Consensus molecular subtype classification of colorectal adenomas
Open accessAbstract
Consensus molecular subtyping is an RNA expression‐based classification system for colorectal cancer (CRC). Genomic alterations accumulate during CRC pathogenesis, including the premalignant adenoma stage, leading to changes in RNA expression. Only a minority of adenomas progress to malignancies, a transition that is associated with specific DNA copy number aberrations or microsatellite instability (MSI). We aimed to investigate whether colorectal adenomas can already be stratified into consensus molecular subtype (CMS) classes, and whether specific CMS classes are related to the presence of specific DNA copy number aberrations associated with progression to malignancy. RNA sequencing was performed on 62 adenomas and 59 CRCs. MSI status was determined with polymerase chain reaction‐based methodology. DNA copy number was assessed by low‐coverage DNA sequencing (n = 30) or array‐comparative genomic hybridisation (n = 32). Adenomas were classified into CMS classes together with CRCs from the study cohort and from The Cancer Genome Atlas (n = 556), by use of the established CMS classifier. As a result, 54 of 62 (87%) adenomas were classified according to the CMS. The CMS3 ‘metabolic subtype’, which was least common among CRCs, was most prevalent among adenomas (n = 45; 73%). One of the two adenomas showing MSI was classified as CMS1 (2%), the ‘MSI immune’ subtype. Eight adenomas (13%) were classified as the ‘canonical’ CMS2. No adenomas were classified as the ‘mesenchymal’ CMS4, consistent with the fact that adenomas lack invasion‐associated stroma. The distribution of the CMS classes among adenomas was confirmed in an independent series. CMS3 was enriched with adenomas at low risk of progressing to CRC, whereas relatively more high‐risk adenomas were observed in CMS2. We conclude that adenomas can be stratified into the CMS classes. Considering that CMS1 and CMS2 expression signatures may mark adenomas at increased risk of progression, the distribution of the CMS classes among adenomas is consistent with the proportion of adenomas expected to progress to CRC. © 2018 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of Pathological Society of Great Britain and Ireland.
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The CMS4 subtype is barely if not detected in adenomas and arises at the carcinoma stage, notably after transition from an indolent CMS3 subtype.
“A consensus that emerged from several studies is that the CMS4 subtype is barely if not detected in adenomas and arises at the carcinoma stage (17, 18), notably after transition from an indolent CMS3 subtype.”
From Clinical Challenges of Consensus Molecular Subtype CMS4 Colon Cancer in the Era of Precision Medicine (2024) · cites this paper as [17]
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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Trimmomatic: a flexible trimmer for Illumina sequence data
Bolger, A. M., Lohse, M., & Usadel, B. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu170 · Cited by 65,548 · see citing works
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
Liao, Y., Smyth, G. K., & Shi, W. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt656 · Cited by 27,219 · see citing works
GSVA: gene set variation analysis for microarray and RNA-Seq data
Hänzelmann, S., Castelo, R., & Guinney, J. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-7 · Cited by 15,440 · see citing works
The Molecular Signatures Database Hallmark Gene Set Collection
Liberzon, A., Birger, C., Thorvaldsdóttir, H., Ghandi, M., Mesirov, J. P., & Tamayo, P. (2015) · Cell Systems · doi:10.1016/j.cels.2015.12.004 · Cited by 13,807 · see citing works
A genetic model for colorectal tumorigenesis
Fearon, E. R., & Vogelstein, B. (1990) · Cell · doi:10.1016/0092-8674(90)90186-i · Cited by 12,132 · see citing works
Inferring tumour purity and stromal and immune cell admixture from expression data
