European Journal of Cancer
Volume 45, Issue 1 , Pages 33-47 , January 2009

Prognostic molecular markers in cholangiocarcinoma: A systematic review

  • Christopher D. Briggs

      Affiliations

    • Cancer Biomarkers and Prevention Group, Department of Cancer Studies and Molecular Medicine, Biocentre, University of Leicester, University Road, Leicester LE1 7RH, United Kingdom
    • Corresponding Author InformationCorresponding author: Tel.: +44 07980748257; fax: +44 0116 2231840.
    • ,
  • Christopher P. Neal

      Affiliations

    • Cancer Biomarkers and Prevention Group, Department of Cancer Studies and Molecular Medicine, Biocentre, University of Leicester, University Road, Leicester LE1 7RH, United Kingdom
    • ,
  • Christopher D. Mann

      Affiliations

    • Cancer Biomarkers and Prevention Group, Department of Cancer Studies and Molecular Medicine, Biocentre, University of Leicester, University Road, Leicester LE1 7RH, United Kingdom
    • ,
  • William P. Steward

      Affiliations

    • Cancer Biomarkers and Prevention Group, Department of Cancer Studies and Molecular Medicine, Biocentre, University of Leicester, University Road, Leicester LE1 7RH, United Kingdom
    • ,
  • Margaret M. Manson

      Affiliations

    • Cancer Biomarkers and Prevention Group, Department of Cancer Studies and Molecular Medicine, Biocentre, University of Leicester, University Road, Leicester LE1 7RH, United Kingdom
    • ,
  • David P. Berry

      Affiliations

    • Department of Hepatobiliary and Pancreatic Surgery, Leicester General Hospital, University Hospitals of Leicester, Gwendolen Road, Leicester LE5 4PW, United Kingdom

Received 17 April 2008 ,Revised 6 August 2008 ,Accepted 26 August 2008.

