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Pathogenesis, Diagnosis, and Management of Cholangiocarcinoma SUMERA RIZVI and GREGORY J

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Pathogenesis, Diagnosis, and Management of Cholangiocarcinoma SUMERA RIZVI and GREGORY J GASTROENTEROLOGY 2013;145:1215–1229 REVIEWS IN BASIC AND CLINICAL AND GASTROENTEROLOGY AND HEPATOLOGY REVIEWS PERSPECTIVES Robert F. Schwabe and John W. Wiley, Section Editors Pathogenesis, Diagnosis, and Management of Cholangiocarcinoma SUMERA RIZVI and GREGORY J. GORES Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, Minnesota Cholangiocarcinomas (CCAs) are hepatobiliary can- encasement.3 pCCA is the most common type of CCA. In a cers with features of cholangiocyte differentiation; large series of patients with bile duct cancer, 8% had iCCA, they can be classified anatomically as intrahepatic 50% had pCCA, and 42% had distal CCA.4 CCA has a poor CCA (iCCA), perihilar CCA (pCCA), or distal CCA. prognosis; patients have a median survival of 24 months These subtypes differ not only in their anatomic after diagnosis. The only curative treatment option is sur- location, but in epidemiology, origin, etiology, path- gery, for early stage disease.5 ogenesis, and treatment. The incidence and mortality of iCCA has been increasing over the past 3 decades, Epidemiology and only a low percentage of patients survive until 5 years after diagnosis. Geographic variations in the inci- Cholangiocarcinoma accounts for 3% of all gastro- intestinal tumors. Over the past 3 decades, the overall dence of CCA are related to variations in risk factors. 6 Changes in oncogene and inflammatory signaling path- incidence of CCA appears to have increased. The percent- age of patients who survive 5 years after diagnosis has not ways, as well as genetic and epigenetic alterations and 7,8 chromosome aberrations, have been shown to contribute increased during this time period, remaining at 10%. to the development of CCA. Furthermore, CCAs are In the United States, Hispanics and Asians have the surrounded by a dense stroma that contains many highest incidence of CCA (2.8 per 100,000 and 3.3 per cancer-associated fibroblasts, which promotes their 100,000, respectively), whereas African Americans have the progression. We have gained a better understanding of lowest incidence of CCA (2.1 per 100,000). African Amer- the imaging characteristics of iCCAs and have developed icans also have lower age-adjusted mortality rates advanced cytologic techniques to detect pCCAs. Patients compared with whites (1.4 per 100,000 vs 1.7 per 100,000). Men have a slightly higher incidence of CCA and mortality with iCCAs usually are treated surgically, whereas liver 7 transplantation after neoadjuvant chemoradiation is an from cancer than women. With the exception of patients option for a subset of patients with pCCAs. We review with primary sclerosing cholangitis (PSC), a diagnosis of recent developments in our understanding of the epide- CCA is uncommon before age 40 years. miology and pathogenesis of CCA, along with advances fi in classi cation, diagnosis, and treatment. Abbreviations used in this paper: a-SMA, a-smooth muscle actin; CA19-9, carbohydrate antigen 19-9; CAF, cancer-associated fibroblast; Keywords: Cancer-Associated Fibroblasts; Distal Chol- CCA, cholangiocarcinoma; CT, computed tomography; CXCR4, chemo- angiocarcinoma; Intrahepatic Cholangiocarcinoma; kine (C-X-C motif) receptor 4; dCCA, distal cholangiocarcinoma; ECM, Molecular Pathogenesis. extracellular matrix; EGFP, enhanced green fluorescent protein; EGFR, epidermal growth factor–receptor; EMT, epithelial–mesenchymal tran- sition; ERBB2, v-erb-b2 avian erythroblastic leukemia viral oncogene homolog 2; ERC, endoscopic retrograde cholangiography; ERK, extra- holangiocarcinoma (CCA) is the most common cellular signal regulated kinase; FGFR, fibroblast growth factor receptor; C biliary malignancy and the second most common FISH, fluorescence in situ hybridization; HGF, hepatocyte growth factor; hepatic malignancy after hepatocellular carcinoma (HCC).1 HBV, hepatitis B virus; HCC, hepatocellular carcinoma; HCV, hepatitis C CCAs are epithelial tumors with features of cholangiocyte virus; iCCA, intrahepatic cholangiocarcinoma; IDH, isocitrate dehydro- differentiation. Intrahepatic cholangiocarcinomas (iCCAs) genase; IL 6, interleukin 6; KRAS, Kirsten rat sarcoma viral oncogene homolog; MAPK, mitogen-activated protein kinase; miR, microRNA; are located within the hepatic parenchyma. The second- MCL1, myeloid cell leukemia sequence 1; MET, met proto-oncogene; order bile ducts serve as the point of separation between MMP, matrix metalloproteinase; MRI, magnetic resonance imaging; OR, iCCAs and perihilar CCAs (pCCAs) or distal CCAs odds ratio; pCCA, perihilar cholangiocarcinoma; PDGF, platelet-derived (dCCAs)—the cystic duct is the anatomic boundary between growth factor; PI, phosphatidyl