Yoshihara, K., Shahmoradgoli, M., Martínez, E., Vegesna, R., Kim, H., Torres-Garcia, W., Treviño, V., Shen, H., Laird, P. W., Levine, D. A., et al. (2013) · Nature Communications · doi:10.1038/ncomms3612 · Cited by 9,778 · see citing works
Comprehensive molecular characterization of human colon and rectal cancer
The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11252 · Cited by 8,499 · see citing works
The consensus molecular subtypes of colorectal cancer
Guinney, J., Dienstmann, R., Wang, X., de Reyniès, A., Schlicker, A., Soneson, C., Marisa, L., Roepman, P., Nyamundanda, G., Angelino, P., et al. (2015) · Nature Medicine · doi:10.1038/nm.3967 · Cited by 5,170 · see citing works
Self-citationLessons from hereditary colorectal cancer
Kinzler, K. W., & Vogelstein, B. (1996) · Cell · doi:10.1016/s0092-8674(00)81333-1 · Cited by 4,919 · see citing works
GENCODE: The reference human genome annotation for The ENCODE Project
Harrow, J., Frankish, A., Gonzalez, J. M., Tapanari, E., Diekhans, M., Kokocinski, F., Aken, B. L., Barrell, D., Zadissa, A., Searle, S., et al. (2012) · Genome Research · doi:10.1101/gr.135350.111 · Cited by 4,585 · see citing works
Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt
Durinck, S., Spellman, P. T., Birney, E., & Huber, W. K. (2009) · Nature Protocols · doi:10.1038/nprot.2009.97 · Cited by 4,081 · see citing works
Circular binary segmentation for the analysis of array-based DNA copy number data
Olshen, A. B., Venkatraman, E. S., Lucito, R., & Wigler, M. H. (2004) · Biostatistics · doi:10.1093/biostatistics/kxh008 · Cited by 2,256 · see citing works
Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data
Dai, M. (2005) · Nucleic Acids Research · doi:10.1093/nar/gni179 · Cited by 1,797 · see citing works
Toward a Shared Vision for Cancer Genomic Data
Grossman, R. L., Heath, A. P., Ferretti, V., Varmus, H. E., Lowy, D. R., Kibbe, W. A., & Staudt, L. M. (2016) · New England Journal of Medicine · doi:10.1056/nejmp1607591 · Cited by 1,680 · see citing works
Marisa, L., de Reyniès, A., Duval, A., Selves, J., Gaub, M. P., Vescovo, L., Etienne-Grimaldi, M.-C., Schiappa, R., Guenot, D., Ayadi, M., et al. (2013) · PLoS Medicine · doi:10.1371/journal.pmed.1001453 · Cited by 1,507 · see citing works
Jass, J. R. (2006) · Histopathology · doi:10.1111/j.1365-2559.2006.02549.x · Cited by 1,381 · see citing works
Modeling colorectal cancer using CRISPR-Cas9–mediated engineering of human intestinal organoids
Matano, M., Date, S., Shimokawa, M., Takano, A., Fujii, M., Ohta, Y., Watanabe, T., Kanai, T., & Sato, T. (2015) · Nature Medicine · doi:10.1038/nm.3802 · Cited by 1,135 · see citing works
Stromal gene expression defines poor-prognosis subtypes in colorectal cancer
Calon, A., Lonardo, E., Berenguer-Llergo, A., Espinet, E., Hernando-Momblona, X., Iglesias, M., Sevillano, M., Palomo-Ponce, S., Tauriello, D. V. F., Byrom, D., et al. (2015) · Nature Genetics · doi:10.1038/ng.3225 · Cited by 1,070 · see citing works
Sadanandam, A., Lyssiotis, C. A., Homicsko, K., Collisson, E. A., Gibb, W. J., Wullschleger, S., Ostos, L. C. G., Lannon, W. A., Grotzinger, C., Del Rio, M., et al. (2013) · Nature Medicine · doi:10.1038/nm.3175 · Cited by 960 · see citing works
Fujii, M., Shimokawa, M., Date, S., Takano, A., Matano, M., Nanki, K., Ohta, Y., Toshimitsu, K., Nakazato, Y., Kawasaki, K., et al. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.04.003 · Cited by 852 · see citing works
De Sousa E Melo, F., Wang, X., Jansen, M., Fessler, E., Trinh, A., de Rooij, L. P. M. H., de Jong, J. H., de Boer, O. J., van Leersum, R., Bijlsma, M. F., et al. (2013) · Nature Medicine · doi:10.1038/nm.3174 · Cited by 771 · see citing works
Stromal contribution to the colorectal cancer transcriptome
Isella, C., Terrasi, A., Bellomo, S. E., Petti, C., Galatola, G., Muratore, A., Mellano, A., Senetta, R., Cassenti, A., Sonetto, C., et al. (2015) · Nature Genetics · doi:10.1038/ng.3224 · Cited by 640 · see citing works
Morphology, Anatomic Distribution and Cancer Potential of Colonic Polyps
