Skip to main content
Top
Published in: BMC Surgery 1/2012

Open Access 01-12-2012 | Research article

Tumor budding as a risk factor of lymph node metastasis in submucosal invasive T1 colorectal carcinoma: a retrospective study

Authors: Bong-Hyeon Kye, Ji-Han Jung, Hyung-Jin Kim, Se-Goo Kang, Hyeon-Min Cho, Jun-Gi Kim

Published in: BMC Surgery | Issue 1/2012

Login to get access

Abstract

Background

This study was designed to identify risk factors for lymph node metastasis of early stage colorectal cancer, which was confirmed to a carcinoma that invaded the submucosa after radical resection.

Methods

In total, 55 patients revealing submucosal invasive colorectal carcinoma on pathology who underwent curative radical resection at the Department of Surgery, St. Vincent’s Hospital, The Catholic University of Korea from January 2007 to September 2010 were evaluated retrospectively. Tumor size, depth of submucosal invasion, histologic grade, lymphovascular invasion, tumor budding, and microacinar structure were reviewed by a single pathologist. Student t-test for continuous variables and Chi-square test for categorical variables were used for comparing the clinicopathological features between two groups (whether lymph node involvement existed or not). Continuous variables are expressed as the mean ± standard error while statistical significance is accepted at P < 0.05.

Results

The mean age of 55 patients (34 males and 21 females) was 61.2 ± 9.6 years (range, 43–83). Histologically, eight (14.5%) patients had metastatic lymph node. In the univariate analysis, tumor budding (P = 0.047) was the only factor that was significantly associated with lymph node metastasis. Also, the tumor budding had a sensitivity of 83.3%, a specificity of 60.5%, and a negative predictive value of 0.958 for lymph node metastasis in submucosal invasive T1 colorectal cancer.

