DOI QR코드

DOI QR Code

Is partial hepatectomy a curable treatment option for hepatocellular carcinoma accompanied by cirrhosis? A meta-analysis and cure model analysis

  • Byungje Bae (Department of Surgery, Catholic Kwandong University International St. Mary's Hospital) ;
  • Keera Kang (Department of Surgery, Catholic Kwandong University International St. Mary's Hospital) ;
  • Sung Kyu Song (Department of Surgery, Catholic Kwandong University International St. Mary's Hospital) ;
  • Chul-Woon Chung (Department of Surgery, Catholic Kwandong University International St. Mary's Hospital) ;
  • Yongkeun Park (Department of Surgery, Catholic Kwandong University International St. Mary's Hospital)
  • 투고 : 2021.06.03
  • 심사 : 2021.08.17
  • 발행 : 2022.02.28

초록

Backgrounds/Aims: It is challenging to assess the efficacy of partial hepatectomy (PH) as a treatment option for patients with hepatocellular carcinoma (HCC) accompanied by cirrhosis. This study aimed to determine the cure fraction of PH for HCC accompanied by cirrhosis compared to that for HCC without cirrhosis. Methods: A systematic review was performed on outcomes of previous studies that compared recurrence-free survival (RFS) after PH in patients with HCC with or without cirrhosis. A meta-analysis was conducted to obtain the cumulative hazard ratio for two patient groups: cirrhosis and non-cirrhosis. Cure fractions after PH in both groups were determined using a cure model analysis. Results: A total of 18 studies were eligible for meta-analysis and 13 studies were selected for the cure model analysis. The cumulative hazard ratio for RFS of the cirrhosis group compared to that of the non-cirrhosis group was 1.66 (95% confidence interval [CI], 1.43-1.93). Survival data of 3,512 patients in both groups were reconstructed from survival curves of original articles for cure model analysis. The probability of being statistically cured after PH for HCC was 14.1% (95% CI, 10.6%-18.1%) in the cirrhosis group lower than that (32.5%) in the non-cirrhosis group (95% CI, 28.6%-36.4%). Conclusions: The prognosis after PH for HCC accompanied by cirrhosis is inferior to that for HCC without cirrhosis. However, a cure can be expected for one-seventh of patients with HCC accompanied by cirrhosis after PH.

