Advertisement

Journal of Gastrointestinal Surgery

, Volume 17, Issue 7, pp 1312–1321 | Cite as

A Systematic Review of Repeat Hepatectomy for Recurrent Colorectal Liver Metastases

  • Vincent W. T. Lam
  • Tony Pang
  • Jerome M. Laurence
  • Emma Johnston
  • Michael J. Hollands
  • Henry C. C. Pleass
  • Arthur J. Richardson
Review Article

Abstract

Background

Selected patients with recurrent colorectal liver metastases (CLM) may be resectable by repeat hepatectomy approach. In this review, we aim to collate and evaluate the published evidence for repeat hepatectomy in patients with recurrent CLM.

Methods

Searches of the Medline and Embase databases were undertaken to identify studies of repeat hepatectomy in patients with recurrent CLM focusing on the perioperative treatment regimen, operative strategy, morbidity, technical success and survival outcomes.

Results

Twenty-two observational studies were reviewed. A total of 1,610 patients underwent second hepatectomy for recurrent CLM. The median percentage of extra-hepatic disease was 15 % (range, 0–39 %). Preoperative chemotherapy was reported in 5/22 studies. Major liver resection was undertaken in 25 % (range, 9–59 %) of patients and the R0 resection rate was 90 % (range, 77–96 %). Postoperative morbidity and mortality after the second hepatectomy were 23 % and 1.2 %, respectively. Recurrence rate after second hepatectomy was 63.9 % (range, 42–91 %) with a median follow-up period of 32 months (range, 19–59 months). Median overall survival was 35 months (range, 19–56 months). The 3-year and 5-year overall survival rates were 55 % (range, 11–82 %) and 42 % (range, 31–73 %), respectively.

Conclusion

Second hepatectomy is safe and feasible in selected patients with recurrent CLM and is associated with acceptable perioperative and survival outcomes. Future prospective studies are required to further define the patient selection criteria for repeat hepatectomy and the exact role of perioperative chemotherapy.

