Tumor budding in upper gastrointestinal carcinomas

Frontiers in Oncology

Volumn 4 JUL, Issue , 2014, Pages

  Koelzer, Viktor Hendrik ^a   Langer, Rupert ^a   Zlobec, Inti ^a   Lugli, Alessandro ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER PROGNOSIS; CANCER STAGING; CELL BUDDING; DISTANT METASTASIS; ENDOSCOPIC MUCOSAL RESECTION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS; ESOPHAGUS CARCINOMA; GASTROINTESTINAL CARCINOMA; HISTOLOGY; HUMAN; RADIOFREQUENCY ABLATION; RECURRENT DISEASE; REVIEW; RISK ASSESSMENT; SCORING SYSTEM; STOMACH ADENOCARCINOMA; TUMOR BUDDING; TUMOR INVASION; TUMOR VOLUME; ARTICLE; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGUS RESECTION; IMMUNOHISTOCHEMISTRY; MULTICENTER STUDY (TOPIC); NEOPLASM; SURVIVAL RATE;

PEPTIDES AND PROTEINS; TROPOMYOSIN RELATED RECEPTOR KINASE B; UNCLASSIFIED DRUG;

EID: 84906318495     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00216     Document Type: Review

References (68)

1. F.T. Bosman, World Health Organization., and International Agency for Research on Cancer., WHO classification of tumours of the digestive system, International Agency for Research on Cancer, Lyon, 2010.
2. M. Stahl, W. Budach, H.J. Meyer, A. Cervantes, and E.G.W. Group, Esophageal cancer: Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of oncology: official journal of the European Society for Medical Oncology / ESMO 21 Suppl 5 (2010) v46-9.
3. T.W. Rice, E.H. Blackstone, and V.W. Rusch, 7th edition of the AJCC Cancer Staging Manual: esophagus and esophagogastric junction. Annals of surgical oncology 17 (2010) 1721-4.
4. S. Raja, T.W. Rice, J.R. Goldblum, L.A. Rybicki, S.C. Murthy, D.P. Mason, and E.H. Blackstone, Esophageal submucosa: the watershed for esophageal cancer. The Journal of thoracic and cardiovascular surgery 142 (2011) 1403-11 e1.
5. A.P. Barbour, M. Jones, I. Brown, D.C. Gotley, I. Martin, J. Thomas, A. Clouston, and B.M. Smithers, Risk stratification for early esophageal adenocarcinoma: analysis of lymphatic spread and prognostic factors. Annals of surgical oncology 17 (2010) 2494-502.
6. I. Zlobec, and A. Lugli, Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: tumor budding as oncotarget. Oncotarget 1 (2010) 651-61.
7. B. De Craene, and G. Berx, Regulatory networks defining EMT during cancer initiation and progression. Nature reviews. Cancer 13 (2013) 97-110.
8. D. Kevans, L.M. Wang, K. Sheahan, J. Hyland, D. O'Donoghue, H. Mulcahy, and J. O'Sullivan, Epithelial-mesenchymal transition (EMT) protein expression in a cohort of stage II colorectal cancer patients with characterized tumor budding and mismatch repair protein status. International journal of surgical pathology 19 (2011) 751-60.
9. A. Lugli, G. Iezzi, I. Hostettler, M.G. Muraro, V. Mele, L. Tornillo, V. Carafa, G. Spagnoli, L. Terracciano, and I. Zlobec, Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. British journal of cancer 103 (2010) 382-90.
10. F. Prall, Tumour budding in colorectal carcinoma. Histopathology 50 (2007) 151-62.
11. M.S. Roh, J.I. Lee, and P.J. Choi, Tumor budding as a useful prognostic marker in esophageal squamous cell carcinoma. Diseases of the esophagus: official journal of the International Society for Diseases of the Esophagus / I.S.D.E 17 (2004) 333-7.
12. M. Koike, Y. Kodera, Y. Itoh, G. Nakayama, M. Fujiwara, N. Hamajima, and A. Nakao, Multivariate analysis of the pathologic features of esophageal squamous cell cancer: tumor budding is a significant independent prognostic factor. Annals of surgical oncology 15 (2008) 1977-82.
13. H. Miyata, A. Yoshioka, M. Yamasaki, Y. Nushijima, S. Takiguchi, Y. Fujiwara, T. Nishida, M. Mano, M. Mori, and Y. Doki, Tumor budding in tumor invasive front predicts prognosis and survival of patients with esophageal squamous cell carcinomas receiving neoadjuvant chemotherapy. Cancer 115 (2009) 3324-34.
