Advertisement

Colorectal Cancer Liver Metastases

Multimodal Therapy
  • Berk Aykut
    Affiliations
    Department of Surgery, Division of Surgical Oncology, Duke University Medical Center, Box 3966, 10 Bryan Searle Drive, 466G Seeley G. Mudd Building, Durham, NC 27710, USA
    Search for articles by this author
  • Michael E. Lidsky
    Correspondence
    Corresponding author.
    Affiliations
    Department of Surgery, Division of Surgical Oncology, Duke University Medical Center, Box 3966, 10 Bryan Searle Drive, 466G Seeley G. Mudd Building, Durham, NC 27710, USA
    Search for articles by this author
Published:November 03, 2022DOI:https://doi.org/10.1016/j.soc.2022.07.009

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribers receive full online access to your subscription and archive of back issues up to and including 2002.

      Content published before 2002 is available via pay-per-view purchase only.

      Subscribe:

      Subscribe to Surgical Oncology Clinics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Siegel R.L.
        • Miller K.D.
        • Goding Sauer A.
        • et al.
        Colorectal cancer statistics, 2020.
        CA Cancer J Clin. 2020; 70: 145-164https://doi.org/10.3322/caac.21601
        • Dekker E.
        • Tanis P.J.
        • Vleugels J.L.A.
        • et al.
        Colorectal cancer.
        Lancet. 2019; 394: 1467-1480https://doi.org/10.1016/S0140-6736(19)32319-0
        • Kneuertz P.J.
        • Chang G.J.
        • Hu C.Y.
        • et al.
        Overtreatment of young adults with colon cancer: more intense treatments with unmatched survival gains.
        JAMA Surg. 2015; 150: 402-409https://doi.org/10.1001/jamasurg.2014.3572
        • Liang J.T.
        • Huang K.C.
        • Cheng A.L.
        • et al.
        Clinicopathological and molecular biological features of colorectal cancer in patients less than 40 years of age.
        Br J Surg. 2003; 90: 205-214https://doi.org/10.1002/bjs.4015
        • Siegel R.L.
        • Torre L.A.
        • Soerjomataram I.
        • et al.
        Global patterns and trends in colorectal cancer incidence in young adults.
        Gut. 2019; 68: 2179-2185https://doi.org/10.1136/gutjnl-2019-319511
        • Lieu C.H.
        • Renfro L.A.
        • de Gramont A.
        • et al.
        Association of age with survival in patients with metastatic colorectal cancer: analysis from the ARCAD Clinical Trials Program.
        J Clin Oncol. 2014; 32: 2975-2984https://doi.org/10.1200/JCO.2013.54.9329
        • Nitsche U.
        • Stogbauer F.
        • Spath C.
        • et al.
        Right Sided Colon Cancer as a Distinct Histopathological Subtype with Reduced Prognosis.
        Dig Surg. 2016; 33: 157-163https://doi.org/10.1159/000443644
        • Gervaz P.
        • Bucher P.
        • Morel P.
        Two colons-two cancers: paradigm shift and clinical implications.
        J Surg Oncol. 2004; 88: 261-266https://doi.org/10.1002/jso.20156
        • Yahagi M.
        • Okabayashi K.
        • Hasegawa H.
        • et al.
        The Worse Prognosis of Right-Sided Compared with Left-Sided Colon Cancers: a Systematic Review and Meta-analysis.
        J Gastrointest Surg. 2016; 20: 648-655https://doi.org/10.1007/s11605-015-3026-6
        • Brule S.Y.
        • Jonker D.J.
        • Karapetis C.S.
        • et al.
        Location of colon cancer (right-sided versus left-sided) as a prognostic factor and a predictor of benefit from cetuximab in NCIC CO.17.
        Eur J Cancer. 2015; 51: 1405-1414https://doi.org/10.1016/j.ejca.2015.03.015
        • Engstrand J.
        • Nilsson H.
        • Stromberg C.
        • et al.
        Colorectal cancer liver metastases - a population-based study on incidence, management and survival.
        BMC Cancer. 2018; 18: 78https://doi.org/10.1186/s12885-017-3925-x
        • Petrelli F.
        • Tomasello G.
        • Borgonovo K.
        • et al.
        Prognostic Survival Associated With Left-Sided vs Right-Sided Colon Cancer: A Systematic Review and Meta-analysis.
