Skip to main content
Top
Published in: Journal of Gastrointestinal Surgery 5/2012

01-05-2012 | Original Article

Meta-analysis of Histopathological Features of Primary Colorectal Cancers that Predict Lymph Node Metastases

Authors: Sean C. Glasgow, Joshua I. S. Bleier, Lawrence J. Burgart, Charles O. Finne, Ann C. Lowry

Published in: Journal of Gastrointestinal Surgery | Issue 5/2012

Login to get access

Abstract

Background

Treatment decisions for colorectal cancer vary based on lymph node status. While some histopathological features of the primary tumor correlate with lymph node spread, the relative influences of these risk factors are not well quantified.

Objective

This study aims to systematically review published studies relating histopathological features of primary colorectal cancer to the presence of lymph node metastases and to determine how reliable certain factors might be at predicting nodal metastasis when only the primary lesion is available for study.

Data Sources

Inclusive literature search using EMBASE and Ovid MEDLINE databases plus manual reference checks of all articles correlating lymphatic spread with colorectal cancer (any T stage) from 1984 to mid-2008 was performed.

Study Selection

This search generated two levels of screening utilized on 602 citations, yielding 123 articles for full review. Data reported from 76 articles were chosen.

Main Outcome Measures

The relative influence of each histopathological feature on the likelihood of lymphatic metastases was determined. Fixed-effects meta-analysis was performed, and results were reported as Mantel–Haenszel odds ratios (OR).

Results

Of 42 histopathological features analyzed, only 40.4% were reported in >2 articles. The positive predictive values for the top quartile of most frequently reported risk factors were 25.5–86.4%. Among the commonly reported histopathological findings, lymphatic invasion (OR, 8.62) significantly outperformed tumor depth (T2 vs. T1; OR, 2.62) and overall differentiation (OR, 2.38) in predicting nodal spread. For the rectal cancer subset, risk factors differed from the overall colorectal group in predictive ability; poor differentiation at the invasive front (OR, 6.08) and tumor budding (OR, 5.82) were the most predictive.

Limitations

This literature search is limited by the small number of studies examining only rectal cancers and the potential changes in histological and/or surgical techniques over the study period.