Conclusions

The tumor budding seems to have a high sensitivity (83.3%), acceptable specificity (60.5%), and a high negative predictive value (0.958). A close examination of pathologic finding including tumor budding should be performed in order to manage early CRC properly.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kudo S, Tamegai Y, Yamano H, Imai Y, Kogure E, Kashida H: Endoscopic mucosal resection of the colon: the Japanese technique. Gastrointest Endosc Clin N Am. 2001, 11: 519-535.PubMed Kudo S, Tamegai Y, Yamano H, Imai Y, Kogure E, Kashida H: Endoscopic mucosal resection of the colon: the Japanese technique. Gastrointest Endosc Clin N Am. 2001, 11: 519-535.PubMed
2.
go back to reference Yamamoto H, Koiwai H, Yube T, Isoda N, Sato Y, Sekine Y, Higashizawa T, Utsunomity K, Ido K, Sugano K: A successful single-step endoscopic resection of a 40 millimeter flat-elevated tumor in the rectum: endoscopic mucosal resection using sodium hyaluronate. Gastrointest Endosc. 1999, 50: 701-704. 10.1016/S0016-5107(99)80026-1.CrossRefPubMed Yamamoto H, Koiwai H, Yube T, Isoda N, Sato Y, Sekine Y, Higashizawa T, Utsunomity K, Ido K, Sugano K: A successful single-step endoscopic resection of a 40 millimeter flat-elevated tumor in the rectum: endoscopic mucosal resection using sodium hyaluronate. Gastrointest Endosc. 1999, 50: 701-704. 10.1016/S0016-5107(99)80026-1.CrossRefPubMed
3.
go back to reference Hurlstone DP, Sanders DS, Cross SS, Adam I, Shorthouse AJ, Brown S, Drew K, Lobo AJ: Colonoscopic resection of lateral spreading tumours: a prospective analysis of endoscopic mucosal resection. Gut. 2004, 53: 1334-1339. 10.1136/gut.2003.036913.CrossRefPubMedPubMedCentral Hurlstone DP, Sanders DS, Cross SS, Adam I, Shorthouse AJ, Brown S, Drew K, Lobo AJ: Colonoscopic resection of lateral spreading tumours: a prospective analysis of endoscopic mucosal resection. Gut. 2004, 53: 1334-1339. 10.1136/gut.2003.036913.CrossRefPubMedPubMedCentral
4.
go back to reference Kudo S, Kashida H, Tamura T, Kogure E, Imai Y, Yamano H, Hart AR: Colonoscopic diagnosis and management of nonpolypoid early colorectal cancer. World J Surg. 2000, 24: 1081-1090. 10.1007/s002680010154.CrossRefPubMed Kudo S, Kashida H, Tamura T, Kogure E, Imai Y, Yamano H, Hart AR: Colonoscopic diagnosis and management of nonpolypoid early colorectal cancer. World J Surg. 2000, 24: 1081-1090. 10.1007/s002680010154.CrossRefPubMed
5.
go back to reference Nivatvongs S: Surgical management of early colorectal cancer. World J Surg. 2000, 24: 1052-1055. 10.1007/s002680010148.CrossRefPubMed Nivatvongs S: Surgical management of early colorectal cancer. World J Surg. 2000, 24: 1052-1055. 10.1007/s002680010148.CrossRefPubMed
6.
go back to reference Sung HY, Kang WK, Kim SW, Nam KW, Jung CK, Chang JH, Cho YK, Park JM, Lee IS, Lee JI, Oh ST, Choi MK, Chung IS: Risk factors for lymph node metastasis in patients with submucosal invasive colorectal carcinoma. J Korean Surg Soc. 2010, 78: 207-212. 10.4174/jkss.2010.78.4.207.CrossRef Sung HY, Kang WK, Kim SW, Nam KW, Jung CK, Chang JH, Cho YK, Park JM, Lee IS, Lee JI, Oh ST, Choi MK, Chung IS: Risk factors for lymph node metastasis in patients with submucosal invasive colorectal carcinoma. J Korean Surg Soc. 2010, 78: 207-212. 10.4174/jkss.2010.78.4.207.CrossRef
7.
go back to reference Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R, Fujiyoshi T, Uchida Y: Management of early invasive colorectal cancer; Risk of recurrence and clinical guidelines. Dis Colon Rectum. 1995, 38: 1286-1295. 10.1007/BF02049154.CrossRefPubMed Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R, Fujiyoshi T, Uchida Y: Management of early invasive colorectal cancer; Risk of recurrence and clinical guidelines. Dis Colon Rectum. 1995, 38: 1286-1295. 10.1007/BF02049154.CrossRefPubMed
8.
go back to reference Rossini FP, Ferrari A, Coverlizza S, Spandre M, Risio M, Gemme C, Cavallero M: Large bowel adenomas containing carcinoma–a diagnostic and therapeutic approach. Int J Colorectal Dis. 1988, 3: 47-52. 10.1007/BF01649684.CrossRefPubMed Rossini FP, Ferrari A, Coverlizza S, Spandre M, Risio M, Gemme C, Cavallero M: Large bowel adenomas containing carcinoma–a diagnostic and therapeutic approach. Int J Colorectal Dis. 1988, 3: 47-52. 10.1007/BF01649684.CrossRefPubMed
