Repeat Curative Intent Liver Surgery is Safe and Effective for Recurrent Colorectal Liver Metastasis: Results from an International Multi-institutional Analysis

  • Mechteld C. de Jong
  • Skye C. Mayo
  • Carlo Pulitano
  • Serena Lanella
  • Dario Ribero
  • Jennifer Strub
  • Catherine Hubert
  • Jean-François Gigot
  • Richard D. Schulick
  • Michael A. Choti
  • Luca Aldrighetti
  • Gilles Mentha
  • Lorenzo Capussotti
  • Timothy M. Pawlik
2009 SSAT Plenary Presentation



Although 5-year survival approaches 55% following resection of colorectal liver metastasis, most patients develop recurrent disease that is often isolated to the liver. Although repeat curative intent surgery (CIS) is increasingly performed for recurrent colorectal liver metastasis, only small series have been reported. We sought to determine safety and efficacy of repeat CIS for recurrent colorectal liver metastasis as well as determine factors predictive of survival in a large multicenter cohort of patients.


Between 1982 and 2008, 1,706 patients who underwent CIS—defined as curative intent hepatic resection/radiofrequency ablation (RFA)—for colorectal liver metastasis were identified from an international multi-institutional database. Two hundred forty-six (14.4%) patients underwent 301 repeat CIS. Data on clinico-pathologic factors, morbidity, and mortality were collected and analyzed.


Following initial CIS, 645 (37.8%) patients had recurrence within the liver. Of these, 246 patients underwent repeat CIS for recurrent disease. The majority had hepatic resection alone as initial therapy (n = 219; 89.0%). A subset of patients underwent third (n = 46) or fourth (n = 9) repeat CIS. Mean interval between surgeries was similar (first → second, 19.1 months; second → third, 21.5 months; third → fourth, 11.3 months; P = 0.20). Extent of hepatic resection decreased with subsequent CIS (≥hemihepatectomy: first CIS, 30.9% versus second CIS, 21.1% versus third/fourth CIS, 16.4%; P = 0.004). RFA was utilized in one quarter of patients undergoing repeat CIS (second CIS, 21.1% versus third/fourth CIS, 25.5%). Mortality and morbidity were similar following second, third, and fourth CIS, respectively (all P > 0.05). Five-year survival was 47.1%, 32.6%, and 23.8% following the first, second, and third CIS, respectively. Presence of extra-hepatic disease was predictive of worse survival (HR = 2.26, P = 0.01).


Repeat CIS for recurrent colorectal liver metastasis can be performed with low morbidity and near-zero mortality. Patients with no extra-hepatic disease are best candidates for repeat CIS. In these patients, repeat CIS can offer the chance of long-term survival.