Keywords

Colorectal liver metastases Hepatectomy Surgery Recurrence Colorectal cancer 

Reference

  1. 1.
    Parkin DM, Bray F, Ferlay J, Pisani P: Global cancer statistics, 2002. CA Cancer J Clin 2005, 55(2):74–108.PubMedCrossRefGoogle Scholar
  2. 2.
    Steele GJ, Ravikumar TS: Resection of hepatic metastases from colorectal metastases: Biologic perspectives. Ann Surg 1989, 210:127–138.PubMedCrossRefGoogle Scholar
  3. 3.
    Van Cutsem E, Rivera F, Berry S, Kretzschmar A, Michael M, Dibartolomeo M, Mazier M-A, Canon J-L, Georgoulias V, Peeters M et al.: Safety and efficacy of first-line bevacizumab with FOLFOX, XELOX, FOLFIRI and fluoropyrimidines in metastatic colorectal cancer: the BEAT study. Ann Oncol 2009, 20(11):1842–1847.PubMedCrossRefGoogle Scholar
  4. 4.
    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(5):502–508.PubMedCrossRefGoogle Scholar
  5. 5.
    Abdalla EK, Vauthey JN, Ellis LM, Ellis V, Pollock R, Broglio KR, Hess K, Curley SA: Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 2004, 239(6):818–825; discussion 825–817.PubMedCrossRefGoogle Scholar
  6. 6.
    Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, Lillemoe KD, Yeo CJ, Cameron JL: Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg 2002, 235(6):759–766.PubMedCrossRefGoogle Scholar
  7. 7.
    Fernandez FG, Drebin JA, Linehan DC, Dehdashti F, Siegel BA, Strasberg SM: Five-year survival after resection of hepatic metastases from colorectal cancer in patients screened by positron emission tomography with F-18 fluorodeoxyglucose (FDG-PET). Ann Surg 2004, 240(3):438–447.PubMedCrossRefGoogle Scholar
  8. 8.
    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(3):309–318; discussion 318–321.PubMedCrossRefGoogle Scholar
  9. 9.
    Minagawa M, Makuuchi M, Torzilli G, Takayama T, Kawasaki S, Kosuge T, Yamamoto J, Imamura H: Extension of the frontiers of surgical indications in the treatment of liver metastases from colorectal cancer: long-term results. Ann Surg 2000, 231(4):487–499.PubMedCrossRefGoogle Scholar
  10. 10.
    Nordlinger B, Guiguet M, Vaillant JC, Balladur P, Boudjema K, Bachellier P, Jaeck D: Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Cancer 1996, 77(7):1254–1262.PubMedCrossRefGoogle Scholar
  11. 11.
    Rees M, Tekkis PP, Welsh FKS, O'Rourke T, John TG: Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg 2008, 247(1):125–135.PubMedCrossRefGoogle Scholar
  12. 12.
    Scheele J, Stang R, Altendorf-Hofmann A, Paul M: Resection of colorectal liver metastases. World J Surg 1995, 19(1):59–71.PubMedCrossRefGoogle Scholar
  13. 13.
    Jones RP, Jackson R, Dunne DFJ, Malik HZ, Fenwick SW, Poston GJ, Ghaneh P: Systematic review and meta-analysis of follow-up after hepatectomy for colorectal liver metastases. Br J Surg 2012, 99(4):477–486.PubMedCrossRefGoogle Scholar
  14. 14.
    McKenzie S, Barnes S, Schwartz RW: The surgical management of locoregional and metastatic colorectal cancer recurrences. Curr Surg 2005, 62(6):585–590.PubMedCrossRefGoogle Scholar
  15. 15.
    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 Metastasis. Ann Surg 2009, 250(3):440–448.PubMedGoogle Scholar
  16. 16.
    Wells GA, Shea B, O'Connell D, Peterson J, Welch V, Losos M, Tugwell P: The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. In: Third Symposium on Systematic Reviews: Beyond the Basics. Oxford; July 2000.Google Scholar
  17. 17.
    National Health and Medical Research Council: A guide to the development, implementation and evaluation of clinical practice guidelines. Canberra, ACT: AusInfo; 1999.Google Scholar
