Validation of clinical AJCC/UICC TNM staging system for hepatocellular carcinoma: Analysis of 5,613 cases from a medical center in southern Taiwan
Kwong-Ming Kee
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorJing-Houng Wang
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChuan-Mo Lee
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChao-Long Chen
Department of Surgery, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChi-Sin Changchien
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorTsung-Hui Hu
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorYu-Fan Cheng
Department of Radiology, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorHsuan-Chih Hsu
Department of Radiation Oncology, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChih-Chi Wang
Department of Surgery, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorTai-Yi Chen
Department of Radiology, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChih-Yun Lin
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorCorresponding Author
Sheng-Nan Lu
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Fax: +886-7-7322402.
Division of Hepatogastroenterology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, 123 Ta Pei Road, Niao Sung 833, Kaohsiung, TaiwanSearch for more papers by this authorKwong-Ming Kee
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorJing-Houng Wang
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChuan-Mo Lee
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChao-Long Chen
Department of Surgery, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChi-Sin Changchien
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorTsung-Hui Hu
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorYu-Fan Cheng
Department of Radiology, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorHsuan-Chih Hsu
Department of Radiation Oncology, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChih-Chi Wang
Department of Surgery, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorTai-Yi Chen
Department of Radiology, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorChih-Yun Lin
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Search for more papers by this authorCorresponding Author
Sheng-Nan Lu
Division of Hepatogastroenterology, Department of Internal Medicine, Chang Gung Memorial Hospital-Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, Taiwan
Fax: +886-7-7322402.
Division of Hepatogastroenterology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, 123 Ta Pei Road, Niao Sung 833, Kaohsiung, TaiwanSearch for more papers by this authorAbstract
This study was aimed to validate the 5th and 6th editions of tumor-node-metastasis (TNM) system for patients with hepatocellular carcinoma (HCC), and attempted to improve prognostic stratification by modifying the 6th edition according to vascular invasion and tumor size. From 1986 to 2002, a total of 5,613 HCC cases from Kaohsiung Chang Gung Memorial Hospital in southern Taiwan were enrolled. The 6th edition was modified by dividing stage I into stages IA (single tumor, ≤2cm) and IB (single tumor, >2cm), and by dividing stage II into IIA (multiple tumors, none >5cm) and IIB (tumor with segmental macro vascular invasion). The Akaike information criteria (AIC), within a Cox proportional hazard regression model were used; lower AIC value indicated a better discriminatory ability for staging system. The 1-, 3-, 5-, and 7-year overall survival rates were 45.6, 25.9, 17.9, and 13.4%, respectively. Significant differences in survival curve existed in the 5th, 6th, and modified 6th edition TNM systems. For the modified 6th edition TNM, survival differed significantly between stages IA and IB, and between stage IIA and IIB. The AIC values of 5th (72,328), 6th (72,188), modified 6th (71,991) edition TNM system were decreasing. This investigation demonstrated better prognostic stratifications for the 6th edition than the 5th edition TNM staging system. Moreover, the modified 6th edition staging system demonstrated better prognostic prediction than the former two. Pretreatment staging and simple classification of current modified 6th edition TNM staging can be applied to all HCC patients and are clinically useful. © 2007 Wiley-Liss, Inc.
References
- 1Department of Health Cancer Registry Annual Report, 1992–2001. Bureau of health promotion, department of health, executure yuan, Republic of China, 2004.
- 2 FL Greene, DL Page, ID Fleming, A Fritz, CM Balch, DG Haller, M Morrow, eds. AJCC cancer staging manual, 6th edn. Chicago: Springer, 2002. 435p.
- 3
Okuda K,
Ohtsuki T,
Obata H,
Tomimatsu M,
Okazaki N,
Hasegawa H,
Nakajima Y,
Ohnishi K.
Natural history of hepatocellular carcinoma and prognosis in relation to treatment. Study of 850 patients.
Cancer
1985;
56:
918–28.
10.1002/1097-0142(19850815)56:4<918::AID-CNCR2820560437>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
- 4 The Cancer of the Liver Italian Program (CLIP) investigators. A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients. Hepatology 1998; 28: 751–5.
