Differences in immunohistochemical biomarkers between intra‐ and extrahepatic cholangiocarcinoma: A systematic review and meta‐analysis

Cholangiocarcinomas of different locations differ in growth patterns, symptoms, treatment response, and survival. Still, they are regarded in many studies as a uniform malignancy. Because intra‐ (iCCA) and extrahepatic (eCCA) cholangiocarcinoma display such differences, we performed a systematic review and meta‐analysis to analyze differences in the immunohistochemical profile of these tumors.

[1]  F. T. ten Kate,et al.  Prognostic Biomarkers in Patients with Resected Cholangiocarcinoma: A Systematic Review and Meta-analysis , 2014, Annals of Surgical Oncology.

[2]  N. Sunaga,et al.  Clinical significance of L-type amino acid transporter 1 expression as a prognostic marker and potential of new targeting therapy in biliary tract cancer , 2013, BMC Cancer.

[3]  Jian Li,et al.  Differential Expression of Fascin, E-cadherin and Vimentin: Proteins Associated With Survival of Cholangiocarcinoma Patients , 2013, The American journal of the medical sciences.

[4]  Y. Sakamoto,et al.  Enhancer of Zeste Homolog 2 (EZH2) Promotes Progression of Cholangiocarcinoma Cells by Regulating Cell Cycle and Apoptosis , 2013, Annals of Surgical Oncology.

[5]  Shu-guang Wang,et al.  Aberrant expression of GATA binding protein 6 correlates with poor prognosis and promotes metastasis in cholangiocarcinoma. , 2013, European journal of cancer.

[6]  S. Maithel,et al.  Excision repair cross‐complementing gene‐1, ribonucleotide reductase subunit M1, ribonucleotide reductase subunit M2, and human equilibrative nucleoside transporter‐1 expression and prognostic value in biliary tract malignancy , 2013, Cancer.

[7]  Y. Jeng,et al.  S100P immunostaining identifies a subset of peripheral‐type intrahepatic cholangiocarcinomas with morphological and molecular features similar to those of perihilar and extrahepatic cholangiocarcinomas , 2012, Histopathology.

[8]  D. Gouma,et al.  Survival analysis and prognostic nomogram for patients undergoing resection of extrahepatic cholangiocarcinoma. , 2012, Annals of oncology : official journal of the European Society for Medical Oncology.

[9]  Y. Murakami,et al.  Human Equilibrative Nucleoside Transporter 1 Expression Predicts Survival of Advanced Cholangiocarcinoma Patients Treated With Gemcitabine-Based Adjuvant Chemotherapy After Surgical Resection , 2012, Annals of surgery.

[10]  T. Roskams,et al.  Histological diversity in cholangiocellular carcinoma reflects the different cholangiocyte phenotypes , 2012, Hepatology.

[11]  M. Rugge,et al.  Nuclear expression of S100A4 calcium‐binding protein increases cholangiocarcinoma invasiveness and metastasization , 2011, Hepatology.

[12]  C. Tudur-Smith,et al.  Meta-analysis of immunohistochemical prognostic markers in resected pancreatic cancer , 2011, British Journal of Cancer.

[13]  N. Jamieson,et al.  Tissue Biomarkers for Prognosis in Pancreatic Ductal Adenocarcinoma: A Systematic Review and Meta-analysis , 2011, Clinical Cancer Research.

[14]  A. Bardelli,et al.  Targeting EGFR/HER2 pathways enhances the antiproliferative effect of gemcitabine in biliary tract and gallbladder carcinomas , 2010, BMC Cancer.

[15]  N. Probst-Hensch,et al.  Cell adhesion molecules P-cadherin and CD24 are markers for carcinoma and dysplasia in the biliary tract. , 2010, Human pathology.

[16]  Michele Tarsilla Cochrane Handbook for Systematic Reviews of Interventions , 2010, Journal of MultiDisciplinary Evaluation.

[17]  A. Zhu,et al.  Genetics of biliary tract cancers and emerging targeted therapies. , 2010, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[18]  C. Subimerb,et al.  Tissue invasive macrophage density is correlated with prognosis in cholangiocarcinoma. , 2010, Molecular medicine reports.

[19]  Didier Samuel,et al.  Identification of Cellular Targets in Human Intrahepatic Cholangiocarcinoma Using Laser Microdissection and Accurate Mass and Time Tag Proteomics* , 2010, Molecular & Cellular Proteomics.

[20]  M. Koch,et al.  Meta-analysis shows that detection of circulating tumor cells indicates poor prognosis in patients with colorectal cancer. , 2010, Gastroenterology.

[21]  D. Cunningham,et al.  Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. , 2010, The New England journal of medicine.

[22]  S. Kakar,et al.  Epidermal growth factor receptor and HER-2/neu status by immunohistochemistry and fluorescence in situ hybridization in adenocarcinomas of the biliary tree and gallbladder. , 2010, Human pathology.

[23]  K. Schmid,et al.  Metallothionein overexpression and its prognostic relevance in intrahepatic cholangiocarcinoma and extrahepatic hilar cholangiocarcinoma (Klatskin tumors). , 2009, Human pathology.