Colorectal cancer Metastasis Liver Repeat Resection 



  1. 1.
    Howe HL, Wu X, Ries LA, et al. Annual report to the nation on the status of cancer, 1975–2003, featuring cancer among U.S. Hispanic/Latino populations. Cancer 2006;107(8):1711–1742.CrossRefPubMedGoogle Scholar
  2. 2.
    Rudy DR, Zdon MJ. Update on colorectal cancer. Am Fam Physician 2000;61(6):1759–1770. 1773–1774.PubMedGoogle Scholar
  3. 3.
    Jemal A, Murray T, Ward E, et al. Cancer statistics, 2005. CA Cancer J Clin 2005;55(1):10–30.CrossRefPubMedGoogle Scholar
  4. 4.
    Steele G Jr., Ravikumar TS. Resection of hepatic metastases from colorectal cancer. Biologic perspective. Ann Surg 1989;210(2):127–138.CrossRefPubMedGoogle Scholar
  5. 5.
    Cady B, Monson DO, Swinton NW. Survival of patients after colonic resection for carcinoma with simultaneous liver metastases. Surg Gynecol Obstet 1970;131(4):697–700.PubMedGoogle Scholar
  6. 6.
    Blumgart LH, Allison DJ. Resection and embolization in the management of secondary hepatic tumors. World J Surg 1982;6(1):32–45.CrossRefPubMedGoogle Scholar
  7. 7.
    Jatzko G, Wette V, Muller M, et al. Simultaneous resection of colorectal carcinoma and synchronous liver metastases in a district hospital. Int J Colorectal Dis 1991;6(2):111–114.CrossRefPubMedGoogle Scholar
  8. 8.
    Finlay IG, McArdle CS. Occult hepatic metastases in colorectal carcinoma. Br J Surg 1986;73(9):732–735.CrossRefPubMedGoogle Scholar
  9. 9.
    Scheele J, Stang R, Altendorf-Hofmann A, Paul M. Resection of colorectal liver metastases. World J Surg 1995;19(1):59–71.CrossRefPubMedGoogle Scholar
  10. 10.
    Altendorf-Hofmann A, Scheele J. A critical review of the major indicators of prognosis after resection of hepatic metastases from colorectal carcinoma. Surg Oncol Clin N Am 2003;12(1):165–192. xi.CrossRefPubMedGoogle Scholar
  11. 11.
    Scheele J, Stangl R, Altendorf-Hofmann A, Gall FP. Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery 1991;110(1):13–29.PubMedGoogle Scholar
  12. 12.
    Pawlik TM, Schulick RD, Choti MA. Expanding criteria for resectability of colorectal liver metastases. Oncologist 2008;13(1):51–64.CrossRefPubMedGoogle Scholar
  13. 13.
    Pawlik TM, Choti MA. Surgical therapy for colorectal metastases to the liver. J Gastrointest Surg 2007;11(8):1057–1077.CrossRefPubMedGoogle Scholar
  14. 14.
    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(6):818–825. discussion 825–827.CrossRefPubMedGoogle Scholar
  15. 15.
    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(11):1241–1246.CrossRefPubMedGoogle Scholar
  16. 16.
    Choti MA, Sitzmann JV, Tiburi MF, et al. Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg 2002;235(6):759–766.CrossRefPubMedGoogle Scholar
  17. 17.
    Hughes KS, Rosenstein RB, Songhorabodi S, et al. Resection of the liver for colorectal carcinoma metastases. A multi-institutional study of long-term survivors. Dis Colon Rectum 1988;31(1):1–4.CrossRefPubMedGoogle Scholar
  18. 18.
    Fong Y, Fortner J, Sun RL, et al. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 1999;230(3):309–318. discussion 318–321.CrossRefPubMedGoogle Scholar
  19. 19.
    Adson MA, van Heerden JA, Adson MH, et al. Resection of hepatic metastases from colorectal cancer. Arch Surg 1984;119(6):647–651.PubMedGoogle Scholar
  20. 20.
    Gayowski TJ, Iwatsuki S, Madariaga JR, et al. Experience in hepatic resection for metastatic colorectal cancer: analysis of clinical and pathologic risk factors. Surgery 1994;116(4):703–710. discussion 710–711.PubMedGoogle Scholar
  21. 21.
    Jenkins LT, Millikan KW, Bines SD, et al. Hepatic resection for metastatic colorectal cancer. Am Surg 1997;63(7):605–610.PubMedGoogle Scholar
  22. 22.
    Jamison RL, Donohue JH, Nagorney DM, et al. Hepatic resection for metastatic colorectal cancer results in cure for some patients. Arch Surg 1997;132(5):505–510. discussion 511.PubMedGoogle Scholar
  23. 23.