- 5 Kudo M, Chung H, Osaki Y. Prognostic staging system for hepatocellular carcinoma (CLIP score): its value and limitations, and a proposal for a new staging system, the Japan integrated staging score (JIS score). J Gastroenterol 2003; 38: 207–15.
- 6 Llovet JM, Bru C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 1999; 19: 329–38.
- 7 ID Fleming, JS Cooper, DE Henson, RVP Hutter, BJ Kennedy, GP Murphy, BO Sullivan, LH Sobin, JW Yarbro, eds. AJCC cancer staging manual, 5th ed. Philadelphia: Lippincott-Raven, 1997. 294p.
- 8 Vauthey JN, Lauwers GY, Esnaola NF, Do KA, Belghiti J, Mirza N, Curley SA, Ellis LM, Regimbeau JM, Rashid A, Cleary KR, Nagorney DM. Simplified staging for hepatocellular carcinoma. J Clin Oncol 2002; 20: 1527–36.
- 9 Varotti G, Ramacciato G, Ercolani G, Grazi GL, Vetrone G, Cescon M, Del Gaudio M, Ravaioli M, Ziparo V, Lauro A, Pinna A. Comparison between the fifth and sixth editions of the AJCC/UICC TNM staging systems for hepatocellular carcinoma: multicentric study on 393 cirrhotic resected patients. Eur J Surg Oncol 2005; 31: 760–7.
- 10 Ramacciato G, Mercantini P, Cautero N, Corigliano N, Di Benedetto F, Quintini C, Ercolani G, Varotti G, Ziparo V, Pinna AD. Prognostic evaluation of the new American joint committee on cancer/international union against cancer staging system for hepatocellular carcinoma: analysis of 112 cirrhotic patients resected for hepatocellular carcinoma. Ann Surg Oncol 2005; 12: 289–97.
- 11 Poon RT, Fan ST. Evaluation of the new AJCC/UICC staging system for hepatocellular carcinoma after hepatic resection in Chinese patients. Surg Oncol Clin N Am 2003; 12: 35–50.
- 12 Lai EC, Fan ST, Lo CM, Chu KM, Liu CL, Wong J. Hepatic resection for hepatocellular carcinoma. An audit of 343 patients. Ann Surg 1995; 221: 291–8.
- 13 Pawlik TM, Delman KA, Vauthey JN, Nagorney DM, Ng IO, Ikai I, Yamaoka Y, Belghiti J, Lauwers GY, Poon RT, Abdalla EK. Tumor size predicts vascular invasion and histologic grade: Implications for selection of surgical treatment for hepatocellular carcinoma. Liver Transpl 2005; 11: 1086–92.
- 14 Tsai TJ, Chau GY, Lui WY, Tsay SH, King KL, Loong CC, Hsia CY, Wu CW. Clinical significance of microscopic tumor venous invasion in patients with resectable hepatocellular carcinoma. Surgery 2000; 127: 603–8.
- 15 Jonas S, Bechstein WO, Steinmuller 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: 1080–6.
- 16 Yamamoto M, Takasaki K, Otsubo T, Katsuragawa H, Katagiri S, Yoshitoshi K, Ariizumi S, Saito A, Nakano M. Favorable surgical outcomes in patients with early hepatocellular carcinoma. Ann Surg 2004; 239: 395–9.
- 17 Ikai I, Arii S, Kojiro M, Ichida T, Makuuchi M, Matsuyama Y, Nakanuma Y, Okita K, Omata M, Takayasu K, Yamaoka Y. Reevaluation of prognostic factors for survival after liver resection in patients with hepatocellular carcinoma in a Japanese nationwide survey. Cancer 2004; 101: 796–802.
- 18 Chen MS, Li JQ, Zheng Y, Guo RP, Liang HH, Zhang YQ, Lin XJ, Lau WY. A prospective randomized trial comparing percutaneous local ablative therapy and partial hepatectomy for small hepatocellular carcinoma. Ann Surg 2006; 243: 321–8.
- 19 Huang GT, Lee PH, Tsang YM, Lai MY, Yang PM, Hu RH, Chen PJ, Kao JH, Sheu JC, Lee CZ, Chen DS. Percutaneous ethanol injection versus surgical resection for the treatment of small hepatocellular carcinoma: a prospective study. Ann Surg 2005; 242: 36–42.
