Abstract
Background
The role of surgical resection in patients with large or multinodular hepatocellular carcinoma (HCC) remains unclear. This study evaluated the long-term outcome of patients with hepatic resection for large (>5 cm in diameter) or multinodular (more than three nodules) HCC by using a multi-institutional database.
Methods
The perioperative and long-term outcomes of 404 patients with small HCC (<5 cm in diameter; group 1) were compared with those of 380 patients with large or multinodular HCC (group 2). The prognostic factors in the latter group were analyzed.
Results
The postoperative complication rate (27% vs. 23%; P = .16) and hospital mortality rate (2.4% vs. 2.7%; P = .82) were similar between groups. The overall survival rates were significantly higher in group 1 than group 2 (1 year, 88% vs. 74%; 3 years, 76% vs. 50%; 5 years, 58% vs. 39%; P < .001). Among patients in group 2, five independent prognostic factors were identified to be associated with a worse overall survival: namely, symptomatic disease, presence of cirrhosis, multinodular tumor, microvascular tumor invasion, and positive histological margin.
Conclusions
Hepatic resection can be safely performed in patients with large or multinodular HCC, with an overall 5-year survival rate of 39%. Symptomatic disease, the presence of cirrhosis, a multinodular tumor, microvascular invasion, and a positive histological margin are independently associated with a less favorable survival outcome.
Similar content being viewed by others
References
DM Parkin F Bray J Ferlay P Pisani (2001) ArticleTitleEstimating the world cancer burden: Globocan 2000 Int J Cancer 94 153–6 Occurrence Handle10.1002/ijc.1440 Occurrence Handle1:CAS:528:DC%2BD3MXntVGlu78%3D Occurrence Handle11668491
E Mor RT Kaspa P Sheiner M Schwartz (1998) ArticleTitleTreatment of hepatocellular carcinoma associated with cirrhosis in the era of liver transplantation Ann Intern Med 129 643–53 Occurrence Handle1:STN:280:DyaK1cvkt12gtw%3D%3D Occurrence Handle9786813
K Ota S Teraoka T Kawai (1995) ArticleTitleDonor difficulties in Japan and Asian countries Transplant Proc 27 83–6 Occurrence Handle1:STN:280:DyaK2M7osVymtQ%3D%3D Occurrence Handle7879197
A Mazziotti GL Grazi A Cavallari (1998) ArticleTitleSurgical treatment of hepatocellular carcinoma on cirrhosis: a Western experience Hepatogastroenterology 45 IssueIDSuppl 3 1281–7 Occurrence Handle9730389
ST Fan CM Lo CL Liu et al. (1999) ArticleTitleHepatectomy for hepatocellular carcinoma: toward zero hospital deaths Ann Surg 229 322–30 Occurrence Handle10.1097/00000658-199903000-00004 Occurrence Handle10077043
G Torzilli M Makuuchi K Inoue et al. (1999) ArticleTitleNo-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? A prospective analysis of our approach Arch Surg 134 984–92 Occurrence Handle10.1001/archsurg.134.9.984 Occurrence Handle1:STN:280:DyaK1MvhsFGgtw%3D%3D Occurrence Handle10487594
RT Poon ST Fan CM Lo et al. (2001) ArticleTitleImproving survival results after resection of hepatocellular carcinoma: a prospective study of 377 patients over 10 years Ann Surg 234 63–70 Occurrence Handle10.1097/00000658-200107000-00010 Occurrence Handle1:STN:280:DC%2BD3MzlvFChsQ%3D%3D Occurrence Handle11420484