9.
go back to reference Yasuda K, Inomata M, Shiromizu A, Shiraishi N, Higashi H, Kitano S: Risk factors for occult lymph node metastasis of colorectal cancer invading the submucosa and indications for endoscopic mucosal resection. Dis Colon Rectum. 2007, 50: 1370-1376. 10.1007/s10350-007-0263-0.CrossRefPubMed Yasuda K, Inomata M, Shiromizu A, Shiraishi N, Higashi H, Kitano S: Risk factors for occult lymph node metastasis of colorectal cancer invading the submucosa and indications for endoscopic mucosal resection. Dis Colon Rectum. 2007, 50: 1370-1376. 10.1007/s10350-007-0263-0.CrossRefPubMed
10.
go back to reference Ishikawa Y, Akishima-Fukasawa Y, Ito K, Akasaka Y, Yokoo T, Ishii T: Toho Study Group for Cancer Biological Behavior: Histopathologic determinants of regional lymph node metastasis in early colorectal cancer. Cancer. 2008, 112: 924-933. 10.1002/cncr.23248.CrossRefPubMed Ishikawa Y, Akishima-Fukasawa Y, Ito K, Akasaka Y, Yokoo T, Ishii T: Toho Study Group for Cancer Biological Behavior: Histopathologic determinants of regional lymph node metastasis in early colorectal cancer. Cancer. 2008, 112: 924-933. 10.1002/cncr.23248.CrossRefPubMed
11.
go back to reference The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon. Gastrointest Endosc. 2003, 58: S3--S43. November 30 to December 1, 2002 The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon. Gastrointest Endosc. 2003, 58: S3--S43. November 30 to December 1, 2002
12.
go back to reference Goldstein NS, Hart J: Histologic features associated with lymph node metastasis in stage T1 and superficial T2 rectal adenocarcinomas in abdominoperineal resection specimen: Identifying a subset of patients for whom treatment with adjuvant therapy or completion abdominoperineal resection should be considered after local excision. Am J Clin Pathol. 1999, 111: 51-58.CrossRefPubMed Goldstein NS, Hart J: Histologic features associated with lymph node metastasis in stage T1 and superficial T2 rectal adenocarcinomas in abdominoperineal resection specimen: Identifying a subset of patients for whom treatment with adjuvant therapy or completion abdominoperineal resection should be considered after local excision. Am J Clin Pathol. 1999, 111: 51-58.CrossRefPubMed
13.
go back to reference Volk EE, Goldblum JR, Petras RE, Carev WD, Fazio VW: Management and outcome of patients with invasive carcinoma arising in colorectal polyps. Gastroenterology. 1995, 109: 1801-1807. 10.1016/0016-5085(95)90746-7.CrossRefPubMed Volk EE, Goldblum JR, Petras RE, Carev WD, Fazio VW: Management and outcome of patients with invasive carcinoma arising in colorectal polyps. Gastroenterology. 1995, 109: 1801-1807. 10.1016/0016-5085(95)90746-7.CrossRefPubMed
14.
go back to reference Seitz U, Bohnacker S, Seewald S, Thonke F, Brand B, Bräutigam T, Soehendra N: Is endoscopic polypectomy an adequate therapy for malignant colorectal adenomas? Presentation of 114 patients and review of the literature. Dis Colon Rectum. 2004, 47: 1789-1797. 10.1007/s10350-004-0680-2.CrossRefPubMed Seitz U, Bohnacker S, Seewald S, Thonke F, Brand B, Bräutigam T, Soehendra N: Is endoscopic polypectomy an adequate therapy for malignant colorectal adenomas? Presentation of 114 patients and review of the literature. Dis Colon Rectum. 2004, 47: 1789-1797. 10.1007/s10350-004-0680-2.CrossRefPubMed
15.
go back to reference Kitajima K, Fujimori T, Fujii S, Takeda J, Ohkura Y, Kawamata H, Kumamoto T, Ishiguro S, Kato Y, Shimoda T, Iwashita A, Ajioka Y, Watanabe H, Watanabe T, Muto T, Nagasako K: Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol. 2004, 39: 534-543.CrossRefPubMed Kitajima K, Fujimori T, Fujii S, Takeda J, Ohkura Y, Kawamata H, Kumamoto T, Ishiguro S, Kato Y, Shimoda T, Iwashita A, Ajioka Y, Watanabe H, Watanabe T, Muto T, Nagasako K: Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol. 2004, 39: 534-543.CrossRefPubMed
16.