References 

  1. West J, Wood H, Logan RF, Quinn M, Aithal GP. Trends in the incidence of primary liver and biliary tract cancers in England and Wales 1971–2001. Br J Cancer. 2006;94(11):1751–1758
  2. Taylor-Robinson SD, Toledano MB, Arora S, et al. Increase in mortality rates from intrahepatic cholangiocarcinoma in England and Wales 1968–1998. Gut. 2001;48(6):816–820
  3. Patel T. Increasing incidence and mortality of primary intrahepatic cholangiocarcinoma in the United States. Hepatology. 2001;33(6):1353–1357
  4. Malhi H, Gores GJ. Cholangiocarcinoma: modern advances in understanding a deadly old disease. J Hepatol. 2006;45(6):856–867
  5. Khan SA, Davidson BR, Goldin R, et al. Guidelines for the diagnosis and treatment of cholangiocarcinoma: consensus document. Gut. 2002;51(Suppl. 6):VII-9
  6. Su CH, Tsay SH, Wu CC, et al. Factors influencing postoperative morbidity, mortality, and survival after resection for hilar cholangiocarcinoma. Ann Surg. 1996;223(4):384–394
  7. Cameron JL, Pitt HA, Zinner MJ, Kaufman SL, Coleman J. Management of proximal cholangiocarcinomas by surgical resection and radiotherapy. Am J Surg. 1990;159(1):91–97[discussion 97–8]
  8. Nimura Y, Hayakawa N, Kamiya J, Kondo S, Shionoya S. Hepatic segmentectomy with caudate lobe resection for bile duct carcinoma of the hepatic hilus. World J Surg. 1990;14(4):535–543[discussion 544]
  9. Nakeeb A, Tran KQ, Black MJ, et al. Improved survival in resected biliary malignancies. Surgery. 2002;132(4):555–563[discussion 563–64]
  10. Feng Z, Hu W, Rajagopal G, Levine AJ. The tumor suppressor p53: cancer and aging. Cell Cycle. 2008;7(7):842–847
  11. Havlik R, Sbisa E, Tullo A, et al. Results of resection for hilar cholangiocarcinoma with analysis of prognostic factors. Hepatogastroenterology. 2000;47(34):927–931
  12. Tannapfel A, Weinans L, Geissler F, et al. Mutations of p53 tumor suppressor gene, apoptosis, and proliferation in intrahepatic cholangiocellular carcinoma of the liver. Dig Dis Sci. 2000;45(2):317–324
  13. Liu XF, Zhang H, Zhu SG, et al. Correlation of p53 gene mutation and expression of P53 protein in cholangiocarcinoma. World J Gastroenterol. 2006;12(29):4706–4709
  14. Limpaiboon T, Krissadarak K, Sripa B, et al. Microsatellite alterations in liver fluke related cholangiocarcinoma are associated with poor prognosis. Cancer Lett. 2002;181(2):215–222
  15. Jenkins JR, Rudge K, Chumakov P, Currie GA. The cellular oncogene p53 can be activated by mutagenesis. Nature. 1985;317(6040):816–818
  16. Kuroda Y, Aishima S, Taketomi A, et al. 14-3-3sigma negatively regulates the cell cycle, and its down-regulation is associated with poor outcome in intrahepatic cholangiocarcinoma. Hum Pathol. 2007;38(7):1014–1022
  17. Hoang MP, Murakata LA, Katabi N, Henson DE, Albores-Saavedra J. Invasive papillary carcinomas of the extrahepatic bile ducts: a clinicopathologic and immunohistochemical study of 13 cases. Mod Pathol. 2002;15(12):1251–1258
  18. Li X, Hui A, Takayama T, Cui X, Shi Y, Makuuchi M. Altered p21(WAF1/CIP1) expression is associated with poor prognosis in extrahepatic bile duct carcinoma. Cancer Lett. 2000;154(1):85–91
  19. Albores-Saavedra J, Murakata L, Krueger JE, Henson DE. Noninvasive and minimally invasive papillary carcinomas of the extrahepatic bile ducts. Cancer. 2000;89(3):508–515
  20. Arora DS, Ramsdale J, Lodge JP, Wyatt JI. p53 but not bcl-2 is expressed by most cholangiocarcinomas: a study of 28 cases. Histopathology. 1999;34(6):497–501
  21. Kim HJ, Yun SS, Jung KH, Kwun WH, Choi JH. Intrahepatic cholangiocarcinoma in Korea. J Hepatobiliary Pancreat Surg. 1999;6(2):142–148
  22. Shrestha ML, Miyake H, Kikutsuji T, Tashiro S. Prognostic significance of Ki-67 and p53 antigen expression in carcinomas of bile duct and gallbladder. J Med Invest. 1998;45(1–4):95–102
  23. Suto T, Sugai T, Nakamura S, et al. Assessment of the expression of p53, MIB-1 (Ki-67 antigen), and argyrophilic nucleolar organizer regions in carcinoma of the extrahepatic bile duct. Cancer. 1998;82(1):86–95
