J Liver Cancer.  2023 Sep;23(2):300-315. 10.17998/jlc.2023.08.27.

Management of early-stage hepatocellular carcinoma: challenges and strategies for optimal outcomes

Affiliations
  • 1Department of Gastroenterology and hepatology, Chonnam National University Hospital, Chonnam National University Medical School, Gwangju, Korea

Abstract

Although hepatocellular carcinoma (HCC) is associated with a poor prognosis, management of early-stage HCC is often successful with highly efficacious treatment modalities such as liver transplantation, surgical resection, and radiofrequency ablation. However, unfavorable clinical outcomes have been observed under certain circumstances, even after efficient treatment. Factors that predict unsuitable results after treatment include tumor markers, inflammatory markers, imaging findings reflecting tumor biology, specific outcome indicators for each treatment modality, liver functional reserve, and the technical feasibility of the treatment modalities. Various strategies may overcome these challenges, including the application of reinforced treatment indication criteria with predictive markers reflecting tumor biology, compensation for technical issues with up-to-date technologies, modification of treatment modalities, downstaging with locoregional therapies (such as transarterial chemotherapy or radiotherapy), and recently introduced combination immunotherapies. In this review, we discuss the challenges to achieving optimal outcomes in the management of early-stage HCC and suggest strategies to overcome these obstacles.

Keyword

Carcinoma, hepatocellular; Liver transplantation; Prognosis; Radiofrequency ablation; Hepatectomy

Figure

  • Figure 1. Pitfalls leading to insufficient treatment outcomes in early-stage hepatocellular carcinoma. ICG-R15, indocyanine green retention rate at 15 minutes; ALBI, albumin-bilirubin; LSM, liver stiffness measurement; AFP, alpha-fetoprotien; PIKVA-II, prothrombin induced by vitamin K absence or antagonist-II; NLR, neutrophil-to-lymphocyte ratio; CRP, C-reactive protein; MVI, microvascular invasion; PET, positron emission tomography.


Cited by  2 articles

Radiofrequency for hepatocellular carcinoma larger than 3 cm: potential for applications in daily practice
Ji Hoon Kim, Pil Soo Sung
J Liver Cancer. 2024;24(1):1-2.    doi: 10.17998/jlc.2024.02.13.

Heavy smoking increases early mortality risk in patients with hepatocellular carcinoma after curative treatment
Jaejun Lee, Jong Young Choi, Soon Kyu Lee
J Liver Cancer. 2024;24(2):253-262.    doi: 10.17998/jlc.2024.06.02.


Reference

References

1. Reig M, Forner A, Rimola J, Ferrer-Fàbrega J, Burrel M, GarciaCriado Á, et al. BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol. 2022; 76:681–693.
2. Ueno S, Tanabe G, Nuruki K, Hamanoue M, Komorizono Y, Oketani M, et al. Prognostic performance of the new classification of primary liver cancer of Japan (4th edition) for patients with hepatocellular carcinoma: a validation analysis. Hepatol Res. 2002; 24:395–403.
3. 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.
4. Korean Liver Cancer Association (KLCA); National Cancer Center (NCC) Korea. 2022 KLCA-NCC Korea practice guidelines for the management of hepatocellular carcinoma. Clin Mol Hepatol. 2022; 28:583–705.
5. Lee SG, Hwang S, Moon DB, Ahn CS, Kim KH, Sung KB, et al. Expanded indication criteria of living donor liver transplantation for hepatocellular carcinoma at one large-volume center. Liver Transpl. 2008; 14:935–945.
6. Yao FY, Xiao L, Bass NM, Kerlan R, Ascher NL, Roberts JP. Liver transplantation for hepatocellular carcinoma: validation of the UCSF-expanded criteria based on preoperative imaging. Am J Transplant. 2007; 7:2587–2596.
7. Lee JH, Cho Y, Kim HY, Cho EJ, Lee DH, Yu SJ, et al. Serum tumor markers provide refined prognostication in selecting liver transplantation candidate for hepatocellular carcinoma patients beyond the Milan criteria. Ann Surg. 2016; 263:842–850.
8. Notarpaolo A, Layese R, Magistri P, Gambato M, Colledan M, Magini G, et al. Validation of the AFP model as a predictor of HCC recurrence in patients with viral hepatitis-related cirrhosis who had received a liver transplant for HCC. J Hepatol. 2017; 66:552–559.
