The DOI matches its Crossref record; 69 of the 69 references it cites were found in a registry or an index.
Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: Tumor budding as oncotarget
Open accessAbstract
Epithelial mesenchymal transition (EMT) is proposed as a critical mechanism for the acquisition of malignant phenotypes by epithelial cells. In colorectal cancer, tumor cells having undergone EMT are histologically represented by the presence of tumor buds defined as single cells or small clusters of de-differentiated tumor cells at the invasive front. Tumor budding is not a static, histological feature rather it represents a snap-shot of a dynamic process undertaken by an aggressive tumor with the potential to disseminate and metastasize. Strong, consistent evidence shows that tumor budding is a predictor of lymph node metastasis, distant metastatic disease, local recurrence, worse overall and disease-free survival time and an independent prognostic factor. Moreover, the International Union against Cancer (UICC) recognizes tumor budding as a highly relevant, additional prognostic parameter. The aim of this review is to summarize the evidence supporting the implementation of tumor budding into diagnostic pathology and patient management and additionally to illustrate its worthiness as a potential therapeutic target.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The basics of epithelial-mesenchymal transition
Kalluri, R., & Weinberg, R. A. (2009) · Journal of Clinical Investigation · doi:10.1172/jci39104 · Cited by 10,196
CpG island methylator phenotype in colorectal cancer
Toyota, M., Ahuja, N., Ohe-Toyota, M., Herman, J. G., Baylin, S. B., & Issa, J.-P. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.15.8681 · Cited by 2,523
CD44: From adhesion molecules to signalling regulators
Ponta, H., Sherman, L., & Herrlich, P. A. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1004 · Cited by 2,386
Systematic Review of Microsatellite Instability and Colorectal Cancer Prognosis
Popat, S., Hubner, R., & Houlston, R. S. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.01.086 · Cited by 1,830
Migrating cancer stem cells — an integrated concept of malignant tumour progression
Brabletz, T., Jung, A., Spaderna, S., Hlubek, F., & Kirchner, T. (2005) · Nature Reviews Cancer · doi:10.1038/nrc1694 · Cited by 1,352
Brabletz, T., Jung, A., Reu, S., Porzner, M., Hlubek, F., Kunz-Schughart, L. A., Knuechel, R., & Kirchner, T. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171610498 · Cited by 1,049
EMT: When epithelial cells decide to become mesenchymal-like cells
Kalluri, R. (2009) · Journal of Clinical Investigation · doi:10.1172/jci39675 · Cited by 952
The role of epithelial-mesenchymal transition in cancer pathology
guarino, M., rubino, B., & ballabio, G. (2007) · Pathology · doi:10.1080/00313020701329914 · Cited by 790
Risk factors for an adverse outcome in early invasive colorectal carcinoma
Ueno, H., Mochizuki, H., Hashiguchi, Y., Shimazaki, H., Aida, S., Hase, K., Matsukuma, S., Kanai, T., Kurihara, H., Ozawa, K., et al. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.04.022 · Cited by 758
