Hepatic resection versus transarterial chemoembolization for the initial treatment of hepatocellular carcinoma: A systematic review and meta-analysis

Oncotarget

Volumn 6, Issue 21, 2015, Pages 18715-18733

  Qi, Xingshun ^a   Wang, Diya ^b   Su, Chunping ^b   Li, Hongyu ^a   Guo, Xiaozhong ^a  

^a GENERAL HOSPITAL OF NORTHERN THEATER COMMAND   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

BCLC stage; Chemoembolization; Hepatocellular carcinoma; Resection; Survival

Indexed keywords

ARTICLE; CANCER STAGING; CHEMOEMBOLIZATION; HUMAN; INTERMETHOD COMPARISON; LIVER CELL CARCINOMA; LIVER RESECTION; OVERALL SURVIVAL; PORTAL VEIN TUMOR THROMBUS; SENSITIVITY ANALYSIS; SURVIVAL RATE; SURVIVAL TIME; SYSTEMATIC REVIEW; TUMOR THROMBUS; CARCINOMA, HEPATOCELLULAR; LIVER NEOPLASMS; META ANALYSIS; MORTALITY; OUTCOME ASSESSMENT; PROCEDURES; PROPORTIONAL HAZARDS MODEL; STATISTICS AND NUMERICAL DATA; SURVIVAL ANALYSIS;

CARCINOMA, HEPATOCELLULAR; CHEMOEMBOLIZATION, THERAPEUTIC; HEPATECTOMY; HUMANS; LIVER NEOPLASMS; NEOPLASM STAGING; OUTCOME ASSESSMENT (HEALTH CARE); PROPORTIONAL HAZARDS MODELS; SURVIVAL ANALYSIS; SURVIVAL RATE;

EID: 84938818924     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4134     Document Type: Article

References (67)

