Liver transplantation for hepatocellular carcinoma on cirrhosis: Strategies to avoid tumor recurrence

World Journal of Gastroenterology

Volumn 17, Issue 43, 2011, Pages 4741-4746

  Vivarelli, Marco ^a   Risaliti, Andrea ^b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Chemotherapy; Hepatocellular carcinoma; Immunosuppression; Liver transplantation; Tumor recurrence

Indexed keywords

CYCLOSPORIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; TACROLIMUS;

CANCER CHEMOTHERAPY; CANCER STAGING; COMPARATIVE STUDY; DISEASE SEVERITY; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER TRANSPLANTATION; PROGNOSIS; REVIEW; TUMOR RECURRENCE;

EID: 82455166801     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v17.i43.4741     Document Type: Review

References (59)

1. Nordenstedt H, White DL, El-Serag HB. The changing pattern of epidemiology in hepatocellular carcinoma. Dig Liver Dis 2010; 42 Suppl 3: S206-S214
2. Poon RT. Optimal initial treatment for early hepatocellularcarcinoma in patients with preserved liver function: transplantation or resection? Ann Surg Oncol 2007; 14: 541-547
3. Iwatsuki S, Gordon RD, Shaw BW, Starzl TE. Role of liver transplantation in cancer therapy. Ann Surg 1985; 202: 401-407
4. O'Grady JG, Polson RJ, Rolles K, Calne RY, Williams R. Liver transplantation for malignant disease. Results in 93 consecutive patients. Ann Surg 1988; 207: 373-379
5. 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 1991; 15: 270-285
6. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, Montalto F, Ammatuna M, Morabito A, Gennari L. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 1996; 334: 693-699
7. Bruix J, Fuster J, Llovet JM. Liver transplantation for hepatocellular carcinoma: Foucault pendulum versus evidencebased decision. Liver Transpl 2003; 9: 700-702
8. Bartlett A, Heaton N. Hepatocellular carcinoma: defining the place of surgery in an era of organ shortage. World J Gastroenterol 2008; 14: 4445-4453
9. Yao FY, Ferrell L, Bass NM, Watson JJ, Bacchetti P, Venook A, Ascher NL, Roberts JP. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology 2001; 33: 1394-1403
10. Sotiropoulos GC, Malagó M, Molmenti E, Paul A, Nadalin S, Brokalaki E, Kühl H, Dirsch O, Lang H, Broelsch CE. Liver transplantation for hepatocellular carcinoma in cirrhosis: is clinical tumor classification before transplantation realistic? Transplantation 2005; 79: 483-487
11. Shah SA, Tan JC, McGilvray ID, Cattral MS, Cleary SP, Levy GA, Greig PD, Grant DR. Accuracy of staging as a predictor for recurrence after liver transplantation for hepatocellular carcinoma. Transplantation 2006; 81: 1633-1639
12. Grasso A, Stigliano R, Morisco F, Martines H, Quaglia A, Dhillon AP, Patch D, Davidson BR, Rolles K, Burroughs AK. Liver transplantation and recurrent hepatocellular carcinoma: predictive value of nodule size in a retrospective and explant study. Transplantation 2006; 81: 1532-1541
13. Toso C, Trotter J, Wei A, Bigam DL, Shah S, Lancaster J, Grant DR, Greig PD, Shapiro AM, Kneteman NM. Total tumor volume predicts risk of recurrence following liver transplantation in patients with hepatocellular carcinoma. Liver Transpl 2008; 14: 1107-1115
14. Mazzaferro V, Llovet JM, Miceli R, Bhoori S, Schiavo M, Mariani L, Camerini T, Roayaie S, Schwartz ME, Grazi GL, Adam R, Neuhaus P, Salizzoni M, Bruix J, Forner A, De Carlis L, Cillo U, Burroughs AK, Troisi R, Rossi M, Gerunda GE, Lerut J, Belghiti J, Boin I, Gugenheim J, Rochling F, Van Hoek B, Majno P. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol 2009; 10: 35-43