Mann, B., Gelos, M., Siedow, A., Hanski, M. L., Gratchev, A., Ilyas, M., Bodmer, W. F., Moyer, M. P., Riecken, E. O., Buhr, H. J., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1603 · Cited by 663
Tumour `budding' as an index to estimate the potential of aggressiveness in rectal cancer
Ueno, H., Murphy, J., Jass, J. R., Mochizuki, H., & Talbot, I. C. (2002) · Histopathology · doi:10.1046/j.1365-2559.2002.01324.x · Cited by 655
Epithelial Cell Adhesion Molecule
Trzpis, M., McLaughlin, P. M. J., de Leij, L. M. F. H., & Harmsen, M. C. (2007) · The American Journal of Pathology · doi:10.2353/ajpath.2007.070152 · Cited by 578
The grading of rectal cancer: historical perspectives and a multivariate analysis of 447 cases
JASS, J. R., ATKIN, W. S., CUZICK, J., BUSSEY, H. J. R., MORSON, B. C., NORTHOVER, J. M. A., & TODD, I. P. (1986) · Histopathology · doi:10.1111/j.1365-2559.1986.tb02497.x · Cited by 538
Prognostic value of tumor “budding” in patients with colorectal cancer
Hase, K., Shatney, C., Johnson, D., Trollope, M., & Vierra, M. (1993) · Diseases of the Colon & Rectum · doi:10.1007/bf02238588 · Cited by 536
Brabletz, T., Hlubek, F., Spaderna, S., Schmalhofer, O., Hiendlmeyer, E., Jung, A., & Kirchner, T. (2005) · Cells Tissues Organs · doi:10.1159/000084509 · Cited by 528
Sánchez-Tilló, E., Lázaro, A., Torrent, R., Cuatrecasas, M., Vaquero, E. C., Castells, A., Engel, P., & Postigo, A. (2010) · Oncogene · doi:10.1038/onc.2010.102 · Cited by 504
Morphology of sporadic colorectal cancer with DNA replication errors
Jass, J. R., Do, K.-A., Simms, L. A., Iino, H., Wynter, C., Pillay, S. P., Searle, J., Radford-Smith, G., Young, J., & Leggett, B. (1998) · Gut · doi:10.1136/gut.42.5.673 · Cited by 466
Pyke, C., Salo, S., Ralfkiaer, E. M., Rømer, J., Danø, K., & Tryggvason, K. (1995) · PubMed · Cited by 376
Jenkins, M. A., Hayashi, S., O’Shea, A.-M., Burgart, L. J., Smyrk, T. C., Shimizu, D., Waring, P. M., Ruszkiewicz, A. R., Pollett, A. F., Redston, M., et al. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.04.044 · Cited by 373
Tumour budding in colorectal carcinoma
Prall, F. (2007) · Histopathology · doi:10.1111/j.1365-2559.2006.02551.x · Cited by 369
Lymphocytic infiltration and survival in rectal cancer.
Jass, J. R. (1986) · Journal of Clinical Pathology · doi:10.1136/jcp.39.6.585 · Cited by 356
Moreno-Bueno, G., Cubillo, E., Sarrió, D., Peinado, H., Rodríguez-Pinilla, S. M., Villa, S., Bolós, V., Jordá, M., Fabra, A., Portillo, F., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0479 · Cited by 320
Tumor Budding is a Strong and Reproducible Prognostic Marker in T3N0 Colorectal Cancer
Wang, L. M., Kevans, D., Mulcahy, H., O'Sullivan, J., Fennelly, D., Hyland, J., O'Donoghue, D., & Sheahan, K. (2009) · American Journal of Surgical Pathology · doi:10.1097/pas.0b013e318184cd55 · Cited by 280
van Rijnsoever, M., Elsaleh, H., Joseph, D. J., McCaul, K. A., & Iacopetta, B. J. (2003) · PubMed · Cited by 267
Katoh, M., & Katoh, M. (2006) · Cancer Biology & Therapy · doi:10.4161/cbt.5.9.3151 · Cited by 253
Morodomi, T., Isomoto, H., Shirouzu, K., Kakegawa, K., Irie, K., & Morimatsu, M. (1989) · Cancer · doi:10.1002/1097-0142(19890201)63:3<539::aid-cncr2820630323>3.0.co;2-s · Cited by 241
