European Journal of Surgical Oncology
Volume 33 , Pages S42-S51 , December 2007

Bringing unresectable liver disease to resection with curative intent

  • D.A. Wicherts

      Affiliations

    • AP-HP Hôpital Paul Brousse, Centre Hépato-Biliaire, Villejuif F-94804, France
    • Department of Surgery, University Medical Center Utrecht, Utrecht, The Netherlands
  • ,
  • R.J. de Haas

      Affiliations

    • AP-HP Hôpital Paul Brousse, Centre Hépato-Biliaire, Villejuif F-94804, France
    • Department of Surgery, University Medical Center Utrecht, Utrecht, The Netherlands
  • ,
  • R. Adam

      Affiliations

    • AP-HP Hôpital Paul Brousse, Centre Hépato-Biliaire, Villejuif F-94804, France
    • Université Paris-Sud, UMR-S 785, Villejuif F-94804, France
    • Inserm, Unité 785, Villejuif F-94804, France
    • Corresponding Author InformationCorresponding author. AP-HP Hôpital Paul Brousse, Centre Hépato-Biliaire, 12 Avenue Paul Vaillant Couturier, 94804 Villejuif, France. Tel.: +33 1 4559 3049; fax: +33 1 4559 3857.

,Accepted 26 September 2007.