        JAMA Oncol. 2017; 3: 211-219https://doi.org/10.1001/jamaoncol.2016.4227
        • Vayrynen V.
        • Wirta E.V.
        • Seppala T.
        • et al.
        Incidence and management of patients with colorectal cancer and synchronous and metachronous colorectal metastases: a population-based study.
        BJS Open. 2020; 4: 685-692https://doi.org/10.1002/bjs5.50299
        • Andres A.
        • Mentha G.
        • Adam R.
        • et al.
        Surgical management of patients with colorectal cancer and simultaneous liver and lung metastases.
        Br J Surg. 2015; 102: 691-699https://doi.org/10.1002/bjs.9783
        • Wagner J.S.
        • Adson M.A.
        • Van Heerden J.A.
        • et al.
        The natural history of hepatic metastases from colorectal cancer. A comparison with resective treatment.
        Ann Surg. 1984; 199: 502-508https://doi.org/10.1097/00000658-198405000-00002
        • Nordlinger B.
        • Guiguet M.
        • Vaillant J.C.
        • et al.
        Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Assoc Francaise de Chirurgie.
        Cancer. 1996; 77: 1254-1262
        • Garden O.J.
        • Rees M.
        • Poston G.J.
        • et al.
        Guidelines for resection of colorectal cancer liver metastases.
        Gut. 2006; 55: 1-8https://doi.org/10.1136/gut.2006.098053
        • Hekimoglu K.
        • Ustundag Y.
        • Dusak A.
        • et al.
        Small colorectal liver metastases: detection with SPIO-enhanced MRI in comparison with gadobenate dimeglumine-enhanced MRI and CT imaging.
        Eur J Radiol. 2011; 77: 468-472https://doi.org/10.1016/j.ejrad.2009.09.002
        • Sahani D.V.
        • Bajwa M.A.
        • Andrabi Y.
        • et al.
        Current status of imaging and emerging techniques to evaluate liver metastases from colorectal carcinoma.
        Ann Surg. 2014; 259: 861-872https://doi.org/10.1097/SLA.0000000000000525
        • Muhi A.
        • Ichikawa T.
        • Motosugi U.
        • et al.
        Diagnosis of colorectal hepatic metastases: comparison of contrast-enhanced CT, contrast-enhanced US, superparamagnetic iron oxide-enhanced MRI, and gadoxetic acid-enhanced MRI.
        J Magn Reson Imaging. 2011; 34: 326-335https://doi.org/10.1002/jmri.22613
        • Gorgec B.
        • Hansen I.
        • Kemmerich G.
        • et al.
        Clinical added value of MRI to CT in patients scheduled for local therapy of colorectal liver metastases (CAMINO): study protocol for an international multicentre prospective diagnostic accuracy study.
        BMC Cancer. 2021; 21: 1116https://doi.org/10.1186/s12885-021-08833-1
        • Creasy J.M.
        • Sadot E.
        • Koerkamp B.G.
        • et al.
        Actual 10-year survival after hepatic resection of colorectal liver metastases: what factors preclude cure?.
        Surgery. 2018; 163: 1238-1244https://doi.org/10.1016/j.surg.2018.01.004
        • Fong Y.
        • Fortner J.
        • Sun R.L.
        • et al.
        Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases.
        Ann Surg. 1999; 230 (; discussion 318-21): 309-318https://doi.org/10.1097/00000658-199909000-00004
        • Mann C.D.
        • Metcalfe M.S.
        • Leopardi L.N.
        • et al.
        The clinical risk score: emerging as a reliable preoperative prognostic index in hepatectomy for colorectal metastases.
        Arch Surg. 2004; 139: 1168-1172https://doi.org/10.1001/archsurg.139.11.1168
        • Nagashima I.
        • Takada T.
        • Adachi M.
        • et al.
        Proposal of criteria to select candidates with colorectal liver metastases for hepatic resection: comparison of our scoring system to the positive number of risk factors.
        World J Gastroenterol. 2006; 12: 6305-6309https://doi.org/10.3748/wjg.v12.i39.6305
        • Konopke R.
        • Kersting S.
        • Distler M.
        • et al.
        Prognostic factors and evaluation of a clinical score for predicting survival after resection of colorectal liver metastases.
        Liver Int. 2009; 29: 89-102https://doi.org/10.1111/j.1478-3231.2008.01845.x
        • Vega E.A.
        • Salehi O.
        • Nicolaescu D.
        • et al.
