Skip to main content

Advertisement

SpringerLink
Log in

HCC: current surgical treatment concepts

  • Review Article
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract

Purpose

The purpose of this study is to review indications and results of surgical treatments of hepatocellular carcinoma (HCC). This tumor, which represents one of the most common malignancies worldwide, is characterized by its prominent development in patients with chronic liver disease (CLD). Liver transplantation (LT) is considered as the ideal treatment of limited HCC removing both tumor(s) and the pre-neoplasic underlying diseased liver. However, this treatment, which is not available in many countries, is restricted to patients with minimum risk of tumor recurrence under immunosuppression. The risk of recurrence is minimized in patients fulfilling the Milan criteria with a tendency to accept slight expansion of size in patients with favourable natural history and low AFP level. Increasing duration in the waiting list before LT leads several teams to use neoadjuvant therapies such as percutaneous ablation, TACE and liver resection. Liver resection in cirrhotic patients with good liver function remains the most available efficient treatment of patients with HCC. Better liver function assessment, understanding of the segmental liver anatomy with more accurate imaging studies and surgical technique refinements are the most important factors that have contributed to reduce mortality with an expecting 5 years survival of 70%. There is considerable interest in combined treatment associating resection and LT. Transplantable patients with good liver function should be considered for liver resection as primary therapy and for LT in case of tumor recurrence. This salvage strategy is refined using pathological analysis of the resected specimen which identifies histological pejorative factors allowing selecting patients who should transplanted before recurrence.

Conclusions

The improvement of survival in HCC patients after surgical treatment results from refinements in surgical technique and better identification of adverse prognostic factors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

HCC:

Hepatocellular carcinoma

LR:

Liver resection

LT:

Liver transplantation

TACE:

Transarterial chemoembolization

RFA:

Radiofrequency ablation

MC:

Milan criteria

MELD:

Model for end-stage liver disease

CLD:

Chronic liver disease

MRI:

Magnetic resonance imaging

PH:

Portal hypertension

References

  1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893–2917

    Article  PubMed  CAS  Google Scholar 

  2. Rahbari NN, Mehrabi A, Mollberg NM, Müller SA, Koch M, Büchler MW, Weitz J (2011) Hepatocellular carcinoma: current management and perspectives for the future. Ann Surg 253:453–469

    Article  PubMed  Google Scholar 

  3. El-Serag HB, Marrero JA, Rudolph L, Reddy KR (2008) Diagnosis and treatment of hepatocellular carcinoma. Gastroenterology 134:1752–1763

    Article  PubMed  Google Scholar 

  4. Llovet JM, Burroughs A, Bruix J (2003) Hepatocellular carcinoma. Lancet 362:1907–1917

    Article  PubMed  Google Scholar 

  5. Forner A, Reig ME, de Lope CR, Bruix J (2010) Current strategy for staging and treatment: the BCLC update and future prospects. Semin Liver Dis 30:61–74

    Article  PubMed  CAS  Google Scholar 

  6. Eguchi S, Kanematsu T, Arii S, for the Liver Cancer Study Group of Japan (2011) Recurrence-free survival more than 10 years after liver resection for hepatocellular carcinoma. Br J Surg 98:552–557

    Article  PubMed  CAS  Google Scholar 

  7. Cucchetti A, Vitale A, Gaudio MD, Pinna AD (2010) Harm and benefits of primary liver resection and salvage transplantation for hepatocellular carcinoma. Am J Transplant 10:619–627

    Article  PubMed  CAS  Google Scholar 

  8. Fuks D, Dokmak S, Paradis V, Diouf M, Durand F, Belghiti J (2012) Benefit of initial resection of hepatocellular carcinoma followed by transplantation in case of recurrence: An intention-to-treat analysis. Hepatology 55:132–140

    Article  PubMed  Google Scholar 

  9. Belghiti J, Cortes A, Abdalla EK, Re’gimbeau JM, Prakash K, Durand F et al (2003) Resection prior to liver transplantation for hepatocellular carcinoma. Ann Surg 238:885–893

    Article  PubMed  Google Scholar 

  10. Poon RT, Fan ST, Lo CM, Liu CL, Wong J (2002) Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg 235:373–382

    Article  PubMed  Google Scholar 

  11. Starley BQ, Calcagno CJ, Harrison SA (2010) Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology 51:1820–1832

    Article  PubMed  Google Scholar 

  12. Bedossa P, Moucari R, Chelbi E et al (2007) Evidence for a role of nonalcoholic steatohepatitis in hepatitis C: a prospective study. Hepatology 46:380–387

    Article  PubMed  CAS  Google Scholar 

  13. Paradis V, Zalinski S, Chelbi E et al (2009) Hepatocellular carcinoma in patients with metabolic syndrome often develops without significant liver fibrosis: a pathological analysis. Hepatology 49:851–859

    Article  PubMed  Google Scholar 

  14. Takuma Y, Nouso K (2010) Nonalcoholic steatohepatitis-associated hepatocellular carcinoma: our case series and literature review. World J Gastroenterol 16:1436–1441

    Article  PubMed  CAS  Google Scholar 

  15. Bralet MP, Regimbeau JM, Pineau P, Dubois S, Loas G, Degos F et al (2000) Hepatocellular carcinoma occurring in nonfibrotic liver: epidemiologic and histopathologic analysis of 80 French cases. Hepatology 32:200–204

