Treatment of small hepatocellular carcinoma: A comparison of techniques and long-term results

European Journal of Gastroenterology and Hepatology

Volumn 18, Issue 6, 2006, Pages 659-672

  Saverio Ferrari, Francesco ^a   Stella, Andrea ^a   Pasquinucci, Paolo ^a   Vigni, Francesco ^a   Civeli, Letizia ^a   Pieraccini, Massimo ^a   Magnolfi, Fabrizio ^b  

^a UNIVERSITY HOSPITAL OF SIENA   (Italy)

^b St Donato Hospital   (Italy)

Author keywords

Chemotherapeutic embolization; Interstitial therapy; Interventional procedures; Lasers; Liver neoplasm; Percutaneous ethanol injection; Therapy

Indexed keywords

ALCOHOL; BUPRENORPHINE; CISPLATIN; DOXORUBICIN; EPIRUBICIN; FARMARUBICINA; IODINATED POPPYSEED OIL; IOPROMIDE; MITOMYCIN C; SHU 508;

ADULT; AGED; ARTICLE; CANCER SURVIVAL; CANCER THERAPY; CHEMOEMBOLIZATION; COMPUTER ASSISTED TOMOGRAPHY; FEMALE; HUMAN; LASER SURGERY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER NECROSIS; LIVER NODULE; MAJOR CLINICAL STUDY; MALE; PERCUTANEOUS ETHANOL INJECTION; PRIORITY JOURNAL;

EID: 33744463115     PISSN: 0954691X     EISSN: None     Source Type: Journal    
DOI: 10.1097/00042737-200606000-00014     Document Type: Article

References (70)