        Correction to: Failure to Cure Patients with Colorectal Liver Metastases: The Impact of the Liver Surgeon.
        Ann Surg Oncol. 2021; 28: 879https://doi.org/10.1245/s10434-021-10185-w
        • Akita H.
        • Sasaki Y.
        • Yamada T.
        • et al.
        Real-time intraoperative assessment of residual liver functional reserve using pulse dye densitometry.
        World J Surg. 2008; 32: 2668-2674https://doi.org/10.1007/s00268-008-9752-0
        • Kauffmann R.
        • Fong Y.
        Post-hepatectomy liver failure.
        Hepatobiliary Surg Nutr. 2014; 3: 238-246https://doi.org/10.3978/j.issn.2304-3881.2014.09.01
        • Margonis G.A.
        • Sergentanis T.N.
        • Ntanasis-Stathopoulos I.
        • et al.
        Impact of Surgical Margin Width on Recurrence and Overall Survival Following R0 Hepatic Resection of Colorectal Metastases: A Systematic Review and Meta-analysis.
        Ann Surg. 2018; 267: 1047-1055https://doi.org/10.1097/SLA.0000000000002552
        • Pawlik T.M.
        • Scoggins C.R.
        • Zorzi D.
        • et al.
        Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases.
        Ann Surg. 2005; 241 (discussion 722-4): 715-722https://doi.org/10.1097/01.sla.0000160703.75808.7d
        • Margonis G.A.
        • Buettner S.
        • Andreatos N.
        • et al.
        Anatomical Resections Improve Disease-free Survival in Patients With KRAS-mutated Colorectal Liver Metastases.
        Ann Surg. 2017; 266: 641-649https://doi.org/10.1097/SLA.0000000000002367
        • Muratore A.
        • Ribero D.
        • Zimmitti G.
        • et al.
        Resection margin and recurrence-free survival after liver resection of colorectal metastases.
        Ann Surg Oncol. 2010; 17: 1324-1329https://doi.org/10.1245/s10434-009-0770-4
        • Matsumura M.
        • Mise Y.
        • Saiura A.
        • et al.
        Parenchymal-Sparing Hepatectomy Does Not Increase Intrahepatic Recurrence in Patients with Advanced Colorectal Liver Metastases.
        Ann Surg Oncol. 2016; 23: 3718-3726https://doi.org/10.1245/s10434-016-5278-0
        • Kingham T.P.
        • Correa-Gallego C.
        • D'Angelica M.I.
        • et al.
        Hepatic parenchymal preservation surgery: decreasing morbidity and mortality rates in 4,152 resections for malignancy.
        J Am Coll Surg. 2015; 220: 471-479https://doi.org/10.1016/j.jamcollsurg.2014.12.026
        • Deng G.
        • Li H.
        • Jia G.Q.
        • et al.
        Parenchymal-sparing versus extended hepatectomy for colorectal liver metastases: A systematic review and meta-analysis.
        Cancer Med. 2019; 8: 6165-6175https://doi.org/10.1002/cam4.2515
        • Moris D.
        • Ronnekleiv-Kelly S.
        • Rahnemai-Azar A.A.
        • et al.
        Parenchymal-Sparing Versus Anatomic Liver Resection for Colorectal Liver Metastases: a Systematic Review.
        J Gastrointest Surg. 2017; 21: 1076-1085https://doi.org/10.1007/s11605-017-3397-y
        • Matsuki R.
        • Mise Y.
        • Saiura A.
        • et al.
        Parenchymal-sparing hepatectomy for deep-placed colorectal liver metastases.
        Surgery. 2016; 160: 1256-1263https://doi.org/10.1016/j.surg.2016.06.041
        • Mise Y.
        • Aloia T.A.
        • Brudvik K.W.
        • et al.
        Parenchymal-sparing Hepatectomy in Colorectal Liver Metastasis Improves Salvageability and Survival.
        Ann Surg. 2016; 263: 146-152https://doi.org/10.1097/SLA.0000000000001194
        • Ruers T.
        • Punt C.
        • Van Coevorden F.
        • 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: 2619-2626https://doi.org/10.1093/annonc/mds053
        • Siperstein A.E.
        • Berber E.
        • Ballem N.
        • et al.
        Survival after radiofrequency ablation of colorectal liver metastases: 10-year experience.
        Ann Surg. 2007; 246 (; discussion 565-7): 559-565https://doi.org/10.1097/SLA.0b013e318155a7b6
        • Shibata T.
