Advertisement

The management of colorectal liver metastases amenable of surgical resection: How to shape treatment strategies according to clinical, radiological, pathological and molecular features

Published:March 20, 2022DOI:https://doi.org/10.1016/j.ctrv.2022.102382

      Highlights

      • Surgery allows long-term survival in patients with colorectal liver metastases (CRLM).
      • Among resected patients, about two-thirds experience disease relapse.
      • Risk stratification is crucial to individualize the treatment of patients with CRLM.
      • Clinical, radiological, pathological and molecular factors affect outcome.
      • Technical resectability and oncological prognosis should drive the approach to CRLM.

      Abstract

      Metastatic colorectal cancer (mCRC) patients have poor chances of long term survival, being < 15% of them still alive after 5 years from diagnosis. Nonetheless, patients with colorectal liver metastases (CRLM) may be eligible for metastases resection thus being able to achieve long-term disease remission and survival. The likelihood for patients with CRLM of being or becoming eligible for liver metastasectomy is increasing, thanks to the evolution of surgical techniques, the availability of active systemic treatments and the widespread diffusion of experienced multidisciplinary boards to manage these patients. However, disease relapse after liver surgery is common and occurs in two-thirds of resected patients. Therefore, adequate radiological staging and risk stratification is crucial for the optimal selection of patients candidate to surgery in order to maximize the benefit-risk ratio of liver metastasectomy and to individualize the treatment strategy. Based on the multidimensional assessment, three possible approaches are available: upfront liver surgery followed by adjuvant chemotherapy, perioperative chemotherapy preceding and following liver surgery, and an upfront systemic treatment including chemotherapy plus a targeted agent, both chosen according to patients’ and tumours’ characteristics, then followed by liver surgery if indicated. In this review, we describe the most important factors impacting the therapeutic choices in patients with resectable and potentially resectable CRLM, and we discuss the most promising factors that may reshape the future decision-making process of these patients.

      Keywords

      To read this article in full you will need to make a payment
      ESMO Member Login
      Login with your ESMO username and password.
      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'

      Purchase one-time access:

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

      References

        • Arnold M.
        • Sierra M.S.
        • Laversanne M.
        • Soerjomataram I.
        • Jemal A.
        • Bray F.
        Global patterns and trends in colorectal cancer incidence and mortality.
        Gut. 2017; 66: 683-691https://doi.org/10.1136/gutjnl-2015-310912
        • Kanas G.P.
        • Taylor A.
        • Primrose J.N.
        • Langeberg W.J.
        • Kelsh M.A.
        • Mowat F.S.
        • et al.
        Survival after liver resection in metastatic colorectal cancer: review and meta-analysis of prognostic factors.
        Clin Epidemiol. 2012; 4: 283-301https://doi.org/10.2147/CLEP.S34285
        • Van Cutsem E.
        • Cervantes A.
        • Adam R.
        • Sobrero A.
        • Van Krieken J.H.
        • Aderka D.
        • et al.
        ESMO consensus guidelines for the management of patients with metastatic colorectal cancer.
        Ann Oncol. 2016; 27: 1386-1422
        • Benson A.B.
        • Venook A.P.
        • Al-Hawary M.M.
        • Arain M.A.
        • Chen Y.-J.
        • Ciombor K.K.
        • et al.
        Colon Cancer, Version 2.2021, NCCN Clinical Practice Guidelines in Oncology.
        J Natl Compr Canc Netw. 2021; 19: 329-359
        • Jones R.P.
        • Poston G.J.
        Resection of liver metastases in colorectal cancer in the era of expanding systemic therapy.
        Annu Rev Med. 2017; 68: 183-196https://doi.org/10.1146/annurev-med-062415-093510
        • Folprecht G.
        • Gruenberger T.
        • Bechstein W.
        • Raab H.-R.
        • Weitz J.
        • Lordick F.
        • 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: 1018-1025
        • Dhir M.
        • Sasson A.R.
        Surgical Management of Liver Metastases From Colorectal Cancer.
        J Oncol Pract. 2016; 12: 33-39https://doi.org/10.1200/JOP.2015.009407
        • Cremolini C.
        • Casagrande M.
        • Loupakis F.
        • Aprile G.
        • Bergamo F.
        • Masi G.
        • 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
        • Osterlund P.
        • Salminen T.
        • Soveri L.-M.
        • Kallio R.
        • Kellokumpu I.
        • Lamminmäki A.
        • et al.
        Repeated centralized multidisciplinary team assessment of resectability, clinical behavior, and outcomes in 1086 Finnish metastatic colorectal cancer patients (RAXO): A nationwide prospective intervention study.
        Lancet Reg Health Eur. 2021; 3: 100049
        • Virani S.
        • Michaelson J.S.
        • Hutter M.M.
        • Lancaster R.T.
        • Warshaw A.L.
        • Henderson W.G.
        • et al.
        Morbidity and mortality after liver resection: results of the patient safety in surgery study.
        J Am Coll Surg. 2007; 204: 1284-1292
        • Imai K.
        • Allard M.-A.
        • Benitez C.C.
        • Vibert E.
        • Sa Cunha A.
        • Cherqui D.
        • et al.
        Early recurrence after hepatectomy for colorectal liver metastases: what optimal definition and what predictive factors?.
        Oncologist. 2016; 21: 887-894
        • de Jong M.C.
        • Pulitano C.
        • Ribero D.
        • Strub J.
        • Mentha G.
        • Schulick R.D.
        • et al.
        Rates and patterns of recurrence following curative intent surgery for colorectal liver metastasis: an international multi-institutional analysis of 1669 patients.
        Ann Surg. 2009; 250: 440-448
        • Clavien P.-A.
        • Petrowsky H.
        • DeOliveira M.L.
        • Graf R.
        Strategies for safer liver surgery and partial liver transplantation.
        N Engl J Med. 2007; 356: 1545-1559https://doi.org/10.1056/NEJMra065156
        • Marcus R.K.
        • Aloia T.A.
        Defining Resectability of Colorectal Cancer Liver Metastases: Technical and Oncologic Perspectives.
        in: Correia M.M. Choti M.A. Rocha F.G. Wakabayashi G. Colorectal Cancer Liver Metastases: A Comprehensive Guide to Management. Springer International Publishing, Cham2020: 129-144https://doi.org/10.1007/978-3-030-25486-5_11
        • Kanemitsu Y.
        • Shimizu Y.
        • Mizusawa J.
        • Inaba Y.
        • Hamaguchi T.
        • Shida D.
        • 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: 3789-3799
        • Nordlinger B.
        • Sorbye H.
        • Glimelius B.
        • Poston G.J.
        • Schlag P.M.
        • Rougier P.
        • et al.
        Perioperative chemotherapy with FOLFOX4 and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC Intergroup trial 40983): a randomised controlled trial.
        The Lancet. 2008; 371: 1007-1016
        • Adam R.
        • de Gramont A.
        • Figueras J.
        • Kokudo N.
        • Kunstlinger F.
        • Loyer E.
        • et al.
        Managing synchronous liver metastases from colorectal cancer: a multidisciplinary international consensus.
        Cancer Treat Rev. 2015; 41: 729-741
        • Niekel M.C.
        • Bipat S.
        • Stoker J.
        Diagnostic imaging of colorectal liver metastases with CT, MR imaging, FDG PET, and/or FDG PET/CT: a meta-analysis of prospective studies including patients who have not previously undergone treatment.
        Radiology. 2010; 257: 674-684https://doi.org/10.1148/radiol.10100729
        • Floriani I.
        • Torri V.
        • Rulli E.
        • Garavaglia D.
        • Compagnoni A.
        • Salvolini L.
        • 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: 19-31
        • Kulemann V.
        • Schima W.
        • Tamandl D.
        • Kaczirek K.
        • Gruenberger T.
        • Wrba F.
        • et al.
        Preoperative detection of colorectal liver metastases in fatty liver: MDCT or MRI?.
        Eur J Radiol. 2011; 79: e1-e6
        • Sibinga Mulder B.G.
        • Visser K.
        • Feshtali S.
        • Vahrmeijer A.L.
        • Swijnenburg R.J.
        • Hartgrink H.H.
        • et al.
        Gadoxetic acid-enhanced magnetic resonance imaging significantly influences the clinical course in patients with colorectal liver metastases.
        BMC Med Imaging. 2018; 18https://doi.org/10.1186/s12880-018-0289-x
        • Kim H.J.
        • Lee S.S.
        • Byun J.H.
        • Kim J.C.
        • Yu C.S.
        • Park S.H.
        • et al.
        Incremental value of liver MR imaging in patients with potentially curable colorectal hepatic metastasis detected at CT: a prospective comparison of diffusion-weighted imaging, gadoxetic acid-enhanced MR imaging, and a combination of both MR techniques.
        Radiology. 2015; 274: 712-722
        • Knowles B.
        • Welsh F.K.S.
        • Chandrakumaran K.
        • John T.G.