14. Y. Nakanishi, M. Ohara, H. Doumen, N. Kimura, T. Ishidate, and S. Kondo, Correlation between tumor budding and post-resection prognosis in patients with invasive squamous cell carcinoma of the thoracic esophagus. World journal of surgery 35 (2011) 349-56.
15. H. Teramoto, M. Koike, C. Tanaka, S. Yamada, G. Nakayama, T. Fujii, H. Sugimoto, M. Fujiwara, Y. Suzuki, and Y. Kodera, Tumor budding as a useful prognostic marker in T1-stage squamous cell carcinoma of the esophagus. Journal of surgical oncology 108 (2013) 42-6.
16. M. Brown, K. Sillah, E.A. Griffiths, R. Swindell, C.M. West, R.D. Page, I.M. Welch, and S.A. Pritchard, Tumour budding and a low host inflammatory response are associated with a poor prognosis in oesophageal and gastro-oesophageal junction cancers. Histopathology 56 (2010) 893-9.
17. S. Thies, J. Slotta-Huspenina, and I. Zlobec, The impact of tumor budding in oesophageal adenocarcinomas. Der Pathologe 34 (2013) 78.
18. J.A. Nowak, A. Agoston, Y. Zheng, R. Bueno, R.D. Odze, and A. Srivastava, Tumor budding is a predictor of nodal metastasis and tumor recurrence in T1 esophageal adenocarcinoma. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc 26 (2013) 169A.
19. M.S. Landau, S.M. Hastings, T.J. Foxwell, J.D. Luketich, K.S. Nason, and J.M. Davison, Tumor budding is associated with an increased risk of lymph node metastasis and poor prognosis in superficial esophageal adenocarcinoma. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc (2014).
20. H.E. Gabbert, S. Meier, C.D. Gerharz, and G. Hommel, Tumor-cell dissociation at the invasion front: a new prognostic parameter in gastric cancer patients. International journal of cancer. Journal international du cancer 50 (1992) 202-7.
21. K. Tanaka, T. Shimura, T. Kitajima, S. Kondo, S. Ide, Y. Okugawa, S. Saigusa, Y. Toiyama, Y. Inoue, T. Araki, K. Uchida, Y. Mohri, and M. Kusunoki, Tropomyosin-related receptor kinase B at the invasive front and tumour cell dedifferentiation in gastric cancer. British journal of cancer (2014).
22. H. Ueno, H. Mochizuki, Y. Hashiguchi, H. Shimazaki, S. Aida, K. Hase, S. Matsukuma, T. Kanai, H. Kurihara, K. Ozawa, K. Yoshimura, and S. Bekku, Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology 127 (2004) 385-94.
23. T. Nakamura, H. Mitomi, H. Kanazawa, Y. Ohkura, and M. Watanabe, Tumor budding as an index to identify high-risk patients with stage II colon cancer. Diseases of the colon and rectum 51 (2008) 568-72.
24. L.M. Wang, D. Kevans, H. Mulcahy, J. O'Sullivan, D. Fennelly, J. Hyland, D. O'Donoghue, and K. Sheahan, Tumor budding is a strong and reproducible prognostic marker in T3N0 colorectal cancer. The American journal of surgical pathology 33 (2009) 134-41.
25. E. Karamitopoulou, I. Zlobec, V. Kolzer, A. Kondi-Pafiti, E.S. Patsouris, K. Gennatas, and A. Lugli, Proposal for a 10-high-power-fields scoring method for the assessment of tumor budding in colorectal cancer. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc 26 (2013) 295-301.
26. T. Masaki, H. Matsuoka, M. Sugiyama, N. Abe, A. Sakamoto, T. Watanabe, H. Nagawa, and Y. Atomi, Tumor budding and evidence-based treatment of T2 rectal carcinomas. Journal of surgical oncology 92 (2005) 59-63.
27. B. Mitrovic, D.F. Schaeffer, R.H. Riddell, and R. Kirsch, Tumor budding in colorectal carcinoma: time to take notice. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc 25 (2012) 1315-25.
28. H. Ueno, H. Mochizuki, E. Shinto, Y. Hashiguchi, K. Hase, and I.C. Talbot, Histologic indices in biopsy specimens for estimating the probability of extended local spread in patients with rectal carcinoma. Cancer 94 (2002) 2882-91.
29. T. Okuyama, M. Oya, and H. Ishikawa, Budding as a useful prognostic marker in pT3 well- or moderately-differentiated rectal adenocarcinoma. Journal of surgical oncology 83 (2003) 42-7.