K Okuda T Ohtsuki H Obata et al. (1985) ArticleTitleNatural history of hepatocellular carcinoma and prognosis in relation to treatment Study of 850 patients. Cancer 56 918–28 Occurrence Handle1:STN:280:DyaL2M3lsVaqtw%3D%3D
Greene FL, Page DL, Fleming ID. Liver including intrahepatic bile ducts. In: American Joint Committee on Cancer Staging Manual. NewYork: Springer-Verlag, 2002
J Bruix JM Llovet (2002) ArticleTitlePrognostic prediction and treatment strategy in hepatocellular carcinoma Hepatology 35 519–24 Occurrence Handle10.1053/jhep.2002.32089 Occurrence Handle11870363
RN Pugh IM Murray-Lyon JL Dawson MC Pietroni R Williams (1973) ArticleTitleTransection of the oesophagus for bleeding oesophageal varices Br J Surg 60 646–9 Occurrence Handle1:STN:280:DyaE3s3jsVWqsw%3D%3D Occurrence Handle4541913 Occurrence Handle10.1002/bjs.1800600817
JB Sorensen M Klee T Palshof HH Hansen (1993) ArticleTitlePerformance status assessment in cancer patients. An inter-observer variability study Br J Cancer 67 773–5 Occurrence Handle1:STN:280:DyaK3s3ivFamuw%3D%3D Occurrence Handle8471434
Y Fong RL Sun W Jarnagin LH Blumgart (1999) ArticleTitleAn analysis of 412 cases of hepatocellular carcinoma at a Western center Ann Surg 229 790–9 Occurrence Handle10.1097/00000658-199906000-00005 Occurrence Handle1:STN:280:DyaK1M3ptVGlsg%3D%3D Occurrence Handle10363892
G Otto U Heuschen WJ Hofmann G Krumm U Hinz C Herfarth (1998) ArticleTitleSurvival and recurrence after liver transplantation versus liver resection for hepatocellular carcinoma: a retrospective analysis Ann Surg 227 424–32 Occurrence Handle10.1097/00000658-199803000-00015 Occurrence Handle1:STN:280:DyaK1c7os1aqtw%3D%3D Occurrence Handle9527066
JM Llovet J Fuster J Bruix (1999) ArticleTitleIntention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation Hepatology 30 1434–40 Occurrence Handle10.1002/hep.510300629 Occurrence Handle1:STN:280:DC%2BD3c%2Fkt1eiug%3D%3D Occurrence Handle10573522
J Yamamoto S Okada K Shimada et al. (2001) ArticleTitleTreatment strategy for small hepatocellular carcinoma: comparison of long-term results after percutaneous ethanol injection therapy and surgical resection Hepatology 34 707–13 Occurrence Handle10.1053/jhep.2001.27950 Occurrence Handle1:STN:280:DC%2BD3Mrjs1Squw%3D%3D Occurrence Handle11584366
K Shirabe M Shimada T Gion et al. (1999) ArticleTitlePostoperative liver failure after major hepatic resection for hepatocellular carcinoma in the modern era with special reference to remnant liver volume J Am Coll Surg 188 304–9 Occurrence Handle10.1016/S1072-7515(98)00301-9 Occurrence Handle1:STN:280:DyaK1M7mtlOjsQ%3D%3D Occurrence Handle10065820
T Matsumata Y Ikeda H Hayashi T Kamakura A Taketomi K Sugimachi (1993) ArticleTitleThe association between transfusion and cancer-free survival after curative resection for hepatocellular carcinoma Cancer 72 1866–71 Occurrence Handle1:STN:280:DyaK3szntlahtA%3D%3D Occurrence Handle8395966 Occurrence Handle10.1002/1097-0142(19930915)72:6<1866::AID-CNCR2820720613>3.0.CO;2-F
AS Befeler AM Di Bisceglie (2002) ArticleTitleHepatocellular carcinoma: diagnosis and treatment Gastroenterology 122 1609–19 Occurrence Handle12016426 Occurrence Handle10.1053/gast.2002.33411