        • Rees M.
        Detailed liver-specific imaging prior to pre-operative chemotherapy for colorectal liver metastases reduces intra-hepatic recurrence and the need for a repeat hepatectomy.
        HPB (Oxford). 2012; 14: 298-309https://doi.org/10.1111/j.1477-2574.2012.00447.x
        • Zech C.J.
        • Korpraphong P.
        • Huppertz A.
        • Denecke T.
        • Kim M.-J.
        • Tanomkiat W.
        • et al.
        Randomized multicentre trial of gadoxetic acid-enhanced MRI versus conventional MRI or CT in the staging of colorectal cancer liver metastases.
        Br J Surg. 2014; 101: 613-621
        • Maffione A.M.
        • Lopci E.
        • Bluemel C.
        • Giammarile F.
        • Herrmann K.
        • Rubello D.
        Diagnostic accuracy and impact on management of (18)F-FDG PET and PET/CT in colorectal liver metastasis: a meta-analysis and systematic review.
        Eur J Nucl Med Mol Imaging. 2015; 42: 152-163https://doi.org/10.1007/s00259-014-2930-4
        • Daza J.F.
        • Solis N.M.
        • Parpia S.
        • Gallinger S.
        • Moulton C.-A.
        • Belley-Cote E.P.
        • et al.
        A meta-analysis exploring the role of PET and PET-CT in the management of potentially resectable colorectal cancer liver metastases.
        Eur J Surg Oncol. 2019; 45: 1341-1348
        • Berger K.L.
        • Nicholson S.A.
        • Dehdashti F.
        • Siegel B.A.
        FDG PET evaluation of mucinous neoplasms: correlation of FDG uptake with histopathologic features.
        AJR Am J Roentgenol. 2000; 174: 1005-1008https://doi.org/10.2214/ajr.174.4.1741005
        • Russolillo N.
        • Borello A.
        • Langella S.
        • Tesoriere R.L.
        • Forchino F.
        • Ferrero A.
        Diagnostic performance of the FDG PET/CT in patients with mucinous colorectal liver metastases.
        HPB. 2018; 20: S345-S346https://doi.org/10.1016/j.hpb.2018.06.2567
        • Borello A.
        • Russolillo N.
        • Lo Tesoriere R.
        • Langella S.
        • Guerra M.
        • Ferrero A.
        Diagnostic performance of the FDG-PET/CT in patients with resected mucinous colorectal liver metastases.
        Surgeon. 2021; 19: e140-e145https://doi.org/10.1016/j.surge.2020.09.004
        • Furtado F.S.
        • Suarez-Weiss K.E.
        • Vangel M.
        • Clark J.W.
        • Cusack J.C.
        • Hong T.
        • et al.
        Clinical impact of PET/MRI in oligometastatic colorectal cancer.
        Br J Cancer. 2021; 125: 975-982
        • van der Poel M.J.
        • Tanis P.J.
        • Marsman H.A.
        • Rijken A.M.
        • Gertsen E.C.
        • Ovaere S.
        • et al.
        Laparoscopic combined resection of liver metastases and colorectal cancer: a multicenter, case-matched study using propensity scores.
        Surg Endosc. 2019; 33: 1124-1130
        • Reddy S.K.
        • Pawlik T.M.
        • Zorzi D.
        • Gleisner A.L.
        • Ribero D.
        • Assumpcao L.
        • et al.
        Simultaneous resections of colorectal cancer and synchronous liver metastases: a multi-institutional analysis.
        Ann Surg Oncol. 2007; 14: 3481-3491
        • Viganò L.
        • Torzilli G.
        • Troisi R.
        • Aldrighetti L.
        • Ferrero A.
        • Majno P.
        • et al.
        Minor hepatectomies: focusing a blurred picture: analysis of the outcome of 4471 open resections in patients without cirrhosis.
        Ann Surg. 2019; 270: 842-851
        • Ruers T.
        • Van Coevorden F.
        • Punt C.J.A.
        • Pierie J.-P.
        • Borel-Rinkes I.
        • Ledermann J.A.
        • et al.
        Local treatment of unresectable colorectal liver metastases: results of a randomized phase II trial.
        J Natl Cancer Inst. 2017; 109https://doi.org/10.1093/jnci/djx015
        • Kelly M.E.
        • Spolverato G.
        • Lê G.N.
        • Mavros M.N.
        • Doyle F.
        • Pawlik T.M.
        • et al.
        Synchronous colorectal liver metastasis: a network meta-analysis review comparing classical, combined, and liver-first surgical strategies.
        J Surg Oncol. 2015; 111: 341-351
        • Waisberg J.
        • Ivankovics I.G.
        Liver-first approach of colorectal cancer with synchronous hepatic metastases: A reverse strategy.
        World J Hepatol. 2015; 7: 1444-1449https://doi.org/10.4254/wjh.v7.i11.1444
        • Ayez N.
        • Burger J.W.A.
        • van der Pool A.E.
        • Eggermont A.M.M.
        • Grunhagen D.J.
        • de Wilt J.H.W.
        • et al.
        Long-term results of the “liver first” approach in patients with locally advanced rectal cancer and synchronous liver metastases.
        Dis Colon Rectum. 2013; 56: 281-287https://doi.org/10.1097/DCR.0b013e318279b743
        • Giuliante F.
        • Viganò L.
        • De Rose A.M.
        • Mirza D.F.
        • Lapointe R.
        • Kaiser G.
        • et al.
        Liver-first approach for synchronous colorectal metastases: analysis of 7360 patients from the LiverMetSurvey registry.
        Ann Surg Oncol. 2021; 28: 8198-8208
        • Beard R.E.
        • Khan S.
        • Troisi R.I.
        • Montalti R.
        • Vanlander A.
        • Fong Y.
        • et al.
        Long-Term and Oncologic Outcomes of Robotic Versus Laparoscopic Liver Resection for Metastatic Colorectal Cancer: A Multicenter, Propensity Score Matching Analysis.
        World J Surg. 2020; 44: 887-895
        • Guadagni S.
        • Furbetta N.
        • Di Franco G.
        • Palmeri M.
        • Gianardi D.
        • Bianchini M.
        • et al.
        Robotic-assisted surgery for colorectal liver metastasis: A single-centre experience.
        J Minim Access Surg. 2020; 16: 160
        • Guerra F.
        • Guadagni S.
        • Pesi B.
        • Furbetta N.
        • Di Franco G.
        • Palmeri M.
        • et al.
        Outcomes of robotic liver resections for colorectal liver metastases. A multi-institutional analysis of minimally invasive ultrasound-guided robotic surgery.
        Surg Oncol. 2019; 28: 14-18
        • Fretland Å.A.
        • Dagenborg V.J.
        • Bjørnelv G.M.W.
        • Kazaryan A.M.
        • Kristiansen R.
        • Fagerland M.W.
        • et al.
        Laparoscopic versus open resection for colorectal liver metastases: The OSLO-COMET randomized controlled trial.
        Ann Surg. 2018; 267: 199-207
        • Tanaka K.
        • Kumamoto T.
        • Nojiri K.
        • Matsuyama R.
        • Takeda K.
        • Endo I.
        Impact of postoperative morbidity on long-term survival after resection for colorectal liver metastases.
        Ann Surg Oncol. 2016; 23: 929-937https://doi.org/10.1245/s10434-010-1352-1