        • Niinobu T.
        • Ogata N.
        • et al.
        Microwave coagulation therapy for multiple hepatic metastases from colorectal carcinoma.
        Cancer. 2000; 89: 276-284
        • Cheng Y.
        • Zhang L.
        • Li H.
        • et al.
        Laparoscopic versus open liver resection for colorectal liver metastases: a systematic review.
        J Surg Res. 2017; 220: 234-246https://doi.org/10.1016/j.jss.2017.05.110
        • Syn N.L.
        • Kabir T.
        • Koh Y.X.
        • et al.
        Survival Advantage of Laparoscopic Versus Open Resection For Colorectal Liver Metastases: A Meta-analysis of Individual Patient Data From Randomized Trials and Propensity-score Matched Studies.
        Ann Surg. 2020; 272: 253-265https://doi.org/10.1097/SLA.0000000000003672
        • Fretland A.A.
        • Dagenborg V.J.
        • Bjornelv G.M.W.
        • et al.
        Laparoscopic Versus Open Resection for Colorectal Liver Metastases: The OSLO-COMET Randomized Controlled Trial.
        Ann Surg. 2018; 267: 199-207https://doi.org/10.1097/SLA.0000000000002353
        • Portier G.
        • Elias D.
        • Bouche O.
        • et al.
        Multicenter randomized trial of adjuvant fluorouracil and folinic acid compared with surgery alone after resection of colorectal liver metastases: FFCD ACHBTH AURC 9002 trial.
        J Clin Oncol. 2006; 24: 4976-4982https://doi.org/10.1200/JCO.2006.06.8353
        • Mitry E.
        • Fields A.L.
        • Bleiberg H.
        • et al.
        Adjuvant chemotherapy after potentially curative resection of metastases from colorectal cancer: a pooled analysis of two randomized trials.
        J Clin Oncol. 2008; 26: 4906-4911https://doi.org/10.1200/JCO.2008.17.3781
        • Ychou M.
        • Raoul J.L.
        • Douillard J.Y.
        • et al.
        A phase III randomised trial of LV5FU2 + irinotecan versus LV5FU2 alone in adjuvant high-risk colon cancer (FNCLCC Accord02/FFCD9802).
        Ann Oncol. 2009; 20: 674-680https://doi.org/10.1093/annonc/mdn680
        • Kanemitsu Y.
        • Shimizu Y.
        • Mizusawa J.
        • et al.
        Hepatectomy Followed by mFOLFOX6 Versus Hepatectomy Alone for Liver-Only Metastatic Colorectal Cancer (JCOG0603): A Phase II or III Randomized Controlled Trial.
        J Clin Oncol. 2021; 39: 3789-3799https://doi.org/10.1200/JCO.21.01032
        • Nordlinger B.
        • Sorbye H.
        • Glimelius 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: 1007-1016https://doi.org/10.1016/S0140-6736(08)60455-9
        • Nordlinger B.
        • Sorbye H.
        • Glimelius B.
        • et al.
        Perioperative FOLFOX4 chemotherapy and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC 40983): long-term results of a randomised, controlled, phase 3 trial.
        Lancet Oncol. 2013; 14: 1208-1215https://doi.org/10.1016/S1470-2045(13)70447-9
        • Ayez N.
        • van der Stok E.P.
        • de Wilt H.
        • et al.
        Neo-adjuvant chemotherapy followed by surgery versus surgery alone in high-risk patients with resectable colorectal liver metastases: the CHARISMA randomized multicenter clinical trial.
        BMC Cancer. 2015; 15: 180https://doi.org/10.1186/s12885-015-1199-8
        • Primrose J.
        • Falk S.
        • Finch-Jones M.
        • 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: 601-611https://doi.org/10.1016/S1470-2045(14)70105-6
        • Bridgewater J.A.
        • Pugh S.A.
        • Maishman T.
        • et al.
        Systemic chemotherapy with or without cetuximab in patients with resectable colorectal liver metastasis (New EPOC): long-term results of a multicentre, randomised, controlled, phase 3 trial.
        Lancet Oncol. 2020; 21: 398-411https://doi.org/10.1016/S1470-2045(19)30798-3
        • Breedis C.
        • Young G.
        The blood supply of neoplasms in the liver.
        Am J Pathol. 1954; 30: 969-977
        • Clarkson B.
        • Young C.
        • Dierick W.
        • et al.