15. Mazzaferro V, Chun YS, Poon RT, Schwartz ME, Yao FY, Marsh JW, Bhoori S, Lee SG. Liver transplantation for hepatocellular carcinoma. Ann Surg Oncol 2008; 15: 1001-1007
16. Jonas S, Bechstein WO, Steinmüller T, Herrmann M, Radke C, Berg T, Settmacher U, Neuhaus P. Vascular invasion and histopathologic grading determine outcome after liver transplantation for hepatocellular carcinoma in cirrhosis. Hepatology 2001; 33: 1080-1086
17. Cillo U, Vitale A, Bassanello M, Boccagni P, Brolese A, Zanus G, Burra P, Fagiuoli S, Farinati F, Rugge M, D'Amico DF. Liver transplantation for the treatment of moderately or well-differentiated hepatocellular carcinoma. Ann Surg 2004; 239: 150-159
18. Edmondson Ha, Steiner Pe. Primary carcinoma of the liver: a study of 100 cases among 48,900 necropsies. Cancer 1954; 7: 462-503
19. Esnaola NF, Lauwers GY, Mirza NQ, Nagorney DM, Doherty D, Ikai I, Yamaoka Y, Regimbeau JM, Belghiti J, Curley SA, Ellis LM, Vauthey JN. Predictors of microvascular invasion in patients with hepatocellular carcinoma who are candidates for orthotopic liver transplantation. J Gastrointest Surg 2002; 6: 224-232; discussion 232
20. Jonas S, Al-Abadi H, Benckert C, Thelen A, Hippler-Benscheid M, Saribeyoglu K, Radtke B, Pratschke J, Neuhaus P. Prognostic significance of the DNA-index in liver transplantation for hepatocellular carcinoma in cirrhosis. Ann Surg 2009; 250: 1008-1013
21. Fiorentino M, Altimari A, Ravaioli M, Gruppioni E, Gabusi E, Corti B, Vivarelli M, Bringuier PP, Scoazec JY, Grigioni WF, D'Errico-Grigioni A. Predictive value of biological markers for hepatocellular carcinoma patients treated with orthotopic liver transplantation. Clin Cancer Res 2004; 10: 1789-1795
22. Sotiropoulos GC, Lang H, Nadalin S, Neuhäuser M, Molmenti EP, Baba HA, Paul A, Saner FH, Weber F, Hilgard P, Frilling A, Broelsch CE, Malagó M. Liver transplantation for hepatocellular carcinoma: University Hospital Essen experience and metaanalysis of prognostic factors. J Am Coll Surg 2007; 205: 661-675
23. Yang SH, Suh KS, Lee HW, Cho EH, Cho JY, Cho YB, Kim IH, Yi NJ, Lee KU. A revised scoring system utilizing serum alphafetoprotein levels to expand candidates for living donor transplantation in hepatocellular carcinoma. Surgery 2007; 141: 598-609
24. Vibert E, Azoulay D, Hoti E, Iacopinelli S, Samuel D, Salloum C, Lemoine A, Bismuth H, Castaing D, Adam R. Progression of alphafetoprotein before liver transplantation for hepatocellular carcinoma in cirrhotic patients: a critical factor. Am J Transplant 2010; 10: 129-137
25. Schwartz M, Roayaie S, Uva P. Treatment of HCC in patients awaiting liver transplantation. Am J Transplant 2007; 7: 1875-1881
26. Chapman WC, Majella Doyle MB, Stuart JE, Vachharajani N, Crippin JS, Anderson CD, Lowell JA, Shenoy S, Darcy MD, Brown DB. Outcomes of neoadjuvant transarterial chemoembolization to downstage hepatocellular carcinoma before liver transplantation. Ann Surg 2008; 248: 617-625
27. Ravaioli M, Grazi GL, Piscaglia F, Trevisani F, Cescon M, Ercolani G, Vivarelli M, Golfieri R, D'Errico Grigioni A, Panzini I, Morelli C, Bernardi M, Bolondi L, Pinna AD. Liver transplantation for hepatocellular carcinoma: results of down-staging in patients initially outside the Milan selection criteria. Am J Transplant 2008; 8: 2547-2557
28. Toso C, Mentha G, Kneteman NM, Majno P. The place of downstaging for hepatocellular carcinoma. J Hepatol 2010; 52: 930-936
29. Yao FY, Kerlan RK, Hirose R, Davern TJ, Bass NM, Feng S, Peters M, Terrault N, Freise CE, Ascher NL, Roberts JP. Excellent outcome following down-staging of hepatocellular carcinoma prior to liver transplantation: an intention-totreat analysis. Hepatology 2008; 48: 819-827