        • Bridgewater J.A.
        • Pugh S.A.
        • Maishman T.
        • Eminton Z.
        • Mellor J.
        • Whitehead A.
        • 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: 398-411
        • Gruenberger T.
        • Bridgewater J.
        • Chau I.
        • García Alfonso P.
        • Rivoire M.
        • Mudan S.
        • 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: 702-708
        • Bolhuis K.
        • Grosheide L.
        • Wesdorp N.J.
        • Komurcu A.
        • Chapelle T.
        • Dejong C.H.C.
        • et al.
        Short-term outcomes of secondary liver surgery for initially unresectable colorectal liver metastases following modern induction systemic therapy in the dutch CAIRO5 trial.
        Annals of Surgery Open. 2021; 2: e081
        • Gaujoux S.
        • Goéré D.
        • Dumont F.
        • Souadka A.
        • Dromain C.
        • Ducreux M.
        • et al.
        Complete radiological response of colorectal liver metastases after chemotherapy: what can we expect?.
        Dig Surg. 2011; 28: 114-120
        • Bahadoer R.R.
        • Dijkstra E.A.
        • van Etten B.
        • Marijnen C.A.M.
        • Putter H.
        • Kranenbarg E.-K.
        • et al.
        Short-course radiotherapy followed by chemotherapy before total mesorectal excision (TME) versus preoperative chemoradiotherapy, TME, and optional adjuvant chemotherapy in locally advanced rectal cancer (RAPIDO): a randomised, open-label, phase 3 trial.
        Lancet Oncol. 2021; 22: 29-42
        • Conroy T.
        • Bosset J.-F.
        • Etienne P.-L.
        • Rio E.
        • François É.
        • Mesgouez-Nebout N.
        • et al.
        Neoadjuvant chemotherapy with FOLFIRINOX and preoperative chemoradiotherapy for patients with locally advanced rectal cancer (UNICANCER-PRODIGE 23): a multicentre, randomised, open-label, phase 3 trial.
        Lancet Oncol. 2021; 22: 702-715
        • Glynne-Jones R.
        • Wyrwicz L.
        • Tiret E.
        • Brown G.
        • Rödel C.
        • Cervantes A.
        • et al.
        Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up.
        Ann Oncol. 2017; 28: iv22-iv40
        • Spelt L.
        • Andersson B.
        • Nilsson J.
        • Andersson R.
        Prognostic models for outcome following liver resection for colorectal cancer metastases: A systematic review.
        Eur J Surg Oncol. 2012; 38: 16-24https://doi.org/10.1016/j.ejso.2011.10.013
        • Fong Y.
        • Fortner J.
        • Sun R.L.
        • Brennan M.F.
        • Blumgart L.H.
        Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases.
        Ann Surg. 1999; 230: 309
        • Fromer M.W.
        • Scoggins C.R.
        • Egger M.E.
        • Philips P.
        • McMasters K.M.
        • Martin II R.C.G.
        Preventing futile liver resection: a risk-based approach to surgical selection in major hepatectomy for colorectal cancer.
        Ann Surg Oncol. 2022; 29: 905-912
        • Margonis G.A.
        • Kim Y.
        • Spolverato G.
        • Ejaz A.
        • Gupta R.
        • Cosgrove D.
        • et al.
        Association between specific mutations in KRAS codon 12 and colorectal liver metastasis.
        JAMA Surgery. 2015; 150: 722
        • Margonis G.A.
        • Kim Y.
        • Sasaki K.
        • Samaha M.
        • Amini N.
        • Pawlik T.M.
        Codon 13 KRAS mutation predicts patterns of recurrence in patients undergoing hepatectomy for colorectal liver metastases.
        Cancer. 2016; 122: 2698-2707https://doi.org/10.1002/cncr.30085
        • Margonis G.A.
        • Sasaki K.
        • Gholami S.
        • Kim Y.
        • Andreatos N.
        • Rezaee N.
        • et al.
        Genetic And Morphological Evaluation (GAME) score for patients with colorectal liver metastases.
        Br J Surg. 2018; 105: 1210-1220
        • Brudvik K.W.
        • Kopetz S.E.
        • Li L.
        • Conrad C.
        • Aloia T.A.
        • Vauthey J.-N.
        Meta-analysis of KRAS mutations and survival after resection of colorectal liver metastases.
        Br J Surg. 2015; 102: 1175-1183https://doi.org/10.1002/bjs.9870
        • Tosi F.
        • Magni E.
        • Amatu A.
        • Mauri G.
        • Bencardino K.
        • Truini M.
        • et al.
        Effect of KRAS and BRAF mutations on survival of metastatic colorectal cancer after liver resection: a systematic review and meta-analysis.
        Clin Colorectal Cancer. 2017; 16: e153-e163
        • Schirripa M.
        • Bergamo F.
        • Cremolini C.
        • Casagrande M.
        • Lonardi S.
        • Aprile G.
        • et al.
        BRAF and RAS mutations as prognostic factors in metastatic colorectal cancer patients undergoing liver resection.
        Br J Cancer. 2015; 112: 1921-1928
        • Gagnière J.
        • Dupré A.
        • Gholami S.S.
        • Pezet D.
        • Boerner T.
        • Gönen M.
        • et al.
        Is hepatectomy justified for BRAF mutant colorectal liver metastases?: a multi-institutional analysis of 1497 patients.
        Ann Surg. 2020; 271: 147-154
        • Margonis G.A.
        • Buettner S.
        • Andreatos N.
        • Kim Y.
        • Wagner D.
        • Sasaki K.
        • et al.
        Association of BRAF mutations with survival and recurrence in surgically treated patients with metastatic colorectal liver cancer.
        JAMA Surgery. 2018; 153: e180996
        • Brudvik K.W.
        • Jones R.P.
        • Giuliante F.
        • Shindoh J.
        • Passot G.
        • Chung M.H.
        • et al.
        RAS mutation clinical risk score to predict survival after resection of colorectal liver metastases.
        Ann Surg. 2019; 269: 120-126
        • Kawaguchi Y.
        • Kopetz S.
        • Tran Cao H.S.
        • Panettieri E.
        • De Bellis M.
        • Nishioka Y.
        • et al.
        Contour prognostic model for predicting survival after resection of colorectal liver metastases: development and multicentre validation study using largest diameter and number of metastases with RAS mutation status.
        Br J Surg. 2021; 108: 968-975
        • Margonis G.A.
        • Buettner S.
        • Andreatos N.
        • Sasaki K.
        • Ijzermans J.N.M.
        • van Vugt J.L.A.
        • et al.
        Anatomical resections improve disease-free survival in patients with KRAS-mutated colorectal liver metastases.
        Ann Surg. 2017; 266: 641-649
      1. Reply to Viganò L, Costa G, Toso C, Cimino M, Andres A, Rubbia-Brandt L, et al. “Precision Surgery” for Colorectal Liver Metastases: Is the Time Ripe? Annals of Surgery 2018;269:1. https://doi.org/10.1097/SLA.0000000000002855.

