Recurrence of hepatocellular carcinoma after liver transplantation: An update

Future Oncology

Volumn 11, Issue 21, 2015, Pages 2923-2936

  Mazzola, Alessandra ^a,b   Costantino, Andrea ^a   Petta, Salvatore ^a   Bartolotta, Tommaso Vincenzo ^a   Raineri, Maurizio ^a   Sacco, Rodolfo ^c   Brancatelli, Giuseppe ^a   Cammà, Calogero ^a   Cabibbo, Giuseppe ^a  

^a UNIVERSITY OF PALERMO   (Italy)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c CISANELLO HOSPITAL   (Italy)

Author keywords

hepatocellular carcinoma; immunosuppression; liver transplantation; living donors; recurrence

Indexed keywords

CANCER ADJUVANT THERAPY; CANCER PATIENT; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SIZE; CANCER SURGERY; CANCER SURVIVAL; CANCER TRANSPLANTATION; CHEMOEMBOLIZATION; DISEASE SEVERITY; HOSPITAL ADMISSION; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; LIVER CELL CARCINOMA; LIVER TRANSPLANTATION; LIVING DONOR; NEUTROPHIL LYMPHOCYTE RATIO; ORGAN DONOR; POSTOPERATIVE PERIOD; PREOPERATIVE PERIOD; PRIORITY JOURNAL; RADIOFREQUENCY ABLATION; RECURRENCE FREE SURVIVAL; REVIEW; SURVIVAL RATE; SYSTEMIC THERAPY; TUMOR INVASION; CARCINOMA, HEPATOCELLULAR; GENETICS; LEUKOCYTE COUNT; LIVER NEOPLASMS; META ANALYSIS; METABOLISM; MORTALITY; MULTIMODALITY CANCER THERAPY; PATHOLOGY; PERIOPERATIVE PERIOD; PROCEDURES; RISK FACTOR; TUMOR RECURRENCE; TUMOR VOLUME;

ALPHA FETOPROTEIN; TUMOR MARKER;

ALPHA-FETOPROTEINS; BIOMARKERS, TUMOR; CARCINOMA, HEPATOCELLULAR; COMBINED MODALITY THERAPY; HUMANS; LEUKOCYTE COUNT; LIVER NEOPLASMS; LIVER TRANSPLANTATION; NEOPLASM RECURRENCE, LOCAL; PERIOPERATIVE PERIOD; RISK FACTORS; TUMOR BURDEN;

EID: 84946195398     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.15.239     Document Type: Review

References (96)