[24]  N. Probst-Hensch,et al.  IMP3 expression in lesions of the biliary tract: a marker for high-grade dysplasia and an independent prognostic factor in bile duct carcinomas. , 2009, Human pathology.

[25]  H. Honda,et al.  CD10+ fibroblasts are more involved in the progression of hilar/extrahepatic cholangiocarcinoma than of peripheral intrahepatic cholangiocarcinoma , 2009, Histopathology.

[26]  K. Jang,et al.  Expression of MUC1, MUC2, MUC5AC and MUC6 in cholangiocarcinoma: prognostic impact. , 2009, Oncology reports.

[27]  M. Asaka,et al.  Fascin is involved in tumor necrosis factor-α-dependent production of MMP9 in cholangiocarcinoma , 2009, Laboratory Investigation.

[28]  V. Paradis,et al.  Comparative protein expression profiles of hilar and peripheral hepatic cholangiocarcinomas. , 2009, Journal of hepatology.

[29]  N. Probst-Hensch,et al.  Golgi phosphoprotein 2 (GOLPH2) expression in liver tumors and its value as a serum marker in hepatocellular carcinomas , 2009, Hepatology.

[30]  M. Bracken,et al.  Tissue biomarkers for prognosis in cutaneous melanoma: a systematic review and meta-analysis. , 2009, Journal of the National Cancer Institute.

[31]  Y. Jeng,et al.  Nuclear Overexpression of Mitotic Regulatory Proteins in Biliary Tract Cancer: Correlation with Clinicopathologic Features and Patient Survival , 2009, Cancer Epidemiology Biomarkers & Prevention.

[32]  A. Jarry,et al.  N-cadherin serves as diagnostic biomarker in intrahepatic and perihilar cholangiocarcinomas , 2009, Modern Pathology.

[33]  H. Moch,et al.  Frequent expression of the novel cancer testis antigen MAGE‐C2/CT‐10 in hepatocellular carcinoma , 2009, International journal of cancer.

[34]  L. Terracciano,et al.  Clinical significance of cell cycle- and apoptosis-related markers in biliary tract cancer: a tissue microarray-based approach revealing a distinctive immunophenotype for intrahepatic and extrahepatic cholangiocarcinomas. , 2008, American journal of clinical pathology.

[35]  C. Su,et al.  Glycine N‐methyltransferase is a favorable prognostic marker for human cholangiocarcinoma , 2008, Journal of gastroenterology and hepatology.

[36]  W. Jochum,et al.  Rare PIK3CA hotspot mutations in carcinomas of the biliary tract , 2008, Genes, chromosomes & cancer.

[37]  B. Li,et al.  Inverse correlation of aberrant expression of fragile histidine triad (FHIT) protein with cyclin D1 protein and prognosis in Chinese patients with cholangiocarcinoma , 2008, Acta oncologica.

[38]  S. Hirohashi,et al.  Clinicopathological and prognostic significance of EGFR, VEGF, and HER2 expression in cholangiocarcinoma , 2007, British Journal of Cancer.

[39]  T. Gruenberger,et al.  Activated Mammalian Target of Rapamycin Is an Adverse Prognostic Factor in Patients with Biliary Tract Adenocarcinoma , 2007, Clinical Cancer Research.

[40]  Y. Jeng,et al.  Expression of the caudal‐type homeodomain transcription factor CDX2 is related to clinical outcome in biliary tract carcinoma , 2007, Journal of gastroenterology and hepatology.

[41]  Xin Chen,et al.  Podocalyxin-like protein 1 expression is useful to differentiate pancreatic ductal adenocarcinomas from adenocarcinomas of the biliary and gastrointestinal tracts. , 2007, Human pathology.

[42]  C. Pairojkul,et al.  Expression of phosphorylated ERK1/2 and homeodomain protein CDX2 in cholangiocarcinoma , 2006, Journal of Cancer Research and Clinical Oncology.

[43]  C. Pairojkul,et al.  Liver fluke-associated and sporadic cholangiocarcinoma: an immunohistochemical study of bile duct, peribiliary gland and tumour cell phenotypes , 2006, Journal of Clinical Pathology.

[44]  Douglas G Altman,et al.  Reporting recommendations for tumor marker prognostic studies. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[45]  H. Fujii,et al.  Amplification and overexpression of c‐erbB‐2, epidermal growth factor receptor, and c‐met in biliary tract cancers , 2005, The Journal of pathology.

[46]  M. Gonen,et al.  Differential cell cycle-regulatory protein expression in biliary tract adenocarcinoma: correlation with anatomic site, pathologic variables, and clinical outcome. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[47]  M. Fiorentino,et al.  Expression of connective tissue growth factor is a prognostic marker for patients with intrahepatic cholangiocarcinoma. , 2005, Digestive and liver disease : official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver.

[48]  P. Argani,et al.  Regulators of apoptosis in cholangiocarcinoma. , 2005, Archives of pathology & laboratory medicine.

[49]  K. Mizumoto,et al.  Immunohistochemical Study of DPC4 and p53 Proteins in Gallbladder and Bile Duct Cancers , 2004, World Journal of Surgery.