        • Si A.
        • Li J.
        • Yang Z.
        • Xia Y.
        • Yang T.
        • Lei Z.
        • et al.
        Impact of anatomical versus non-anatomical liver resection on short- and long-term outcomes for patients with intrahepatic cholangiocarcinoma.
        Ann Surg Oncol. 2019; 26: 1841-1850
        • Bachet J.-B.
        • Moreno-Lopez N.
        • Vigano L.
        • Marchese U.
        • Gelli M.
        • Raoux L.
        • et al.
        BRAF mutation is not associated with an increased risk of recurrence in patients undergoing resection of colorectal liver metastases.
        Br J Surg. 2019; 106: 1237-1247
        • Goldstein J.
        • Tran B.
        • Ensor J.
        • Gibbs P.
        • Wong H.L.
        • Wong S.F.
        • et al.
        Multicenter retrospective analysis of metastatic colorectal cancer (CRC) with high-level microsatellite instability (MSI-H).
        Ann Oncol. 2014; 25: 1032-1038
        • Margonis G.A.
        • Buettner S.
        • Wagner D.
        • McVey J.
        • Andreatos N.
        • Beer A.
        • et al.
        Microsatellite instability in resectable colorectal liver metastasis: An international multi-institutional analysis.
        JCO. 2018; 36: 220
        • Dijkstra M.
        • Nieuwenhuizen S.
        • Puijk R.S.
        • Timmer F.E.F.
        • Geboers B.
        • Schouten E.A.C.
        • et al.
        Primary Tumor Sidedness, RAS and BRAF Mutations and MSI Status as Prognostic Factors in Patients with Colorectal Liver Metastases Treated with Surgery and Thermal Ablation: Results from the Amsterdam Colorectal Liver Met Registry (AmCORE).
        Biomedicines. 2021; 9: 962
        • Kim C.G.
        • Ahn J.B.
        • Jung M.
        • Beom S.H.
        • Kim C.
        • Kim J.H.
        • et al.
        Effects of microsatellite instability on recurrence patterns and outcomes in colorectal cancers.
        Br J Cancer. 2016; 115: 25-33
        • Le D.T.
        • Durham J.N.
        • Smith K.N.
        • Wang H.
        • Bartlett B.R.
        • Aulakh L.K.
        • et al.
        Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade.
        Science. 2017; 357: 409-413
        • Ludford K.
        • Cohen R.
        • Svrcek M.
        • Foo W.C.
        • Colle R.
        • Parc Y.
        • et al.
        Pathological tumor response following immune checkpoint blockade for deficient mismatch repair advanced colorectal cancer.
        JNCI: J Natl Cancer Inst. 2021; 113: 208-211
        • Heinemann V.
        • Stintzing S.
        • Modest D.P.
        • Giessen-Jung C.
        • Michl M.
        • Mansmann U.R.
        Early tumour shrinkage (ETS) and depth of response (DpR) in the treatment of patients with metastatic colorectal cancer (mCRC).
        Eur J Cancer. 2015; 51: 1927-1936https://doi.org/10.1016/j.ejca.2015.06.116
        • Douillard J.-Y.
        • Siena S.
        • Peeters M.
        • Koukakis R.
        • Terwey J.-H.
        • Tabernero J.
        Impact of early tumour shrinkage and resection on outcomes in patients with wild-type RAS metastatic colorectal cancer.
        Eur J Cancer. 2015; 51: 1231-1242https://doi.org/10.1016/j.ejca.2015.03.026
        • Cremolini C.
        • Loupakis F.
        • Antoniotti C.
        • Lonardi S.
        • Masi G.
        • Salvatore L.
        • et al.
        Early tumor shrinkage and depth of response predict long-term outcome in metastatic colorectal cancer patients treated with first-line chemotherapy plus bevacizumab: results from phase III TRIBE trial by the Gruppo Oncologico del Nord Ovest.
        Ann Oncol. 2015; 26: 1188-1194
        • Tomasello G.
        • Petrelli F.
        • Ghidini M.
        • Russo A.
        • Passalacqua R.
        • Barni S.
        FOLFOXIRI Plus Bevacizumab as Conversion Therapy for Patients With Initially Unresectable Metastatic Colorectal Cancer: A Systematic Review and Pooled Analysis.
        JAMA Oncol. 2017; 3: e170278
      2. Adam R, Pascal G, Castaing D, Azoulay D, Delvart V, Paule B, et al. Tumor progression while on chemotherapy: a contraindication to liver resection for multiple colorectal metastases? Ann Surg 2004;240:1052–61; discussion 1061-1064. https://doi.org/10.1097/01.sla.0000145964.08365.01.