  18. 18.
    Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D: The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 2009, 62(10):e1-34.PubMedCrossRefGoogle Scholar
  19. 19.
    Rolff HC, Calatayud D, Larsen PN, Wettergren A: Good results after repeated resection for colorectal liver metastases. Danish Medical Journal 2012, 59(2):A4373.PubMedGoogle Scholar
  20. 20.
    Jones NB, McNally ME, Malhotra L, Abdel-Misih S, Martin EW, Bloomston M, Schmidt CR: Repeat hepatectomy for metastatic colorectal cancer is safe but marginally effective. Ann Surg Oncol 2012, 19(7):2224–2229.PubMedCrossRefGoogle Scholar
  21. 21.
    Andreou A, Brouquet A, Abdalla EK, Aloia TA, Curley SA, Vauthey J-N: Repeat hepatectomy for recurrent colorectal liver metastases is associated with a high survival rate. HPB 2011, 13(11):774–782.PubMedCrossRefGoogle Scholar
  22. 22.
    de Jong MC, Mayo SC, Pulitano C, Lanella S, Ribero D, Strub J, Hubert C, Gigot J-F, Schulick RD, Choti MA et al.: Repeat curative intent liver surgery is safe and effective for recurrent colorectal liver metastasis: results from an international multi-institutional analysis. J Gastrointest Surg 2009, 13(12):2141–2151.PubMedCrossRefGoogle Scholar
  23. 23.
    Brachet D, Lermite E, Rouquette A, Lorimier G, Hamy A, Arnaud J-P: 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.PubMedCrossRefGoogle Scholar
  24. 24.
    Thelen A, Jonas S, Benckert C, Schumacher G, Lopez-Hanninen E, Rudolph B, Neumann U, Neuhaus P: Repeat liver resection for recurrent liver metastases from colorectal cancer. Eur J Surg Oncol 2007, 33(3):324–328.PubMedCrossRefGoogle Scholar
  25. 25.
    Sa Cunha A, Laurent C, Rault A, Couderc P, Rullier E, Saric J: A second liver resection due to recurrent colorectal liver metastases. Arch Surg 2007, 142(12):1144–1149.PubMedCrossRefGoogle Scholar
  26. 26.
    Nishio H, Hamady ZZR, Malik HZ, Fenwick S, Rajendra Prasad K, Toogood GJ, Lodge JPA: Outcome following repeat liver resection for colorectal liver metastases. Eur J Surg Oncol 2007, 33(6):729–734.PubMedCrossRefGoogle Scholar
  27. 27.
    Yan TD, Lian KQ, Chang D, Morris DL: Management of intrahepatic recurrence after curative treatment of colorectal liver metastases. Br J Surg 2006, 93(7):854–859.PubMedCrossRefGoogle Scholar
  28. 28.
    Shaw IM, Rees M, Welsh FKS, Bygrave S, John TG: Repeat hepatic resection for recurrent colorectal liver metastases is associated with favourable long-term survival. Br J Surg 2006, 93(4):457–464.PubMedCrossRefGoogle Scholar
  29. 29.
    Ishiguro S, Akasu T, Fujimoto Y, Yamamoto J, Sakamoto Y, Sano T, Shimada K, Kosuge T, Yamamoto S, Fujita S et al.: Second hepatectomy for recurrent colorectal liver metastasis: analysis of preoperative prognostic factors. Ann Surg Oncol 2006, 13(12):1579–1587.PubMedCrossRefGoogle Scholar
  30. 30.
    Sugawara G, Isogai M, Kaneoka Y, Suzuki M, Yamaguchi A: Repeat hepatectomy for recurrent colorectal metastases. Surg Today 2005, 35(4):282–289.PubMedCrossRefGoogle Scholar
  31. 31.
    Tanaka K, Shimada H, Ohta M, Togo S, Saitou S, Yamaguchi S, Endo I, Sekido H: Procedures of choice for resection of primary and recurrent liver metastases from colorectal cancer. World J Surg 2004, 28(5):482–487.PubMedCrossRefGoogle Scholar
  32. 32.
    Takahashi S, Inoue K, Konishi M, Nakagouri T, Kinoshita T: Prognostic factors for poor survival after repeat hepatectomy in patients with colorectal liver metastases. Surgery 2003, 133(6):627–634.PubMedCrossRefGoogle Scholar