1. Colombo M, Franchis R, Del Ninno E, Sangiovanni A, De Fazio C, Tommasini M, et al. Hepatocellular carcinoma in Italian patients with cirrhosis. N Engl J Med 1991; 325:675-680.
2. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001; 94:153-156.
3. Donato F, Boffetta P, Puoti M. A meta-analysis of epidemiological studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma. Int J Cancer 1998; 75:347-354.
4. Bolondi L. Screening for hepatocellular carcinoma in cirrhosis. J Hepatol 2003; 39:1076-1084.
5. Sheu JC, Huang GT, Chou HC, Lee PH, Wang JT, Lee HS, et al. Multiple hepatocellular carcinomas at the early stage have different clonality. Gastroenterology 1993; 105:1471-1476.
6. Takenaka K, Adachi E, Nishizaki T, Hiroshige K, Ikeda T, Tsuneyoshi M, et al. Possible multicentric occurrence of hepatocellular carcinoma: a clinicopathological study. Hepatology 1994; 19:889-894.
7. Ryu M, Shimamura Y, Kinoshita T, Konishi M, Kawano N, Iwasaki M, et al. Therapeutic results of resection, transcatheter arterial embolization and percutaneous transhepatic ethanol injection in 3225 patients with hepatocellular carcinoma: a retrospective multicenter study. Jpn J Clin Oncol 1997; 27:251-257.
8. Yu AS, Keeffe EB. Management of hepatocellular carcinoma. Rev Gastroenterol Disord 2003; 3:8-24.
9. A new prognostic system for hepatocellular carcinoma: a retrospective study of 453 patients. The Cancer of the Liver Italian Program (CLIP) investigator [no authors listed]. Hepatology 1998; 28:751-755.
10. Hemming AW, Cattral MS, Reed AI, Van Der Werf WJ, Greig PD, Howard RJ. Liver transplantation for hepatocellular carcinoma. Ann Surg 2001; 233:652-659.
11. Livraghi T. Treatment of hepatocellular carcinoma by interventional methods. Eur Radiol 2001; 11:2207-2219.
12. Poon RT, Fan ST, Tsang FH, Wong J. Locoregional therapies for hepatocellular carcinoma: a critical review from the surgeon's perspective. Ann Surg 2002; 235:466-486.
13. Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001; 35:421-430.
14. Veltri A, Grosso M, Martina MC, Ciancio A, David E, Salizzoni M, et al. Effect of preoperative radiological treatment of hepatocellular carcinoma before liver transplantation: a retrospective study. Cardiovasc Intervent Radiol 1998; 21:393-398.
15. Vilana R, Llovet JM, Bianchi L, Sanchez M, Pages M, Sala M, et al. Contrast-enhanced power Doppler sonography and helical computed tomography for assessment of vascularity of small hepatocellular carcinomas before and after percutaneous ablation. J Clin Ultrasound 2003; 31:119-128.
16. Quaia E, Forgacs B, Calderan L, Bertolotto M, Pozzi Mucelli R. Characterization of focal hepatic lesions in cirrhotic patients by Pulse Inversion Harmonic Imaging US contrast specific technique with Levovist. Radiol Med 2002; 104:285-294.
17. Pacella CM, Bizzarri G, Magnolfi F, Cecconi P, Caspani B, Anelli V, et al. Laser thermal ablation in the treatment of small hepatocellular carcinoma: long-term results in 74 patients. Radiology 2001; 221:712-720.
18. Pacella CM, Bizzarri G, Anelli V, Valle D, Fabbrini R, Bianchini A, et al. Evaluation of the vascular pattern of hepatocellular carcinoma with dynamic computed tomography and its use in identifying optimal temporal windows for helical computed tomography. Eur Radiol 1998; 8:30-35.
19. Lim JH, Cho JM, Kim EY, Park CK. Dysplastic nodules in liver cirrhosis: evaluation of hemodynamics with CT during arterial portography and CT hepatic arteriography. Radiology 2000; 214:869-874.
20. Baron RL, Oliver JH 3rd, Dodd GD 3rd, Nalesnik M, Holbert BL, Carr B. Hepatocellular carcinoma: evaluation with biphasic, contrast-enhanced, helical CT. Radiology 1996; 199:505-511.
21. Uchida H, Ohishi H, Matsuo N, Nishimine K, Yoshioka T, Ohishi H, et al. Transcatheter hepatic segmental arterial embolization using lipiodol mixed with an anticancer drug and Gelfoam particles for hepatocellular carcinoma. Cardiovasc Intervent Radiol 1990; 13:140-145.
22. Stuart K. Chemoembolization in the management of liver tumors. Oncologist 2003; 8:425-437.
23. Bartolozzi C, Lencioni R, Caramella D, Vignali C, Cioni R, Mazzeo S, et al. Treatment of large HCC: transcatheteral arterial chemoembolization combined with percutaneous ethanol injection versus repeated transcatheteral arterial chemoembolization. Radiology 1995; 197:812-818.
24. Pacella CM, Bizzarri G, Ferrari FS, Anelli V, Valle D, Bianchini A, et al. Interstitial photocoagulation with laser in the treatment of liver metastasis. Radiol Med 1996; 92:438-447.
25. Giorgio A, Tarantino L, De Stefano G, Farella N, Catalano O, Cusati B, et al. Interstitial laser photocoagulation under ultrasound guidance of liver tumors: result in 104 treated patients. Eur J Ultrasound 2000; 11:181-188.