        Effects of continuous hepatic artery infusion of antimetabolites on primary and metastatic cancer of the liver.
        Cancer. 1962; 15: 472-488
        • Sullivan R.D.
        • Norcross J.W.
        • Watkins Jr., E.
        Chemotherapy of Metastatic Liver Cancer by Prolonged Hepatic-Artery Infusion.
        N Engl J Med. 1964; 270: 321-327https://doi.org/10.1056/NEJM196402132700701
        • Kemeny N.
        • Huang Y.
        • Cohen A.M.
        • et al.
        Hepatic arterial infusion of chemotherapy after resection of hepatic metastases from colorectal cancer.
        N Engl J Med. 1999; 341: 2039-2048https://doi.org/10.1056/NEJM199912303412702
        • Kemeny N.E.
        • Chou J.F.
        • Boucher T.M.
        • 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: 477-484https://doi.org/10.1002/jso.24189
        • Groot Koerkamp B.
        • Sadot E.
        • Kemeny N.E.
        • et al.
        Perioperative Hepatic Arterial Infusion Pump Chemotherapy Is Associated With Longer Survival After Resection of Colorectal Liver Metastases: A Propensity Score Analysis.
        J Clin Oncol. 2017; 35: 1938-1944https://doi.org/10.1200/JCO.2016.71.8346
        • Gholami S.
        • Kemeny N.E.
        • Boucher T.M.
        • et al.
        Adjuvant Hepatic Artery Infusion Chemotherapy is Associated With Improved Survival Regardless of KRAS Mutation Status in Patients With Resected Colorectal Liver Metastases: A Retrospective Analysis of 674 Patients.
        Ann Surg. 2020; 272: 352-356https://doi.org/10.1097/SLA.0000000000003248
        • Altendorf-Hofmann A.
        • Scheele J.
        A critical review of the major indicators of prognosis after resection of hepatic metastases from colorectal carcinoma.
        Surg Oncol Clin N Am. 2003; 12 (xi): 165-192https://doi.org/10.1016/s1055-3207(02)00091-1
        • Adam R.
        • Delvart V.
        • Pascal G.
        • et al.
        Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival.
        Ann Surg. 2004; 240 ([discussion: 657-8]): 644-657https://doi.org/10.1097/01.sla.0000141198.92114.f6
        • Pozzo C.
        • Basso M.
        • Cassano A.
        • et al.
        Neoadjuvant treatment of unresectable liver disease with irinotecan and 5-fluorouracil plus folinic acid in colorectal cancer patients.
        Ann Oncol. 2004; 15: 933-939https://doi.org/10.1093/annonc/mdh217
        • Bismuth H.
        • Adam R.
        • Levi F.
        • et al.
        Resection of nonresectable liver metastases from colorectal cancer after neoadjuvant chemotherapy.
        Ann Surg. 1996; 224 ([discussion 520-2]): 509-520https://doi.org/10.1097/00000658-199610000-00009
        • Ychou M.
        • Rivoire M.
        • Thezenas S.
        • et al.
        A randomized phase II trial of three intensified chemotherapy regimens in first-line treatment of colorectal cancer patients with initially unresectable or not optimally resectable liver metastases. The METHEP trial.
        Ann Surg Oncol. 2013; 20: 4289-4297https://doi.org/10.1245/s10434-013-3217-x
        • Folprecht G.
        • Gruenberger T.
        • Bechstein W.O.
        • et al.
        Tumour response and secondary resectability of colorectal liver metastases following neoadjuvant chemotherapy with cetuximab: the CELIM randomised phase 2 trial.
        Lancet Oncol. 2010; 11: 38-47https://doi.org/10.1016/S1470-2045(09)70330-4
        • Folprecht G.
        • Gruenberger T.
        • Bechstein W.
        • et al.
        Survival of patients with initially unresectable colorectal liver metastases treated with FOLFOX/cetuximab or FOLFIRI/cetuximab in a multidisciplinary concept (CELIM study).
        Ann Oncol. 2014; 25: 1018-1025https://doi.org/10.1093/annonc/mdu088
        • Van Cutsem E.
        • Kohne C.H.
        • Hitre E.
        • et al.
        Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer.
        N Engl J Med. 2009; 360: 1408-1417https://doi.org/10.1056/NEJMoa0805019
        • Bokemeyer C.
        • Bondarenko I.
        • Hartmann J.T.
        • et al.
