Refining adjuvant therapy for non-metastatic colon cancer, new standards and perspectives

Stewart, 2014 Lecomte T, André T, Panis Y, Laurent-Puig P, Bibeau F, Taieb J. Cancer du Colon. In: Thésaurus National de Cancérologie Digestive [Internet]; 2018. Available from: <http://www.tncd.org>. Van Cutsem, 2016, ESMO consensus guidelines for the management of patients with metastatic colorectal cancer, Ann Oncol Off J Eur Soc Med Oncol ESMO, 27, 1386, 10.1093/annonc/mdw235 Gunderson, 2010, Revised TN categorization for colon cancer based on national survival outcomes data, J Clin Oncol Off J Am Soc Clin Oncol, 28, 264, 10.1200/JCO.2009.24.0952 Quasar Collaborative Group, 2007, Adjuvant chemotherapy versus observation in patients with colorectal cancer: a randomised study, Lancet, 370, 2020, 10.1016/S0140-6736(07)61866-2 Efficacy of adjuvant fluorouracil and folinic acid in B2 colon cancer, 1999, International multicentre pooled analysis of B2 colon cancer trials (IMPACT B2) investigators, J Clin Oncol Off J Am Soc Clin Oncol, 17, 1356 Smith, 2004, Randomized trial of adjuvant therapy in colon carcinoma: 10-year results of NSABP protocol C-01, J Natl Cancer Inst., 96, 1128, 10.1093/jnci/djh220 Wolmark, 2001, National surgical adjuvant breast and bowel project trials in colon cancer, Semin Oncol., 28, 9, 10.1016/S0093-7754(01)90245-3 Wolmark, 1990, Adjuvant therapy of Dukes’ A, B, and C adenocarcinoma of the colon with portal-vein fluorouracil hepatic infusion: preliminary results of National Surgical Adjuvant Breast and Bowel Project Protocol C-02, J Clin Oncol Off J Am Soc Clin Oncol, 8, 1466, 10.1200/JCO.1990.8.9.1466 André, 2004, Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer, N Engl J Med, 350, 2343, 10.1056/NEJMoa032709 André, 2015, Adjuvant fluorouracil, leucovorin, and oxaliplatin in stage II to III colon cancer: updated 10-year survival and outcomes according to BRAF mutation and mismatch repair status of the MOSAIC study, J Clin Oncol Off J Am Soc Clin Oncol, 33, 4176, 10.1200/JCO.2015.63.4238 Ribic, 2003, Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer, N Engl J Med, 349, 247, 10.1056/NEJMoa022289 Moertel, 1990, Levamisole and fluorouracil for adjuvant therapy of resected colon carcinoma, N Engl J Med, 322, 352, 10.1056/NEJM199002083220602 Zaniboni, 1998, Cancer, 82, 2135, 10.1002/(SICI)1097-0142(19980601)82:11<2135::AID-CNCR7>3.0.CO;2-U André, 2007, Phase III study comparing a semimonthly with a monthly regimen of fluorouracil and leucovorin as adjuvant treatment for stage II and III colon cancer patients: final results of GERCOR C96.1, J Clin Oncol Off J Am Soc Clin Oncol, 25, 3732, 10.1200/JCO.2007.12.2234 Köhne, 2013, Eur J Cancer Oxf Engl 1990, 49, 1868 Twelves, 2005, Capecitabine as adjuvant treatment for stage III colon cancer, N Engl J Med, 352, 2696, 10.1056/NEJMoa043116 Scheithauer, 2003, Oral capecitabine as an alternative to i.v. 5-fluorouracil-based adjuvant therapy for colon cancer: safety results of a randomized, phase III trial, Ann Oncol Off J Eur Soc Med Oncol, 14, 1735, 10.1093/annonc/mdg500 Hamaguchi, 2011, Final results of randomized trials by the National Surgical Adjuvant Study of Colorectal Cancer (NSAS-CC), Cancer Chemother Pharmacol, 67, 587, 10.1007/s00280-010-1358-1 Kato, 2002, Efficacy of oral UFT as adjuvant chemotherapy to curative resection of colorectal cancer: multicenter prospective randomized trial, Langenbecks Arch Surg, 386, 575, 10.1007/s00423-002-0278-x Hamaguchi, 2018, Capecitabine versus S-1 as adjuvant chemotherapy for patients with stage III colorectal cancer (JCOG0910): an open-label, non-inferiority, randomised, phase 