Shinya, H., & Wolff, W. I. (1979) · Annals of Surgery · doi:10.1097/00000658-197912000-00001 · Cited by 524 · see citing works
The significance of unstable chromosomes in colorectal cancer
Rajagopalan, H., Nowak, M. A., Vogelstein, B., & Christoph Lengauer, C. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1165 · Cited by 502 · see citing works
Scheinin, I., Sie, D., Bengtsson, H. L., van de Wiel, M. A., Olshen, A. B., van Thuijl, H. F., Essen, H. F. H. V., Eijk, P. P., Rustenburg, F., Meijer, G. A., et al. (2014) · Genome Research · doi:10.1101/gr.175141.114 · Cited by 491 · see citing works
Self-citationBrenner, H., Hoffmeister, M., Stegmaier, C., Brenner, G., Altenhofen, L., & Haug, U. (2007) · Gut · doi:10.1136/gut.2007.122739 · Cited by 438 · see citing works
Gene expression patterns unveil a new level of molecular heterogeneity in colorectal cancer
Budínská, E., Popovici, V. C., Tejpar, S., D’Ario, G., Lapique, N., Sikora, K. O., Narzo, A. F. D., Yan, P., Hodgson, J., Weinrich, S. L., et al. (2013) · The Journal of Pathology · doi:10.1002/path.4212 · Cited by 409 · see citing works
Ried, T., Knutzen, R., Steinbeck, R. G., Blegen, H., Schröck, E., Heselmeyer, K. M., du Manoir, S., & Auer, G. (1996) · Genes Chromosomes and Cancer · doi:10.1002/(sici)1098-2264(199604)15:4 · Cited by 404 · see citing works
Skrzypczak, M., Goryca, K., Rubel, T., Paziewska, A., Mikuła, M., Jarosz, D., Pachlewski, J., Olędzki, J., & Ostrowski, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013091 · Cited by 395 · see citing works
Roepman, P., Schlicker, A., Tabernero, J. M., Majewski, I. J., Tian, S., Moreno, V. R., Snel, M. H. J., Chresta, C. M., Rosenberg, R., Nitsche, U., et al. (2013) · International Journal of Cancer · doi:10.1002/ijc.28387 · Cited by 341 · see citing works
Self-citationColorectal adenoma to carcinoma progression follows multiple pathways of chromosomal instability
Hermsen, M. A. J. A., Postma, C., Baak, J. P. A., Weiss, M. M., Rapallo, A., Sciutto, A., Roemen, G. M. J. M., Arends, J., Williams, R. D., Giaretti, W., et al. (2002) · Gastroenterology · doi:10.1053/gast.2002.36051 · Cited by 329 · see citing works
Self-citationIsella, C., Brundu, F. G., Bellomo, S. E., Galimi, F., Zanella, E. R., Porporato, R., Petti, C., Fiori, A., Orzan, F., Senetta, R., et al. (2017) · Nature Communications · doi:10.1038/ncomms15107 · Cited by 298 · see citing works
Schlicker, A., Beran, G. J., Chresta, C. M., McWalter, G., Pritchard, A., Weston, S. L., Runswick, S. K., Davenport, S., Heathcote, K., Alférez, D., et al. (2012) · BMC Medical Genomics · doi:10.1186/1755-8794-5-66 · Cited by 253 · see citing works
Self-citationCGHcall: calling aberrations for array CGH tumor profiles
van de Wiel, M. A., Kim, K. I., Vosse, S. J., van Wieringen, W. N., Wilting, S. M., & Ylstra, B. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm030 · Cited by 240 · see citing works
Carvalho, B. G., Postma, C., Mongera, S., Hopmans, E. S., Diskin, S. J., van de Wiel, M. A., Criekinge, W. V., Thas, O., Matthäi, A., Cuesta, M. A., et al. (2008) · Gut · doi:10.1136/gut.2007.143065 · Cited by 235 · see citing works
Self-citationMeijer, G. A., Hermsen, M. A. J. A., Baak, J. P. A., van Diest, P. J., Meuwissen, S. G. M., Beliën, J. A. M., Hoovers, J. M. N., Joenje, H., Snijders, P. J. F., & Walboomers, J. M. M. (1998) · Journal of Clinical Pathology · doi:10.1136/jcp.51.12.901 · Cited by 196 · see citing works
Self-citationDouglas, E. J., Fiegler, H., Rowan, A., Halford, S. E. R., Bicknell, D., Bodmer, W. F., Tomlinson, I. P. M., & Carter, N. P. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0328 · Cited by 192 · see citing works
Dunne, P. D., McArt, D. G., Bradley, C. A., O’Reilly, P. G., Barrett, H. L., Cummins, R., O’Grady, T., Arthur, K., Loughrey, M. B., Allen, W. L., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0032 · Cited by 162 · see citing works
