Skip to main content
Erschienen in: Journal of Gastroenterology 9/2014

01.09.2014 | Original Article—Alimentary Tract

Novel risk factors for lymph node metastasis in early invasive colorectal cancer: a multi-institution pathology review

verfasst von: Hideki Ueno, Kazuo Hase, Yojiro Hashiguchi, Hideyuki Shimazaki, Shinji Yoshii, Shin-ei Kudo, Masafumi Tanaka, Yoshito Akagi, Takeshi Suto, Shinji Nagata, Keiji Matsuda, Koji Komori, Kazuhiko Yoshimatsu, Yasuhiko Tomita, Shozo Yokoyama, Eiji Shinto, Takahiro Nakamura, Kenichi Sugihara

Erschienen in: Journal of Gastroenterology | Ausgabe 9/2014

Einloggen, um Zugang zu erhalten

Abstract

Background

Novel risk factors for lymph node metastasis (LNM) in T1 colorectal cancer (CRC) have been recently proposed, but most have not been implemented because of the lack of validation. Here we determined the value of poorly differentiated clusters (PDCs) in a multi-institutional cohort of T1 CRC cases.

Methods

A pathology review involving 30 institutions was conducted for 3556 T1 CRCs. PDC was defined as malignant clusters comprising ≥5 cells and lacking a glandular formation. The ability to identify LNM risk was compared using Akaike’s information criterion (AIC).

Results

PDC was observed in 1401 tumors (39.4 %), including 94 (17.8 %) with <1000 µm submucosal invasion and 1307 (43.2 %) with ≥1000 µm submucosal invasion (P < 0.0001). The incidence of LNM was higher in PDC-positive tumors (17.4 %) than in PDC-negative tumors (6.9 %; P < 0.0001), and PDCs had an adverse impact on LNM irrespective of the degree of submucosal invasion. Grade 3, vascular invasion, budding, and submucosal invasion depth were also significant factors (all, P < 0.0001). AIC of risk factor to identify LNM risk was most favorable for vascular invasion (2273.4), followed by PDC (2357.4); submucosal invasion depth (2429.1) was the most unfavorable. Interinstitutional judgment disparities were smaller in PDC (kappa, 0.51) than vascular invasion (0.33) or tumor grade (0.48).