9. Kwon CH, Kim DJ, Han YS, Park JB, Choi GS, Kim SJ, et al. HCC in living donor liver transplantation: can we expand the Milan criteria? Dig Dis. 2007; 25:313–319.
10. Suh KS, Cho EH, Lee HW, Shin WY, Yi NJ, Lee KU. Liver transplantation for hepatocellular carcinoma in patients who do not meet the Milan criteria. Dig Dis. 2007; 25:329–333.
11. Choi HJ, Kim DG, Na GH, Han JH, Hong TH, You YK. Clinical outcome in patients with hepatocellular carcinoma after living-donor liver transplantation. World J Gastroenterol. 2013; 19:4737–4744.
12. Carr BI, Kanke F, Wise M, Satomura S. Clinical evaluation of lens culinaris agglutinin-reactive alpha-fetoprotein and des-gammacarboxy prothrombin in histologically proven hepatocellular carcinoma in the United States. Dig Dis Sci. 2007; 52:776–782.
13. Shirabe K, Itoh S, Yoshizumi T, Soejima Y, Taketomi A, Aishima S, et al. The predictors of microvascular invasion in candidates for liver transplantation with hepatocellular carcinoma-with special reference to the serum levels of des-gamma-carboxy prothrombin. J Surg Oncol. 2007; 95:235–240.
14. Todo S, Furukawa H, Tada M; Japanese Liver Transplantation Study Group. Extending indication: role of living donor liver transplantation for hepatocellular carcinoma. Liver Transpl. 2007; 13 Suppl 2:S48–S54.
15. Halazun KJ, Hardy MA, Rana AA, Woodland DC 4th, Luyten EJ, Mahadev S, et al. Negative impact of neutrophil-lymphocyte ratio on outcome after liver transplantation for hepatocellular carcinoma. Ann Surg. 2009; 250:141–151.
16. Harimoto N, Shirabe K, Nakagawara H, Toshima T, Yamashita Y, Ikegami T, et al. Prognostic factors affecting survival at recurrence of hepatocellular carcinoma after living-donor liver transplantation: with special reference to neutrophil/lymphocyte ratio. Transplantation. 2013; 96:1008–1012.
17. An HJ, Jang JW, Bae SH, Choi JY, Yoon SK, Lee MA, et al. Serum C-reactive protein is a useful biomarker for predicting outcomes after liver transplantation in patients with hepatocellular carcinoma. Liver Transpl. 2012; 18:1406–1414.
18. Na GH, Kim DG, Han JH, Kim EY, Lee SH, Hong TH, et al. Inflammatory markers as selection criteria of hepatocellular carcinoma in living-donor liver transplantation. World J Gastroenterol. 2014; 20:6594–6601.
19. Kornberg A, Schernhammer M, Friess H. 18F-FDG-PET for assessing biological viability and prognosis in liver transplant patients with hepatocellular carcinoma. J Clin Transl Hepatol. 2017; 5:224–234.
20. Yaprak O, Acar S, Ertugrul G, Dayangac M. Role of pre-transplant 18F-FDG PET/CT in predicting hepatocellular carcinoma recurrence after liver transplantation. World J Gastrointest Oncol. 2018; 10:336–343.
21. Lee SD, Lee B, Kim SH, Joo J, Kim SK, Kim YK, et al. Proposal of new expanded selection criteria using total tumor size and (18) F-fluorodeoxyglucose - positron emission tomography/computed tomography for living donor liver transplantation in patients with hepatocellular carcinoma: The National Cancer Center Korea criteria. World J Transplant. 2016; 6:411–422.
22. Ling LL, Hsu CC, Yong CC, Elsarawy AM, Chan YC, Wang CC, et al. FDG-PET predicted unfavorable tumor histology in living donor liver transplant recipients: a retrospective cohort study. Int J Surg. 2019; 69:124–131.
23. Kornberg A, Freesmeyer M, Bärthel E, Jandt K, Katenkamp K, Steenbeck J, et al. 18F-FDG-uptake of hepatocellular carcinoma on PET predicts microvascular tumor invasion in liver transplant patients. Am J Transplant. 2009; 9:592–600.
24. Yang SH, Suh KS, Lee HW, Cho EH, Cho JY, Cho YB, et al. The role of (18)F-FDG-PET imaging for the selection of liver transplantation candidates among hepatocellular carcinoma patients. Liver Transpl. 2006; 12:1655–1660.
25. Hwang S, Lee YJ, Kim KH, Ahn CS, Moon DB, Ha TY, et al. Longterm outcome after resection of huge hepatocellular carcinoma ≥ 10 cm: single-institution experience with 471 patients. World J Surg. 2015; 39:2519–2528.