    Article  PubMed  CAS  Google Scholar 

  16. Grando-Lemaire V, Guettier C, Chevret S, Beaugrand M, Trinchet JC (1999) Hepatocellular carcinoma without cirrhosis in the West: epidemiological factors and histopathology of the non-tumorous liver. Groupe d’Etude et de Traitement du Carcinome Hepatocellulaire. J Hepatol 31:508–513

    Article  PubMed  CAS  Google Scholar 

  17. El Serag HB, Davila JA (2004) Is fibrolamellar carcinoma different from hepatocellular carcinoma? A US population-based study. Hepatology 39:798–803

    Article  PubMed  Google Scholar 

  18. Ringe B, Wittekind C, Weimann A, Tusch G, Pichlmayr R (1992) Results of hepatic resection and transplantation for fibrolamellar carcinoma. Surg Gynecol Obstet 175:299–305

    PubMed  CAS  Google Scholar 

  19. Poon RT, Fan ST, Wong J (2002) Selection criteria for hepatic resection in patients with large hepatocellular carcinoma larger than 10 cm in diameter. J Am Coll Surg 194:592–602

    Article  PubMed  Google Scholar 

  20. Regimbeau JM, Farges O, Shen BY, Sauvanet A, Belghiti J (1999) Is surgery for large hepatocellular carcinoma justified? J Hepatol 31:1062–1068

    Article  PubMed  CAS  Google Scholar 

  21. Yeh CN, Lee WC, Chen MF (2003) Hepatic resection and prognosis for patients with hepatocellular carcinoma larger than 10 cm: two decades of experience at Chang Gung memorial hospital. Ann Surg Oncol 10:1070–1076

    Article  PubMed  Google Scholar 

  22. Belghiti J, Regimbeau JM, Durand F, Kianmanesh AR, Dondero F, Terris B et al (2002) Resection of hepatocellular carcinoma: a European experience on 328 cases. Hepatogastroenterology 49:41–46

    PubMed  CAS  Google Scholar 

  23. Smoot RL, Nagorney DM, Chandan VS et al (2011) Resection of hepatocellular carcinoma in patients without cirrhosis. Br J Surg 98:697–703

    Article  PubMed  CAS  Google Scholar 

  24. Bilimoria MM, Lauwers GY, Doherty DA, Nagomey DM, Belghiti J, Do KA et al (2001) Underlying liver disease, not tumor factors, predicts long-term survival after resection of hepatocellular carcinoma. Arch Surg 136:528–235

    Article  PubMed  CAS  Google Scholar 

  25. Lerut J, Mergental H, Kahn D, Albuquerque L, Marrero J, Vauthey JN, Porte RJ (2011) Place of liver transplantation in the treatment of hepatocellular carcinoma in the normal liver. Liver Transpl 17(Suppl 2):S90–7

    Article  PubMed  Google Scholar 

  26. Ishizawa T, Hasegawa K, Aoki T, Takahashi M, Inoue Y, Sano K, Imamura H, Sugawara Y, Kokudo N, Makuuchi M (2008) Neither multiple tumors nor portal hypertension are surgical contraindications for hepatocellular carcinoma. Gastroenterology 134:1908–1916

    Article  PubMed  Google Scholar 

  27. Makuuchi M, Sano K (2004) The surgical approach to HCC: our progress and results in Japan. Liver Transpl 10:S46–52

    Article  PubMed  Google Scholar 

  28. Roayaie S, Blume IN, Thung SN, Guido M, Fiel MI, Hiotis S et al (2009) A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology 137:850–855

    Article  PubMed  Google Scholar 

  29. Imamura H, Matsuyama Y, Miyagawa Y, Ishida K, Shimada R, Miyagawa S et al (1999) Prognostic significance of anatomical resection and des-gamma-carboxy prothrombin in patients with hepatocellular carcinoma. Br J Surg 86:1032–1038

    Article  PubMed  CAS  Google Scholar 

  30. Regimbeau JM, Kianmanesh R, Farges O, Dondero F, Sauvanet A, Belghiti J (2002) Extent of liver resection influences the outcome in patients with cirrhosis and small hepatocellular carcinoma. Surgery 131:311–317

    Article  PubMed  Google Scholar 

  31. Arii S, Tanaka S, Mitsunori Y, Nakamura N, Kudo A, Noguchi N, Irie T (2010) Surgical strategies for hepatocellular carcinoma with special reference to anatomical hepatic resection and intraoperative contrast-enhanced ultrasonography. Oncology 78(Suppl 1):125–30

    Article  PubMed  Google Scholar 

  32. Eguchi S, Kanematsu T, Arii S, Okazaki M, Okita K, Omata M, Ikai I, Kudo M, Kojiro M, Makuuchi M, Monden M, Matsuyama Y, Nakanuma Y, Takayasu K, Liver Cancer Study Group of Japan (2008) Comparison of the outcomes between an anatomical subsegmentectomy and a non-anatomical minor hepatectomy for single hepatocellular carcinomas based on a Japanese nationwide survey. Surgery 143:469–475

    Article  PubMed  Google Scholar 

  33. Wakai T, Shirai Y, Sakata J, Kaneko K, Cruz PV, Akazawa K, Hatakeyama K (2007) Anatomic resection independently improves long-term survival in patients with T1-T2 hepatocellular carcinoma. Ann Surg Oncol 14:1356–1365

    Article  PubMed  Google Scholar 

  34. Ueno S, Kubo F, Sakoda M, Hiwatashi K, Tateno T, Mataki Y, Maemura K, Shinchi H, Natsugoe S, Aikou T (2008) Efficacy of anatomic resection vs nonanatomic resection for small nodular hepatocellular carcinoma based on gross classification. J Hepatobiliary Pancreat Surg 15:493–500