Conclusions

No single histopathological feature of colorectal cancer reliably predicted lymph node metastases. Several risk factors that correlate highly with nodal disease are not routine components of standard pathology reports. Until further research establishes histopathological or molecular patterns for predicting lymph node spread, caution should be exercised when basing treatment decisions solely on these factors.
Literature
1.
go back to reference Smith FM, Reynolds JV, Miller N, Stephens RB, Kennedy MJ. Pathological and molecular predictors of the response of rectal cancer to neoadjuvant radiochemotherapy. Eur J Surg Oncol. 2006;32:55–64.PubMed Smith FM, Reynolds JV, Miller N, Stephens RB, Kennedy MJ. Pathological and molecular predictors of the response of rectal cancer to neoadjuvant radiochemotherapy. Eur J Surg Oncol. 2006;32:55–64.PubMed
2.
go back to reference Kuremsky JG, Tepper JE, McLeod HL. Biomarkers for response to neoadjuvant chemoradiation for rectal cancer. Int J Radiat Oncol Biol Phys. 2009;74:673–88.PubMedCrossRef Kuremsky JG, Tepper JE, McLeod HL. Biomarkers for response to neoadjuvant chemoradiation for rectal cancer. Int J Radiat Oncol Biol Phys. 2009;74:673–88.PubMedCrossRef
3.
go back to reference Walther A, Johnstone E, Swanton C, Midgley R, Tomlinson I, Kerr D. Genetic prognostic and predictive markers in colorectal cancer. Nat Rev Cancer. 2009;9:489–99.PubMedCrossRef Walther A, Johnstone E, Swanton C, Midgley R, Tomlinson I, Kerr D. Genetic prognostic and predictive markers in colorectal cancer. Nat Rev Cancer. 2009;9:489–99.PubMedCrossRef
4.
go back to reference Negri FV, Campanini N, Camisa R, et al. Biological predictive factors in rectal cancer treated with preoperative radiotherapy or radiochemotherapy. Br J Cancer. 2008;98:143–7.PubMedCrossRef Negri FV, Campanini N, Camisa R, et al. Biological predictive factors in rectal cancer treated with preoperative radiotherapy or radiochemotherapy. Br J Cancer. 2008;98:143–7.PubMedCrossRef
5.
go back to reference Liersch T, Langer C, Ghadimi BM, et al. Lymph node status and TS gene expression are prognostic markers in stage II/III rectal cancer after neoadjuvant fluorouracil-based chemoradiotherapy. J Clin Oncol. 2006;24:4062–8.PubMedCrossRef Liersch T, Langer C, Ghadimi BM, et al. Lymph node status and TS gene expression are prognostic markers in stage II/III rectal cancer after neoadjuvant fluorouracil-based chemoradiotherapy. J Clin Oncol. 2006;24:4062–8.PubMedCrossRef
6.
go back to reference Smith AJ, Driman DK, Spithoff K, et al. Guideline for optimization of colorectal cancer surgery and pathology. J Surg Oncol. 2010;101:5–12.PubMedCrossRef Smith AJ, Driman DK, Spithoff K, et al. Guideline for optimization of colorectal cancer surgery and pathology. J Surg Oncol. 2010;101:5–12.PubMedCrossRef
7.
go back to reference Kim YW, Kim NK, Min BS, Lee KY, Sohn SK, Cho CH. The influence of the number of retrieved lymph nodes on staging and survival in patients with stage II and III rectal cancer undergoing tumor-specific mesorectal excision. Ann Surg. 2009;249:965–72.PubMedCrossRef Kim YW, Kim NK, Min BS, Lee KY, Sohn SK, Cho CH. The influence of the number of retrieved lymph nodes on staging and survival in patients with stage II and III rectal cancer undergoing tumor-specific mesorectal excision. Ann Surg. 2009;249:965–72.PubMedCrossRef
8.
go back to reference Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA. Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst. 2007;99:433–41.PubMedCrossRef Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA. Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst. 2007;99:433–41.PubMedCrossRef
9.
go back to reference Sakuragi M, Togashi K, Konishi F, et al. Predictive factors for lymph node metastasis in T1 stage colorectal carcinomas. Dis Colon Rectum. 2003;46:1626–32.PubMedCrossRef Sakuragi M, Togashi K, Konishi F, et al. Predictive factors for lymph node metastasis in T1 stage colorectal carcinomas. Dis Colon Rectum. 2003;46:1626–32.PubMedCrossRef
10.
go back to reference You YN, Baxter NN, Stewart A, Nelson H. Is the increasing rate of local excision for stage I rectal cancer in the United States justified?: a nationwide cohort study from the National Cancer Database. Ann Surg. 2007;245:726–33.PubMedCrossRef You YN, Baxter NN, Stewart A, Nelson H. Is the increasing rate of local excision for stage I rectal cancer in the United States justified?: a nationwide cohort study from the National Cancer Database. Ann Surg. 2007;245:726–33.PubMedCrossRef
11.
go back to reference Ricciardi R, Madoff RD, Rothenberger DA, Baxter NN. Population-based analyses of lymph node metastases in colorectal cancer. Clin Gastroenterol Hepatol. 2006;4:1522–7.PubMedCrossRef Ricciardi R, Madoff RD, Rothenberger DA, Baxter NN. Population-based analyses of lymph node metastases in colorectal cancer. Clin Gastroenterol Hepatol. 2006;4:1522–7.PubMedCrossRef
12.
