The predictors and oncological outcomes of repeat surgery for recurrence after hepatectomy for colorectal liver metastases

  • Katsunori Imai
  • Yo-ichi Yamashita
  • Yuji Miyamoto
  • Shigeki Nakagawa
  • Hirohisa Okabe
  • Daisuke Hashimoto
  • Akira Chikamoto
  • Hideo Baba
Original Article



Although recurrence after hepatectomy for colorectal liver metastases (CRLM) is common, the optimal treatment strategy remains unclear. The aims of this study were to clarify the impact of repeat surgery and identify the predictive factors for repeat surgery.


Among the 170 patients who underwent potentially curative surgery for CRLM, 113 developed recurrence. The predictive factors for the performance of repeat surgery were identified and a predictive model was constructed.


The patterns of recurrence were as follows; single site [n = 100 (liver, n = 61; lung, n = 22; other, n = 17)], multiple site (n = 13). Repeat surgery was performed in 54 patients (47.8%) including re-hepatectomy (n = 25), radiofrequency ablation (n = 12), and resection of the extrahepatic recurrent disease (n = 17), and their overall survival (OS) was significantly better than that of those who could not (5-year OS 60.7 vs 19.5%, P < 0.0001). A multivariate analysis revealed that a primary N-negative status [relative risk (RR) 2.93, P = 0.017], indocyanine retention rate at 15 min ≤ 10% before hepatectomy (RR 2.49, P = 0.04), and carcinoembryonic antigen ≤ 5 ng/mL before hepatectomy (RR 2.96, P = 0.017) independently predicted the performance of repeat surgery. For patients who did not present any factors, the probability of repeat surgery was 19.6%. The addition of each subsequent factor increased the probability to 41.9, 67.8, and 84.0% (for 1, 2, and 3 factors, respectively).


Repeat surgery for not only intrahepatic but also extrahepatic recurrence is crucial for prolonging the survival of CRLM patients. The proposed model may help to predict the possibility of repeat surgery and provide optimal individualized treatment.


Colorectal liver metastases Hepatectomy Repeat surgery Predictive model 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

10147_2018_1273_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 28 kb)