  24. Washington K, Gottfried MR. Expression of p53 in adenocarcinoma of the gallbladder and bile ducts. Liver. 1996;16(2):99–104
  25. Ahrendt SA, Rashid A, Chow JT, Eisenberger CF, Pitt HA, Sidransky D. p53 overexpression and k-ras gene mutations in primary sclerosing cholangitis-associated biliary tract cancer. J Hepatobiliary Pancreat Surg. 2000;7(4):426–431
  26. Rijken AM, Offerhaus GJ, Polak MM, Gouma DJ, van Gulik TM. P53 expression as a prognostic determinant in resected distal bile duct carcinoma. Eur J Surg Oncol. 1999;25(3):297–301
  27. Takamori S, Yoshimoto J, Kojima K, Matsumoto T, Beppu T, Futagawa S. Prognostic implication and intratumoral heterogeneity of p53, Ki-67, CEA and CA19-9 expressions in cholangiocellular carcinoma. Hepatol Res. 1997;8(2):81–94
  28. Diamantis I, Karamitopoulou E, Perentes E, Zimmermann A. p53 protein immunoreactivity in extrahepatic bile duct and gallbladder cancer: correlation with tumor grade and survival. Hepatology. 1995;22(3):774–779
  29. Cheng Q, Luo X, Zhang B, Jiang X, Yi B, Wu M. Distal bile duct carcinoma: prognostic factors after curative surgery. A series of 112 cases. Ann Surg Oncol. 2007;14(3):1212–1219
  30. Argani P, Shaukat A, Kaushal M, et al. Differing rates of loss of DPC4 expression and of p53 overexpression among carcinomas of the proximal and distal bile ducts. Cancer. 2001;91(7):1332–1341
  31. Ross S, Hill CS. How the smads regulate transcription. Int J Biochem Cell Biol. 2008;40(3):383–408
  32. Sun A, Bagella L, Tutton S, Romano G, Giordano A. From G0 to S phase: a view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway. J Cell Biochem. 2007;102(6):1400–1404
  33. Tannapfel A, Sommerer F, Benicke M, et al. Genetic and epigenetic alterations of the INK4a-ARF pathway in cholangiocarcinoma. J Pathol. 2002;197(5):624–631
  34. Cui X, Hui AM, Li X, et al. Alterations of retinoblastoma protein and p16INK4 protein expression in extrahepatic bile duct carcinomas. Hepatogastroenterology. 2000;47(35):1216–1220
  35. Buhlmann S, Putzer BM. DNp73 a matter of cancer: mechanisms and clinical implications. Biochim Biophys Acta. 2008;1785(2):207–216
  36. Tannapfel A, Engeland K, Weinans L, et al. Expression of p73, a novel protein related to the p53 tumour suppressor p53, and apoptosis in cholangiocellular carcinoma of the liver. Br J Cancer. 1999;80(7):1069–1074
  37. Rodriguez-Viciana P, Tetsu O, Oda K, Okada J, Rauen K, McCormick F. Cancer targets in the Ras pathway. Cold Spring Harb Symp Quant Biol. 2005;70:461–467
  38. Isa T, Tomita S, Nakachi A, et al. Analysis of microsatellite instability, K-ras gene mutation and p53 protein overexpression in intrahepatic cholangiocarcinoma. Hepatogastroenterology. 2002;49(45):604–608
  39. Rijken AM, van Gulik TM, Polak MM, Sturm PD, Gouma DJ, Offerhaus GJ. Diagnostic and prognostic value of incidence of K-ras codon 12 mutations in resected distal bile duct carcinoma. J Surg Oncol. 1998;68(3):187–192
  40. Lee CS. Ras p21 protein immunoreactivity and its relationship to p53 expression and prognosis in gallbladder and extrahepatic biliary carcinoma. Eur J Surg Oncol. 1997;23(3):233–237
  41. Tannapfel A, Benicke M, Katalinic A, et al. Frequency of p16(INK4A) alterations and K-ras mutations in intrahepatic cholangiocarcinoma of the liver. Gut. 2000;47(5):721–727
  42. Miettinen M, Lasota J. KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl Immunohistochem Mol Morphol. 2005;13(3):205–220
  43. Hong SM, Hwang I, Song DE, Choi J, Yu E. Clinical and prognostic significances of nuclear and cytoplasmic KIT expressions in extrahepatic bile duct carcinomas. Mod Pathol. 2007;20(5):562–569
  44. Del Gaizo Moore V, Letai A. Rational design of therapeutics targeting the BCL-2 family: are some cancer cells primed for death but waiting for a final push?. Adv Exp Med Biol. 2008;615:159–175