  33. 33.
    Adam R, Pascal G, Azoulay D, Tanaka K, Castaing D, Bismuth H: Liver resection for colorectal metastases: the third hepatectomy. Ann Surg 2003, 238(6):871–883.PubMedCrossRefGoogle Scholar
  34. 34.
    Petrowsky H, Gonen M, Jarnagin W, Lorenz M, DeMatteo R, Heinrich S, Encke A, Blumgart L, Fong Y: 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.PubMedCrossRefGoogle Scholar
  35. 35.
    Suzuki S, Sakaguchi T, Yokoi Y, Kurachi K, Okamoto K, Okumura T, Tsuchiya Y, Nakamura T, Konno H, Baba S et al.: Impact of repeat hepatectomy on recurrent colorectal liver metastases. Surgery 2001, 129(4):421–428.PubMedGoogle Scholar
  36. 36.
    Fernández-Trigo V, Shamsa F, Sugarbaker PH: Repeat liver resections from colorectal metastasis. Surgery 1995, 117(3):296–304.PubMedCrossRefGoogle Scholar
  37. 37.
    Scheele J, Stangl R, Schmidt K, Altendorf-Hofmann A: Recurrent tumor after R0 resection of colorectal liver metastases. Incidence, resectability and prognosis. Chirurg 1995, 66(10):965–973.PubMedGoogle Scholar
  38. 38.
    Nordlinger B, Vaillant JC, Guiguet M, Balladur P, Paris F, Bachellier P, Jaeck D: Survival benefit of repeat liver resections for recurrent colorectal metastases: 143 Cases. J Clin Oncol 1994, 12(7):1491–1496.PubMedGoogle Scholar
  39. 39.
    Nicoli N, Marchiori L, Mangiante G, Bortolasi L, Dal Dosso I, Aurola PP, Delaini GG, Serio G: Repeated liver resections for metastases from colorectal carcinoma: the experience of 23 cases. Chir Ital 1994, 46(1):37–44.PubMedGoogle Scholar
  40. 40.
    Que FG, Nagorney DM: Resection of 'recurrent' colorectal metastases to the liver. Br J Surg 1994, 81(2):255–258.PubMedCrossRefGoogle Scholar
  41. 41.
    Adam R, Bismuth H, Castaing D, Waechter F, Navarro F, Abascal A, Majno P, Engerran L: Repeat hepatectomy for colorectal liver metastases. Ann Surg 1997, 225(1):51–60.PubMedCrossRefGoogle Scholar
  42. 42.
    Yamamoto J, Kosuge T, Shimada K, Yamasaki S, Moriya Y, Sugihara K: Repeat liver resection for recurrent colorectal liver metastases. Am J Surg 1999, 178(4):275–281.PubMedCrossRefGoogle Scholar
  43. 43.
    Antoniou A, Lovegrove RE, Tilney HS, Heriot AG, John TG, Rees M, Tekkis PP, Welsh FKS: Meta-analysis of clinical outcome after first and second liver resection for colorectal metastases. Surgery 2007, 141(1):9–18.PubMedCrossRefGoogle Scholar
  44. 44.
    Yan TD, Sim J, Black D, Niu R, Morris DL: Systematic review on safety and efficacy of repeat hepatectomy for recurrent liver metastases from colorectal carcinoma. Ann Surg Oncol 2007, 14(7):2069–2077.PubMedCrossRefGoogle Scholar
  45. 45.
    Elias D, Lasser P, Hoang JM, Leclere J, Debaene B, Bognel C, Spencer A, Rougier P: Repeat hepatectomy for cancer. The British journal of surgery 1993, 80(12):1557–1562.PubMedCrossRefGoogle Scholar
  46. 46.
    Tomlinson JS, Jarnagin WR, Dematteo RP, Fong Y, Kornprat P, Gönen M, Kemeny N, Brennan MF, Blumgart LH, D'Angelica M: Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol 2007, 25(29):4575–4580.Google Scholar
  47. 47.
    Viganò L, Ferrero A, lo Tesoriere R, Capussotti L: Liver Surgery for Colorectal Metastases: Results after 10 Years of Follow-Up. Long-Term Survivors, Late Recurrences, and Prognostic Role of Morbidity. Ann Surg Oncol 2008, 15(9):2458–2464.PubMedCrossRefGoogle Scholar
  48. 48.
    Pulitano C, Castillo F, Aldrighetti L, Bodingbauer M, Parks RW, Ferla G, Wigmore SJ, Garden OJ: What defines "cure" after liver resection for colorectal metastases? Results after 10 years of follow-up. HPB 2010, 12(4):244–249.PubMedGoogle Scholar