키워드

참고문헌

  1. Lafaro KJ, Demirjian AN, Pawlik TM. Epidemiology of hepatocellular carcinoma. Surg Oncol Clin N Am 2015;24:1-17. 
  2. Fujiwara N, Friedman SL, Goossens N, Hoshida Y. Risk factors and prevention of hepatocellular carcinoma in the era of precision medicine. J Hepatol 2018;68:526-549. 
  3. Petrick JL, Kelly SP, Altekruse SF, McGlynn KA, Rosenberg PS. Future of hepatocellular carcinoma incidence in the United States forecast through 2030. J Clin Oncol 2016;34:1787-1794. 
  4. McGlynn KA, Petrick JL, London WT. Global epidemiology of hepatocellular carcinoma: an emphasis on demographic and regional variability. Clin Liver Dis 2015;19:223-238. 
  5. El-Serag HB, Siegel AB, Davila JA, Shaib YH, Cayton-Woody M, McBride R, et al. 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. 
  6. op den Winkel M, Nagel D, Sappl J, op den Winkel P, Lamerz R, Zech CJ, et al. Prognosis of patients with hepatocellular carcinoma. Validation and ranking of established staging-systems in a large western HCC-cohort. PLoS One 2012;7:e45066. 
  7. Byam J, Renz J, Millis JM. Liver transplantation for hepatocellular carcinoma. Hepatobiliary Surg Nutr 2013;2:22-30. 
  8. Halazun KJ, Najjar M, Abdelmessih RM, Samstein B, Griesemer AD, Guarrera JV, et al. Recurrence after liver transplantation for hepatocellular carcinoma: a new MORAL to the story. Ann Surg 2017;265:557-564. 
  9. Yao FY, Ferrell L, Bass NM, Watson JJ, Bacchetti P, Venook A, et al. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology 2001;33:1394-1403. 
  10. Krenzien F, Schmelzle M, Struecker B, Raschzok N, Benzing C, Jara M, et al. Liver transplantation and liver resection for cirrhotic patients with hepatocellular carcinoma: comparison of long-term survivals. J Gastrointest Surg 2018;22:840-848. 
  11. Zheng Z, Liang W, Milgrom DP, Zheng Z, Schroder PM, Kong NS, et al. Liver transplantation versus liver resection in the treatment of hepatocellular carcinoma: a meta-analysis of observational studies. Transplantation 2014;97:227-234. 
  12. Pinna AD, Yang T, Mazzaferro V, De Carlis L, Zhou J, Roayaie S, et al. Liver transplantation and hepatic resection can achieve cure for hepatocellular carcinoma. Ann Surg 2018;268:868-875. 
  13. Tsilimigras DI, Bagante F, Moris D, Merath K, Paredes AZ, Sahara K, et al. Defining the chance of cure after resection for hepatocellular carcinoma within and beyond the Barcelona Clinic Liver Cancer guidelines: a multi-institutional analysis of 1,010 patients. Surgery 2019;166:967-974. 
  14. Lambert PC, Thompson JR, Weston CL, Dickman PW. Estimating and modeling the cure fraction in population-based cancer survival analysis. Biostatistics 2007;8:576-594. 
  15. Othus M, Barlogie B, Leblanc ML, Crowley JJ. Cure models as a useful statistical tool for analyzing survival. Clin Cancer Res 2012;18:3731-3736. 
  16. Guyot P, Ades AE, Ouwens MJ, Welton NJ. Enhanced secondary analysis of survival data: reconstructing the data from published Kaplan-Meier survival curves. BMC Med Res Methodol 2012;12:9. 
  17. R Development Core Team. R: a language and environment for statistical computing [Internet]. Vienna: R Foundation for Statistical Computing 2017 [cited 2020 Dec 1]. Available from: https://www.R-project.org/. 
  18. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557-560. 
  19. Chang CH, Chau GY, Lui WY, Tsay SH, King KL, Wu CW. Long-term results of hepatic resection for hepatocellular carcinoma originating from the noncirrhotic liver. Arch Surg 2004;139:320-325. 
  20. Yamashita Y, Taketomi A, Itoh S, Kitagawa D, Kayashima H, Harimoto N, et al. Longterm favorable results of limited hepatic resections for patients with hepatocellular carcinoma: 20 years of experience. J Am Coll Surg 2007;205:19-26. 