References 

  1. Steele G, Ravikumar TS. Resection of hepatic metastases from colorectal cancer: biologic perspectives. Ann Surg. 1989;210:127–138
  2. Fong Y, Cohen AM, Fortner JG, et al. Liver resection for colorectal metastases. J Clin Oncol. 1997;15:938–946
  3. Scheele J, Altendorf-Hofmann A. Resection of colorectal liver metastases. Langenbecks Arch Surg. 1999;384:313–327
  4. Baden H, Andersen B. Survival of patients with untreated liver metastases from colorectal cancer. Scand J Gastroenterol. 1975;10:221–223
  5. Goslin R, Steele G, Zamcheck N, Mayer R, MacIntyre J. Factors influencing survival in patients with hepatic metastases from adenocarcinoma of the colon or rectum. Dis Colon Rectum. 1982;25:749–754
  6. Wagner JS, Adson MA, Van Heerden JA, Adson MH, Ilstrup DM. The natural history of hepatic metastases from colorectal cancer. A comparison with resective treatment. Ann Surg. 1984;199:502–508
  7. Scheele J, Stangl R, Altendorf-Hofmann A. Hepatic metastases from colorectal carcinoma: impact of surgical resection on the natural history. Br J Surg. 1990;77:1241–1246
  8. Adam R. Chemotherapy and surgery: new perspectives on the treatment of unresectable liver metastases. Ann Oncol. 2003;14(Suppl 2):ii13–ii16
  9. Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230:309–318
  10. Nordlinger B, Guiguet M, Vaillant JC, et al. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Association Française de Chirurgie. Cancer. 1996;77:1254–1262
  11. Minagawa M, Makuuchi M, Torzilli G, et al. Extension of the frontiers of surgical indications in the treatment of liver metastases from colorectal cancer: long-term results. Ann Surg. 2000;231:487–499
  12. Adam R, Avisar E, Ariche A, et al. Five-year survival following hepatic resection after neoadjuvant therapy for nonresectable colorectal. Ann Surg Oncol. 2001;8:347–353
  13. Elias D, Cavalcanti A, Sabourin JC, et al. Resection of liver metastases from colorectal cancer: the real impact of the surgical margin. Eur J Surg Oncol. 1998;24:174–179
  14. Murata S, Moriya Y, Akasu T, Fujita S, Sugihara K. Resection of both hepatic and pulmonary metastases in patients with colorectal carcinoma. Cancer. 1998;83:1086–1093
  15. Bertheault-Cvitkovic F, Jami A, Ithzaki M, et al. Biweekly intensified ambulatory chronomodulated chemotherapy with oxaliplatin, fluorouracil, and leucovorin in patients with metastatic colorectal cancer. J Clin Oncol. 1996;14:2950–2958
  16. de Gramont A, Figer A, Seymour M, et al. Leucovorin and fluorouracil with or without oxaliplatin as first-line treatment in advanced colorectal cancer. J Clin Oncol. 2000;18:2938–2947
  17. Douillard JY, Cunningham D, Roth AD, et al. Irinotecan combined with fluorouracil compared with fluorouracil alone as first-line treatment for metastatic colorectal cancer: a multicentre randomised trial. Lancet. 2000;355:1041–1047
  18. Falcone A, Masi G, Allegrini G, et al. Biweekly chemotherapy with oxaliplatin, irinotecan, infusional Fluorouracil, and leucovorin: a pilot study in patients with metastatic colorectal cancer. J Clin Oncol. 2002;20:4006–4014
  19. Giacchetti S, Perpoint B, Zidani R, et al. Phase III multicenter randomized trial of oxaliplatin added to chronomodulated fluorouracil-leucovorin as first-line treatment of metastatic colorectal cancer. J Clin Oncol. 2000;18:136–147
  20. Köhne CH, van Cutsem E, Wils J, et al. Phase III study of weekly high-dose infusional fluorouracil plus folinic acid with or without irinotecan in patients with metastatic colorectal cancer: European Organisation for Research and Treatment of Cancer Gastrointestinal Group Study 40986. J Clin Oncol. 2005;23:4856–4865
  21. Levi F, Misset JL, Brienza S, et al. A chronopharmacologic phase II clinical trial with 5-fluorouracil, folinic acid, and oxaliplatin using an ambulatory multichannel programmable pump. High antitumor effectiveness against metastatic colorectal cancer. Cancer. 1992;69:893–900