Z Hassoun GJ Gores (2003) ArticleTitleTreatment of hepatocellular carcinoma Clin Gastroenterol Hepatol 1 10–8 Occurrence Handle10.1053/jcgh.2003.50003 Occurrence Handle15017512
N Nagasue H Kohno YC Chang et al. (1993) ArticleTitleLiver resection for hepatocellular carcinoma. Results of 229 consecutive patients during 11 years Ann Surg 217 375–84 Occurrence Handle1:STN:280:DyaK3s3itFamuw%3D%3D Occurrence Handle8385442 Occurrence Handle10.1097/00000658-199304000-00009
L Capussotti G Borgonovo H Bouzari C Smadja D Grange D Franco (1994) ArticleTitleResults of major hepatectomy for large primary liver cancer in patients with cirrhosis Br J Surg 81 427–31 Occurrence Handle1:STN:280:DyaK2c3ivValug%3D%3D Occurrence Handle8173920 Occurrence Handle10.1002/bjs.1800810335
T Shuto K Hirohashi S Kubo et al. (1999) ArticleTitleEfficacy of major hepatic resection for large hepatocellular carcinoma Hepatogastroenterology 46 413–6 Occurrence Handle1:STN:280:DyaK1M3ksFGitA%3D%3D Occurrence Handle10228832
K Hanazaki S Kajikawa N Shimozawa et al. (2001) ArticleTitleHepatic resection for large hepatocellular carcinoma Am J Surg 181 347–53 Occurrence Handle10.1016/S0002-9610(01)00584-0 Occurrence Handle1:STN:280:DC%2BD3MzotV2jsA%3D%3D Occurrence Handle11438270
NH Lee GY Chau WY Lui KL King SH Tsay CW Wu (1998) ArticleTitleSurgical treatment and outcome in patients with a hepatocellular carcinoma greater than 10 cm in diameter Br J Surg 85 1654–7 Occurrence Handle10.1046/j.1365-2168.1998.00918.x Occurrence Handle1:STN:280:DyaK1M%2FptFaqtQ%3D%3D Occurrence Handle9876069
K Hanazaki S Kajikawa N Shimozawa et al. (2002) ArticleTitleHepatic resection for hepatocellular carcinoma in diameter of > or = 10 cm Hepatogastroenterology 49 518–23 Occurrence Handle11995486
RT Poon ST Fan J Wong (2002) ArticleTitleSelection criteria for hepatic resection in patients with large hepatocellular carcinoma larger than 10 cm in diameter J Am Coll Surg 194 592–602 Occurrence Handle10.1016/S1072-7515(02)01163-8 Occurrence Handle12022599
H Lau K Man ST Fan WC Yu CM Lo J Wong (1997) ArticleTitleEvaluation of preoperative hepatic function in patients with hepatocellular carcinoma undergoing hepatectomy Br J Surg 84 1255–9 Occurrence Handle10.1002/bjs.1800840917 Occurrence Handle1:STN:280:DyaK2svlvV2gsA%3D%3D Occurrence Handle9313707
JM Llovet C Bru J Bruix (1999) ArticleTitlePrognosis of hepatocellular carcinoma: the BCLC staging classification Semin Liver Dis 19 329–38 Occurrence Handle1:STN:280:DyaK1Mvks1Grsg%3D%3D Occurrence Handle10518312 Occurrence Handle10.1055/s-2007-1007122
G Pelletier A Roche O Ink et al. (1990) ArticleTitleA randomized trial of hepatic arterial chemoembolization in patients with unresectable hepatocellular carcinoma J Hepatol 11 181–4 Occurrence Handle1:STN:280:DyaK3M%2Fnt12hsQ%3D%3D Occurrence Handle2174933 Occurrence Handle10.1016/0168-8278(90)90110-D
MV Madden JE Krige S Bailey et al. (1993) ArticleTitleRandomised trial of targeted chemotherapy with lipiodol and 5-epidoxorubicin compared with symptomatic treatment for hepatoma Gut 34 1598–600 Occurrence Handle1:STN:280:DyaK2c%2FmtlKgug%3D%3D Occurrence Handle8244149 Occurrence Handle10.1136/gut.34.11.1598