1. Bruix J and Sherman M. Management of hepatocellular carcinoma: an update. Hepatology. 2011; 53:1020-1022.
2. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2012; 56:908-943.
3. Farinati F, Vanin V, Giacomin A, Pozzan C, Cillo U, Vitale A, Di Nolfo AM, Del Poggio P, Benvegnu L, Rapaccini G, Zoli M, Borzio F, Giannini EG, Caturelli E and Trevisani F. BCLC stage B hepatocellular carcinoma and transcatheter arterial chemoembolization: a 20-year survey by the Italian Liver Cancer group. Liver Int. 2015; 35:223-231.
4. Vitale A, Burra P, Frigo AC, Trevisani F, Farinati F, Spolverato G, Volk M, Giannini EG, Ciccarese F, Piscaglia F, Rapaccini GL, Di Marco M, Caturelli E, Zoli M, Borzio F, Cabibbo G, et al. Survival benefit of liver resection for patients with hepatocellular carcinoma across different Barcelona Clinic Liver Cancer stages: A multicentre study. J Hepatol. 2015; 62:617-624.
5. Roayaie S, Jibara G, Tabrizian P, Park JW, Yang J, Yan L, Schwartz M, Han G, Izzo F, Chen M, Blanc JF, Johnson P, Kudo M, Roberts LR and Sherman M. The Role of hepatic resection in the treatment of hepatocellular cancer. Hepatology. 2015.
6. Cheng SQ, Wu MC, Chen H, Shen F, Yang JH, Cong WM, Zhao YX, Wang PJ and Ding GH. Hepatocellular carcinoma with tumor thrombi in the portal vein. A comparison of therapeutic effects by different treatments. Zhonghua zhong liu za zhi [Chinese journal of oncology]. 2005; 27:183-185.
7. Choi SH, Choi GH, Kim SU, Park JY, Joo DJ, Ju MK, Kim MS, Choi JS, Han KH and Kim SI. Role of surgical resection for multiple hepatocellular carcinomas. World J Gastroenterol. 2013; 19:366-374.
8. Ciria R, Gallardo AB, Cabrera J, Luque A, Ayllon MD, Rodriguez-Peralvarez M, Montero JL, Lopez-Cillero P, De La Mata M and Briceno J. Modern surgical liver resections offer better results than transarterial chemoembolization in cirrhotic patients with B-BCLC stage hepatocellular carcinoma. Journal of Hepatology. 2014; 60:S402.
9. Colella G, Bottelli R, De Carlis L, Sansalone CV, Rondinara GF, Alberti A, Belli LS, Gelosa F, Iamoni GM, Rampoldi A, De Gasperi A, Corti A, Mazza E, Aseni P, Meroni A, Slim AO, et al. Hepatocellular carcinoma: comparison between liver transplantation, resective surgery, ethanol injection, and chemoembolization. Transplant international: official journal of the European Society for Organ Transplantation. 1998; 11 Suppl 1((Colella G.; Bottelli R.; De Carlis L.; Sansalone C.V.; Rondinara G.F.; Alberti A.; Belli L.S.; Gelosa F.; Iamoni G.M.; Rampoldi A.; De Gasperi A.; Corti A.; Mazza E.; Aseni P.; Meroni A.; Slim A.O.; Finzi M.; Di Benedetto F.; Manochehri F.; Follini M.L.; Ideo G.; Forti D.) Department of Surgery and Abdominal Organ Transplantation, Niguarda Hospital, Milan, Italy.):S193-196.
10. El-Serag HB, Siegel AB, Davila JA, Shaib YH, Cayton-Woody M, McBride R and McGlynn KA. Treatment and outcomes of treating of hepatocellular carcinoma among Medicare recipients in the United States: a population-based study. J Hepatol. 2006; 44:158-166.
11. Fan HL, Hsieh CB, Chang WC, Huang SH, Chan DC, Yu JC, Chu CH and Chen TW. Advanced age is not a contraindication for liver resection in cases of large hepatocellular carcinoma. Eur J Surg Oncol. 2014; 40:214-219.
12. Gerunda GE, Neri D, Merenda R, Barbazza F, Zangrandi F, Meduri F, Bisello M, Valmasoni M, Gangemi A and Faccioli AM. Role of transarterial chemoembolization before liver resection for hepatocarcinoma. Liver Transpl. 2000; 6:619-626.
13. Guglielmi A, Ruzzenente A, Capra F, Campagnaro T, Valdegamberi A, Ieluzzi D, Turcato G and Iacono C. Surgical versus non surgical therapy of hcc on cirrhosis: Results of an observational study on 692 cases. HPB. 2011; 13((Guglielmi A.; Ruzzenente A.; Campagnaro T.; Valdegamberi A.; Turcato G.; Iacono C.) Department of Surgery, Division of General Surgery 'a', GB Rossi University Hospital, Verona, Italy):40.