- 20 Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet 2003; 362: 1907–17.
- 21 Klintmalm GB. Liver transplantation for hepatocellular carcinoma: a registry report of the impact of tumour characteristics on outcome. Ann Surg 1998; 228: 479–90.
- 22 Lencioni R, Cioni D, Crocetti L, Franchini C, Pina CD, Lera J, Bartolozzi C. Early-stage hepatocellular carcinoma in patients with cirrhosis: long-term results of percutaneous image-guided radiofrequency ablation. Radiology 2005; 234: 961–7.
- 23 Cha C, Fong Y, Jarnagin WR, Blumgart LH, DeMatteo RP. Predictors and patterns of recurrence after resection of hepatocellular carcinoma. J Am Coll Surg 2003; 197: 753–8.
- 24 Ueno S, Tanabe G, Sako K, Hiwaki T, Hokotate H, Fukukura Y, Baba Y, Imamura Y, Aikou T. Discrimination value of the new western prognostic system (CLIP score) for hepatocellular carcinoma in 662 Japanese patients. Cancer of the liver Italian program. Hepatology 2001; 34: 529–34.
- 25 Stone M. Akaike's criteria. In: P Armitage, T Colton, eds. Encyclopedia of biostatistics. Chichester: Wiley, 1998. 123–4.
- 26 Makuuchi M, Belghiti J, Belli G, Fan ST, Lau JW, Ringe B, Strasberg SM, Vauthey JN, Yamaoka Y, Yamasaki S, Working Group of the International Scientific Committee of the International Hepato-Pancreato-Biliary Association. IHPBA concordant classification of primary liver cancer: working group report. J Hepatobiliary Pancreat Surg 2003; 10: 26–30.
- 27 Liaw YF, Tai DI, Chu CM, Lin DY, Sheen IS, Chen TJ, Pao CC. Early detection of hepatocellular carcinoma in patients with chronic type B hepatitis. A prospective study. Gastroenterology 1986; 90: 263–7.
- 28 Chen CH, Su WW, Yang SS, Chang TT, Cheng KS, Lin HH, Wu SS, Lee CM, Changchien CS, Chen CJ, Sheu JC, Chen DS, et al. Long-term trends and geographic variations in the survival of hepatocellular carcinoma patients: analysis of 11,312 patients in Taiwan. J Gastroenterol Hepatol 2006; 21: 1561–6.
- 29 Poon RT, Fan ST, Ng IO, Wong J. Prognosis after hepatic resection for stage IVA hepatocellular carcinoma: a need for reclassification. Ann Surg 2003; 237: 376–83.
- 30 Izumi R, Shimizu K, Ii T, Yagi M, Matsui O, Nonomura A, Miyazaki I. Prognostic factors of hepatocellular carcinoma in patients undergoing hepatic resection. Gastroenterology 1994; 106: 720–7.
- 31 Matsumata T, Kanematsu T, Takenaka K, Yoshida Y, Nishizaki T, Sugimachi K. Patterns of intrahepatic recurrence after curative resection of hepatocellular carcinoma. Hepatology 1989; 9: 457–60.
- 32 Zavaglia C, De Carlis L, Alberti AB, Minola E, Belli LS, Slim AO, Airoldi A, Giacomoni A, Rondinara G, Tinelli C, Forti D, Pinzello G. Predictors of long-term survival after liver transplantation for hepatocellular carcinoma. Am J Gastroenterol 2005; 100: 2708–16.
- 33 Yeung YP, Lo CM, Liu CL, Wong BC, Fan ST, Wong J. Natural history of untreated nonsurgical hepatocellular carcinoma. Am J Gastroenterol 2005; 100: 1995–2004.
- 34 Llovet JM, Bustamante J, Castells A, Vilana R, Ayuso Mdel C, Sala M, Bru C, Rodes J, Bruix J. Natural history of untreated nonsurgical hepatocellular carcinoma: rationale for the design and evaluation of therapeutic trials. Hepatology 1999; 29: 62–7.
- 35 Pawarode A, Voravud N, Sriuranpong V, Kullavanijaya P, Patt YZ. Natural history of untreated primary hepatocellular carcinoma: a retrospective study of 157 patients. Am J Clin Oncol 1998; 21: 386–91.