30. Otto G, Herber S, Heise M, Lohse AW, Mönch C, Bittinger F, Hoppe-Lotichius M, Schuchmann M, Victor A, Pitton M. Response to transarterial chemoembolization as a biological selection criterion for liver transplantation in hepatocellular carcinoma. Liver Transpl 2006; 12: 1260-1267
31. Millonig G, Graziadei IW, Freund MC, Jaschke W, Stadlmann S, Ladurner R, Margreiter R, Vogel W. Response to preoperative chemoembolization correlates with outcome after liver transplantation in patients with hepatocellular carcinoma. Liver Transpl 2007; 13: 272-279
32. Samuel M, Chow PK, Chan Shih-Yen E, Machin D, Soo KC. Neoadjuvant and adjuvant therapy for surgical resection of hepatocellular carcinoma. Cochrane Database Syst Rev 2009; CD001199
33. Olthoff KM, Rosove MH, Shackleton CR, Imagawa DK, Farmer DG, Northcross P, Pakrasi AL, Martin P, Goldstein LI, Shaked A. Adjuvant chemotherapy improves survival after liver transplantation for hepatocellular carcinoma. Ann Surg 1995; 221: 734-741; discussion 731-743
34. Roayaie S, Frischer JS, Emre SH, Fishbein TM, Sheiner PA, Sung M, Miller CM, Schwartz ME. Long-term results with multimodal adjuvant therapy and liver transplantation for the treatment of hepatocellular carcinomas larger than 5 centimeters. Ann Surg 2002; 235: 533-539
35. Pokorny H, Gnant M, Rasoul-Rockenschaub S, Gollackner B, Steiner B, Steger G, Steininger R, Mühlbacher F. Does additional doxorubicin chemotherapy improve outcome in patients with hepatocellular carcinoma treated by liver transplantation? Am J Transplant 2005; 5: 788-794
36. Söderdahl G, Bäckman L, Isoniemi H, Cahlin C, Höckerstedt K, Broomé U, Mäkisalo H, Friman S, Ericzon BG. A prospective, randomized, multi-centre trial of systemic adjuvant chemotherapy versus no additional treatment in liver transplantation for hepatocellular carcinoma. Transpl Int 2006; 19: 288-294
37. Bernal E, Montero JL, Delgado M, Fraga E, Costán G, Barrera P, López-Vallejos P, Solórzano G, Rufián S, Briceño J, Padillo J, López-Cillero P, Marchal T, Muntané J, de la Mata M. Adjuvant chemotherapy for prevention of recurrence of invasive hepatocellular carcinoma after orthotopic liver transplantation. Transplant Proc 2006; 38: 2495-2498
38. Alves RC, Alves D, Guz B, Matos C, Viana M, Harriz M, Terrabuio D, Kondo M, Gampel O, Polletti P. Advanced hepatocellular carcinoma. Review of targeted molecular drugs. Ann Hepatol 2011; 10: 21-27
39. Yokoyama I, Carr B, Saitsu H, Iwatsuki S, Starzl TE. Accelerated growth rates of recurrent hepatocellular carcinoma after liver transplantation. Cancer 1991; 68: 2095-2100
40. Fung JJ, Jain A, Kwak EJ, Kusne S, Dvorchik I, Eghtesad B. De novo malignancies after liver transplantation: a major cause of late death. Liver Transpl 2001; 7: S109-S118
41. Guba M, Graeb C, Jauch KW, Geissler EK. Pro-and anticancer effects of immunosuppressive agents used in organ transplantation. Transplantation 2004; 77: 1777-1782
42. Fung J, Kelly D, Kadry Z, Patel-Tom K, Eghtesad B. Immunosuppression in liver transplantation: beyond calcineurin inhibitors. Liver Transpl 2005; 11: 267-280
43. Yang L. TGFbeta, a potent regulator of tumor microenvironment and host immune response, implication for therapy. Curr Mol Med 2010; 10: 374-380
44. Dantal J, Hourmant M, Cantarovich D, Giral M, Blancho G, Dreno B, Soulillou JP. Effect of long-term immunosuppression in kidney-graft recipients on cancer incidence: randomized comparison of two cyclosporin regimens. Lancet 1998; 351: 623-628