    Article  PubMed  Google Scholar 

  35. Shi M, Guo RP, Lin XJ et al (2007) Partial hepatectomy with wide versus narrow resection margin for solitary hepatocellular carcinoma: a prospective randomized trial. Ann Surg 245:36–43

    Article  PubMed  Google Scholar 

  36. Poon RT, Fan ST, Ng IO, Lo CM, Liu CL, Wong J (2000) Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer 89:500–507

    Article  PubMed  CAS  Google Scholar 

  37. Radtke A, Sotiropoulos GC, Molmenti EP, Schroeder T, Peitgen HO, Frilling A, Broering DC, Broelsch CE, Malago M (2010) Computer-assisted surgery planning for complex liver resections: when is it helpful? A single-center experience over an 8-year period. Ann Surg 252:876–883

    Article  PubMed  Google Scholar 

  38. Pugh RN, Murray-Lyon IM, Dawson JL, Pietroni MC, Williams R (1973) Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 60:646–649

    Article  PubMed  CAS  Google Scholar 

  39. Torzilli G, Makuuchi M, Inoue K, Takayama T, Sakamoto Y, Sugawara Y et al (1999) No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? A prospective analysis of our approach. Arch Surg 134:984–992

    Article  PubMed  CAS  Google Scholar 

  40. Wakabayashi H, Ishimura K, Izuishi K, Karasawa Y, Maeta H (2004) Evaluation of liver function for hepatic resection for hepatocellular carcinoma in the liver with damaged parenchyma. J Surg Res 116:248–252

    Article  PubMed  Google Scholar 

  41. Fan ST, Lai EC, Lo CM et al (1995) Hospital mortality of major hepatectomy for hepatocellular carcinoma associated with cirrhosis. Arch Surg 130:198–203

    Article  PubMed  CAS  Google Scholar 

  42. Lam CM, Fan ST, Lo CM et al (1999) Major hepatectomy for hepatocellular carcinoma in patients with an unsatisfactory indocyanine green clearance test. Br J Surg 86:1012–1017

    Article  PubMed  CAS  Google Scholar 

  43. Fan ST (2010) Liver functional reserve estimation: state of the art and relevance for local treatments: the Eastern perspective. J Hepatobiliary Pancreat Sci 17:380–384

    Article  PubMed  Google Scholar 

  44. Belli G, Fantini C, Belli A, Limongelli P (2011) Laparoscopic liver resection for hepatocellular carcinoma in cirrhosis: long-term outcomes. Dig Surg 28:134–140

    Article  PubMed  Google Scholar 

  45. Hsu KY, Chau GY, Lui WY, Tsay SH, King KL, Wu CW (2009) Predicting morbidity and mortality after hepatic resection in patients with hepatocellular carcinoma: the role of Model for End-Stage Liver Disease score. World J Surg 33:2412–2419

    Article  PubMed  Google Scholar 

  46. Delis SG, Bakoyiannis A, Biliatis I, Athanassiou K, Tassopoulos N, Dervenis C (2009) Model for end-stage liver disease (MELD) score, as a prognostic factor for post-operative morbidity and mortality in cirrhotic patients, undergoing hepatectomy for hepatocellular carcinoma. HPB (Oxford) 11:351–357

    Article  Google Scholar 

  47. Stockmann M, Lock JF, Riecke B, Heyne K, Martus P, Fricke M, Lehmann S, Niehues SM, Schwabe M, Lemke AJ, Neuhaus P (2009) Prediction of postoperative outcome after hepatectomy with a new bedside test for maximal liver function capacity. Ann Surg 250:119–125

    Article  PubMed  Google Scholar 

  48. Lesurtel M, Graf R, Aleil B, Walther DJ, Tian Y, Jochum W, Gachet C, Bader M, Clavien PA (2006) Platelet-derived serotonin mediates liver regeneration. Science 312:104–107

    Article  PubMed  CAS  Google Scholar 

  49. Maithel SK, Kneuertz PJ, Kooby DA, Scoggins CR, Weber SM, Martin RC 2nd, McMasters KM, Cho CS, Winslow ER, Wood WC, Staley CA 3rd (2011) Importance of low preoperative platelet count in selecting patients for resection of hepatocellular carcinoma: a multi-institutional analysis. J Am Coll Surg 212:638–650

    Article  PubMed  Google Scholar 

  50. Farges O, Malassagne B, Flejou JF, Balzan S, Sauvanet A, Belghiti J (1999) Risk of major liver resection in patients with underlying chronic liver disease: a reappraisal. Ann Surg 229:210–215

    Article  PubMed  CAS  Google Scholar 

  51. Yamakado K, Takeda K, Matsumura K, Nakatsuka A, Hirano T, Kato N et al (1997) Regeneration of the un-embolized liver parenchyma following portal vein embolization. J Hepatol 27:871–880

    Article  PubMed  CAS  Google Scholar 

  52. Ogata S, Belghiti J, Farges O, Varma D, Sibert A, Vilgrain V (2006) Sequential arterial and portal vein embolizations before right hepatectomy in patients with cirrhosis and hepatocellular carcinoma. Br J Surg 93:1091–1098

    Article  PubMed  CAS  Google Scholar 

  53. Yoo H, Kim JH, Ko GY, Kim KW, Gwon DI, Lee SG, Hwang S (2011) Sequential transcatheter arterial chemoembolization and portal vein embolization versus portal vein embolization only before major hepatectomy for patients with hepatocellular carcinoma. Ann Surg Oncol 18:1251–1257

