Background: Due to the uncertain benefit of liver resection for non-colorectal liver metastases (NCLM), patient selection for surgery is generally difficult. Therefore, the aim of this article was to propose standard and extended indications for liver resection in this heterogeneous disease collective. Methods: Review of the literature. Results: The myriad of biologically different primary tumor entities as well as the mostly small and retrospective studies investigating the benefit of surgery for NCLM limits the proposal of general recommendations. Only resection of neuroendocrine liver metastases (NELM) appears to offer a clear benefit with a 5- and 10-year overall survival (OS) of 74 and 51%, respectively, in the largest series. Resection of liver metastases from genitourinary primaries might offer reasonable benefit in selected cases - with a 5-year OS of up to 61% for breast cancer and of 38% for renal cell cancer. The long-term outcome following surgery for other entities was remarkably poorer, e.g., gastric cancer, pancreatic cancer, and melanoma reached a 5-year OS of 20-42, 17-25, and about 20%, respectively. Conclusion: Liver resection for NELM can be defined as a standard indication for the resection of NCLM while lesions of genitourinary origin might be defined as an extended indication.

1.
McCarter MD, Fong Y: Metastatic liver tumors. Semin Surg Oncol 2000;19:177-188.
2.
Rees M, Tekkis PP, Welsh FK, 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;247:125-135.
3.
Vigano 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;15:2458-2464.
4.
van Ruth S, Mutsaerts E, Zoetmulder FA, van Coevorden F: Metastasectomy for liver metastases of non-colorectal primaries. Eur J Surg Oncol 2001;27:662-667.
5.
Metcalfe MS, Mullin EJ, Maddern GJ: Hepatectomy for metastatic noncolorectal gastrointestinal, breast and testicular tumours. ANZ J Surg 2006;76:246-250.
6.
O'Rourke TR, Tekkis P, Yeung S, Fawcett J, Lynch S, Strong R, Wall D, John TG, Welsh F, Rees M: Long-term results of liver resection for non-colorectal, non-neuroendocrine metastases. Ann Surg Oncol 2008;15:207-218.
7.
Glazer ES, Tseng JF, Al-Refaie W, Solorzano CC, Liu P, Willborn KA, Abdalla EK, Vauthey JN, Curley SA: Long-term survival after surgical management of neuroendocrine hepatic metastases. HPB (Oxford) 2010;12:427-433.
8.
Lendoire J, Moro M, Andriani O, Grondona J, Gil O, Raffin G, Silva J, Bracco R, Podesta G, Valenzuela C, Imventarza O, Pekolj J, De Santibanes E: Liver resection for non-colorectal, non-neuroendocrine metastases: analysis of a multicenter study from Argentina. HPB (Oxford) 2007;9:435-439.
9.
Haddad AJ, Bani Hani M, Pawlik TM, Cunningham SC: Colorectal liver metastases. Int J Surg Oncol 2011;2011:285840.
10.
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
11.
Kulik U, Bektas H, Klempnauer J, Lehner F: Repeat liver resection for colorectal metastases. Br J Surg 2013;100:926-932.
12.
Kulik U, Framke T, Grosshennig A, Ceylan A, Bektas H, Klempnauer J, Lehner F: Liver resection of colorectal liver metastases in elderly patients. World J Surg 2011;35:2063-2072.
13.
Welsh FK, Tekkis PP, John TG, Rees M: Predictive models in colorectal liver metastases - can we personalize treatment and outcome? Dig Surg 2008;25:406-412.
14.
Modlin IM, Lye KD, Kidd M: A 5-decade analysis of 13,715 carcinoid tumors. Cancer 2003;97:934-959.
15.
Frilling A, Li J, Malamutmann E, Schmid KW, Bockisch A, Broelsch CE: Treatment of liver metastases from neuroendocrine tumours in relation to the extent of hepatic disease. Br J Surg 2009;96:175-184.
16.
Mayo SC, de Jong MC, Pulitano C, et al: Surgical management of hepatic neuroendocrine tumor metastasis: results from an international multi-institutional analysis. Ann Surg Oncol 2010;17:3129-3136.
17.
Landry CS, Scoggins CR, McMasters KM, Martin RC 2nd: Management of hepatic metastasis of gastrointestinal carcinoid tumors. J Surg Oncol 2008;97:253-258.
18.
Sarmiento JM, Heywood G, Rubin J, Ilstrup DM, Nagorney DM, Que FG: Surgical treatment of neuroendocrine metastases to the liver: a plea for resection to increase survival. J Am Coll Surg 2003;197:29-37.
19.