30. M. Vieth, P. Quirke, R. Lambert, L. von Karsa, M. Risio, and C. International Agency for Research on, European guidelines for quality assurance in colorectal cancer screening and diagnosis. First Edition--Annotations of colorectal lesions. Endoscopy 44 Suppl 3 (2012) SE131-9.
31. T. Watanabe, M. Itabashi, Y. Shimada, S. Tanaka, Y. Ito, Y. Ajioka, T. Hamaguchi, I. Hyodo, M. Igarashi, H. Ishida, M. Ishiguro, Y. Kanemitsu, N. Kokudo, K. Muro, A. Ochiai, M. Oguchi, Y. Ohkura, Y. Saito, Y. Sakai, H. Ueno, T. Yoshino, T. Fujimori, N. Koinuma, T. Morita, G. Nishimura, Y. Sakata, K. Takahashi, H. Takiuchi, O. Tsuruta, T. Yamaguchi, M. Yoshida, N. Yamaguchi, K. Kotake, K. Sugihara, C. Japanese Society for Cancer of the, and Rectum, Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. International journal of clinical oncology 17 (2012) 1-29.
32. H.J. Schmoll, E. Van Cutsem, A. Stein, V. Valentini, B. Glimelius, K. Haustermans, B. Nordlinger, C.J. van de Velde, J. Balmana, J. Regula, I.D. Nagtegaal, R.G. Beets-Tan, D. Arnold, F. Ciardiello, P. Hoff, D. Kerr, C.H. Kohne, R. Labianca, T. Price, W. Scheithauer, A. Sobrero, J. Tabernero, D. Aderka, S. Barroso, G. Bodoky, J.Y. Douillard, H. El Ghazaly, J. Gallardo, A. Garin, R. Glynne-Jones, K. Jordan, A. Meshcheryakov, D. Papamichail, P. Pfeiffer, I. Souglakos, S. Turhal, and A. Cervantes, ESMO Consensus Guidelines for management of patients with colon and rectal cancer. a personalized approach to clinical decision making. Annals of oncology: official journal of the European Society for Medical Oncology / ESMO 23 (2012) 2479-516.
33. C.J. van de Velde, P.G. Boelens, J.M. Borras, J.W. Coebergh, A. Cervantes, L. Blomqvist, R.G. Beets-Tan, C.B. van den Broek, G. Brown, E. Van Cutsem, E. Espin, K. Haustermans, B. Glimelius, L.H. Iversen, J.H. van Krieken, C.A. Marijnen, G. Henning, J. Gore-Booth, E. Meldolesi, P. Mroczkowski, I. Nagtegaal, P. Naredi, H. Ortiz, L. Pahlman, P. Quirke, C. Rodel, A. Roth, H. Rutten, H.J. Schmoll, J.J. Smith, P.J. Tanis, C. Taylor, A. Wibe, T. Wiggers, M.A. Gambacorta, C. Aristei, and V. Valentini, EURECCA colorectal: multidisciplinary management: European consensus conference colon & rectum. European journal of cancer 50 (2014) 1 e1-1 e34.
34. J.R. Jass, M. Barker, L. Fraser, M.D. Walsh, V.L. Whitehall, B. Gabrielli, J. Young, and B.A. Leggett, APC mutation and tumour budding in colorectal cancer. Journal of clinical pathology 56 (2003) 69-73.
35. K. Guzinska-Ustymowicz, MMP-9 and cathepsin B expression in tumor budding as an indicator of a more aggressive phenotype of colorectal cancer (CRC). Anticancer research 26 (2006) 1589-94.
36. C. Pyke, S. Salo, E. Ralfkiaer, J. Romer, K. Dano, and K. Tryggvason, Laminin-5 is a marker of invading cancer cells in some human carcinomas and is coexpressed with the receptor for urokinase plasminogen activator in budding cancer cells in colon adenocarcinomas. Cancer research 55 (1995) 4132-9.
37. V.H. Koelzer, E. Karamitopoulou, H. Dawson, A. Kondi-Pafiti, I. Zlobec, and A. Lugli, Geographic analysis of RKIP expression and its clinical relevance in colorectal cancer. British journal of cancer 108 (2013) 2088-96.
38. H. Dawson, V.H. Koelzer, E. Karamitopoulou, M. Economou, C. Hammer, D.E. Muller, A. Lugli, and I. Zlobec, The apoptotic and proliferation rate of tumour budding cells in colorectal cancer outlines a heterogeneous population of cells with various impacts on clinical outcome. Histopathology 64 (2014) 577-84.