  45. Romani AA, Soliani P, Desenzani S, Borghetti AF, Crafa P. The associated expression of Maspin and Bax proteins as a potential prognostic factor in intrahepatic cholangiocarcinoma. BMC Cancer. 2006;6:255
  46. Gozuacik D, Kimchi A. DAPk protein family and cancer. Autophagy. 2006;2(2):74–79
  47. Tozawa T, Tamura G, Honda T, et al. Promoter hypermethylation of DAP-kinase is associated with poor survival in primary biliary tract carcinoma patients. Cancer Sci. 2004;95(9):736–740
  48. Whiteside TL. The role of death receptor ligands in shaping tumor microenvironment. Immunol Invest. 2007;36(1):25–46
  49. Murakami M, Sasaki T, Miyata H, Yamasaki S, Kuwahara K, Chayama K. Fas and Fas ligand: expression and soluble circulating levels in bile duct carcinoma. Oncol Rep. 2004;11(6):1183–1186
  50. Shimonishi T, Isse K, Shibata F, 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. Hepatology. 2000;32(4 Pt 1):761–769
  51. Pennati M, Folini M, Zaffaroni N. Targeting survivin in cancer therapy. Expert Opin Ther Targets. 2008;12(4):463–476
  52. Miyachi K, Sasaki K, Onodera S, et al. Correlation between survivin mRNA expression and lymph node metastasis in gastric cancer. Gastric cancer. 2003;6(4):217–224
  53. Schultz IJ, Kiemeney LA, Witjes JA, et al. Survivin mRNA expression is elevated in malignant urothelial cell carcinomas and predicts time to recurrence. Anticancer Res. 2003;23(4):3327–3331
  54. Cohen C, Lohmann CM, Cotsonis G, Lawson D, Santoianni R. Survivin expression in ovarian carcinoma: correlation with apoptotic markers and prognosis. Mod Pathol. 2003;16(6):574–583
  55. Javle MM, Tan D, Yu J, et al. Nuclear survivin expression predicts poor outcome in cholangiocarcinoma. Hepatogastroenterology. 2004;51(60):1653–1657
  56. Sharma PS, Sharma R, Tyagi R. Inhibitors of cyclin dependent kinases: useful targets for cancer treatment. Curr Cancer Drug Targets. 2008;8(1):53–75
  57. Hui AM, Cui X, Makuuchi M, Li X, Shi YZ, Takayama T. Decreased p27(Kip1) expression and cyclin D1 overexpression, alone and in combination, influence recurrence and survival of patients with resectable extrahepatic bile duct carcinoma. Hepatology. 1999;30(5):1167–1173
  58. Sugimachi K, Aishima S, Taguchi K, et al. The role of overexpression and gene amplification of cyclin D1 in intrahepatic cholangiocarcinoma. J Hepatol. 2001;35(1):74–79
  59. Fiorentino M, Altimari A, D’Errico A, et al. Low p27 expression is an independent predictor of survival for patients with either hilar or peripheral intrahepatic cholangiocarcinoma. Clin Cancer Res. 2001;7(12):3994–3999
  60. Taguchi K, Aishima S, Asayama Y, et al. The role of p27kip1 protein expression on the biological behavior of intrahepatic cholangiocarcinoma. Hepatology. 2001;33(5):1118–1123
  61. Shibahara H, Tamada S, Higashi M, et al. MUC4 is a novel prognostic factor of intrahepatic cholangiocarcinoma-mass forming type. Hepatology. 2004;39(1):220–229
  62. Tamada S, Shibahara H, Higashi M, et al. MUC4 is a novel prognostic factor of extrahepatic bile duct carcinoma. Clin Cancer Res. 2006;12(14 Pt 1):4257–4264
  63. Canepa ET, Scassa ME, Ceruti JM, et al. INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life. 2007;59(7):419–426
  64. Hong SM, Choi J, Ryu K, Ro JY, Yu E. Promoter hypermethylation of the p16 gene and loss of its protein expression is correlated with tumor progression in extrahepatic bile duct carcinomas. Arch Pathol Lab Med. 2006;130(1):33–38
  65. Ichikawa K, Imura J, Kawamata H, Takeda J, Fujimori T. Down-regulated p16 expression predicts poor prognosis in patients with extrahepatic biliary tract carcinomas. Int J Oncol. 2002;20(3):453–461
  66. Nishida T, Nakao K, Hamaji M, Nakahara MA, Tsujimoto M. Prognostic significance of proliferative cell nuclear antigen in carcinoma of the extrahepatic bile duct. World J Surg. 1997;21(6):634–639
  67. Yamada Y, Yamauchi H, Kakizaki K, Suzuki H. Expression of Ki-67 by monoclonal antibody MIB-1 in carcinoma of the middle and lower bile duct. Tohoku J Exp Med. 1995;177(4):375–377