go back to reference Tulchinsky H, Shmueli E, Figer A, Klausner JM, Rabau M. An interval >7 weeks between neoadjuvant therapy and surgery improves pathologic complete response and disease-free survival in patients with locally advanced rectal cancer. Ann Surg Oncol. 2008;15:2661–7.PubMedCrossRef Tulchinsky H, Shmueli E, Figer A, Klausner JM, Rabau M. An interval >7 weeks between neoadjuvant therapy and surgery improves pathologic complete response and disease-free survival in patients with locally advanced rectal cancer. Ann Surg Oncol. 2008;15:2661–7.PubMedCrossRef
13.
go back to reference Joseph NE, Sigurdson ER, Hanlon AL, et al. Accuracy of determining nodal negativity in colorectal cancer on the basis of the number of nodes retrieved on resection. Ann Surg Oncol. 2003;10:213–8.PubMedCrossRef Joseph NE, Sigurdson ER, Hanlon AL, et al. Accuracy of determining nodal negativity in colorectal cancer on the basis of the number of nodes retrieved on resection. Ann Surg Oncol. 2003;10:213–8.PubMedCrossRef
14.
go back to reference Gopaul D, Belliveau P, Vuong T, et al. Outcome of local excision of rectal carcinoma. Dis Colon Rectum. 2004;47:1780–8.PubMedCrossRef Gopaul D, Belliveau P, Vuong T, et al. Outcome of local excision of rectal carcinoma. Dis Colon Rectum. 2004;47:1780–8.PubMedCrossRef
15.
go back to reference Madbouly KM, Remzi FH, Erkek BA, et al. Recurrence after transanal excision for T1 rectal cancer: should we be concerned? Dis Colon Rectum. 2005;48:719–21.CrossRef Madbouly KM, Remzi FH, Erkek BA, et al. Recurrence after transanal excision for T1 rectal cancer: should we be concerned? Dis Colon Rectum. 2005;48:719–21.CrossRef
16.
go back to reference Mellgren A, Sirivongs P, Rothenberger DA, Madoff RD, García-Aguilar J. Is local excision adequate therapy for early rectal cancer? Dis Colon Rectum. 2000;43:1064–71; discussion 1071–4.PubMedCrossRef Mellgren A, Sirivongs P, Rothenberger DA, Madoff RD, García-Aguilar J. Is local excision adequate therapy for early rectal cancer? Dis Colon Rectum. 2000;43:1064–71; discussion 1071–4.PubMedCrossRef
17.
go back to reference Paty PB, Nash GM, Baron P, et al. Long-term results of local excision for rectal cancer. Ann Surg. 2002;236:522–30.PubMedCrossRef Paty PB, Nash GM, Baron P, et al. Long-term results of local excision for rectal cancer. Ann Surg. 2002;236:522–30.PubMedCrossRef
18.
go back to reference Endreseth BH, Myrvold HE, Romundstad P, et al. Transanal excision vs. major surgery for T1 rectal cancer. Dis Colon Rectum. 2005;48:1380–8.PubMedCrossRef Endreseth BH, Myrvold HE, Romundstad P, et al. Transanal excision vs. major surgery for T1 rectal cancer. Dis Colon Rectum. 2005;48:1380–8.PubMedCrossRef
19.
go back to reference Bentrem DJ, Okabe S, Wong WD, et al. T1 adenocarcinoma of the rectum. Transanal excision or radical surgery? Ann Surg. 2005;242:472–9.PubMed Bentrem DJ, Okabe S, Wong WD, et al. T1 adenocarcinoma of the rectum. Transanal excision or radical surgery? Ann Surg. 2005;242:472–9.PubMed
20.
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;45:200–6.PubMedCrossRef 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;45:200–6.PubMedCrossRef
21.
go back to reference Nash GM, Weiser MR, Guillem JG, et al. Long-term survival after transanal excision of T1 rectal cancer. Dis Colon Rectum. 2009;52:577–82.PubMedCrossRef Nash GM, Weiser MR, Guillem JG, et al. Long-term survival after transanal excision of T1 rectal cancer. Dis Colon Rectum. 2009;52:577–82.PubMedCrossRef
22.
go back to reference Christoforidis D, Cho HM, Dixon MR, Mellgren AF, Madoff RD, Finne CO. Transanal Endoscopic Microsurgery Versus Conventional Transanal Excision for Patients With Early Rectal Cancer. Ann Surg. 2009;249:776.PubMedCrossRef Christoforidis D, Cho HM, Dixon MR, Mellgren AF, Madoff RD, Finne CO. Transanal Endoscopic Microsurgery Versus Conventional Transanal Excision for Patients With Early Rectal Cancer. Ann Surg. 2009;249:776.PubMedCrossRef
23.
go back to reference Garcia-Aguilar J, Mellgren A, Sirivongs P, Buie D, Madoff RD, Rothenberger DA. Local excision of rectal cancer without adjuvant therapy: a word of caution. Ann Surg. 2000;231:345–51.PubMedCrossRef Garcia-Aguilar J, Mellgren A, Sirivongs P, Buie D, Madoff RD, Rothenberger DA. Local excision of rectal cancer without adjuvant therapy: a word of caution. Ann Surg. 2000;231:345–51.PubMedCrossRef
24.
go back to reference Aoki R, Tanaka S, Haruma K, et al. MUC-1 expression as a predictor of the curative endoscopic treatment of submucosally invasive colorectal carcinoma. Dis Colon Rectum. 1998;41:1262–72.PubMedCrossRef Aoki R, Tanaka S, Haruma K, et al. MUC-1 expression as a predictor of the curative endoscopic treatment of submucosally invasive colorectal carcinoma. Dis Colon Rectum. 1998;41:1262–72.PubMedCrossRef
25.
go back to reference Masaki T, Muto T. Predictive value of histology at the invasive margin in the prognosis of early invasive colorectal carcinoma. J Gastroenterol. 2000;35:195–200.PubMedCrossRef Masaki T, Muto T. Predictive value of histology at the invasive margin in the prognosis of early invasive colorectal carcinoma. J Gastroenterol. 2000;35:195–200.PubMedCrossRef
26.
go back to reference Masaki T, Matsuoka H, Sugiyama M, et al. Budding as a useful determinant of the optimal treatment for T1 rectal carcinomas. Hepatogastroenterology. 2003;50:388–91.PubMed Masaki T, Matsuoka H, Sugiyama M, et al. Budding as a useful determinant of the optimal treatment for T1 rectal carcinomas. Hepatogastroenterology. 2003;50:388–91.PubMed
