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Liver-Directed and Systemic Therapies for Colorectal Cancer Liver Metastases

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References

  1. 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.

  2. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30.

    Article  PubMed  Google Scholar 

  3. 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.

    Article  PubMed  Google Scholar 

  4. Tarraga Lopez PJ, Albero JS, Rodriguez-Montes JA. Primary and secondary prevention of colorectal cancer. Clin Med Insights Gastroenterol. 2014;7:33–46.

    PubMed  PubMed Central  Google Scholar 

  5. 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.

    Article  PubMed  Google Scholar 

  6. Pitroda SP, et al. Integrated molecular subtyping defines a curable oligometastatic state in colorectal liver metastasis. Nat Commun. 2018;9(1):1793.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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.

    Article  CAS  PubMed  Google Scholar 

  8. Tan C, Du X. KRAS mutation testing in metastatic colorectal cancer. World J Gastroenterol. 2012;18(37):5171–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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.

    PubMed  PubMed Central  Google Scholar 

  13. Nojadeh JN, Behrouz Sharif S, Sakhinia E. Microsatellite instability in colorectal cancer. EXCLI J. 2018;17:159–68.

    PubMed  PubMed Central  Google Scholar 

  14. 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.

    Article  PubMed Central  Google Scholar 

  15. 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.

    Article  PubMed  Google Scholar 

  16. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 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.

    Article  PubMed  Google Scholar 

  18. 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.

    Article  PubMed  Google Scholar 

  19. 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.

    Article  PubMed  Google Scholar 

  20. 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.

    Article  PubMed  Google Scholar 

  21. Bipat S, et al. Colorectal liver metastases: CT, MR imaging, and PET for diagnosis—meta-analysis. Radiology. 2005;237(1):123–31.

    Article  PubMed  Google Scholar 

  22. 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.

    Article  PubMed  Google Scholar 

  23. Kulemann V, et al. Preoperative detection of colorectal liver metastases in fatty liver: MDCT or MRI? Eur J Radiol. 2011;79(2):e1–6.

    Article  PubMed  Google Scholar 

  24. Yoo HJ, Lee JS, Lee JM. Integrated whole body MR/PET: where are we? Korean J Radiol. 2015;16(1):32–49.

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  26. 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.

    Article  CAS  PubMed  Google Scholar 

  27. Cameron J, Andrew C. Current surgical therapy. E-book 12 ed. Philadelphia: Elsevier Health Sciences; 2016.

    Google Scholar 

  28. Adam R, Vinet E. Regional treatment of metastasis: surgery of colorectal liver metastases. Ann Oncol. 2004;15(Suppl 4):iv103–6.

    PubMed  Google Scholar 

  29. Parkin DM, et al. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55(2):74–108.

    Article  PubMed  Google Scholar 

  30. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Andre T, et al. Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N Engl J Med. 2004;350(23):2343–51.

    Article  CAS  PubMed  Google Scholar 

  32. 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.

    Article  CAS  PubMed  Google Scholar 

  33. 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.

    PubMed  Google Scholar 

  34. 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.

    CAS  PubMed  Google Scholar 

  35. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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.

    Article  CAS  PubMed  Google Scholar 

  37. 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.

    Article  CAS  PubMed  Google Scholar 

  38. 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.

    CAS  PubMed  Google Scholar 

  39. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Beppu T, et al. FOLFOX enables high resectability and excellent prognosis for initially unresectable colorectal liver metastases. Anticancer Res. 2010;30(3):1015–20.

    CAS  PubMed  Google Scholar 

  41. 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.

    Article  PubMed  Google Scholar 

  42. 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.

    Article  CAS  PubMed  Google Scholar 

  43. Van Cutsem E, et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med. 2009;360(14):1408–17.

    Article  PubMed  Google Scholar 

  44. 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.

    Article  CAS  PubMed  Google Scholar 

  45. 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.

    Article  CAS  PubMed  Google Scholar 

  46. 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.

    Article  PubMed  Google Scholar 

  47. 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.

    Article  CAS  PubMed  Google Scholar 

  48. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  49. 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.

    Article  PubMed  Google Scholar 

  50. 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.

    Article  CAS  PubMed  Google Scholar 

  51. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  52. 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.

    Google Scholar 

  53. 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.

    Article  PubMed  Google Scholar 

  54. 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.

    Article  CAS  PubMed  Google Scholar 

  55. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. 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).

  57. 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.