  68. Rijken AM, Umezawa A, van Gulik TM, et al. Prognostic value of cell proliferation (Ki-67 antigen) and nuclear DNA content in clinically resectable, distal bile duct carcinoma. Ann Surg Oncol. 1998;5(8):699–705
  69. Aishima S, Kuroda Y, Nishihara Y, et al. Gastric mucin phenotype defines tumour progression and prognosis of intrahepatic cholangiocarcinoma: gastric foveolar type is associated with aggressive tumour behaviour. Histopathology. 2006;49(1):35–44
  70. Uberall I, Kolar Z, Trojanec R, Berkovcova J, Hajduch M. The status and role of ErbB receptors in human cancer. Exp Mol Pathol. 2008;84(2):79–89
  71. Javle MM, Yu J, Khoury T, et al. Akt expression may predict favorable prognosis in cholangiocarcinoma. J Gastroenterol Hepatol. 2006;21(11):1744–1751
  72. Gwak GY, Yoon JH, Shin CM, et al. Detection of response-predicting mutations in the kinase domain of the epidermal growth factor receptor gene in cholangiocarcinomas. J Cancer Res Clin Oncol. 2005;131(10):649–652
  73. Vogel CL, Cobleigh MA, Tripathy D, et al. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol. 2002;20(3):719–726
  74. Kim HJ, Yoo TW, Park DI, et al. Gene amplification and protein overexpression of HER-2/neu in human extrahepatic cholangiocarcinoma as detected by chromogenic in situ hybridization and immunohistochemistry: its prognostic implication in node-positive patients. Ann Oncol. 2007;18(5):892–897
  75. Ogo Y, Nio Y, Yano S, et al. Immunohistochemical expression of HER-1 and HER-2 in extrahepatic biliary carcinoma. Anticancer Res. 2006;26(1B):763–770
  76. Orend G. Potential oncogenic action of tenascin-C in tumorigenesis. Int J Biochem Cell Biol. 2005;37(5):1066–1083
  77. Aishima S, Taguchi K, Terashi T, Matsuura S, Shimada M, Tsuneyoshi M. Tenascin expression at the invasive front is associated with poor prognosis in intrahepatic cholangiocarcinoma. Mod Pathol. 2003;16(10):1019–1027
  78. Yeger H, Perbal B. The CCN family of genes: a perspective on CCN biology and therapeutic potential. J Cell Commun Signal. 2007;1(3–4):159–164
  79. Gardini A, Corti B, Fiorentino M, et al. Expression of connective tissue growth factor is a prognostic marker for patients with intrahepatic cholangiocarcinoma. Dig Liver Dis. 2005;37(4):269–274
  80. Bleau AM, Planque N, Perbal B. CCN proteins and cancer: two to tango. Front Biosci. 2005;10:998–1009
  81. Davies SR, Watkins G, Mansel RE, Jiang WG. Differential expression and prognostic implications of the CCN family members WISP-1, WISP-2, and WISP-3 in human breast cancer. Ann Surg Oncol. 2007;14(6):1909–1918
  82. Tanaka S, Sugimachi K, Kameyama T, et al. Human WISP1v, a member of the CCN family, is associated with invasive cholangiocarcinoma. Hepatology. 2003;37(5):1122–1129
  83. Hirohashi S, Kanai Y. Cell adhesion system and human cancer morphogenesis. Cancer Sci. 2003;94(7):575–581
  84. Hugo H, Ackland ML, Blick T, et al. Epithelial–mesenchymal and mesenchymal–epithelial transitions in carcinoma progression. J Cell Physiol. 2007;213(2):374–383
  85. Mikami T, Saegusa M, Mitomi H, Yanagisawa N, Ichinoe M, Okayasu I. Significant correlations of E-cadherin, catenin, and CD44 variant form expression with carcinoma cell differentiation and prognosis of extrahepatic bile duct carcinomas. Am J Clin Pathol. 2001;116(3):369–376
  86. Inki P, Jalkanen M. The role of syndecan-1 in malignancies. Ann Med. 1996;28(1):63–67
  87. Harada K, Masuda S, Hirano M, Nakanuma Y. Reduced expression of syndecan-1 correlates with histologic dedifferentiation, lymph node metastasis, and poor prognosis in intrahepatic cholangiocarcinoma. Hum Pathol. 2003;34(9):857–863
  88. Kuespert K, Pils S, Hauck CR. CEACAMs: their role in physiology and pathophysiology. Curr Opin Cell Biol. 2006;18(5):565–571
  89. Ieta K, Tanaka F, Utsunomiya T, Kuwano H, Mori M. CEACAM6 gene expression in intrahepatic cholangiocarcinoma. Br J Cancer. 2006;95(4):532–540
