Manual Surgical Treatment of Hilar and Intrahepatic Cholangiocarcinoma (Updates in Surgery)

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Cholangiocarcinoma can be classified into intrahepatic ICC and extrahepatic including hilar and distal bile duct according to its anatomic location within the biliary tree with respect to the liver. This paper reviews the management of ICC, focusing on the epidemiology, risk factors, diagnosis, and surgical and nonsurgical management. Cholangiocarcinoma is a highly fatal primary cancer of the bile ducts that arises from malignant transformation of bile duct epithelium.

Recent research in mouse models suggests the possibility that cholangiocarcinoma can arise directly from the transdifferentiation of hepatocytes [ 1 , 2 ]. ICC can arise in patients both with a normal liver and with underlying chronic liver disease [ 3 ]. The global incidence of ICC has been increasing [ 5 ]. An increase in incidence has also been seen in other countries such as the United Kingdom [ 7 ] and Japan [ 8 ]. Some of this increase in incidence may be attributed to the disease being historically underdiagnosed due to less sophisticated radiologic and endoscopic imaging, as well as misclassification.

A study in the US found an increase in mortality rates in ICC between and with an estimated annual percent change of 9. A different study in the UK reported a fold increase in age specific mortality rates from 0. Mortality from ICC tripled in Germany between and [ 12 ].

Italy noted an even more dramatic increase in mortality rates between and , reporting an increase from 0. There are several risk factors associated with ICC and the development of disease is likely multifactorial. The risk of ICC increases with older age as well as female sex. In addition, several other risk factors include primary sclerosing cholangitis, hepatolithiasis, choledochal cysts, primary biliary cirrhosis, parasitic biliary infection with Clonorchis sinensis or Opisthorchis viverrini , inflammatory bowel disease, and chronic pancreatitis [ 14 ], as well as the historical use of the radiologic contrast agent Thorotrast.

More recently, several risk factors that have traditionally been considered risk factors for hepatocellular carcinoma HCC such as alcoholic liver disease [ 14 ], obesity [ 15 ], diabetes [ 14 , 16 ], cirrhosis, hepatitis B infection [ 15 , 17 , 18 ], and tobacco use [ 14 ] have been implicated in ICC [ 15 ]. A meta-analysis of seven case-control studies with a total study population of , reported an overall OR of Of note, with regard to the noted risk factors, there has been no appreciable increase in any specific factor that can fully account for the increase in incidence of ICC over the past 30 years Table 1.

Two risk factors that have increased in incidence worldwide are nonalcoholic fatty liver disease NAFLD and hepatitis C. NAFLD, which is associated with obesity and metabolic syndrome, is an increasing concern worldwide and especially in the United States. Recently, investigators have looked at these factors in the setting of cholangiocarcinoma.

Metabolic syndrome was implicated as a risk factor for ICC odds ratio: This study did not, however, stratify patients by type of cholangiocarcinoma. In a different study, Reddy et al. A meta-analysis that combined 3 case-control studies evaluating obesity as a risk factor for ICC found an overall OR of 1. While many of these risk factors are relatively common, only a very small percentage of patients with ICC actually have an identifiable risk factor.

As such, it is likely that there are additional contributing factors to the development of ICC. While cholangiocarcinoma of the hilum or distal ducts often presents with biliary obstruction, ICC is often an incidental radiologic finding.

Radical resection of hilar cholangiocarcinoma and regional hilar lymphadenectomy

Thus, clinical presentation alone is rarely sufficient for diagnosis. At very late stages, patients may develop hepatomegaly, malaise, weight loss, failure to thrive, abdominal pain, night sweats, or jaundice; however, the frequent biliary obstruction seen in hilar or distal lesions is rarely present in ICC. Lesions detected on radiologic imaging can be evaluated using bile duct brushings or biopsied using endoscopic ultrasound and fine needle aspiration EUS-FNA to distinguish cholangiocarcinomas from hepatocellular carcinoma and metastatic disease.


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While there is a theoretical risk of seeding the needle track while performing the biopsy, a study by El-Chafic et al. This histologic appearance when diagnosed on a core biopsy of the liver can be very similar to the appearance of metastatic lesions to the liver from extrahepatic adenocarcinomas of the foregut [ 36 ]. A search to rule out an extrahepatic primary tumor should therefore usually be performed using upper and lower endoscopy to rule out occult gastrointestinal malignancy; in addition, cross-sectional imaging of the chest, abdomen, and pelvis to rule out an intrathoracic or intra-abdominal primary tumor can also be helpful.

In addition to these imaging studies, laboratory values including tumor markers should be assessed Figure 1. However, it must be noted that biliary obstruction and acute cholangitis may also cause an increase in CA; therefore markers should be measured after biliary decompression and drainage. Reports of more specific serum marks such as CYFRA, claudin-4, insulin-like growth factor binding protein 5 IGFBP-5 , and biglycan exist; however, none of these are routinely clinically used [ 39 , 40 ]. ICC is often diagnosed as an incidental radiologic finding on cross-sectional imaging performed for other reasons.