39. H.A.E. Dawson, I. Zlobec, V.H. Koelzer, E. Karamitopoulou, and A. Lugli, Expression pattern of TrkB in colorectal cancer supports anoikis-resistance as a survival mechanism for tumor budding cells.. Virchows Archiv 463 (2013).
40. A. Jung, M. Schrauder, U. Oswald, C. Knoll, P. Sellberg, R. Palmqvist, G. Niedobitek, T. Brabletz, and T. Kirchner, The invasion front of human colorectal adenocarcinomas shows colocalization of nuclear beta-catenin, cyclin D1, and p16INK4A and is a region of low proliferation. The American journal of pathology 159 (2001) 1613-7.
41. A.C. Rogers, D. Gibbons, A.M. Hanly, J.M. Hyland, P.R. O'Connell, D.C. Winter, and K. Sheahan, Prognostic significance of tumor budding in rectal cancer biopsies before neoadjuvant therapy. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc (2013).
42. R. Tallerico, M. Todaro, S. Di Franco, C. Maccalli, C. Garofalo, R. Sottile, C. Palmieri, L. Tirinato, P.N. Pangigadde, R. La Rocca, O. Mandelboim, G. Stassi, E. Di Fabrizio, G. Parmiani, A. Moretta, F. Dieli, K. Karre, and E. Carbone, Human NK cells selective targeting of colon cancer-initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules. Journal of immunology 190 (2013) 2381-90.
43. I. Zlobec, P. Minoo, L. Terracciano, K. Baker, and A. Lugli, Characterization of the immunological microenvironment of tumour buds and its impact on prognosis in mismatch repair-proficient and -deficient colorectal cancers. Histopathology 59 (2011) 482-95.
44. L. Hostettler, I. Zlobec, L. Terracciano, and A. Lugli, ABCG5-positivity in tumor buds is an indicator of poor prognosis in node-negative colorectal cancer patients. World journal of gastroenterology: WJG 16 (2010) 732-9.
45. T. Morodomi, H. Isomoto, K. Shirouzu, K. Kakegawa, K. Irie, and M. Morimatsu, An index for estimating the probability of lymph node metastasis in rectal cancers. Lymph node metastasis and the histopathology of actively invasive regions of cancer. Cancer 63 (1989) 539-43.
46. K. Hase, C. Shatney, D. Johnson, M. Trollope, and M. Vierra, Prognostic value of tumor "budding" in patients with colorectal cancer. Diseases of the colon and rectum 36 (1993) 627-35.
47. T. Nakamura, H. Mitomi, S. Kikuchi, Y. Ohtani, and K. Sato, Evaluation of the usefulness of tumor budding on the prediction of metastasis to the lung and liver after curative excision of colorectal cancer. Hepato-gastroenterology 52 (2005) 1432-5.
48. H. Ueno, J. Murphy, J.R. Jass, H. Mochizuki, and I.C. Talbot, Tumour 'budding' as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology 40 (2002) 127-32.
49. M. Ono, M. Sakamoto, Y. Ino, Y. Moriya, K. Sugihara, T. Muto, and S. Hirohashi, Cancer cell morphology at the invasive front and expression of cell adhesion-related carbohydrate in the primary lesion of patients with colorectal carcinoma with liver metastasis. Cancer 78 (1996) 1179-86.
50. K.J. Park, H.J. Choi, M.S. Roh, H.C. Kwon, and C. Kim, Intensity of tumor budding and its prognostic implications in invasive colon carcinoma. Diseases of the colon and rectum 48 (2005) 1597-602.
51. A. Lugli, E. Karamitopoulou, I. Panayiotides, P. Karakitsos, G. Rallis, G. Peros, G. Iezzi, G. Spagnoli, M. Bihl, L. Terracciano, and I. Zlobec, CD8+ lymphocytes/ tumour-budding index: an independent prognostic factor representing a 'pro-/anti-tumour' approach to tumour host interaction in colorectal cancer. British journal of cancer 101 (2009) 1382-92.
52. N. Ohike, I. Coban, G.E. Kim, O. Basturk, T. Tajiri, A. Krasinskas, S. Bandyopadhyay, T. Morohoshi, Y. Shimada, D.A. Kooby, C.A. Staley, M. Goodman, and N.V. Adsay, Tumor budding as a strong prognostic indicator in invasive ampullary adenocarcinomas. The American journal of surgical pathology 34 (2010) 1417-24.
53. M. Horcic, V.H. Koelzer, E. Karamitopoulou, L. Terracciano, G. Puppa, I. Zlobec, and A. Lugli, Tumor budding score based on 10 high-power fields is a promising basis for a standardized prognostic scoring system in stage II colorectal cancer. Human pathology 44 (2013) 697-705.
