Progenitor cell markers predict outcome of patients with hepatocellular carcinoma beyond Milan criteria undergoing liver transplantation

Journal of Hepatology

Volumn 63, Issue 6, 2015, Pages 1368-1377

  Miltiadous, Oriana ^a   Sia, Daniela ^a,b   Hoshida, Yujin ^a   Fiel, Maria Isabel ^a   Harrington, Andrew N ^a   Thung, Swan N ^a   Tan, Poh Seng ^a,c   Dong, Hui ^d   Revill, Kate ^a   Chang, Charissa Y ^a   Roayaie, Sasan ^e   Byrne, Thomas J ^f   Mazzaferro, Vincenzo ^b   Rakela, Jorge ^f   Florman, Sander ^a   Schwartz, Myron ^a   Llovet, Josep M ^a,g,h  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (Italy)

^c NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

^e LENOX HILL HOSPITAL   (United States)

^f MAYO CLINIC   (United States)

^g UNIVERSITY OF BARCELONA   (Spain)

^h INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

Gene expression; Gene signature; Prognosis; Stem cell; Survival

Indexed keywords

ALBUMIN; ALPHA FETOPROTEIN; BETA CATENIN; BILIRUBIN; BIOLOGICAL MARKER; CYTOKERATIN 19; EPITHELIAL CELL ADHESION MOLECULE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; PROTEIN S2; PROTEIN S6; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; EPCAM PROTEIN, HUMAN; TUMOR ANTIGEN; TUMOR MARKER;

ADULT; ARTICLE; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SIZE; CANCER SURVIVAL; FEMALE; FOLLOW UP; HUMAN; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; LIVER TRANSPLANTATION; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STEM CELL; AGED; CANCER STEM CELL; CARCINOMA, HEPATOCELLULAR; COHORT ANALYSIS; GENE EXPRESSION PROFILING; GENETICS; LIVER NEOPLASMS; METABOLISM; MIDDLE AGED; MORTALITY; PROGNOSIS;

ADULT; AGED; ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; CARCINOMA, HEPATOCELLULAR; CELL ADHESION MOLECULES; COHORT STUDIES; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; KERATIN-19; LIVER NEOPLASMS; LIVER TRANSPLANTATION; MALE; MIDDLE AGED; NEOPLASTIC STEM CELLS; PROGNOSIS;

EID: 84983189783     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2015.07.025     Document Type: Article

References (45)