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Fessler, E., Drost, J., van Hooff, S. R., Linnekamp, J. F., Wang, X., Jansen, M., De Sousa E Melo, F., Prasetyanti, P. R., IJspeert, J. E., Franitza, M., et al. (2016) · EMBO Molecular Medicine · doi:10.15252/emmm.201606184 · Cited by 159 · see citing works
TPX2 and AURKA promote 20q amplicon-driven colorectal adenoma to carcinoma progression
Sillars-Hardebol, A. H., Carvalho, B. G., Tijssen, M., Beliën, J. A. M., de Wit, M., Diemen, P. M. D., Pontén, F., van de Wiel, M. A., Fijneman, R. J. A., & Meijer, G. A. (2011) · Gut · doi:10.1136/gutjnl-2011-301153 · Cited by 133 · see citing works
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Belt, E. J. T., Fijneman, R. J. A., van den Berg, E. G., Bril, H., Diemen, P. M. D., Tijssen, M., Essen, H. F. H. V., Klerk, E. S. M. D. L., Beliën, J. A. M., Stockmann, H. B. A. C., et al. (2011) · European Journal of Cancer · doi:10.1016/j.ejca.2011.04.025 · Cited by 132 · see citing works
Self-citationPérez‐Villamil, B., Romera-López, A., Prieto, S. H., López–Campos, G., Calles, A., Asenjo, J. A. L., Sanz‐Ortega, J., Fernández, C., Sastre, J., Alfonso, R., et al. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-260 · Cited by 126 · see citing works
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Stein, C. K., Qu, P., Epstein, J., Buros, A. F., Rosenthal, A., Crowley, J. J., Morgan, G. J., & Barlogie, B. (2015) · BMC Bioinformatics · doi:10.1186/s12859-015-0478-3 · Cited by 100 · see citing works
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Self-citationCamps, J., Grade, M., Nguyen, Q. T., Hörmann, P., Becker, S., Hummon, A. B., Rodriguez, V., Chandrasekharappa, S. C., Chen, Y., Difilippantonio, M. J., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-2864 · Cited by 84 · see citing works
Skrzypczak, M., Goryca, K., Rubel, T., Paziewska, A., Mikuła, M., Jarosz, D., Pachlewski, J., Olędzki, J., & Ostrowski, J. (2010) · PLoS ONE · doi:10.1371/annotation/8c585739-a354-4fc9-a7d0-d5ae26fa06ca · Cited by 83 · see citing works
Sillars-Hardebol, A. H., Carvalho, B. G., de Wit, M., Postma, C., Diemen, P. M. D., Mongera, S., Ylstra, B., van de Wiel, M. A., Meijer, G. A., & Fijneman, R. J. A. (2010) · Tumor Biology · doi:10.1007/s13277-009-0012-1 · Cited by 79 · see citing works
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Borràs, E., Lucas, F. A. S., Chang, K., Zhou, R., Masand, G., Fowler, J., Mork, M. E., You, Y. N., Taggart, M. W., McAllister, F. M., et al. (2016) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-16-0081 · Cited by 77 · see citing works
Carvalho, B. G., Sillars-Hardebol, A. H., Postma, C., Mongera, S., Droste, J. S. T. S., Obulkasim, A., van de Wiel, M. A., Criekinge, W. V., Ylstra, B., Fijneman, R. J. A., et al. (2012) · Cellular Oncology · doi:10.1007/s13402-011-0065-1 · Cited by 73 · see citing works
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Pesson, M., Volant, A., Uguen, A., Trillet, K., de la Grange, P., Aubry, M., Daoulas, M., Robaszkiewicz, M., Gac, G. L., Morel, A., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087761 · Cited by 59 · see citing works
de Groen, F. L. M., Krijgsman, O., Tijssen, M., Vriend, L. E. M., Ylstra, B., Hooijberg, E., Meijer, G. A., Steenbergen, R. D. M., & Carvalho, B. G. (2014) · Genes Chromosomes and Cancer · doi:10.1002/gcc.22144 · Cited by 35 · see citing works
Self-citationde Wit, M., Carvalho, B. G., Diemen, P. M. D., van Alphen, C., Beliën, J. A. M., Meijer, G. A., & Fijneman, R. J. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0174768 · Cited by 32 · see citing works
Self-citationHirsch, D. D., Camps, J., Varma, S., Kemmerling, R., Stapleton, M., Ried, T., & Gaiser, T. (2012) · Genes Chromosomes and Cancer · doi:10.1002/gcc.21937 · Cited by 27 · see citing works
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Hu, L., Lan, H., Huang, D., Li, X., & Jin, K. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.769305 · Cited by 34 · see citing works