1. Cabibbo G, Enea M, Attanasio M, Bruix J, Craxì A, Cammà C. A meta-analysis of survival rates of untreated patients in randomized clinical trials of hepatocellular carcinoma. Hepatology 51(4), 1274-1283 (2010).
2. Villa E, Critelli R, Lei B et al. Neoangiogenesis-related genes are hallmarks of fast-growing hepatocellular carcinomas and worst survival. Results from a prospective study. Gut doi:10.1136/gutjnl-2014-308483 (2015) (Epub ahead of print).
3. Mazzaferro V, Regalia E, Doci R et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N. Engl. J. Med. 334(11), 693-699 (1996).
4. Yao FY, Ferrell L, Bass NM et al. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology 33(6), 1394-1403 (2001).
5. Mazzaferro V, Llovet JM, Miceli R et al. Investigator Study Group. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol. 10(1), 35-43 (2009).
6. Yao FY. Liver transplantation for hepatocellular carcinoma: beyond the Milan criteria. Am. J. Transplant. 8(10), 1982-1989 (2008).
7. Ringe B, Pichlmayr R, Wittekind C, Tusch G. Surgical treatment of hepatocellular carcinoma: experience with liver resection and transplantation in 198 patients. World J. Surg. 15(2), 270-285 (1991).
8. Herrero J, Sangro B, Quiroga J et al. Influence of tumor characteristics on the outcome of liver transplantation among patients with liver cirrhosis and hepatocellular carcinoma. Liver Transpl. 7(7), 631-636 (2001).
9. Roayaie S, Frischer JS, Emre SH et al. Long-term results with multimodal adjuvant therapy and liver transplantation for the treatment of hepatocellular carcinomas larger than 5 centimeters. Ann. Surg. 235(4), 533-539 (2002).
10. Kneteman NM, Oberholzer J, Al Saghier M et al. Sirolimus-based immunosuppression for liver transplantation in the presence of extended criteria for hepatocellular carcinoma. Liver Transpl. 10(10), 1301-1311 (2004).
11. Onaca N, Davis GL, Goldstein RM, Jennings LW, Klintmalm GB. Expanded criteria for liver transplantation in patients with hepatocellular carcinoma: a report from the International Registry of Hepatic Tumors in Liver Transplantation. Liver Transpl. 13(3), 391-399 (2007).
12. Lai Q, Avolio AW, Manzia TM et al. Combination of biological and morphological parameters for the selection of patients with hepatocellular carcinoma waiting for liver transplantation. Clin. Transpl. 26(2), E125-E131 (2012).
13. Toso C, Trotter J, Wei A et al. Total tumor volume predicts risk of recurrence following liver transplantation in patients with hepatocellular carcinoma. Liver Transpl. 14(8), 1107-1115 (2008).
14. Macaron C, Hanouneh IA, Lopez R, Aucejo F, Zein NN. Total tumor volume predicts recurrence of hepatocellular carcinoma after liver transplantation in patients beyond Milan or UCSF criteria. Transplant. Proc. 42(10), 4585-4592 (2010).
15. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J. Hepatol. 56(4), 908-943 (2012).
16. Bruix J, Sherman M; American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma: an update. Hepatology 53(3), 1020-1022 (2011).
17. 2014 KLCSG-NCC Korea practice guideline for the management of hepatocellular carcinoma. Gut Korean Liver Cancer Study Group (KLCSG); National Cancer Center, Korea (NCC). Liver 9(3), 267-317 (2015).
18. Oliveri RS, Wetterslev J, Gluud C. Transarterial (chemo) em-bolisation for unresectable hepatocellular carcinoma. Cochrane Database Syst. Rev. 3, CD004787 (2011).
19. Ni JY, Liu SS, Xu LF, Sun HL, Chen YT. Meta-analysis of radiofrequency ablation in combination with transarterial chemoembolization for hepatocellular carcinoma. World J. Gastroenterol. 19(24), 3872-3882 (2013).
20. Ravaioli M, Grazi GL, Piscaglia F et al. Liver transplantation for hepatocellular carcinoma: results of down-staging in patients initially outside the Milan selection criteria. Am. J. Transplant. 8(12), 2547-2557 (2008).