14. Guo Z, Zhong JH, Jiang JH, Zhang J, Xiang BD and Li LQ. Comparison of survival of patients with BCLC stage A hepatocellular carcinoma after hepatic resection or transarterial chemoembolization: a propensity score-based analysis. Ann Surg Oncol. 2014; 21:3069-3076.
15. Hasse F, Mehring UM, Castaneda F, Jager H, Mathias KD and Lohlein D. Comparison of liver resection with sequential transarterial chemoembolization in stage pT3 or pT4 hepatocellular carcinoma. Langenbecks Archiv für Chirurgie Supplement Kongressband Deutsche Gesellschaft für Chirurgie Kongress. 1996; 113((Hasse F.; Mehring U.M.; Castaneda F.; Jager H.; Mathias K.D.; Lohlein D.) Chirurgische Klinik, Stadtische Kliniken Dortmund.):208-210.
16. Helmberger T, Dogan S, Straub G, Schrader A, Jungst C, Reiser M, Waggershauser T, Jakobs T, Hoffmann RT, Lohe F, Graeb C, Rau HG, Schauer R, Jauch KW, Caselmann WH, Goke B, et al. Liver resection or combined chemoembolization and radiofrequency ablation improve survival in patients with hepatocellular carcinoma. Digestion. 2007; 75:104-112.
17. Herold C, Reck T, Fischler P, Ott R, Radespiel-Troeger M, Ganslmayer M, Hohenberger W, Hahn EG and Schuppan D. Prognosis of a large cohort of patients with hepatocellular carcinoma in a single European centre. Liver. 2002; 22:23-28.
18. Ho MC, Huang GT, Tsang YM, Lee PH, Chen DS, Sheu JC and Chen CH. Liver resection improves the survival of patients with multiple hepatocellular carcinomas. Ann Surg Oncol. 2009; 16:848-855.
19. Hsu CY, Hsia CY, Huang YH, Su CW, Lin HC, Pai JT, Loong CC, Chiou YY, Lee RC, Lee FY, Huo TI and Lee SD. Comparison of surgical resection and transarterial chemoembolization for hepatocellular carcinoma beyond the Milan criteria: a propensity score analysis. Ann Surg Oncol. 2012; 19:842-849.
20. Hsu KF, Chu CH, Chan DC, Yu JC, Shih ML, Hsieh HF, Hsieh TY, Yu CY and Hsieh CB. Superselective transarterial chemoembolization vs hepatic resection for resectable early-stage hepatocellular carcinoma in patients with Child-Pugh class a liver function. Eur J Radiol. 2012; 81:466-471.
21. Huang YH, Wu JC, Chau GY, Lui WY, King KL, Chiang JH, Yen SH, Sheng WY, Hou MC, Lu CL, Chang FY and Lee SD. Supportive treatment, resection and transcatheter arterial chemoembolization in resectable hepatocellular carcinoma: an analysis of survival in 419 patients. Eur J Gastroenterol Hepatol. 1999; 11:315-321.
22. Jianyong L, Lunan Y, Wentao W, Yong Z, Bo L, Tianfu W, Minqing X and Jiaying Y. Barcelona clinic liver cancer stage B hepatocellular carcinoma: transarterial chemoembolization or hepatic resection? Medicine (Baltimore). 2014; 93:e180.
23. Jin YJ, Lee JW, Choi YJ, Chung HJ, Kim YS, Lee KY, Ahn SI, Shin WY, Cho SG and Jeon YS. Surgery versus transarterial chemoembolization for solitary large hepatocellular carcinoma of BCLC stage A. J Gastrointest Surg. 2014; 18:555-561.
24. Kang S, Kim SU, Choi GH, Choi JS, Park JY, Lee KH, Lee DY, Kim DY, Ahn SH, Han KH and Chon CY. Comparing the outcomes of transarterial chemoembolization and hepatic resection in patients with single hepatocellular carcinoma less than 3 cm. Hepatology International. 2010; 4:304-305.
25. Kirchner G, Hebestreit A, Farkas S, Zorger N, Schnitzbauer A, Hartl J, Loss M, Baier L, Wiest R, Scherer MN and Schlitt HJ. Less than 10% of patients with hepatocellular carcinoma qualify for liver transplantation and show best long-term survival rates. Transplant International. 2011; 24((Kirchner G.; Hebestreit A.; Hartl J.; Wiest R.) Universitatsklinikum Regensburg, Klinik fur Innere Medizin i, Regensburg, Germany):20.