  90. Friederichs J, Zeller Y, Hafezi-Moghadam A, Grone HJ, Ley K, Altevogt P. The CD24/P-selectin binding pathway initiates lung arrest of human A125 adenocarcinoma cells. Cancer Res. 2000;60(23):6714–6722
  91. Aigner S, Ramos CL, Hafezi-Moghadam A, et al. CD24 mediates rolling of breast carcinoma cells on P-selectin. Faseb J. 1998;12(12):1241–1251
  92. Su MC, Hsu C, Kao HL, Jeng YM. CD24 expression is a prognostic factor in intrahepatic cholangiocarcinoma. Cancer Lett. 2006;235(1):34–39
  93. Agrawal S, Kuvshmoff BW, Khoury T, et al. CD24 expression is an independent prognostic marker in cholangiocarcinoma. J Gastrointest Surg. 2007;11(4):445–451
  94. Yasuda M, Nakano K, Yasumoto K, Tanaka Y. CD44: functional relevance to inflammation and malignancy. Histol Histopathol. 2002;17(3):945–950
  95. Yokoyama Y, Hiyama E, Murakami Y, Matsuura Y, Yokoyama T. Lack of CD44 variant 6 expression in advanced extrahepatic bile duct/ampullary carcinoma. Cancer. 1999;86(9):1691–1699
  96. Chambers AF, Matrisian LM. Changing views of the role of matrix metalloproteinases in metastasis. J Natl Cancer Inst. 1997;89(17):1260–1270
  97. Miwa S, Miyagawa S, Soeda J, Kawasaki S. Matrix metalloproteinase-7 expression and biologic aggressiveness of cholangiocellular carcinoma. Cancer. 2002;94(2):428–434
  98. Park BK, Paik YH, Park JY, et al. The clinicopathologic significance of the expression of vascular endothelial growth factor-C in intrahepatic cholangiocarcinoma. Am J Clin Oncol – Cancer Clin Trials. 2006;29(2):138–142
  99. Tang D, Nagano H, Yamamoto H, et al. Angiogenesis in cholangiocellular carcinoma: expression of vascular endothelial growth factor, angiopoietin-1/2, thrombospondin-1 and clinicopathological significance. Oncol Rep. 2006;15(3):525–532
  100. Sasaki M, Ikeda H, Nakanuma Y. Expression profiles of MUC mucins and trefoil factor family (TFF) peptides in the intrahepatic biliary system: physiological distribution and pathological significance. Prog Histochem Cytochem. 2007;42(2):61–110
  101. Higashi M, Yonezawa S, Ho JJ, et al. Expression of MUC1 and MUC2 mucin antigens in intrahepatic bile duct tumors: its relationship with a new morphological classification of cholangiocarcinoma. Hepatology. 1999;30(6):1347–1355
  102. Matsumura N, Yamamoto M, Aruga A, Takasaki K, Nakano M. Correlation between expression of MUC1 core protein and outcome after surgery in mass-forming intrahepatic cholangiocarcinoma. Cancer. 2002;94(6):1770–1776
  103. Suh KS, Chang SH, Lee HJ, Roh HR, Kim SH, Lee KU. Clinical outcomes and apomucin expression of intrahepatic cholangiocarcinoma according to gross morphology. J Am Coll Surg. 2002;195(6):782–789
  104. Takao S, Uchikura K, Yonezawa S, Shinchi H, Aikou T. Mucin core protein expression in extrahepatic bile duct carcinoma is associated with metastases to the liver and poor prognosis. Cancer. 1999;86(10):1966–1975
  105. Tamada S, Goto M, Nomoto M, et al. Expression of MUC1 and MUC2 mucins in extrahepatic bile duct carcinomas: its relationship with tumor progression and prognosis. Pathol Int. 2002;52(11):713–723
  106. Yuan SF, Li KZ, Wang L, et al. Expression of MUC1 and its significance in hepatocellular and cholangiocarcinoma tissue. World J Gastroenterol. 2005;11(30):4661–4666
  107. Boonla C, Sripa B, Thuwajit P, et al. MUC1 and MUC5AC mucin expression in liver fluke-associated intrahepatic cholangiocarcinoma. World J Gastroenterol. 2005;11(32):4939–4946
  108. Hong SM, Cho H, Moskaluk CA, Frierson HF, Yu E, Ro JY. CDX2 and MUC2 protein expression in extrahepatic bile duct carcinoma. Am J Clin Pathol. 2005;124(3):361–370
  109. Yonezawa S, Sueyoshi K, Nomoto M, et al. MUC2 gene expression is found in noninvasive tumors but not in invasive tumors of the pancreas and liver: its close relationship with prognosis of the patients. Hum Pathol. 1997;28(3):344–352
  110. Boonla C, Wongkham S, Sheehan JK, et al. Prognostic value of serum MUC5AC mucin in patients with cholangiocarcinoma. Cancer. 2003;98(7):1438–1443