Conclusions

PDC is a promising new parameter with good ability to identify LNM risk. Use of its appropriate judgment criteria will enable us determine whether an observational policy can be safely applied following local tumor excision in T1 CRC cases.
Literatur
1.
Zurück zum Zitat Repici A, Hassan C, Pessoa DDP, Pagano N, Arezzo A, Zullo A, et al. Efficacy and safety of endoscopic submucosal dissection for colorectal neoplasia: a systematic review. Endoscopy. 2012;44:137–47.PubMedCrossRef Repici A, Hassan C, Pessoa DDP, Pagano N, Arezzo A, Zullo A, et al. Efficacy and safety of endoscopic submucosal dissection for colorectal neoplasia: a systematic review. Endoscopy. 2012;44:137–47.PubMedCrossRef
2.
Zurück zum Zitat Kiriyama S, Saito Y, Yamamoto S, Soetikno R, Matsuda T, Nakajima T, et al. Comparison of endoscopic submucosal dissection with laparoscopic-assisted colorectal surgery for early-stage colorectal cancer: a retrospective analysis. Endoscopy. 2012;44:1024–30.PubMedCrossRef Kiriyama S, Saito Y, Yamamoto S, Soetikno R, Matsuda T, Nakajima T, et al. Comparison of endoscopic submucosal dissection with laparoscopic-assisted colorectal surgery for early-stage colorectal cancer: a retrospective analysis. Endoscopy. 2012;44:1024–30.PubMedCrossRef
3.
Zurück zum Zitat Lee EJ, Lee JB, Lee SH, Kim DS, Lee DH, Lee DS, et al. Endoscopic submucosal dissection for colorectal tumors-1000 colorectal ESD cases: one specialized institute’s experiences. Surg Endosc 2012 (Epub ahead of print). Lee EJ, Lee JB, Lee SH, Kim DS, Lee DH, Lee DS, et al. Endoscopic submucosal dissection for colorectal tumors-1000 colorectal ESD cases: one specialized institute’s experiences. Surg Endosc 2012 (Epub ahead of print).
4.
Zurück zum Zitat Cooper HS. Surgical pathology of endoscopically removed malignant polyps of the colon and rectum. Am J Surg Pathol. 1983;7:613–23.PubMedCrossRef Cooper HS. Surgical pathology of endoscopically removed malignant polyps of the colon and rectum. Am J Surg Pathol. 1983;7:613–23.PubMedCrossRef
5.
Zurück zum Zitat Morson BC, Whiteway JE, Jones EA, Macrae FA, Williams CB. Histopathology and prognosis of malignant colorectal polyps treated by endoscopic polypectomy. Gut. 1984;25:437–44.PubMedCentralPubMedCrossRef Morson BC, Whiteway JE, Jones EA, Macrae FA, Williams CB. Histopathology and prognosis of malignant colorectal polyps treated by endoscopic polypectomy. Gut. 1984;25:437–44.PubMedCentralPubMedCrossRef
6.
Zurück zum Zitat Colacchio TA, Forde KA, Scantlebury VP. Endoscopic polypectomy: inadequate treatment for invasive colorectal carcinoma. Ann Surg. 1981;194:704–7.PubMedCentralPubMedCrossRef Colacchio TA, Forde KA, Scantlebury VP. Endoscopic polypectomy: inadequate treatment for invasive colorectal carcinoma. Ann Surg. 1981;194:704–7.PubMedCentralPubMedCrossRef
7.
Zurück zum Zitat Sugihara K, Muto T, Morioka Y. Management of patients with invasive carcinoma removed by colonoscopic polypectomy. Dis Colon Rectum. 1989;32:829–34.PubMedCrossRef Sugihara K, Muto T, Morioka Y. Management of patients with invasive carcinoma removed by colonoscopic polypectomy. Dis Colon Rectum. 1989;32:829–34.PubMedCrossRef
8.
Zurück zum Zitat Cranley JP, Petras RE, Carey WD, Paradis K, Sivak MV. When is endoscopic polypectomy adequate therapy for colonic polyps containing invasive carcinoma? Gastroenterology. 1986;91:419–27.PubMed Cranley JP, Petras RE, Carey WD, Paradis K, Sivak MV. When is endoscopic polypectomy adequate therapy for colonic polyps containing invasive carcinoma? Gastroenterology. 1986;91:419–27.PubMed
9.
Zurück zum Zitat Coverlizza S, Risio M, Ferrari A, Fenoglio-Preiser CM, Rossini FP. Colorectal adenomas containing invasive carcinoma: pathologic assessment of lymph node metastatic potential. Cancer. 1989;64:1937–47.PubMedCrossRef Coverlizza S, Risio M, Ferrari A, Fenoglio-Preiser CM, Rossini FP. Colorectal adenomas containing invasive carcinoma: pathologic assessment of lymph node metastatic potential. Cancer. 1989;64:1937–47.PubMedCrossRef
10.
Zurück zum Zitat Muller S, Chesner IM, Egan MJ, Rowlands DC, Collard MJ, Swarbrick ET, et al. Significance of venous and lymphatic invasion in malignant polyps of the colon and rectum. Gut. 1989;30:1385–91.PubMedCentralPubMedCrossRef Muller S, Chesner IM, Egan MJ, Rowlands DC, Collard MJ, Swarbrick ET, et al. Significance of venous and lymphatic invasion in malignant polyps of the colon and rectum. Gut. 1989;30:1385–91.PubMedCentralPubMedCrossRef