go back to reference Ueno H, Mochizuki H, Hashiguchi Y, Shimazaki H, Aida S, Hase K, Matsukuma S, Kanai T, Kurihara H, Ozawa K, Yoshimura K, Nekku S: Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology. 2004, 127: 385-394. 10.1053/j.gastro.2004.04.022.CrossRefPubMed Ueno H, Mochizuki H, Hashiguchi Y, Shimazaki H, Aida S, Hase K, Matsukuma S, Kanai T, Kurihara H, Ozawa K, Yoshimura K, Nekku S: Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology. 2004, 127: 385-394. 10.1053/j.gastro.2004.04.022.CrossRefPubMed
17.
go back to reference Nascimbeni R, Burgart LJ, Nivatvongs S, Larson DR: Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum. 2002, 45: 200-206. 10.1007/s10350-004-6147-7.CrossRefPubMed Nascimbeni R, Burgart LJ, Nivatvongs S, Larson DR: Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum. 2002, 45: 200-206. 10.1007/s10350-004-6147-7.CrossRefPubMed
18.
go back to reference Compton C, Fenoglio-Preiser CM, Pettigrew N, Fielding LP: American joint committee on cancer prognostic factors consensus conference: colorectal working group. Cancer. 2000, 88: 1739-1757. 10.1002/(SICI)1097-0142(20000401)88:7<1739::AID-CNCR30>3.0.CO;2-T.CrossRefPubMed Compton C, Fenoglio-Preiser CM, Pettigrew N, Fielding LP: American joint committee on cancer prognostic factors consensus conference: colorectal working group. Cancer. 2000, 88: 1739-1757. 10.1002/(SICI)1097-0142(20000401)88:7<1739::AID-CNCR30>3.0.CO;2-T.CrossRefPubMed
19.
go back to reference Ishii M, Ota M, Saito S, Kinugasa Y, Akamoto S, Ito I: Lymphatic vessel invasion detected by monoclonal antibody D2-40 as a predictor of lymph node metastasis in T1 colorectal cancer. Int J Colorectal Dis. 2009, 24: 1069-1074. 10.1007/s00384-009-0699-x.CrossRefPubMed Ishii M, Ota M, Saito S, Kinugasa Y, Akamoto S, Ito I: Lymphatic vessel invasion detected by monoclonal antibody D2-40 as a predictor of lymph node metastasis in T1 colorectal cancer. Int J Colorectal Dis. 2009, 24: 1069-1074. 10.1007/s00384-009-0699-x.CrossRefPubMed
20.
go back to reference Fujimori T, Fujii S, Saito N, Sugihara K: Pathological diagnosis or early colorectal carcinoma and its clinical implications. Digestion. 2009, 79: 40-51.CrossRefPubMed Fujimori T, Fujii S, Saito N, Sugihara K: Pathological diagnosis or early colorectal carcinoma and its clinical implications. Digestion. 2009, 79: 40-51.CrossRefPubMed
21.
go back to reference Morodomi T, Isomoto H, Shirouzu K, Kakegawa K, Irie K, Morimatsu M: 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. 1989, 63: 539-543. 10.1002/1097-0142(19890201)63:3<539::AID-CNCR2820630323>3.0.CO;2-S.CrossRefPubMed Morodomi T, Isomoto H, Shirouzu K, Kakegawa K, Irie K, Morimatsu M: 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. 1989, 63: 539-543. 10.1002/1097-0142(19890201)63:3<539::AID-CNCR2820630323>3.0.CO;2-S.CrossRefPubMed
22.
go back to reference Okuyama T, Oya M, Ishikawa H: Budding as a risk factor for lymph node metastasis in pT1 or pT2 well-differentiated colorectal adenocarcinoma. Dis Colon Rectum. 2002, 45: 628-634. 10.1007/s10350-004-6259-0.CrossRefPubMed Okuyama T, Oya M, Ishikawa H: Budding as a risk factor for lymph node metastasis in pT1 or pT2 well-differentiated colorectal adenocarcinoma. Dis Colon Rectum. 2002, 45: 628-634. 10.1007/s10350-004-6259-0.CrossRefPubMed
23.
go back to reference Okuyama T, Oya M, Ishikawa H: Budding as a useful prognostic marker in pT3 well- or moderately-differentiated rectal adenocarcinoma. J Surg Oncol. 2003, 83: 42-47. 10.1002/jso.10230.CrossRefPubMed Okuyama T, Oya M, Ishikawa H: Budding as a useful prognostic marker in pT3 well- or moderately-differentiated rectal adenocarcinoma. J Surg Oncol. 2003, 83: 42-47. 10.1002/jso.10230.CrossRefPubMed
24.
go back to reference Zolbec I, Lugli A: Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: Tumor budding as oncotarget. Oncotarget. 2010, 1: 651-661.CrossRef Zolbec I, Lugli A: Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: Tumor budding as oncotarget. Oncotarget. 2010, 1: 651-661.CrossRef
Metadata
Title
Tumor budding as a risk factor of lymph node metastasis in submucosal invasive T1 colorectal carcinoma: a retrospective study
Authors
Bong-Hyeon Kye
Ji-Han Jung
Hyung-Jin Kim
Se-Goo Kang
Hyeon-Min Cho
Jun-Gi Kim
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Surgery / Issue 1/2012
Electronic ISSN: 1471-2482
DOI
https://doi.org/10.1186/1471-2482-12-16

Other articles of this Issue 1/2012

BMC Surgery 1/2012 Go to the issue