  111. Takada A, Ohmori K, Yoneda T, et al. Contribution of carbohydrate antigens sialyl Lewis A and sialyl Lewis X to adhesion of human cancer cells to vascular endothelium. Cancer Res. 1993;53(2):354–361
  112. Kannagi R. Carbohydrate antigen sialyl Lewis a – its pathophysiological significance and induction mechanism in cancer progression. Chang Gung Med J. 2007;30(3):189–209
  113. Ohtsuka M, Ito H, Kimura F, et al. Results of surgical treatment for intrahepatic cholangiocarcinoma and clinicopathological factors influencing survival. Br J Surg. 2002;89(12):1525–1531
  114. Heimbach JK, Gores GJ, Haddock MG, et al. Predictors of disease recurrence following neoadjuvant chemoradiotherapy and liver transplantation for unresectable perihilar cholangiocarcinoma. Transplantation. 2006;82(12):1703–1707
  115. Huang JL, Biehl TR, Lee FT, Zimmer PW, Ryan JA. Outcomes after resection of cholangiocellular carcinoma. Am J Surg. 2004;187(5):612–617
  116. Abdel Wahab M, Fathy O, Elghwalby N, et al. Resectability and prognostic factors after resection of hilar cholangiocarcinoma. Hepatogastroenterology. 2006;53(67):5–10
  117. Miwa S, Miyagawa S, Kobayashi A, et al. Predictive factors for intrahepatic cholangiocarcinoma recurrence in the liver following surgery. J Gastroenterol. 2006;41(9):893–900
  118. Hirohashi K, Uenishi T, Kubo S, et al. Macroscopic types of intrahepatic cholangiocarcinoma: clinicopathologic features and surgical outcomes. Hepatogastroenterology. 2002;49(44):326–329
  119. Yi B, Zhang BH, Zhang YJ, et al. Surgical procedure and prognosis of hilar cholangiocarcinoma. Hepatobiliary Pancreat Dis Int. 2004;3(3):453–457
  120. Mahmoud FA, Rivera NI. The role of C-reactive protein as a prognostic indicator in advanced cancer. Curr Oncol Rep. 2002;4(3):250–255
  121. Gerhardt T, Milz S, Schepke M, et al. C-reactive protein is a prognostic indicator in patients with perihilar cholangiocarcinoma. World J Gastroenterol. 2006;12(34):5495–5500
  122. Wongkham S, Bhudhisawasdi V, Chau-in S, et al. Clinical significance of serum total sialic acid in cholangiocarcinoma. Clin Chim Acta. 2003;327(1–2):139–147
  123. Juntavee A, Sripa B, Pugkhem A, Khuntikeo N, Wongkham S. Expression of sialyl Lewis(a) relates to poor prognosis in cholangiocarcinoma. World J Gastroenterol. 2005;11(2):249–254
  124. Ellis CN, Burnette JJ, Sedlak R, Dyas C, Blakemore WS. Prognostic applications of DNA analysis in solid malignant lesions in humans. Surg Gynecol Obstet. 1991;173(4):329–342
  125. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature. 1998;396(6712):643–649
  126. Lindberg B, Enochsson L, Tribukait B, Arnelo U, Bergquist A. Diagnostic and prognostic implications of DNA ploidy and S-phase evaluation in the assessment of malignancy in biliary strictures. Endoscopy. 2006;38(6):561–565
  127. Iachino C, Catsicojannis N, Dallera F. Prognostic significance of tumor DNA content in carcinoma of the hepatic duct confluence. J Exp Clin Cancer Res. 1998;17(4):425–430
  128. Kawaki J, Miyazaki M, Ito H, et al. Allelic loss in human intrahepatic cholangiocarcinoma: correlation between chromosome 8p22 and tumor progression. Int J Cancer. 2000;88(2):228–231
  129. Muenphon K, Limpaiboon T, Jearanaikoon P, Pairojkul C, Sripa B, Bhudhisawasdi V. Amplification of chromosome 21q22.3 harboring trefoil factor family genes in liver fluke related cholangiocarcinoma is associated with poor prognosis. World J Gastroenterol. 2006;12(26):4143–4148
  130. Limpaiboon T, Tapdara S, Jearanaikoon P, Sripa B, Bhudhisawasdi V. Prognostic significance of microsatellite alterations at 1p36 in cholangiocarcinoma. World J Gastroenterol. 2006;12(27):4377–4382
  131. De Angelis PM, Stokke T, Beigi M, Mjaland O, Clausen OP. Prognostic significance of recurrent chromosomal aberrations detected by comparative genomic hybridization in sporadic colorectal cancer. Int J Colorectal Dis. 2001;16(1):38–45
  132. Casorelli I, Russo MT, Bignami M. Role of mismatch repair and MGMT in response to anticancer therapies. Anticancer Agents Med Chem. 2008;8(4):368–380