        • Yasuno M.
        • Uetake H.
        • Ishiguro M.
        • Mizunuma N.
        • Komori T.
        • Miyata G.o.
        • et al.
        mFOLFOX6 plus bevacizumab to treat liver-only metastases of colorectal cancer that are unsuitable for upfront resection (TRICC0808): a multicenter phase II trial comprising the final analysis for survival.
        Int J Clin Oncol. 2019; 24: 516-525
        • Tang W.
        • Ren L.i.
        • Liu T.
        • Ye Q.
        • Wei Y.e.
        • He G.
        • 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: 3175-3184
        • Folprecht G.
        • Grothey A.
        • Alberts S.
        • Raab H.-R.
        • Köhne C.-H.
        Neoadjuvant treatment of unresectable colorectal liver metastases: correlation between tumour response and resection rates.
        Ann Oncol. 2005; 16: 1311-1319https://doi.org/10.1093/annonc/mdi246
        • Jones R.P.
        • Hamann S.
        • Malik H.Z.
        • Fenwick S.W.
        • Poston G.J.
        • Folprecht G.
        Defined criteria for resectability improves rates of secondary resection after systemic therapy for liver limited metastatic colorectal cancer.
        Eur J Cancer. 2014; 50: 1590-1601https://doi.org/10.1016/j.ejca.2014.02.024
        • Primavesi F.
        • Fadinger N.
        • Biggel S.
        • Braunwarth E.
        • Gasser E.
        • Sprung S.
        • et al.
        Early response evaluation during preoperative chemotherapy for colorectal liver metastases: Combined size and morphology-based criteria predict pathological response and survival after resection.
        J Surg Oncol. 2020; 121: 382-391
        • Ilic I.
        • Jankovic S.
        • Ilic M.
        • Chang Y.-J.
        Bevacizumab combined with chemotherapy improves survival for patients with metastatic colorectal cancer: evidence from meta analysis.
        PLoS ONE. 2016; 11: e0161912
        • Saltz L.B.
        • Clarke S.
        • Díaz-Rubio E.
        • Scheithauer W.
        • Figer A.
        • Wong R.
        • et al.
        Bevacizumab in combination with oxaliplatin-based chemotherapy as first-line therapy in metastatic colorectal cancer: a randomized phase III study.
        J Clin Oncol. 2008; 26: 2013-2019
        • Cremolini C.
        • Loupakis F.
        • Masi G.
        • Lonardi S.
        • Granetto C.
        • Mancini M.L.
        • et al.
        FOLFOXIRI or FOLFOXIRI plus bevacizumab as first-line treatment of metastatic colorectal cancer: a propensity score-adjusted analysis from two randomized clinical trials.
        Ann Oncol. 2016; 27: 843-849
        • Chun Y.S.
        • Vauthey J.-N.
        • Boonsirikamchai P.
        • Maru D.M.
        • Kopetz S.
        • Palavecino M.
        • et al.
        Association of computed tomography morphologic criteria with pathologic response and survival in patients treated with bevacizumab for colorectal liver metastases.
        JAMA. 2009; 302: 2338-2344https://doi.org/10.1001/jama.2009.1755
        • Hurwitz H.
        • Fehrenbacher L.
        • Novotny W.
        • Cartwright T.
        • Hainsworth J.
        • Heim W.
        • et al.
        Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer.
        N Engl J Med. 2004; 350: 2335-2342
        • Shindoh J.
        • Loyer E.M.
        • Kopetz S.
        • Boonsirikamchai P.
        • Maru D.M.
        • Chun Y.S.
        • et al.
        Optimal morphologic response to preoperative chemotherapy: an alternate outcome end point before resection of hepatic colorectal metastases.
        J Clin Oncol. 2012; 30: 4566-4572
        • Vera R.
        • Gómez M.L.
        • Ayuso J.R.
        • Figueras J.
        • García-Alfonso P.
        • Martínez V.
        • et al.
        Correlation of RECIST, computed tomography morphological response, and pathological regression in hepatic metastasis secondary to colorectal cancer: the AVAMET study.
        Cancers (Basel). 2020; 12: 2259
        • Mazard T.
        • Boonsirikamchai P.
        • Overman M.J.
        • Asran M.A.
        • Choi H.
        • Herron D.
        • et al.
        Comparison of early radiological predictors of outcome in patients with colorectal cancer with unresectable hepatic metastases treated with bevacizumab.
        Gut. 2018; 67: 1095-1102
        • Cho C.S.
        • Curran S.
        • Schwartz L.H.
        • Kooby D.A.
        • Klimstra D.S.
        • Shia J.
        • et al.
        Preoperative radiographic assessment of hepatic steatosis with histologic correlation.
        J Am Coll Surg. 2008; 206: 480-488
      3. Ding Y, Rao S-X, Wang W-T, Chen C-Z, Li R-C, Zeng M. Gd-EOB-DTPA-enhanced MR findings in chemotherapy-induced sinusoidal obstruction syndrome in colorectal liver metastases. J Int Med Res 2020;48:300060520926031. https://doi.org/10.1177/0300060520926031.