  22. Levi F, Zidani R, Misset JL. Randomised multicentre trial of chronotherapy with oxaliplatin, fluorouracil, and folinic acid in metastatic colorectal cancer. International Organization for Cancer Chronotherapy. Lancet. 1997;350:681–686
  23. Levi F, Zidani R, Brienza S, et al. A multicenter evaluation of intensified, ambulatory, chronomodulated chemotherapy with oxaliplatin, 5-fluorouracil, and leucovorin as initial treatment of patients with metastatic colorectal carcinoma. International Organization for Cancer Chronotherapy. Cancer. 1999;85:2532–2540
  24. Saltz LB, Cox JV, Blanke C, et al. Irinotecan plus fluorouracil and leucovorin for metastatic colorectal cancer. Irinotecan Study Group. N Engl J Med. 2000;343:905–914
  25. Tournigand C, Andre T, Achille E, et al. FOLFIRI followed by FOLFOX6 or the reverse sequence in advanced colorectal cancer: a randomized GERCOR study. J Clin Oncol. 2004;22:229–237
  26. Adam R, Delvart V, Pascal G, et al. Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann Surg. 2004;240:644–657
  27. Giacchetti S, Itzhaki M, Gruia G, et al. Long-term survival of patients with unresectable colorectal cancer liver metastases following infusional chemotherapy with 5-fluorouracil, leucovorin, oxaliplatin and surgery. Ann Oncol. 1999;10:663–669
  28. Folprecht G, Grothey A, Alberts S, Raab HR, Kohne CH. Neoadjuvant treatment of unresectable colorectal liver metastases: correlation between tumour response and resection rates. Ann Oncol. 2005;16:1311–1319
  29. Alberts SR, Horvath WL, Sternfeld WC, et al. Oxaliplatin, fluorouracil, and leucovorin for patients with unresectable liver-only metastases from colorectal cancer: a North Central Cancer Treatment Group phase II study. J Clin Oncol. 2005;23:9243–9249
  30. Bismuth H, Adam R, Levi F, et al. Resection of nonresectable liver metastases from colorectal cancer after neoadjuvant chemotherapy. Ann Surg. 1996;224:509–520
  31. de la Camara J, Rodriguez J, Rotellar F. Triplet therapy with oxaliplatin, irinotecan, 5-fluorouracil and folinic acid within a combined modality approach in patients with liver metastases from colorectal cancer. Proc Am Soc Clin Oncol. 2004;23:[Abstract 3593]
  32. Ho WM, Ma B, Mok T, et al. Liver resection after irinotecan, 5-fluorouracil, and folinic acid for patients with unresectable colorectal liver metastases: a multicenter phase II study by the Cancer Therapeutic Research Group. Med Oncol. 2005;22:303–312
  33. Masi G, Cupini S, Marcucci L, et al. Treatment with 5-fluorouracil/folinic acid, oxaliplatin, and irinotecan enables surgical resection of metastases in patients with initially unresectable metastatic colorectal cancer. Ann Surg Oncol. 2006;13:58–65
  34. Pozzo C, Basso M, Cassano A, et al. Neoadjuvant treatment of unresectable liver disease with irinotecan and 5-fluorouracil plus folinic acid in colorectal cancer patients. Ann Oncol. 2004;15:933–939
  35. Quenet F, Nordlinger B, Rivoire M. Resection of previously unresectable liver metastases from colorectal cancer (LMCRC) after chemotherapy (CT) with CPT-11/L-OHP/LV5FU (Folfirinox): a prospective phase II trial. Proc Am Soc Clin Oncol. 2004;23:[Abstract 3613]
  36. Baselga J. The EGFR as a target for anticancer therapy—focus on cetuximab. Eur J Cancer. 2001;37(Suppl 4):S16–S22
  37. Borner M, Mingrone W, Koeberle D, et al. The impact of cetuximab on the capecitabine plus oxaliplatin (XELOX) combination in first-line treatment of metastatic colorectal cancer (MCC): a randomized phase II trial of the Swiss Group for Clinical Cancer Research (SAKK). Journal of Clinical Oncology 2006 ASCO Annual Meeting Proceedings Part I; 24:Abstract 3551.
  38. Chung KY, Shia J, Kemeny NE, et al. Cetuximab shows activity in colorectal cancer patients with tumors that do not express the epidermal growth factor receptor by immunohistochemistry. J Clin Oncol. 2005;23:1803–1810