45. Freise CE, Ferrell L, Liu T, Ascher NL, Roberts JP. Effect of systemic cyclosporine on tumor recurrence after liver transplantation in a model of hepatocellular carcinoma. Transplantation 1999; 67: 510-513
46. Vivarelli M, Bellusci R, Cucchetti A, Cavrini G, De Ruvo N, Aden AA, La Barba G, Brillanti S, Cavallari A. Low recurrence rate of hepatocellular carcinoma after liver transplantation: better patient selection or lower immunosuppression? Transplantation 2002; 74: 1746-1751
47. Vivarelli M, Cucchetti A, Piscaglia F, La Barba G, Bolondi L, Cavallari A, Pinna AD. Analysis of risk factors for tumor recurrence after liver transplantation for hepatocellular carcinoma: key role of immunosuppression. Liver Transpl 2005; 11: 497-503
48. Vivarelli M, Cucchetti A, La Barba G, Ravaioli M, Del Gaudio M, Lauro A, Grazi GL, Pinna AD. Liver transplantation for hepatocellular carcinoma under calcineurin inhibitors: reassessment of risk factors for tumor recurrence. Ann Surg 2008; 248: 857-862
49. Boffa DJ, Luan F, Thomas D, Yang H, Sharma VK, Lagman M, Suthanthiran M. Rapamycin inhibits the growth and metastatic progression of non-small cell lung cancer. Clin Cancer Res 2004; 10: 293-300
50. Euvrard S, Ulrich C, Lefrancois N. Immunosuppressants and skin cancer in transplant patients: focus on rapamycin. Dermatol Surg 2004; 30: 628-633
51. Stallone G, Schena A, Infante B, Di Paolo S, Loverre A, Maggio G, Ranieri E, Gesualdo L, Schena FP, Grandaliano G. Sirolimus for Kaposi's sarcoma in renal-transplant recipients. N Engl J Med 2005; 352: 1317-1323
52. Kauffman HM, Cherikh WS, Cheng Y, Hanto DW, Kahan BD. Maintenance immunosuppression with target-of-rapamycin inhibitors is associated with a reduced incidence of de novo malignancies. Transplantation 2005; 80: 883-889
53. Rizell M, Cahlin C, Friman S, Hafström L, Lönn L, Olausson M, Lindner P. Impressive regression of primary liver cancer after treatment with sirolimus. Acta Oncol 2005; 44: 496
54. Stippel DL, Kasper HU, Schleimer K, Töx U, Bangard C, Hölscher AH, Beckurts KT. Successful use of sirolimus in a patient with bulky ovarian metastasis of hepatocellular carcinoma after liver transplantation. Transplant Proc 2005; 37: 2185-2187
55. Elsharkawi M, Staib L, Henne-Bruns D, Mayer J. Complete remission of postransplant lung metastases from hepatocellular carcinoma under therapy with sirolimus and mycophenolate mofetil. Transplantation 2005; 79: 855-857
56. Campistol JM, Eris J, Oberbauer R, Friend P, Hutchison B, Morales JM, Claesson K, Stallone G, Russ G, Rostaing L, Kreis H, Burke JT, Brault Y, Scarola JA, Neylan JF. Sirolimus therapy after early cyclosporine withdrawal reduces the risk for cancer in adult renal transplantation. J Am Soc Nephrol 2006; 17: 581-589
57. Kneteman NM, Oberholzer J, Al Saghier M, Meeberg GA, Blitz M, Ma MM, Wong WW, Gutfreund K, Mason AL, Jewell LD, Shapiro AM, Bain VG, Bigam DL. Sirolimus-based immunosuppression for liver transplantation in the presence of extended criteria for hepatocellular carcinoma. Liver Transpl 2004; 10: 1301-1311
58. Vivarelli M, Dazzi A, Zanello M, Cucchetti A, Cescon M, Ravaioli M, Del Gaudio M, Lauro A, Grazi GL, Pinna AD. Effect of different immunosuppressive schedules on recurrence- free survival after liver transplantation for hepatocellular carcinoma. Transplantation 2010; 89: 227-231
59. Toso C, Merani S, Bigam DL, Shapiro AM, Kneteman NM. Sirolimus-based immunosuppression is associated with increased survival after liver transplantation for hepatocellular carcinoma. Hepatology 2010; 51: 1237-1243