[50]  K. Tsuneyama,et al.  Expression of MAGE‐A3 in intrahepatic cholangiocarcinoma and its precursor lesions , 2004, Pathology international.

[51]  Y. Maehara,et al.  Decreased expression of osteopontin is related to tumor aggressiveness and clinical outcome of intrahepatic cholangiocarcinoma , 2004, Liver international : official journal of the International Association for the Study of the Liver.

[52]  Kohzoh Imai,et al.  MUC4 is a novel prognostic factor of intrahepatic cholangiocarcinoma‐mass forming type , 2004, Hepatology.

[53]  D. Altman,et al.  Measuring inconsistency in meta-analyses , 2003, BMJ : British Medical Journal.

[54]  E. Montgomery,et al.  Loss of Stk11/Lkb1 Expression in Pancreatic and Biliary Neoplasms , 2003, Modern Pathology.

[55]  H. Lee,et al.  Expression of Mucins and Cytokeratins in Primary Carcinomas of the Digestive System , 2003, Modern Pathology.

[56]  T. Oshikiri,et al.  Caveolin-I overexpression is a favourable prognostic factor for patients with extrahepatic bile duct carcinoma. , 2003, British journal of cancer.

[57]  K. Sugimachi,et al.  The Utility of Keratin 903 as a New Prognostic Marker in Mass-Forming-Type Intrahepatic Cholangiocarcinoma , 2002, Modern Pathology.

[58]  S. Zou,et al.  Expression of cyclooxygenase-1 and -2 in extra-hepatic cholangiocarcinoma. , 2002, Hepatobiliary & pancreatic diseases international : HBPD INT.

[59]  H. Mitomi,et al.  Significant correlations of E-cadherin, catenin, and CD44 variant form expression with carcinoma cell differentiation and prognosis of extrahepatic bile duct carcinomas. , 2001, American journal of clinical pathology.

[60]  R. Hruban,et al.  Differing rates of loss of DPC4 expression and of p53 overexpression among carcinomas of the proximal and distal bile ducts , 2001, Cancer.

[61]  J. Hirabayashi,et al.  Expression of endogenous galectin-1 and galectin-3 in intrahepatic cholangiocarcinoma. , 2001, Human pathology.

[62]  K. Tsuneyama,et al.  Up‐regulation of Fas ligand at early stages and down‐regulation of Fas at progressed stages of intrahepatic cholangiocarcinoma reflect evasion from immune surveillance , 2000, Hepatology.

[63]  Y. Nakanuma,et al.  Cytokeratin profile relates to histological subtypes and intrahepatic location of intrahepatic cholangiocarcinoma and primary sites of metastatic adenocarcinoma of liver , 2000, Histopathology.

[64]  B. le Bail,et al.  Cytokeratin 7 and 20 expression in cholangiocarcinomas varies along the biliary tract but still differs from that in colorectal carcinoma metastasis. , 2000, The American journal of surgical pathology.

[65]  M. Monden,et al.  ets-1 Expression in Extrahepatic Bile Duct Carcinoma and Cholangiocellular Carcinoma , 2000, Oncology.

[66]  G. Gores,et al.  Biliary tract cancers. , 1999, The New England journal of medicine.

[67]  Harada,et al.  Protein expression and genetic alterations of p53 and ras in intrahepatic cholangiocarcinoma , 1999, Histopathology.

[68]  D Tripathy,et al.  Phase II study of receptor-enhanced chemosensitivity using recombinant humanized anti-p185HER2/neu monoclonal antibody plus cisplatin in patients with HER2/neu-overexpressing metastatic breast cancer refractory to chemotherapy treatment. , 1998, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[69]  M. Shrestha,et al.  Prognostic significance of Ki-67 and p53 antigen expression in carcinomas of bile duct and gallbladder. , 1998, The journal of medical investigation : JMI.

[70]  G. Smith,et al.  Bias in meta-analysis detected by a simple, graphical test , 1997, BMJ.

[71]  D. Sackett,et al.  Cochrane Collaboration , 1994, BMJ.

[72]  N. Laird,et al.  Meta-analysis in clinical trials. , 1986, Controlled clinical trials.

[73]  A. Warth,et al.  BRAF V600E-specific immunohistochemistry reveals low mutation rates in biliary tract cancer and restriction to intrahepatic cholangiocarcinoma , 2014, Modern Pathology.

[74]  N. Probst-Hensch,et al.  Expression of the extracellular matrix protein periostin in liver tumours and bile duct carcinomas. , 2010, Histopathology.

[75]  H. Nagura,et al.  Immunohistochemistry of carcinoembryonic antigen, secretory component and lysozyme in benign and malignant common bile duct tissues , 2004, Virchows Archiv A.

[76]  G. Gores,et al.  Clinicopathological correlates of aspartyl (asparaginyl) beta-hydroxylase over-expression in cholangiocarcinoma. , 2004, Cancer detection and prevention.

[77]  S. Fan,et al.  Intrahepatic Cholangiocarcinoma , 1997, World Journal of Surgery.