27.
go back to reference Park YJ, Kim WH, Paeng SS, Park JG. Histoclinical analysis of early colorectal cancer. World J Surg. 2000;24:1029–35.PubMedCrossRef Park YJ, Kim WH, Paeng SS, Park JG. Histoclinical analysis of early colorectal cancer. World J Surg. 2000;24:1029–35.PubMedCrossRef
28.
go back to reference Ishikawa Y, Akishima-Fukasawa Y, Ito K, et al. Histopathologic determinants of regional lymph node metastasis in early colorectal cancer. Cancer. 2008;112:924–33.PubMedCrossRef Ishikawa Y, Akishima-Fukasawa Y, Ito K, et al. Histopathologic determinants of regional lymph node metastasis in early colorectal cancer. Cancer. 2008;112:924–33.PubMedCrossRef
29.
go back to reference Kurokawa S, Arimura Y, Yamamoto H, et al. Tumour matrilysin expression predicts metastatic potential of stage I (pT1) colon and rectal cancers. Gut. 2005;54:1751–8.PubMedCrossRef Kurokawa S, Arimura Y, Yamamoto H, et al. Tumour matrilysin expression predicts metastatic potential of stage I (pT1) colon and rectal cancers. Gut. 2005;54:1751–8.PubMedCrossRef
30.
go back to reference Masaki T, Goto A, Sugiyama M, et al. Possible contribution of CD44 variant 6 and nuclear beta-catenin expression to the formation of budding tumor cells in patients with T1 colorectal carcinoma. Cancer. 2001;92:2539–46.PubMedCrossRef Masaki T, Goto A, Sugiyama M, et al. Possible contribution of CD44 variant 6 and nuclear beta-catenin expression to the formation of budding tumor cells in patients with T1 colorectal carcinoma. Cancer. 2001;92:2539–46.PubMedCrossRef
31.
go back to reference Saleh HA, Jackson H, Banerjee M. Immunohistochemical expression of bcl-2 and p53 oncoproteins: correlation with Ki67 proliferation index and prognostic histopathologic parameters in colorectal neoplasia. Appl Immunohistochem Mol Morphol. 2000;8:175–82.PubMedCrossRef Saleh HA, Jackson H, Banerjee M. Immunohistochemical expression of bcl-2 and p53 oncoproteins: correlation with Ki67 proliferation index and prognostic histopathologic parameters in colorectal neoplasia. Appl Immunohistochem Mol Morphol. 2000;8:175–82.PubMedCrossRef
32.
go back to reference Guzińska-Ustymowicz K. MMP-9 and cathepsin B expression in tumor budding as an indicator of a more aggressive phenotype of colorectal cancer (CRC). Anticancer Res. 2006;26:1589–94.PubMed Guzińska-Ustymowicz K. MMP-9 and cathepsin B expression in tumor budding as an indicator of a more aggressive phenotype of colorectal cancer (CRC). Anticancer Res. 2006;26:1589–94.PubMed
33.
go back to reference Kaneko I, Tanaka S, Oka S, et al. Immunohistochemical molecular markers as predictors of curability of endoscopically resected submucosal colorectal cancer. World J Gastroenterol. 2007;13:3829–35.PubMed Kaneko I, Tanaka S, Oka S, et al. Immunohistochemical molecular markers as predictors of curability of endoscopically resected submucosal colorectal cancer. World J Gastroenterol. 2007;13:3829–35.PubMed
34.
go back to reference Oh-e H, Tanaka S, Kitadai Y, Shimamoto F, Yoshihara M, Haruma K. Cathepsin D expression as a possible predictor of lymph node metastasis in submucosal colorectal cancer. Eur J Cancer. 2001;37:180–8.PubMedCrossRef Oh-e H, Tanaka S, Kitadai Y, Shimamoto F, Yoshihara M, Haruma K. Cathepsin D expression as a possible predictor of lymph node metastasis in submucosal colorectal cancer. Eur J Cancer. 2001;37:180–8.PubMedCrossRef
35.
go back to reference Elpek GO, Gelen T, Karpuzoglu G, Karpuzoglu T, Aksoy NH, Keles N. Clinicopathologic evaluation of CDw75 antigen expression in colorectal adenocarcinomas. Pathol Oncol Res. 2002;8:175–82.PubMedCrossRef Elpek GO, Gelen T, Karpuzoglu G, Karpuzoglu T, Aksoy NH, Keles N. Clinicopathologic evaluation of CDw75 antigen expression in colorectal adenocarcinomas. Pathol Oncol Res. 2002;8:175–82.PubMedCrossRef
36.
go back to reference Sitzler PJ, Seow-Choen F, Ho YH, Leong AP. Lymph node involvement and tumor depth in rectal cancers: an analysis of 805 patients. Dis Colon Rectum. 1997;40:1472–6.PubMedCrossRef Sitzler PJ, Seow-Choen F, Ho YH, Leong AP. Lymph node involvement and tumor depth in rectal cancers: an analysis of 805 patients. Dis Colon Rectum. 1997;40:1472–6.PubMedCrossRef
37.
go back to reference Shinto E, Jass JR, Tsuda H, et al. Differential prognostic significance of morphologic invasive markers in colorectal cancer: tumor budding and cytoplasmic podia. Dis Colon Rectum. 2006;49:1422–30.PubMedCrossRef Shinto E, Jass JR, Tsuda H, et al. Differential prognostic significance of morphologic invasive markers in colorectal cancer: tumor budding and cytoplasmic podia. Dis Colon Rectum. 2006;49:1422–30.PubMedCrossRef
38.
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 specimens. 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;111:51–8.PubMed Goldstein NS, Hart J. Histologic features associated with lymph node metastasis in stage T1 and superficial T2 rectal adenocarcinomas in abdominoperineal resection specimens. 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;111:51–8.PubMed
39.
