Investigation and Management of Colorectal Cancer Liver Metastases
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Abstract
Colorectal cancer remains the third most common cancer worldwide and ranks 2nd in cancer-related mortality in developed countries. The liver is the first organ involved with metastatic disease after lymph node spread is excluded. Colorectal liver metastases (CRLM) are present in over 70% of patients dying from disseminated colorectal cancer. The approach to investigation and management of CRLM remains a complex area, in which practice is continuing to evolve with new evidence, and which ongoing research is ongoing. This review aims to provide a broad, up-to-date overview of the current landscape of the literature in regards to imaging modalities used in diagnosis and staging of CRLM, the multiple surgical management options available, as well as the adjunct therapies and chemotherapy regimens utilised.
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References
2. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA: a cancer journal for clinicians. 2018;68(1):7-30.
3. Weiss L, Grundmann E, Torhorst J, Hartveit F, Moberg I, Eder M, et al. Haematogenous metastatic patterns in colonic carcinoma: an analysis of 1541 necropsies. The Journal of pathology. 1986;150(3):195-203.
4. Pestana C, Reitemeier RJ, Moertel CG, Judd ES, Dockerty MB. THE NATURAL HISTORY OF CARCINOMA OF THE COLON AND RECTUM. American journal of surgery. 1964;108:826-9.
5. Kune GA, Kune S, Field B, White R, Brough W, Schellenberger R, et al. Survival in patients with large-bowel cancer. A population-based investigation from the Melbourne Colorectal Cancer Study. Diseases of the colon and rectum. 1990;33(11):938-46.
6. Steele G, Jr., Ravikumar TS. Resection of hepatic metastases from colorectal cancer. Biologic perspective. Annals of surgery. 1989;210(2):127-38.
7. Jaffe BM, Donegan WL, Watson F, Spratt JS, Jr. Factors influencing survival in patients with untreated hepatic metastases. Surgery, gynecology & obstetrics. 1968;127(1):1-11.
8. Stangl R, Altendorf-Hofmann A, Charnley RM, Scheele J. Factors influencing the natural history of colorectal liver metastases. Lancet. 1994;343(8910):1405-10.
9. Tomlinson JS, Jarnagin WR, DeMatteo RP, Fong Y, Kornprat P, Gonen M, et al. Actual 10-year survival after resection of colorectal liver metastases defines cure. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2007;25(29):4575-80.
10. Misiakos EP, Karidis NP, Kouraklis G. Current treatment for colorectal liver metastases. World journal of gastroenterology. 2011;17(36):4067-75.
11. Kopetz S, Chang GJ, Overman MJ, Eng C, Sargent DJ, Larson DW, et al. Improved survival in metastatic colorectal cancer is associated with adoption of hepatic resection and improved chemotherapy. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2009;27(22):3677-83.
12. Cantisani V, Ricci P, Erturk M, Pagliara E, Drudi F, Calliada F, et al. Detection of hepatic metastases from colorectal cancer: prospective evaluation of gray scale US versus SonoVue(R) low mechanical index real time-enhanced US as compared with multidetector-CT or Gd-BOPTA-MRI. Ultraschall in der Medizin (Stuttgart, Germany : 1980). 2010;31(5):500-5.
13. Xu L-H, Cai S-J, Cai G-X, Peng W-J. Imaging diagnosis of colorectal liver metastases. World Journal of Gastroenterology : WJG. 2011;17(42):4654-9.
14. Bernatik T, Becker D, Neureiter D, Hansler J, Frieser M, Schaber S, et al. [Detection of liver metastases--comparison of contrast--enhanced ultrasound using first versus second generation contrast agents]. Ultraschall in der Medizin (Stuttgart, Germany : 1980). 2003;24(3):175-9.
15. Scaife CL, Ng CS, Ellis LM, Vauthey JN, Charnsangavej C, Curley SA. Accuracy of preoperative imaging of hepatic tumors with helical computed tomography. Annals of surgical oncology. 2006;13(4):542-6.