    Article  PubMed  Google Scholar 

  54. Truant S, Oberlin O, Sregent G et al (2007) Remnant liver vilume to body weight ratio > or =0.5%: A new cut-off to estimate postoperative risks after extended liver resection in noncirrhotic liver. J Am Coll Surg 204:22–33

    Article  PubMed  Google Scholar 

  55. Chun YS, Ribero D, Abdala EK et al (2008) Comparison of two methods of future liver remnant volume measurement. J Gastrointest Surg 12:123–128

    Article  PubMed  Google Scholar 

  56. Farges O, Belghiti J, Kianmanesh R et al (2003) Portal vein embolization before right hepatectomy: Prospective clinical trial. Ann Surg 237:208–217

    PubMed  Google Scholar 

  57. de Graaf W, van Lienden KP, van den Esschert JW et al (2011) Increase in future remnant liver fuction after preoperative portal vein embolization. Br J Surg 98:825–834

    Article  PubMed  Google Scholar 

  58. Yumoto Y, Yagi T, Sato S et al (2010) Preoperative estimation of remnant hepatic function using fusion images obtained by (99 m)Tc-labelled galactosyl-human serum albumin liver scintigraphy and computed tomography. Br J Surg 97:934–944

    Article  PubMed  CAS  Google Scholar 

  59. Capussotti L, Ferrero A, Viganò L, Muratore A, Polastri R, Bouzari H (2006) Portal hypertension: contraindication to liver surgery? World J Surg 30:992–999

    Article  PubMed  Google Scholar 

  60. Bruix J, Sherman M (2005) Management of hepatocellular carcinoma. Hepatology 42:1208–1236

    Article  PubMed  Google Scholar 

  61. Kawano Y, Sasaki A, Kai S et al (2008) Short- and long-term outcomes after hepatic resection for hepatocellular carcinoma with concomitant esophageal varices in patients with cirrhosis. Ann Surg Oncol 15:1670–1676

    Article  PubMed  Google Scholar 

  62. Matsumoto K, Yoshimoto J, Sugo H, Kojima K, Futagawa S, Matsumoto T (2002) Relationship between the histological degrees of hepatitis and the postoperative recurrence of hepatocellular carcinoma in patients with hepatitis C. Hepatol Res 23:196–201

    Article  PubMed  Google Scholar 

  63. Noun R, Jagot P, Farges O, Sauvanet A, Belghiti J (1997) High preoperative serum alanine transferase levels: effect on the risk of liver resection in Child grade A cirrhotic patients. World J Surg 21:390–394

    Article  PubMed  CAS  Google Scholar 

  64. Ettorre GM, Sommacale D, Farges O, Sauvanet A, Guevara O, Belghiti J (2001) Postoperative liver function after elective right hepatectomy in elderly patients. Br J Surg 88:73–76

    Article  PubMed  CAS  Google Scholar 

  65. Yeh CN, Lee WC, Jeng LB, Chen MF, Yu MC (2002) Spontaneous tumour rupture and prognosis in patients with hepatocellular carcinoma. Br J Surg 89:1125–1129

    Article  PubMed  Google Scholar 

  66. Luo YQ, Wang Y, Chen H, Wu MC (2002) Influence of preoperative transcatheter arterial chemoembolization on liver resection in patients with resectable hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int 1:523–526

    PubMed  Google Scholar 

  67. Majno PE, Adam R, Bismuth H, Castaing D, Ariche A, Krissat J et al (1997) Influence of preoperative transarterial lipiodol chemoembolization on resection and transplantation for hepatocellular carcinoma in patients with cirrhosis. Ann Surg 226:688–701

    Article  PubMed  CAS  Google Scholar 

  68. Schwartz JD, Schwartz M, Mandeli J, Sung M (2002) Neoadjuvant and adjuvant therapy for resectable hepatocellular carcinoma: review of the randomised clinical trials. Lancet Oncol 3:593–603

    Article  PubMed  Google Scholar 

  69. Ikai I, Yamamoto Y, Yamamoto N, Terajima H, Hatano E, Shimahara Y et al (2003) Results of hepatic resection for hepatocellular carcinoma invading major portal and/or hepatic veins. Surg Oncol Clin North Am 12:65–75

    Article  Google Scholar 

  70. Kim SU, Kim YR, do Kim Y, Kim JK, Lee HW, Kim BK, Han KH, Chon CY, Moon YM, Ahn SH (2007) Clinical features and treatment outcome of advanced hepatocellular carcinoma with inferior vena caval invasion or atrial tumor thrombus. Korean J Hepatol 13:387–395

    Article  PubMed  Google Scholar 

  71. Yoshidome H, Takeuchi D, Kimura F, Shimizu H, Ohtsuka M, Kato A, Furukawa K, Yoshitomi H, Miyazaki M (2011) Treatment strategy for hepatocellular carcinoma with major portal vein or inferior vena cava invasion: a single institution experience. J Am Coll Surg 212:796–803

    Article  PubMed  Google Scholar 

  72. Vogl TJ, Nour-Eldin NE, Emad-Eldin S, Naguib NN, Trojan J, Ackermann H, Abdelaziz O (2011) Portal vein thrombosis and arterioportal shunts: effects on tumor response after chemoembolization of hepatocellular carcinoma. World J Gastroenterol 17:1267–1275

    Article  PubMed  Google Scholar 

  73. Chung GE, Lee JH, Kim HY, Hwang SY, Kim JS, Chung JW, Yoon JH, Lee HS, Kim YJ (2011) Transarterial chemoembolization can be safely performed in patients with hepatocellular carcinoma invading the main portal vein and may improve the overall survival. Radiology 258:627–634