go back to reference Hase K, Shatney CH, Mochizuki H, et al. Long-term results of curative resection of “minimally invasive” colorectal cancer. Dis Colon Rectum. 1995;38:19–26.PubMedCrossRef Hase K, Shatney CH, Mochizuki H, et al. Long-term results of curative resection of “minimally invasive” colorectal cancer. Dis Colon Rectum. 1995;38:19–26.PubMedCrossRef
40.
go back to reference Kaneko I, Tanaka S, Oka S, et al. Lymphatic vessel density at the site of deepest penetration as a predictor of lymph node metastasis in submucosal colorectal cancer. Dis Colon Rectum. 2007;50:13–21.PubMedCrossRef Kaneko I, Tanaka S, Oka S, et al. Lymphatic vessel density at the site of deepest penetration as a predictor of lymph node metastasis in submucosal colorectal cancer. Dis Colon Rectum. 2007;50:13–21.PubMedCrossRef
41.
go back to reference Kojima M, Shiokawa A, Ohike N, et al. Clinical significance of nuclear morphometry at the invasive front of T1 colorectal cancer and relation to expression of VEGF-A and VEGF-C. Oncology. 2005;68:230–8.PubMedCrossRef Kojima M, Shiokawa A, Ohike N, et al. Clinical significance of nuclear morphometry at the invasive front of T1 colorectal cancer and relation to expression of VEGF-A and VEGF-C. Oncology. 2005;68:230–8.PubMedCrossRef
42.
go back to reference Masaki T, Matsuoka H, Sugiyama M, Abe N, Sakamoto A, Atomi Y. Actual number of tumor budding as a new tool for the individualization of treatment of T1 colorectal carcinomas. J Gastroenterol Hepatol. 2006;21:1115–21.PubMedCrossRef Masaki T, Matsuoka H, Sugiyama M, Abe N, Sakamoto A, Atomi Y. Actual number of tumor budding as a new tool for the individualization of treatment of T1 colorectal carcinomas. J Gastroenterol Hepatol. 2006;21:1115–21.PubMedCrossRef
43.
go back to reference Okuyama T, Oya M, Yamaguchi M. Budding (sprouting) as a useful prognostic marker in colorectal mucinous carcinoma. Jpn J Clin Oncol. 2002;32:412–6.PubMedCrossRef Okuyama T, Oya M, Yamaguchi M. Budding (sprouting) as a useful prognostic marker in colorectal mucinous carcinoma. Jpn J Clin Oncol. 2002;32:412–6.PubMedCrossRef
44.
go back to reference Sohn DK, Chang HJ, Park JW, et al. Histopathological risk factors for lymph node metastasis in submucosal invasive colorectal carcinoma of pedunculated or semipedunculated type. J Clin Pathol. 2007;60:912–5.PubMedCrossRef Sohn DK, Chang HJ, Park JW, et al. Histopathological risk factors for lymph node metastasis in submucosal invasive colorectal carcinoma of pedunculated or semipedunculated type. J Clin Pathol. 2007;60:912–5.PubMedCrossRef
45.
go back to reference Ueno H, Mochizuki H, Shinto E, Hashiguchi Y, Hase K, Talbot IC. Histologic indices in biopsy specimens for estimating the probability of extended local spread in patients with rectal carcinoma. Cancer. 2002;94:2882–91.PubMedCrossRef Ueno H, Mochizuki H, Shinto E, Hashiguchi Y, Hase K, Talbot IC. Histologic indices in biopsy specimens for estimating the probability of extended local spread in patients with rectal carcinoma. Cancer. 2002;94:2882–91.PubMedCrossRef
46.
go back to reference Ueno H, Mochizuki H, Hashiguchi Y, et al. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology. 2004;127:385–94.PubMedCrossRef Ueno H, Mochizuki H, Hashiguchi Y, et al. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology. 2004;127:385–94.PubMedCrossRef
47.
go back to reference Brodsky JT, Richard GK, Cohen AM, Minsky BD. Variables correlated with the risk of lymph node metastasis in early rectal cancer. Cancer. 1992;69:322–6.PubMedCrossRef Brodsky JT, Richard GK, Cohen AM, Minsky BD. Variables correlated with the risk of lymph node metastasis in early rectal cancer. Cancer. 1992;69:322–6.PubMedCrossRef
48.
go back to reference Huddy SP, Husband EM, Cook MG, Gibbs NM, Marks CG, Heald RJ. Lymph node metastases in early rectal cancer. Br J Surg. 1993;80:1457–8.PubMedCrossRef Huddy SP, Husband EM, Cook MG, Gibbs NM, Marks CG, Heald RJ. Lymph node metastases in early rectal cancer. Br J Surg. 1993;80:1457–8.PubMedCrossRef
49.
go back to reference Kikuchi R, Takano M, Takagi K, et al. Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum. 1995;38:1286–95.PubMedCrossRef Kikuchi R, Takano M, Takagi K, et al. Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum. 1995;38:1286–95.PubMedCrossRef
50.
go back to reference Minsky BD, Rich T, Recht A, Harvey W, Mies C. Selection criteria for local excision with or without adjuvant radiation therapy for rectal cancer. Cancer. 1989;63:1421–9.PubMedCrossRef Minsky BD, Rich T, Recht A, Harvey W, Mies C. Selection criteria for local excision with or without adjuvant radiation therapy for rectal cancer. Cancer. 1989;63:1421–9.PubMedCrossRef
51.
go back to reference Nelson JC, Nimr AN, Thomford NR. Criteria for the selection of ‘early’ carcinomas of the rectum. Are they valid? Arch Surg. 1987;122:533–6.PubMedCrossRef Nelson JC, Nimr AN, Thomford NR. Criteria for the selection of ‘early’ carcinomas of the rectum. Are they valid? Arch Surg. 1987;122:533–6.PubMedCrossRef
52.
go back to reference Tanaka S, Yokota T, Saito D, Okamoto S, Oguro Y, Yoshida S. Clinicopathologic features of early rectal carcinoma and indications for endoscopic treatment. Dis Colon Rectum. 1995;38:959–63.PubMedCrossRef Tanaka S, Yokota T, Saito D, Okamoto S, Oguro Y, Yoshida S. Clinicopathologic features of early rectal carcinoma and indications for endoscopic treatment. Dis Colon Rectum. 1995;38:959–63.PubMedCrossRef