3, multicentre trial, Lancet Gastroenterol Hepatol, 3, 47, 10.1016/S2468-1253(17)30297-2 Yothers, 2011, Oxaliplatin as adjuvant therapy for colon cancer: updated results of NSABP C-07 trial, including survival and subset analyses, J Clin Oncol Off J Am Soc Clin Oncol, 29, 3768, 10.1200/JCO.2011.36.4539 Schmoll, 2015, Capecitabine plus oxaliplatin compared with fluorouracil/folinic acid as adjuvant therapy for stage III colon cancer: final results of the NO16968 randomized controlled phase III trial, J Clin Oncol Off J Am Soc Clin Oncol, 33, 3733, 10.1200/JCO.2015.60.9107 Haller, 2011, Capecitabine plus oxaliplatin compared with fluorouracil and folinic acid as adjuvant therapy for stage III colon cancer, J Clin Oncol Off J Am Soc Clin Oncol, 29, 1465, 10.1200/JCO.2010.33.6297 Shah, 2016, Impact of patient factors on recurrence risk and time dependency of oxaliplatin benefit in patients with colon cancer: analysis from modern-era adjuvant studies in the adjuvant colon cancer end points (ACCENT) database, J Clin Oncol Off J Am Soc Clin Oncol, 34, 843, 10.1200/JCO.2015.63.0558 Ychou, 2009, A phase III randomised trial of LV5FU2 + irinotecan versus LV5FU2 alone in adjuvant high-risk colon cancer (FNCLCC Accord02/FFCD9802), Ann Oncol Off J Eur Soc Med Oncol ESMO, 20, 674, 10.1093/annonc/mdn680 Saltz, 2007, Irinotecan fluorouracil plus leucovorin is not superior to fluorouracil plus leucovorin alone as adjuvant treatment for stage III colon cancer: results of CALGB 89803, J Clin Oncol Off J Am Soc Clin Oncol, 25, 3456, 10.1200/JCO.2007.11.2144 Van Cutsem, 2009, Randomized phase III trial comparing biweekly infusional fluorouracil/leucovorin alone or with irinotecan in the adjuvant treatment of stage III colon cancer: PETACC-3, J Clin Oncol Off J Am Soc Clin Oncol, 27, 3117, 10.1200/JCO.2008.21.6663 Allegra, 2011, Phase III trial assessing bevacizumab in stages II and III carcinoma of the colon: results of NSABP protocol C-08, J Clin Oncol Off J Am Soc Clin Oncol, 29, 11, 10.1200/JCO.2010.30.0855 Allegra, 2013, Bevacizumab in stage II–III colon cancer: 5-year update of the National Surgical Adjuvant Breast and Bowel Project C-08 trial, J Clin Oncol Off J Am Soc Clin Oncol, 31, 359, 10.1200/JCO.2012.44.4711 de Gramont, 2012, Bevacizumab plus oxaliplatin-based chemotherapy as adjuvant treatment for colon cancer (AVANT): a phase 3 randomised controlled trial, Lancet Oncol, 13, 1225, 10.1016/S1470-2045(12)70509-0 Alberts, 2012, Effect of oxaliplatin, fluorouracil, and leucovorin with or without cetuximab on survival among patients with resected stage III colon cancer: a randomized trial, JAMA, 307, 1383, 10.1001/jama.2012.385 Taieb, 2014, Oxaliplatin, fluorouracil, and leucovorin with or without cetuximab in patients with resected stage III colon cancer (PETACC-8): an open-label, randomised phase 3 trial, Lancet Oncol, 15, 862, 10.1016/S1470-2045(14)70227-X Taieb, 2017, Adjuvant FOLFOX +/− cetuximab in full RAS and BRAF wildtype stage III colon cancer patients, Ann Oncol Off J Eur Soc Med Oncol, 28, 824, 10.1093/annonc/mdw687 Des Guetz, 2010, Does delaying adjuvant chemotherapy after curative surgery for colorectal cancer impair survival? A meta-analysis, Eur J Cancer Oxf Engl 1990, 46, 1049 Hershman, 2006, Timing of adjuvant chemotherapy initiation after surgery for stage III colon cancer, Cancer, 107, 2581, 10.1002/cncr.22316 Gao, 2018, Impact of timing of adjuvant chemotherapy on survival in stage III colon cancer: a population-based study, BMC Cancer, 18, 234, 10.1186/s12885-018-4138-7 Kim, 2017, The impact of delayed commencement of adjuvant chemotherapy (eight or more weeks) on survival in stage II and III colon cancer: a national population-based cohort study, Oncotarget, 8, 80061, 10.18632/oncotarget.17767 Turner, 2018, Delay in adjuvant chemotherapy and survival advantage in stage III colon cancer, J Am Coll Surg, 226, 670, 10.1016/j.jamcollsurg.2017.12.048 Grothey, 2018, Duration of adjuvant chemotherapy for stage III colon cancer, N Engl J Med, 378, 1177, 10.1056/NEJMoa1713709 Sadahiro, 2015, Randomized phase III trial of treatment duration for oral uracil and tegafur plus leucovorin as adjuvant chemotherapy for patients with stage IIB/III colon cancer: final results of JFMC33-0502, Ann Oncol Off J Eur Soc Med Oncol, 26, 2274, 10.1093/annonc/mdv358 O’Connell, 1998, Prospectively randomized trial of postoperative adjuvant chemotherapy in patients with high-risk colon cancer, J Clin Oncol Off J Am Soc Clin Oncol, 16, 295, 10.1200/JCO.1998.16.1.295 Haller, 2005, Phase III study of fluorouracil, leucovorin, and levamisole in high-risk stage II and III colon cancer: final report of Intergroup 0089, J Clin Oncol Off J Am Soc Clin Oncol, 23, 8671, 10.1200/JCO.2004.00.5686 Chau, 2005, Longitudinal quality of life and quality adjusted survival in a randomised controlled trial comparing six months of bolus fluorouracil/leucovorin vs. twelve weeks of protracted venous infusion fluorouracil as adjuvant chemotherapy for colorectal cancer, Eur J Cancer Oxf Engl 1990, 41, 1551 Sobrero, 2018, FOLFOX or CAPOX in stage II to III colon cancer: efficacy results of the italian three or six colon adjuvant trial, J Clin Oncol Off J Am Soc Clin Oncol, 36, 1478, 10.1200/JCO.2017.76.2187 André, 2018, Three versus 6 months of oxaliplatin-based adjuvant chemotherapy for patients with stage III colon cancer: disease-free survival results from a randomized, open-label, international duration evaluation of adjuvant (IDEA) France, phase III trial, J Clin Oncol Off J Am Soc Clin Oncol, 36, 1469, 10.1200/JCO.2017.76.0355 Kotaka, 2018, Safety data from the phase III Japanese ACHIEVE trial: part of an international, prospective, planned pooled analysis of six phase III trials comparing 3 versus 6 months of oxaliplatin-based adjuvant chemotherapy for stage III colon cancer, ESMO Open, 3, e000354, 10.1136/esmoopen-2018-000354 Iveson, 2018, 3 versus 6 months of adjuvant oxaliplatin-fluoropyrimidine combination therapy for colorectal cancer (SCOT): an international, randomised, phase 3, non-inferiority trial, Lancet Oncol, 19, 562, 10.1016/S1470-2045(18)30093-7 Lonardi, 2016, Phase III trial comparing 3–6 months of adjuvant FOLFOX4/XELOX in stage II–III colon cancer: safety and compliance in the TOSCA trial, Ann Oncol Off J Eur Soc Med Oncol, 27, 2074, 10.1093/annonc/mdw404 FOxTROT Collaborative Group, 2012, Feasibility of preoperative chemotherapy for locally advanced, operable colon cancer: the pilot phase of a randomised controlled trial, Lancet Oncol, 13, 1152, 10.1016/S1470-2045(12)70348-0 Jakobsen, 2015, Neoadjuvant chemotherapy in locally advanced colon cancer. A phase II trial, Acta Oncol Stockh Swed., 54, 1747, 10.3109/0284186X.2015.1037007 Karoui, 2017, Neoadjuvant FOLFOX 4 versus FOLFOX 4 plus cetuximab versus immediate surgery for high-risk stage II and III colon cancers: a phase II multicentre randomised controlled trial (PRODIGE 22), Ann Oncol, 28, v158 Sargent, 2001, A pooled analysis of adjuvant chemotherapy for resected colon cancer in elderly patients, N Engl J Med, 345, 1091, 10.1056/NEJMoa010957 Mayer, 2015, Stratified survival analysis after adjuvant chemotherapy of colon cancer reveals a benefit for older patients, Anticancer