26. Wei CY, Chen PC, Chau GY, Lee RC, Chen PH, Huo TI, et al. Comparison of prognosis between surgical resection and transarterial chemoembolization for patients with solitary huge hepatocellular carcinoma. Ann Transl Med. 2020; 8:238.
27. Yue YY, Zhou WL. Hepatic resection is associated with improved long-term survival compared to radio-frequency ablation in patients with multifocal hepatocellular carcinoma. Front Oncol. 2020; 10:110.
28. Fukami Y, Kaneoka Y, Maeda A, Kumada T, Tanaka J, Akita T, et al. Liver resection for multiple hepatocellular carcinomas: a Japanese nationwide survey. Ann Surg. 2020; 272:145–154.
29. Makuuchi M, Sano K. The surgical approach to HCC: our progress and results in Japan. Liver Transpl. 2004; 10 Suppl 1:S46–S52.
30. Fan ST, Lai EC, Lo CM, Ng IO, Wong J. Hospital mortality of major hepatectomy for hepatocellular carcinoma associated with cirrhosis. Arch Surg. 1995; 130:198–203.
31. Schwarz C, Plass I, Fitschek F, Punzengruber A, Mittlböck M, Kampf S, et al. The value of indocyanine green clearance assessment to predict postoperative liver dysfunction in patients undergoing liver resection. Sci Rep. 2019; 9:8421.
32. Llovet JM, Brú C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis. 1999; 19:329–338.
33. Choi GH, Park JY, Hwang HK, Kim DH, Kang CM, Choi JS, et al. Predictive factors for long-term survival in patients with clinically significant portal hypertension following resection of hepatocellular carcinoma. Liver Int. 2011; 31:485–493.
34. Cucchetti A, Ercolani G, Vivarelli M, Cescon M, Ravaioli M, La Barba G, et al. Impact of model for end-stage liver disease (MELD) score on prognosis after hepatectomy for hepatocellular carcinoma on cirrhosis. Liver Transpl. 2006; 12:966–971.
35. Demirtas CO, D’Alessio A, Rimassa L, Sharma R, Pinato DJ. ALBI grade: evidence for an improved model for liver functional estimation in patients with hepatocellular carcinoma. JHEP Rep. 2021; 3:100347.
36. Cescon M, Colecchia A, Cucchetti A, Peri E, Montrone L, Ercolani G, et al. Value of transient elastography measured with FibroScan in predicting the outcome of hepatic resection for hepatocellular carcinoma. Ann Surg. 2012; 256:706–712. discussion 712-713.
37. Kim SU, Kim BK, Han KH. Clinical application of liver stiffness measurement using transient elastography: a surgical perspective. Digestion. 2013; 88:258–265.
38. Rajakannu M, Cherqui D, Ciacio O, Golse N, Pittau G, Allard MA, et al. Liver stiffness measurement by transient elastography predicts late posthepatectomy outcomes in patients undergoing resection for hepatocellular carcinoma. Surgery. 2017; 162:766–774.
39. Serenari M, Han KH, Ravaioli F, Kim SU, Cucchetti A, Han DH, et al. A nomogram based on liver stiffness predicts postoperative complications in patients with hepatocellular carcinoma. J Hepatol. 2020; 73:855–862.
40. Chan AWH, Zhong J, Berhane S, Toyoda H, Cucchetti A, Shi K, et al. Development of pre and post-operative models to predict early recurrence of hepatocellular carcinoma after surgical resection. J Hepatol. 2018; 69:1284–1293.
41. Tabrizian P, Jibara G, Shrager B, Schwartz M, Roayaie S. Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg. 2015; 261:947–955.
42. Gelli M, Sebagh M, Porcher R, Romanelli E, Vibert E, Sa Cunha A, et al. Liver resection for early hepatocellular carcinoma: preoperative predictors of non transplantable recurrence and implications for treatment allocation. Ann Surg. 2020; 272:820–826.
43. Nitta H, Allard MA, Sebagh M, Golse N, Ciacio O, Pittau G, et al. Ideal surgical margin to prevent early recurrence after hepatic resection for hepatocellular carcinoma. World J Surg. 2021; 45:1159–1167.
44. Wang H, Yu H, Qian YW, Cao ZY, Wu MC, Cong WM. Impact of surgical margin on the prognosis of early hepatocellular carcinoma (≤5 cm): a propensity score matching analysis. Front Med (Lausanne). 2020; 7:139.