Cusati D, Zhang L, Harmsen WS, Hu A, Farnell MB, Nagorney DM, Donohue JH, Que FG, Reid-Lombardo KM, Kendrick ML: Metastatic nonfunctioning pancreatic neuroendocrine carcinoma to liver: surgical treatment and outcomes. J Am Coll Surg 2012;215:117-124; discussion 124-115.
20.
Le Treut YP, Gregoire E, Klempnauer J, et al: Liver transplantation for neuroendocrine tumors in Europe - results and trends in patient selection: a 213-case European liver transplant registry study. Ann Surg 2013;257:807-815.
21.
Fan ST, Le Treut YP, Mazzaferro V, Burroughs AK, Olausson M, Breitenstein S, Frilling A: Liver transplantation for neuroendocrine tumour liver metastases. HPB (Oxford) 2015;17:23-28.
22.
Le Treut YP, Gregoire E, Belghiti J, Boillot O, Soubrane O, Mantion G, Cherqui D, Castaing D, Ruszniewski P, Wolf P, Paye F, Salame E, Muscari F, Pruvot FR, Baulieux J: Predictors of long-term survival after liver transplantation for metastatic endocrine tumors: an 85-case French multicentric report. Am J Transplant 2008;8:1205-1213.
23.
Mazzaferro V, Pulvirenti A, Coppa J: Neuroendocrine tumors metastatic to the liver: how to select patients for liver transplantation? J Hepatol 2007;47:460-466.
24.
Lehner F, Ramackers W, Bektas H, Becker T, Klempnauer J: Liver resection for non-colorectal, non-neuroendocrine liver metastases - is hepatic resection justified as part of the oncosurgical treatment? (Article in German). Zentralbl Chir 2009;134:430-436.
25.
Bresadola V, Rossetto A, Adani GL, Baccarani U, Lorenzin D, Favero A, Bresadola F: Liver resection for noncolorectal and nonneuroendocrine metastases: results of a study on 56 patients at a single institution. Tumori 2011;97:316-322.
26.
Groeschl RT, Nachmany I, Steel JL, Reddy SK, Glazer ES, de Jong MC, Pawlik TM, Geller DA, Tsung A, Marsh JW, Clary BM, Curley SA, Gamblin TC: Hepatectomy for noncolorectal non-neuroendocrine metastatic cancer: a multi-institutional analysis. J Am Coll Surg 2012;214:769-777.
27.
Chua TC, Saxena A, Liauw W, Chu F, Morris DL: Hepatic resection for metastatic breast cancer: a systematic review. Eur J Cancer 2011;47:2282-2290.
28.
Howlader M, Heaton N, Rela M: Resection of liver metastases from breast cancer: towards a management guideline. Int J Surg 2011;9:285-291.
29.
Ruys AT, Tanis PJ, Nagtegaal ID, van Duijvendijk P, Verhoef C, Porte RJ, van Gulik TM: Surgical treatment of renal cell cancer liver metastases: a population-based study. Ann Surg Oncol 2011;18:1932-1938.
30.
Thelen A, Jonas S, Benckert C, Lopez-Hanninen E, Rudolph B, Neumann U, Neuhaus P: Liver resection for metastases from renal cell carcinoma. World J Surg 2007;31:802-807.
31.
Hemming AW, Sielaff TD, Gallinger S, Cattral MS, Taylor BR, Greig PD, Langer B: Hepatic resection of noncolorectal nonneuroendocrine metastases. Liver Transpl 2000;6:97-101.
32.
Slotta JE, Schuld J, Distler S, Richter S, Schilling MK, Kollmar O: Hepatic resection of non-colorectal and non-neuroendocrine liver metastases - survival benefit for patients with non-gastrointestinal primary cancers - a case-controlled study. Int J Surg 2014;12:163-168.
33.
Uggeri F, Ronchi PA, Goffredo P, Garancini M, Degrate L, Nespoli L, Gianotti L, Romano F: Metastatic liver disease from non-colorectal, non-neuroendocrine, non-sarcoma cancers: a systematic review. World J Surg Oncol 2015;13:191.
34.
Kerkar SP, Kemp CD, Avital I: Liver resections in metastatic gastric cancer. HPB (Oxford) 2010;12:589-596.
35.
Koga R, Yamamoto J, Ohyama S, Saiura A, Seki M, Seto Y, Yamaguchi T: Liver resection for metastatic gastric cancer: experience with 42 patients including eight long-term survivors. Jpn J Clin Oncol 2007;37:836-842.
36.