The morphological and molecular features of the epithelial-to-mesenchymal transition
Moreno-Bueno, G., Peinado, H., Molina, P., Olmeda, D., Cubillo, E., Santos, V., Palacios, J., Portillo, F., & Cano, A. (2009) · Nature Protocols · doi:10.1038/nprot.2009.152 · Cited by 221
Jung, A., Schrauder, M., Oswald, U., Knoll, C., Sellberg, P., Palmqvist, R., Niedobitek, G., Brabletz, T., & Kirchner, T. (2001) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63007-6 · Cited by 217
Compton, C. (2002) · Archives of Pathology & Laboratory Medicine · doi:10.5858/2002-126-384a-pfic · Cited by 185
APC mutation and tumour budding in colorectal cancer
Jass, J. R., Barker, M., Fraser, L., Walsh, M. D., Whitehall, V. L. J., Gabrielli, B., Young, J., & Leggett, B. A. (2003) · Journal of Clinical Pathology · doi:10.1136/jcp.56.1.69 · Cited by 160
Tumour budding as prognostic factor in stage I/II colorectal carcinoma
Prall, F., Nizze, H., & Barten, M. (2005) · Histopathology · doi:10.1111/j.1365-2559.2005.02161.x · Cited by 159
A New Prognostic Staging System for Rectal Cancer
Ueno, H., Price, A. B., Wilkinson, K. H., Jass, J. R., Mochizuki, H., & Talbot, I. C. (2004) · Annals of Surgery · doi:10.1097/01.sla.0000143243.81014.f2 · Cited by 158
Gastrointestinal stem cells in development and cancer
Brabletz, S., Schmalhofer, O., & Brabletz, T. (2008) · The Journal of Pathology · doi:10.1002/path.2475 · Cited by 152
Tumor Budding as an Index to Identify High-Risk Patients with Stage II Colon Cancer
Nakamura, T., Mitomi, H., Kanazawa, H., et al. (2008) · Diseases of the Colon & Rectum · doi:10.1007/s10350-008-9192-9 · Cited by 137
Zlobec, I., Lugli, A., Baker, K., Roth, S., Minoo, P., Hayashi, S., Terracciano, L., & Jass, J. R. (2007) · The Journal of Pathology · doi:10.1002/path.2164 · Cited by 136
Self-citationShima, K., Nosho, K., Baba, Y., Cantor, M., Meyerhardt, J. A., Giovannucci, E. L., Fuchs, C. S., & Ogino, S. (2010) · International Journal of Cancer · doi:10.1002/ijc.25432 · Cited by 136
Vessey, C. J., Wilding, J., Folarin, N. I., Hirano, S., Takeichi, M., Soutter, P., Stamp, G., & Pignatelli, M. (1995) · The Journal of Pathology · doi:10.1002/path.1711760208 · Cited by 135
Masaki, T., Matsuoka, H., Sugiyama, M., et al. (2001) · British Journal of Cancer · doi:10.1054/bjoc.2001.1790 · Cited by 130
Invasive front of colorectal cancer: Dynamic interface ofpro-/anti-tumor factors
Zlobec, I., & Lugli, A. (2009) · World Journal of Gastroenterology · doi:10.3748/wjg.15.5898 · Cited by 129
Self-citationLoss of membranous Ep-CAM in budding colorectal carcinoma cells
Gosens, M. J. E. M., van Kempen, L. C. L. T., van de Velde, C. J. �., van Krieken, J. H., & Nagtegaal, I. D. (2007) · Modern Pathology · doi:10.1038/modpathol.3800733 · Cited by 120
Pino, M. S., Kikuchi, H., Zeng, M., Herráiz, M., Sperduti, I., Berger, D. L., Park, D., Iafrate, A. J., Zukerberg, L. R., & Chung, D. C. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.12.010 · Cited by 118
Kim, S., Kang, H. Y., Nam, E.-H., Choi, M. S., Zhao, X.-F., Hong, C. S., Lee, S. E., Lee, J. H., & Park, Y. K. (2010) · Carcinogenesis · doi:10.1093/carcin/bgq024 · Cited by 111
Roger, L., Jullien, L., Gire, V., & Roux, P. (2010) · Journal of Cell Science · doi:10.1242/jcs.061002 · Cited by 108