45. Kim YS, Lim HK, Rhim H, Lee MW, Choi D, Lee WJ, et al. Ten-year outcomes of percutaneous radiofrequency ablation as first-line therapy of early hepatocellular carcinoma: analysis of prognostic factors. J Hepatol. 2013; 58:89–97.
46. Shiina S, Tateishi R, Arano T, Uchino K, Enooku K, Nakagawa H, et al. Radiofrequency ablation for hepatocellular carcinoma: 10-year outcome and prognostic factors. Am J Gastroenterol. 2012; 107:569–577. quiz 578.
47. Livraghi T, Meloni F, Di Stasi M, Rolle E, Solbiati L, Tinelli C, et al. Sustained complete response and complications rates after radiofrequency ablation of very early hepatocellular carcinoma in cirrhosis: is resection still the treatment of choice? Hepatology. 2008; 47:82–89.
48. Feng K, Yan J, Li X, Xia F, Ma K, Wang S, et al. A randomized controlled trial of radiofrequency ablation and surgical resection in the treatment of small hepatocellular carcinoma. J Hepatol. 2012; 57:794–802.
49. Ng KKC, Chok KSH, Chan ACY, Cheung TT, Wong TCL, Fung JYY, et al. Randomized clinical trial of hepatic resection versus radiofrequency ablation for early-stage hepatocellular carcinoma. Br J Surg. 2017; 104:1775–1784.
50. Chen MS, Li JQ, Zheng Y, Guo RP, Liang HH, Zhang YQ, et al. A prospective randomized trial comparing percutaneous local ablative therapy and partial hepatectomy for small hepatocellular carcinoma. Ann Surg. 2006; 243:321–328.
51. Wang Q, Tang M, Zhang S. Comparison of radiofrequency ablation and surgical resection for hepatocellular carcinoma conforming to the Milan criteria: a meta-analysis. ANZ J Surg. 2021; 91:E432–E438.
52. Lee HW, Lee JM, Yoon JH, Kim YJ, Park JW, Park SJ, et al. A prospective randomized study comparing radiofrequency ablation and hepatic resection for hepatocellular carcinoma. Ann Surg Treat Res. 2018; 94:74–82.
53. Yang HJ, Lee JH, Lee DH, Yu SJ, Kim YJ, Yoon JH, et al. Small single-nodule hepatocellular carcinoma: comparison of transarterial chemoembolization, radiofrequency ablation, and hepatic resection by using inverse probability weighting. Radiology. 2014; 271:909–918.
54. Kang TW, Kim JM, Rhim H, Lee MW, Kim YS, Lim HK, et al. Small hepatocellular carcinoma: radiofrequency ablation versus nonanatomic resection--Propensity score analyses of long-term outcomes. Radiology. 2015; 275:908–919.
55. Kim GA, Shim JH, Kim MJ, Kim SY, Won HJ, Shin YM, et al. Radiofrequency ablation as an alternative to hepatic resection for single small hepatocellular carcinomas. Br J Surg. 2016; 103:126–135.
56. Lee DH, Kim JW, Lee JM, Kim JM, Lee MW, Rhim H, et al. Laparoscopic liver resection versus percutaneous radiofrequency ablation for small single nodular hepatocellular carcinoma: comparison of treatment outcomes. Liver Cancer. 2021; 10:25–37.
57. de Baère T, Risse O, Kuoch V, Dromain C, Sengel C, Smayra T, et al. Adverse events during radiofrequency treatment of 582 hepatic tumors. AJR Am J Roentgenol. 2003; 181:695–700.
58. Lee MW, Kang D, Lim HK, Cho J, Sinn DH, Kang TW, et al. Updated 10-year outcomes of percutaneous radiofrequency ablation as first-line therapy for single hepatocellular carcinoma <3 cm: emphasis on association of local tumor progression and overall survival. Eur Radiol. 2020; 30:2391–2400.
59. Song KD, Lim HK, Rhim H, Lee MW, Kang TW, Paik YH, et al. Hepatic resection vs percutaneous radiofrequency ablation of hepatocellular carcinoma abutting right diaphragm. World J Gastrointest Oncol. 2019; 11:227–237.
60. Lee S, Kang TW, Cha DI, Song KD, Lee MW, Rhim H, et al. Radiofrequency ablation vs. surgery for perivascular hepatocellular carcinoma: propensity score analyses of long-term outcomes. J Hepatol. 2018; 69:70–78.