    Article  PubMed  Google Scholar 

  74. Pocard M, Sauvanet A, Regimbeau JM, Duwat O, Farges O, Belghiti J (2002) Limits and benefits of exclusive transthoracic hepatectomy approach for patients with hepatocellular carcinoma. Hepatogastroenterology 49:32–35

    PubMed  Google Scholar 

  75. Ko S, Nakajima Y, Kanehiro H, Aomatsu Y, Yoshimura A, Taki J, Kin T, Yagura K, Ohashi K, Nakano H (1997) Transthoracic transdiaphragmatic approach for hepatectomy of Couinaud’s segments VII and VIII. World J Surg 21:86–90

    Article  PubMed  CAS  Google Scholar 

  76. Torzilli G, Takayama T, Hui AM, Kubota K, Harihara Y, Makuuchi M (1999) A new technical aspect of ultrasound-guided liver surgery. Am J Surg 178:341–343

    Article  PubMed  CAS  Google Scholar 

  77. Kim TK, Lee KH, Khalili K, Jang HJ (2011) Hepatocellular nodules in liver cirrhosis: contrast-enhanced ultrasound. Abdom Imaging 36:244–263

    Article  PubMed  Google Scholar 

  78. Lai EC, Fan ST, Lo CM, Chu KM, Liu CL (1996) Anterior approach for difficult major right hepatectomy. World J Surg 20:314–317

    Article  PubMed  CAS  Google Scholar 

  79. Liu CL, Fan ST, Lo CM, Tung-Ping Poon R, Wong J (2000) Anterior approach for major right hepatic resection for large hepatocellular carcinoma. Ann Surg 232:25–31

    Article  PubMed  CAS  Google Scholar 

  80. Belghiti J, Guevara OA, Noun R, Saldinger PF, Kianmanesh R (2001) Liver hanging maneuver: a safe approach to right hepatectomy without liver mobilization. J Am Coll Surg 193:109–111

    Article  PubMed  CAS  Google Scholar 

  81. Wu TJ, Wang F, Lin YS et al (2010) Right hepatectomy by the anterior method with liver hanging versus conventional approach for large hepatocellular carcinomas. Br J Surg 97:1070–1078

    Article  PubMed  Google Scholar 

  82. Katz SC, Shia J, Liau KH et al (2009) Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg 249:617–623

    Article  PubMed  Google Scholar 

  83. Belghiti J, Noun R, Malafosse R, Jagot P, Sauvanet A, Pierangeli F et al (1999) Continuous versus intermittent portal triad clamping for liver resection: a controlled study. Ann Surg 229:369–375

    Article  PubMed  CAS  Google Scholar 

  84. Ishizaki Y, Yoshimoto J, Miwa K, Sugo H, Kawasaki S (2006) Safety of prolonged intermittent pringle maneuver during hepatic resection. Arch Surg 141:649–653

    Article  PubMed  Google Scholar 

  85. Rahbari NN, Koch M, Zimmermann JB et al (2011) Infrahepatic inferior vena cava clamping for reduction of central venous pressure and blood loss during hepatic resection: a randomized controlled trial. Ann Surg 253:1102–1110

    Article  PubMed  Google Scholar 

  86. Buell JF, Cherqui D, Geller DA et al (2009) The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 250:825–830

    Article  PubMed  Google Scholar 

  87. Dagher I, Belli G, Fantini C et al (2010) Laparoscopic resection for hepatocellular carcinoma: a European experience. J Am Coll Surg 211:16–23

    Article  PubMed  Google Scholar 

  88. Laurent A, Tayar C, Andréoletti M, Lauzet JY, Merle JC, Cherqui D (2009) Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 16:310–314

    Article  PubMed  Google Scholar 

  89. Casaccia M, Andorno E, Nardi I, Santori G, Troilo B, Barabino G, Di Domenico S, Panaro F, Valente U (2009) Laparoscopic staging and radiofrequency of hepatocellular carcinoma in liver ci rrhosis. A “bridge” treatment to liver transplantation. Hepatogastroenterology 56:793–797

    PubMed  Google Scholar 

  90. Ramos Fernandez M, Loinaz Segurola C, Fernandez Cebrian JM, Vega Lopez ML (2011) Laparoscopic and hand-assisted liver resection: preliminary results at a mid-sized hospital. Hepatogastroenterology 58:492–496

    PubMed  Google Scholar 

  91. Paugam-Burtz C, Janny S, Delefosse D, Dahmani S, Dondero F, Mantz J, Belghiti J (2009) Prospective validation of the “fifty-fifty” criteria as an early and accurate predictor of death after liver resection in intensive care unit patients. Ann Surg 249:124–128

    Article  PubMed  Google Scholar 

  92. Mullen JT, Ribero D, Reddy SK et al (2007) Hepatic insufficiency and mortality in 1,059 noncirrhotic patients undergoing major hepatectomy. J Am Coll Surg 204:854–862

    Article  PubMed  Google Scholar 

  93. Balzan S, Belghiti J, Farges O et al (2005) The “50–50 criteria” on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg 242:824–828

    Article  PubMed  Google Scholar 

  94. Shirabe K, Takenaka K, Yamatomto K et al (1997) Impaired systemic immunity and frequent infection in patients with Candida antigen after hepatectomy. Hepatogastroenterology 44:199–204