26. Lee JM, Jang BK, Chung WJ, Hwang JS, Kang KJ, Kim YH, Kweon YO, Park SY, Tak WY, Kim BS and Lee CH. The survival outcomes of hepatic resection compared with transcatheter arterial chemoembolization for hepatocellular carcinoma with portal vein tumor thrombus. Hepatology International. 2014; 8:S22-S23.
27. Lee YB, Lee DH, Cho Y, Yu SJ, Lee JH, Yoon JH, Lee HS, Kim HC, Yi NJ, Lee KW, Suh KS, Chung JW and Kim YJ. Comparison of chemoembolization and hepatic resection for large solitary hepatocellular carcinoma: A propensity score analysis. Journal of Hepatology. 2014; 60:S398.
28. Lin CT, Hsu KF, Chen TW, Yu JC, Chan DC, Yu CY, Hsieh TY, Fan HL, Kuo SM, Chung KP and Hsieh CB. Comparing hepatic resection and transarterial chemoembolization for Barcelona Clinic Liver Cancer (BCLC) stage B hepatocellular carcinoma: change for treatment of choice? World J Surg. 2010; 34:2155-2161.
29. Liu PH, Lee YH, Hsia CY, Hsu CY, Huang YH, Chiou YY, Lin HC and Huo TI. Surgical resection versus transarterial chemoembolization for hepatocellular carcinoma with portal vein tumor thrombosis: a propensity score analysis. Ann Surg Oncol. 2014; 21:1825-1833.
30. Luo J, Peng ZW, Guo RP, Zhang YQ, Li JQ, Chen MS and Shi M. Hepatic resection versus transarterial lipiodol chemoembolization as the initial treatment for large, multiple, and resectable hepatocellular carcinomas: a prospective nonrandomized analysis. Radiology. 2011; 259:286-295.
31. Markovic S, Gadzijev E, Stabuc B, Croce LS, Masutti F, Surlan M, Berden P, Brencic E, Visnar-Perovic A, Sasso F, Ferlan-Marolt V, Mucelli FP, Cesar R, Sponza M and Tiribelli C. Treatment options in Western hepatocellular carcinoma: a prospective study of 224 patients. J Hepatol. 1998; 29:650-659.
32. Martins A, Cortez-Pinto H, Marques-Vidal P, Mendes N, Silva S, Fatela N, Gloria H, Marinho R, Tavora I, Ramalho F and de Moura MC. Treatment and prognostic factors in patients with hepatocellular carcinoma. Liver Int. 2006; 26:680-687.
33. Min YW, Lee JH, Gwak GY, Paik YH, Rhee PL, Koh KC, Paik SW, Yoo BC and Choi MS. Long-term survival after surgical resection for huge hepatocellular carcinoma: comparison with transarterial chemoembolization after propensity score matching. J Gastroenterol Hepatol. 2014; 29:1043-1048.
34. Nagashima J, Okuda K, Tanaka M, Sata M and Aoyagi S. Prognostic benefit in cytoreductive surgery for curatively unresectable hepatocellular carcinoma - comparison to transcatheter arterial chemoembolization. Int J Oncol. 1999; 15:1117-1123.
35. Obed A, Tsui TY, Schnitzbauer AA, Obed M, Schlitt HJ, Becker H and Lorf T. Liver transplantation as curative approach for advanced hepatocellular carcinoma: is it justified? Langenbecks Arch Surg. 2008; 393:141-147.
36. Park KW, Park JW, Choi JI, Kim TH, Kim SH, Park HS, Lee WJ, Park SJ, Hong EK and Kim CM. Survival analysis of 904 patients with hepatocellular carcinoma in a hepatitis B virus-endemic area. J Gastroenterol Hepatol. 2008; 23:467-473.
37. Paul SB, Chalamalasetty SB, Vishnubhatla S, Madan K, Gamanagatti SR, Batra Y, Gupta SD, Panda SK and Acharya SK. Clinical profile, etiology and therapeutic outcome in 324 hepatocellular carcinoma patients at a tertiary care center in India. Oncology. 2009; 77:162-171.
38. Peng ZW, Guo RP, Zhang YJ, Lin XJ, Chen MS and Lau WY. Hepatic resection versus transcatheter arterial chemoembolization for the treatment of hepatocellular carcinoma with portal vein tumor thrombus. Cancer. 2012; 118:4725-4736.
