Homogeneity in immune features between colorectal liver metastases better identifies patients with good prognosis compared to pathological response to preoperative chemotherapy

References

• Pages F, Mlecnik B, Marliot F, Bindea G, Ou F-S, Bifulco C, Lugli A, Zlobec I, Rau TT, Berger MD, et al. International validation of the consensus immunoscore for the classification of colon cancer: a prognostic and accuracy study. Lancet. 2018 May 26;391(10135):2128–8. doi:10.1016/S0140-6736(18)30789-X.
   PubMed Web of Science ®Google Scholar
• Sveen A, Loes IM, Alagaratnam S, Nilsen G, Høland M, Lingjærde OC, Sorbye H, Berg KCG, Horn A, Angelsen J-H, et al. Intra-patient inter-metastatic genetic heterogeneity in colorectal cancer as a key determinant of survival after curative liver resection. PLoS Genet. 2016 Jul;12(7):e1006225. doi:10.1371/journal.pgen.1006225.
   PubMed Web of Science ®Google Scholar
• Angelova M, Mlecnik B, Vasaturo A, Bindea G, Fredriksen T, Lafontaine L, Buttard B, Morgand E, Bruni D, Jouret-Mourin A, et al. Evolution of metastases in space and time under immune selection. Cell. 2018 Oct 18;175(3):751–765.e16. doi:10.1016/j.cell.2018.09.018.
   PubMed Web of Science ®Google Scholar
• Reuben A, Spencer CN, Prieto PA, Gopalakrishnan V, Reddy SM, Miller JP, Mao X, De Macedo MP, Chen J, Song X, et al. Genomic and immune heterogeneity are associated with differential responses to therapy in melanoma. NPJ Genom Med. 2017;2(1). doi:10.1038/s41525-017-0013-8.
   PubMedGoogle Scholar
• Tomlinson JS, Jarnagin WR, DeMatteo RP, Fong Y, Kornprat P, Gonen M, Kemeny N, Brennan MF, Blumgart LH, D’Angelica M, et al. Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol. 2007 Oct 10;25(29):4575–4580. doi:10.1200/JCO.2007.11.0833.
   PubMed Web of Science ®Google Scholar
• Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Annals Of Surgery. 1999 Sep;230(3):309–318. discussion 318-21. doi:10.1097/00000658-199909000-00004.
   PubMed Web of Science ®Google Scholar
• Tsilimigras DI, Ntanasis-Stathopoulos I, Bagante F, Moris D, Cloyd J, Spartalis E, Pawlik TM. Clinical significance and prognostic relevance of KRAS, BRAF, PI3K and TP53 genetic mutation analysis for resectable and unresectable colorectal liver metastases: A systematic review of the current evidence. Surg Oncol. 2018 Jun;27(2):280–288. doi:10.1016/j.suronc.2018.05.012.
   PubMed Web of Science ®Google Scholar
• Rubbia-Brandt L, Giostra E, Brezault C, Roth AD, Andres A, Audard V, Sartoretti P, Dousset B, Majno PE, Soubrane O, 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 Feb;18(2):299–304. doi:10.1093/annonc/mdl386.
   PubMed Web of Science ®Google Scholar
• Blazer DG 3rd, Kishi Y, Maru DM, Kopetz S, Chun YS, Overman MJ, Fogelman D, Eng C, Chang DZ, Wang H, et al. Pathologic response to preoperative chemotherapy: a new outcome end point after resection of hepatic colorectal metastases. J Clin Oncol. 2008 Nov 20;26(33):5344–5351. doi:10.1200/JCO.2008.17.5299.
   PubMed Web of Science ®Google Scholar
• Baldin P, Van den Eynde M, Mlecnik B, Bindea G, Beniuga G, Carrasco J, Haicheur N, Marliot F, Lafontaine L, Fredriksen T, et al. Prognostic assessment of resected colorectal liver metastases integrating pathological features, RAS mutation and Immunoscore. J Pathol Clin Res. 2021 Jan;7(1):27–41. doi:10.1002/cjp2.178.
   PubMedGoogle Scholar
• Van den Eynde M, Mlecnik B, Bindea G, Fredriksen T, Church SE, Lafontaine L, Haicheur N, Marliot F, Angelova M, Vasaturo A, et al. The link between the multiverse of immune microenvironments in metastases and the survival of colorectal cancer patients. Cancer Cell. 2018 Dec 10;34(6):1012–1026.e3. doi:10.1016/j.ccell.2018.11.003.
   PubMed Web of Science ®Google Scholar
• Mlecnik B, Van den Eynde M, Bindea G, Church SE, Vasaturo A, Fredriksen T, Lafontaine L, Haicheur N, Marliot F, Debetancourt D, et al. Comprehensive intrametastatic immune quantification and major impact of immunoscore on survival. J Natl Cancer Inst. 2018 Jan 1;110(1):97–108. doi:10.1093/jnci/djx123.