  133. Kohya N, Miyazaki K, Matsukura S, et al. Deficient expression of O(6)-methylguanine-DNA methyltransferase combined with mismatch-repair proteins hMLH1 and hMSH2 is related to poor prognosis in human biliary tract carcinoma. Ann Surg Oncol. 2002;9(4):371–379
  134. Koga Y, Kitajima Y, Miyoshi A, et al. Tumor progression through epigenetic gene silencing of O(6)-methylguanine-DNA methyltransferase in human biliary tract cancers. Ann Surg Oncol. 2005;12(5):354–363
  135. Schmitz KJ, Lang H, Frey UH, et al. GNAS1 T393C polymorphism is associated with clinical course in patients with intrahepatic cholangiocarcinoma. Neoplasia. 2007;9(2):159–165
  136. Linder S. Cytokeratin markers come of age. Tumour Biol. 2007;28(4):189–195
  137. Aishima S, Asayama Y, Taguchi K, et al. The utility of keratin 903 as a new prognostic marker in mass-forming-type intrahepatic cholangiocarcinoma. Mod Pathol. 2002;15(11):1181–1190
  138. Erickson LA, Lloyd RV. Practical markers used in the diagnosis of endocrine tumors. Adv Anat Pathol. 2004;11(4):175–189
  139. Hong SM, Kim MJ, Pi DY, Jo D, Yu E, Ro JY. Neuroendocrine differentiation in extrahepatic bile duct carcinomas and its prognostic significance. Hum Pathol. 2005;36(7):732–740
  140. Takagi S, Miyagawa S, Ichikawa E, et al. Dendritic cells, T-cell infiltration, and Grp94 expression in cholangiocellular carcinoma. Hum Pathol. 2004;35(7):881–886
  141. Kelloniemi E, Rintala E, Finne P, Stenman UH. Tumor-associated trypsin inhibitor as a prognostic factor during follow-up of bladder cancer. Urology. 2003;62(2):249–253
  142. Paju A, Vartiainen J, Haglund C, Itkonen O, von Boguslawski K, Leminen A, et al. Expression of trypsinogen-1, trypsinogen-2, and tumor-associated trypsin inhibitor in ovarian cancer: prognostic study on tissue and serum. Clin Cancer Res. 2004;10(14):4761–4768
  143. Paju A, Jacobsen J, Rasmuson T, Stenman UH, Ljungberg B. Tumor associated trypsin inhibitor as a prognostic factor in renal cell carcinoma. J Urol. 2001;165(3):959–962
  144. Tonouchi A, Ohtsuka M, Ito H, et al. Relationship between pancreatic secretory trypsin inhibitor and early recurrence of intrahepatic cholangiocarcinoma following surgical resection. Am J Gastroenterol. 2006;101(7):1601–1610
  145. Wang MT, Honn KV, Nie D. Cyclooxygenases, prostanoids, and tumor progression. Cancer Metastasis Rev. 2007;26(3–4):525–534
  146. Schmitz KJ, Lang H, Wohlschlaeger J, Reis H, Sotiropoulos GC, Schmid KW, et al. Elevated expression of cyclooxygenase-2 is a negative prognostic factor for overall survival in intrahepatic cholangiocarcinoma. Virchows Archiv. 2007;450(2):135–141
  147. Kim HJ, Lee KT, Kim EK, et al. Expression of cyclooxygenase-2 in cholangiocarcinoma: correlation with clinicopathological features and prognosis. Journal of Gastroenterology and Hepatology. 2004;19(5):582–588
  148. Garcea G, Neal CP, Pattenden CJ, Steward WP, Berry DP. Molecular prognostic markers in pancreatic cancer: a systematic review. Eur J Cancer. 2005;41(15):2213–2236
  149. Mann CD, Neal CP, Garcea G, Manson MM, Dennison AR, Berry DP. Prognostic molecular markers in hepatocellular carcinoma: a systematic review. Eur J Cancer. 2007;43(6):979–992
  150. Neal CP, Garcea G, Doucas H, Manson MM, Sutton CD, Dennison AR, et al. Molecular prognostic markers in resectable colorectal liver metastases: a systematic review. Eur J Cancer. 2006;42(12):1728–1743
  151. Bonney GK, Craven RA, Prasad R, Melcher AF, Selby PJ, Banks RE. Circulating markers of biliary malignancy: opportunities in proteomics?. Lancet Oncol. 2008;9(2):149–158
  152. Obama K, Ura K, Li M, et al. Genome-wide analysis of gene expression in human intrahepatic cholangiocarcinoma. Hepatology. 2005;41(6):1339–1348

PII: S0959-8049(08)00682-5

doi: 10.1016/j.ejca.2008.08.024

European Journal of Cancer
Volume 45, Issue 1 , Pages 33-47 , January 2009

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