39. Perry JF, Charlton B, Koorey DJ, Waugh RC, Gallagher PJ, Crawford MD, Verran DJ, McCaughan GW and Strasser SI. Outcome of patients with hepatocellular carcinoma referred to a tertiary centre with availability of multiple treatment options including cadaveric liver transplantation. Liver Int. 2007; 27:1240-1248.
40. Sako K, Komorizono Y, Oketani M, Hasegawa S, Yamasaki N, Shibatou T, Maeda M, Kohara K, Shigenobu S, Yasunari H, Sakurai K, Hiwaki T, Ishibashi K and Arima T. Outcome of Patients with Hepatitis C Virus-related Single, Small Hepatocellular Carcinoma. Anticancer Research. 2003; 23:4191-4196.
41. Sasaki Y, Imaoka S, Nakano H, Ishikawa O, Ohigashi H, Yasuda T, Nakamori S, Kameyama M, Hiratsuka M, Kabuto T, Furukawa H, Kasugai H, Inoue A, Fujita M and Inoue E. Indications for hepatectomy for hepatocellular carcinoma - what stage of the disease is the best indication for surgery? J Hepatobiliary Pancreat Surg. 1998; 5:14-17.
42. Schumacher PA, Powell JJ, MacNeill AJ, Buczkowski AK, Erb SR, Ho SG, Scudamore CH, Steinbrecher UP, Weiss A, Yoshida E and Chung SW. Multimodal therapy for hepatocellular carcinoma: a complementary approach to liver transplantation. Ann Hepatol. 2010; 9:23-32.
43. Sotiropoulos GC, Druhe N, Sgourakis G, Molmenti EP, Beckebaum S, Baba HA, Antoch G, Hilgard P, Radtke A, Saner FH, Nadalin S, Paul A, Malago M, Broelsch CE and Lang H. Liver transplantation, liver resection, and transarterial chemoembolization for hepatocellular carcinoma in cirrhosis: which is the best oncological approach? Dig Dis Sci. 2009; 54:2264-2273.
44. Toro A, Ardiri A, Mannino M, Arcerito MC, Mannino G, Palermo F, Bertino G and Di Carlo I. Effect of pre- and post-treatment alpha-fetoprotein levels and tumor size on survival of patients with hepatocellular carcinoma treated by resection, transarterial chemoembolization or radiofrequency ablation: a retrospective study. BMC Surg. 2014; 14:40.
45. Ueno S, Tanabe G, Nuruki K, Oketani M, Komorizono Y, Hokotate H, Fukukura Y, Baba Y, Imamura Y and Aikou T. Prognosis of hepatocellular carcinoma associated with Child class B and C cirrhosis in relation to treatment: a multivariate analysis of 411 patients at a single center. J Hepatobiliary Pancreat Surg. 2002; 9:469-477.
46. Utsunomiya T, Shimada M, Kudo M, Ichida T, Matsui O, Izumi N, Matsuyama Y, Sakamoto M, Nakashima O, Ku Y, Kokudo N and Makuuchi M. Nationwide study of 4741 patients with non-B non-C hepatocellular carcinoma with special reference to the therapeutic impact. Ann Surg. 2014; 259:336-345.
47. Wang Sz, Meng Wj, An HQ, Shi Fs and Wang Xl. Outcome evaluation of hepatocellular carcinoma patients after balancing the covariates between groups through propensity score. Academic Journal of Second Military Medical University. 2012; 33:1090-1094.
48. Wang JH, Kuo YH, Wang CC, Chen CL, Cheng YF, Hsu HC and Lu SN. Surgical resection improves the survival of selected hepatocellular carcinoma patients in Barcelona clinic liver cancer stage C. Dig Liver Dis. 2013; 45:510-515.
49. Worns MA, Bosslet T, Victor A, Koch S, Hoppe-Lotichius M, Heise M, Hansen T, Pitton MB, Niederle IM, Schuchmann M, Weinmann A, Duber C, Galle PR and Otto G. Prognostic factors and outcomes of patients with hepatocellular carcinoma in non-cirrhotic liver. Scand J Gastroenterol. 2012; 47:718-728.
50. Yamagiwa K, Shiraki K, Yamakado K, Mizuno S, Hori T, Yagi S, Hamada T, Iida T, Nakamura I, Fujii K, Usui M, Isaji S, Ito K, Tagawa S, Takeda K, Yokoi H, et al. Survival rates according to the Cancer of the Liver Italian Program scores of 345 hepatocellular carcinoma patients after multimodality treatments during a 10-year period in a retrospective study. J Gastroenterol Hepatol. 2008; 23:482-490.