  1. 1.
    Jemal A, Bray F, Center MM et al (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90. CrossRefPubMedGoogle Scholar
  2. 2.
    House MG, Ito H, Gonen M et al (2010) Survival after hepatic resection for metastatic colorectal cancer: trends in outcomes for 1,600 patients during two decades at a single institution. J Am Coll Surg 210(5):744–752. CrossRefPubMedGoogle Scholar
  3. 3.
    Manfredi S, Lepage C, Hatem C et al (2006) Epidemiology and management of liver metastases from colorectal cancer. Ann Surg 244(2):254–259. CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Leporrier J, Maurel J, Chiche L et al (2006) A population-based study of the incidence, management and prognosis of hepatic metastases from colorectal cancer. Br J Surg 93(4):465–474. CrossRefPubMedGoogle Scholar
  5. 5.
    Tomlinson JS, Jarnagin WR, DeMatteo RP et al (2007) Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol 25(29):4575–4580. CrossRefPubMedGoogle Scholar
  6. 6.
    de Jong MC, Pulitano C, Ribero D et al (2009) Rates and patterns of recurrence following curative intent surgery for colorectal liver metastasis: an international multi-institutional analysis of 1669 patients. Ann Surg 250(3):440–448. PubMedGoogle Scholar
  7. 7.
    Mise Y, Imamura H, Hashimoto T et al (2010) Cohort study of the survival benefit of resection for recurrent hepatic and/or pulmonary metastases after primary hepatectomy for colorectal metastases. Ann Surg 251(5):902–909. CrossRefPubMedGoogle Scholar
  8. 8.
    Butte JM, Gonen M, Allen PJ et al (2015) Recurrence after partial hepatectomy for metastatic colorectal cancer: potentially curative role of salvage repeat resection. Ann Surg Oncol 22(8):2761–2771. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Kulik U, Bektas H, Klempnauer J et al (2013) Repeat liver resection for colorectal metastases. Br J Surg 100(7):926–932. CrossRefPubMedGoogle Scholar
  10. 10.
    Andreou A, Brouquet A, Abdalla EK et al (2011) Repeat hepatectomy for recurrent colorectal liver metastases is associated with a high survival rate. HPB (Oxford) 13(11):774–782. CrossRefPubMedCentralGoogle Scholar
  11. 11.
    Wicherts DA, de Haas RJ, Salloum C et al (2013) Repeat hepatectomy for recurrent colorectal metastases. Br J Surg 100(6):808–818. CrossRefPubMedGoogle Scholar
  12. 12.
    Oba M, Hasegawa K, Shindoh J et al (2016) Survival benefit of repeat resection of successive recurrences after the initial hepatic resection for colorectal liver metastases. Surgery 159(2):632–640. CrossRefPubMedGoogle Scholar
  13. 13.
    Saiura A, Yamamoto J, Koga R et al (2014) Favorable outcome after repeat resection for colorectal liver metastases. Ann Surg Oncol 21(13):4293–4299. CrossRefPubMedGoogle Scholar
  14. 14.
    Imai K, Allard MA, Benitez CC et al (2016) Early recurrence after hepatectomy for colorectal liver metastases: what optimal definition and what predictive factors? Oncologist 21(7):887–894. CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Beppu T, Miyamoto Y, Sakamoto Y et al (2014) Chemotherapy and targeted therapy for patients with initially unresectable colorectal liver metastases, focusing on conversion hepatectomy and long-term survival. Ann Surg Oncol 21(Suppl 3):S405–S413. CrossRefPubMedGoogle Scholar
  16. 16.
    Therasse P, Arbuck SG, Eisenhauer EA et al (2000) New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 92(3):205–216CrossRefPubMedGoogle Scholar
  17. 17.
    Bogaerts J, Ford R, Sargent D et al (2009) Individual patient data analysis to assess modifications to the RECIST criteria. Eur J Cancer 45(2):248–260. CrossRefPubMedGoogle Scholar
  18. 18.
    Mima K, Beppu T, Chikamoto A et al (2013) Hepatic resection combined with radiofrequency ablation for initially unresectable colorectal liver metastases after effective chemotherapy is a safe procedure with a low incidence of local recurrence. Int J Clin Oncol 18(5):847–855. CrossRefPubMedGoogle Scholar
  19. 19.
    D’Angelica M, Kornprat P, Gonen M et al (2011) Effect on outcome of recurrence patterns after hepatectomy for colorectal metastases. Ann Surg Oncol 18(4):1096–1103. CrossRefPubMedGoogle Scholar
  20. 20.
    Petrowsky H, Gonen M, Jarnagin W et al (2002) Second liver resections are safe and effective treatment for recurrent hepatic metastases from colorectal cancer: a bi-institutional analysis. Ann Surg 235(6):863–871CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Adair RA, Young AL, Cockbain AJ et al (2012) Repeat hepatic resection for colorectal liver metastases. Br J Surg 99(9):1278–1283. CrossRefPubMedGoogle Scholar
  22. 22.
    Nanji S, Tsang ME, Wei X et al (2016) Outcomes after repeat hepatic resection for recurrent metastatic colorectal cancer: a population-based study. Am J Surg. PubMedGoogle Scholar
  23. 23.
    Ali MA, Di Sandro S, Lauterio A et al (2015) Repeat hepatectomy for recurrent colorectal liver metastases: is it worth the challenge? J Gastrointest Surg 19(12):2192–2198. CrossRefPubMedGoogle Scholar
  24. 24.
    Luo LX, Yu ZY, Huang JW et al (2014) Selecting patients for a second hepatectomy for colorectal metastases: an systemic review and meta-analysis. Eur J Surg Oncol 40(9):1036–1048. CrossRefPubMedGoogle Scholar
  25. 25.
    Battula N, Tsapralis D, Mayer D et al (2014) Repeat liver resection for recurrent colorectal metastases: a single-centre, 13-year experience. HPB (Oxford) 16(2):157–163. CrossRefGoogle Scholar
  26. 26.
    Takahashi M, Hasegawa K, Oba M et al (2015) Repeat resection leads to long-term survival: analysis of 10-year follow-up of patients with colorectal liver metastases. Am J Surg 210(5):904–910. CrossRefPubMedGoogle Scholar
  27. 27.
    Hof J, Wertenbroek MW, Peeters PM et al (2016) Outcomes after resection and/or radiofrequency ablation for recurrence after treatment of colorectal liver metastases. Br J Surg 103(8):1055–1062. CrossRefPubMedGoogle Scholar
  28. 28.
    Matsuda K, Hotta T, Uchiyama K et al (2007) Repeat reduction surgery after an initial hepatectomy for patients with colorectal cancer. Oncol Rep 18(1):189–194PubMedGoogle Scholar
  29. 29.
    Mise Y, Aloia TA, Brudvik KW et al (2016) Parenchymal-sparing hepatectomy in colorectal liver metastasis improves salvageability and survival. Ann Surg 263(1):146–152. CrossRefPubMedGoogle Scholar

Copyright information

© Japan Society of Clinical Oncology 2018

Authors and Affiliations

  • Katsunori Imai
    • 1
  • Yo-ichi Yamashita
    • 1
  • Yuji Miyamoto
    • 1
  • Shigeki Nakagawa
    • 1
  • Hirohisa Okabe
    • 1
  • Daisuke Hashimoto
    • 1
  • Akira Chikamoto
    • 1
  • Hideo Baba
    • 1
  1. 1.Department of Gastroenterological Surgery, Graduate School of Life SciencesKumamoto UniversityKumamotoJapan

Personalised recommendations