53.
go back to reference Arai T, Akiyama Y, Yamamura A, et al. Allelotype analysis of early colorectal cancers with lymph node metastasis. Int J Cancer. 1998;79:418–23.PubMedCrossRef Arai T, Akiyama Y, Yamamura A, et al. Allelotype analysis of early colorectal cancers with lymph node metastasis. Int J Cancer. 1998;79:418–23.PubMedCrossRef
54.
go back to reference Blumberg D, Paty PB, Guillem JG, et al. All patients with small intramural rectal cancers are at risk for lymph node metastasis. Dis Colon Rectum. 1999;42:881–5.PubMedCrossRef Blumberg D, Paty PB, Guillem JG, et al. All patients with small intramural rectal cancers are at risk for lymph node metastasis. Dis Colon Rectum. 1999;42:881–5.PubMedCrossRef
55.
go back to reference Masaki T, Sugiyama M, Atomi Y, et al. The indication of local excision for T2 rectal carcinomas. Am J Surg. 2001;181:133–7.PubMedCrossRef Masaki T, Sugiyama M, Atomi Y, et al. The indication of local excision for T2 rectal carcinomas. Am J Surg. 2001;181:133–7.PubMedCrossRef
56.
go back to reference Fang WL, Chang SC, Lin JK, et al. Metastatic potential in T1 and T2 colorectal cancer. Hepatogastroenterology. 2005;52:1688–91.PubMed Fang WL, Chang SC, Lin JK, et al. Metastatic potential in T1 and T2 colorectal cancer. Hepatogastroenterology. 2005;52:1688–91.PubMed
57.
go back to reference Maeda K, Yashiro M, Nishihara T, et al. Correlation between vascular endothelial growth factor C expression and lymph node metastasis in T1 carcinoma of the colon and rectum. Surg Today. 2003;33:736–9.PubMedCrossRef Maeda K, Yashiro M, Nishihara T, et al. Correlation between vascular endothelial growth factor C expression and lymph node metastasis in T1 carcinoma of the colon and rectum. Surg Today. 2003;33:736–9.PubMedCrossRef
58.
go back to reference Okabe S, Shia J, Nash G, et al. Lymph node metastasis in T1 adenocarcinoma of the colon and rectum. J Gastrointest Surg. 2004;8:1032–9; discussion 1039–40.PubMedCrossRef Okabe S, Shia J, Nash G, et al. Lymph node metastasis in T1 adenocarcinoma of the colon and rectum. J Gastrointest Surg. 2004;8:1032–9; discussion 1039–40.PubMedCrossRef
59.
go back to reference Shimomura T, Ishiguro S, Konishi H, et al. New indication for endoscopic treatment of colorectal carcinoma with submucosal invasion. J Gastroenterol Hepatol. 2004;19:48–55.PubMedCrossRef Shimomura T, Ishiguro S, Konishi H, et al. New indication for endoscopic treatment of colorectal carcinoma with submucosal invasion. J Gastroenterol Hepatol. 2004;19:48–55.PubMedCrossRef
60.
go back to reference Suzuki T, Sadahiro S, Mukoyama S, et al. Risk of lymph node and distant metastases in patients with early invasive colorectal cancer classified as Haggitt’s level 4 invasion: image analysis of submucosal layer invasion. Dis Colon Rectum. 2003;46:203–8.PubMedCrossRef Suzuki T, Sadahiro S, Mukoyama S, et al. Risk of lymph node and distant metastases in patients with early invasive colorectal cancer classified as Haggitt’s level 4 invasion: image analysis of submucosal layer invasion. Dis Colon Rectum. 2003;46:203–8.PubMedCrossRef
61.
go back to reference Yamamoto S, Watanabe M, Hasegawa H, et al. The risk of lymph node metastasis in T1 colorectal carcinoma. Hepatogastroenterology. 2004;51:998–1000.PubMed Yamamoto S, Watanabe M, Hasegawa H, et al. The risk of lymph node metastasis in T1 colorectal carcinoma. Hepatogastroenterology. 2004;51:998–1000.PubMed
62.
go back to reference Abe A, Fukui H, Fujii S, et al. Involvement of cyclooxygenase-2 and vascular endothelial growth factor in vascularization and lymph node metastasis of colorectal cancers with submucosal invasion. J Gastroenterol Hepatol. 2007;22:1071–7.PubMedCrossRef Abe A, Fukui H, Fujii S, et al. Involvement of cyclooxygenase-2 and vascular endothelial growth factor in vascularization and lymph node metastasis of colorectal cancers with submucosal invasion. J Gastroenterol Hepatol. 2007;22:1071–7.PubMedCrossRef
63.
go back to reference Chok KS, Law WL. Prognostic factors affecting survival and recurrence of patients with pT1 and pT2 colorectal cancer. World J Surg. 2007;31:1485–90.PubMedCrossRef Chok KS, Law WL. Prognostic factors affecting survival and recurrence of patients with pT1 and pT2 colorectal cancer. World J Surg. 2007;31:1485–90.PubMedCrossRef
64.
go back to reference Masaki T, Matsuoka H, Sugiyama M, et al. Tumor budding and evidence-based treatment of T2 rectal carcinomas. J Surg Oncol. 2005;92:59–63.PubMedCrossRef Masaki T, Matsuoka H, Sugiyama M, et al. Tumor budding and evidence-based treatment of T2 rectal carcinomas. J Surg Oncol. 2005;92:59–63.PubMedCrossRef
65.
go back to reference Rasheed S, Bowley DM, Aziz O, et al. Can depth of tumour invasion predict lymph node positivity in patients undergoing resection for early rectal cancer? A comparative study between T1 and T2 cancers. Colorectal Dis. 2008;10:231–8.PubMedCrossRef Rasheed S, Bowley DM, Aziz O, et al. Can depth of tumour invasion predict lymph node positivity in patients undergoing resection for early rectal cancer? A comparative study between T1 and T2 cancers. Colorectal Dis. 2008;10:231–8.PubMedCrossRef