Groupe d’Etude et de (1995) ArticleTitleTraitement du Carcinome Hepatocellu-laire. A comparison of lipiodol chemoembolization and conservative treatment for unresectable hepatocellular carcinoma N Engl J Med 332 1256–61 Occurrence Handle10.1056/NEJM199505113321903 Occurrence Handle7708069
G Pelletier M Ducreux F Gay et al. (1998) ArticleTitleTreatment of unresectable hepatocellular carcinoma with lipiodol chemoembolization: a multicenter randomized trial Groupe CHC. J Hepatol 29 129–34 Occurrence Handle10.1016/S0168-8278(98)80187-6 Occurrence Handle1:CAS:528:DyaK1cXmvVWhsLk%3D
JM Llovet MI Real X Montana et al. (2002) ArticleTitleArterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial Lancet 359 1734–9 Occurrence Handle10.1016/S0140-6736(02)08649-X Occurrence Handle12049862
CM Lo H Ngan WK Tso et al. (2002) ArticleTitleRandomized controlled trial of transarterial lipiodol chemoembolization for unresectable hepatocellular carcinoma Hepatology 35 1164–71 Occurrence Handle10.1053/jhep.2002.33156 Occurrence Handle1:CAS:528:DC%2BD38XktF2hu7w%3D Occurrence Handle11981766
JN Vauthey GY Lauwers NF Esnaola et al. (2002) ArticleTitleSimplified staging for hepatocellular carcinoma J Clin Oncol 20 1527–36 Occurrence Handle10.1200/JCO.20.6.1527 Occurrence Handle11896101
RT Poon ST Fan (2003) ArticleTitleEvaluation of the new AJCC/UICC staging system for hepatocellular carcinoma after hepatic resection in Chinese patients Surg Oncol Clin North Am 12 35–50 Occurrence Handle10.1016/S1055-3207(02)00086-8
Y Shiratori S Shiina M Imamura et al. (1995) ArticleTitleCharacteristic difference of hepatocellular carcinoma between hepatitis B- and C- viral infection in Japan Hepatology 22 1027– 33 Occurrence Handle10.1002/hep.1840220403 Occurrence Handle1:STN:280:DyaK28%2FivFCjtA%3D%3D Occurrence Handle7557847
J Belghiti Y Panis O Farges JP Benhamou F Fekete (1991) ArticleTitleIntrahepatic recurrence after resection of hepatocellular carcinoma complicating cirrhosis Ann Surg 214 114–7 Occurrence Handle1:STN:280:DyaK3MzivVGqtA%3D%3D Occurrence Handle1714267 Occurrence Handle10.1097/00000658-199108000-00004
K Ikeda S Saitoh A Tsubota et al. (1993) ArticleTitleRisk factors for tumor recurrence and prognosis after curative resection of hepatocellular carcinoma Cancer 71 19–25 Occurrence Handle1:STN:280:DyaK3s7gsFentA%3D%3D Occurrence Handle8380116 Occurrence Handle10.1002/1097-0142(19930101)71:1<19::AID-CNCR2820710105>3.0.CO;2-I
RT Poon ST Fan J Wong (2000) ArticleTitleRisk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma Ann Surg 232 10–24 Occurrence Handle10.1097/00000658-200007000-00003 Occurrence Handle10862190
JM Llovet J Bustamante A Castells et al. (1999) ArticleTitleNatural history of untreated nonsurgical hepatocellular carcinoma: rationale for the design and evaluation of therapeutic trials Hepatology 29 62–7 Occurrence Handle10.1002/hep.510290145 Occurrence Handle1:STN:280:DyaK1M%2FotFKrsw%3D%3D Occurrence Handle9862851
Y Ono T Yoshimasu R Ashikaga et al. (2000) ArticleTitleLong-term results of lipiodol-transcatheter arterial embolization with cisplatin or doxorubicin for unresectable hepatocellular carcinoma Am J Clin Oncol 23 564–8 Occurrence Handle10.1097/00000421-200012000-00006 Occurrence Handle1:STN:280:DC%2BD3M7gvVKnsA%3D%3D Occurrence Handle11202797