    Article  CAS  PubMed  Google Scholar 

  58. 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.

    Article  CAS  PubMed  Google Scholar 

  59. 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.

    Article  CAS  PubMed  Google Scholar 

  60. 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.

    Article  CAS  PubMed  Google Scholar 

  61. 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.

    Article  CAS  PubMed  Google Scholar 

  62. 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.

    Article  CAS  PubMed  Google Scholar 

  63. 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.

    Article  PubMed  Google Scholar 

  64. 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.

    Article  CAS  PubMed  Google Scholar 

  65. 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.

    Article  CAS  PubMed  Google Scholar 

  66. 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.

    Article  CAS  PubMed  Google Scholar 

  67. Mayer RJ, et al. Randomized trial of TAS-102 for refractory metastatic colorectal cancer. N Engl J Med. 2015;372(20):1909–19.

    Article  PubMed  Google Scholar 

  68. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Le DT, et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015;372(26):2509–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 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).

  71. 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).

  72. Van Cutsem E, et al. ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol. 2016;27(8):1386–422.

    Article  PubMed  Google Scholar 

  73. Maher B, et al. The management of colorectal liver metastases. Clin Radiol. 2017;72(8):617–25.

    Article  CAS  PubMed  Google Scholar 

  74. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  75. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. 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.

    Article  PubMed  Google Scholar 

  77. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. 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.

    Article  PubMed  Google Scholar 

  79. 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.

    PubMed  Google Scholar 

  80. 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.

    PubMed  Google Scholar 

  81. Wang DS, Louie JD, Sze DY. Intra-arterial therapies for metastatic colorectal cancer. Semin Intervent Radiol. 2013;30(1):12–20.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Gillams AR, Lees WR. Radio-frequency ablation of colorectal liver metastases in 167 patients. Eur Radiol. 2004;14(12):2261–7.

    Article  CAS  PubMed  Google Scholar 

  83. 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.

    Article  PubMed  Google Scholar 

  84. 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.

    Article  PubMed  Google Scholar 

  85. 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.

    Article  CAS  PubMed  Google Scholar 

  86. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  87. 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.

    Article  PubMed  Google Scholar 

  88. Shibata T, et al. Microwave coagulation therapy for multiple hepatic metastases from colorectal carcinoma. Cancer. 2000;89(2):276–84.

    Article  CAS  PubMed  Google Scholar 

  89. 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.

    Article  PubMed  Google Scholar 

  90. Liang P, et al. Prognostic factors for percutaneous microwave coagulation therapy of hepatic metastases. AJR Am J Roentgenol. 2003;181(5):1319–25.

    Article  PubMed  Google Scholar 

  91. 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.

    Article  PubMed  Google Scholar 

  92. 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.

    Article  PubMed  Google Scholar 

  93. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  94. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. 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.

    Article  CAS  PubMed  Google Scholar 

  96. Lyu T, et al. Irreversible electroporation in primary and metastatic hepatic malignancies: a review. Medicine (Baltimore). 2017;96(17):e6386.

    Article  Google Scholar 

  97. Scheffer HJ, et al. Irreversible electroporation for colorectal liver metastases. Tech Vasc Interv Radiol. 2015;18(3):159–69.

    Article  PubMed  Google Scholar 

  98. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Weng M, et al. Radiofrequency ablation versus resection for colorectal cancer liver metastases: a meta-analysis. PLoS ONE. 2012;7(9):e45493.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. 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.

    Article  PubMed  Google Scholar 

  101. Pathak S, et al. Ablative therapies for colorectal liver metastases: a systematic review. Colorectal Dis. 2011;13(9):e252–65.

    Article  CAS  PubMed  Google Scholar 

  102. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Petre EN, et al. Treatment of pulmonary colorectal metastases by radiofrequency ablation. Clin Colorectal Cancer. 2013;12(1):37–44.

    Article  PubMed  Google Scholar 

  104. 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.

    Article  PubMed  Google Scholar 

  105. Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology. 2005;42(5):1208–36.

    Article  PubMed  Google Scholar 

  106. 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.

    Article  PubMed  Google Scholar 

  107. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  108. 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.

    Article  PubMed  Google Scholar 

  109. 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.

    Article  PubMed  Google Scholar 

  110. 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.

    Article  PubMed  Google Scholar 

  111. 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.

    Article  PubMed  Google Scholar 

  112. 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.

    Article  CAS  PubMed  Google Scholar 

  113. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  114. 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.