ICC, however, can often be difficult to diagnose on the basis of radiologic findings alone. On MRI, ICC lesions are generally hypointense on T1-weighted images and heterogeneously hyperintense on T2-weighted images with central hypointensity, indicating central tumor fibrosis [ 41 ]. Lesions can demonstrate initial rim enhancement characterized by progressive and concentric enhancement and pooling of contrast on dynamic contrast-enhanced MRI that again may indicate fibrosis Figure 2 [ 41 , 42 ].

The appearance of ICC on unenhanced CT scan is often as a hypodense mass with irregular margins [ 43 ]. On contrast-enhanced helical CT, rim-like enhancement at the tumor periphery is usually seen in both the arterial and portal venous phase with gradual centripetal enhancement on delayed imaging [ 41 , 44 ]. ICC may only enhance completely on delayed imaging obtained after contrast administration, a finding related to the desmoplastic nature of the tumor. While imaging may be helpful, it cannot reliably distinguish between ICC, metastatic adenocarcinoma from extrahepatic primaries or HCC with cirrhosis [ 46 ].

Two separate staging systems had, however, been proposed based on data from Japan. The first, proposed by Okabayashi et al.


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  5. Taking these four prognostic factors into account, Okaybayashi et al. Regional lymph node metastasis and distant metastasis were also independently associated with outcome and were therefore included. More recently, Nathan et al. The authors noted that the new system had superior discriminatory power. In this analysis, the presence of multiple tumors HR: Tumor size was not predictive of survival after surgical resection.

    As such, the staging system proposed by Nathan et al. In the current staging system, tumor size was removed as a prognostic factor. The T classification is defined as follows: Complete surgical resection of ICC with negative margins R0 resection currently represents the only potentially curative option. Because a subset of patients with ICC will have metastatic disease that was not identified on preoperative imaging, some surgeons advocate for a staging laparoscopy prior to laparotomy for resection.

    While data are lacking with respect to the diagnostic yield of staging laparoscopy, there have been reports suggesting a potential role in ICC.

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    Gastroenterology Research and Practice

    Due to the paucity of evidence, staging laparoscopy is not routinely performed for patients with potentially resectable ICC. Surgical resection should be offered to all patients who are appropriate surgical candidates with potentially resectable disease. While the reasons for which patients did not undergo surgery were not evaluated in the study, the reasons are likely multifactorial. ICC often presents as a large, locally advanced tumor that can make surgery technically challenging, often requiring extensive resection to achieve negative margins. In addition, partial resection of the diaphragm, bile duct reconstruction, and vascular reconstruction were also noted.

    These studies reiterate how extensive resections are often required to obtain R0 margins for of ICC. The use of routine lymphadenectomy is not well defined in ICC resection. While lymphadenectomy is often standard in many Eastern centers, it is not universally performed in many Western countries [ 57 ]. Some investigators, however, argue that the procedure is unnecessary. A retrospective study from Japan which evaluated 68 patients with mass-forming ICC recommended against routine lymphadenectomy as the authors argued that there was survival benefit associated with lymphadenectomy.

    A different retrospective study from China of patients with ICC who underwent surgical resection from to similarly showed no survival benefit among patients who underwent lymphadenectomy and had nodal metastasis [ 59 ]. Lymphadenectomy may, however, be important to accurate stage patients. Multiple studies have noted that overall nodal status N0 versus N1 , as well as the number of nodal metastases, strongly predicts prognosis [ 57 , 60 ].

    N1 disease had an adverse effect on overall survival median survival: A recent retrospective study of patients from Japan similarly reported that lymph node metastasis was a strong, independent prognostic factor of survival , HR: There does seem to be an improvement in overall 5-year survival documented in the past decade, resulting in a cumulative A major concern following surgery for ICC is disease recurrence. In , Choi et al. A different study by Endo et al.

    A larger study of patients who underwent resection for ICC from to found a Recently, a collaboration between 13 major hepatobiliary centers in the US, Europe, and Asia compiled data from patients who underwent surgical resection for ICC from to [ 76 ]. However, association of LN micrometastasis with survival in patients resected for HC without evidence of LN metastasis by traditional histologic examination is controversial.

    In a study by Tojima et al, 31 the rate of LN micrometastasis in N0 patients was Some prognostic factors have been shown to better stratify the prognosis in N1 patients resected for HC, including the LNR 12 , 14 , 16 , 19 and the number of positive LNs. Our multicenter study focused on a unique and specific tumor entity. Patients with intrahepatic cholangiocarcinoma involving the hepatic hilum peri-HC were excluded to evaluate the prognostic association of the LNR in patients with similar long-term outcome.

    To date, few articles 14 , 16 , 19 , 21 have focused on the prognostic effect of the LNR in patients with HC as a unique and specific tumor entity. Results of these studies are controversial, and different LNR cutoff values have been shown to significantly influence survival, ranging from 0. Indeed, patients with an LNR exceeding 0. The accuracy of the LNR has been evaluated in several gastrointestinal tumors and has been increasingly considered an important additional prognostic factor.