   Google Scholar
• Messaoudi N, Henault D, Stephen D, Cousineau I, Simoneau E, Rong Z, Létourneau R, Plasse M, Dagenais M, Roy A, et al. Prognostic implications of adaptive immune features in MMR-proficient colorectal liver metastases classified by histopathological growth patterns. Br J Cancer. 2022 May;126(9):1329–1338. doi:10.1038/s41416-021-01667-5.
   PubMed Web of Science ®Google Scholar
• Nordlinger B, Sorbye H, Glimelius B, Poston GJ, Schlag PM, Rougier P, Bechstein WO, Primrose JN, Walpole ET, Finch-Jones M, 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 Nov;14(12):1208–1215. doi:10.1016/S1470-2045(13)70447-9.
   PubMed Web of Science ®Google Scholar
• Messaoudi N, Cousineau I, Arslanian E, Henault D, Stephen D, Vandenbroucke-Menu F, Dagenais M, Létourneau R, Plasse M, Roy A, et al. Prognostic value of CD73 expression in resected colorectal cancer liver metastasis. Oncoimmunology. 2020;9(1):1746138. doi:10.1080/2162402X.2020.1746138.
   PubMed Web of Science ®Google Scholar
• Turcotte S, Katz SC, Shia J, Jarnagin WR, Kingham TP, Allen PJ, Fong Y, D’Angelica MI, DeMatteo RP. Tumor MHC class I expression improves the prognostic value of T-cell density in resected colorectal liver metastases. Cancer Immunol Res. 2014 Jun;2(6):530–537. doi:10.1158/2326-6066.CIR-13-0180.
   PubMed Web of Science ®Google Scholar
• Brudvik KW, Jones RP, Giuliante F, Shindoh J, Passot G, Chung MH, Song J, Li L, Dagenborg VJ, Fretland ÅA, et al. RAS mutation Clinical risk score to predict survival after resection of colorectal liver metastases. Ann Surg. 2019 Jan;269(1):120–126. doi:10.1097/SLA.0000000000002319.
   PubMed Web of Science ®Google Scholar
• Berg KCG, Brunsell TH, Sveen A, Alagaratnam S, Bjørnslett M, Hektoen M, Brudvik KW, Røsok BI, Bjørnbeth BA, Nesbakken A, et al. Genomic and prognostic heterogeneity among RAS/BRAFV600E/TP53 co-mutated resectable colorectal liver metastases. Mol Oncol. 2021 Apr;15(4):830–845. doi:10.1002/1878-0261.12885.
   PubMed Web of Science ®Google Scholar
• Buikhuisen JY, Torang A, Medema JP. Exploring and modelling colon cancer inter-tumour heterogeneity: opportunities and challenges. Oncogenesis. 2020 Jul 9;9(7):66. doi:10.1038/s41389-020-00250-6.
   PubMed Web of Science ®Google Scholar
• Del Carmen S, Sayagues JM, Bengoechea O, Anduaga MF, Alcazar JA, Gervas R, García J, Orfao A, Bellvis LM, Sarasquete ME, et al. Spatio-temporal tumor heterogeneity in metastatic CRC tumors: a mutational-based approach. Oncotarget. 2018 Sep 28;9(76):34279–34288. doi:10.18632/oncotarget.26081.
   PubMedGoogle Scholar
• Mlecnik B, Bindea G, Kirilovsky A, Angell HK, Obenauf AC, Tosolini M, Church SE, Maby P, Vasaturo A, Angelova M, et al. The tumor microenvironment and immunoscore are critical determinants of dissemination to distant metastasis. Sci Transl Med. 2016 Feb 24;8(327):327ra26. doi:10.1126/scitranslmed.aad6352.
   PubMed Web of Science ®Google Scholar
• Keim S, Zoernig I, Spille A, Lahrmann B, Brand K, Herpel E, Grabe N, Jäger D, Halama N. Sequential metastases of colorectal cancer: Immunophenotypes and spatial distributions of infiltrating immune cells in relation to time and treatments. Oncoimmunology. 2012 Aug 1;1(5):593–599. doi:10.4161/onci.20179.
   PubMed Web of Science ®Google Scholar
• Eide PW, Moosavi SH, Eilertsen IA, Brunsell TH, Langerud J, Berg KCG, Røsok BI, Bjørnbeth BA, Nesbakken A, Lothe RA, et al. Metastatic heterogeneity of the consensus molecular subtypes of colorectal cancer. NPJ Genom Med. 2021 Jul 14;6(1):59. doi:10.1038/s41525-021-00223-7.
   PubMed Web of Science ®Google Scholar
• Picard E, Verschoor CP, Ma GW, Pawelec G. Relationships between immune landscapes, genetic subtypes and responses to immunotherapy in colorectal cancer. Front Immunol. 2020;11:369. doi:10.3389/fimmu.2020.00369.
   PubMed Web of Science ®Google Scholar
• Halama N, Spille A, Lerchl T, Brand K, Herpel E, Welte S, Keim S, Lahrmann B, Klupp F, Kahlert C, et al. Hepatic metastases of colorectal cancer are rather homogeneous but differ from primary lesions in terms of immune cell infiltration. Oncoimmunology. 2013 Apr 1;2(4):e24116. doi:10.4161/onci.24116.
   PubMed Web of Science ®Google Scholar