        Efficacy according to biomarker status of cetuximab plus FOLFOX-4 as first-line treatment for metastatic colorectal cancer: the OPUS study.
        Ann Oncol. 2011; 22: 1535-1546https://doi.org/10.1093/annonc/mdq632
        • Bokemeyer C.
        • Bondarenko I.
        • Makhson A.
        • et al.
        Fluorouracil, leucovorin, and oxaliplatin with and without cetuximab in the first-line treatment of metastatic colorectal cancer.
        J Clin Oncol. 2009; 27: 663-671https://doi.org/10.1200/JCO.2008.20.8397
        • Gruenberger T.
        • Bridgewater J.
        • Chau I.
        • et al.
        Bevacizumab plus mFOLFOX-6 or FOLFOXIRI in patients with initially unresectable liver metastases from colorectal cancer: the OLIVIA multinational randomised phase II trial.
        Ann Oncol. 2015; 26: 702-708https://doi.org/10.1093/annonc/mdu580
        • Tang W.
        • Ren L.
        • Liu T.
        • et al.
        Bevacizumab Plus mFOLFOX6 Versus mFOLFOX6 Alone as First-Line Treatment for RAS Mutant Unresectable Colorectal Liver-Limited Metastases: The BECOME Randomized Controlled Trial.
        J Clin Oncol. 2020; 38: 3175-3184https://doi.org/10.1200/JCO.20.00174
        • Heinemann V.
        • von Weikersthal L.F.
        • Decker T.
        • et al.
        FOLFIRI plus cetuximab versus FOLFIRI plus bevacizumab as first-line treatment for patients with metastatic colorectal cancer (FIRE-3): a randomised, open-label, phase 3 trial.
        Lancet Oncol. 2014; 15: 1065-1075https://doi.org/10.1016/S1470-2045(14)70330-4
        • Heinemann V.
        • von Weikersthal L.F.
        • Decker T.
        • et al.
        FOLFIRI plus cetuximab or bevacizumab for advanced colorectal cancer: final survival and per-protocol analysis of FIRE-3, a randomised clinical trial.
        Br J Cancer. 2021; 124: 587-594https://doi.org/10.1038/s41416-020-01140-9
        • Oki E.
        • Emi Y.
        • Yamanaka T.
        • et al.
        Randomised phase II trial of mFOLFOX6 plus bevacizumab versus mFOLFOX6 plus cetuximab as first-line treatment for colorectal liver metastasis (ATOM trial).
        Br J Cancer. 2019; 121: 222-229https://doi.org/10.1038/s41416-019-0518-2
        • Tucker O.N.
        • Heaton N.
        The 'small for size' liver syndrome.
        Curr Opin Crit Care. 2005; 11: 150-155https://doi.org/10.1097/01.ccx.0000157080.11117.45
        • Adam R.
        • Laurent A.
        • Azoulay D.
        • et al.
        Two-stage hepatectomy: A planned strategy to treat irresectable liver tumors.
        Ann Surg. 2000; 232: 777-785https://doi.org/10.1097/00000658-200012000-00006
        • Jaeck D.
        • Oussoultzoglou E.
        • Rosso E.
        • et al.
        A two-stage hepatectomy procedure combined with portal vein embolization to achieve curative resection for initially unresectable multiple and bilobar colorectal liver metastases.
        Ann Surg. 2004; 240 ([discussion: 1049-51]): 1037-1049https://doi.org/10.1097/01.sla.0000145965.86383.89
        • Rous P.
        • Larimore L.D.
        Relation of the Portal Blood to Liver Maintenance : A Demonstration of Liver Atrophy Conditional on Compensation.
        J Exp Med. 1920; 31: 609-632https://doi.org/10.1084/jem.31.5.609
        • van Gulik T.M.
        • van den Esschert J.W.
        James Cantlie's early messages for hepatic surgeons: how the concept of pre-operative portal vein occlusion was defined.
        HPB (Oxford). 2010; 12: 81-83
        • Kinoshita H.
        • Sakai K.
        • Hirohashi K.
        • et al.
        Preoperative portal vein embolization for hepatocellular carcinoma.
        World J Surg. 1986; 10: 803-808https://doi.org/10.1007/BF01655244
        • Makuuchi M.
        • Thai B.L.
        • Takayasu K.
        • et al.
        Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report.
        Surgery. 1990; 107: 521-527
        • Honjo I.
        • Suzuki T.
        • Ozawa K.
        • et al.