CB O’Suilleabhain RT Poon JL Yong GC Ooi WK Tso ST Fan (2003) ArticleTitleFactors predictive of 5-year survival after transarterial chemoembolization for inoperable hepatocellular carcinoma Br J Surg 90 325–31 Occurrence Handle10.1002/bjs.4045 Occurrence Handle1:STN:280:DC%2BD3s%2Fot1OisQ%3D%3D Occurrence Handle12594668
H Yoshioka M Sato T Sonomura M Terada K Kishi A Yoshikawa (1997) ArticleTitleFactors associated with survival exceeding 5 years after transcatheter arterial embolization for hepatocellular carcinoma Semin Oncol 24 S6 Occurrence Handle1:STN:280:DyaK2s3ps1emsg%3D%3D Occurrence Handle9151914
JM Llovet J Bruix (2003) ArticleTitleSystematic review of randomized trials for unresectable hepatocellular carcinoma: chemoembolization improves survival Hepatology 37 429–42 Occurrence Handle10.1053/jhep.2003.50047 Occurrence Handle1:CAS:528:DC%2BD3sXhsFeltrg%3D Occurrence Handle12540794
SD Ryder PM Rizzi E Metivier J Karani R Williams (1996) ArticleTitleChemoembolisation with lipiodol and doxorubicin: applicability in British patients with hepatocellular carcinoma Gut 38 125–8 Occurrence Handle1:STN:280:DyaK287msFSjuw%3D%3D Occurrence Handle8566839 Occurrence Handle10.1136/gut.38.1.125
EC Lai IO Ng MM Ng et al. (1990) ArticleTitleLong-term results of resection for large hepatocellular carcinoma: a multivariate analysis of clinicopathological features Hepatology 11 815–8 Occurrence Handle1:STN:280:DyaK3c3mvFOmuw%3D%3D Occurrence Handle2161393 Occurrence Handle10.1002/hep.1840110516
M Abdel-Wahab A Sultan A Ghawalby et al. (2001) ArticleTitleIs resection for large hepatocellular carcinoma in cirrhotic patients beneficial? Study of 38 cases Hepatogastroenterology 48 757–61 Occurrence Handle1:STN:280:DC%2BD38%2FitFOktA%3D%3D Occurrence Handle11462920
RT Poon ST Fan CM Lo CL Liu IO Ng J Wong (2000) ArticleTitleLong-term prognosis after resection of hepatocellular carcinoma associated with hepatitis B-related cirrhosis J Clin Oncol 18 1094–101 Occurrence Handle1:STN:280:DC%2BD3c7mtVOmtA%3D%3D Occurrence Handle10694562
RT Poon IO Ng C Lau et al. (2001) ArticleTitleSerum vascular endothelial growth factor predicts venous invasion in hepatocellular carcinoma: a prospective study Ann Surg 233 227– 35 Occurrence Handle10.1097/00000658-200102000-00012 Occurrence Handle1:STN:280:DC%2BD3M7ls1SmsQ%3D%3D Occurrence Handle11176129
JB Dimick JA Cowan SuffixJr. JA Knol GR Upchurch SuffixJr. (2003) ArticleTitleHepatic resection in the United States: indications, outcomes, and hospital procedural volumes from a nationally representative database Arch Surg 138 185–91 Occurrence Handle10.1001/archsurg.138.2.185 Occurrence Handle12578418
Acknowledgment
Supported by the Outstanding Young Researcher Award and the Sun C. Y. Research Foundation for Hepatobiliary and Pancreatic Surgery of the University of Hong Kong.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ng, K.K., Vauthey, JN., Pawlik, T.M. et al. Is Hepatic Resection for Large or Multinodular Hepatocellular Carcinoma Justified? Results From a Multi-Institutional Database. Ann Surg Oncol 12, 364–373 (2005). https://doi.org/10.1245/ASO.2005.06.004
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1245/ASO.2005.06.004