12.
13.
Zurück zum Zitat Suh JH, Han KS, Kim BC, Hong CW, Sohn DK, Chang HJ, et al. Predictors for lymph node metastasis in T1 colorectal cancer. Endoscopy. 2012;44:590–5.PubMedCrossRef Suh JH, Han KS, Kim BC, Hong CW, Sohn DK, Chang HJ, et al. Predictors for lymph node metastasis in T1 colorectal cancer. Endoscopy. 2012;44:590–5.PubMedCrossRef
14.
Zurück zum Zitat Hassan C, Zullo A, Risio M, Rossini FP, Morini S. Histologic risk factors and clinical outcome in colorectal malignant polyp: a pooled-data analysis. Dis Colon Rectum. 2005;48:1588–96.PubMedCrossRef Hassan C, Zullo A, Risio M, Rossini FP, Morini S. Histologic risk factors and clinical outcome in colorectal malignant polyp: a pooled-data analysis. Dis Colon Rectum. 2005;48:1588–96.PubMedCrossRef
15.
Zurück zum Zitat Volk EE, Goldblum JR, Petras RE, Carey WD, Fazio VW. Management and outcome of patients with invasive carcinoma arising in colorectal polyps. Gastroenterology. 1995;109:1801–7.PubMedCrossRef Volk EE, Goldblum JR, Petras RE, Carey WD, Fazio VW. Management and outcome of patients with invasive carcinoma arising in colorectal polyps. Gastroenterology. 1995;109:1801–7.PubMedCrossRef
16.
Zurück zum Zitat Fielding LP, Phillips RKS, Hittinger R. Factors influencing mortality after curative resection for large bowel cancer in elderly patients. Lancet. 1989;18:595–7.CrossRef Fielding LP, Phillips RKS, Hittinger R. Factors influencing mortality after curative resection for large bowel cancer in elderly patients. Lancet. 1989;18:595–7.CrossRef
17.
Zurück zum Zitat Boenicke L, Fein M, Sailer M, Isbert C, Germer C-T, Thalheimer A. The concurrence of histologically positive resection margins and sessile morphology is an important risk factor for lymph node metastasis after complete endoscopic removal of malignant colorectal polyps. Int J Colorectal Dis. 2010;25:433–8.PubMedCrossRef Boenicke L, Fein M, Sailer M, Isbert C, Germer C-T, Thalheimer A. The concurrence of histologically positive resection margins and sessile morphology is an important risk factor for lymph node metastasis after complete endoscopic removal of malignant colorectal polyps. Int J Colorectal Dis. 2010;25:433–8.PubMedCrossRef
18.
Zurück zum Zitat Benizri EI, Bereder J-M, Rahili A, Bernard J-L, Vanbiervliet G, Filippi J, et al. Additional colectomy after colonoscopic polypectomy for T1 colon cancer: a fine balance between oncologic benefit and operative risk. Int J Colorectal Dis. 2012;27:1473–8.PubMedCrossRef Benizri EI, Bereder J-M, Rahili A, Bernard J-L, Vanbiervliet G, Filippi J, et al. Additional colectomy after colonoscopic polypectomy for T1 colon cancer: a fine balance between oncologic benefit and operative risk. Int J Colorectal Dis. 2012;27:1473–8.PubMedCrossRef
19.
Zurück zum Zitat Schmoll HJ, Van Cutsem V, Stein A, Valentini V, Glimelius B, Haustermans K, et al. ESMO consensus guidelines for management of patients with colon and rectal cancer. A personalized approach to clinical decision making. Ann Oncol. 2012;23:2479–516.PubMedCrossRef Schmoll HJ, Van Cutsem V, Stein A, Valentini V, Glimelius B, Haustermans K, et al. ESMO consensus guidelines for management of patients with colon and rectal cancer. A personalized approach to clinical decision making. Ann Oncol. 2012;23:2479–516.PubMedCrossRef
20.
Zurück zum Zitat Watanabe T, Itabashi M, Shimada Y, Tanaka S, Ito Y, Ajioka Y, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. Int J Clin Oncol. 2009;17:1–29.CrossRef Watanabe T, Itabashi M, Shimada Y, Tanaka S, Ito Y, Ajioka Y, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. Int J Clin Oncol. 2009;17:1–29.CrossRef
21.
Zurück zum Zitat Ueno H, Hashiguchi Y, Kajiwara Y, Shinto E, Shimazaki H, Kurihara H, et al. Proposed objective criteria for “grade 3” in early invasive colorectal cancer. Am J Clin Pathol. 2010;134:312–22.PubMedCrossRef Ueno H, Hashiguchi Y, Kajiwara Y, Shinto E, Shimazaki H, Kurihara H, et al. Proposed objective criteria for “grade 3” in early invasive colorectal cancer. Am J Clin Pathol. 2010;134:312–22.PubMedCrossRef
22.