26. Ferrari FS, Burresi F, Poggianti G, Stefani P. Interstitial laser photocoagulation of hepatocellular carcinoma. In: Bartolozzi C, Lencioni R, editors. Liver malignancies - diagnostic and interventional radiology. Berlin: Springer-Verlag; 1999. pp. 311-319.
27. Vogl TJ, Eichler K, Straub R, Engelmann K, Zangos S, Woitashek D, et al. Laser-induced thermotherapy of malignant liver tumors: general principals, equipment(s), procedure(s) - side effects, complications and results. Eur J Ultrasound 2001; 13:117-127.
28. Pacella CM, Bizzarri G, Cecconi P, Caspani B, Magnolfi F, Bianchini A, et al. Hepatocellular carcinoma: long-term results of combined treatment with laser thermal ablation and transcatheter arterial chemoembolization. Radiology 2001; 219:669-678.
29. Ishii H, Okada S, Okusaka T, Yoshimori M, Nakasuka H, Shimada K, et al. Needle tract implantation of hepatocellular carcinoma after percutaneous ethanol injection. Cancer 1998; 82:1638-1642.
30. Cardinale L, Castiglione V. Subcutaneous neoplasm seeding along the needle track. A rare complication following the percutaneous alcoholization of a hepatocarcinoma. Radiol Med 1995; 89:557-559.
31. Shimada M, Maeda T, Saitoh A, Morotomi I, Kano T. Needle track seeding after percutaneous ethanol injection therapy for small hepatocellular carcinoma. J Surg Oncol 1995; 58:278-281.
32. Solbiati L, Goldberg SN, Ierace T, Dellanoce M, Livraghi T, Gazelle GS. Radio-frequency ablation of hepatic metastases: postprocedural assessment with a US microbubble contrast agent - early experience. Radiology 1999; 211:643-649.
33. Choi D, Lim HK, Kim SH, Lee WJ, Yang HJ, Lee JY, et al. Hepatocellular carcinoma treated with percutaneous radio-frequency ablation: usefulness of power doppler US with a microbubble contrast agent in evaluating therapeutic response - preliminary results. Radiology 2000; 217:558-563.
34. Ding H, Kudo M, Onda H, Suetomi Y, Minami Y, Chung H, et al. Evaluation of posttreatment response of hepatocellular carcinoma with contrast enhanced coded phase-inversion harmonic US: comparison with dynamic CT. Radiology 2001; 221:721-730.
35. Lim HK, Choi D, Lee WJ, Kim SH, Lee SJ, Jang HJ, et al. Hepatocellular carcinoma treated with percutaneous radio-frequency ablation: evaluation with follow-up multiphase helical CT. Radiology 2001; 221:447-454.
36. Choi BI, Kim HC, Han JK, Park JH, Kim YI, Kim ST, et al. Therapeutic effect of transcatheter oil embolization therapy for encapsulated nodular hepatocellular carcinoma: CT and pathologic findings. Radiology 1992; 182:709-713.
37. Miller AB, Hoogstraten B, Staquet M, Winkler A. Reporting results of cancer treatment. Cancer 1981; 47:207-214.
38. Kopp AF, Heuschmid M, Claussen CD. Multidetector helical CT of the liver for tumor detection and characterization. Eur Radiol 2002; 12:745-752.
39. Ishii H, Okada S, Nose H, Okusaka T, Yoshimori M, Takayama T, et al. Local recurrence of hepatocellular carcinoma after percutaneous ethanol injection. Cancer 1996; 77:1792-1796.
40. Kuriyama H, Okada S, Okusaka T, Ueno H, Ikeda M. Prognostic factors in patients with small hepatocellular carcinoma treated by percutaneous ethanol injection. J Gastroenterol Hepatol 2002; 17:1205-1210.
41. The Liver Cancer Study Group of Japan. Predictive factors for long-term prognosis after partial hepatectomy for patients with hepatocellular carcinoma in Japan. Cancer 1994; 74:2772-2780.
42. Villa E, Moles A, Ferretti I, Buttafoco P, Grottola A, Del Buono M, et al. Natural history of inoperable hepatocellular carcinoma: estrogen receptors' status in the tumor is the strongest prognostic factor for survival. Hepatology 2000; 32:233-238.
43. Bruix J, Fuster J, Llovet JM. Liver transplantation for hepatocellular carcinoma: foucalt pendulum versus evidence-based decision. Liver Transplantation 2003; 9:700-702.
44. Bismuth H, Chiche L, Adam R, Castaing D, Diamond T, Dennison A. Liver resection versus transplantation for hepatocellular carcinoma in cirrhotic patients. Ann Surg 1993; 218:145-151.
45. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 1996; 334:693-699.
46. Llovet JM, Bruix J, Fuster J, Castells A, Garcia-Valdecasas JC, Grande L, et al. Liver transplantation for treatment of small hepatocellular carcinoma: the tumor-node-metastasis classification does not have prognostic power. Hepatology 1998; 27:1572-1577.
47. Jonas S, Bechstein WO, Steinmuller T, Herrmann M, Radke C, Berg T, et al. Vascular invasion and histopathologic grading determine outcome after liver transplantation for hepatocellular carcinoma in cirrhosis. Hepatology 2001; 33:1080-1086.
48. Figueras J, Ibanez L, Ramos E, Jaurrieta E, Ortiz-de-Urbina J, Pardo F, et al. Selection criteria for liver transplantation in early-stage hepatocellular carcinoma with cirrhosis: results of a multicenter study. Liver Transpl 2001; 7:877-883.