    Article  PubMed  Google Scholar 

  115. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  116. 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.

    Article  PubMed  Google Scholar 

  117. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  118. 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.

    Article  CAS  PubMed  Google Scholar 

  119. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  120. 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.

    Article  PubMed  Google Scholar 

  121. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  122. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  123. 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.

    Article  PubMed  Google Scholar 

  124. 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.

    PubMed  Google Scholar 

  125. 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.

    Article  PubMed  Google Scholar 

  126. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  127. 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.

    CAS  PubMed  Google Scholar 

  128. 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.

    Article  PubMed  Google Scholar 

  129. 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.

    Article  PubMed  Google Scholar 

  130. 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.

    CAS  PubMed  Google Scholar 

  131. Albert M, et al. Chemoembolization of colorectal liver metastases with cisplatin, doxorubicin, mitomycin C, ethiodol, and polyvinyl alcohol. Cancer. 2011;117(2):343–52.

    Article  CAS  PubMed  Google Scholar 

  132. Vogl TJ, et al. Regional chemotherapy of the lung: transpulmonary chemoembolization in malignant lung tumors. Semin Intervent Radiol. 2013;30(2):176–84.

    Article  PubMed  PubMed Central  Google Scholar 

  133. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  134. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  135. Boas FE, Bodei L, Sofocleous CT. Radioembolization of colorectal liver metastases: indications, technique, and outcomes. J Nucl Med. 2017;58(Suppl 2):104s–11s.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. 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.

    Article  PubMed  Google Scholar 

  137. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  138. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  139. Braat A, et al. Adequate SIRT activity dose is as important as adequate chemotherapy dose. Lancet Oncol. 2017;18(11):e636.

    Article  PubMed  Google Scholar 

  140. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Khajornjiraphan N, Thu NA, Chow PK. Yttrium-90 microspheres: a review of its emerging clinical indications. Liver Cancer. 2015;4(1):6–15.

    Article  CAS  PubMed  Google Scholar 

  143. Murray D, McEwan AJ. Radiobiology of systemic radiation therapy. Cancer Biother Radiopharm. 2007;22(1):1–23.

    Article  CAS  PubMed  Google Scholar 

  144. 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.

    Article  CAS  PubMed  Google Scholar 

  145. 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.

    Article  PubMed  Google Scholar 

  146. 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.

    Article  CAS  PubMed  Google Scholar 

  147. 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.

    Article  CAS  PubMed  Google Scholar 

  148. 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.

    Article  CAS  PubMed  Google Scholar 

  149. 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.

    Article  CAS  PubMed  Google Scholar 

  150. 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.

    Article  CAS  PubMed  Google Scholar 

  151. 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.

    Article  CAS  PubMed  Google Scholar 

  152. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Puippe G, Pfammatter T, Schaefer N. Arterial therapies of non-colorectal liver metastases. Viszeralmedizin. 2015;31(6):414–22.

    PubMed  PubMed Central  Google Scholar 

  155. Fan KY, et al. Neuroendocrine tumor liver metastases treated with yttrium-90 radioembolization. Contemp Clin Trials. 2016;50:143–9.

    Article  PubMed  Google Scholar 

  156. Gordon AC, Salem R, Lewandowski RJ. Yttrium-90 radioembolization for breast cancer liver metastases. J Vasc Interv Radiol. 2016;27(9):1316–9.

    Article  PubMed  Google Scholar 

  157. 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.

    Article  PubMed  Google Scholar 

  158. 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.

    Article  PubMed  Google Scholar 

  159. Burrill J, Hafeli U, Liu DM. Advances in radioembolization—embolics and isotopes. Nucl Med Radiat Ther. 2011;2:107.

    Google Scholar 

  160. Piana PM, et al. Early arterial stasis during resin-based yttrium-90 radioembolization: incidence and preliminary outcomes. HPB (Oxford). 2014;16(4):336–41.

    Article  Google Scholar 

  161. 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.

    Article  PubMed  Google Scholar 

  162. 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.

    Article  PubMed  Google Scholar 

  163. 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.

    Article  CAS  PubMed  Google Scholar 

  164. 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.

    Article  CAS  PubMed  Google Scholar 

  165. 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.

    Article  PubMed  Google Scholar 

  166. 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.

    Article  PubMed  Google Scholar 

  167. Song JE, Kim DY. Conventional vs drug-eluting beads transarterial chemoembolization for hepatocellular carcinoma. World J Hepatol. 2017;9(18):808–14.