Pawlik TM, Zorzi D, Abdalla EK, Clary BM, Gershenwald JE, Ross MI, Aloia TA, Curley SA, Camacho LH, Capussotti L, Elias D, Vauthey JN: Hepatic resection for metastatic melanoma: distinct patterns of recurrence and prognosis for ocular versus cutaneous disease. Ann Surg Oncol 2006;13:712-720.
37.
Rivoire M, Kodjikian L, Baldo S, Kaemmerlen P, Negrier S, Grange JD: Treatment of liver metastases from uveal melanoma. Ann Surg Oncol 2005;12:422-428.
38.
Hsueh EC, Essner R, Foshag LJ, Ye X, Wang HJ, Morton DL: Prolonged survival after complete resection of metastases from intraocular melanoma. Cancer 2004;100:122-129.
39.
Adam R, Chiche L, Aloia T, Elias D, Salmon R, Rivoire M, Jaeck D, Saric J, Le Treut YP, Belghiti J, Mantion G, Mentha G; Association Française de Chirurgie: Hepatic resection for noncolorectal nonendocrine liver metastases: analysis of 1,452 patients and development of a prognostic model. Ann Surg 2006;244:524-535.
40.
Sarmiento JM, Que FG: Hepatic surgery for metastases from neuroendocrine tumors. Surg Oncol Clin N Am 2003;12:231-242.
41.
Valadares LJ, Costa Junior W, Ribeiro HS, Diniz AL, Coimbra FJ, Herman P: Resection of liver metastasis from neuroendocrine tumors: evaluation of results and prognostic factors. Rev Col Bras Cir 2015;42:25-31.
42.
Pocard M, Pouillart P, Asselain B, Salmon R: Hepatic resection in metastatic breast cancer: results and prognostic factors. Eur J Surg Oncol 2000;26:155-159.
43.
Yoshimoto M, Tada T, Saito M, Takahashi K, Uchida Y, Kasumi F: Surgical treatment of hepatic metastases from breast cancer. Breast Cancer Res Treat 2000;59:177-184.
44.
Vlastos G, Smith DL, Singletary SE, Mirza NQ, Tuttle TM, Popat RJ, Curley SA, Ellis LM, Roh MS, Vauthey JN: Long-term survival after an aggressive surgical approach in patients with breast cancer hepatic metastases. Ann Surg Oncol 2004;11:869-874.
45.
Sakamoto Y, Yamamoto J, Yoshimoto M, Kasumi F, Kosuge T, Kokudo N, Makuuchi M: Hepatic resection for metastatic breast cancer: prognostic analysis of 34 patients. World J Surg 2005;29:524-527.
46.
Kollmar O, Moussavian MR, Richter S, Bolli M, Schilling MK: Surgery of liver metastasis in gynecological cancer - indication and results. Onkologie 2008;31:375-379.
47.
Alves A, Adam R, Majno P, Delvart V, Azoulay D, Castaing D, Bismuth H: Hepatic resection for metastatic renal tumors: is it worthwhile? Ann Surg Oncol 2003;10:705-710.
48.
Shirabe K, Shimada M, Matsumata T, Higashi H, Yakeishi Y, Wakiyama S, Ikeda Y, Ezaki T, Fukuzawa S, Takenaka K, Kishikawa K, Ikeda T, Taguchi K, Maehara Y, Sugimachi K: Analysis of the prognostic factors for liver metastasis of gastric cancer after hepatic resection: a multi-institutional study of the indications for resection. Hepatogastroenterology 2003;50:1560-1563.
49.
Cheon SH, Rha SY, Jeung HC, Im CK, Kim SH, Kim HR, Ahn JB, Roh JK, Noh SH, Chung HC: Survival benefit of combined curative resection of the stomach (D2 resection) and liver in gastric cancer patients with liver metastases. Ann Oncol 2008;19:1146-1153.
50.
Tiberio GA, Coniglio A, Marchet A, Marrelli D, Giacopuzzi S, Baiocchi L, Roviello F, de Manzoni G, Nitti D, Giulini SM: Metachronous hepatic metastases from gastric carcinoma: a multicentric survey. Eur J Surg Oncol 2009;35:486-491.
51.
Yamada H, Hirano S, Tanaka E, Shichinohe T, Kondo S: Surgical treatment of liver metastases from pancreatic cancer. HPB (Oxford) 2006;8:85-88.
52.
Gleisner AL, Assumpcao L, Cameron JL, Wolfgang CL, Choti MA, Herman JM, Schulick RD, Pawlik TM: Is resection of periampullary or pancreatic adenocarcinoma with synchronous hepatic metastasis justified? Cancer 2007;110:2484-2492.
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