16. D'Hondt M, Vandenbroucke-Menu F, Preville-Ratelle S, Turcotte S, Chagnon M, Plasse M, et al. Is intra-operative ultrasound still useful for the detection of a hepatic tumour in the era of modern pre-operative imaging? HPB : the official journal of the International Hepato Pancreato Biliary Association. 2011;13(9):665-9.
17. Sietses C, Meijerink MR, Meijer S, van den Tol MP. The impact of intraoperative ultrasonography on the surgical treatment of patients with colorectal liver metastases. Surgical Endoscopy. 2010;24(8):1917-22.
18. Ch'en IY, Katz DS, Jeffrey RB, Jr., Daniel BL, Li KC, Beaulieu CF, et al. Do arterial phase helical CT images improve detection or characterization of colorectal liver metastases? Journal of computer assisted tomography. 1997;21(3):391-7.
19. Hale HL, Husband JE, Gossios K, Norman AR, Cunningham D. CT of calcified liver metastases in colorectal carcinoma. Clinical radiology. 1998;53(10):735-41.
20. Kamel IR, Choti MA, Horton KM, Braga HJ, Birnbaum BA, Fishman EK, et al. Surgically staged focal liver lesions: accuracy and reproducibility of dual-phase helical CT for detection and characterization. Radiology. 2003;227(3):752-7.
21. Bipat S, van Leeuwen MS, Comans EF, Pijl ME, Bossuyt PM, Zwinderman AH, et al. Colorectal liver metastases: CT, MR imaging, and PET for diagnosis--meta-analysis. Radiology. 2005;237(1):123-31.
22. Kulinna C, Helmberger T, Kessler M, Reiser M. [Improvement in diagnosis of liver metastases with the multi-detector CT]. Der Radiologe. 2001;41(1):16-23.
23. Valls C, Andia E, Sanchez A, Guma A, Figueras J, Torras J, et al. Hepatic metastases from colorectal cancer: preoperative detection and assessment of resectability with helical CT. Radiology. 2001;218(1):55-60.
24. Jhaveri KS, Fischer SE, Hosseini-Nik H, Sreeharsha B, Menezes RJ, Gallinger S, et al. Prospective comparison of gadoxetic acid-enhanced liver MRI and contrast-enhanced CT with histopathological correlation for preoperative detection of colorectal liver metastases following chemotherapy and potential impact on surgical plan. HPB : the official journal of the International Hepato Pancreato Biliary Association. 2017;19(11):992-1000.
25. Mainenti PP, Romano F, Pizzuti L, Segreto S, Storto G, Mannelli L, et al. Non-invasive diagnostic imaging of colorectal liver metastases. World journal of radiology. 2015;7(7):157-69.
26. Hamm B, Staks T, Muhler A, Bollow M, Taupitz M, Frenzel T, et al. Phase I clinical evaluation of Gd-EOB-DTPA as a hepatobiliary MR contrast agent: safety, pharmacokinetics, and MR imaging. Radiology. 1995;195(3):785-92.
27. Lowenthal D, Zeile M, Lim WY, Wybranski C, Fischbach F, Wieners G, et al. Detection and characterisation of focal liver lesions in colorectal carcinoma patients: comparison of diffusion-weighted and Gd-EOB-DTPA enhanced MR imaging. European radiology. 2011;21(4):832-40.
28. Mainenti PP, Mancini M, Mainolfi C, Camera L, Maurea S, Manchia A, et al. Detection of colo-rectal liver metastases: prospective comparison of contrast enhanced US, multidetector CT, PET/CT, and 1.5 Tesla MR with extracellular and reticulo-endothelial cell specific contrast agents. Abdominal imaging. 2010;35(5):511-21.
29. Choi SH, Kim SY, Park SH, Kim KW, Lee JY, Lee SS, et al. Diagnostic performance of CT, gadoxetate disodium-enhanced MRI, and PET/CT for the diagnosis of colorectal liver metastasis: Systematic review and meta-analysis. Journal of magnetic resonance imaging : JMRI. 2018;47(5):1237-50.