  49. 49.
    Chua TC, Liauw W, Chu F, Morris DL: Viewing metastatic colorectal cancer as a curable chronic disease. Am J Clin Oncol 2012, 35(1):77–80.PubMedCrossRefGoogle Scholar
  50. 50.
    Mohammad WM, Martel G, Mimeault R, Fairfull-Smith RJ, Auer RC, Balaa FK: Evaluating agreement regarding the resectability of colorectal liver metastases: a national case-based survey of hepatic surgeons. HPB 2012, 14(5):291–297.PubMedCrossRefGoogle Scholar
  51. 51.
    Folprecht G, Gruenberger T, Bechstein WO, Raab R, Lordick F, Hartmann JT, Lang H, Frilling A, Stoehlmacher J, Weitz J et al.: Tumour response and secondary resectability of colorectal liver metastases following neoadjavant chemotherapy with cetuximan: the CELIM randomized phase 2 trial. Lancet Oncol 2010, 11:38–47.PubMedCrossRefGoogle Scholar
  52. 52.
    Charnsangavej C, Clary B, Fong Y, Grothey A, Pawlik TM, Choti MA: Selection of patients for resection of hepatic colorectal metastases: expert consensus statement. Ann Surg Oncol 2006, 13(10):1261–1268.PubMedCrossRefGoogle Scholar
  53. 53.
    Adams RB, Aloia TA, Loyer EM, Pawlik TM, Taouli B, Vauthey J-N: Selection for hepatic resection of colorectal liver metastases: expert consensus statement. HPB 2012, (In Press).Google Scholar
  54. 54.
    Chua TC, Saxena A, Liauw W, Chu F, Morris DL: Hepatectomy and resection of concomitant extra-hepatic disease for colorectal liver metastases--a systematic review. Eur J Cancer 2012, 48(12):1757–1765.Google Scholar
  55. 55.
    de Gramont A, Figer A, Seymour M, Homerin M, Hmissi A, Cassidy J, Boni C, Cortes-Funes H, Cervantes A, Freyer G et al.: Leucovorin and fluorouracil with or without oxaliplatin as first-line treatment in advanced colorectal cancer. J Clin Oncol 2000, 18(16):2938–2947.PubMedGoogle Scholar
  56. 56.
    Tournigand C, André T, Achille E, Lledo G, Flesh M, Mery-Mignard D, Quinaux E, Couteau C, Buyse M, Ganem G et al.: FOLFIRI followed by FOLFOX6 or the reverse sequence in advanced colorectal cancer: a randomized GERCOR study. J Clin Oncol 2004, 22(2):229–237.PubMedCrossRefGoogle Scholar
  57. 57.
    Masi G, Loupakis F, Salvatore L, Fornaro L, Cremolini C, Cupini S, Ciarlo A, Del Monte F, Cortesi E, Amoroso D et al.: Bevacizumab with FOLFOXIRI (irinotecan, oxaliplatin, fluorouracil, and folinate) as first-line treatment for metastatic colorectal cancer: a phase 2 trial. Lancet Oncol 2010, 11(9):845–852.PubMedCrossRefGoogle Scholar
  58. 58.
    Nordlinger B, Sorbye H, Glimelius B, Poston GJ, Schlag PM, Rougier P, Bechstein WO, Primrose JN, Walpole ET, Finch-Jones M et al.: Perioperative chemotherapy with FOLFOX4 and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC Intergroup trial 40983): a randomised controlled trial. Lancet 2008, 371(9617):1007–1016.PubMedCrossRefGoogle Scholar
  59. 59.
    Misiakos EP: Current treatment for colorectal liver metastases. World J Gastroenterol 2011, 17(36):4067–4075.PubMedCrossRefGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2013

Authors and Affiliations

  • Vincent W. T. Lam
    • 1
    • 2
  • Tony Pang
    • 1
    • 2
  • Jerome M. Laurence
    • 1
  • Emma Johnston
    • 1
    • 2
  • Michael J. Hollands
    • 1
    • 2
  • Henry C. C. Pleass
    • 1
    • 2
  • Arthur J. Richardson
    • 1
    • 2
  1. 1.Department of Surgery, Westmead HospitalUniversity of SydneySydneyAustralia
  2. 2.Discipline of SurgerySydney Medical SchoolSydneyAustralia

Personalised recommendations