61. Kang TW, Lim HK, Lee MW, Kim YS, Rhim H, Lee WJ, et al. Aggressive intrasegmental recurrence of hepatocellular carcinoma after radiofrequency ablation: risk factors and clinical significance. Radiology. 2015; 276:274–285.
62. Sumie S, Kuromatsu R, Okuda K, Ando E, Takata A, Fukushima N, et al. Microvascular invasion in patients with hepatocellular carcinoma and its predictable clinicopathological factors. Ann Surg Oncol. 2008; 15:1375–1382.
63. Lim KC, Chow PK, Allen JC, Chia GS, Lim M, Cheow PC, et al. Microvascular invasion is a better predictor of tumor recurrence and overall survival following surgical resection for hepatocellular carcinoma compared to the Milan criteria. Ann Surg. 2011; 254:108–113.
64. Renzulli M, Brocchi S, Cucchetti A, Mazzotti F, Mosconi C, Sportoletti C, et al. Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology. 2016; 279:432–442.
65. Imai K, Yamashita YI, Yusa T, Nakao Y, Itoyama R, Nakagawa S, et al. Microvascular invasion in small-sized hepatocellular carcinoma: significance for outcomes following hepatectomy and radiofrequency ablation. Anticancer Res. 2018; 38:1053–1060.
66. Poté N, Cauchy F, Albuquerque M, Voitot H, Belghiti J, Castera L, et al. Performance of PIVKA-II for early hepatocellular carcinoma diagnosis and prediction of microvascular invasion. J Hepatol. 2015; 62:848–854.
67. Lee S, Kang TW, Song KD, Lee MW, Rhim H, Lim HK, et al. Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Ann Surg. 2021; 273:564–571.
68. Mazzaferro V, Citterio D, Bhoori S, Bongini M, Miceli R, De Carlis L, et al. Liver transplantation in hepatocellular carcinoma after tumour downstaging (XXL): a randomised, controlled, phase 2b/3 trial. Lancet Oncol. 2020; 21:947–956.
69. Yao FY, Fidelman N. Reassessing the boundaries of liver transplantation for hepatocellular carcinoma: where do we stand with tumor down-staging? Hepatology. 2016; 63:1014–1025.
70. Rudnick SR, Russo MW. Liver transplantation beyond or downstaging within the Milan criteria for hepatocellular carcinoma. Expert Rev Gastroenterol Hepatol. 2018; 12:265–275.
71. Park JW, Chen M, Colombo M, Roberts LR, Schwartz M, Chen PJ, et al. Global patterns of hepatocellular carcinoma management from diagnosis to death: the BRIDGE study. Liver Int. 2015; 35:2155–2166.
72. Yao FY, Kerlan RK Jr, Hirose R, Davern TJ 3rd, Bass NM, Feng S, et al. Excellent outcome following down-staging of hepatocellular carcinoma prior to liver transplantation: an intention-to-treat analysis. Hepatology. 2008; 48:819–827.
73. Yao FY, Mehta N, Flemming J, Dodge J, Hameed B, Fix O, et al. Downstaging of hepatocellular cancer before liver transplant: long-term outcome compared to tumors within Milan criteria. Hepatology. 2015; 61:1968–1977.
74. Lopez-Lopez V, Miura K, Kuemmerli C, Capel A, Eshmuminov D, Ferreras D, et al. Selecting the appropriate downstaging and bridging therapies for hepatocellular carcinoma: what is the role of transarterial radioembolization? a pooled analysis. Cancers (Basel). 2023; 15:2122.
75. Kim MA, Jang H, Choi NR, Nam JY, Lee YB, Cho EJ, et al. Yttrium90 radioembolization is associated with better clinical outcomes in patients with hepatocellular carcinoma compared with conventional chemoembolization: a propensity score-matched study. J Hepatocell Carcinoma. 2021; 8:1565–1577.
76. Sandroussi C, Dawson LA, Lee M, Guindi M, Fischer S, Ghanekar A, et al. Radiotherapy as a bridge to liver transplantation for hepatocellular carcinoma. Transpl Int. 2010; 23:299–306.
77. Mohkam K, Golse N, Bonal M, Ledochowski S, Rode A, Selmaji IE, et al. Conformal radiotherapy as a bridge to liver transplantation for hepatocellular carcinoma: is it safe? Future Oncol. 2016; 12:1577–1586.
78. Wong TC, Lee VH, Law AL, Pang HH, Lam KO, Lau V, et al. Prospective study of stereotactic body radiation therapy for hepatocellular carcinoma on waitlist for liver transplant. Hepatology. 2021; 74:2580–2594.