51. Yang HJ, Lee JH, Lee DH, Yu SJ, Kim YJ, Yoon JH, Kim HC, Lee JM, Chung JW, Yi NJ, Lee KW, Suh KS and Lee HS. Small single-nodule hepatocellular carcinoma: comparison of transarterial chemoembolization, radiofrequency ablation, and hepatic resection by using inverse probability weighting. Radiology. 2014; 271:909-918.
52. Ye JZ, Zhang YQ, Ye HH, Bai T, Ma L, Xiang BD and Li LQ. Appropriate treatment strategies improve survival of hepatocellular carcinoma patients with portal vein tumor thrombus. World J Gastroenterol. 2014; 20:17141-17147.
53. Yin L, Li H, Li AJ, Lau WY, Pan ZY, Lai EC, Wu MC and Zhou WP. Partial hepatectomy vs. transcatheter arterial chemoembolization for resectable multiple hepatocellular carcinoma beyond Milan Criteria: a RCT. J Hepatol. 2014; 61:82-88.
54. Zhang T, Zeng Y, Huang J, Liao M and Wu H. Combined resection with radiofrequency ablation for bilobar hepatocellular carcinoma: a single-center experience. J Surg Res. 2014; 191:370-378.
55. Zhong JH, Ke Y, Gong WF, Xiang BD, Ma L, Ye XP, Peng T, Xie GS and Li LQ. Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma. Ann Surg. 2014; 260:329-340.
56. Qi X, Tang Y, An D, Bai M, Shi X, Wang J, Han G and Fan D. Radiofrequency ablation versus hepatic resection for small hepatocellular carcinoma: a meta-analysis of randomized controlled trials. J Clin Gastroenterol. 2014; 48:450-457.
57. Llovet JM and Bruix J. Systematic review of randomized trials for unresectable hepatocellular carcinoma: Chemoembolization improves survival. Hepatology. 2003; 37:429-442.
58. Kapitanov T, Neumann UP and Schmeding M. Hepatocellular Carcinoma in Liver Cirrhosis: Surgical Resection versus Transarterial Chemoembolization-A Meta-Analysis. Gastroenterol Res Pract. 2015; 2015:696120.
59. Qi X, Yang M, Ren W, Jia J, Wang J, Han G and Fan D. Find duplicates among the PubMed, EMBASE, and Cochrane Library Databases in systematic review. PLoS One. 2013; 8:e71838.
60. Zhong JH, Xiang BD, Gong WF, Ke Y, Mo QG, Ma L, Liu X and Li LQ. Comparison of long-term survival of patients with BCLC stage B hepatocellular carcinoma after liver resection or transarterial chemoembolization. PLoS One. 2013; 8:e68193.
61. Guo Z, Xiang B, Zhang J, Jiang J and Li L. [Comparison of hepatic resection and transarterial chemoembolization for hepatocellular carcinoma within the Milan criteria]. Zhonghua Yi Xue Za Zhi. 2014; 94:1526-1529.
62. Guo Z, Zhong JH, Jiang JH, Zhang J, Xiang BD and Li LQ. Comparison of survival of patients with BCLC stage a hepatocellular carcinoma after hepatic resection or transarterial chemoembolization: A propensity score-based analysis. Annals of Surgical Oncology. 2014; 21:3069-3076.
63. Ke Y, Zhong J, Guo Z, Liang Y, Li L and Xiang B. [Comparison liver resection with transarterial chemoembolization for Barcelona Clinic Liver Cancer stage B hepatocellular carcinoma patients on long-term survival after SPSS propensity score matching]. Zhonghua Yi Xue Za Zhi. 2014; 94:747-750.
64. Liu X, Li L, Xiang B, Ma L, Zhong J and You X. Efficacy of hepatic resection and transarterial chemoembolization for stage B hepatocellular carcinoma in the Barcelona Clinic Liver Cancer classification. Chinese Journal of Clinical Oncology. 2012; 39:1225-1228.
65. Llovet JM, Di Bisceglie AM, Bruix J, Kramer BS, Lencioni R, Zhu AX, Sherman M, Schwartz M, Lotze M, Talwalkar J and Gores GJ. Design and endpoints of clinical trials in hepatocellular carcinoma. J Natl Cancer Inst. 2008; 100:698-711.
66. Wells GA, Shea B, O'Connell D, Peterson J, Welch V, Losos M and Tugwell P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://wwwohrica/programs/clinical_ epidemiology/oxfordasp.
67. Tierney JF, Stewart LA, Ghersi D, Burdett S and Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007; 8:16.