21. Yao FY, Kerlan RK, Hirose R et al. Excellent outcome following down-staging of hepatocellular carcinoma prior to liver transplantation: an intention-to-treat analysis. Hepatology 48(3), 819-827 (2008).
22. Clavien PA, Lesurtel M, Bossuyt PM et al. Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol. 13(1), e11-e22 (2012).
23. Cabibbo G, Maida M, Genco C et al. Survival of patients with hepatocellular carcinoma (HCC) treated by percutaneous radiofrequency ablation (RFA) is affected by complete radiological response. PLoS ONE 8(7), e70016 (2013).
24. Freeman RB Jr, Wiesner RH, Harper A et al. The new liver allocation system: moving toward evidence-based transplantation policy. Liver Transpl. 8(9), 851-858 (2002).
25. Lai Q, Avolio AW, Manzia TM et al. Role of alpha-fetoprotein in selection of patients with hepatocellular carcinoma waiting for liver transplantation: must we reconsider it? Int. J. Biol. Markers 26(3), 153-159 (2011).
26. Merani S, Majno P, Kneteman NM et al. The impact of waiting list alphafetoprotein changes on the outcome of liver transplant for hepatocellular carcinoma. J. Hepatol. 55 (4), 814-819 (2011).
27. Vibert E, Azoulay D, Hoti E et al. Progression of alphafetoprotein before liver transplantation for hepatocellular carcinoma in cirrhotic patients: a critical factor. Am. J. Transplant. 10(1), 129-137 (2010).
28. Todo S, Furukawa H, Tada M; Japanese Liver Transplantation Study Group. Extending indication: role of living donor liver transplantation for hepatocellular carcinoma. Liver Transpl. 13(11 Suppl. 2), S48-S54 (2007).
29. Lee S, Ahn C, Ha T et al. Liver transplantation for hepatocellular carcinoma: Korean experience. J. Hepatobiliary Pancreat. Sci. 17(5), 539-547 (2010).
30. Lee SG, Hwang S, Moon DB et al. Expanded indication criteria of living donor liver transplantation for hepatocellular carcinoma at one large volume center. Liver Transpl. 14(7), 935-945 (2008).
31. DuBay D, Sandroussi C, Sandhu L et al. Liver transplantation for advanced hepatocellular carcinoma using poor tumor differentiation on biopsy as an exclusion criterion. Ann. Surg. 253(1), 166-172 (2011).
32. Duvoux C, Roudot-Thoraval F, Decaens T et al. Liver transplantation for hepatocellular carcinoma: a model including ?-fetoprotein improves the performance of Milan criteria. Gastroenterology 143(4), 986-994 (2012).
33. Zou WL, Zang YJ, Chen XG, Shen ZY. Risk factors for fatal recurrence of hepatocellular carcinoma and their role in selecting candidates for liver transplantation. Hepatobiliary Pancreat. Dis. Int. 7(2), 145-151 (2008).
34. Lai Q, Avolio AW, Graziadei I et al. European Hepatocellular Cancer Liver Transplant Study Group. Alpha-fetoprotein and modified response evaluation criteria in solid tumors progression after locoregional therapy as predictors of hepatocellular cancer recurrence and death after transplantation. Liver Transpl. 19(10), 1108-1118 (2013).
35. Dumitra TC, Dumitra S, Metrakos PP et al. Pre transplantation ?-fetoprotein slope and Milan criteria: strong predictors of hepatocellular carcinoma recurrence after transplantation. Transplantation 195(1), 228-233 (2013).
36. Han K, Tzimas GN, Barkun JS et al. Preoperative alpha-fetoprotein slope is predictive of hepatocellular carcinoma recurrence after liver transplantation. Can. J. Gastroenterol. 21(1), 39-45 (2007).
37. Chaiteerakij R, Zhang X, Addissie BD et al. Combinations of biomarkers and Milan criteria for predicting hepatocellular carcinoma recurrence after liver transplantation. Liver Transpl. (5) 599-606 2015.
38. Coussens LM, Werb Z. Inflammation and cancer. Nature 420(6917), 860-867 (2002).
39. Mano Y, Shirabe K, Yamashita Y et al. Preoperative neutrophil-to-lymphocyte ratio is a predictor of survival after hepatectomy for hepatocellular carcinoma: a retrospective analysis. Ann. Surg. 258(2), 301-305 (2013).