  39. Cunningham D, Humblet Y, Siena S, et al. Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N Engl J Med. 2004;351:337–345
  40. Díaz Rubio E, Tabernero J, van Cutsem E, et al. Cetuximab in combination with oxaliplatin/5-fluorouracil (5-FU)/folinic acid (FA) (FOLFOX-4) in the first-line treatment of patients with epidermal growth factor receptor (EGFR)-expressing metastatic colorectal cancer: an international phase II study. Journal of Clinical Oncology 2005 ASCO Annual Meeting Proceedings Part I; 23:Abstract 3535.
  41. Folprecht G, Lutz MP, Schoffski P, et al. Cetuximab and irinotecan/5-fluorouracil/folinic acid is a safe combination for the first-line treatment of patients with epidermal growth factor receptor expressing metastatic colorectal carcinoma. Ann Oncol. 2006;17:450–456
  42. Gebbia V, Del Prete S, Borsellino N, et al. Efficacy and safety of cetuximab/irinotecan in chemotherapy-refractory metastatic colorectal adenocarcinomas: a clinical practice setting, multicenter experience. Clin Colorectal Cancer. 2006;5:422–428
  43. Heinemann V, Fischer Von Weikersthal L, Moosmann N, et al. Cetuximab+capecitabine+irinotecan (CCI) versus cetuximab+capecitabine+oxaliplatin (CCO) as first line therapy for patients with metastatic colorectal cancer (CRC): preliminary results of a randomized phase II trial of the AIO CRC Study Group. Journal of Clinical Oncology 2006 ASCO Annual Meeting Proceedings Part I; 24:Abstract 3550.
  44. Lenz HJ, van Cutsem E, Khambata-Ford S, et al. Multicenter phase II and translational study of cetuximab in metastatic colorectal carcinoma refractory to irinotecan, oxaliplatin, and fluoropyrimidines. J Clin Oncol. 2006;24:4914–4921
  45. Rougier P, Raoul J-L, van Laethem J-L, et al. Cetuximab+FOLFIRI as first-line treatment for metastatic colorectal CA. Journal of Clinical Oncology 2004 ASCO Annual Meeting Proceedings; 22:Abstract 3513.
  46. Saltz LB, Meropol NJ, Loehrer PJ, Needle MN, Kopit J, Mayer RJ. Phase II trial of cetuximab in patients with refractory colorectal cancer that expresses the epidermal growth factor receptor. J Clin Oncol. 2004;22:1201–1208
  47. Souglakos J, Kalykaki A, Vamvakas L, et al. Phase II trial of capecitabine and oxaliplatin (CAPOX) plus cetuximab in patients with metastatic colorectal cancer who progressed after oxaliplatin-based chemotherapy. Ann Oncol. 2007;18:305–310
  48. Vincenzi B, Santini D, Rabitti C, et al. Cetuximab and irinotecan as third-line therapy in advanced colorectal cancer patients: a single centre phase II trial. Br J Cancer. 2006;94:792–797
  49. Wilke H, Glynne-Jones R, Thaler J, et al. MABEL – A large multinational study of cetuximab plus irinotecan in irinotecan resistant metastatic colorectal cancer. Journal of Clinical Oncology 2006 ASCO Annual Meeting Proceedings Part I; 24:Abstract 3549.
  50. Adam R, Aloia T, Lévi F, et al. Hepatic resection after rescue cetuximab treatment for colorectal liver metastases previously refractory to conventional systemic therapy. J Clin Oncol. 2007;25:4593–4602
  51. Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004;350:2335–2342
  52. Kopetz S, Abbruzzese JL, Eng C, et al. Preliminary results from a phase II study of infusional 5-FU, leucovorin, and irinotecan (FOLFIRI) plus bevacizumab as first-line treatment for metastatic colorectal cancer (mCRC). Journal of Clinical Oncology 2006 ASCO Annual Meeting Proceedings Part I; 24:Abstract 3579.
  53. Saltz LB, Lenz H, Hochster H, et al. Randomized phase II trial of cetuximab/bevacizumab/irinotecan (CBI) versus cetuximab/bevacizumab (CB) in irinotecan-refractory colorectal cancer. Journal of Clinical Oncology 2005 ASCO Annual Meeting Proceedings Part I; 23:Abstract 3508.
  54. Detroz B, Sugarbaker PH, Knol JA, Petrelli N, Hughes K. Causes of death in patients undergoing liver surgery. In:  Sugarbaker PH editors. Hepatobiliary cancer. Boston: Kluwer academic publishers; 1994;p. 241–257