79. Choi JY, Yu JI, Park HC, Kwon CHD, Kim JM, Joh JW, et al. The possibility of radiotherapy as downstaging to living donor liver transplantation for hepatocellular carcinoma with portal vein tumor thrombus. Liver Transpl. 2017; 23:545–551.
80. Han DH, Joo DJ, Kim MS, Choi GH, Choi JS, Park YN, et al. Living donor liver transplantation for advanced hepatocellular carcinoma with portal vein tumor thrombosis after concurrent chemoradiation therapy. Yonsei Med J. 2016; 57:1276–1281.
81. Mourad M, Mabrut JY, Chellakhi M, Lesurtel M, Prevost C, Ducerf C, et al. Neoadjuvant conformal radiotherapy before liver transplantation for hepatocellular carcinoma: a propensity score matched analysis of postoperative morbidity and oncological results. Future Oncol. 2019; 15:2517–2530.
82. Citterio D, Facciorusso A, Sposito C, Rota R, Bhoori S, Mazzaferro V. Hierarchic interaction of factors associated with liver decompensation after resection for hepatocellular carcinoma. JAMA Surg. 2016; 151:846–853.
83. Witowski J, Rubinkiewicz M, Mizera M, Wysocki M, Gajewska N, Sitkowski M, et al. Meta-analysis of short- and long-term outcomes after pure laparoscopic versus open liver surgery in hepatocellular carcinoma patients. Surg Endosc. 2019; 33:1491–1507.
84. Ciria R, Gomez-Luque I, Ocaña S, Cipriani F, Halls M, Briceño J, et al. A systematic review and meta-analysis comparing the short- and long-term outcomes for laparoscopic and open liver resections for hepatocellular carcinoma: updated results from the European guidelines meeting on laparoscopic liver surgery, Southampton, UK, 2017. Ann Surg Oncol. 2019; 26:252–263.
85. Oh JH, Sinn DH, Choi GS, Kim JM, Joh JW, Kang TW, et al. Comparison of outcome between liver resection, radiofrequency ablation, and transarterial therapy for multiple small hepatocellular carcinoma within the Milan criteria. Ann Surg Treat Res. 2020; 99:238–246.
86. Vouche M, Lewandowski RJ, Atassi R, Memon K, Gates VL, Ryu RK, et al. Radiation lobectomy: time-dependent analysis of future liver remnant volume in unresectable liver cancer as a bridge to resection. J Hepatol. 2013; 59:1029–1036.
87. Braat AJAT, Huijbregts JE, Molenaar IQ, Rinkes IHMB, van den Bosch MAAJ, Lam MGEH. Hepatic radioembolization as a bridge to liver surgery. Front Oncol. 2014; 4:199.
88. Gaba RC, Lewandowski RJ, Kulik LM, Riaz A, Ibrahim SM, Mulcahy MF, et al. Radiation lobectomy: preliminary findings of hepatic volumetric response to lobar yttrium-90 radioembolization. Ann Surg Oncol. 2009; 16:1587–1596.
89. Lee HS, Choi GH, Choi JS, Kim KS, Han KH, Seong J, et al. Surgical resection after down-staging of locally advanced hepatocellular carcinoma by localized concurrent chemoradiotherapy. Ann Surg Oncol. 2014; 21:3646–3653.
90. Hamaoka M, Kobayashi T, Kuroda S, Iwako H, Okimoto S, Kimura T, et al. Hepatectomy after down-staging of hepatocellular carcinoma with portal vein tumor thrombus using chemoradiotherapy: a retrospective cohort study. Int J Surg. 2017; 44:223–228.
91. Chong JU, Choi GH, Han DH, Kim KS, Seong J, Han KH, et al. Downstaging with localized concurrent chemoradiotherapy can identify optimal surgical candidates in hepatocellular carcinoma with portal vein tumor thrombus. Ann Surg Oncol. 2018; 25:3308–3315.
92. Wei X, Jiang Y, Zhang X, Feng S, Zhou B, Ye X, et al. Neoadjuvant three-dimensional conformal radiotherapy for resectable hepatocellular carcinoma with portal vein tumor thrombus: a randomized, open-label, multicenter controlled study. J Clin Oncol. 2019; 37:2141–2151.
93. Bargellini I, Sacco R, Bozzi E, Bertini M, Ginanni B, Romano A, et al. Transarterial chemoembolization in very early and early-stage hepatocellular carcinoma patients excluded from curative treatment: a prospective cohort study. Eur J Radiol. 2012; 81:1173–1178.