Zurück zum Zitat Barresi V, Bonetti LR, Branca G, Gregorio CD, de Leon MP, Tuccari G. Colorectal carcinoma grading by quantifying poorly differentiated cell clusters is more reproducible and provides more robust prognostic information than conventional grading. Virchows Arch. 2012;461:621–8.PubMedCrossRef Barresi V, Bonetti LR, Branca G, Gregorio CD, de Leon MP, Tuccari G. Colorectal carcinoma grading by quantifying poorly differentiated cell clusters is more reproducible and provides more robust prognostic information than conventional grading. Virchows Arch. 2012;461:621–8.PubMedCrossRef
23.
Zurück zum Zitat Ueno H, Shimazaki H, Shinto E, Hashiguchi Y, Nakanishi K, Maekawa K, et al. New criteria for histologic grading of colorectal cancer. Am J Surg Pathol. 2012;36:193–201.PubMedCrossRef Ueno H, Shimazaki H, Shinto E, Hashiguchi Y, Nakanishi K, Maekawa K, et al. New criteria for histologic grading of colorectal cancer. Am J Surg Pathol. 2012;36:193–201.PubMedCrossRef
24.
Zurück zum Zitat Haggitt RC, Glotzbach RE, Soffer EE, Wruble LD. Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology. 1985;89:328–36.PubMed Haggitt RC, Glotzbach RE, Soffer EE, Wruble LD. Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology. 1985;89:328–36.PubMed
25.
Zurück zum Zitat Ueno H, Mochizuki H, Hashiguchi Y, Shimazaki H, Aida S, Hase K, 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, Shimazaki H, Aida S, Hase K, et al. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology. 2004;127:385–94.PubMedCrossRef
26.
Zurück zum Zitat Akaike H. Information theory and an extension of the maximum likelihood principle. Budapest: Akademia Kiado; 1973. Akaike H. Information theory and an extension of the maximum likelihood principle. Budapest: Akademia Kiado; 1973.
27.
Zurück zum Zitat R Development Core Team. A language and environment for statistical computing. R. Foundation for Statistical Computing; 2006. R Development Core Team. A language and environment for statistical computing. R. Foundation for Statistical Computing; 2006.
28.
Zurück zum Zitat Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy. 1993;25:455–61.PubMedCrossRef Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy. 1993;25:455–61.PubMedCrossRef
29.
Zurück zum Zitat Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R, Fujiyoshi T, 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, Fujimoto N, Nozaki R, Fujiyoshi T, et al. Management of early invasive colorectal cancer-risk of recurrence and clinical guidelines. Dis Colon Rectum. 1995;38:1286–95.PubMedCrossRef
30.
Zurück zum Zitat Suzuki T, Sadahiro S, Mukoyama S, Ishikawa K, Yasuda S, Tajima T, et al. Risk of lymph node and distant metastases in patients with early invasive colorectal cancer classified as Haggitt’s level 4 invasion. Dis Colon Rectum. 2003;46:203–8.PubMedCrossRef Suzuki T, Sadahiro S, Mukoyama S, Ishikawa K, Yasuda S, Tajima T, et al. Risk of lymph node and distant metastases in patients with early invasive colorectal cancer classified as Haggitt’s level 4 invasion. Dis Colon Rectum. 2003;46:203–8.PubMedCrossRef
31.
Zurück zum Zitat Tateishi Y, Nakanishi Y, Taniguchi H, Shimoda T, Uemura S. Pathological prognostic factors predicting lymph node metastasis in submucosal invasive (T1) colorectal carcinoma. Mod Pathol. 2010;23:1068–72.PubMedCrossRef Tateishi Y, Nakanishi Y, Taniguchi H, Shimoda T, Uemura S. Pathological prognostic factors predicting lymph node metastasis in submucosal invasive (T1) colorectal carcinoma. Mod Pathol. 2010;23:1068–72.PubMedCrossRef
32.
Zurück zum Zitat Araki Y, Isomoto H, Shirouzu K, Miura K, Iwanaga H, Okita A, et al. Clinicopathological characteristics of colorectal submucosal carcinoma with lymph node metastasis. Kurume Med J. 1993;40:123–7.PubMedCrossRef Araki Y, Isomoto H, Shirouzu K, Miura K, Iwanaga H, Okita A, et al. Clinicopathological characteristics of colorectal submucosal carcinoma with lymph node metastasis. Kurume Med J. 1993;40:123–7.PubMedCrossRef
33.
Zurück zum Zitat Hase K, Shatney CH, Mochizuki H, Johnson DL, Tamakuma S, Vierra M, 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, Johnson DL, Tamakuma S, Vierra M, et al. Long-term results of curative resection of “minimally invasive” colorectal cancer. Dis Colon Rectum. 1995;38:19–26.PubMedCrossRef
34.