1. V. Mazzaferro, E. Regalia, R. Doci, S. Andreola, A. Pulvirenti, F. Bozzetti, and et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis N Engl J Med 334 1996 693 700
2. J.M. Llovet, M. Ducreux, R. Lencioni, A.M. Di Bisceglie, P.R. Galle, J.F. Dufour, and et al. J EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma Hepatology 56 2012 908 943
3. J.M. Llovet, J. Fuster, and J. Bruix Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation Hepatology 30 1999 1434 1440
4. F.Y. Yao, L. Ferrell, N.M. Bass, J.J. Watson, P. Bacchetti, A. Venook, and et al. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival Hepatology 33 2001 1394 1403
5. S. Roayaie, J.S. Frischer, S.H. Emre, T.M. Fishbein, P.A. Sheiner, M. Sung, and et al. Long-term results with multimodal adjuvant therapy and liver transplantation for the treatment of hepatocellular carcinoma larger than 5 centimeters Ann Surg 235 2002 533 539
6. S.G. Lee, S. Hwang, D.B. Moon, C.S. Ahn, K.H. Kim, K.B. Sung, and et al. Expanded indication criteria of living donor liver transplantation for hepatocellular carcinoma at one large-volume center Liver Transpl 14 2008 935 945
7. F.Y. Yao Liver transplantation for hepatocellular carcinoma: Beyond the Milan criteria Am J Transplant 8 2008 1982 1989
8. V. Mazzaferro, J.M. Llovet, R. Miceli, S. Bhoori, M. Schiavo, L. Mariani, and et al. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis Lancet Oncol 10 2009 35 43
9. P.A. Clavien, M. Lesurtel, P.M. Bossuyt, G.J. Gores, B. Langer, A. Perrier, and et al. Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report Lancet Oncol 13 2012 e11 e22
10. S. Jonas, W.O. Bechstein, T. Steinmüller, M. Herrmann, C. Radke, T. Berg, and et al. Vascular invasion and histopathologic grading determine outcome after liver transplantation for hepatocellular carcinoma in cirrhosis Hepatology 33 2001 1080 1086
11. A. Villanueva, V. Hernandez-Gea, and J.M. Llovet Medical therapies for hepatocellular carcinoma: a critical view of the evidence Nat Rev Gastroenterol Hepatol 10 2013 34 42
12. C.L. Sawyer The cancer biomarker problem Nature 452 2008 548 552
13. Y. Hoshida, S.M. Nijman, M. Kobayashi, J.A. Chan, J.P. Brunet, D.Y. Chiang, and et al. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma Cancer Res 69 2009 7385 7392
14. Q.H. Ye, L.X. Qin, M. Forgues, P. He, J.W. Kim, A.C. Peng, and et al. Predicting hepatitis B virus-positive metastatic hepatocellular carcinomas using gene expression profiling and supervised machine learning Nat Med 9 2003 416 423
15. N. Iizuka, M. Oka, H. Yamada-Okabe, M. Nishida, Y. Maeda, N. Mori, and et al. Oligonucleotide microarray for prediction of early intrahepatic recurrence of hepatocellular carcinoma after curative resection Lancet 361 2003 923 929
16. J.S. Lee, I.S. Chu, J. Heo, D.F. Calvisi, Z. Sun, T. Roskams, and et al. Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling Hepatology 40 2004 667 676
17. Y. Kurokawa, R. Matoba, I. Takemasa, H. Nagano, K. Dono, S. Nakamori, and et al. Molecular-based prediction of early recurrence in hepatocellular carcinoma J Hepatol 41 2004 284 291
18. P. Kaposi-Novak, J.S. Lee, L. Gòmez-Quiroz, C. Coulouarn, V.M. Factor, and S.S. Thorgeirsson Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype J Clin Invest 116 2006 1582 1595
19. S. Boyault, D.S. Rickman, A. de Reyniès, C. Balabaud, S. Rebouissou, E. Jeannot, and et al. Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets Hepatology 45 2007 42 52
20. D.Y. Chiang, A. Villanueva, Y. Hoshida, J. Peix, P. Newell, B. Minguez, and et al. Focal gains of VEGFA and molecular classification of hepatocellular carcinoma Cancer Res 68 2008 6779 6788
21. A. Villanueva, Y. Hoshida, C. Battiston, V. Tovar, D. Sia, C. Alsinet, and et al. Combining clinical, pathology, and gene expression data to predict recurrence of hepatocellular carcinoma Gastroenterology 140 2011 1501 1512
22. B. Mínguez, Y. Hoshida, A. Villanueva, S. Toffanin, L. Cabellos, S. Thung, and et al. Gene-expression signature of vascular invasion in hepatocellular carcinoma J Hepatol 55 2011 1325 1331
23. C. Coulouarn, V.M. Factor, and S.S. Thorgeirsson Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer Hepatology 47 2008 2059 2067
24. H.G. Woo, E.S. Park, J.H. Cheon, J.H. Kim, J.S. Lee, B.J. Park, and et al. Gene expression-based recurrence prediction of hepatitis B virus-related human hepatocellular carcinoma Clin Cancer Res 14 2008 2056 2064