94. Bai S, Hu L, Liu J, Sun M, Sun Y, Xue F. Prognostic nomograms combined adjuvant lenvatinib for hepatitis B virus-related hepatocellular carcinoma with microvascular invasion after radical resection. Front Oncol. 2022; 12:919824.
95. Dai MG, Liu SY, Lu WF, Liang L, Ye B. Survival benefits from adjuvant lenvatinib for patients with hepatocellular carcinoma and microvascular invasion after curative hepatectomy. Clin Med Insights Oncol. 2023; 17:11795549231180351.
96. Hack SP, Spahn J, Chen M, Cheng AL, Kaseb A, Kudo M, et al. IMbrave 050: a phase III trial of atezolizumab plus bevacizumab in high-risk hepatocellular carcinoma after curative resection or ablation. Future Oncol. 2020; 16:975–989.
97. Bai S, Yang P, Xie Z, Li J, Lei Z, Xia Y, et al. Preoperative estimated risk of microvascular invasion is associated with prognostic differences following liver resection versus radiofrequency ablation for early hepatitis B virus-related hepatocellular carcinoma. Ann Surg Oncol. 2021; 28:8174–8185.
98. Wang Y, Deng T, Zeng L, Chen W. Efficacy and safety of radiofrequency ablation and transcatheter arterial chemoembolization for treatment of hepatocellular carcinoma: a meta-analysis. Hepatol Res. 2016; 46:58–71.
99. Yan S, Xu D, Sun B. Combination of radiofrequency ablation with transarterial chemoembolization for hepatocellular carcinoma: a meta-analysis. Dig Dis Sci. 2013; 58:2107–2113.
100. Chen SL, Xiao H, Xie ZL, Shen JX, Chen ZB, Wang YQ, et al. The presence of microvascular invasion guides treatment strategy in recurrent HBV-related HCC. Eur Radiol. 2020; 30:3473–3485.
101. Song I, Rhim H, Lim HK, Kim YS, Choi D. Percutaneous radiofrequency ablation of hepatocellular carcinoma abutting the diaphragm and gastrointestinal tracts with the use of artificial ascites: safety and technical efficacy in 143 patients. Eur Radiol. 2009; 19:2630–2640.
102. Ahn SJ, Lee JM, Lee DH, Lee SM, Yoon JH, Kim YJ, et al. Real-time US-CT/MR fusion imaging for percutaneous radiofrequency ablation of hepatocellular carcinoma. J Hepatol. 2017; 66:347–354.
103. Calandri M, Mauri G, Yevich S, Gazzera C, Basile D, Gatti M, et al. Fusion imaging and virtual navigation to guide percutaneous thermal ablation of hepatocellular carcinoma: a review of the literature. Cardiovasc Intervent Radiol. 2019; 42:639–647.
104. Lee SK, Chung DJ, Cho SH. A real-world comparative study of microwave and radiofrequency ablation in treatment-naïve and recurrent hepatocellular carcinoma. J Clin Med. 2022; 11:302.
105. Park SJ, Cho EJ, Lee JH, Yu SJ, Kim YJ, Yoon JH, et al. Switching monopolar no-touch radiofrequency ablation using octopus electrodes for small hepatocellular carcinoma: a randomized clinical trial. Liver Cancer. 2021; 10:72–81.
106. Suh YS, Choi JW, Yoon JH, Lee DH, Kim YJ, Lee JH, et al. No-touch vs. conventional radiofrequency ablation using twin internally cooled wet electrodes for small hepatocellular carcinomas: a randomized prospective comparative study. Korean J Radiol. 2021; 22:1974–1984.
107. Lee DH, Lee MW, Kim PN, Lee YJ, Park HS, Lee JM. Outcome of no-touch radiofrequency ablation for small hepatocellular carcinoma: a multicenter clinical trial. Radiology. 2021; 301:229–236.
108. Kim N, Cheng J, Jung I, Liang J, Shih YL, Huang WY, et al. Stereotactic body radiation therapy vs. radiofrequency ablation in Asian patients with hepatocellular carcinoma. J Hepatol. 2020; 73:121–129.
109. Shin HS, Lee SH, Jun BG, Kim HS, Kang SH, Park JY, et al. Stereotactic body radiotherapy versus radiofrequency ablation as initial treatment of small hepatocellular carcinoma. Eur J Gastroenterol Hepatol. 2022; 34:1187–1194.
110. Yang D, Converse MC, Mahvi DM, Webster JG. Measurement and analysis of tissue temperature during microwave liver ablation. IEEE Trans Biomed Eng. 2007; 54:150–155.