Long-term results of curative resection of “minimally invasive” colorectal cancer
Hase, K., Shatney, C. H., Mochizuki, H., et al. (1995) · Diseases of the Colon & Rectum · doi:10.1007/bf02053852 · Cited by 105
Li, C.-Y., Li, B.-X., Liang, Y., Peng, R.-Q., Ding, Y., Xu, D.-Z., Zhang, X., Wan, D.-S., Wan, D. S., Zeng, Y.-X., et al. (2009) · Journal of Translational Medicine · doi:10.1186/1479-5876-7-56 · Cited by 102
Intensity of Tumor Budding and Its Prognostic Implications in Invasive Colon Carcinoma
Park, K., Choi, H., Roh, M.-S., Kwon, H.-C., & Kim, C. (2005) · Diseases of the Colon & Rectum · doi:10.1007/s10350-005-0060-6 · Cited by 97
Yasuda, K., Inomata, M., Shiromizu, A., Shiraishi, N., Higashi, H., & Kitano, S. (2007) · Diseases of the Colon & Rectum · doi:10.1007/s10350-007-0263-0 · Cited by 92
Nakamura, T., Mitomi, H., Kikuchi, S., Ohtani, Y., & Sato, K. (2005) · PubMed · Cited by 92
Prognostic Significance of CXCL12 Expression in Patients With Colorectal Carcinoma
Akishima‐Fukasawa, Y., Nakanishi, Y., Ino, Y., Moriya, Y., Kanai, Y., & Hirohashi, S. (2009) · American Journal of Clinical Pathology · doi:10.1309/ajcpk35vzjewcutl · Cited by 86
Prognostic value of immunohistochemical analysis of tumor budding in colorectal carcinoma.
Ohtsuki, K., Koyama, F., Tamura, T., et al. (2008) · PubMed · Cited by 83
Fujiya, M., Watari, J., Ashida, T., Honda, M., Tanabe, H., Fujiki, T., Saitoh, Y., & Kohgo, Y. (2001) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.2001.tb01062.x · Cited by 79
Pathologic Prognostic Factors in the Recurrence of Rectal Cancer
Compton, C. C. (2002) · Clinical Colorectal Cancer · doi:10.3816/ccc.2002.n.020 · Cited by 78
Masaki, T., Goto, A., Sugiyama, M., Matsuoka, H., Abe, N., Sakamoto, A., & Atomi, Y. (2001) · Cancer · Cited by 71
CD44V6 expression in human colorectal carcinoma
Coppola, D., Hyacinthe, M., Fu, L., Cantor, A. B., Karl, R. C., Marcet, J. E., Cooper, D. L., Nicosia, S. V., & Cooper, H. S. (1998) · Human Pathology · doi:10.1016/s0046-8177(98)80014-2 · Cited by 66
Baker, K., Zlobec, I., Tornillo, L., Terracciano, L., Jass, J. R., & Lugli, A. (2007) · European Journal of Cancer · doi:10.1016/j.ejca.2006.11.012 · Cited by 64
Self-citationProposed Objective Criteria for “Grade 3” in Early Invasive Colorectal Cancer
Ueno, H., Hashiguchi, Y., Kajiwara, Y., Shinto, E., Shimazaki, H., Kurihara, H., Mochizuki, H., & Hase, K. (2010) · American Journal of Clinical Pathology · doi:10.1309/ajcpmq7i5zttzsom · Cited by 57
Cyclin D2 activates Cdk2 in preference to Cdk4 in human breast epithelial cells
Sweeney, K. J. E., Šarčević, B., Sutherland, R. L., & Musgrove, E. A. (1997) · Oncogene · doi:10.1038/sj.onc.1200951 · Cited by 54
Tumor budding predicts response to anti-EGFR therapies in metastatic colorectal cancer patients
Zlobec, I., Molinari, F., Martin, V., Mazzucchelli, L., Saletti, P., Trezzi, R., Dosso, S. D., Vlajnic, T., Frattini, M., & Lugli, A. (2010) · World Journal of Gastroenterology · doi:10.3748/wjg.v16.i38.4823 · Cited by 52
Self-citationZlobec, I., Minoo, P., Terracciano, L., Baker, K., & Lugli, A. (2011) · Histopathology · doi:10.1111/j.1365-2559.2011.03975.x · Cited by 49
