstruction until the late stage, when the tumor itself or metastatic hilar lymphadenopathy causes obstruction of the common hepatic duct .
Imaging is the main diagnostic modality for HCC. It is essential in planning the best management of these patients, estimating the curative resection, or establishing palliative treatment .
The aim of this study was to assess the role of the MDCT in detecting and staging cholangiocarcinoma and also evaluating the global performance of combined axial, MPR, and MinIP image reconstructions.
According to the Sainani et al.  classification, our patients were classified into four groups: group I: intrahepatic level obstruction (21 cases): 10 cases, mass-forming lesion; one case, infiltrating lesion; eight cases, multicentric lesions; and two cases, combined HCC–cholangiocarcinoma. Group II: hilar level obstruction (27 cases): 12 cases, mass-forming lesion and 15 cases, infiltrating lesion. Group III: extrahepatic level obstruction (one case): Infiltrating lesion. Group IV: mixed obstruction (one case): Intrahepatic and hilar cholangiocarcinoma.
Sainani et al.  reported that US is relatively less accurate in the estimation of tumor spread in the abdomen and the determination of tumor resectability. In addition, the accuracy of US varies with tumor type, equipment quality, and operator experience. Therefore, other imaging modalities are generally relied upon for further evaluation.
Sainani et al.  reported that MDCT has become the noninvasive diagnostic test of choice for detailed evaluation and staging of cholangiocarcinoma. MDCT is versatile and available widely. It shows the level and cause of biliary obstruction and enables a survey of the entire abdomen for disease staging. Multiphase scanning with a focused technique is usually recommended for the initial evaluation of cholangiocarcinoma.
In our study, intrahepatic lesions were detected in 21 patients, classified into mass-forming lesion in 10 (47.6%) patients and infiltrating lesion in one (4.8%) patient. Multiple intrahepatic variable-sized focal lesions, multicentric cholangiocarcinoma, were detected in eight (38.1%) patients. Combined HCC–cholangiocarcinoma was detected in two (9.5%) patients. Most of the lesions showed peripheral enhancement at the arterial phase with retention of contrast at the delayed phase apart from two cases (combined HCC–cholangiocarcinoma), which showed arterial heterogeneous enhancement with delayed contrast retention.
In intrahepatic cholangiocarcinoma, vascular involvement was detected in 12 patients, portal vein involvement in six (28.6%) patients, hepatic artery involvement in two (9.5%) patients, hepatic vein involvement in two (9.5%) patients, and retrohepatic IVC involvement in two (9.5%) patients.
In the present study, MDCT cholangiography correctly diagnosed all patients with hilar obstruction that had occurred at the porta hepatis in 27 patients. A mass-forming lesion was observed in 12 (44.4%) patients, whereas an infiltrating lesion was observed in 16 (55.6%) patients, which is in agreement with the study carried out by Madhusudhan et al. .
In perihilar cholangiocarcinoma, vascular involvement was detected in 24 patients. Portal vein involvement was found in 12 (44.4%) patients compared with 13 patients in the study carried out by Silva et al. , who reported a diagnostic accuracy of 94.4% in the detection of portal vein involvement. Hepatic artery involvement was found in 10 (37%) patients, compared with 11 patients in the study carried out by Chen et al. , who reported a diagnostic accuracy of 88.9% in the detection of hepatic artery involvement. The hepatic vein involvement in our study was detected in two (7.4%) patients, whereas no retrohepatic IVC involvement was detected in those patients.
In our study, extrahepatic (distal) cholangiocarcinoma was detected in one (2%) patient, observed on MDCT as dilated CBD with mural wall thickening and enhancement, which was associated with mild intrahepatic biliary radicle dilatation. No vascular involvement was observed on MDCT angiography. Mixed cholangiocarcinoma (intrahepatic and perihilar) was detected in one (2%) patient. An intrahepatic lesion is mass forming, whereas a hilar lesion is polypoid (intraductal). MDCT angiography showed right portal vein invasion by the intrahepatic lesion. Retrohepatic IVC compression and invasion by the intrahepatic mass was also detected.
Slattery and Sahani  showed that there are three main staging systems for patients with cholangiocarcinoma: the TNM staging system, the Bismuth–Corlette classification system, and the Blumgart modifications. Chung et al.  reported that the Bismuth–Corlette classification has been used to define the longitudinal tumor extension in hilar cholangiocarcinoma. Khan et al.  reported that the T category is based on the number of tumor nodules, vascular invasion, and direct extension into extrahepatic tissues. Unlike HCC, tumor size is not considered important: N category for nodal disease and M category for distant metastases.
Our study showed that MinIP and MPR images had an additional value in the staging of cholangiocarcinoma rather than the use of axial images alone.
For perihilar cholangiocarcinoma, our study showed that according to the Bismuth classification of hilar obstruction, no patients had type I obstruction; four (14.8%) patients had type II obstruction; seven (25.9%) patients had type IIIa obstruction; six (22.2%) patients had type IIIb obstruction; and ten (37%) patients had type IV obstruction.
In our study, TNM classification of the cases studied showed that four (8%) patients had been classified as T1 (all patients had intrahepatic cholangiocarcinoma); six (12%) patients had been classified as T2 (two patients were intrahepatic; three were perihilar; and one had distal extrahepatic cholangiocarcinoma); 31 (62%) patients had been classified as T3 (13 patients were intrahepatic; 17 were perihilar, and one had mixed cholangiocarcinoma); and nine (18%) patients had been classified as T4 (two patients were intrahepatic and seven had perihilar cholangiocarcinoma). Thirty (60%) patients had been classified as N0; 20 (40%) patients had been classified as N1 (10 patients were intrahepatic and 10 had perihilar cholangiocarcinoma). Forty-five (90%) patients had been classified as M0; five (10%) patients had been classified as M1 (three patients were intrahepatic and two had perihilar cholangiocarcinoma).
An accurate assessment of the extent of cholangiocarcinoma is crucial for treatment planning, which could be either surgical resection (in resectable patients) or palliative treatment (in unresectable patients) . In our study, MDCT of the cases studied showed that cholangiocarcinoma was resectable in 13 (26%) patients and unresectable in 37 (74%) patients.
In unresectable patients, the tumor was unresectable at the time of presentation and palliation was the only treatment possible to improve patients' quality of life. Among 13 resectable cases (four patients had intrahepatic cholangiocarcinoma; eight had perihilar cholangiocarcinoma; and one had extrahepatic distal cholangiocarcinoma), ten (76.9%) patients were consistent with preoperative MDCT findings; three (23.1%) patients were inconsistent.
Therefore, our study showed that MDCT and its reformatted images (MinIP and MPR) were satisfactory for staging of cholangiocarcinoma and accurate preoperative assessment of the tumor extent with reference to the surgical procedures and findings.
| Conclusion|| |
MDCT can be considered a noninvasive and fast imaging tool in the assessment of patients with cholangiocarcinoma. MPR and MinIP images provide improved visualization of the liver and the biliary system. It represents a valuable supplement to the conventional MDCT imaging of cholangiocarcinoma.
Our study showed that MDCT and its reformatted images were satisfactory for accurately estimating the preoperative evaluation and staging of cholangiocarcinoma with reference to the surgical procedures and findings.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]