40. Gomez D, Farid S, Malik HZ et al. Preoperative neutrophil-to-lymphocyte ratio as a prognostic predictor after curative resection for hepatocellular carcinoma. World J. Surg. 32(8), 1757-1762 (2008).
41. Chen TM, Lin CC, Huang PT, Wen CF. Neutrophil-to-lymphocyte ratio associated with mortality in early hepatocellular carcinoma patients after radiofrequency ablation. J. Gastroenterol. Hepatol. 27(3), 553-561 (2012).
42. Dan J, Zhang Y, Peng Z et al. Postoperative neutrophil-to-lymphocyte ratio change predicts survival of patients with small hepatocellular carcinoma undergoing radiofrequency ablation. PLoS ONE 8(3), e5818 (2013).
43. Sharaiha RZ, Halazun KJ et al. Elevated preoperative neutrophil: lymphocyte ratio as a predictor of postoperative disease recurrence in esophageal cancer. Ann. Surg. Oncol. 18(12), 3362-3369 (2011).
44. Malik HZ, Prasad KR, Halazun KJ et al. Preoperative prognostic score for predicting survival after hepatic resection for colorectal liver metastases. Ann. Surg. 246(5), 806-814 (2007).
45. Halazun KJ, Aldoori A, Malik HZ et al. Elevated preoperative neutrophil to lymphocyte ratio predicts survival following hepatic resection for colorectal liver metastases. Eur. J. Surg. Oncol. 34(1), 55-60 (2008).
46. Bhatti I, Peacock O, Lloyd G, Larvin M, Hall RI. Preoperative hematologic markers as independent predictors of prognosis in resected pancreatic ductal. Am. J. Surg. 200(2), 197-203 (2010).
47. Bertuzzo VR, Cescon M, Ravaioli M et al. Analysis of factors affecting recurrence of hepatocellular carcinoma after liver transplantation with a special focus on inflammation markers. Transplantation 91(11), 1279-1285 (2011).
48. Limaye AR, Clark V, Soldevila-Pico C et al. Neutrophil-lymphocyte ratio predicts overall and recurrence free survival after liver transplantation for hepatocellular carcinoma. Hepatol. Res. 43(7), 757-764 (2013).
49. Motomura T, Shirabe K, Mano Y et al. Neutrophil-lymphocyte ratio reflects hepatocellular carcinoma recurrence after liver transplantation via inflammatory microenvironment. J. Hepatol. 58(1), 58-64 (2013).
50. Yoshizumi T, Ikegami T, Yoshiya S et al. Impact of tumor size, number of tumors and neutrophil-to-lymphocyte ratio in liver transplantation for recurrent hepatocellular carcinoma. Hepatol. Res. 43(7), 709-716 (2013).
51. Cescon M, Bertuzzo VR, Ercolani G, Ravaioli M, Odaldi F, Pinna AD. Liver transplantation for hepatocellular carcinoma: role of inflammatory and immunological state on recurrence and prognosis. World J. Gastroenterol. 19(48), 9174-9182 (2013).
52. Kemeny F, Vadrot J, Wu A, Smadja C, Meakins JL, Franco D. Morphological and histological features of resected hepatocellular carcinoma in cirrhotic patients in the west. Hepatology 9(2), 253-257 (1989).
53. Sasaki Y, Imaoka S, Ishiguro S et al. Clinical features of small hepatocellular carcinoma as assessed by histologic grades. Surgery 119(3), 252-260 (1996).
54. Schlitt HJ, Neipp M, Weimann A et al. Recurrence patterns of hepatocellular and fibrolamellar carcinoma after liver transplantation. J. Clin. Oncol. 17(1), 324-331(1999).
55. Jonas S, Bechstein WO, Steinmuller T et al. Vascular invasion and histopathologic grading determine outcome after liver transplantation for hepatocellular carcinoma in cirrhosis. Hepatology 33(5), 1080-1086 (2001).
56. Klintmalm GB. Liver transplantation for hepatocellular carcinoma: a registry report of the impact of the tumor characteristics on outcome. Ann. Surg. 228(4), 479-490 (1998).
57. Salizzoni M, Zamboni F, Lupo F, Franchello A, David E, Rizzetto M. Liver transplantation for early-detected, multifocal hepatocellular carcinoma. Br. J. Surg. 88(9), 1194-1195 (2001).
58. Kirimlioglu H, Dvorchick I, Ruppert K et al. Hepatocellular carcinomas in native livers from patients with orthotopic liver transplantation: biologic and therapeutic implications. Hepatology 34(3), 502-510 (2001).