        • Barimani D.
        • Kauppila J.H.
        • Sturesson C.
        • Sparrelid E.
        Imaging in disappearing colorectal liver metastases and their accuracy: a systematic review.
        World J Surgical Oncol. 2020; 18: 264https://doi.org/10.1186/s12957-020-02037-w
        • Zendel A.
        • Lahat E.
        • Dreznik Y.
        • Zakai B.B.
        • Eshkenazy R.
        • Ariche A.
        “Vanishing liver metastases”-A real challenge for liver surgeons.
        Hepatobiliary Surg Nutr. 2014; 3: 295-302https://doi.org/10.3978/j.issn.2304-3881.2014.09.13
        • Sturesson C.
        • Nilsson J.
        • Lindell G.
        • Andersson R.G.
        • Keussen I.
        Disappearing liver metastases from colorectal cancer: impact of modern imaging modalities.
        HPB (Oxford). 2015; 17: 983-987https://doi.org/10.1111/hpb.12476
        • Park M.J.
        • Hong N.
        • Han K.
        • Kim M.J.
        • Lee Y.J.
        • Park Y.S.
        • et al.
        Use of imaging to predict complete response of colorectal liver metastases after chemotherapy: MR imaging versus CT imaging.
        Radiology. 2017; 284: 423-431
        • Kim S.S.
        • Song K.D.
        • Kim Y.K.
        • Kim H.C.
        • Huh J.W.
        • Park Y.S.
        • et al.
        Disappearing or residual tiny (≤5 mm) colorectal liver metastases after chemotherapy on gadoxetic acid-enhanced liver MRI and diffusion-weighted imaging: Is local treatment required?.
        Eur Radiol. 2017; 27: 3088-3096
        • Arita J.
        • Ono Y.
        • Takahashi M.
        • Inoue Y.
        • Takahashi Y.
        • Saiura A.
        Usefulness of contrast-enhanced intraoperative ultrasound in identifying disappearing liver metastases from colorectal carcinoma after chemotherapy.
        Ann Surg Oncol. 2014; 21: S390-S397https://doi.org/10.1245/s10434-014-3576-y
        • Oba A.
        • Mise Y.
        • Ito H.
        • Hiratsuka M.
        • Inoue Y.
        • Ishizawa T.
        • et al.
        Clinical implications of disappearing colorectal liver metastases have changed in the era of hepatocyte-specific MRI and contrast-enhanced intraoperative ultrasonography.
        HPB (Oxford). 2018; 20: 708-714
        • Owen J.W.
        • Fowler K.J.
        • Doyle M.B.
        • Saad N.E.
        • Linehan D.C.
        • Chapman W.C.
        Colorectal liver metastases: disappearing lesions in the era of Eovist hepatobiliary magnetic resonance imaging.
        HPB (Oxford). 2016; 18: 296-303https://doi.org/10.1016/j.hpb.2015.10.009
        • van Vledder M.G.
        • de Jong M.C.
        • Pawlik T.M.
        • Schulick R.D.
        • Diaz L.A.
        • Choti M.A.
        Disappearing colorectal liver metastases after chemotherapy: should we be concerned?.
        J Gastrointest Surg. 2010; 14: 1691-1700https://doi.org/10.1007/s11605-010-1348-y
        • Karoui M.
        • Penna C.
        • Amin-Hashem M.
        • Mitry E.
        • Benoist S.
        • Franc B.
        • et al.
        Influence of preoperative chemotherapy on the risk of major hepatectomy for colorectal liver metastases.
        Ann Surg. 2006; 243: 1-7
        • Kuhlmann K.
        • van Hilst J.
        • Fisher S.
        • Poston G.
        Management of disappearing colorectal liver metastases.
        Eur J Surg Oncol. 2016; 42: 1798-1805https://doi.org/10.1016/j.ejso.2016.05.005
        • Donati F.
        • Boraschi P.
        • Pacciardi F.
        • Cervelli R.
        • Castagna M.
        • Urbani L.
        • et al.
        3T diffusion-weighted MRI in the response assessment of colorectal liver metastases after chemotherapy: Correlation between ADC value and histological tumour regression grading.
        Eur J Radiol. 2017; 91: 57-65
        • Uutela A.
        • Ovissi A.
        • Hakkarainen A.
        • Ristimäki A.
        • Lundbom N.
        • Kallio R.
        • et al.
        Treatment response of colorectal cancer liver metastases to neoadjuvant or conversion therapy: a prospective multicentre follow-up study using MRI, diffusion-weighted imaging and 1H-MR spectroscopy compared with histology (subgroup in the RAXO trial).
        ESMO Open. 2021; 6: 100208
        • Boraschi P.
        • Donati F.
        • Cervelli R.
        • Pacciardi F.
        • Tarantini G.
        • Castagna M.
        • et al.
        Colorectal liver metastases: ADC as an imaging biomarker of tumor behavior and therapeutic response.
        Eur J Radiol. 2021; 137: 109609
        • Zaniboni A.
        • Savelli G.
        • Pizzocaro C.
        • Basile P.
        • Massetti V.
        Positron emission tomography for the response evaluation following treatment with chemotherapy in patients affected by colorectal liver metastases: a selected review.
        Gastroenterology Research and Practice. 2015; 2015: 1-7
        • Xia Q.
        • Liu J.
        • Wu C.
        • Song S.
        • Tong L.
        • Huang G.
        • et al.
        Prognostic significance of 18FDG PET/CT in colorectal cancer patients with liver metastases: a meta-analysis.
        Cancer Imaging. 2015; 15https://doi.org/10.1186/s40644-015-0055-z
        • Adie S.
        • Yip C.
        • Chu F.
        • Morris D.L.
        Resection of liver metastases from colorectal cancer: does preoperative chemotherapy affect the accuracy of PET in preoperative planning?.
        ANZ J Surg. 2009; 79: 358-361https://doi.org/10.1111/j.1445-2197.2009.04889.x
        • Dhir M.
        • Lyden E.R.
        • Wang A.
        • Smith L.M.
        • Ullrich F.
        • Are C.
        Influence of margins on overall survival after hepatic resection for colorectal metastasis: a meta-analysis.
        Ann Surg. 2011; 254: 234-242https://doi.org/10.1097/SLA.0b013e318223c609
        • de Haas R.J.
        • Wicherts D.A.
        • Flores E.
        • Azoulay D.
        • Castaing D.
        • Adam R.
        R1 resection by necessity for colorectal liver metastases: is it still a contraindication to surgery?.
        Ann Surg. 2008; 248: 626-637https://doi.org/10.1097/SLA.0b013e31818a07f1
        • Nuzzo G.
        • Giuliante F.
        • Ardito F.
        • Vellone M.
        • Giovannini I.
        • Federico B.
        • et al.
        Influence of surgical margin on type of recurrence after liver resection for colorectal metastases: a single-center experience.
        Surgery. 2008; 143: 384-393
        • Margonis G.A.
        • Sergentanis T.N.
        • Ntanasis-Stathopoulos I.
        • Andreatos N.
        • Tzanninis I.-G.
        • Sasaki K.
        • 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: 1047-1055
        • Margonis G.A.
        • Sasaki K.
        • Andreatos N.
        • Kim Y.
        • Merath K.
        • Wagner D.
        • et al.
        KRAS mutation status dictates optimal surgical margin width in patients undergoing resection of colorectal liver metastases.
        Ann Surg Oncol. 2017; 24: 264-271
        • Andreou A.
        • Knitter S.
        • Schmelzle M.
        • Kradolfer D.
        • Maurer M.H.
        • Auer T.A.
        • et al.
        Recurrence at surgical margin following hepatectomy for colorectal liver metastases is not associated with R1 resection and does not impact survival.
        Surgery. 2021; 169: 1061-1068
        • Viganò L.
        • Procopio F.
        • Cimino M.M.
        • Donadon M.
        • Gatti A.
        • Costa G.
        • et al.
        Is tumor detachment from vascular structures equivalent to r0 resection in surgery for colorectal liver metastases? An observational cohort.
        Ann Surg Oncol. 2016; 23: 1352-1360
        • Rubbia-Brandt L.
        • Giostra E.
        • Brezault C.
        • Roth A.D.
        • Andres A.
        • Audard V.
        • et al.
        Importance of histological tumor response assessment in predicting the outcome in patients with colorectal liver metastases treated with neo-adjuvant chemotherapy followed by liver surgery.
        Ann Oncol. 2007; 18: 299-304
      4. Viganò L, Capussotti L, De Rosa G, De Saussure WO, Mentha G, Rubbia-Brandt L. Liver resection for colorectal metastases after chemotherapy: impact of chemotherapy-related liver injuries, pathological tumor response, and micrometastases on long-term survival. Ann Surg 2013;258:731–40; discussion 741-742. https://doi.org/10.1097/SLA.0b013e3182a6183e.