  21. Chua TC, Saxena A, Chu F, Liauw W, Zhao J, Morris DL. Clinicopathological determinants of survival after hepatic resection of hepatocellular carcinoma in 97 patients--experience from an Australian hepatobiliary unit. J Gastrointest Surg 2010;14:1370-1380. 
  22. Gassmann P, Spieker T, Haier J, Schmidt F, Mardin WA, Senninger N. Prognostic impact of underlying liver fibrosis and cirrhosis after curative resection of hepatocellular carcinoma. World J Surg 2010;34:2442-2451. 
  23. Fan ST, Poon RT, Yeung C, Lam CM, Lo CM, Yuen WK, et al. Outcome after partial hepatectomy for hepatocellular cancer within the Milan criteria. Br J Surg 2011;98:1292-1300. 
  24. Ho CM, Lee PH, Chen CL, Ho MC, Wu YM, Hu RH. Long-term outcomes after resection versus transplantation for hepatocellular carcinoma within UCSF criteria. Ann Surg Oncol 2012;19:826-833. 
  25. Mizuguchi T, Kawamoto M, Meguro M, Nakamura Y, Ota S, Hui TT, et al. Prognosis and predictors of surgical complications in hepatocellular carcinoma patients with or without cirrhosis after hepatectomy. World J Surg 2013;37:1379-1387. 
  26. Yang LY, Chang RM, Lau WY, Ou DP, Wu W, Zeng ZJ. Mesohepatectomy for centrally located large hepatocellular carcinoma: indications, techniques, and outcomes. Surgery 2014;156:1177-1187. 
  27. Yap AQ, Millan CA, Wang JH, Wang CC, Lu SN, Wang SH, et al. How to improve the outcome in patients with AJCC stage I hepatocellular carcinoma. Anticancer Res 2014;34:3093-3103. 
  28. Chapman WC, Klintmalm G, Hemming A, Vachharajani N, Majella Doyle MB, DeMatteo R, et al. Surgical treatment of hepatocellular carcinoma in North America: can hepatic resection still be justified? J Am Coll Surg 2015;220:628-637. 
  29. Kluger MD, Salceda JA, Laurent A, Tayar C, Duvoux C, Decaens T, et al. Liver resection for hepatocellular carcinoma in 313 Western patients: tumor biology and underlying liver rather than tumor size drive prognosis. J Hepatol 2015;62:1131-1140. 
  30. Huang ZY, Liang BY, Xiong M, Dong KS, Zhang ZY, Zhang EL, et al. Severity of cirrhosis should determine the operative modality for patients with early hepatocellular carcinoma and compensated liver function. Surgery 2016;159:621-631. 
  31. Lee HW, Choi GH, Kim DY, Park YN, Kim KS, Choi JS, et al. Less fibrotic burden differently affects the long-term outcomes of hepatocellular carcinoma after curative resection. Oncology 2017;93:224-232. 
  32. Shehta A, Han HS, Yoon YS, Cho JY, Choi Y. Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients: 10-year single-center experience. Surg Endosc 2016;30:638-648. 
  33. Lee EC, Kim SH, Park H, Lee SD, Lee SA, Park SJ. Survival analysis after liver resection for hepatocellular carcinoma: a consecutive cohort of 1002 patients. J Gastroenterol Hepatol 2017;32:1055-1063. 
  34. Cipriani F, Fantini C, Ratti F, Lauro R, Tranchart H, Halls M, et al. Laparoscopic liver resections for hepatocellular carcinoma. Can we extend the surgical indication in cirrhotic patients? Surg Endosc 2018;32:617-626. 
  35. Famularo S, Di Sandro S, Giani A, Lauterio A, Sandini M, De Carlis R, et al. Long-term oncologic results of anatomic vs. parenchyma-sparing resection for hepatocellular carcinoma. A propensity score-matching analysis. Eur J Surg Oncol 2018;44:1580-1587. 
  36. Golse N, El Bouyousfi A, Marques F, Bancel B, Mohkam K, Ducerf C, et al. Large hepatocellular carcinoma: does fibrosis really impact prognosis after resection? J Visc Surg 2018;155:265-273. 
  37. Akcam AT, Saritas AG, Ulku A, Rencuzogullari A. Oncological outcomes of hepatic resection vs transplantation for localized hepatocellular carcinoma. Transplant Proc 2019;51:1147-1152. 