49. Llovet JM, Fuster J, Bruix J. Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology 1999; 30:1434-1440.
50. Graziadei IW, Sandmueller H, Waldenberger P, Koenigsrainer A, Nachbaur K, Jaschke W, et al. Chemoembolization followed by liver transplantation for hepatocellular carcinoma impedes tumor progression while on the waiting list and leads to excellent outcome. Liver Transpl 2003; 9:557-563.
51. Llovet JM, Mas X, Aponte JJ, Fuster J, Navasa M, Christensen E, et al. Cost effectiveness of adjuvant therapy for hepatocellular carcinoma during the waiting list for liver transplantation. Gut 2002; 50:123-128.
52. Lau WY, Leung TW, Yu SC, Ho SK. Percutaneous local ablative therapy for hepatocellular carcinoma: a review and look into the future. Ann Surg 2003; 237:171-179.
53. Livraghi T, Giorgio A, Marin G, Salmi A, De Sio I, Bolondi L, et al. Hepatocellular carcinoma and cirrhosis in 746 patients: long-term results of percutaneous ethanol injection. Radiology 1995; 197:101-108.
54. Lau H, Fan ST, Ng IO, Wong J. Long term prognosis after hepatectomy for hepatocellular carcinoma: a survival analysis of 204 consecutive patients. Cancer 1998; 83:2302-2311.
55. Higuchi T, Kikuchi M, Okazaki M. Hepatocellular carcinoma after transcatheter hepatic arterial embolization: a histopathologic study of 84 resected cases. Cancer 1994; 73:2259-2267.
56. Groupe d'Etude et de Traitement du Carcinome Hèpatocellulaire. A comparison of lipiodol chemoembolization and conservative treatment for unresectable hepatocellular carcinoma. N Engl J Med 1995; 332:1256-1261.
57. Bruix J, Llovet JM, Castells A, Montana X, Bru C, Ayuso MC, et al. Transarterial embolization versus symptomatic treatment in patients with advanced hepatocellular carcinoma. Results of a randomized controlled trial in a single institution. Hepatology 1998; 27:1578-1583.
58. Qian J, Feng GS, Vogl T. Combined interventional therapies of hepatocellular carcinoma. World J Gastroenterol 2003; 9:1885-1891.
59. Shiina S, Tagawa K, Unuma T, Takanashi R, Yoshiura K, Komatsu Y, et al. Percutaneous ethanol injection therapy for hepatocellular carcinoma: a histopathologic study. Cancer 1991; 68:1524-1530.
60. Ebara M, Ohto M, Sugiura N, Kita K, Yoshikawa M, Okuda K, et al. Percutaneous ethanol injection for the treatment of small hepatocellular carcinoma: study of 95 patients. J Gastroenterol Hepatol 1990; 5:616-626.
61. Livraghi T, Bolondi L, Lazzaroni S, Marin C, Morabito A, Rapaccini GL, et al. Percutaneous ethanol injection in the treatment of hepatocellular carcinoma in cirrhosis: a study on 207 patients. Cancer 1992; 69:925-929.
62. Lin SM, Lin DY, Lin CJ. Percutaneous ethanol injection treatment in 47 cirrhotic patients with hepatocellular carcinoma 5 cm or less: a long-term result. Int J Clin Pract 1999; 53:257-262.
63. Lencioni R, Pinto F, Armillotta N, Bassi AM, Moretti M, Di Giulio M, et al. Long-term results of percutaneous ethanol injection therapy for hepatocellular carcinoma in cirrhosis: a European experience. Eur Radiol 1997; 7:514-519.
64. Livraghi T, Goldberg SN, Lazzaroni S, Meloni F, Solbiati L, Gazelle GS. Small hepatocellular carcinoma: treatment with radio-frequency ablation versus ethanol injection. Radiology 1999; 210:655-661.
65. Lencioni RA, Allgaier HP, Cioni D, Olschewski M, Deibert P, Crocetti L, et al. Small hepatocellular carcinoma in cirrhosis: randomized comparison of radio-frequency thermal ablation versus percutaneous ethanol injection. Radiology 2003; 228:235-240.
66. Buscarini L, Buscarini E, Di Stasi, Vallisa D, Quaretti P, Rocca A. Percutaneous radiofrequency ablation of small hepatocellular carcinoma: long term results. Eur Radiol 2001; 11:914-921.
67. Livraghi T, Solbiati L, Meloni MF, Gazelle GS, Halpern EF, Goldberg SN. Treatment of focal liver tumors with percutaneous radio-frequency ablation: complications encountered in a multicenter study. Radiology 2003; 226:441-451.
68. Lencioni R, Paolicchi A, Moretti M, Pinto F, Armillotta N, Di Giulio M, et al. Combined transcatheter arterial chemoembolization and percutaneous ethanol injection for the treatment of large hepatocellular carcinoma: local therapeutic effect and long-term survival rate. Eur Radiol 1998; 8:439-444.
69. Rossi S, Garbagnati F, Lencioni R, Allgaier HP, Marchiano A, Fornari F, et al. Percutaneous radiofrequency thermal ablation of nonresectable hepatocellular carcinoma after occlusion of tumor blood supply. Radiology 2000; 217:119-126.
70. Llovet JM, Bustamante J, Castells A, Vilana R, Ayuso Mdel C, Sala M, et al. Natural history of untreated nonsurgical hepatocellular carcinoma: rationale for the design and evaluation of therapeutic trials. Hepatology 1999; 29:62-67.