Zelli, V., Manno, A., Compagnoni, C., Ibraheem, R., Zazzeroni, F., Alesse, E., Rossi, F., Arbib, C., & Tessitore, A. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04720-4 · Cited by 32 · see citing works
Haasnoot, K. J. C., Backes, Y., Moons, L. M. G., Kranenburg, O., Trinh, A., Vermeulen, L., Noë, M., Tuynman, J. B., van Lent, A. U. G., van Ginneken, R., et al. (2020) · Modern Pathology · doi:10.1038/s41379-020-0598-9 · Cited by 30 · see citing works
Hong, Q., Li, B., Cai, X., Lv, Z., Cai, S., Zhong, Y., & Wen, B. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.704531 · Cited by 27 · see citing works
Xu, Y., Liu, K., Li, M., Li, M., Zhou, X., Sun, M., Zhang, L., Wang, S., Liu, F., & Xu, Y. (2024) · EBioMedicine · doi:10.1016/j.ebiom.2024.105142 · Cited by 27 · see citing works
Ding, X., Huang, H., Zhang, F., & Jiang, J. (2024) · Current Treatment Options in Oncology · doi:10.1007/s11864-024-01282-5 · Cited by 21 · see citing works
Kozuka, M., Battaglin, F., Jayachandran, P., Wang, J., Arai, H., Soni, S., Zhang, W., Hirai, M., Matsusaka, S., & Lenz, H. (2021) · Cancers · doi:10.3390/cancers13194862 · Cited by 20 · see citing works
Flanagan, D. J., Amirkhah, R., Vincent, D. F., Gündüz, N., Gentaz, P., Cammareri, P., McCooey, A. J., McCorry, A. M. B., Fisher, N. C., Belnoue-Davis, H. L., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-35134-3 · Cited by 18 · see citing works
Somatic targeted mutation profiling of colorectal cancer precursor lesions
dos Santos, W., dos Reis, M. B., Porto, J., de Carvalho, A. C., Matsushita, M. D. M., Oliveira, G. D. S., Syrjänen, K. J., Reis, R. M., & Guimarães, D. P. (2022) · BMC Medical Genomics · doi:10.1186/s12920-022-01294-w · Cited by 17 · see citing works
Otálora-Otálora, B. A., Rivera, J. J. L., Aristizábal-Guzmán, C., Isaza-Ruget, M. A., & Álvarez, C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242316638 · Cited by 17 · see citing works
Transcriptomic subtyping of gastrointestinal malignancies
de Back, T. R., van Hooff, S. R., Sommeijer, D. W., & Vermeulen, L. (2024) · Trends in cancer · doi:10.1016/j.trecan.2024.06.007 · Cited by 17 · see citing works
Huang, H., Cao, W., Long, Z., Kuang, L., Li, X., Feng, Y., Wu, Y., Zhao, Y., Chen, Y., Sun, P., et al. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2022.1030335 · Cited by 16 · see citing works
Value of methylation markers in colorectal cancer (Review)
Kong, C., & Fu, T. (2021) · Oncology Reports · doi:10.3892/or.2021.8128 · Cited by 16 · see citing works
Li, X., Wu, D., Li, Q., Gu, J., Gao, W., Zhu, X., Yin, W., Zhu, R., Zhu, L., & Jiao, N. (2023) · Physiological Genomics · doi:10.1152/physiolgenomics.00103.2023 · Cited by 15 · see citing works
Kemp, S. R. M., Komor, M. A., Hegi, R., Bolijn, A. S., Tijssen, M., de Groen, F. L. M., Depla, A. C. T. M., van Leerdam, M. E., Meijer, G. A., Fijneman, R. J. A., et al. (2022) · Neoplasia · doi:10.1016/j.neo.2022.100820 · Cited by 14 · see citing works
Self-citationBhandari, Y. R., Krishna, V., Powers, R., Parmar, S., Thursby, S.-J., Gupta, E., Kulak, O., Gokare, P. R., Reumers, J., Wesenbeeck, L. V., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2301536120 · Cited by 14 · see citing works
Pan, P., Li, J., Wang, B., Tan, X., Yin, H., Han, Y., Wang, H., Shi, X., Li, X., Xie, C., et al. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1067849 · Cited by 13 · see citing works
Hoogstrate, Y., Komor, M. A., Böttcher, R., van Riet, J., van de Werken, H. J. G., van Lieshout, S., Hoffmann, R., van den Broek, E., Bolijn, A. S., Dits, N. F. J., et al. (2021) · GigaScience · doi:10.1093/gigascience/giab080 · Cited by 13 · see citing works
Self-citationCheng, C.-T., Lai, J.-M., Chang, P. M., Hong, Y., Huang, C. F., & Wang, F. (2023) · PLoS ONE · doi:10.1371/journal.pone.0286032 · Cited by 11 · see citing works
Philipovskiy, A. V., Ghafouri, S. R., Dwivedi, A. K., Alvarado, L. A., McCallum, R. W., Maegawa, F. B., Konstantinidis, I. T., Hakim, N., Shurmur, S. W., Awasthi, S., et al. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2021.772225 · Cited by 9 · see citing works