    Article  PubMed  PubMed Central  Google Scholar 

  168. 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.

    Article  CAS  PubMed  Google Scholar 

  169. Levy EB, et al. First human experience with directly image-able iodinated embolization microbeads. Cardiovasc Intervent Radiol. 2016;39(8):1177–86.

    Article  PubMed  PubMed Central  Google Scholar 

  170. 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.

    Article  CAS  PubMed  Google Scholar 

  171. 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.

    Article  CAS  PubMed  Google Scholar 

  172. 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.

    Article  PubMed  Google Scholar 

  173. 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.

    Article  CAS  PubMed  Google Scholar 

  174. 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.

    Article  PubMed  Google Scholar 

  175. 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.

    Article  PubMed  Google Scholar 

  176. 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.

    Article  PubMed  Google Scholar 

  177. Ahmed M, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria—a 10-year update. Radiology. 2014;273(1):241–60.

    Article  PubMed  Google Scholar 

  178. 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.

    Article  PubMed  Google Scholar 

  179. Padia SA, et al. Radioembolization of hepatic malignancies: background, quality improvement guidelines, and future directions. J Vasc Interv Radiol. 2017;28(1):1–15.

    Article  PubMed  Google Scholar 

  180. Gaba RC, et al. Transcatheter therapy for hepatic malignancy: standardization of terminology and reporting criteria. J Vasc Interv Radiol. 2016;27(4):457–73.

    Article  PubMed  Google Scholar 

  181. Kemeny NE, Gonen M. Hepatic arterial infusion after liver resection. N Engl J Med. 2005;352(7):734–5.

    Article  CAS  PubMed  Google Scholar 

  182. 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.

    Article  PubMed  Google Scholar 

  183. 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.

    Article  CAS  PubMed  Google Scholar 

  184. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  185. 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.

    Article  CAS  PubMed  Google Scholar 

  186. 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.

    Article  PubMed  Google Scholar 

  187. 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.

    Article  CAS  PubMed  Google Scholar 

  188. 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.

    Article  PubMed  Google Scholar 

  189. 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.

    Article  PubMed  Google Scholar 

  190. 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.

    PubMed  Google Scholar 

  191. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  192. 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.

    Article  PubMed  Google Scholar 

  193. 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.

    Article  Google Scholar 

  194. 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.

    Article  Google Scholar 

  195. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Broughton G 2nd, Janis JE, Attinger CE. Wound healing: an overview. Plast Reconstr Surg. 2006;117(7 Suppl):1–32e-S.

    Google Scholar 

  197. 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.

    Article  CAS  PubMed  Google Scholar 

  198. 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.

    Article  PubMed  Google Scholar 

  199. 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.

    Article  PubMed  Google Scholar 

  200. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  201. Takahashi Y, et al. Immunological effect of local ablation combined with immunotherapy on solid malignancies. Chin J Cancer. 2017;36(1):49.

    Article  PubMed  PubMed Central  Google Scholar 

  202. Slovak R, et al. Immuno-thermal ablations—boosting the anticancer immune response. J Immunother Cancer. 2017;5(1):78.

    Article  PubMed  PubMed Central  Google Scholar 

  203. Lemdani K, et al. Improvement of immune response after radiofrequency ablation in colorectal cancer. J Clin Oncol. 2018;36(5_suppl):102.

    Article  Google Scholar 

  204. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  205. 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.

    Article  CAS  PubMed  Google Scholar 

  206. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  207. Haen SP, et al. More than just tumor destruction: immunomodulation by thermal ablation of cancer. Clin Dev Immunol. 2011;2011:160250.

    Article  PubMed  PubMed Central  Google Scholar 

  208. Fagnoni FF, et al. Combination of radiofrequency ablation and immunotherapy. Front Biosci. 2008;13:369–81.

    Article  CAS  PubMed  Google Scholar 

  209. 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.

    Article  CAS  Google Scholar 

  210. den Brok MH, et al. Saponin-based adjuvants induce cross-presentation in dendritic cells by intracellular lipid body formation. Nat Commun. 2016;7:13324.

    Article  CAS  Google Scholar 

  211. 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.

    Article  PubMed  Google Scholar 

  212. 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.

    Article  CAS  PubMed  Google Scholar 

  213. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. 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.

    CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Constantinos T. Sofocleous.

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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.

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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

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