    PubMed  CAS  Google Scholar 

  95. Adani GL, Baccarani U, Risaliti A et al (2007) Percutaneous transhepatic portography for the treatment of early portal vein thrombosis after surgery. Cardiovasc Intervent Radiol 30:1222–1226

    Article  PubMed  Google Scholar 

  96. Chen LP, Li C, Wang C, Wen TF, Yan LN, Li B (2012) Risk factors of ascites after hepatectomy for patients with hepatocellular carcinoma and hepatitis B virus-associated cirrhosis. Hepatogastroenterology 59(113):292–295

    Article  PubMed  CAS  Google Scholar 

  97. Rahbari NN, Garden OJ, Padbury R, Maddern G, Koch M, Hugh TJ, Fan ST, Nimura Y, Figueras J, Vauthey JN, Rees M, Adam R, Dematteo RP, Greig P, Usatoff V, Banting S, Nagino M, Capussotti L, Yokoyama Y, Brooke-Smith M, Crawford M, Christophi C, Makuuchi M, Büchler MW, Weitz J (2004) Post-hepatectomy haemorrhage: a definition and grading by the International Study Group of Liver Surgery (ISGLS). HPB (Oxford) 13:528–535

    Article  Google Scholar 

  98. Ikai I, Itai Y, Okita K, Omata M, Kojiro M, Kobayashi K et al (2004) Report of the 15th follow-up survey of primary liver cancer. Hepatol Res 28:21–29

    Article  PubMed  Google Scholar 

  99. Cha CH, Ruo L, Fong Y, Jarnagin WR, Shia J, Blumgart LH et al (2003) Resection of hepatocellular carcinoma in patients otherwise eligible for transplantation. Ann Surg 238:315–321

    PubMed  Google Scholar 

  100. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S et al (2003) Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 38:200–207

    Article  PubMed  Google Scholar 

  101. Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, Gupta S, Moore J, Wrobel MJ, Lerner J, Reich M, Chan JA, Glickman JN, Ikeda K, Hashimoto M, Watanabe G, Daidone MG, Roayaie S, Schwartz M, Thung S, Salvesen HB, Gabriel S, Mazzaferro V, Bruix J, Friedman SL, Kumada H, Llovet JM, Golub TR (2008) Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med 359:1995–2004

    Article  PubMed  CAS  Google Scholar 

  102. Subramanian J, Simon R (2010) What should physicians look for in evaluating prognostic gene-expression signatures? Nat Rev Clin Oncol 7:327–334

    Article  PubMed  Google Scholar 

  103. Zhou WP, Lai EC, Li AJ, Fu SY, Zhou JP, Pan ZY, Lau WY, Wu MC (2009) A prospective, randomized, controlled trial of preoperative transarterial chemoembolization for resectable large hepatocellular carcinoma. Ann Surg 249:195–202

    Article  PubMed  Google Scholar 

  104. Lau WY, Leung TW, Ho SK, Chan M, Machin D, Lau J, Chan AT, Yeo W, Mok TS, Yu SC, Leung NW, Johnson PJ (1999) Adjuvant intra-arterial iodine-131-labelled lipiodol for resectable hepatocellular carcinoma: a prospective randomised trial. Lancet 353:797–801

    Article  PubMed  CAS  Google Scholar 

  105. Takayama T, Sekine T, Makuuchi M, Yamasaki S, Kosuge T, Yamamoto J, Shimada K, Sakamoto M, Hirohashi S, Ohashi Y, Kakizoe T (2000) Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet 356:802–807

    Article  PubMed  CAS  Google Scholar 

  106. Muto Y, Moriwaki H, Ninomiya M, Adachi S, Saito A, Takasaki KT, Tanaka T, Tsurumi K, Okuno M, Tomita E, Nakamura T, Kojima T (1996) Prevention of second primary tumors by an acyclic retinoid, polyprenoic acid, in patients with hepatocellular carcinoma. Hepatoma Prevention Study Group. N Engl J Med 334:1561–1567

    Article  PubMed  CAS  Google Scholar 

  107. Breitenstein S, Dimitroulis D, Petrowsky H, Puhan MA, Müllhaupt B, Clavien PA (2009) Systematic review and meta-analysis of interferon after curative treatment of hepatocellular carcinoma in patients with viral hepatitis. Br J Surg 96:975–981

    Article  PubMed  CAS  Google Scholar 

  108. Miyake Y, Takaki A, Iwasaki Y, Yamamoto K (2010) Meta-analysis: interferon-alpha prevents the recurrence after curative treatment of hepatitis C virus-related hepatocellular carcinoma. J Viral Hepat 17:287–292

    Article  PubMed  CAS  Google Scholar 

  109. Shen YC, Hsu C, Chen LT, Cheng CC, Hu FC, Cheng AL (2010) Adjuvant interferon therapy after curative therapy for hepatocellular carcinoma (HCC): a meta-regression approach. J Hepatol 52:889–894

    Article  PubMed  CAS  Google Scholar 

  110. Lau WY (2002) Management of hepatocellular carcinoma. J R Coll Surg Edinb 47:389–399

    PubMed  CAS  Google Scholar 

  111. Poon RT, Fan ST, O’Suilleabhain CB, Wong J (2002) Aggressive management of patients with extrahepatic and intrahepatic recurrences of hepatocellular carcinoma by combined resection and locoregional therapy. J Am Coll Surg 195:311–318

    Article  PubMed  Google Scholar 

  112. Minagawa M, Makuuchi M, Takayama T, Kokudo N (2003) Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg 238:703–710