59. Sotiropoulos GC, Molmenti EP, Lösch C, Beckebaum S, Broelsch CE, Lang H. Meta-analysis of tumor recurrence after liver transplantation for hepatocellular carcinoma based on 1,198 cases. Eur. J. Med. Res. 12(10), 527-534 (2007).
60. Kornberg A, Kupper B, Tannapfel A et al. Long-term survival after recurrent hepatocellular carcinoma in liver transplant patients: clinical patterns and outcome variables. Eur. J. Surg. Oncol. 36(3), 275-280 (2010).
61. Saborido BP, Diaz JC, Los Galanes SJ et al. Does preoperative fine needle aspirationbiopsy produce tumor recurrence in patients following liver transplantation for hepatocellular carcinoma? Transplant. Proc. 37(9), 3874-3877 (2005).
62. Marelli L, Grasso A, Pleguezuelo M et al. Tumour size and differentiation in predicting recurrence of hepatocellular carcinoma after liver transplantation: external validation of a new prognostic score. Ann. Surg. Oncol. 15(12), 3503-3511(2008).
63. Ravaioli M, Grazi GL, Ercolani G et al. Partial necrosis on hepatocellular carcinoma nodules facilitates tumor recurrence after liver transplantation. Transplantation 78(12), 1780-1786 (2004).
64. Sarasin FP, Majno PE, Llovet JM, Bruix J, Mentha G, Hadengue A. Living donor liver transplantation for early hepatocellular carcinoma: a life-expectancy and cost-effectiveness perspective. Hepatology 33(5), 1073-1079 (2001).
65. Lo CM, Fan ST, Liu CL, Chan SC, Wong J. The role and limitation of living donor liver transplantation for hepatocellular carcinoma. Liver Transpl. 10(3), 440-447 (2004).
66. Majno P, Mazzaferro V. Living donor liver transplantation for hepatocellular carcinoma exceeding conventional criteria: questions, answers and demands for a common language. Liver Transpl. 12(6), 896-898 (2006).
67. Kulik L, Abecassis M. Living donor liver transplantation for hepatocellular carcinoma. Gastroenterology 127(Suppl. 1), S277-S282 (2004).
68. Vakili K, Pomposelli JJ, Cheah YL et al. Living donor liver transplantation for hepatocellular carcinoma: increased recurrence but improved survival. Liver Transpl. 15(12), 1861-1866 (2009).
69. Lo CM, Fan ST, Liu CL, Chan SC, Ng IO, Wong J. Living donor versus deceased donor liver transplantation for early irresectable hepatocellular carcinoma. Br. J. Surg. 94(1), 78-86 (2007).
70. Fisher RA, Kulik LM, Freise CE et al. A2ALL Study Group. Hepatocellular carcinoma recurrence and death following living and deceased donor liver transplantation. Am. J. Transplant. 7(6), 1601-1608 (2007).
71. Sandhu L, Sandroussi C, Guba M et al. Living donor liver transplantation versus deceased donor liver transplantation for hepatocellular carcinoma: comparable survival and recurrence. Liver Transpl. 18(3), 315-322(2012).
72. Park MS, Lee KW, Suh SW et al. Livingdonor liver transplantation associated with higher incidence of hepatocellular carcinoma recurrence than deceased-donor liver transplantation. Transplantation 97(1), 71-77 (2014).
73. Di Sandro S, Slim AO, Giacomoni A et al. Living donor liver transplantation for hepatocellular carcinoma: long-term results compared with deceased donor liver transplantation. Transplant. Proc. 41(4), 1283-1285 (2009).
74. Picardo A, Karpoff HM, Ng B, Lee J, Brennan MF, Fong Y. Partial hepatectomy accelerates local tumor growth: potential roles of local cytokine activation. Surgery 124(1), 57-64 (1998).
75. Yao FY, Bass NM, Nikolai B et al. Liver transplantation for hepatocellular carcinoma: analysis of survival according to the intentionto-treat principle and dropout from the waiting list. Liver Transpl. 8(10), 873-883 (2002).
76. Vivarelli M, Bellusci R, Cucchetti A et al. Low recurrence rate of hepatocellular carcinoma after liver transplantation: better patient selection or lower immunosuppression? Transplantation 74(12), 1746-1751 (2002).
77. Vivarelli M, Cucchetti A, Piscaglia F et al. Analysis of risk factors for tumor recurrence after liver transplantation for hepatocellular carcinoma: key role of immunosuppression. Liver Transpl. 11(5), 497-503 (2005).