66.
go back to reference Wang HS, Liang WY, Lin TC, et al. Curative resection of T1 colorectal carcinoma: risk of lymph node metastasis and long-term prognosis. Dis Colon Rectum. 2005;48:1182–92.PubMedCrossRef Wang HS, Liang WY, Lin TC, et al. Curative resection of T1 colorectal carcinoma: risk of lymph node metastasis and long-term prognosis. Dis Colon Rectum. 2005;48:1182–92.PubMedCrossRef
67.
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;50:1370–6.PubMedCrossRef 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;50:1370–6.PubMedCrossRef
68.
go back to reference Garinis GA, Manolis EN, Spanakis NE, Patrinos GP, Peros G, Menounos PG. High frequency of concomitant nm23-H1 and E-cadherin transcriptional inactivation in primary non-inheriting colorectal carcinomas. J Mol Med. 2003;81:256–63.PubMed Garinis GA, Manolis EN, Spanakis NE, Patrinos GP, Peros G, Menounos PG. High frequency of concomitant nm23-H1 and E-cadherin transcriptional inactivation in primary non-inheriting colorectal carcinomas. J Mol Med. 2003;81:256–63.PubMed
69.
go back to reference Guzińska-Ustymowicz K, Chetnik A, Kemona A. Effects of changes at the site of E-cadherin expression as an indicator of colon cancer aggressiveness. Rocz Akad Med Bialymst. 2004;49 Suppl 1:70–2.PubMed Guzińska-Ustymowicz K, Chetnik A, Kemona A. Effects of changes at the site of E-cadherin expression as an indicator of colon cancer aggressiveness. Rocz Akad Med Bialymst. 2004;49 Suppl 1:70–2.PubMed
70.
go back to reference Pan W, Terai T, Abe S, et al. Location of early colorectal cancers at fold-top may reduce the risk of lymph node metastasis. Dis Colon Rectum. 2006;49:579–87.PubMedCrossRef Pan W, Terai T, Abe S, et al. Location of early colorectal cancers at fold-top may reduce the risk of lymph node metastasis. Dis Colon Rectum. 2006;49:579–87.PubMedCrossRef
71.
go back to reference Sakashita M, Aoyama N, Minami R, et al. Glut1 expression in T1 and T2 stage colorectal carcinomas: its relationship to clinicopathological features. Eur J Cancer. 2001;37:204–9.PubMedCrossRef Sakashita M, Aoyama N, Minami R, et al. Glut1 expression in T1 and T2 stage colorectal carcinomas: its relationship to clinicopathological features. Eur J Cancer. 2001;37:204–9.PubMedCrossRef
72.
go back to reference Lenander C, Habermann JK, Ost A, et al. Laminin-5 gamma 2 chain expression correlates with unfavorable prognosis in colon carcinomas. Anal Cell Pathol. 2001;22:201–9.PubMed Lenander C, Habermann JK, Ost A, et al. Laminin-5 gamma 2 chain expression correlates with unfavorable prognosis in colon carcinomas. Anal Cell Pathol. 2001;22:201–9.PubMed
73.
go back to reference Kubo H, Miki C, Kusunoki M. Evaluation of genetic mutations of tumor suppresser genes in colorectal cancer patients. Hepatogastroenterology. 2004;51:114–7.PubMed Kubo H, Miki C, Kusunoki M. Evaluation of genetic mutations of tumor suppresser genes in colorectal cancer patients. Hepatogastroenterology. 2004;51:114–7.PubMed
74.
go back to reference Kazama S, Watanabe T, Ajioka Y, Kanazawa T, Nagawa H. Tumour budding at the deepest invasive margin correlates with lymph node metastasis in submucosal colorectal cancer detected by anticytokeratin antibody CAM5.2. Br J Cancer. 2006;94:293-8.PubMedCrossRef Kazama S, Watanabe T, Ajioka Y, Kanazawa T, Nagawa H. Tumour budding at the deepest invasive margin correlates with lymph node metastasis in submucosal colorectal cancer detected by anticytokeratin antibody CAM5.2. Br J Cancer. 2006;94:293-8.PubMedCrossRef
75.
go back to reference Ishikawa F, Saito N, Koda K, et al. Nuclear morphometric analysis of T2 lesions of the rectum—a simple, reproducible method for predicting malignancy potential. Am J Surg. 2002;183:686–91.PubMedCrossRef Ishikawa F, Saito N, Koda K, et al. Nuclear morphometric analysis of T2 lesions of the rectum—a simple, reproducible method for predicting malignancy potential. Am J Surg. 2002;183:686–91.PubMedCrossRef
76.
go back to reference Makino M, Yamane N, Taniguchi T, Honboh T, Kurayoshi K, Kaibara N. p53 as an indicator of lymph node metastases in invasive early colorectal cancer. Anticancer Res. 2000;20:2055–9.PubMed Makino M, Yamane N, Taniguchi T, Honboh T, Kurayoshi K, Kaibara N. p53 as an indicator of lymph node metastases in invasive early colorectal cancer. Anticancer Res. 2000;20:2055–9.PubMed
77.
go back to reference Sory A, Minamoto T, Ohta T, et al. Does p53 overexpression cause metastases in early invasive colorectal adenocarcinoma? Eur J Surg. 1997;163:685–92.PubMed Sory A, Minamoto T, Ohta T, et al. Does p53 overexpression cause metastases in early invasive colorectal adenocarcinoma? Eur J Surg. 1997;163:685–92.PubMed
78.
go back to reference Starzynska T, Bromley M, Ghosh A, Stern PL. Prognostic significance of p53 overexpression in gastric and colorectal carcinoma. Br J Cancer. 1992;66:558–62.PubMedCrossRef Starzynska T, Bromley M, Ghosh A, Stern PL. Prognostic significance of p53 overexpression in gastric and colorectal carcinoma. Br J Cancer. 1992;66:558–62.PubMedCrossRef
79.