    Article  PubMed  Google Scholar 

  113. Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022

    Article  PubMed  Google Scholar 

  114. Clavien PA, Lesurtel M, Bossuyt PM, Gores GJ, Langer B, Perrier A, on behalf of the OLT for HCC Consensus Group (2012) Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol 13:e11–e22

    Article  PubMed  Google Scholar 

  115. Germani G, Gurusamy K, Garcovich M, Toso C, Fede G, Hemming A, Suh KS, Weber A, Burroughs AK (2011) Which matters most: number of tumors, size of the largest tumor, or total tumor volume? Liver Transpl 17(Suppl 2):S58–66

    Article  PubMed  Google Scholar 

  116. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F et al (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334:693–699

    Article  PubMed  CAS  Google Scholar 

  117. Mazzaferro V, Bhoori S, Sposito C, Bongini M, Langer M, Miceli R, Mariani L (2011) Milan criteria in liver transplantation for hepatocellular carcinoma: an evidence-based analysis of 15 years of experience. Liver Transpl 17:S44–57

    Article  PubMed  Google Scholar 

  118. Yao FY, Xiao L, Bass NM et al (2007) Liver transplantation for hepatocellular carcinoma: validation of the UCSF-expanded criteria based on preoperative imaging. Am J Transplant 7:2587–2596

    Article  PubMed  CAS  Google Scholar 

  119. Clavien PA, Petrowsky H, DeOliveira ML et al (2007) Strategies for safer liver surgery and partial liver transplantation. N Engl J Med 356:1545–1559

    Article  PubMed  Google Scholar 

  120. Molmenti EP, Klintmalm GB (2002) Liver transplantation in association with hepatocellular carcinoma: an update of the International tumor registry. Liver Transpl 9:736–748

    Article  Google Scholar 

  121. Leung JY, Zhu AX, Gordon FD, Pratt DS, Mithoefer A, Garrigan K et al (2004) Liver transplantation outcomes for early stage hepatocellular carcinoma: results of a multicenter study. Liver Transpl 10:1343–1354

    Article  PubMed  Google Scholar 

  122. Todo S, Furukawa H, on behalf of the Japanese study group on organ transplantation (2004) Living donor liver transplantation for adult patients with hepatocellular carcinoma: experience in Japan. Ann Surg 240:451–461

    Article  PubMed  Google Scholar 

  123. Hwang S, Lee SG, Joh KW, Suh KS, Kim DG (2005) Liver transplantation for adult patients with hepatocellular carcinoma in Korea: comparison between cadaveric donor and living donor liver transplantations. Liver Transpl 11:1265–1272

    Article  PubMed  Google Scholar 

  124. Zavaglia C, De Carlis L, Alberti AB, Minola E, Belli LS, Slim AO et al (2005) Predictors for long-term survival after transplantation for hepatocellular carcinoma. Am J Gastroentreol 100:2708–2716

    Article  Google Scholar 

  125. Duffy JP, Vardanian A, Benjamin E et al (2007) Liver transplantation criteria for hepatocellular carcinoma should be expanded: a 22-year experience with 467 patients at UCLA. Ann Surg 246:502–509

    Article  PubMed  Google Scholar 

  126. Mazzaferro V, Llovet JM, Miceli R et al (2009) Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol 10:35–43

    Article  PubMed  Google Scholar 

  127. Vibert E, Azoulay D, Hoti E et al (2010) Progression of alphafetoprotein before liver transplantation for hepatocellular carcinoma in cirrhotic patients: a critical factor. Am J Transplant 10:129–137

    Article  PubMed  CAS  Google Scholar 

  128. Sandhu L, Sandroussi C, Guba M, et al (2011) Live donor versus deceased donor liver transplantation for hepatocellular carcinoma: comparable survival and recurrence. Liver Transpl (in press)

  129. Axelrod DA, Guidinger MK, Finlayson S et al (2008) Rates of solid-organ wait-listing, transplantation, and survival among residents of rural and urban areas. JAMA 299:202–207

    Article  PubMed  CAS  Google Scholar 

  130. Llovet JM, Fuster J, Bruix J (1999) Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology 30:1434–1440

    Article  PubMed  CAS  Google Scholar 

  131. Ratcliffe J, Young T, Buxton M et al (2001) A simulation modelling approach to evaluating alternative policies for the management of the waiting list for liver transplantation. Health Care Manag Sci 4:117–124

    Article  PubMed  CAS  Google Scholar 

  132. Foxton MR, Al-Freah MA, Portal AJ et al (2010) Increased model for end-stage liver disease score at the time of liver transplant results in prolonged hospitalization and overall intensive care unit costs. Liver Transpl 16:668–677

    PubMed  Google Scholar 

  133. Saab S, Wang V, Ibrahim AB, Durazo F, Han S, Farmer DG et al (2003) MELD score predicts 1-year patient survival post orthotopic liver transplantation. Liver Transpl 9:473–476

    Article  PubMed  Google Scholar 

  134. Sarasin FP, Majno PE, Llovet JM, Bruix J, Mentha G, Hadengue A (2001) Living donor liver transplantation for early hepatocellular carcinoma: a life-expectancy and cost-effectiveness perspective. Hepatology 33:1073–1079

    Article  PubMed  CAS  Google Scholar 

  135. Strong RW (1999) Whither living donor liver transplantation? Liver Transpl Surg 5:536–538

    Article  PubMed  CAS  Google Scholar 

  136. Cherqui D, Laurent A, Mocellin N, Tayar C, Luciani A, Nhieu V et al (2009) Liver resection for transplantable hepatocellular carcinoma: long-term survival and role of secondary liver transplantation. Ann Surg 250:738–746