  55. Kubota K, Makuuchi M, Kusaka K, et al. Measurement of liver volume and hepatic functional reserve as a guide to decision-making in resectional surgery for hepatic tumors. Hepatology. 1997;26:1176–1181
  56. Vauthey JN, Chaoui A, Do KA, et al. Standardized measurement of the future liver remnant prior to extended liver resection: methodology and clinical associations. Surgery. 2000;127:512–519
  57. Azoulay D, Castaing D, Smail A, et al. Resection of nonresectable liver metastases from colorectal cancer after percutaneous portal vein embolization. Ann Surg. 2000;231:480–486
  58. Azoulay D, Raccuia JS, Castaing D, Bismuth H. Right portal vein embolization in preparation for major hepatic resection. J Am Coll Surg. 1995;181:266–269
  59. Makuuchi M, Thai BL, Takayasu K, et al. Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report. Surgery. 1990;107:521–527
  60. Abdalla EK, Hicks ME, Vauthey JN. Portal vein embolization: rationale, technique and future prospects. Br J Surg. 2001;88:165–175
  61. Elias D, De Baere T, Roche A, Ducreux M, Leclere J, Lasser P. During liver regeneration following right portal embolization the growth rate of liver metastases is more rapid than that of the liver parenchyma. Br J Surg. 1999;86:784–788
  62. Adam R, Laurent A, Azoulay D, Castaing D, Bismuth H. Two-stage hepatectomy: a planned strategy to treat irresectable liver tumors. Ann Surg. 2000;232:777–785
  63. Elias D, Ouellet JF, De Baere T, Lasser P, Roche A. Preoperative selective portal vein embolization before hepatectomy for liver metastases: long-term results and impact on survival. Surgery. 2002;131:294–299
  64. Jaeck D, Oussoultzoglou E, Rosso E, Greget M, Weber JC, Bachellier P. A two-stage hepatectomy procedure combined with portal vein embolization to achieve curative resection for initially unresectable multiple and bilobar colorectal liver metastases. Ann Surg. 2004;240:1037–1049
  65. Lindner P, Cahlin C, Friman S, et al. Extended right-sided liver resection for colorectal liver metastases—impact of percutaneous portal venous embolisation. Eur J Surg Oncol. 2006;32:292–296
  66. Togo S, Nagano Y, Masui H, et al. Two-stage hepatectomy for multiple bilobular liver metastases from colorectal cancer. Hepatogastroenterology. 2005;52:913–919
  67. Buscarini L, Rossi S. Technology for radiofrequency thermal ablation of liver tumors. Semin Laparosc Surg. 1997;4:96–101
  68. McCarty TM, Kuhn JA. Cryotherapy for liver tumors. Oncology. 1998;12:979–987
  69. Abdalla EK, Vauthey JN, Ellis LM, et al. Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg. 2004;239:818–825
  70. Pawlik TM, Izzo F, Cohen DS, Morris JS, Curley SA. Combined resection and radiofrequency ablation for advanced hepatic malignancies: results in 172 patients. Ann Surg Oncol. 2003;10:1059–1069
  71. Adam R, Akpinar E, Johann M, Kunstlinger F, Majno P, Bismuth H. Place of cryosurgery in the treatment of malignant liver tumors. Ann Surg. 1997;225:39–50
  72. Brooks AJ, Wang F, Alfredson M, Yan TD, Morris DL. Synchronous liver resection and cryotherapy for colorectal metastases: survival analysis. Surgeon. 2005;3:265–268
  73. Weaver ML, Atkinson D, Zemel R. Hepatic cryosurgery in treating colorectal metastases. Cancer. 1995;76:210–214
  74. Vogl TJ, Straub R, Zangos S, Mack MG, Eichler K. MR-guided laser-induced thermotherapy (LITT) of liver tumours: experimental and clinical data. Int J Hyperthermia. 2004;20:713–724
  75. Vogl TJ, Straub R, Eichler K, Sollner O, Mack MG. Colorectal carcinoma metastases in liver: laser-induced interstitial thermotherapy—local tumor control rate and survival data. Radiology. 2004;230:450–458
  76. Heaney JP, Stanton WK, Halbert DS, Seidel J, Vice T. An improved technic for vascular isolation of the liver: experimental study and case reports. Ann Surg. 1966;163:237–241