  38. Xu XF, Xing H, Han J, Li ZL, Lau WY, Zhou YH, et al. Risk factors, patterns, and outcomes of late recurrence after liver resection for hepatocellular carcinoma: a multicenter study from China. JAMA Surg 2019;154:209-217. 
  39. Li ZL, Yu JJ, Guo JW, Sui CJ, Dai BH, Zhang WG, et al. Liver resection is justified for multinodular hepatocellular carcinoma in selected patients with cirrhosis: a multicenter analysis of 1,066 patients. Eur J Surg Oncol 2019;45:800-807. 
  40. Affo S, Yu LX, Schwabe RF. The role of cancer-associated fibroblasts and fibrosis in liver cancer. Annu Rev Pathol 2017;12:153-186. 
  41. Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004;127(5 Suppl 1):S35-S50. 
  42. Ju MJ, Qiu SJ, Fan J, Xiao YS, Gao Q, Zhou J, et al. Peritumoral activated hepatic stellate cells predict poor clinical outcome in hepatocellular carcinoma after curative resection. Am J Clin Pathol 2009;131:498-510. 
  43. Yu DC, Liu J, Chen J, Shao JJ, Shen X, Xia HG, et al. GGPPS1 predicts the biological character of hepatocellular carcinoma in patients with cirrhosis. BMC Cancer 2014;14:248. 
  44. Lin Y, Liang R, Ye J, Li Q, Liu Z, Gao X, et al. A twenty gene-based gene set variation score reflects the pathological progression from cirrhosis to hepatocellular carcinoma. Aging (Albany NY) 2019;11:11157-11169. 
  45. Harimoto N, Yoshizumi T, Fujimoto Y, Motomura T, Mano Y, Toshima T, et al. Surgery for hepatocellular carcinoma in patients with Child-Pugh B cirrhosis: hepatic resection versus living donor liver transplantation. World J Surg 2018;42:2606-2616. 
  46. Margarit C, Escartin A, Castells L, Vargas V, Allende E, Bilbao I. Resection for hepatocellular carcinoma is a good option in Child-Turcotte-Pugh class A patients with cirrhosis who are eligible for liver transplantation. Liver Transpl 2005;11:1242-1251. 
  47. Madkhali AA, Fadel ZT, Aljiffry MM, Hassanain MM. Surgical treatment for hepatocellular carcinoma. Saudi J Gastroenterol 2015;21:11-17. 
  48. Kulik L, Heimbach JK, Zaiem F, Almasri J, Prokop LJ, Wang Z, et al. Therapies for patients with hepatocellular carcinoma awaiting liver transplantation: a systematic review and meta-analysis. Hepatology 2018;67:381-400. 
  49. Chedid MF, Kruel CRP, Pinto MA, Grezzana-Filho TJM, Leipnitz I, Kruel CDP, et al. Hepatocellular carcinoma: diagnosis and operative management. Arq Bras Cir Dig 2017;30:272-278. 
  50. Jadlowiec CC, Taner T. Liver transplantation: current status and challenges. World J Gastroenterol 2016;22:4438-4445. 
  51. Chan DL, Alzahrani NA, Morris DL, Chua TC. Systematic review of efficacy and outcomes of salvage liver transplantation after primary hepatic resection for hepatocellular carcinoma. J Gastroenterol Hepatol 2014;29:31-41. 
  52. Muaddi H, Al-Adra DP, Beecroft R, Ghanekar A, Moulton CA, Doyle A, et al. Liver transplantation is equally effective as a salvage therapy for patients with hepatocellular carcinoma recurrence following radiofrequency ablation or liver resection with curative intent. Ann Surg Oncol 2018;25:991-999. 
  53. Qu W, Zhu ZJ, Sun LY, Wei L, Liu Y, Zeng ZG. Salvage liver transplantation for hepatocellular carcinoma recurrence after primary liver resection. Clin Res Hepatol Gastroenterol 2015;39:93-97. 
  54. Zheng S, Xie Q, Cheng J. Salvage liver transplant for hepatocellular carcinoma: rescues and benefits. Transl Gastroenterol Hepatol 2018;3:65. 
  55. Lacaze L, Scotte M. Surgical treatment of intra hepatic recurrence of hepatocellular carcinoma. World J Hepatol 2015;7:1755-1760. 
  56. Chan AC, Chan SC, Chok KS, Cheung TT, Chiu DW, Poon RT, et al. Treatment strategy for recurrent hepatocellular carcinoma: salvage transplantation, repeated resection, or radiofrequency ablation? Liver Transpl 2013;19:411-419.