        Ligation of a branch of the portal vein for carcinoma of the liver.
        Am J Surg. 1975; 130: 296-302https://doi.org/10.1016/0002-9610(75)90389-x
        • Shindoh J.
        • Truty M.J.
        • Aloia T.A.
        • et al.
        Kinetic growth rate after portal vein embolization predicts posthepatectomy outcomes: toward zero liver-related mortality in patients with colorectal liver metastases and small future liver remnant.
        J Am Coll Surg. 2013; 216: 201-209https://doi.org/10.1016/j.jamcollsurg.2012.10.018
        • Leung U.
        • Simpson A.L.
        • Araujo R.L.
        • et al.
        Remnant growth rate after portal vein embolization is a good early predictor of post-hepatectomy liver failure.
        J Am Coll Surg. 2014; 219: 620-630https://doi.org/10.1016/j.jamcollsurg.2014.04.022
        • Brouquet A.
        • Abdalla E.K.
        • Kopetz S.
        • et al.
        High survival rate after two-stage resection of advanced colorectal liver metastases: response-based selection and complete resection define outcome.
        J Clin Oncol. 2011; 29: 1083-1090https://doi.org/10.1200/JCO.2010.32.6132
        • Hwang S.
        • Lee S.G.
        • Ko G.Y.
        • et al.
        Sequential preoperative ipsilateral hepatic vein embolization after portal vein embolization to induce further liver regeneration in patients with hepatobiliary malignancy.
        Ann Surg. 2009; 249: 608-616https://doi.org/10.1097/SLA.0b013e31819ecc5c
        • Schnitzbauer A.A.
        • Lang S.A.
        • Goessmann H.
        • et al.
        Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings.
        Ann Surg. 2012; 255: 405-414https://doi.org/10.1097/SLA.0b013e31824856f5
        • Kang D.
        • Schadde E.
        Hypertrophy and Liver Function in ALPPS: Correlation with Morbidity and Mortality.
        Visc Med. 2017; 33: 426-433https://doi.org/10.1159/000479477
        • Sandstrom P.
        • Rosok B.I.
        • Sparrelid E.
        • et al.
        ALPPS Improves Resectability Compared With Conventional Two-stage Hepatectomy in Patients With Advanced Colorectal Liver Metastasis: Results From a Scandinavian Multicenter Randomized Controlled Trial (LIGRO Trial).
        Ann Surg. 2018; 267: 833-840https://doi.org/10.1097/SLA.0000000000002511
        • Hasselgren K.
        • Rosok B.I.
        • Larsen P.N.
        • et al.
        ALPPS Improves Survival Compared With TSH in Patients Affected of CRLM: Survival Analysis From the Randomized Controlled Trial LIGRO.
        Ann Surg. 2021; 273: 442-448https://doi.org/10.1097/SLA.0000000000003701
        • Eshmuminov D.
        • Raptis D.A.
        • Linecker M.
        • et al.
        Meta-analysis of associating liver partition with portal vein ligation and portal vein occlusion for two-stage hepatectomy.
        Br J Surg. 2016; 103: 1768-1782https://doi.org/10.1002/bjs.10290
        • Tournigand C.
        • Andre T.
        • Achille E.
        • et al.
        FOLFIRI followed by FOLFOX6 or the reverse sequence in advanced colorectal cancer: a randomized GERCOR study.
        J Clin Oncol. 2004; 22: 229-237https://doi.org/10.1200/JCO.2004.05.113
        • Bennouna J.
        • Sastre J.
        • Arnold D.
        • et al.
        Continuation of bevacizumab after first progression in metastatic colorectal cancer (ML18147): a randomised phase 3 trial.
        Lancet Oncol. 2013; 14: 29-37https://doi.org/10.1016/S1470-2045(12)70477-1
        • Adams R.A.
        • Fisher D.J.
        • Graham J.
        • et al.
        Capecitabine Versus Active Monitoring in Stable or Responding Metastatic Colorectal Cancer After 16 Weeks of First-Line Therapy: Results of the Randomized FOCUS4-N Trial.
        J Clin Oncol. 2021; 39: 3693-3704https://doi.org/10.1200/JCO.21.01436
        • Kemeny N.E.
        • Niedzwiecki D.
        • Hollis D.R.
        • et al.
        Hepatic arterial infusion versus systemic therapy for hepatic metastases from colorectal cancer: a randomized trial of efficacy, quality of life, and molecular markers (CALGB 9481).