inositol; PI3K, phosphatidylinositol-4,5- these latter 2 subtypes (Figure 1A).2 The Bismuth–Corlette bisphosphate 3-kinase; PSC, primary sclerosing cholangitis; STAT, signal fi fi transducer and activator of transcription; TP53, tumor protein 53. classi cation strati es perihilar tumors on the basis of © 2013 by the AGA Institute biliary involvement. This classification recently was 0016-5085/$36.00 extended to also take into account arterial and venous http://dx.doi.org/10.1053/j.gastro.2013.10.013 1216 RIZVI AND GORES GASTROENTEROLOGY Vol. 145, No. 6 PERSPECTIVES Globally, hepatobiliary malignancies account for 13% of In the West, PSC is the most common predisposing REVIEWS cancer-related deaths; 10%–20% of these are attributable to condition for CCA. Among patients with PSC, the annual AND CCA. The mean age at diagnosis of CCA is 50 years. The risk of development of CCA is 0.5%–1.5%, with a lifetime global incidence of iCCA varies widely, from rates of 113 prevalence of 5%–10%17; CCA is diagnosed within 2 years per 100,000 in Thailand to 0.1 per 100,000 in Australia.9,10 of PSC in most of these patients. A number of potential Differences in the prevalence of genetic and other risk risk factors for CCA in patients with PSC have been factors presumably account for this extensive variation. studied, including smoking and alcohol, although defin- Epidemiologic studies have indicated that the age-adjusted itive data are lacking.8 mortality rate for iCCA is increasing, whereas the mortality Hepatitis B virus (HBV) or hepatitis C virus (HCV) infec- – rate from pCCA and dCCA could be decreasing.9 14 Astudy tion and cirrhosis have been proposed as potential etiologies – of a World Health Organization database reported a sub- of iCCA.23 25 A recent meta-analysis of 11 studies found that stantial global increase in iCCA mortality, with a decreasing cirrhosis, HBV, and HCV were major risk factors for iCCA, trend in mortality from pCCA plus dCCA.15 Although this with odds ratios (ORs) of 22.92, 5.1, and 4.8, respectively.26 A observed increase in the incidence of CCA over the past 30 case-control study from Korea found a significant associa- years has been recorded as an increase in iCCA, it could result tion between HBV (OR, 2.3) and CCA, but not HCV and from misclassification of perihilar tumors as iCCAs.16 Ac- CCA. Cirrhosis also was found to be a significant risk factor cording to the US Surveillance, Epidemiology, and End Re- for CCA, with an OR of 13.6. HCV and cirrhosis were asso- sults database, the age-adjusted incidence rate for iCCA ciated with iCCA in a US case-control study. Compared with increased from 0.59 per 100,000 in 1990 to 0.91 per 100,000 controls, patients with iCCA had a higher prevalence of in 2001. It subsequently decreased to 0.6 per 100,000 by 2007. anti-HCV antibodies, with an OR of 7.9.24 Conversely, the incidence rate for pCCA plus dCCA remained CCA development has been associated with other risk around 0.8 per 100,000 until 2001, and then gradually factors, including inflammatory bowel disease indepen- increased to 0.97 per 100,000 by 2007. Perihilar tumors were dent of PSC, alcohol, smoking, fatty liver disease, diabetes, – coded as iCCAs before 2001 and subsequently were coded as cholelithiasis, and choledocholithiasis.8,27 29 Additional pCCAs after implementation of the third edition of the In- studies have associated variants of genes that regulate ternational Classification of Disease for Oncology. This up- DNA repair, inflammation, and carcinogen metabolism date likely influenced the aforementioned changes in with CCA development.8 Further studies are necessary to incidence rates of both CCA subtypes. Similar trends in the verify these potential associations. incidence of CCA subtypes were noted in the United Kingdom after the change to the third edition of the Inter- national Classification of Disease for Oncology in 2008.6,16 Cells of Origin iCCA is a histologically diverse hepatobiliary ma- lignancy considered to develop from biliary epithelial cells Risk Factors or hepatic progenitor cells (Figure 1B). A recently pro- There are several established risk factors for CCA, posed classification of iCCAs subdivided these tumors and most cases are sporadic.6,8,17 Geographic variations in into the conventional, bile ductular, or intraductal incidence rates of CCA are related in part to variations in neoplasm type, or rare variants (combined hepatocellular risk factors. For example, in Southeast Asia, which has one CCA, undifferentiated type, squamous/adenosquamous of the highest incidence rates of CCA, infection with the type). The conventional type includes small-duct or pe- hepatobiliary flukes Opisthorchis viverrini and Clonorchis ripheral type and large-duct or perihilar type.30 Neural cell sinensis has been associated with the development of CCA. adhesion molecule, a marker of hepatic progenitor cells,
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