30. Schulz A, Viktil E, Godt JC, Johansen CK, Dormagen JB, Holtedahl JE, et al. Diagnostic performance of CT, MRI and PET/CT in patients with suspected colorectal liver metastases: the superiority of MRI. Acta radiologica. 2016;57(9):1040-8.
31. Seo HJ, Kim MJ, Lee JD, Chung WS, Kim YE. Gadoxetate disodium-enhanced magnetic resonance imaging versus contrast-enhanced 18F-fluorodeoxyglucose positron emission tomography/computed tomography for the detection of colorectal liver metastases. Investigative radiology. 2011;46(9):548-55.
32. Huebner RH, Park KC, Shepherd JE, Schwimmer J, Czernin J, Phelps ME, et al. A meta-analysis of the literature for whole-body FDG PET detection of recurrent colorectal cancer. Journal of nuclear medicine : official publication, Society of Nuclear Medicine. 2000;41(7):1177-89.
33. Kong G, Jackson C, Koh DM, Lewington V, Sharma B, Brown G, et al. The use of 18F-FDG PET/CT in colorectal liver metastases--comparison with CT and liver MRI. European journal of nuclear medicine and molecular imaging. 2008;35(7):1323-9.
34. Lee DH, Lee JM, Hur BY, Joo I, Yi NJ, Suh KS, et al. Colorectal Cancer Liver Metastases: Diagnostic Performance and Prognostic Value of PET/MR Imaging. Radiology. 2016;280(3):782-92.
35. Nielsen K, Scheffer HJ, Pieters IC, van Tilborg AA, van Waesberghe JH, Oprea-Lager DE, et al. The use of PET-MRI in the follow-up after radiofrequency- and microwave ablation of colorectal liver metastases. BMC medical imaging. 2014;14:27.
36. Adam R, de Gramont A, Figueras J, Kokudo N, Kunstlinger F, Loyer E, et al. Managing synchronous liver metastases from colorectal cancer: a multidisciplinary international consensus. Cancer treatment reviews. 2015;41(9):729-41.
37. Hamady ZZ, Lodge JP, Welsh FK, Toogood GJ, White A, John T, et al. One-millimeter cancer-free margin is curative for colorectal liver metastases: a propensity score case-match approach. Annals of surgery. 2014;259(3):543-8.
38. Cady B, Jenkins RL, Steele GD, Jr., Lewis WD, Stone MD, McDermott WV, et al. Surgical margin in hepatic resection for colorectal metastasis: a critical and improvable determinant of outcome. Annals of surgery. 1998;227(4):566-71.
39. Pawlik TM, Scoggins CR, Zorzi D, Abdalla EK, Andres A, Eng C, et al. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Annals of surgery. 2005;241(5):715-22, discussion 22-4.
40. Are C, Gonen M, Zazzali K, Dematteo RP, Jarnagin WR, Fong Y, et al. The impact of margins on outcome after hepatic resection for colorectal metastasis. Annals of surgery. 2007;246(2):295-300.
41. de Baere T, Roche A, Elias D, Lasser P, Lagrange C, Bousson V. Preoperative portal vein embolization for extension of hepatectomy indications. Hepatology (Baltimore, Md). 1996;24(6):1386-91.
42. Shoup M, Gonen M, D'Angelica M, Jarnagin WR, DeMatteo RP, Schwartz LH, et al. Volumetric analysis predicts hepatic dysfunction in patients undergoing major liver resection. Journal of gastrointestinal surgery : official journal of the Society for Surgery of the Alimentary Tract. 2003;7(3):325-30.
43. de Graaf W, van Lienden KP, van Gulik TM, Bennink RJ. (99m)Tc-mebrofenin hepatobiliary scintigraphy with SPECT for the assessment of hepatic function and liver functional volume before partial hepatectomy. Journal of nuclear medicine : official publication, Society of Nuclear Medicine. 2010;51(2):229-36.
44. Mattar RE, Al-Alem F, Simoneau E, Hassanain M. Preoperative selection of patients with colorectal cancer liver metastasis for hepatic resection. World journal of gastroenterology. 2016;22(2):567-81.
45. Hayashi H, Beppu T, Okabe H, Kuroki H, Nakagawa S, Imai K, et al. Functional assessment versus conventional volumetric assessment in the prediction of operative outcomes after major hepatectomy. Surgery. 2015;157(1):20-6.
46. 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. Annals of surgery. 1999;230(3):309-18; discussion 18-21.
47. Lykoudis PM, O'Reilly D, Nastos K, Fusai G. Systematic review of surgical management of synchronous colorectal liver metastases. The British journal of surgery. 2014;101(6):605-12.
48. Kelly ME, Spolverato G, Le GN, Mavros MN, Doyle F, Pawlik TM, et al. Synchronous colorectal liver metastasis: a network meta-analysis review comparing classical, combined, and liver-first surgical strategies. Journal of surgical oncology. 2015;111(3):341-51.
49. Feng Q, Wei Y, Zhu D, Ye L, Lin Q, Li W, et al. Timing of hepatectomy for resectable synchronous colorectal liver metastases: for whom simultaneous resection is more suitable--a meta-analysis. PloS one. 2014;9(8):e104348.
50. Yin Z, Liu C, Chen Y, Bai Y, Shang C, Yin R, et al. Timing of hepatectomy in resectable synchronous colorectal liver metastases (SCRLM): Simultaneous or delayed? Hepatology (Baltimore, Md). 2013;57(6):2346-57.
51. Ruers TJ, Hagendoorn J. Treatment dilemmas in patients with synchronous colorectal liver metastases. Recent results in cancer research Fortschritte der Krebsforschung Progres dans les recherches sur le cancer. 2012;196:37-49.
52. Lambert LA, Colacchio TA, Barth RJ, Jr. Interval hepatic resection of colorectal metastases improves patient selection. Archives of surgery (Chicago, Ill : 1960). 2000;135(4):473-9; discussion 9-80.
53. Waisberg J, Ivankovics IG. Liver-first approach of colorectal cancer with synchronous hepatic metastases: A reverse strategy. World journal of hepatology. 2015;7(11):1444-9.
54. Verhoef C, van der Pool AE, Nuyttens JJ, Planting AS, Eggermont AM, de Wilt JH. The "liver-first approach" for patients with locally advanced rectal cancer and synchronous liver metastases. Diseases of the colon and rectum. 2009;52(1):23-30.
55. Patrlj L, Kopljar M, Klicek R, Patrlj MH, Kolovrat M, Rakic M, et al. The surgical treatment of patients with colorectal cancer and liver metastases in the setting of the "liver first" approach. Hepatobiliary surgery and nutrition. 2014;3(5):324-9.
56. Andres A, Toso C, Adam R, Barroso E, Hubert C, Capussotti L, et al. A survival analysis of the liver-first reversed management of advanced simultaneous colorectal liver metastases: a LiverMetSurvey-based study. Annals of surgery. 2012;256(5):772-8; discussion 8-9.
57. Farges O, Belghiti J, Kianmanesh R, Regimbeau JM, Santoro R, Vilgrain V, et al. Portal vein embolization before right hepatectomy: prospective clinical trial. Annals of surgery. 2003;237(2):208-17.
58. Shindoh J, Tzeng CW, Aloia TA, Curley SA, Zimmitti G, Wei SH, et al. Portal vein embolization improves rate of resection of extensive colorectal liver metastases without worsening survival. The British journal of surgery. 2013;100(13):1777-83.
59. Mayo SC, Pawlik TM. Current management of colorectal hepatic metastasis. Expert review of gastroenterology & hepatology. 2009;3(2):131-44.
60. Abulkhir A, Limongelli P, Healey AJ, Damrah O, Tait P, Jackson J, et al. Preoperative portal vein embolization for major liver resection: a meta-analysis. Annals of surgery. 2008;247(1):49-57.
61. Giglio MC, Giakoustidis A, Draz A, Jawad ZAR, Pai M, Habib NA, et al. Oncological Outcomes of Major Liver Resection Following Portal Vein Embolization: A Systematic Review and Meta-analysis. Annals of surgical oncology. 2016;23(11):3709-17.
62. Hwang S, Lee SG, Ko GY, Kim BS, Sung KB, Kim MH, et al. Sequential preoperative ipsilateral hepatic vein embolization after portal vein embolization to induce further liver regeneration in patients with hepatobiliary malignancy. Annals of surgery. 2009;249(4):608-16.
63. Buac S, Schadde E, Schnitzbauer AA, Vogt K, Hernandez-Alejandro R. The many faces of ALPPS: surgical indications and techniques among surgeons collaborating in the international registry. HPB : the official journal of the International Hepato Pancreato Biliary Association. 2016;18(5):442-8.
64. Zhang GQ, Zhang ZW, Lau WY, Chen XP. Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): a new strategy to increase resectability in liver surgery. International journal of surgery. 2014;12(5):437-41.
65. Sala S, Ardiles V, Ulla M, Alvarez F, Pekolj J, de Santibanes E. Our initial experience with ALPPS technique: encouraging results. Updates in surgery. 2012;64(3):167-72.
66. Berger NG, Kim B, Gholami S, Margonis GA, Ethun C, Silva JP, et al. Two-stage hepatectomy for colorectal liver metastases: A multi-institutional retrospective review. Journal of Clinical Oncology. 2017;35(4_suppl):351-.
67. Wicherts DA, de Haas RJ, Salloum C, Andreani P, Pascal G, Sotirov D, et al. Repeat hepatectomy for recurrent colorectal metastases. The British journal of surgery. 2013;100(6):808-18.
68. Rodgers MS, McCall JL. Surgery for colorectal liver metastases with hepatic lymph node involvement: a systematic review. The British journal of surgery. 2000;87(9):1142-55.
69. Aloia T, Sebagh M, Plasse M, Karam V, Levi F, Giacchetti S, et al. Liver histology and surgical outcomes after preoperative chemotherapy with fluorouracil plus oxaliplatin in colorectal cancer liver metastases. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2006;24(31):4983-90.
70. Simmonds PC, Primrose JN, Colquitt JL, Garden OJ, Poston GJ, Rees M. Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. British journal of cancer. 2006;94(7):982-99.
71. Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, et al. Trends in long-term survival following liver resection for hepatic colorectal metastases. Annals of surgery. 2002;235(6):759-66.
72. Brouquet A, Abdalla EK, Kopetz S, Garrett CR, Overman MJ, Eng C, et al. High survival rate after two-stage resection of advanced colorectal liver metastases: response-based selection and complete resection define outcome. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2011;29(8):1083-90.
73. House MG, Ito H, Gonen M, Fong Y, Allen PJ, DeMatteo RP, et al. Survival after hepatic resection for metastatic colorectal cancer: trends in outcomes for 1,600 patients during two decades at a single institution. Journal of the American College of Surgeons. 2010;210(5):744-52, 52-5.
74. Robertson DJ, Stukel TA, Gottlieb DJ, Sutherland JM, Fisher ES. Survival after hepatic resection of colorectal cancer metastases: a national experience. Cancer. 2009;115(4):752-9.
75. Stang A, Fischbach R, Teichmann W, Bokemeyer C, Braumann D. A systematic review on the clinical benefit and role of radiofrequency ablation as treatment of colorectal liver metastases. European journal of cancer. 2009;45(10):1748-56.
76. Gleisner AL, Choti MA, Assumpcao L, Nathan H, Schulick RD, Pawlik TM. Colorectal liver metastases: recurrence and survival following hepatic resection, radiofrequency ablation, and combined resection-radiofrequency ablation. Archives of surgery (Chicago, Ill : 1960). 2008;143(12):1204-12.
77. Correa-Gallego C, Fong Y, Gonen M, D'Angelica MI, Allen PJ, DeMatteo RP, et al. A retrospective comparison of microwave ablation vs. radiofrequency ablation for colorectal cancer hepatic metastases. Annals of surgical oncology. 2014;21(13):4278-83.
78. Bala MM, Riemsma RP, Wolff R, Kleijnen J. Microwave coagulation for liver metastases. The Cochrane database of systematic reviews. 2013;10:CD010163.
79. Hur H, Ko YT, Min BS, Kim KS, Choi JS, Sohn SK, et al. Comparative study of resection and radiofrequency ablation in the treatment of solitary colorectal liver metastases. American journal of surgery. 2009;197(6):728-36.
80. Mulier S, Ni Y, Jamart J, Ruers T, Marchal G, Michel L. Local recurrence after hepatic radiofrequency coagulation: multivariate meta-analysis and review of contributing factors. Annals of surgery. 2005;242(2):158-71.
81. Leung U, Kuk D, D'Angelica MI, Kingham TP, Allen PJ, DeMatteo RP, et al. Long-term outcomes following microwave ablation for liver malignancies. The British journal of surgery. 2015;102(1):85-91.
82. Gillams A, Goldberg N, Ahmed M, Bale R, Breen D, Callstrom M, et al. Thermal ablation of colorectal liver metastases: a position paper by an international panel of ablation experts, the interventional oncology sans frontieres meeting 2013. European radiology. 2015.
83. Townsend A, Price T, Karapetis C. Selective internal radiation therapy for liver metastases from colorectal cancer. The Cochrane database of systematic reviews. 2009(4):CD007045.
84. van Hazel GA, Heinemann V, Sharma NK, Findlay MPN, Ricke J, Peeters M, et al. SIRFLOX: Randomized Phase III Trial Comparing First-Line mFOLFOX6 (Plus or Minus Bevacizumab) Versus mFOLFOX6 (Plus or Minus Bevacizumab) Plus Selective Internal Radiation Therapy in Patients With Metastatic Colorectal Cancer. Journal of Clinical Oncology. 2016;34(15):1723-31.
85. Townsend AR, Chong LC, Karapetis C, Price TJ. Selective internal radiation therapy for liver metastases from colorectal cancer. Cancer treatment reviews. 2016;50:148-54.
86. Dutton SJ, Kenealy N, Love SB, Wasan HS, Sharma RA. FOXFIRE protocol: an open-label, randomised, phase III trial of 5-fluorouracil, oxaliplatin and folinic acid (OxMdG) with or without interventional Selective Internal Radiation Therapy (SIRT) as first-line treatment for patients with unresectable liver-only or liver-dominant metastatic colorectal cancer. BMC Cancer. 2014;14(1):497.
87. Nordlinger B, Sorbye H, Glimelius B, Poston GJ, Schlag PM, Rougier P, 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):1007-16.
88. Nordlinger B, Sorbye H, Glimelius B, Poston GJ, Schlag PM, Rougier P, et al. Perioperative FOLFOX4 chemotherapy and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC 40983): long-term results of a randomised, controlled, phase 3 trial. The Lancet Oncology. 2013;14(12):1208-15.
89. Adam R, Avisar E, Ariche A, Giachetti S, Azoulay D, Castaing D, et al. Five-year survival following hepatic resection after neoadjuvant therapy for nonresectable colorectal. Annals of surgical oncology. 2001;8(4):347-53.
90. Beppu T, Sakamoto Y, Hayashi H, Baba H. Perioperative chemotherapy and hepatic resection for resectable colorectal liver metastases. Hepatobiliary surgery and nutrition. 2015;4(1):72-5.
91. Vauthey JN, Pawlik TM, Ribero D, Wu TT, Zorzi D, Hoff PM, et al. Chemotherapy regimen predicts steatohepatitis and an increase in 90-day mortality after surgery for hepatic colorectal metastases. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2006;24(13):2065-72.
92. Rubbia-Brandt L, Audard V, Sartoretti P, Roth AD, Brezault C, Le Charpentier M, et al. Severe hepatic sinusoidal obstruction associated with oxaliplatin-based chemotherapy in patients with metastatic colorectal cancer. Annals of oncology : official journal of the European Society for Medical Oncology / ESMO. 2004;15(3):460-6.
93. Welsh FK, Tilney HS, Tekkis PP, John TG, Rees M. Safe liver resection following chemotherapy for colorectal metastases is a matter of timing. British journal of cancer. 2007;96(7):1037-42.
94. Mitry E, Fields AL, Bleiberg H, Labianca R, Portier G, Tu D, et al. Adjuvant chemotherapy after potentially curative resection of metastases from colorectal cancer: a pooled analysis of two randomized trials. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2008;26(30):4906-11.
95. Portier G, Elias D, Bouche O, Rougier P, Bosset JF, Saric J, et al. Multicenter randomized trial of adjuvant fluorouracil and folinic acid compared with surgery alone after resection of colorectal liver metastases: FFCD ACHBTH AURC 9002 trial. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2006;24(31):4976-82.
96. Brandi G, De Lorenzo S, Nannini M, Curti S, Ottone M, Dall'Olio FG, et al. Adjuvant chemotherapy for resected colorectal cancer metastases: Literature review and meta-analysis. World journal of gastroenterology. 2016;22(2):519-33.
97. Ychou M, Hohenberger W, Thezenas S, Navarro M, Maurel J, Bokemeyer C, et al. A randomized phase III study comparing adjuvant 5-fluorouracil/folinic acid with FOLFIRI in patients following complete resection of liver metastases from colorectal cancer. Annals of oncology : official journal of the European Society for Medical Oncology / ESMO. 2009;20(12):1964-70.
98. Masi G, Loupakis F, Pollina L, Vasile E, Cupini S, Ricci S, et al. Long-term outcome of initially unresectable metastatic colorectal cancer patients treated with 5-fluorouracil/leucovorin, oxaliplatin, and irinotecan (FOLFOXIRI) followed by radical surgery of metastases. Annals of surgery. 2009;249(3):420-5.
99. Venook AP, Niedzwiecki D, Lenz H-J, Innocenti F, Mahoney MR, O'Neil BH, et al. CALGB/SWOG 80405: Phase III trial of irinotecan/5-FU/leucovorin (FOLFIRI) or oxaliplatin/5-FU/leucovorin (mFOLFOX6) with bevacizumab (BV) or cetuximab (CET) for patients (pts) with KRAS wild-type (wt) untreated metastatic adenocarcinoma of the colon or rectum (MCRC). Journal of Clinical Oncology. 2014;32(15_suppl):LBA3-LBA.
100. Heinemann V, von Weikersthal LF, Decker T, Kiani A, Vehling-Kaiser U, Al-Batran S-E, et al. FOLFIRI plus cetuximab versus FOLFIRI plus bevacizumab as first-line treatment for patients with metastatic colorectal cancer (FIRE-3): a randomised, open-label, phase 3 trial. The Lancet Oncology.15(10):1065-75.
101. Peeters M, Price TJ, Cervantes A, Sobrero AF, Ducreux M, Hotko Y, et al. Randomized phase III study of panitumumab with fluorouracil, leucovorin, and irinotecan (FOLFIRI) compared with FOLFIRI alone as second-line treatment in patients with metastatic colorectal cancer. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2010;28(31):4706-13.
102. Haraldsdottir S, Wu C, Bloomston M, Goldberg RM. What is the optimal neo-adjuvant treatment for liver metastasis? Therapeutic advances in medical oncology. 2013;5(4):221-34.
103. Adam R, Delvart V, Pascal G, Valeanu A, Castaing D, Azoulay D, et al. Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Annals of surgery. 2004;240(4):644-57; discussion 57-8.
104. Nelson R, Freels S. Hepatic artery adjuvant chemotherapy for patients having resection or ablation of colorectal cancer metastatic to the liver. The Cochrane database of systematic reviews. 2006(4):CD003770.
105. Cattell RB. Successful removal of liver metastasis from a carcinoma of the rectum. Lahey Clin Bull. 1940;2(7).