    Pawlik TM, Scoggins CR, Zorzi D, et al. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 2005;241(5):715–722. discussion 722–724.CrossRefPubMedGoogle Scholar
  24. 24.
    Nordlinger B, Quilichini MA, Parc R, et al. Hepatic resection for colorectal liver metastases. Influence on survival of preoperative factors and surgery for recurrences in 80 patients. Ann Surg 1987;205(3):256–263.CrossRefPubMedGoogle Scholar
  25. 25.
    Bozzetti F, Doci R, Bignami P, et al. Patterns of failure following surgical resection of colorectal cancer liver metastases. Rationale for a multimodal approach. Ann Surg 1987;205(3):264–270.CrossRefPubMedGoogle Scholar
  26. 26.
    Ekberg H, Tranberg KG, Andersson R, et al. Pattern of recurrence in liver resection for colorectal secondaries. World J Surg 1987;11(4):541–547.CrossRefPubMedGoogle Scholar
  27. 27.
    Adam R, Bismuth H, Castaing D, et al. Repeat hepatectomy for colorectal liver metastases. Ann Surg 1997;225(1):51–60. discussion 60–62.CrossRefPubMedGoogle Scholar
  28. 28.
    de Jong MC, Pulitano C, Ribero D, Strub J, Mentha G, Schulick RD, Choti MA, Aldrighetti L, Capussotti L, Pawlik TM. Rates and patterns of recurrence following curative intent surgery for colorectal liver metastases: an international multi-institutional analysis of 1669 patients. Ann Surg 2009;250(3):440–448.CrossRefPubMedGoogle Scholar
  29. 29.
    Lange JF, Leese T, Castaing D, Bismuth H. Repeat hepatectomy for recurrent malignant tumors of the liver. Surg Gynecol Obstet 1989;169(2):119–126.PubMedGoogle Scholar
  30. 30.
    Pinson CW, Wright JK, Chapman WC, et al. Repeat hepatic surgery for colorectal cancer metastasis to the liver. Ann Surg 1996;223(6):765–773. discussion 773–776.CrossRefPubMedGoogle Scholar
  31. 31.
    Nishio H, Hamady ZZ, Malik HZ, et al. Outcome following repeat liver resection for colorectal liver metastases. Eur J Surg Oncol 2007;33(6):729–734.PubMedGoogle Scholar
  32. 32.
    Yamamoto J, Kosuge T, Shimada K, et al. Repeat liver resection for recurrent colorectal liver metastases. Am J Surg 1999;178(4):275–281.CrossRefPubMedGoogle Scholar
  33. 33.
    Petrowsky H, Gonen M, Jarnagin W, et al. Second liver resections are safe and effective treatment for recurrent hepatic metastases from colorectal cancer: a bi–institutional analysis. Ann Surg 2002;235(6):863–871.CrossRefPubMedGoogle Scholar
  34. 34.
    Sa Cunha A, Laurent C, Rault A, et al. A second liver resection due to recurrent colorectal liver metastases. Arch Surg 2007;142(12):1144–1149. discussion 1150.CrossRefPubMedGoogle Scholar
  35. 35.
    Nordlinger B, Vaillant JC, Guiguet M, et al. Survival benefit of repeat liver resections for recurrent colorectal metastases: 143 cases. Association Francaise de Chirurgie. J Clin Oncol 1994;12(7):1491–1496.PubMedGoogle Scholar
  36. 36.
    Tuttle TM, Curley SA, Roh MS. Repeat hepatic resection as effective treatment of recurrent colorectal liver metastases. Ann Surg Oncol 1997;4(2):125–130.CrossRefPubMedGoogle Scholar
  37. 37.
    Stone MD, Cady B, Jenkins RL, et al. Surgical therapy for recurrent liver metastases from colorectal cancer. Arch Surg 1990;125(6):718–721. discussion 722.PubMedGoogle Scholar
  38. 38.
    Vaillant JC, Balladur P, Nordlinger B, et al. Repeat liver resection for recurrent colorectal metastases. Br J Surg 1993;80(3):340–344.CrossRefPubMedGoogle Scholar
  39. 39.
    Fong Y, Blumgart LH, Cohen A, et al. Repeat hepatic resections for metastatic colorectal cancer. Ann Surg 1994;220(5):657–662.CrossRefPubMedGoogle Scholar
  40. 40.
    Nagakura S, Shirai Y, Suda T, Hatakeyama K. Multiple repeat resections of intra- and extrahepatic recurrences in patients undergoing initial hepatectomy for colorectal carcinoma metastases. World J Surg 2002;26(2):141–147.CrossRefPubMedGoogle Scholar
  41. 41.
    Brachet D, Lermite E, Rouquette A, et al. Prognostic factors of survival in repeat liver resection for recurrent colorectal metastases: review of sixty-two cases treated at a single institution. Dis Colon Rectum 2009;52(3):475–483.PubMedGoogle Scholar