    Article  PubMed  Google Scholar 

  137. Poon RT, Fan ST, Lo CM, Liu CL, Wong J (2007) Difference in tumor invasiveness in cirrhotic patients with hepatocellular carcinoma fulfilling the Milan criteria treated by resection and transplantation: impact on long-term survival. Ann Surg 245:51–58

    Article  PubMed  Google Scholar 

  138. Majno PE, Sarasin FP, Mentha G, Hadengue A (2000) Primary liver resection and salvage transplantation or primary liver transplantation in patients with single, small hepatocellular carcinoma and preserved liver function: an outcome-oriented decision analysis. Hepatology 31:899–906

    Article  PubMed  CAS  Google Scholar 

  139. Del Gaudio M, Ercolani G, Ravaioli M, Cescon M, Lauro A, VCivarelli M et al (2008) Liver transplantation for recurrent hepatocellular carcinoma on cirrhosis after liver resection: University of Bologna experience. Am J Transplant 8:1177–1185

    Article  PubMed  Google Scholar 

  140. Belghiti J, Carr BI, Greig PD, Lencioni R, Poon RT (2008) Treatment before liver transplantation for HCC. Ann Surg Oncol 15:993–1000

    Article  PubMed  CAS  Google Scholar 

  141. Sala M, Fuster J, Llovet JM, Navasa M, Soli M, Varela M et al (2004) High pathological risk of recurrence after surgical resection for hepatocellular carcinoma: an indication for salvage liver transplantation. Liver Transpl 10:1294–1300

    Article  PubMed  Google Scholar 

  142. Sapisochin G, Fidelman N, Roberts JP, Yao FY (2011) Mixed hepatocellular cholangiocarcinoma and intrahepatic choangiocarcinoma in patients undergoing transplantation for hepatocellular carcinoma. Liver Transpl 17:934–942

    Article  PubMed  Google Scholar 

  143. Hoshida Y (2009) Risk of recurrence in hepatitis B-related hepatocellular carcinoma: impact of viral load in late recurrence. J Hepatol 51:842–844

    Article  PubMed  Google Scholar 

  144. Saneto H, Kobayashi M, Kawamura Y, Yatsuji H, Sezaki H, Hosaka T et al (2008) Clinicopathological features, background liver disease, and survival analysis of HCV-positive patients with hepatocellular carcinoma: differences between young and elderly patients. J Gastroenterol 43:975–981

    Article  PubMed  CAS  Google Scholar 

  145. Tsuchiya M, Parker JS, Kono H, Matsuda M, Fuji H, Rusyn I (2010) Gene expression in nontumoral liver tissue and recurrence-free survival in hepatitis C virus-positive hepatocellular carcinoma. Mol Cancer 9:74

    Article  PubMed  CAS  Google Scholar 

  146. Dienstag JL, Ghany MG, Morgan TR, Di Biscegli AM, Bonkovsky HL, Kim H-Y, for the HALT-C Trial Group (2011) A prospective study of the rate of progression in compensated, histologically advanced chronic hepatitis C (HEP-10-2210). Hepatology 54:396–405

    Article  PubMed  Google Scholar 

  147. Berenguer M, Palau A, Aguilera V, Benlloch S, Aguilera V, Prieto M et al (2008) Clinical benefits of antiviral therapy in patients with recurrent hepatitis C following liver transplantation. Am J Transplant 8:679–687

    Article  PubMed  CAS  Google Scholar 

  148. Carrio’n JA, Navasa M, Garcı’a-Retortillo M, Garcia-Pagan JC, Crespo G, Briguera M et al (2007) Efficacy of antiviral therapy on hepatitis C recurrence after liver transplantation: a randomized controlled study. Gastroenterology 132:1746–1756

    Article  CAS  Google Scholar 

  149. Chirica M, Durand F, Sommacale D et al (2004) Long-term outcome after resection for small HCC in patients with hepatitis C virus infection: arguments for a strategy of resection as a bridge to transplantation rather that salvage transplantation [Abstract]. Hepatology 40(Suppl S4):A162

    Google Scholar 

  150. Cucchetti A, Cescon M, Ercolani G, Morelli MC, Del Gaudio M, Zanello M et al (2011) Comparison between observed survival after resection of transplantable hepatocellular carcinoma and predicted survival after listing through a Markov model simulation. Transpl Int 24:787–796

    Article  PubMed  Google Scholar 

  151. Pomfret EA, Washburn K, Wald C, Nalesnik MA, Douglas D, Russo M et al (2010) Report of a national conference on liver allocation in patients with hepatocellular carcinoma in the United States. Liver Transpl 16:262–278

    Article  PubMed  Google Scholar 

Download references

Conflicts of interest

None

Author information

Authors and Affiliations

  1. Beaujon Hospital, Assistance Publique Hôpitaux de Paris, Clichy, France, University Denis Diderot-Paris 7, Paris, France

    F. Cauchy, D. Fuks & J. Belghiti

  2. Department of Surgery, Hospital Beaujon, 100 Boulevard du Général Leclerc, 92118, Clichy Cedex, France

    J. Belghiti

Authors
  1. F. Cauchy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. Fuks
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Belghiti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Belghiti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cauchy, F., Fuks, D. & Belghiti, J. HCC: current surgical treatment concepts. Langenbecks Arch Surg 397, 681–695 (2012). https://doi.org/10.1007/s00423-012-0911-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-012-0911-2

Keywords

Search

Navigation