  77. Azoulay D, Eshkenazy R, Andreani P, et al. In situ hypothermic perfusion of the liver versus standard total vascular exclusion for complex liver resection. Ann Surg. 2005;241:277–285
  78. Belghiti J, Noun R, Zante E, Ballet T, Sauvanet A. Portal triad clamping or hepatic vascular exclusion for major liver resection. A controlled study. Ann Surg. 1996;224:155–161
  79. Berney T, Mentha G, Morel P. Total vascular exclusion of the liver for the resection of lesions in contact with the vena cava or the hepatic veins. Br J Surg. 1998;85:485–488
  80. Bismuth H, Castaing D, Garden OJ. Major hepatic resection under total vascular exclusion. Ann Surg. 1989;210:13–19
  81. Cherqui D, Malassagne B, Colau PI, Brunetti F, Rotman N, Fagniez PL. Hepatic vascular exclusion with preservation of the caval flow for liver resections. Ann Surg. 1999;230:24–30
  82. Delva E, Camus Y, Nordlinger B, et al. Vascular occlusions for liver resections. Operative management and tolerance to hepatic ischemia: 142 cases. Ann Surg. 1989;209:211–218
  83. Emre S, Schwartz ME, Katz E, Miller CM. Liver resection under total vascular isolation. Variations on a theme. Ann Surg. 1993;217:15–19
  84. Evans PM, Vogt DP, Mayes JT, Henderson JM, Walsh RM. Liver resection using total vascular exclusion. Surgery. 1998;124:807–813
  85. Habib N, Zografos G, Dalla SG, Greco L, Bean A. Liver resection with total vascular exclusion for malignant tumours. Br J Surg. 1994;81:1181–1184
  86. Shaw BW, Martin DJ, Marquez JM, et al. Venous bypass in clinical liver transplantation. Ann Surg. 1984;200:524–534
  87. Huguet C, Gavelli A, Chieco PA, et al. Liver ischemia for hepatic resection: where is the limit?. Surgery. 1992;111:251–259
  88. Fortner JG, Shiu MH, Kinne DW, et al. Major hepatic resection using vascular isolation and hypothermic perfusion. Ann Surg. 1974;180:644–652
  89. Azoulay D, Andreani P, Maggi U, et al. Combined liver resection and reconstruction of the supra-renal vena cava: the Paul Brousse experience. Ann Surg. 2006;244:80–88
  90. Arii S, Teramoto K, Kawamura T, et al. Significance of hepatic resection combined with inferior vena cava resection and its reconstruction with expanded polytetrafluoroethylene for treatment of liver tumors. J Am Coll Surg. 2003;196:243–249
  91. Hemming AW, Reed AI, Langham MR, Fujita S, Howard RJ. Combined resection of the liver and inferior vena cava for hepatic malignancy. Ann Surg. 2004;239:712–719
  92. Madariaga JR, Fung J, Gutierrez J, Bueno J, Iwatsuki S. Liver resection combined with excision of vena cava. J Am Coll Surg. 2000;191:244–250
  93. Miyazaki M, Ito H, Nakagawa K, et al. Aggressive surgical resection for hepatic metastases involving the inferior vena cava. Am J Surg. 1999;177:294–298
  94. Adam R, Pascal G, Castaing D, et al. Tumor progression while on chemotherapy: a contraindication to liver resection for multiple colorectal metastases?. Ann Surg. 2004;240:1052–1061
  95. Benoist S, Brouquet A, Penna C, et al. Complete response of colorectal liver metastases after chemotherapy: does it mean cure?. J Clin Oncol. 2006;24:3939–3945
  96. Aloia T, Sebagh M, Plasse M, et al. Liver histology and surgical outcomes after preoperative chemotherapy with fluorouracil plus oxaliplatin in colorectal cancer liver metastases. J Clin Oncol. 2006;24:4983–4990
  97. Karoui M, Penna C, Amin-Hashem M, et al. Influence of preoperative chemotherapy on the risk of major hepatectomy for colorectal liver metastases. Ann Surg. 2006;243:1–7
  98. Vauthey JN, Pawlik TM, Ribero D, et al. Chemotherapy regimen predicts steatohepatitis and an increase in 90-day mortality after surgery for hepatic colorectal metastases. J Clin Oncol. 2006;24:2065–2072

PII: S0748-7983(07)00546-X

doi: 10.1016/j.ejso.2007.09.017

European Journal of Surgical Oncology
Volume 33 , Pages S42-S51 , December 2007