25. T. Yamashita, M. Forgues, W. Wang, J.W. Kim, Q. Ye, H. Jia, and et al. EpCAM and alpha-fetoprotein expression defines novel prognostic subtypes of hepatocellular carcinoma Cancer Res 68 2008 1451 1461
26. S. Cairo, C. Armengol, A. De Reyniès, Y. Wei, E. Thomas, C.A. Renard, and et al. Hepatic stem-like phenotype and interplay of Wnt/beta-catenin and Myc signaling in aggressive childhood liver cancer Cancer Cell 14 2008 471 484
27. S. Yoshioka, I. Takemasa, H. Nagano, N. Kittaka, T. Noda, H. Wada, and et al. Molecular prediction of early recurrence after resection of hepatocellular carcinoma Eur J Cancer 45 2009 881 889
28. J.B. Andersen, R. Loi, A. Perra, V.M. Factor, G.M. Ledda-Columbano, A. Columbano, and et al. Progenitor-derived hepatocellular carcinoma model in the rat Hepatology 51 2010 1401 1409
29. H.G. Woo, J.H. Lee, J.H. Yoon, C.Y. Kim, H.S. Lee, J.J. Jang, and et al. Identification of a cholangiocarcinoma-like gene expression trait in hepatocellular carcinoma Cancer Res 70 2010 3034 3041
30. S. Roessler, E.L. Long, A. Budhu, Y. Chen, X. Zhao, J. Ji, and et al. Integrative genomic identification of genes on 8p associated with hepatocellular carcinoma progression and patient survival Gastroenterology 142 2012 957 966
31. J.C. Nault, A. De Reyniès, A. Villanueva, J. Calderaro, S. Rebouissou, G. Couchy, and et al. A hepatocellular carcinoma 5-gene score associated with survival of patients after liver resection Gastroenterology 145 2013 176 187
32. M. Komuta, B. Spee, S. Vander Borght, R. De Vos, C. Verslype, R. Aerts, and et al. Clinicopathological study on cholangiolocellular carcinoma suggesting hepatic progenitor cell origin Hepatology 47 2008 1544 1556
33. A. Lachenmayer, C. Alsinet, R. Savic, L. Cabellos, S. Toffanin, Y. Hoshida, and et al. Wnt-pathway activation in two molecular classes of hepatocellular carcinoma and experimental modulation by sorafenib Cancer Res 18 2012 4997 5007
34. M.A. Bjornsti, and P.J. Houghton The tor pathway: a target for cancer therapy Nat Rev Cancer 4 2004 335 348
35. A. Villanueva, D.Y. Chiang, P. Newell, J. Peix, S. Thung, C. Alsinet, and et al. Pivotal role of mTOR signaling in hepatocellular carcinoma Gastroenterology 135 2008 1972 1983
36. J. Bruix, M. Sherman American Association for the Study of Liver Diseases Management of hepatocellular carcinoma: an update Hepatology 53 2011 1020 1022
37. S. Roayaie, I.N. Blume, S.N. Thung, M. Guido, M.I. Fiel, S. Hiotis, and et al. A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma Gastroenterology 137 2009 850 855
38. P.T. Kim, N. Onaca, S. Chinnakotla, G.L. Davis, L.W. Jennings, G.J. McKenna, and et al. Tumor biology and pre-transplant locoregional treatments determine outcomes in patients with T3 hepatocellular carcinoma undergoing liver transplantation Clin Transplant 27 2013 311 318
39. U. Cillo, A. Vitale, F. Grigoletto, E. Gringeri, F. D'Amico, M. Valmasoni, and et al. Intention-to-treat analysis of liver transplantation in selected, aggressively treated HCC patients exceeding the Milan criteria Am J Transplant 7 2007 972 981
40. D. DuBay, C. Sandroussi, L. Sandhu, S. Cleary, M. Guba, M.S. Cattral, and et al. Liver transplantation for advanced hepatocellular carcinoma using poor tumor differentiation on biopsy as an exclusion criterion Ann Surg 253 2011 166 172
41. C. Toso, S. Asthana, D.L. Bigam, A.M. Shapiro, and N.M. Kneteman Reassessing selection criteria prior to liver transplantation for hepatocellular carcinoma utilizing the Scientific Registry of Transplant Recipients database Hepatology 49 2009 832 838
42. F.Y. Yao, R.K. Kerlan Jr, R. Hirose, T.J. Davern, N.M. Bass, S. Feng, and et al. Excellent outcome following down-staging of hepatocellular carcinoma prior to liver transplantation: an intention-to-treat analysis Hepatology 48 2008 819 827
43. M. Schwartz, I. Dvorchik, S. Roayaie, M.I. Fiel, S. Finkelstein, J.W. Marsh, and et al. Liver transplantation for hepatocellular carcinoma: extension of indications based on molecular markers J Hepatol 49 2008 581 588
44. Y. Hoshida, A. Villanueva, M. Kobayashi, J. Peix, D.Y. Chiang, A. Camargo, and et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma N Engl J Med 359 2008 1995 2004
45. S. Banerjee, D.S. Wang, H.J. Kim, C.B. Sirlin, M.G. Chan, R.L. Korn, and et al. A computed tomography radiogenomic biomarker predicts microvascular invasion and clinical outcomes in hepatocellular carcinoma Hepatology 30 2015