        • Xu D.
        • Yan X.-L.
        • Liu J.-M.
        • Li J.
        • Xing B.-C.
        The characteristics and long-term survival of patients with colorectal liver metastases with pathological complete response after chemotherapy.
        J Cancer. 2020; 11: 6256-6263https://doi.org/10.7150/jca.47911
        • Margonis G.A.
        • Amini N.
        • Andreatos N.
        • Sasaki K.
        • McVey J.
        • Mirza M.B.
        • et al.
        KRAS mutational status impacts pathologic response to pre-hepatectomy chemotherapy: a study from the International Genetic Consortium for Liver Metastases.
        HPB (Oxford). 2019; 21: 1527-1534
        • Vera R.
        • Gomez Dorronsoro M.
        • Lopez-Ben S.
        • Viudez A.
        • Queralt B.
        • Hernandez I.
        • et al.
        Retrospective analysis of pathological response in colorectal cancer liver metastases following treatment with bevacizumab.
        Clin Transl Oncol. 2014; 16: 739-745
        • Noepel-Duennebacke S.
        • Juette H.
        • Lugnier C.
        • Paul Modest D.
        • Martens U.
        • Klaassen-Mielke R.
        • et al.
        Histopathologic Regression and Survival in RAS Wildtype Metastatic Colorectal Cancer Under First-Line Treatment – Subgroup Analysis of the VOLFI Trial (AIO-KRK-0109).
        Int J Clin Oncol Cancer Res. 2021; 6: 130
        • Wang Y.
        • Yuan Y.-F.
        • Lin H.-C.
        • Li B.-K.
        • Wang F.-H.
        • Wang Z.-Q.
        • et al.
        Pathologic response after preoperative therapy predicts prognosis of Chinese colorectal cancer patients with liver metastases.
        Chin J Cancer. 2017; 36https://doi.org/10.1186/s40880-017-0244-1
        • Carrasco J.
        • Gizzi M.
        • Pairet G.
        • Lannoy V.
        • Lefesvre P.
        • Gigot J.-F.
        • et al.
        Pathological responses after angiogenesis or EGFR inhibitors in metastatic colorectal cancer depend on the chemotherapy backbone.
        Br J Cancer. 2015; 113: 1298-1304
        • Loupakis F.
        • Schirripa M.
        • Caparello C.
        • Funel N.
        • Pollina L.
        • Vasile E.
        • et al.
        Histopathologic evaluation of liver metastases from colorectal cancer in patients treated with FOLFOXIRI plus bevacizumab.
        Br J Cancer. 2013; 108: 2549-2556
        • Cremolini C.
        • Milione M.
        • Marmorino F.
        • Morano F.
        • Zucchelli G.
        • Mennitto A.
        • et al.
        Differential histopathologic parameters in colorectal cancer liver metastases resected after triplets plus bevacizumab or cetuximab: a pooled analysis of five prospective trials.
        Br J Cancer. 2018; 118: 955-965
        • van Dam P.-J.
        • van der Stok E.P.
        • Teuwen L.-A.
        • Van den Eynden G.G.
        • Illemann M.
        • Frentzas S.
        • et al.
        International consensus guidelines for scoring the histopathological growth patterns of liver metastasis.
        Br J Cancer. 2017; 117: 1427-1441
        • Stremitzer S.
        • Vermeulen P.
        • Graver S.
        • Kockx M.
        • Dirix L.
        • Yang D.
        • et al.
        Immune phenotype and histopathological growth pattern in patients with colorectal liver metastases.
        Br J Cancer. 2020; 122: 1518-1524
        • Antoniotti C.
        • Pietrantonio F.
        • Corallo S.
        • De Braud F.
        • Falcone A.
        • Cremolini C.
        Circulating tumor DNA analysis in colorectal cancer: from dream to reality.
        JCO Precision Oncology. 2019; : 1-14https://doi.org/10.1200/PO.18.00397
        • Jones R.P.
        • Pugh S.A.
        • Graham J.
        • Primrose J.N.
        • Barriuso J.
        Circulating tumour DNA as a biomarker in resectable and irresectable stage IV colorectal cancer; a systematic review and meta-analysis.
        Eur J Cancer. 2021; 144: 368-381https://doi.org/10.1016/j.ejca.2020.11.025
        • Kobayashi S.
        • Nakamura Y.
        • Taniguchi H.
        • Odegaard J.I.
        • Nomura S.
        • Kojima M.
        • et al.
        Impact of preoperative circulating tumor DNA status on survival outcomes after hepatectomy for resectable colorectal liver metastases.
        Ann Surg Oncol. 2021; 28: 4744-4755
        • Bidard F.-C.
        • Kiavue N.
        • Ychou M.
        • Cabel L.
        • Stern M.-H.
        • Madic J.
        • et al.
        Circulating tumor cells and circulating tumor DNA detection in potentially resectable metastatic colorectal cancer: a prospective ancillary study to the unicancer prodige-14 trial.
        Cells. 2019; 8: 516
        • Loupakis F.
        • Sharma S.
        • Derouazi M.
        • Murgioni S.
        • Biason P.
        • Rizzato M.D.
        • et al.
        Detection of molecular residual disease using personalized circulating tumor DNA assay in patients with colorectal cancer undergoing resection of metastases.
        JCO Precis Oncol. 2021; : 1166-1177
        • Fiz F.
        • Viganò L.
        • Gennaro N.
        • Costa G.
        • La Bella L.
        • Boichuk A.
        • et al.
        Radiomics of liver metastases: a systematic review.
        Cancers (Basel). 2020; 12: 2881
        • Beckers R.C.J.
        • Trebeschi S.
        • Maas M.
        • Schnerr R.S.
        • Sijmons J.M.L.
        • Beets G.L.
        • et al.
        CT texture analysis in colorectal liver metastases and the surrounding liver parenchyma and its potential as an imaging biomarker of disease aggressiveness, response and survival.
        Eur J Radiol. 2018; 102: 15-21
        • Rahmim A.
        • Bak-Fredslund K.P.
        • Ashrafinia S.
        • Lu L.
        • Schmidtlein C.R.
        • Subramaniam R.M.
        • et al.
        Prognostic modeling for patients with colorectal liver metastases incorporating FDG PET radiomic features.
        Eur J Radiol. 2019; 113: 101-109
        • Shur J.
        • Orton M.
        • Connor A.
        • Fischer S.
        • Moulton C.-A.
        • Gallinger S.
        • et al.
        A clinical-radiomic model for improved prognostication of surgical candidates with colorectal liver metastases.
        J Surg Oncol. 2020; 121: 357-364
        • Ma Y.-Q.
        • Wen Y.
        • Liang H.
        • Zhong J.-G.
        • Pang P.-P.
        Magnetic resonance imaging-radiomics evaluation of response to chemotherapy for synchronous liver metastasis of colorectal cancer.
        World J Gastroenterol. 2021; 27: 6465-6475https://doi.org/10.3748/wjg.v27.i38.6465
        • Zhang H.
        • Li W.
        • Hu F.
        • Sun Y.
        • Hu T.
        • Tong T.
        MR texture analysis: potential imaging biomarker for predicting the chemotherapeutic response of patients with colorectal liver metastases.
        Abdom Radiol (NY). 2019; 44: 65-71https://doi.org/10.1007/s00261-018-1682-1
        • Fridman W.H.
        • Zitvogel L.
        • Sautès-Fridman C.
        • Kroemer G.
        The immune contexture in cancer prognosis and treatment.
        Nat Rev Clin Oncol. 2017; 14: 717-734https://doi.org/10.1038/nrclinonc.2017.101
        • Junttila M.R.
        • de Sauvage F.J.
        Influence of tumour micro-environment heterogeneity on therapeutic response.
        Nature. 2013; 501: 346-354https://doi.org/10.1038/nature12626
        • Moretto R.
        • Corallo S.
        • Belfiore A.
        • Rossini D.
        • Boccaccino A.
        • Lonardi S.
        • et al.
        Prognostic impact of immune-microenvironment in colorectal liver metastases resected after triplets plus a biologic agent: A pooled analysis of five prospective trials.
        Eur J Cancer. 2020; 135: 78-88
        • Tanis E.
        • Julié C.
        • Emile J.-F.
        • Mauer M.
        • Nordlinger B.
        • Aust D.
        • et al.
        Prognostic impact of immune response in resectable colorectal liver metastases treated by surgery alone or surgery with perioperative FOLFOX in the randomised EORTC study 40983.
        Eur J Cancer. 2015; 51: 2708-2717
        • Donadon M.
        • Torzilli G.
        • Cortese N.
        • Soldani C.
        • Di Tommaso L.
        • Franceschini B.
        • et al.
        Macrophage morphology correlates with single-cell diversity and prognosis in colorectal liver metastasis.
        J Exp Med. 2020; 217e20191847https://doi.org/10.1084/jem.20191847
        • Arnold D.
        • Lueza B.
        • Douillard J.-Y.
        • Peeters M.
        • Lenz H.-J.
        • Venook A.
        • et al.
        Prognostic and predictive value of primary tumour side in patients with RAS wild-type metastatic colorectal cancer treated with chemotherapy and EGFR directed antibodies in six randomized trials.
        Ann Oncol. 2017; 28: 1713-1729
        • Holch J.W.
        • Ricard I.
        • Stintzing S.
        • Modest D.P.
        • Heinemann V.
        The relevance of primary tumour location in patients with metastatic colorectal cancer: A meta-analysis of first-line clinical trials.
        Eur J Cancer. 2017; 70: 87-98https://doi.org/10.1016/j.ejca.2016.10.007
        • Cremolini C.
        • Antoniotti C.
        • Stein A.
        • Bendell J.
        • Gruenberger T.
        • Rossini D.
        • et al.
        Individual patient data meta-analysis of FOLFOXIRI plus bevacizumab versus doublets plus bevacizumab as initial therapy of unresectable metastatic colorectal cancer.
        J Clin Oncol. 2020; 38: 3314-3324
        • Kishi Y.
        • Zorzi D.
        • Contreras C.M.
        • Maru D.M.
        • Kopetz S.
        • Ribero D.
        • et al.
        Extended preoperative chemotherapy does not improve pathologic response and increases postoperative liver insufficiency after hepatic resection for colorectal liver metastases.
        Ann Surg Oncol. 2010; 17: 2870-2876