78. Vivarelli M, Cucchetti A, La Barba G et al. Liver transplantation for hepatocellular carcinoma under calcineurin inhibitors: reassessment of risk factors for tumor recurrence. Ann. Surg. 248(5), 857-862 (2008).
79. Haddad EM, McAlister VC, Renouf E, Malthaner R, Kjaer MS, Gluud LL. Cyclosporin versus tacrolimus for liver transplanted patients. Cochrane Database Syst. Rev. 4, CD005161 (2006).
80. Cheng JW, Shi YH, Fan J et al. An immune function assay predicts post-transplant recurrence in patients with hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 137(10), 1445-1453 (2011).
81. Sahin F, Kannangai R, Adegbola O, Wang J, Su G, Torbenson M. mTOR and P70 S6 kinase expression in primary liver neoplasms. Clin. Cancer Res. 10(24), 8421-8425 (2004).
82. Boyault S, Rickman DS, de Reyniès A et al. Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets. Hepatology 45(1), 42-52 (2007).
83. Menon KV, Hakeem AR, Heaton ND. Meta-analysis:recurrence and survival following the use of sirolimus in liver transplantation for hepatocellular carcinoma. Aliment. Pharmacol. Ther. 37 (4), 411-419 (2013).
84. Schnitzbauer AA, Zuelke C, Graeb C et al. A prospective randomised, openlabeled, trial comparing sirolimus-containing versus mTOR inhibitor-free immunosuppression in patients undergoing liver transplantation for hepatocellular carcinoma. BMC Cancer 10, 190 (2010).
85. Zhu AX, Kudo M, Assenat E et al. Effect of everolimus on survival in advanced hepatocellular carcinoma after failure of sorafenib: the EVOLVE-1 randomized clinical trial. JAMA 312(1), 57-67 (2014).
86. Maida M, Iavarone M, Raineri M, Cammà C, Cabibbo G. Second line systemic therapies for hepatocellular carcinoma: Reasons for the failure. World J. Hepatol. 7(17), 2053-2057 (2015).
87. An HJ, Jang JW, Bae SH et al. Serum C-reactive protein is a useful biomarker for predicting outcomes after liver transplantation in patients with hepatocellular carcinoma. Liver Transpl. 18(12), 1406-1414 (2012).
88. Burgio Dioguardi M, Ronot M, Fuks D et al. Follow-up imaging after liver transplantation should take into consideration primary hepatocellular carcinoma characteristics. Transplantation 99(8), 1613-1618 (2015).
89. Cherqui D. Role of adjuvant treatment in liver transplantation for advanced hepatocellular carcinoma. J. Hepatobiliary Pancreat. Surg. 5(1), 35-40 (1998).
90. Pokorny H, Gnant M, Rasoul-Rockenschaub S et al. Does additional doxorubicin chemotherapy improve outcome in patients with hepatocellular carcinoma treated by liver transplantation? Am. J. Transplant. 5(4), 788-794 (2005).
91. Söderdahl G, Ba7die;ckman L, Isoniemi H et al. A prospective, randomized, multi-centre trial of systemic adjuvant chemotherapy versus no additional treatment in liver transplantation for hepatocellular carcinoma. Transplant 19(4), 288-294 (2006).
92. Xu J, Shen ZY, Chen XG et al. A randomized controlled trial of Licartin for preventing hepatoma recurrence after liver transplantation. Hepatology 45(2), 269-276 (2007).
93. Valdivieso A, Bustamante J, Gastaca M et al. Management of hepatocellular carcinoma recurrence after liver transplantation. Transplant. Proc. 42, 660 (2010).
94. Llovet JM, Ricci S, Mazzaferro V et al. Sorafenib in advanced hepatocellular carcinoma. N. Engl. J. Med. 359(4), 378-390 (2008).
95. Mancuso A, Mazzola A, Cabibbo G et al. Survival of patients treated with sorafenib for hepatocellular carcinoma recurrence after liver transplantation: a systematic review and meta-analysis. Dig. Liver Dis. 47(4), 324-330 (2015).
96. Sacco R, Gadaleta-Caldarola G, Galati G, Lombardi G, Mazza G, Cabibbo G. European Association for the Study of the Liver Hepatocellular Carcinoma summit 2014: old questions, new (or few) answers? Future Oncol. 10(10), 1719-1721 (2014).