        J Clin Oncol. 2006; 24: 1395-1403https://doi.org/10.1200/JCO.2005.03.8166
        • D'Angelica M.I.
        • Correa-Gallego C.
        • Paty P.B.
        • 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: 353-360https://doi.org/10.1097/SLA.0000000000000614
        • Pak L.M.
        • Kemeny N.E.
        • Capanu M.
        • 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: 634-643https://doi.org/10.1002/jso.24898
        • Allen P.J.
        • Nissan A.
        • Picon A.I.
        • et al.
        Technical complications and durability of hepatic artery infusion pumps for unresectable colorectal liver metastases: an institutional experience of 544 consecutive cases.
        J Am Coll Surg. 2005; 201: 57-65https://doi.org/10.1016/j.jamcollsurg.2005.03.019
        • Chakedis J.
        • Beal E.W.
        • Sun S.
        • et al.
        Implementation and early outcomes for a surgeon-directed hepatic arterial infusion pump program for colorectal liver metastases.
        J Surg Oncol. 2018; 118: 1065-1073https://doi.org/10.1002/jso.25249
        • Creasy J.M.
        • Napier K.J.
        • Reed S.A.
        • et al.
        Implementation of a Hepatic Artery Infusion Program: Initial Patient Selection and Perioperative Outcomes of Concurrent Hepatic Artery Infusion and Systemic Chemotherapy for Colorectal Liver Metastases.
        Ann Surg Oncol. 2020; https://doi.org/10.1245/s10434-020-08972-y
        • Dhir M.
        • Jones H.L.
        • Shuai Y.
        • et al.
        Hepatic Arterial Infusion in Combination with Modern Systemic Chemotherapy is Associated with Improved Survival Compared with Modern Systemic Chemotherapy Alone in Patients with Isolated Unresectable Colorectal Liver Metastases: A Case-Control Study.
        Ann Surg Oncol. 2017; 24: 150-158https://doi.org/10.1245/s10434-016-5418-6
        • Muaddi H.
        • D'Angelica M.
        • Wiseman J.T.
        • et al.
        Safety and feasibility of initiating a hepatic artery infusion pump chemotherapy program for unresectable colorectal liver metastases: A multicenter, retrospective cohort study.
        J Surg Oncol. 2021; 123: 252-260https://doi.org/10.1002/jso.26270
        • Dueland S.
        • Syversveen T.
        • Solheim J.M.
        • et al.
        Survival Following Liver Transplantation for Patients With Nonresectable Liver-only Colorectal Metastases.
        Ann Surg. 2020; 271: 212-218https://doi.org/10.1097/SLA.0000000000003404
        • Dueland S.
        • Yaqub S.
        • Syversveen T.
        • et al.
        Survival Outcomes After Portal Vein Embolization and Liver Resection Compared With Liver Transplant for Patients With Extensive Colorectal Cancer Liver Metastases.
        JAMA Surg. 2021; 156: 550-557https://doi.org/10.1001/jamasurg.2021.0267
        • Hernandez-Alejandro R.
        • Ruffolo L.I.
        • Sasaki K.
        • et al.
        Recipient and Donor Outcomes After Living-Donor Liver Transplant for Unresectable Colorectal Liver Metastases.
        JAMA Surg. 2022; https://doi.org/10.1001/jamasurg.2022.0300
        • Fukuoka S.
        • Hara H.
        • Takahashi N.
        • et al.
        Regorafenib Plus Nivolumab in Patients With Advanced Gastric or Colorectal Cancer: An Open-Label, Dose-Escalation, and Dose-Expansion Phase Ib Trial (REGONIVO, EPOC1603).
        J Clin Oncol. 2020; 38: 2053-2061https://doi.org/10.1200/JCO.19.03296
        • Mettu N.B.
        • Ou F.S.
        • Zemla T.J.
        • et al.
        Assessment of Capecitabine and Bevacizumab With or Without Atezolizumab for the Treatment of Refractory Metastatic Colorectal Cancer: A Randomized Clinical Trial.
        JAMA Netw Open. 2022; 5: e2149040https://doi.org/10.1001/jamanetworkopen.2021.49040
        • Yu J.
        • Green M.D.
        • Li S.
        • et al.
        Liver metastasis restrains immunotherapy efficacy via macrophage-mediated T cell elimination.
        Nat Med. 2021; 27: 152-164https://doi.org/10.1038/s41591-020-1131-x