    Therefore, the LNR can be considered a simple staging system with strong ability to predict outcome at different institutions with variable LN dissection procedures. However, because the accuracy of the LNR has been largely validated in several tumor types eg, gastric, colorectal, or pancreatic tumors but not in HC, the reason may be that the TLNC in other malignant neoplasms in the gastrointestinal tractare is often larger than those reported in HC.

    With regard to gastric cancer, in a study by Persiani et al 4 of patients who underwent resection, the reported median number of examined LNs was 30 range, As shown by Aoba et al, 21 the median number of harvested nodes in patients resected for HC reported in the Western literature is often small at less than 10 LNs. When the TLNC was 5 or higher, approximately These results are similar to those reported by Aoba et al, 21 whereby the LNR in patients with a TLNC of 16 or higher was significantly smaller than that in patients with a TLNC ranging between 3 and 5 or between 6 and The small TLNC in patients resected for HC results in inaccurate staging of these patients, with differences in OS, and may explain why the accuracy of the LNR has not been largely validated in this type of tumor.

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    In the seventh edition of the TNM classification, 35 the minimum number of harvested nodes required for histologic examination was increased from 3 to 15, but this number does not represent normal clinical practice. Furthermore, an increase in LN retrieval exceeding 5 showed no additional improvement in predicting survival. Five-year OS in patients with 1 to 5 retrieved LNs was significantly lower than that in patients with 6 to 7 retrieved LNs and in patients with 8 or more retrieved LNs These results were confirmed in the ROC curve analysis performed among N0R0 patients, in whom more than 5 LNs retrieved was the most accurate cutoff to predict 5-year OS.

    However, in patients resected for HC, the LNR was influenced by the total number of retrieved LNs, and removal of more than 5 LNs was the minimum number required to be harvested for adequate staging.

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    Dr Ardito had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Critical revision of the manuscript for important intellectual content: Conflict of Interest Disclosures: Prognostic significance of pathologic nodal status in patients with resected pancreatic cancer.

    PubMed Google Scholar Crossref. Lymph node metastasis as a significant prognostic factor in gastric cancer: Increased lymph node yield is associated with improved survival in rectal cancer irrespective of neoadjuvant treatment: Ratio of metastatic lymph nodes: Eur J Surg Oncol.

    Multidisciplinary Care of Patients with Intrahepatic Cholangiocarcinoma: Updates in Management

    Metastatic lymph node ratio as an important prognostic factor in pancreatic ductal adenocarcinoma. The number of metastatic lymph nodes and the ratio between metastatic and examined lymph nodes are independent prognostic factors in esophageal cancer regardless of neoadjuvant chemoradiation or lymphadenectomy extent. The prognostic value of lymph node ratio in a population-based collective of colorectal cancer patients.

    Surgical treatment of hilar cholangiocarcinoma in the new era: J Hepatobiliary Pancreat Sci. Lymph node metastasis from hilar cholangiocarcinoma: Improvement in perioperative and long-term outcome after surgical treatment of hilar cholangiocarcinoma: Lymph node dissection in resectable perihilar cholangiocarcinoma: Prognostic relevance of the lymph node ratio in surgical patients with extrahepatic cholangiocarcinoma. Prognostic significance of lymph node ratio after resection of peri-hilar cholangiocarcinoma. Does the extent of lymphadenectomy, number of lymph nodes, positive lymph node ratio and neutrophil-lymphocyte ratio impact surgical outcome of perihilar cholangiocarcinoma?

    Eur J Gastroenterol Hepatol. Comparison of number versus ratio of positive lymph nodes in the assessment of lymph node status in extrahepatic cholangiocarcinoma. Surgical treatment for digestive cancer: Survival and recurrence free benefits with different lymphadenectomy for resectable gastric cancer: Assessment of nodal status for perihilar cholangiocarcinoma location, number, or ratio of involved nodes. Adequate lymph node assessment for extrahepatic bile duct adenocarcinoma.

    Assessment of nodal status for perihilar cholangiocarcinoma: Intrahepatic cholangioenteric anastomosis in carcinoma of the hilus of the liver.


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    Extended resections for hilar cholangiocarcinoma. Aggressive surgical resection for hilar cholangiocarcinoma: Changes in the surgical approach to hilar cholangiocarcinoma during an year period in a Western single center. Surgery for hilar cholangiocarcinoma: The Blumgart preoperative staging system for hilar cholangiocarcinoma: J Am Coll Surg.

    Surgical treatment of hilar cholangiocarcinoma in a new era: Immunohistochemically demonstrated lymph node micrometastasis and prognosis in patients with otherwise node-negative hilar cholangiocarcinoma. Lymph node ratio after curative surgery for intrahepatic cholangiocarcinoma.

    Correlation between metastatic lymph node ratio and prognosis in patients with extrahepatic cholangiocarcinoma.

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