CpG Site-Based Signature Predicts Survival of Colorectal Cancer
Wu, J., Zhang, L., Kuchi, A., Otohinoyi, D. A., & Hicks, C. (2022) · Biomedicines · doi:10.3390/biomedicines10123163 · Cited by 9 · see citing works
A Gene Signature Derived from the Loss of CDKN1A (p21) Is Associated with CMS4 Colorectal Cancer
Bueno-Fortes, S., Muenzner, J. K., Berral-González, A., Hampel, C., Lindner, P., Berninger, A., Huebner, K., Kunze, P., Bäuerle, T., Erlenbach‐Wuensch, K., et al. (2021) · Cancers · doi:10.3390/cancers14010136 · Cited by 9 · see citing works
Chen, R., Sugiyama, A., Seno, H., & Sugimoto, M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0221772 · Cited by 8 · see citing works
Han, R., Shi, J., Cheng, K., Wang, Z., Chen, Y., Spellecy, O., Faisal, A. S. M., Aryal, I., Chen, J., Craven, R. J., et al. (2025) · Cancer Medicine · doi:10.1002/cam4.71227 · Cited by 7 · see citing works
Nasab, S. J., Clark, C. C. T., & Entezari, M. H. (2023) · European Journal of Cancer Prevention · doi:10.1097/cej.0000000000000861 · Cited by 7 · see citing works
Zhang, Y., Wang, Y., Wang, J., & Zhang, K. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.852708 · Cited by 7 · see citing works
Murcia, Ó., Martínez‐Roca, A., Juárez, M., Giner-Calabuig, M., Alustiza, M., Mira, C., Mangas‐Sanjuán, C., Serrano, E., Ruiz-Gómez, F. A., Baile‐Maxía, S., et al. (2021) · Cancers · doi:10.3390/cancers13020246 · Cited by 7 · see citing works
Consensus molecular subtype transition during progression of colorectal cancer
van de Weerd, S., Torang, A., Zwager, L. W., Koelink, P. J., Koster, J., Bastiaansen, B. A., Lammers, V., Longobardi, C., Roodhart, J. M., van Krieken, J. H., et al. (2023) · The Journal of Pathology · doi:10.1002/path.6176 · Cited by 6 · see citing works
Ras Family of Small GTPases in CRC: New Perspectives for Overcoming Drug Resistance
Río-Vilariño, A., del Puerto‐Nevado, L., García‐Foncillas, J., & Cebrián, A. (2021) · Cancers · doi:10.3390/cancers13153757 · Cited by 6 · see citing works
Two intertwined compartments coexisting in sporadic conventional colon adenomas
Rubio, C. A. (2020) · Intestinal Research · doi:10.5217/ir.2019.00133 · Cited by 5 · see citing works
Chen, Q., Xu, Y., Kang, S., Lin, W., Luo, L., Yang, L.-P., Zhang, Q., Yang, P., Huang, J., Zhang, X., et al. (2024) · MedComm · doi:10.1002/mco2.70011 · Cited by 5 · see citing works
Emast Frequency in Colorectal Cancer: A Meta-Analysis and Literature Review
Ranjbar, R., Esfahani, A. T., Mojarad, E. N., Olfatifar, M., Aghdaei, H. A., & Mohammadpour, S. (2020) · Biomarkers in Medicine · doi:10.2217/bmm-2020-0068 · Cited by 5 · see citing works
McFerran, E., McKay, D., Loughrey, M. B., Lawler, M., & McSorley, S. T. (2026) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2026.102092 · Cited by 4 · see citing works
Role of Deep Learning in Diagnosis, Treatment, and Prognosis of Oncological Conditions
Umar, M., Shiwlani, A., Saeed, F., Ahmad, A., Shah, M. H. A., & Tahir, A. (2023) · International Journal of Membrane Science and Technology · doi:10.15379/ijmst.v10i5.3695 · Cited by 4 · see citing works
Severe grade of melanosis coli is associated with a higher detection rate of colorectal adenoma
Katsumata, R., Manabe, N., Monobe, Y., Tanikawa, T., Ayaki, M., Suehiro, M., Fujita, M., Kamada, T., Haruma, K., & Kawamoto, H. (2022) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.22-19 · Cited by 4 · see citing works
Mohammadpour, S., Noukabadi, F. N., Esfahani, A. T., Kazemi, F., Esmaeili, S., Zafarjafarzadeh, N., Sarpash, S., & Mojarad, E. N. (2023) · Current Molecular Medicine · doi:10.2174/1566524023666230523155719 · Cited by 4 · see citing works
Reyila, A., Gao, X., Yu, J. Q., & Nie, Y. (2025) · Epigenomics · doi:10.1080/17501911.2025.2476380 · Cited by 3 · see citing works
Risk factor analysis of malignant adenomas detected during colonoscopy
Hu, H., Gong, X., Xu, K. L., Luo, S., Gao, W., Li, B., & Jing, D.-D. (2023) · Frontiers in Medicine · doi:10.3389/fmed.2023.1106272 · Cited by 3 · see citing works