go back to reference Kasakura Y, Fujii M, Mochizuki F, Kobayashi M, Yamagata M. Clinicopathological analyses of advanced colorectal cancers of different sizes—especially those of 20 mm or less in diameter. Hepatogastroenterology. 2001;48:696–701.PubMed Kasakura Y, Fujii M, Mochizuki F, Kobayashi M, Yamagata M. Clinicopathological analyses of advanced colorectal cancers of different sizes—especially those of 20 mm or less in diameter. Hepatogastroenterology. 2001;48:696–701.PubMed
80.
go back to reference Fujiya M, Watari J, Ashida T, et al. Reduced expression of syndecan-1 affects metastatic potential and clinical outcome in patients with colorectal cancer. Jpn J Cancer Res. 2001;92:1074–81.PubMedCrossRef Fujiya M, Watari J, Ashida T, et al. Reduced expression of syndecan-1 affects metastatic potential and clinical outcome in patients with colorectal cancer. Jpn J Cancer Res. 2001;92:1074–81.PubMedCrossRef
81.
go back to reference Guzinska-Ustymowicz K, Kemona A. Transforming growth factor beta can be a parameter of aggressiveness of pT1 colorectal cancer. World J Gastroenterol. 2005;11:1193–5.PubMed Guzinska-Ustymowicz K, Kemona A. Transforming growth factor beta can be a parameter of aggressiveness of pT1 colorectal cancer. World J Gastroenterol. 2005;11:1193–5.PubMed
82.
go back to reference Xiong B, Gong LL, Zhang F, Hu MB, Yuan HY. TGF beta1 expression and angiogenesis in colorectal cancer tissue. World J Gastroenterol. 2002;8:496–8.PubMed Xiong B, Gong LL, Zhang F, Hu MB, Yuan HY. TGF beta1 expression and angiogenesis in colorectal cancer tissue. World J Gastroenterol. 2002;8:496–8.PubMed
83.
go back to reference Famulski W, Guzińska-Ustymowicz K, Sulkowska M, et al. Tumour budding intensity in relation to cathepsin D expression and some clinicopathological features of colorectal cancer. Folia Histochem Cytobiol. 2001;39 Suppl 2:171–2.PubMed Famulski W, Guzińska-Ustymowicz K, Sulkowska M, et al. Tumour budding intensity in relation to cathepsin D expression and some clinicopathological features of colorectal cancer. Folia Histochem Cytobiol. 2001;39 Suppl 2:171–2.PubMed
84.
go back to reference Hase K, Shatney C, Johnson D, Trollope M, Vierra M. Prognostic value of tumor “budding” in patients with colorectal cancer. Dis Colon Rectum. 1993;36:627–35.PubMedCrossRef Hase K, Shatney C, Johnson D, Trollope M, Vierra M. Prognostic value of tumor “budding” in patients with colorectal cancer. Dis Colon Rectum. 1993;36:627–35.PubMedCrossRef
85.
go back to reference Okuyama T, Nakamura T, Yamaguchi M. Budding is useful to select high-risk patients in stage II well-differentiated or moderately differentiated colon adenocarcinoma. Dis Colon Rectum. 2003;46:1400–6.PubMedCrossRef Okuyama T, Nakamura T, Yamaguchi M. Budding is useful to select high-risk patients in stage II well-differentiated or moderately differentiated colon adenocarcinoma. Dis Colon Rectum. 2003;46:1400–6.PubMedCrossRef
86.
go back to reference Guzińska-Ustymowicz K. The role of tumour budding at the front of invasion and recurrence of rectal carcinoma. Anticancer Res. 2005;25:1269–72.PubMed Guzińska-Ustymowicz K. The role of tumour budding at the front of invasion and recurrence of rectal carcinoma. Anticancer Res. 2005;25:1269–72.PubMed
87.
go back to reference Hörkkö TT, Klintrup K, Mäkinen JM, et al. Budding invasive margin and prognosis in colorectal cancer—no direct association with beta-catenin expression. Eur J Cancer. 2006;42:964–71.PubMedCrossRef Hörkkö TT, Klintrup K, Mäkinen JM, et al. Budding invasive margin and prognosis in colorectal cancer—no direct association with beta-catenin expression. Eur J Cancer. 2006;42:964–71.PubMedCrossRef
88.
go back to reference Choi HJ, Park KJ, Shin JS, Roh MS, Kwon HC, Lee HS. Tumor budding as a prognostic marker in stage-III rectal carcinoma. Int J Colorectal Dis. 2007;22:863–8.PubMedCrossRef Choi HJ, Park KJ, Shin JS, Roh MS, Kwon HC, Lee HS. Tumor budding as a prognostic marker in stage-III rectal carcinoma. Int J Colorectal Dis. 2007;22:863–8.PubMedCrossRef
89.
go back to reference Kanazawa H, Mitomi H, Nishiyama Y, et al. Tumour budding at invasive margins and outcome in colorectal cancer. Colorectal Dis. 2008;10:41–7.PubMed Kanazawa H, Mitomi H, Nishiyama Y, et al. Tumour budding at invasive margins and outcome in colorectal cancer. Colorectal Dis. 2008;10:41–7.PubMed
90.
go back to reference Fried GM, Hreno A, Duguid WP, Hampson LG. Rational management of malignant colon polyps based on long-term follow-up. Surgery. 1984;96:815–22.PubMed Fried GM, Hreno A, Duguid WP, Hampson LG. Rational management of malignant colon polyps based on long-term follow-up. Surgery. 1984;96:815–22.PubMed
Metadata
Title
Meta-analysis of Histopathological Features of Primary Colorectal Cancers that Predict Lymph Node Metastases
Authors
Sean C. Glasgow
Joshua I. S. Bleier
Lawrence J. Burgart
Charles O. Finne
Ann C. Lowry
Publication date
01-05-2012
Publisher
Springer-Verlag
Published in
Journal of Gastrointestinal Surgery / Issue 5/2012
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI
https://doi.org/10.1007/s11605-012-1827-4

Other articles of this Issue 5/2012

Journal of Gastrointestinal Surgery 5/2012 Go to the issue