54. H. Teramoto, M. Koike, C. Tanaka, S. Yamada, G. Nakayama, T. Fujii, H. Sugimoto, M. Fujiwara, Y. Suzuki, and Y. Kodera, Tumor budding as a useful prognostic marker in T1-stage squamous cell carcinoma of the esophagus. Journal of surgical oncology (2013).
55. I. Gockel, G. Sgourakis, O. Lyros, U. Polotzek, C.C. Schimanski, H. Lang, T. Hoppo, and B.A. Jobe, Risk of lymph node metastasis in submucosal esophageal cancer: a review of surgically resected patients. Expert review of gastroenterology & hepatology 5 (2011) 371-84.
56. O.T. Giger, S.C. Comtesse, A. Lugli, I. Zlobec, and M.O. Kurrer, Intra-tumoral budding in preoperative biopsy specimens predicts lymph node and distant metastasis in patients with colorectal cancer. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc 25 (2012) 1048-53.
57. I. Zlobec, M. Hadrich, H. Dawson, V.H. Koelzer, M. Borner, M. Mallaev, B. Schnuriger, D. Inderbitzin, and A. Lugli, Intratumoural budding (ITB) in preoperative biopsies predicts the presence of lymph node and distant metastases in colon and rectal cancer patients. British journal of cancer 110 (2014) 1008-13.
58. T. Waddell, M. Verheij, W. Allum, D. Cunningham, A. Cervantes, D. Arnold, O. European Society for Medical, O. European Society of Surgical, R. European Society of, and Oncology, Gastric cancer: ESMO-ESSO-ESTRO clinical practice guidelines for diagnosis, treatment and followup. European journal of surgical oncology: the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology 40 (2014) 584-91.
59. NCCN practice guidelines for upper gastrointestinal carcinomas. National Comprehensive Cancer Network. Oncology 12 (1998) 179-223.
60. V.E. Strong, T.A. D'Amico, L. Kleinberg, and J. Ajani, Impact of the 7th Edition AJCC staging classification on the NCCN clinical practice guidelines in oncology for gastric and esophageal cancers. Journal of the National Comprehensive Cancer Network: JNCCN 11 (2013) 60-6.
61. J.S. Macdonald, S.R. Smalley, J. Benedetti, S.A. Hundahl, N.C. Estes, G.N. Stemmermann, D.G. Haller, J.A. Ajani, L.L. Gunderson, J.M. Jessup, and J.A. Martenson, Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. The New England journal of medicine 345 (2001) 725-30.
62. M.A. Smit, T.R. Geiger, J.Y. Song, I. Gitelman, and D.S. Peeper, A Twist-Snail axis critical for TrkBinduced epithelial-mesenchymal transition-like transformation, anoikis resistance, and metastasis. Molecular and cellular biology 29 (2009) 3722-37.
63. K. Tanaka, Y. Mohri, J. Nishioka, M. Ohi, T. Yokoe, C. Miki, H. Tonouchi, T. Nobori, and M. Kusunoki, Neurotrophic receptor, tropomyosin-related kinase B, as a chemoresistant marker in oesophageal cancer. Clinical oncology 21 (2009) 362-3.
64. P. Guilford, J. Hopkins, J. Harraway, M. McLeod, N. McLeod, P. Harawira, H. Taite, R. Scoular, A. Miller, and A.E. Reeve, E-cadherin germline mutations in familial gastric cancer. Nature 392 (1998) 402-5.
65. J.R. Jass, W.S. Atkin, J. Cuzick, H.J. Bussey, B.C. Morson, J.M. Northover, and I.P. Todd, The grading of rectal cancer: historical perspectives and a multivariate analysis of 447 cases. Histopathology 10 (1986) 437-59.
66. J.R. Jass, S.B. Love, and J.M. Northover, A new prognostic classification of rectal cancer. Lancet 1 (1987) 1303-6.
67. K. Ohtsuki, F. Koyama, T. Tamura, Y. Enomoto, H. Fujii, T. Mukogawa, T. Nakagawa, K. Uchimoto, S. Nakamura, A. Nonomura, and Y. Nakajima, Prognostic value of immunohistochemical analysis of tumor budding in colorectal carcinoma. Anticancer research 28 (2008) 1831-6.
68. P.D. Caie, A.K. Turnbull, S.M. Farrington, A. Oniscu, and D.J. Harrison, Quantification of tumour budding, lymphatic vessel density and invasion through image analysis in colorectal cancer. Journal of translational medicine 12 (2014) 156.