Gut microbial subtypes and clinicopathological value for colorectal cancer
Han, S., Jing, Z., Song, Y., Wu, X., Yu, X., Ye, T., Chu, J., Qu, Z., Wu, Y., Han, S., et al. (2024) · Cancer Medicine · doi:10.1002/cam4.70180 · Cited by 3 · see citing works
Saller, J. J., Qin, D., Felder, S. I., & Coppola, D. (2020) · Clinical Colorectal Cancer · doi:10.1016/j.clcc.2020.02.003 · Cited by 3 · see citing works
Maletzki, C., Hühns, M., Bauer, I., Prall, F., Junghanß, C., & Henze, L. (2019) · The Oncologist · doi:10.1634/theoncologist.2018-0614 · Cited by 3 · see citing works
He, X., Cheng, G., Xiao, F., Zhang, L., Jin, G., Zhao, X., Liu, Y., Liang, J., Li, Y., Liu, Z., et al. (2021) · Journal of Gastrointestinal Oncology · doi:10.21037/jgo-20-600 · Cited by 3 · see citing works
Non-Coding RNAs as Potential Biomarkers for Colorectal Polyps and Cancer Detection
Plut, S., Gavrić, A., & Glavač, D. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26094106 · Cited by 2 · see citing works
High expression of ZEB1 is associated with EMAST & metastasis in colorectal cancer patients
Mohammadpour, S., Esfahani, A. T., Khorasaniasl, S., Karimpour, R., Bakhshian, F., Moradi, A., & Mojarad, E. N. (2022) · International Journal of Microbiology Research · doi:10.4103/ijmr.ijmr_1062_20 · Cited by 2 · see citing works
Wang, X., Liu, S., Cao, H., Li, X., Rong, Y., Liu, G., Du, H., & Shen, H. (2021) · Pathology & Oncology Research · doi:10.3389/pore.2021.587029 · Cited by 2 · see citing works
Snow, S., Matkowskyj, K. A., Maresh, M. E., Clipson, L. J., Vo, T. N., Johnson, K. A., Deming, D. A., Newton, M. A., Grady, W. M., Pickhardt, P. J., et al. (2021) · Human Pathology · doi:10.1016/j.humpath.2021.10.002 · Cited by 2 · see citing works
Chen, Z., Kim, D., Wang, J., Huang, Q., Gao, Y., Zheng, J., Lyu, L., Li, Y., Lu, L., Xie, R., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-17653-3 · Cited by 1 · see citing works
COLORECTAL MOLECULAR SUBTYPES – PROGRESS OR DEADLOCK?
Fedyanin, M. Y., Ignatova, E. O., & Tryakin, А. А. (2021) · Practical oncology · doi:10.31917/2201072 · Cited by 1 · see citing works
Li, X., Zhang, W., Yuan, S., Mao, Q., Zhang, C., Cai, R., Lin, H., & Wang, X. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1142703 · Cited by 1 · see citing works
Tang, E., Tang, C., Lin, X., Chen, Y., Zhou, Y., Pan, C., & Jiang, H. (2024) · Gene · doi:10.1016/j.gene.2024.148745 · Cited by 1 · see citing works
Developing a comprehensive molecular subgrouping model for cervical cancer using machine learning
Han, G. H. (2024) · American Journal of Cancer Research · doi:10.62347/mter1763 · Cited by 1 · see citing works
Simonetto, C., Mansmann, U., & Kaiser, J. C. (2023) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010831 · Cited by 1 · see citing works
Merlo, J. P., Mahmoud, Y. D., Veigas, F., Scheidegger, M. A., Cagnoni, A. J., Fernández, E. A., Rabinovich, G. A., & Mariño, K. V. (2023) · Regular and Young Investigator Award Abstracts · doi:10.1136/jitc-2023-sitc2023.0217 · Cited by 1 · see citing works
Epigenetic Alterations in Colorectal Cancer
Ko, B., Hanna, M., Yu, M., & Grady, W. M. (2023) · Epigenetics and human health · doi:10.1007/978-3-031-42365-9_10 · Cited by 1 · see citing works
Ahlmanner, F. (2019) · Gothenburg University Publications Electronic Archive (Gothenburg University)
Colonoscopy surveillance after adenoma removal: current guidelines
Dekker, E., & de Klaver, W. (2021) · Springer eBooks · doi:10.1007/978-3-030-29964-4_25-1
Metagenomics from bench to bedside and from bedside to bench
Jia, H. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-91369-0.00006-6 · Cited by 1 · see citing works
Colonoscopy Surveillance After Adenoma Removal: Current Guidelines
Dekker, E., & de Klaver, W. (2021) · Springer eBooks · doi:10.1007/978-3-030-56993-8_25
Value of 18F-FDG PET/CT in the diagnosis and grading of incidental colorectal adenomas
Zhang, Q., Tang, K., Lu, X., Zhu, Y., & Xu, N. (2024) · Revista Española de Medicina Nuclear e Imagen Molecular (English Edition) · doi:10.1016/j.remnie.2024.500075