  42. 42.
    Clavien PA, Emond J, Vauthey JN, et al. Protection of the liver during hepatic surgery. J Gastrointest Surg 2004;8(3):313–327.CrossRefPubMedGoogle Scholar
  43. 43.
    Strasberg SM. For the International Hepato-Pancreato-Biliary Association Terminology Committee Survey. The Brisbane 2000 Terminology of Liver Anatomy and Resections. HPB 2000;2(3):333–339.Google Scholar
  44. 44.
    Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. Am Stat Assoc J 1958;53:457–480.CrossRefGoogle Scholar
  45. 45.
    Fernandez-Trigo V, Shamsa F, Sugarbaker PH. Repeat liver resections from colorectal metastasis. Repeat Hepatic Metastases Registry. Surgery 1995;117(3):296–304.CrossRefPubMedGoogle Scholar
  46. 46.
    Aramaki M, Kawano K, Kai T, et al. Postoperative complications of repeat hepatectomy for liver metastasis from colorectal carcinoma. Hepatogastroenterology 2000;47(32):478–480.PubMedGoogle Scholar
  47. 47.
    Elias D, Lasser P, Hoang JM, et al. Repeat hepatectomy for cancer. Br J Surg 1993;80(12):1557–1562.CrossRefPubMedGoogle Scholar
  48. 48.
    Adam R, Pascal G, Azoulay D, et al. Liver resection for colorectal metastases: the third hepatectomy. Ann Surg 2003;238(6):871–883. discussion 883–884.CrossRefPubMedGoogle Scholar
  49. 49.
    Ishiguro S, Akasu T, Fujimoto Y, et al. Second hepatectomy for recurrent colorectal liver metastasis: analysis of preoperative prognostic factors. Ann Surg Oncol 2006;13(12):1579–1587.CrossRefPubMedGoogle Scholar
  50. 50.
    Pawlik TM, Izzo F, Cohen DS, et al. Combined resection and radiofrequency ablation for advanced hepatic malignancies: results in 172 patients. Ann Surg Oncol 2003;10(9):1059–1069.CrossRefPubMedGoogle Scholar
  51. 51.
    Elias D, De Baere T, Smayra T, et al. Percutaneous radiofrequency thermoablation as an alternative to surgery for treatment of liver tumour recurrence after hepatectomy. Br J Surg 2002;89(6):752–756.CrossRefPubMedGoogle Scholar
  52. 52.
    Tsai S, Pawlik TM. Outcomes of ablation versus resection for colorectal metastases: are we comparing apples to oranges? Ann Surg Oncol 2009;16(9):2422–2428.CrossRefPubMedGoogle Scholar
  53. 53.
    Gleisner AL, Choti MA, Assumpcao L, et al. Colorectal liver metastases: recurrence and survival following hepatic resection, radiofrequency ablation, and combined resection-radiofrequency ablation. Arch Surg 2008;143(12):1204–1212.CrossRefPubMedGoogle Scholar
  54. 54.
    Asiyanbola B, Chang D, Gleisner AL, et al. Operative mortality after hepatic resection: are literature-based rates broadly applicable? J Gastrointest Surg 2008;12(5):842–851.CrossRefPubMedGoogle Scholar
  55. 55.
    Muratore A, Polastri R, Bouzari H, et al. Repeat hepatectomy for colorectal liver metastases: A worthwhile operation? J Surg Oncol 2001;76(2):127–132.CrossRefPubMedGoogle Scholar
  56. 56.
    Pessaux P, Lermite E, Brehant O, et al. Repeat hepatectomy for recurrent colorectal liver metastases. J Surg Oncol 2006;93(1):1–7.CrossRefPubMedGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2009

Authors and Affiliations

  • Mechteld C. de Jong
    • 1
  • Skye C. Mayo
    • 1
  • Carlo Pulitano
    • 2
  • Serena Lanella
    • 3
  • Dario Ribero
    • 3
  • Jennifer Strub
    • 4
  • Catherine Hubert
    • 5
  • Jean-François Gigot
    • 5
  • Richard D. Schulick
    • 1
  • Michael A. Choti
    • 1
  • Luca Aldrighetti
    • 2
  • Gilles Mentha
    • 4
  • Lorenzo Capussotti
    • 3
  • Timothy M. Pawlik
    • 1
  1. 1.Department of SurgeryJohns Hopkins University School of MedicineBaltimoreUSA
  2. 2.Ospedale San RaffaeleMilanItaly
  3. 3.Ospedale Mauriziano Umberto ITurinItaly
  4. 4.Hôpitaux Universitaires de GenèveGenevaSwitzerland
  5. 5.Saint-Luc University Hospital, Université Catholique de LouvainBrusselsBelgium

Personalised recommendations