111. Violi NV, Duran R, Guiu B, Cercueil JP, Aubé C, Digklia A, et al. Efficacy of microwave ablation versus radiofrequency ablation for the treatment of hepatocellular carcinoma in patients with chronic liver disease: a randomised controlled phase 2 trial. Lancet Gastroenterol Hepatol. 2018; 3:317–325.
112. Chong CCN, Lee KF, Cheung SYS, Chu CCM, Fong AKW, Wong J, et al. Prospective double-blinded randomized controlled trial of microwave versus radiofrequency ablation for hepatocellular carcinoma (McRFA trial). HPB (Oxford). 2020; 22:1121–1127.
113. Gupta P, Maralakunte M, Kumar-M P, Chandel K, Chaluvashetty SB, Bhujade H, et al. Overall survival and local recurrence following RFA, MWA, and cryoablation of very early and early HCC: a systematic review and Bayesian network meta-analysis. Eur Radiol. 2021; 31:5400–5408.
114. Tan W, Deng Q, Lin S, Wang Y, Xu G. Comparison of microwave ablation and radiofrequency ablation for hepatocellular carcinoma : a systematic review and meta-analysis. Int J Hyperthermia. 2019; 36:264–272.
115. Ahmed M, Brace CL, Lee FT Jr, Goldberg SN. Principles of and advances in percutaneous ablation. Radiology. 2011; 258:351–369.
116. Wang C, Wang H, Yang W, Hu K, Xie H, Hu KQ, et al. Multicenter randomized controlled trial of percutaneous cryoablation versus radiofrequency ablation in hepatocellular carcinoma. Hepatology. 2015; 61:1579–1590.
117. Kim R, Kang TW, Cha DI, Song KD, Lee MW, Rhim H, et al. Percutaneous cryoablation for perivascular hepatocellular carcinoma: therapeutic efficacy and vascular complications. Eur Radiol. 2019; 29:654–662.
118. Ko SE, Lee MW, Rhim H, Kang TW, Song KD, Cha DI, et al. Comparison of procedure-related complications between percutaneous cryoablation and radiofrequency ablation for treating periductal hepatocellular carcinoma. Int J Hyperthermia. 2020; 37:1354–1361.
119. DuBay D, Sandroussi C, Sandhu L, Cleary S, Guba M, Cattral MS, et al. Liver transplantation for advanced hepatocellular carcinoma using poor tumor differentiation on biopsy as an exclusion criterion. Ann Surg. 2011; 253:166–172.
120. Toso C, Meeberg G, Hernandez-Alejandro R, Dufour JF, Marotta P, Majno P, et al. Total tumor volume and alpha-fetoprotein for selection of transplant candidates with hepatocellular carcinoma: a prospective validation. Hepatology. 2015; 62:158–165.
121. Wan P, Xia Q, Zhang JJ, Li QG, Xu N, Zhang M, et al. Liver transplantation for hepatocellular carcinoma exceeding the Milan criteria: a single-center experience. J Cancer Res Clin Oncol. 2014; 140:341–348.
122. Duvoux C, Roudot-Thoraval F, Decaens T, Pessione F, Badran H, Piardi T, et al. Liver transplantation for hepatocellular carcinoma: a model including α-fetoprotein improves the performance of Milan criteria. Gastroenterology. 2012; 143:986–994.e3. quiz e14-e15.
123. Kaido T, Ogawa K, Mori A, Fujimoto Y, Ito T, Tomiyama K, et al. Usefulness of the Kyoto criteria as expanded selection criteria for liver transplantation for hepatocellular carcinoma. Surgery. 2013; 154:1053–1060.
124. Ito T, Takada Y, Ueda M, Haga H, Maetani Y, Oike F, et al. Expansion of selection criteria for patients with hepatocellular carcinoma in living donor liver transplantation. Liver Transpl. 2007; 13:1637–1644.
125. Soejima Y, Taketomi A, Yoshizumi T, Uchiyama H, Aishima S, Terashi T, et al. Extended indication for living donor liver transplantation in patients with hepatocellular carcinoma. Transplantation. 2007; 83:893–899.
126. Shindoh J, Sugawara Y, Nagata R, Kaneko J, Tamura S, Aoki T, et al. Evaluation methods for pretransplant oncologic markers and their prognostic impacts in patient undergoing living donor liver transplantation for hepatocellular carcinoma. Transpl Int. 2014; 27:391–398.
Full Text Links
  • JLC
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr