This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
National Cancer Institute Surveillance Epidemiology and End Results Program. Cancer stat facts: colon and rectum cancer. https://seer.cancer.gov/statfacts/html/colorect.html. Accessed May 17, 2018.
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30.
Ghiringhelli F, et al. Epidemiology and prognosis of synchronous and metachronous colon cancer metastases: a French population-based study. Dig Liver Dis. 2014;46(9):854–8.
Tarraga Lopez PJ, Albero JS, Rodriguez-Montes JA. Primary and secondary prevention of colorectal cancer. Clin Med Insights Gastroenterol. 2014;7:33–46.
Lee MS, Menter DG, Kopetz S. Right versus left colon cancer biology: integrating the consensus molecular subtypes. J Natl Compr Canc Netw. 2017;15(3):411–9.
Pitroda SP, et al. Integrated molecular subtyping defines a curable oligometastatic state in colorectal liver metastasis. Nat Commun. 2018;9(1):1793.
Pollock CB, et al. Oncogenic K-RAS is required to maintain changes in cytoskeletal organization, adhesion, and motility in colon cancer cells. Cancer Res. 2005;65(4):1244–50.
Tan C, Du X. KRAS mutation testing in metastatic colorectal cancer. World J Gastroenterol. 2012;18(37):5171–80.
Brudvik KW, et al. RAS mutation predicts positive resection margins and narrower resection margins in patients undergoing resection of colorectal liver metastases. Ann Surg Oncol. 2016;23(8):2635–43.
Odisio BC, et al. Local tumour progression after percutaneous ablation of colorectal liver metastases according to RAS mutation status. Br J Surg. 2017;104(6):760–8.
Shady W, et al. Kras mutation is a marker of worse oncologic outcomes after percutaneous radiofrequency ablation of colorectal liver metastases. Oncotarget. 2017;8(39):66117–27.
Clarke CN, Kopetz ES. BRAF mutant colorectal cancer as a distinct subset of colorectal cancer: clinical characteristics, clinical behavior, and response to targeted therapies. J Gastrointest Oncol. 2015;6(6):660–7.
Nojadeh JN, Behrouz Sharif S, Sakhinia E. Microsatellite instability in colorectal cancer. EXCLI J. 2018;17:159–68.
Ruers T, et al. Local treatment of unresectable colorectal liver metastases: results of a randomized phase II trial. J Natl Cancer Inst. 2017;109(9):djx015.
Creasy JM, et al. Actual 10-year survival after hepatic resection of colorectal liver metastases: what factors preclude cure? Surgery. 2018;163(6):1238–44.
Fong Y, et al. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230(3):309–18 discussion 318–21.
Shady W, et al. Percutaneous microwave versus radiofrequency ablation of colorectal liver metastases: ablation with clear margins (A0) provides the best local tumor control. J Vasc Interv Radiol. 2018;29(2):268–275.e1.
Shady W, et al. Percutaneous radiofrequency ablation of colorectal cancer liver metastases: factors affecting outcomes—a 10-year experience at a single center. Radiology. 2016;278(2):601–11.
Sotirchos VS, et al. Colorectal cancer liver metastases: biopsy of the ablation zone and margins can be used to predict oncologic outcome. Radiology. 2016;280(3):949–59.
Kurilova I, et al. Factors affecting oncologic outcomes of 90Y radioembolization of heavily pre-treated patients with colon cancer liver metastases. Clin Colorectal Cancer. 2019;18(1):8–18.
Bipat S, et al. Colorectal liver metastases: CT, MR imaging, and PET for diagnosis—meta-analysis. Radiology. 2005;237(1):123–31.
Floriani I, et al. Performance of imaging modalities in diagnosis of liver metastases from colorectal cancer: a systematic review and meta-analysis. J Magn Reson Imaging. 2010;31(1):19–31.
Kulemann V, et al. Preoperative detection of colorectal liver metastases in fatty liver: MDCT or MRI? Eur J Radiol. 2011;79(2):e1–6.
Yoo HJ, Lee JS, Lee JM. Integrated whole body MR/PET: where are we? Korean J Radiol. 2015;16(1):32–49.
Dietrich CF, et al. Assessment of metastatic liver disease in patients with primary extrahepatic tumors by contrast-enhanced sonography versus CT and MRI. World J Gastroenterol. 2006;12(11):1699–705.
Benson AB 3rd, et al. Colon cancer, version 1.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2017;15(3):370–98.
Cameron J, Andrew C. Current surgical therapy. E-book 12 ed. Philadelphia: Elsevier Health Sciences; 2016.
Adam R, Vinet E. Regional treatment of metastasis: surgery of colorectal liver metastases. Ann Oncol. 2004;15(Suppl 4):iv103–6.
Parkin DM, et al. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55(2):74–108.
Kemeny NE, et al. Updated long-term survival for patients with metastatic colorectal cancer treated with liver resection followed by hepatic arterial infusion and systemic chemotherapy. J Surg Oncol. 2016;113(5):477–84.
Andre T, et al. Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N Engl J Med. 2004;350(23):2343–51.
Kemeny N, et al. Hepatic arterial infusion of chemotherapy after resection of hepatic metastases from colorectal cancer. N Engl J Med. 1999;341(27):2039–48.
Kemeny MM, et al. Combined-modality treatment for resectable metastatic colorectal carcinoma to the liver: surgical resection of hepatic metastases in combination with continuous infusion of chemotherapy—an intergroup study. J Clin Oncol. 2002;20(6):1499–505.
Lygidakis NJ, et al. Metastatic liver disease of colorectal origin: the value of locoregional immunochemotherapy combined with systemic chemotherapy following liver resection. Results of a prospective randomized study. Hepatogastroenterology. 2001;48(42):1685–91.
Lorenz M, et al. Randomized trial of surgery versus surgery followed by adjuvant hepatic arterial infusion with 5-fluorouracil and folinic acid for liver metastases of colorectal cancer. German Cooperative on Liver Metastases (Arbeitsgruppe Lebermetastasen). Ann Surg. 1998;228(6):756–62.
Kemeny N, et al. Hepatic arterial infusion of floxuridine and dexamethasone plus high-dose Mitomycin C for patients with unresectable hepatic metastases from colorectal carcinoma. J Surg Oncol. 2005;91(2):97–101.
Ducreux M, et al. Hepatic arterial oxaliplatin infusion plus intravenous chemotherapy in colorectal cancer with inoperable hepatic metastases: a trial of the gastrointestinal group of the Federation Nationale des Centres de Lutte Contre le Cancer. J Clin Oncol. 2005;23(22):4881–7.
Chen Y, et al. Hepatic arterial infusion with irinotecan, oxaliplatin, and floxuridine plus systemic chemotherapy as first-line treatment of unresectable liver metastases from colorectal cancer. Onkologie. 2012;35(9):480–4.
Nordlinger B, 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.
Beppu T, et al. FOLFOX enables high resectability and excellent prognosis for initially unresectable colorectal liver metastases. Anticancer Res. 2010;30(3):1015–20.
Uetake H, et al. A multicenter phase II trial of mFOLFOX6 plus bevacizumab to treat liver-only metastases of colorectal cancer that are unsuitable for upfront resection (TRICC0808). Ann Surg Oncol. 2015;22(3):908–15.
Primrose J, et al. Systemic chemotherapy with or without cetuximab in patients with resectable colorectal liver metastasis: the New EPOC randomised controlled trial. Lancet Oncol. 2014;15(6):601–11.
Van Cutsem E, et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med. 2009;360(14):1408–17.
Bokemeyer C, et al. Fluorouracil, leucovorin, and oxaliplatin with and without cetuximab in the first-line treatment of metastatic colorectal cancer. J Clin Oncol. 2009;27(5):663–71.
Falcone A, et al. Phase III trial of infusional fluorouracil, leucovorin, oxaliplatin, and irinotecan (FOLFOXIRI) compared with infusional fluorouracil, leucovorin, and irinotecan (FOLFIRI) as first-line treatment for metastatic colorectal cancer: the Gruppo Oncologico Nord Ovest. J Clin Oncol. 2007;25(13):1670–6.
Masi G, 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. Ann Surg. 2009;249(3):420–5.
Cremolini C, et al. Efficacy of FOLFOXIRI plus bevacizumab in liver-limited metastatic colorectal cancer: a pooled analysis of clinical studies by Gruppo Oncologico del Nord Ovest. Eur J Cancer. 2017;73:74–84.
Tomasello G, et al. FOLFOXIRI plus bevacizumab as conversion therapy for patients with initially unresectable metastatic colorectal cancer: a systematic review and pooled analysis. JAMA Oncol. 2017;3(7):e170278.
D’Angelica MI, et al. Phase II trial of hepatic artery infusional and systemic chemotherapy for patients with unresectable hepatic metastases from colorectal cancer: conversion to resection and long-term outcomes. Ann Surg. 2015;261(2):353–60.
Pak LM, et al. Prospective phase II trial of combination hepatic artery infusion and systemic chemotherapy for unresectable colorectal liver metastases: long term results and curative potential. J Surg Oncol. 2018;117(4):634–43.
Shah JL, et al. Neoadjuvant transarterial radiation lobectomy for colorectal hepatic metastases: a small cohort analysis on safety, efficacy, and radiopathologic correlation. J Gastrointest Oncol. 2017;8(3):E43–e51.
Jones RP, et al. Neoadjuvant treatment of colorectal liver metastases (CRLM) with drug eluting beads trans-arterial chemoembolization (DEBIRI-TACE): a multi-institute phase II study in resectable metastases. J Clin Oncol. 2012;30(15_suppl):3613.
Livraghi T, et al. Percutaneous radiofrequency ablation of liver metastases in potential candidates for resection: the “test-of-time approach”. Cancer. 2003;97(12):3027–35.
Tournigand C, et al. FOLFIRI followed by FOLFOX6 or the reverse sequence in advanced colorectal cancer: a randomized GERCOR study. J Clin Oncol. 2004;22(2):229–37.
Venook AP, et al. Effect of first-line chemotherapy combined with cetuximab or bevacizumab on overall survival in patients with KRAS wild-type advanced or metastatic colorectal cancer: a randomized clinical trial. JAMA. 2017;317(23):2392–401.
Venook AP, Niedzwiecki D, Innocenti F, et al. Impact of primary (1°) tumor location on overall survival (OS) and progression-free survival (PFS) in patients (pts) with metastatic colorectal cancer (mCRC): analysis of CALGB/SWOG 80405 (alliance). J Clin Oncol. 2016; 34, 2016 (suppl; abstr 3504).
Hecht JR, et al. A randomized phase IIIB trial of chemotherapy, bevacizumab, and panitumumab compared with chemotherapy and bevacizumab alone for metastatic colorectal cancer. J Clin Oncol. 2009;27(5):672–80.
Tol J, et al. A randomised phase III study on capecitabine, oxaliplatin and bevacizumab with or without cetuximab in first-line advanced colorectal cancer, the CAIRO2 study of the Dutch Colorectal Cancer Group (DCCG). An interim analysis of toxicity. Ann Oncol. 2008;19(4):734–8.
Douillard JY, et al. Randomized, phase III trial of panitumumab with infusional fluorouracil, leucovorin, and oxaliplatin (FOLFOX4) versus FOLFOX4 alone as first-line treatment in patients with previously untreated metastatic colorectal cancer: the PRIME study. J Clin Oncol. 2010;28(31):4697–705.
Peeters M, 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. J Clin Oncol. 2010;28(31):4706–13.
Yamada Y, et al. Leucovorin, fluorouracil, and oxaliplatin plus bevacizumab versus S-1 and oxaliplatin plus bevacizumab in patients with metastatic colorectal cancer (SOFT): an open-label, non-inferiority, randomised phase 3 trial. Lancet Oncol. 2013;14(13):1278–86.
Muro K, et al. Irinotecan plus S-1 (IRIS) versus fluorouracil and folinic acid plus irinotecan (FOLFIRI) as second-line chemotherapy for metastatic colorectal cancer: a randomised phase 2/3 non-inferiority study (FIRIS study). Lancet Oncol. 2010;11(9):853–60.
Van Cutsem E, et al. Aflibercept plus FOLFIRI vs. placebo plus FOLFIRI in second-line metastatic colorectal cancer: a post hoc analysis of survival from the phase III VELOUR study subsequent to exclusion of patients who had recurrence during or within 6 months of completing adjuvant oxaliplatin-based therapy. Target Oncol. 2016;11(3):383–400.
Folprecht G, et al. Oxaliplatin and 5-FU/folinic acid (modified FOLFOX6) with or without aflibercept in first-line treatment of patients with metastatic colorectal cancer: the AFFIRM study. Ann Oncol. 2016;27(7):1273–9.
Tabernero J, et al. Ramucirumab versus placebo in combination with second-line FOLFIRI in patients with metastatic colorectal carcinoma that progressed during or after first-line therapy with bevacizumab, oxaliplatin, and a fluoropyrimidine (RAISE): a randomised, double-blind, multicentre, phase 3 study. Lancet Oncol. 2015;16(5):499–508.
Grothey A, et al. Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet. 2013;381(9863):303–12.
Mayer RJ, et al. Randomized trial of TAS-102 for refractory metastatic colorectal cancer. N Engl J Med. 2015;372(20):1909–19.
Cercek A, et al. Response rates of hepatic arterial infusion pump therapy in patients with metastatic colorectal cancer liver metastases refractory to all standard chemotherapies. J Surg Oncol. 2016;114(6):655–63.
Le DT, et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015;372(26):2509–20.
Le DT, Uram J, Wang H, et al. Programmed death-1 blockade in mismatch repair deficient colorectal cancer (abstract). J Clin Oncol. 2016; 34, 2016 (suppl; abstr 103).
Overman MJ, Kopetz S, McDermott RS, et al. Nivolumab ± ipilimumab in treatment (tx) of patients (pts) with metastatic colorectal cancer (mCRC) with and without high microsatellite instability (MSI-H): CheckMate-142 interim results (abstract). J Clin Oncol. 2016; 34, 2016 (suppl; abstr 3501).
Van Cutsem E, et al. ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol. 2016;27(8):1386–422.
Maher B, et al. The management of colorectal liver metastases. Clin Radiol. 2017;72(8):617–25.
Gillams A, 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. Eur Radiol. 2015;25(12):3438–54.
Wasan HS, et al. First-line selective internal radiotherapy plus chemotherapy versus chemotherapy alone in patients with liver metastases from colorectal cancer (FOXFIRE, SIRFLOX, and FOXFIRE-Global): a combined analysis of three multicentre, randomised, phase 3 trials. Lancet Oncol. 2017;18(9):1159–71.
Yamakado K, et al. Radiofrequency ablation combined with hepatic arterial chemoembolization using degradable starch microsphere mixed with Mitomycin C for the treatment of liver metastasis from colorectal cancer: a prospective multicenter study. Cardiovasc Intervent Radiol. 2017;40(4):560–7.
Wu ZB, et al. Percutaneous microwave ablation combined with synchronous transcatheter arterial chemoembolization for the treatment of colorectal liver metastases: results from a follow-up cohort. Onco Targets Ther. 2016;9:3783–9.
Vogl TJ, et al. Survival of patients with non-resectable, chemotherapy-resistant colorectal cancer liver metastases undergoing conventional lipiodol-based transarterial chemoembolization (cTACE) palliatively versus neoadjuvantly prior to percutaneous thermal ablation. Eur J Radiol. 2018;102:138–45.
Ishikawa T, et al. Multiple liver metastases due to sigmoid colon cancer successfully treated by degradable starch microspheres (DSM)-TAE, radiofrequency ablation therapy, and Uzel/UFT. Gan To Kagaku Ryoho. 2010;37(2):335–8.
Fong ZV, et al. Combined hepatic arterial embolization and hepatic ablation for unresectable colorectal metastases to the liver. Am Surg. 2012;78(11):1243–8.
Wang DS, Louie JD, Sze DY. Intra-arterial therapies for metastatic colorectal cancer. Semin Intervent Radiol. 2013;30(1):12–20.
Gillams AR, Lees WR. Radio-frequency ablation of colorectal liver metastases in 167 patients. Eur Radiol. 2004;14(12):2261–7.
Siperstein AE, et al. Survival after radiofrequency ablation of colorectal liver metastases: 10-year experience. Ann Surg. 2007;246(4):559–65 discussion 565-7.
Veltri A, et al. Radiofrequency ablation of colorectal liver metastases: small size favorably predicts technique effectiveness and survival. Cardiovasc Intervent Radiol. 2008;31(5):948–56.
Gillams AR, Lees WR. Five-year survival in 309 patients with colorectal liver metastases treated with radiofrequency ablation. Eur Radiol. 2009;19(5):1206–13.
Sofocleous CT, et al. CT-guided radiofrequency ablation as a salvage treatment of colorectal cancer hepatic metastases developing after hepatectomy. J Vasc Interv Radiol. 2011;22(6):755–61.
Solbiati L, et al. Small liver colorectal metastases treated with percutaneous radiofrequency ablation: local response rate and long-term survival with up to 10-year follow-up. Radiology. 2012;265(3):958–68.
Shibata T, et al. Microwave coagulation therapy for multiple hepatic metastases from colorectal carcinoma. Cancer. 2000;89(2):276–84.
Tanaka K, et al. Outcome after hepatic resection versus combined resection and microwave ablation for multiple bilobar colorectal metastases to the liver. Surgery. 2006;139(2):263–73.
Liang P, et al. Prognostic factors for percutaneous microwave coagulation therapy of hepatic metastases. AJR Am J Roentgenol. 2003;181(5):1319–25.
Shyn PB, et al. Percutaneous imaging-guided cryoablation of liver tumors: predicting local progression on 24-hour MRI. AJR Am J Roentgenol. 2014;203(2):W181–91.
Vogl TJ, et al. Thermal ablation of liver metastases from colorectal cancer: radiofrequency, microwave and laser ablation therapies. Radiol Med. 2014;119(7):451–61.
Sartori S, et al. Laser ablation of liver tumors: an ancillary technique, or an alternative to radiofrequency and microwave? World J Radiol. 2017;9(3):91–6.
Sartori S, Tombesi P, Di Vece F. Thermal ablation in colorectal liver metastases: lack of evidence or lack of capability to prove the evidence? World J Gastroenterol. 2016;22(13):3511–5.
Park MY, et al. Preliminary experience using high intensity focused ultrasound for treating liver metastasis from colon and stomach cancer. Int J Hyperthermia. 2009;25(3):180–8.
Lyu T, et al. Irreversible electroporation in primary and metastatic hepatic malignancies: a review. Medicine (Baltimore). 2017;96(17):e6386.
Scheffer HJ, et al. Irreversible electroporation for colorectal liver metastases. Tech Vasc Interv Radiol. 2015;18(3):159–69.
Schoellhammer HF, et al. Colorectal liver metastases: making the unresectable resectable using irreversible electroporation for microscopic positive margins—a case report. BMC Cancer. 2015;15:271.
Weng M, et al. Radiofrequency ablation versus resection for colorectal cancer liver metastases: a meta-analysis. PLoS ONE. 2012;7(9):e45493.
Mulier S, et al. Radiofrequency ablation versus resection for resectable colorectal liver metastases: time for a randomized trial? An update. Dig Surg. 2008;25(6):445–60.
Pathak S, et al. Ablative therapies for colorectal liver metastases: a systematic review. Colorectal Dis. 2011;13(9):e252–65.
Ruers T, et al. Radiofrequency ablation combined with systemic treatment versus systemic treatment alone in patients with non-resectable colorectal liver metastases: a randomized EORTC Intergroup phase II study (EORTC 40004). Ann Oncol. 2012;23(10):2619–26.
Petre EN, et al. Treatment of pulmonary colorectal metastases by radiofrequency ablation. Clin Colorectal Cancer. 2013;12(1):37–44.
Mouli SK, et al. The role of percutaneous image-guided thermal ablation for the treatment of pulmonary malignancies. AJR Am J Roentgenol. 2017;209(4):740–51.
Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology. 2005;42(5):1208–36.
Kudo M, Okanoue T. Management of hepatocellular carcinoma in Japan: consensus-based clinical practice manual proposed by the Japan Society of Hepatology. Oncology. 2007;72(Suppl 1):2–15.
Omata M, et al. Asian Pacific Association for the Study of the Liver consensus recommendations on hepatocellular carcinoma. Hepatol Int. 2010;4(2):439–74.
Ayav A, et al. Radiofrequency ablation of unresectable liver tumors: factors associated with incomplete ablation or local recurrence. Am J Surg. 2010;200(4):435–9.
Amersi FF, et al. Long-term survival after radiofrequency ablation of complex unresectable liver tumors. Arch Surg. 2006;141(6):581–7 discussion 587-8.
Veenendaal LM, Borel Rinkes IH, van Hillegersberg R. Multipolar radiofrequency ablation of large hepatic metastases of endocrine tumours. Eur J Gastroenterol Hepatol. 2006;18(1):89–92.
Hur H, et al. Comparative study of resection and radiofrequency ablation in the treatment of solitary colorectal liver metastases. Am J Surg. 2009;197(6):728–36.
Kim YS, et al. Intrahepatic recurrence after percutaneous radiofrequency ablation of hepatocellular carcinoma: analysis of the pattern and risk factors. Eur J Radiol. 2006;59(3):432–41.
Mulier S, et al. Local recurrence after hepatic radiofrequency coagulation: multivariate meta-analysis and review of contributing factors. Ann Surg. 2005;242(2):158–71.
Lee WS, et al. Clinical outcomes of hepatic resection and radiofrequency ablation in patients with solitary colorectal liver metastasis. J Clin Gastroenterol. 2008;42(8):945–9.
Van Tilborg AA, et al. Long-term results of radiofrequency ablation for unresectable colorectal liver metastases: a potentially curative intervention. Br J Radiol. 2011;84(1002):556–65.
Berber E, Pelley R, Siperstein AE. Predictors of survival after radiofrequency thermal ablation of colorectal cancer metastases to the liver: a prospective study. J Clin Oncol. 2005;23(7):1358–64.
Abdalla EK, et al. Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg. 2004;239(6):818–25 discussion 825-7.
Wang X, et al. Margin size is an independent predictor of local tumor progression after ablation of colon cancer liver metastases. Cardiovasc Intervent Radiol. 2013;36(1):166–75.
Ryan ER, et al. Split-dose technique for FDG PET/CT-guided percutaneous ablation: a method to facilitate lesion targeting and to provide immediate assessment of treatment effectiveness. Radiology. 2013;268(1):288–95.
Sofocleous CT, et al. Histopathologic and immunohistochemical features of tissue adherent to multitined electrodes after RF ablation of liver malignancies can help predict local tumor progression: initial results. Radiology. 2008;249(1):364–74.
Puijk RS, et al. Colorectal liver metastases: surgery versus thermal ablation (COLLISION)—a phase III single-blind prospective randomized controlled trial. BMC Cancer. 2018;18(1):821.
Correa-Gallego C, et al. A retrospective comparison of microwave ablation vs. radiofrequency ablation for colorectal cancer hepatic metastases. Ann Surg Oncol. 2014;21(13):4278–83.
Qian GJ, et al. Efficacy of microwave versus radiofrequency ablation for treatment of small hepatocellular carcinoma: experimental and clinical studies. Eur Radiol. 2012;22(9):1983–90.
Di Vece F, et al. Coagulation areas produced by cool-tip radiofrequency ablation and microwave ablation using a device to decrease back-heating effects: a prospective pilot study. Cardiovasc Intervent Radiol. 2014;37(3):723–9.
Cavagnaro M, et al. A minimally invasive antenna for microwave ablation therapies: design, performances, and experimental assessment. IEEE Trans Biomed Eng. 2011;58(4):949–59.
Sag AA, Selcukbiricik F, Mandel NM. Evidence-based medical oncology and interventional radiology paradigms for liver-dominant colorectal cancer metastases. World J Gastroenterol. 2016;22(11):3127–49.
Aliberti C, et al. Trans-arterial chemoembolization of metastatic colorectal carcinoma to the liver adopting DC Bead(R), drug-eluting bead loaded with irinotecan: results of a phase II clinical study. Anticancer Res. 2011;31(12):4581–7.
Martin RC, et al. Hepatic intra-arterial injection of drug-eluting bead, irinotecan (DEBIRI) in unresectable colorectal liver metastases refractory to systemic chemotherapy: results of multi-institutional study. Ann Surg Oncol. 2011;18(1):192–8.
Iezzi R, et al. Trans-arterial chemoembolization with irinotecan-loaded drug-eluting beads (DEBIRI) and capecitabine in refractory liver prevalent colorectal metastases: a phase II single-center study. Cardiovasc Intervent Radiol. 2015;38(6):1523–31.
Fiorentini G, et al. Intra-arterial infusion of irinotecan-loaded drug-eluting beads (DEBIRI) versus intravenous therapy (FOLFIRI) for hepatic metastases from colorectal cancer: final results of a phase III study. Anticancer Res. 2012;32(4):1387–95.
Albert M, et al. Chemoembolization of colorectal liver metastases with cisplatin, doxorubicin, mitomycin C, ethiodol, and polyvinyl alcohol. Cancer. 2011;117(2):343–52.
Vogl TJ, et al. Regional chemotherapy of the lung: transpulmonary chemoembolization in malignant lung tumors. Semin Intervent Radiol. 2013;30(2):176–84.
Sofocleous CT, et al. Radioembolization as a salvage therapy for heavily pretreated patients with colorectal cancer liver metastases: factors that affect outcomes. Clin Colorectal Cancer. 2015;14(4):296–305.
Shady W, et al. Metabolic tumor volume and total lesion glycolysis on FDG-PET/CT can predict overall survival after (90)Y radioembolization of colorectal liver metastases: a comparison with SUVmax, SUVpeak, and RECIST 1.0. Eur J Radiol. 2016;85(6):1224–31.
Boas FE, Bodei L, Sofocleous CT. Radioembolization of colorectal liver metastases: indications, technique, and outcomes. J Nucl Med. 2017;58(Suppl 2):104s–11s.
Sofocleous CT, et al. Phase I trial of selective internal radiation therapy for chemorefractory colorectal cancer liver metastases progressing after hepatic arterial pump and systemic chemotherapy. Clin Colorectal Cancer. 2014;13(1):27–36.
Sotirchos VS, et al. Safe and successful Yttrium-90 resin microsphere radioembolization in a heavily pretreated patient with chemorefractory colorectal liver metastases after biliary stent placement above the papilla. Case Reports Hepatol. 2014;2014:921406.
Ziv E, et al. PI3K pathway mutations are associated with longer time to local progression after radioembolization of colorectal liver metastases. Oncotarget. 2017;8(14):23529–38.
Braat A, et al. Adequate SIRT activity dose is as important as adequate chemotherapy dose. Lancet Oncol. 2017;18(11):e636.
Dutton SJ, et al. 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;14:497.
Gibbs P, et al. Selective Internal Radiation Therapy (SIRT) with yttrium-90 resin microspheres plus standard systemic chemotherapy regimen of FOLFOX versus FOLFOX alone as first-line treatment of non-resectable liver metastases from colorectal cancer: the SIRFLOX study. BMC Cancer. 2014;14:897.
Khajornjiraphan N, Thu NA, Chow PK. Yttrium-90 microspheres: a review of its emerging clinical indications. Liver Cancer. 2015;4(1):6–15.
Murray D, McEwan AJ. Radiobiology of systemic radiation therapy. Cancer Biother Radiopharm. 2007;22(1):1–23.
Campbell AM, Bailey IH, Burton MA. Analysis of the distribution of intra-arterial microspheres in human liver following hepatic yttrium-90 microsphere therapy. Phys Med Biol. 2000;45(4):1023–33.
Kennedy A, et al. Recommendations for radioembolization of hepatic malignancies using yttrium-90 microsphere brachytherapy: a consensus panel report from the radioembolization brachytherapy oncology consortium. Int J Radiat Oncol Biol Phys. 2007;68(1):13–23.
Hendlisz A, et al. Phase III trial comparing protracted intravenous fluorouracil infusion alone or with yttrium-90 resin microspheres radioembolization for liver-limited metastatic colorectal cancer refractory to standard chemotherapy. J Clin Oncol. 2010;28(23):3687–94.
Van Hazel G, et al. Randomised phase 2 trial of SIR-Spheres plus fluorouracil/leucovorin chemotherapy versus fluorouracil/leucovorin chemotherapy alone in advanced colorectal cancer. J Surg Oncol. 2004;88(2):78–85.
Gray B, et al. Randomised trial of SIR-Spheres plus chemotherapy vs. chemotherapy alone for treating patients with liver metastases from primary large bowel cancer. Ann Oncol. 2001;12(12):1711–20.
Kennedy AS, et al. Pathologic response and microdosimetry of (90)Y microspheres in man: review of four explanted whole livers. Int J Radiat Oncol Biol Phys. 2004;60(5):1552–63.
Sharma RA, et al. Radioembolization of liver metastases from colorectal cancer using yttrium-90 microspheres with concomitant systemic oxaliplatin, fluorouracil, and leucovorin chemotherapy. J Clin Oncol. 2007;25(9):1099–106.
Vente MA, et al. Yttrium-90 microsphere radioembolization for the treatment of liver malignancies: a structured meta-analysis. Eur Radiol. 2009;19(4):951–9.
Cosimelli M, et al. Multi-centre phase II clinical trial of yttrium-90 resin microspheres alone in unresectable, chemotherapy refractory colorectal liver metastases. Br J Cancer. 2010;103(3):324–31.
Kurilova I, et al. (90)Y resin microspheres radioembolization for colon cancer liver metastases using full-strength contrast material. Cardiovasc Intervent Radiol. 2018;41(9):1419–27.
Puippe G, Pfammatter T, Schaefer N. Arterial therapies of non-colorectal liver metastases. Viszeralmedizin. 2015;31(6):414–22.
Fan KY, et al. Neuroendocrine tumor liver metastases treated with yttrium-90 radioembolization. Contemp Clin Trials. 2016;50:143–9.
Gordon AC, Salem R, Lewandowski RJ. Yttrium-90 radioembolization for breast cancer liver metastases. J Vasc Interv Radiol. 2016;27(9):1316–9.
Bester L, et al. Radioembolisation with Yttrium-90 microspheres: an effective treatment modality for unresectable liver metastases. J Med Imaging Radiat Oncol. 2013;57(1):72–80.
Seidensticker R, et al. Matched-pair comparison of radioembolization plus best supportive care versus best supportive care alone for chemotherapy refractory liver-dominant colorectal metastases. Cardiovasc Intervent Radiol. 2012;35(5):1066–73.
Burrill J, Hafeli U, Liu DM. Advances in radioembolization—embolics and isotopes. Nucl Med Radiat Ther. 2011;2:107.
Piana PM, et al. Early arterial stasis during resin-based yttrium-90 radioembolization: incidence and preliminary outcomes. HPB (Oxford). 2014;16(4):336–41.
Murthy R, et al. Yttrium 90 resin microspheres for the treatment of unresectable colorectal hepatic metastases after failure of multiple chemotherapy regimens: preliminary results. J Vasc Interv Radiol. 2005;16(7):937–45.
Chao C, et al. Effect of substituting 50% isovue for sterile water as the delivery medium for SIR-spheres: improved dose delivery and decreased incidence of stasis. Clin Nucl Med. 2017;42(3):176–9.
Prince JF, et al. Efficacy of radioembolization with (166)Ho-microspheres in salvage patients with liver metastases: a phase 2 study. J Nucl Med. 2018;59(4):582–8.
van Hazel GA, 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. J Clin Oncol. 2016;34(15):1723–31.
Gibbs P, et al. Effect of primary tumor side on survival outcomes in untreated patients with metastatic colorectal cancer when selective internal radiation therapy is added to chemotherapy: combined analysis of two randomized controlled studies. Clin Colorectal Cancer. 2018;17(4):e617–29.
Richardson AJ, Laurence JM, Lam VW. Transarterial chemoembolization with irinotecan beads in the treatment of colorectal liver metastases: systematic review. J Vasc Interv Radiol. 2013;24(8):1209–17.
Song JE, Kim DY. Conventional vs drug-eluting beads transarterial chemoembolization for hepatocellular carcinoma. World J Hepatol. 2017;9(18):808–14.
Jones RP, et al. PARAGON II—a single arm multicentre phase II study of neoadjuvant therapy using irinotecan bead in patients with resectable liver metastases from colorectal cancer. Eur J Surg Oncol. 2016;42(12):1866–72.
Levy EB, et al. First human experience with directly image-able iodinated embolization microbeads. Cardiovasc Intervent Radiol. 2016;39(8):1177–86.
Caine M, et al. Comparison of microsphere penetration with LC Bead LUMI versus other commercial microspheres. J Mech Behav Biomed Mater. 2018;78:46–55.
Yoshino T, et al. Pan-Asian adapted ESMO consensus guidelines for the management of patients with metastatic colorectal cancer: a JSMO–ESMO initiative endorsed by CSCO, KACO, MOS, SSO and TOS. Ann Oncol. 2018;29(1):44–70.
Lahti SJ, et al. KRAS status as an independent prognostic factor for survival after Yttrium-90 radioembolization therapy for unresectable colorectal cancer liver metastases. J Vasc Interv Radiol. 2015;26(8):1102–11.
Janowski E, et al. Yttrium-90 radioembolization for colorectal cancer liver metastases in KRAS wild-type and mutant patients: clinical and ccfDNA studies. Oncol Rep. 2017;37(1):57–65.
Calandri M, et al. Ablation of colorectal liver metastasis: interaction of ablation margins and RAS mutation profiling on local tumour progression-free survival. Eur Radiol. 2018;28(7):2727–34.
Reimer RP, Reimer P, Mahnken AH. Assessment of therapy response to transarterial radioembolization for liver metastases by means of post-treatment MRI-based texture analysis. Cardiovasc Intervent Radiol. 2018;41(10):1545–56.
Letzen B, Wang CJ, Chapiro J. The role of artificial intelligence in interventional oncology: a primer. J Vasc Interv Radiol. 2019;30(1):38–41.e1.
Ahmed M, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria—a 10-year update. Radiology. 2014;273(1):241–60.
Gaba RC, et al. Quality improvement guidelines for transarterial chemoembolization and embolization of hepatic malignancy. J Vasc Interv Radiol. 2017;28(9):1210–1223.e3.
Padia SA, et al. Radioembolization of hepatic malignancies: background, quality improvement guidelines, and future directions. J Vasc Interv Radiol. 2017;28(1):1–15.
Gaba RC, et al. Transcatheter therapy for hepatic malignancy: standardization of terminology and reporting criteria. J Vasc Interv Radiol. 2016;27(4):457–73.
Kemeny NE, Gonen M. Hepatic arterial infusion after liver resection. N Engl J Med. 2005;352(7):734–5.
Clavien PA, et al. Downstaging of hepatocellular carcinoma and liver metastases from colorectal cancer by selective intra-arterial chemotherapy. Surgery. 2002;131(4):433–42.
Kemeny N, et al. Phase I trial of systemic oxaliplatin combination chemotherapy with hepatic arterial infusion in patients with unresectable liver metastases from colorectal cancer. J Clin Oncol. 2005;23(22):4888–96.
Kemeny NE, et al. Conversion to resectability using hepatic artery infusion plus systemic chemotherapy for the treatment of unresectable liver metastases from colorectal carcinoma. J Clin Oncol. 2009;27(21):3465–71.
Gallagher DJ, et al. Hepatic arterial infusion plus systemic irinotecan in patients with unresectable hepatic metastases from colorectal cancer previously treated with systemic oxaliplatin: a retrospective analysis. Ann Oncol. 2007;18(12):1995–9.
Goere D, et al. Prolonged survival of initially unresectable hepatic colorectal cancer patients treated with hepatic arterial infusion of oxaliplatin followed by radical surgery of metastases. Ann Surg. 2010;251(4):686–91.
Levi FA, et al. Conversion to resection of liver metastases from colorectal cancer with hepatic artery infusion of combined chemotherapy and systemic cetuximab in multicenter trial OPTILIV. Ann Oncol. 2016;27(2):267–74.
Cercek A, et al. Floxuridine hepatic arterial infusion associated biliary toxicity is increased by concurrent administration of systemic bevacizumab. Ann Surg Oncol. 2014;21(2):479–86.
Xu C, et al. Radiofrequency ablation for liver metastases after transarterial chemoembolization: a systemic analysis. Asian Pac J Cancer Prev. 2015;16(12):5101–6.
Bloomston M, et al. Transcatheter arterial chemoembolization with or without radiofrequency ablation in the management of patients with advanced hepatic malignancy. Am Surg. 2002;68(9):827–31.
Meiers C, et al. Safety and initial efficacy of radiation segmentectomy for the treatment of hepatic metastases. J Gastrointest Oncol. 2018;9(2):311–5.
Vouche M, et al. Unresectable solitary hepatocellular carcinoma not amenable to radiofrequency ablation: multicenter radiology-pathology correlation and survival of radiation segmentectomy. Hepatology. 2014;60(1):192–201.
Teo JY, et al. A systematic review of contralateral liver lobe hypertrophy after unilobar selective internal radiation therapy with Y90. HPB (Oxford). 2016;18(1):7–12.
Fernandez-Ros N, et al. Partial liver volume radioembolization induces hypertrophy in the spared hemiliver and no major signs of portal hypertension. HPB (Oxford). 2014;16(3):243–9.
Marabelle A, et al. Starting the fight in the tumor: expert recommendations for the development of human intratumoral immunotherapy (HIT-IT). Ann Oncol. 2018;29(11):2163–74.
Broughton G 2nd, Janis JE, Attinger CE. Wound healing: an overview. Plast Reconstr Surg. 2006;117(7 Suppl):1–32e-S.
Li LY, et al. Prospective comparison of five mediators of the systemic response after high-intensity focused ultrasound and targeted cryoablation for localized prostate cancer. BJU Int. 2009;104(8):1063–7.
Schell SR, et al. Pro- and antiinflammatory cytokine production after radiofrequency ablation of unresectable hepatic tumors. J Am Coll Surg. 2002;195(6):774–81.
de Jong KP, et al. Serum response of hepatocyte growth factor, insulin-like growth factor-I, interleukin-6, and acute phase proteins in patients with colorectal liver metastases treated with partial hepatectomy or cryosurgery. J Hepatol. 2001;34(3):422–7.
Erinjeri JP, et al. Image-guided thermal ablation of tumors increases the plasma level of interleukin-6 and interleukin-10. J Vasc Interv Radiol. 2013;24(8):1105–12.
Takahashi Y, et al. Immunological effect of local ablation combined with immunotherapy on solid malignancies. Chin J Cancer. 2017;36(1):49.
Slovak R, et al. Immuno-thermal ablations—boosting the anticancer immune response. J Immunother Cancer. 2017;5(1):78.
Lemdani K, et al. Improvement of immune response after radiofrequency ablation in colorectal cancer. J Clin Oncol. 2018;36(5_suppl):102.
Katz SC, et al. Phase I hepatic immunotherapy for metastases study of intra-arterial chimeric antigen receptor-modified T-cell therapy for CEA + liver metastases. Clin Cancer Res. 2015;21(14):3149–59.
Fong Y, et al. A herpes oncolytic virus can be delivered via the vasculature to produce biologic changes in human colorectal cancer. Mol Ther. 2009;17(2):389–94.
Mehta A, Oklu R, Sheth RA. Thermal ablative therapies and immune checkpoint modulation: can locoregional approaches effect a systemic response? Gastroenterol Res Pract. 2016;2016:9251375.
Haen SP, et al. More than just tumor destruction: immunomodulation by thermal ablation of cancer. Clin Dev Immunol. 2011;2011:160250.
Fagnoni FF, et al. Combination of radiofrequency ablation and immunotherapy. Front Biosci. 2008;13:369–81.
den Brok MH, et al. Saponin-based adjuvants create a highly effective anti-tumor vaccine when combined with in situ tumor destruction. Vaccine. 2012;30(4):737–44.
den Brok MH, et al. Saponin-based adjuvants induce cross-presentation in dendritic cells by intracellular lipid body formation. Nat Commun. 2016;7:13324.
van den Bijgaart RJ, et al. Thermal and mechanical high-intensity focused ultrasound: perspectives on tumor ablation, immune effects and combination strategies. Cancer Immunol Immunother. 2017;66(2):247–58.
Nierkens S, et al. In vivo colocalization of antigen and CpG [corrected] within dendritic cells is associated with the efficacy of cancer immunotherapy. Cancer Res. 2008;68(13):5390–6.
Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883–99.
Trikha M, et al. Targeted anti-interleukin-6 monoclonal antibody therapy for cancer: a review of the rationale and clinical evidence. Clin Cancer Res. 2003;9(13):4653–65.
Conflict of interest
Authors Jia Li, Ieva Kurilova and Juan C Camacho declare that they have no conflict of interest. Nancy Kemeny received research fund from Amgen. Constantinos T. Sofocleous declares Research Support: Ethicon J&J, BTG, Consultant/Advisory Board: Terumo, Ethicon J&J, GE.
This article does not contain any studies with human participants or animals performed by any of the authors.
Consent for Publication
Consent for publication was obtained for every individual person’s data included in the study.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Kemeny, N., Kurilova, I., Li, J. et al. Liver-Directed and Systemic Therapies for Colorectal Cancer Liver Metastases. Cardiovasc Intervent Radiol 42, 1240–1254 (2019). https://doi.org/10.1007/s00270-019-02284-9