Res, 35, 5587 Haller, 2015, Impact of age and medical comorbidity on adjuvant treatment outcomes for stage III colon cancer: a pooled analysis of individual patient data from four randomized, controlled trials, Ann Oncol Off J Eur Soc Med Oncol, 26, 715, 10.1093/annonc/mdv003 Tournigand, 2012, J Clin Oncol Off J Am Soc Clin Oncol, 30, 3353, 10.1200/JCO.2012.42.5645 Sanoff, 2012, Effect of adjuvant chemotherapy on survival of patients with stage III colon cancer diagnosed after age 75 years, J Clin Oncol Off J Am Soc Clin Oncol, 30, 2624, 10.1200/JCO.2011.41.1140 McCleary, 2013, Impact of age on the efficacy of newer adjuvant therapies in patients with stage II/III colon cancer: findings from the ACCENT database, J Clin Oncol Off J Am Soc Clin Oncol, 31, 2600, 10.1200/JCO.2013.49.6638 Konishi, 2018, Association of preoperative and postoperative serum carcinoembryonic antigen and colon cancer outcome, JAMA Oncol, 4, 309, 10.1001/jamaoncol.2017.4420 Auclin E, Taieb J, Lepage C, Aparicio T, Faroux R, Mini E, et al. Carcinoembryonic antigen levels and survival in stage III colon cancer: post hoc analysis of the MOSAIC and PETACC-8 trials. Cancer Epidemiol Biomarkers Prev [in press]. Auclin, 2018, Low-level postoperative carcinoembryonic antigen improves survival outcomes stratification in patients with stage II colon cancer treated with standard adjuvant treatments, Eur J Cancer Oxf Engl 1990, 97, 55 Margalit, 2018, Assessing the prognostic value of carcinoembryonic antigen levels in stage I and II colon cancer, Eur J Cancer Oxf Engl 1990, 194, 1 Kim, 2017, Preoperative serum carcinoembryonic antigen level as a prognostic factor for recurrence and survival after curative resection followed by adjuvant chemotherapy in stage III colon cancer, Ann Surg Oncol, 24, 227, 10.1245/s10434-016-5613-5 Yothers, 2013, Validation of the 12-gene colon cancer recurrence score in NSABP C-07 as a predictor of recurrence in patients with stage II and III colon cancer treated with fluorouracil and leucovorin (FU/LV) and FU/LV plus oxaliplatin, J Clin Oncol Off J Am Soc Clin Oncol, 31, 4512, 10.1200/JCO.2012.47.3116 Jiang, 2008, Development of a clinically feasible molecular assay to predict recurrence of stage II colon cancer, J Mol Diagn JMD, 10, 346, 10.2353/jmoldx.2008.080011 Salazar, 2011, Gene expression signature to improve prognosis prediction of stage II and III colorectal cancer, J Clin Oncol Off J Am Soc Clin Oncol, 29, 17, 10.1200/JCO.2010.30.1077 Galon, 2006, Type, density, and location of immune cells within human colorectal tumors predict clinical outcome, Science, 313, 1960, 10.1126/science.1129139 Galon, 2014, Towards the introduction of the “Immunoscore” in the classification of malignant tumours, J Pathol, 232, 199, 10.1002/path.4287 Galon, 2007, The adaptive immunologic microenvironment in colorectal cancer: a novel perspective, Cancer Res, 67, 1883, 10.1158/0008-5472.CAN-06-4806 Galon J, Mlecnik B, Marliot F, Ou F-S, Bifulco CB, Lugli A, et al. Validation of the Immunoscore (IM) as a prognostic marker in stage I/II/III colon cancer: Results of a worldwide consortium-based analysis of 1336 patients. J Clin Oncol [Internet] 2016 [cited 2016 Dec 14];34(suppl; abstr 3500). Available from: <http://meetinglibrary.asco.org/content/168666-176>. Emile J-F, Malicot KL, Tabernero J, Mini E, Folprecht G, Laethem J-LV, et al. Validation of the prognostic impact of lymphocyte infiltration (LI) in patients (pts) with stage III colon cancer (CC) treated with adjuvant FOLFOX+/− cetuximab: A PETACC8 translational study. J Clin Oncol [Internet] 2016 [cited 2016 Dec 14];34(suppl 