Qi, Z., Tang, K., Lu, X., Zhu, Y., & Xu, N. (2024) · Revista Española de Medicina Nuclear e Imagen Molecular · doi:10.1016/j.remn.2024.500075
Precision Medicine and Computational Cytology
Dey, P. (2025) · Springer eBooks · doi:10.1007/978-981-95-3272-8_11
Aneuploidy patterns in colorectal cancer
Zaalberg, I. C., Ketelaars, S. L. C., Jodal, H. C., Løberg, M., Kalager, M., Meijer, G. A., Carvalho, B. G., & Lens, S. M. A. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116721
Self-citationZelli, V., Manno, A., Compagnoni, C., Ibraheem, R., Zazzeroni, F., Alesse, E., Rossi, F., Arbib, C., & Tessitore, A. (2024) · Figshare · doi:10.6084/m9.figshare.26643322
Knowledge-guided learning with curated prior genetic biomarkers for robust model interpretation
Baek, B., Jang, E., Parsa, S. P., Kim, Y. H., & Kang, M. (2026) · Bioinformatics · doi:10.1093/bioinformatics/btag411
Lee, J., Jang, S., Lee, B., Shin, J., Gong, J.-R., & Shin, D. (2026) · BMC Biology · doi:10.1186/s12915-026-02559-x
Artificial Intelligence in Oncology: Revolutionizing Cancer Care
Tantray, J., Patel, A., Nagdev, S. A., Lodhi, D. S., Golani, P., & Alok, S. (2026) · BENTHAM SCIENCE PUBLISHERS eBooks · doi:10.2174/9798898814144126010007
Chen, K., Xu, K., Ding, Y., Yin, H., Feng, Z., Li, L., Xu, H., Hu, W., & Wen, Y. R. (2026) · Discover Oncology · doi:10.1007/s12672-026-05492-1
Andreu‐Ballester, J. C., Amorós, C., Benlloch, S., Galindo-Regal, L., García‐Ballesteros, C., Uribe, N., Jiménez, A., López-Chuliá, F., Izquierdo, F., Valdivieso, E., et al. (2026) · Cancers · doi:10.3390/cancers18142273
- Authors
- Komor, M. A., Bosch, L. J., Bounova, G., Bolijn, A. S., Delis‐van Diemen, P. M., Rausch, C., Hoogstrate, Y., Stubbs, A. P., de Jong, M., Jenster, G., van Grieken, N. C., Carvalho, B., Wessels, L. F., Jimenez, C. R., Fijneman, R. J., Meijer, G. A., & In collaboration with the NGS‐ProToCol Consortium:
- Affiliations
- The Netherlands Cancer Institute (NL)
- Translational Gastrointestinal Oncology, Department of Pathology Netherlands Cancer Institute Amsterdam The Netherlands
- Erasmus MC (NL)
- GenomeScan Leiden The Netherlands
- Department of Pathology VU University Medical Centre Amsterdam The Netherlands
- Oncoproteomics Laboratory, Department of Medical Oncology VU University Medical Centre Amsterdam The Netherlands
- Corresponding author
- Fijneman, Remond JA
- ORCID
- Venue
- The Journal of Pathology
- Publisher
- Wiley
- Published
- 2018-08-31
- Volume
- 246
- Issue
- 3
- Pages
- 266-276
- ISSN
- 0022-3417 (ISSN-L)
- 1096-9896
- PMC
- PMC6221003
- OpenAlex
- W2809907085
- Cited by
- 86
- References
- 61
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 10 · 2023: 18 · 2022: 12 · 2021: 19 · 2020: 8 · 2019: 6 · 2018: 1
- FWCI
- 6.47
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Journal of Pathology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
- Pure Amsterdam UMC (submittedVersion, cc-by)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Research Repository (Delft University of Technology) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Center for Translational Molecular Medicine (03O‐402)
- KWF Kankerbestrijding (2013‐5885, 2013‐6025)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Health Sciences › Medicine › Oncology › Colorectal Cancer Surgical Treatments
- Keywords
- colorectal adenoma, consensus molecular subtypes, colorectal cancer, adenoma-to-carcinoma progression, microsatellite instability, DNA copy number aberrations, metabolic subtypes, mesenchymal subtype
- MeSH terms
- Adenoma, Carcinoma, Cell Differentiation, Humans, Neoplasm Staging, Phenotype, Predictive Value of Tests, Biomarkers, Tumor, Colorectal Neoplasms, Reproducibility of Results, Disease Progression, Gene Dosage, Genetic Predisposition to Disease, Gene Expression Profiling, Consensus, Microsatellite Instability, DNA Copy Number Variations, Transcriptome
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