Self-citationBates, R. C., Pursell, B. M., & Mercurio, A. M. (2007) · Cells Tissues Organs · doi:10.1159/000101300 · Cited by 48
Newer Pathologic Assessment Techniques for Colorectal Carcinoma
Turner, R. R., Li, C., & Compton, C. C. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1151 · Cited by 46
Lugli, A., Zlobec, I., Minoo, P., Baker, K., Tornillo, L., Terracciano, L., & Jass, J. R. (2006) · Human Pathology · doi:10.1016/j.humpath.2006.03.002 · Cited by 43
Self-citationTumour budding, uPA and PAI‐1 are associated with aggressive behaviour in colon cancer
Märkl, B., Renk, P. I., Oruzio, D. V., Jähnig, H., Schenkirsch, G., Schöler, C., Ehret, P. W., Arnholdt, H., Anthuber, M., & Spatz, H. (2010) · Journal of Surgical Oncology · doi:10.1002/jso.21611 · Cited by 41
Hörkkö, T. T., Klintrup, K., Mäkinen, J. M., Näpänkangas, J. P., Tuominen, H. J., Mäkelä, J. T., Karttunen, T. J., & Mäkinen, M. J. (2006) · European Journal of Cancer · doi:10.1016/j.ejca.2006.01.017 · Cited by 41
Peláez, I. M., Καλογεροπούλου, Μ., Ferraro, A., Voulgari, A., Pankotai, T., Boros, I., & Pintzas, A. (2010) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2010.01.024 · Cited by 40
Tumor Budding and Survival After Potentially Curative Resection of Node-Positive Colon Cancer
Sy, J. S., Fung, C. L.-S., Dent, O. F., Chapuis, P. H., Bokey, L., & Chan, C. (2010) · Diseases of the Colon & Rectum · doi:10.1007/dcr.0b013e3181c3ed05 · Cited by 40
Novel Snail1 Target Proteins in Human Colon Cancer Identified by Proteomic Analysis
Larriba, M. J., Casado‐Vela, J., Pendás-Franco, N., Peña, R., de Herreros, A. G., Berciano, M. T., Lafarga, M., Casal, J. I., & Múñoz, A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010221 · Cited by 33
Zlobec, I., Günthert, U., Tornillo, L., Iezzi, G., Baumhoer, D., Terracciano, L., & Lugli, A. (2009) · Histopathology · doi:10.1111/j.1365-2559.2009.03421.x · Cited by 30
Self-citationPrall, F., Ostwald, C., Weirich, V., & Nizze, H. (2006) · Human Pathology · doi:10.1016/j.humpath.2006.01.005 · Cited by 14
Cited by
To differentiate or not — routes towards metastasis
Brabletz, T. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3265 · Cited by 623
Determinants of metastatic competency in colorectal cancer
Tauriello, D. V. F., Calon, A., Lonardo, E., & Batlle, E. (2017) · Molecular Oncology · doi:10.1002/1878-0261.12018 · Cited by 258
Trinh, A., Trumpi, K., De Sousa E Melo, F., Wang, X., de Jong, J. H., Fessler, E., Kuppen, P. J. K., Reimers, M. S., Swets, M., Koopman, M., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0680 · Cited by 180
De Smedt, L., Palmans, S., Andel, D., Govaere, O., Boeckx, B., Smeets, D., Galle, E., Wouters, J., Barras, D., Suffiotti, M., et al. (2017) · British Journal of Cancer · doi:10.1038/bjc.2016.382 · Cited by 163
Metadata
- Authors
- Zlobec, I., & Lugli, A.
- Venue
- Oncotarget
- Publisher
- Impact Journals, LLC
- Published
- 2010-11-28
- Volume
- 1
- Issue
- 7
- Pages
- 651-661
- ISSN
- 1949-2553 (ISSN-L)
- OpenAlex
- W2160120862
- Cited by
- 331
- References
- 69
- FWCI
- 6.41
- Type
- journal article
- Language
- en
- Open access
- hybrid
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