4S; abstr 553). Available from: <http://meetinglibrary.asco.org/content/158705-173>. Pagès, 2018, International validation of the consensus immunoscore for the classification of colon cancer: a prognostic and accuracy study, Lancet Lond Engl, 391, 2128, 10.1016/S0140-6736(18)30789-X Galon, 2019, Immunoscore clinical utility to identify good prognostic colon cancer stage II patients with high-risk clinico-pathological features for whom adjuvant treatment may be avoided, J Clin Oncol, 37, 10.1200/JCO.2019.37.4_suppl.487 Taieb, 2016, Prognostic effect of BRAF and KRAS mutations in patients with stage III colon cancer treated with leucovorin, fluorouracil, and oxaliplatin with or without cetuximab: a post hoc analysis of the PETACC-8 trial, JAMA Oncol, 14, 1 Taieb, 2017, Prognostic value of BRAF and KRAS mutations in MSI and MSS stage III colon cancer, J Natl Cancer Inst, 109, 10.1093/jnci/djw272 Gallois, 2018, Prognostic value of methylator phenotype in stage III colon cancer treated with oxaliplatin-based adjuvant chemotherapy, Clin Cancer Res Off J Am Assoc Cancer Res, 24, 4745, 10.1158/1078-0432.CCR-18-0866 Gallois, 2016, Methylator phenotype in colorectal cancer: A prognostic factor or not?, Crit Rev Oncol Hematol, 99, 74, 10.1016/j.critrevonc.2015.11.001 Hinoi, 2001, Loss of CDX2 expression and microsatellite instability are prominent features of large cell minimally differentiated carcinomas of the colon, Am J Pathol., 159, 2239, 10.1016/S0002-9440(10)63074-X Lugli, 2008, Differential diagnostic and functional role of the multi-marker phenotype CDX2/CK20/CK7 in colorectal cancer stratified by mismatch repair status, Mod Pathol Off J U S Can Acad Pathol Inc, 21, 1403 Baba, 2009, Relationship of CDX2 loss with molecular features and prognosis in colorectal cancer, Clin Cancer Res Off J Am Assoc Cancer Res, 15, 4665, 10.1158/1078-0432.CCR-09-0401 Bae, 2015, Loss of CDX2 expression is associated with poor prognosis in colorectal cancer patients, World J Gastroenterol, 21, 1457, 10.3748/wjg.v21.i5.1457 Dalerba, 2016, CDX2 as a prognostic biomarker in stage II and stage III colon cancer, N Engl J Med, 374, 211, 10.1056/NEJMoa1506597 Liao, 2012, Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival, N Engl J Med, 367, 1596, 10.1056/NEJMoa1207756 Ng, 2015, Aspirin and COX-2 inhibitor use in patients with stage III colon cancer, J Natl Cancer Inst, 107, 345, 10.1093/jnci/dju345 Fan, 2017, Prognostic value of circulating tumor DNA in patients with colon cancer: systematic review, PLoS ONE, 12, e0171991, 10.1371/journal.pone.0171991 Lecomte, 2002, Detection of free-circulating tumor-associated DNA in plasma of colorectal cancer patients and its association with prognosis, Int J Cancer, 100, 542, 10.1002/ijc.10526 Tie, 2016, Circulating tumor DNA analysis detects minimal residual disease and predicts recurrence in patients with stage II colon cancer, Sci Transl Med, 8, 346ra92, 10.1126/scitranslmed.aaf6219 Overman, 2017, Nivolumab in patients with metastatic DNA mismatch repair-deficient or microsatellite instability-high colorectal cancer (CheckMate 142): an open-label, multicentre, phase 2 study, Lancet Oncol, 18, 1182, 10.1016/S1470-2045(17)30422-9 Weber, 2017, Adjuvant nivolumab versus ipilimumab in resected stage III or IV melanoma, N Engl J Med, 377, 1824, 10.1056/NEJMoa1709030 Sartore-Bianchi, 2016, Dual-targeted therapy with trastuzumab and lapatinib in treatment-refractory, KRAS codon 12/13 wild-type, HER2-positive metastatic colorectal cancer (HERACLES): a proof-of-concept, multicentre, open-label, phase 2 trial, Lancet Oncol, 17, 738, 10.1016/S1470-2045(16)00150-9