Zurück zum Zitat Egashira Y, Yoshida T, Hirata I, Hamamoto N, Akutagawa H, Takeshita A, et al. Analysis of pathological risk factors for lymph node metastasis of submucosal invasive colon cancer. Mod Pathol. 2004;17:503–11.PubMedCrossRef Egashira Y, Yoshida T, Hirata I, Hamamoto N, Akutagawa H, Takeshita A, et al. Analysis of pathological risk factors for lymph node metastasis of submucosal invasive colon cancer. Mod Pathol. 2004;17:503–11.PubMedCrossRef
35.
Zurück zum Zitat Liang P, Hong J-W, Ubukata H, Liu G, Katano M, Motohashi G, et al. Myofibroblasts correlate with lymphatic microvessel density and lymph node metastasis in early-stage invasive colorectal carcinoma. Anticancer Res. 2005;25:2705–12.PubMed Liang P, Hong J-W, Ubukata H, Liu G, Katano M, Motohashi G, et al. Myofibroblasts correlate with lymphatic microvessel density and lymph node metastasis in early-stage invasive colorectal carcinoma. Anticancer Res. 2005;25:2705–12.PubMed
36.
Zurück zum Zitat Oh-e H, Tanaka S, Kitadai Y, Shimamoto F, Yoshihara M, Haruma K. Angiogenesis at the site of deepest penetration predicts lymph node metastasis of submucosal colorectal cancer. Dis Colon Rectum. 2001;44:1129–36.PubMedCrossRef Oh-e H, Tanaka S, Kitadai Y, Shimamoto F, Yoshihara M, Haruma K. Angiogenesis at the site of deepest penetration predicts lymph node metastasis of submucosal colorectal cancer. Dis Colon Rectum. 2001;44:1129–36.PubMedCrossRef
37.
Zurück zum Zitat Sakuragi M, Togashi K, Konishi F, Koinuma K, Kawamura Y, Okada M, 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, Koinuma K, Kawamura Y, Okada M, et al. Predictive factors for lymph node metastasis in T1 stage colorectal carcinomas. Dis Colon Rectum. 2003;46:1626–32.PubMedCrossRef
38.
Zurück zum Zitat Kitajima K, Fujimori T, Fujii S, Takeda J, Ohkura Y, Kawamata H, et al. Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaboration study. J Gastroenterol. 2004;39:534–43.PubMedCrossRef Kitajima K, Fujimori T, Fujii S, Takeda J, Ohkura Y, Kawamata H, et al. Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaboration study. J Gastroenterol. 2004;39:534–43.PubMedCrossRef
39.
41.
Zurück zum Zitat Kaneko I, Shinji S, Oka S, Kawamura T, Hiyama T, Ito M, 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. 2006;50:13–21.CrossRef Kaneko I, Shinji S, Oka S, Kawamura T, Hiyama T, Ito M, 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. 2006;50:13–21.CrossRef
42.
Zurück zum Zitat Kaneko I, Tanaka S, Oka S, Yoshida S, Hiyama T, Arihiro K, et al. Immunohistochemical molecular markers as predictors of curability of endoscopically resected submucosal colorectal cancer. World J Gastroenterol. 2007;28:3829–35. Kaneko I, Tanaka S, Oka S, Yoshida S, Hiyama T, Arihiro K, et al. Immunohistochemical molecular markers as predictors of curability of endoscopically resected submucosal colorectal cancer. World J Gastroenterol. 2007;28:3829–35.
43.
Zurück zum Zitat Yamauchi H, Togashi K, Kawamura Y, Horie H, Sasaki J, Tsujinaka S, et al. Pathological predictors for lymph node metastasis in T1 colorectal cancer. Surg Today. 2008;38:905–10.PubMedCrossRef Yamauchi H, Togashi K, Kawamura Y, Horie H, Sasaki J, Tsujinaka S, et al. Pathological predictors for lymph node metastasis in T1 colorectal cancer. Surg Today. 2008;38:905–10.PubMedCrossRef
44.
Zurück zum Zitat Suzuki A, Togashi K, Nokubi M, Koinuma K, Miyakura Y, Horie H, et al. Evaluation of venous invasion by elastica van Gieson stain and tumor budding predicts local and distant metastases in patients with T1 stage colorectal cancer. Am J Surg Pathol. 2009;33:1601–7.PubMedCrossRef Suzuki A, Togashi K, Nokubi M, Koinuma K, Miyakura Y, Horie H, et al. Evaluation of venous invasion by elastica van Gieson stain and tumor budding predicts local and distant metastases in patients with T1 stage colorectal cancer. Am J Surg Pathol. 2009;33:1601–7.PubMedCrossRef
45.
Zurück zum Zitat Komori K, Hirai T, Kanemitsu Y, Shimizu Y, Sano T, Ito S, et al. Is “depth of submucosal invasion >=1,000 mm” an important predictive factor for lymph node metastasis in early invasive colorectal cancer (PT1)? Hepatogastroenterology. 2010;57:1123–7.PubMed Komori K, Hirai T, Kanemitsu Y, Shimizu Y, Sano T, Ito S, et al. Is “depth of submucosal invasion >=1,000 mm” an important predictive factor for lymph node metastasis in early invasive colorectal cancer (PT1)? Hepatogastroenterology. 2010;57:1123–7.PubMed
46.
Zurück zum Zitat Nakadoi K, Tanaka S, Kanao H, Terasaki M, Takata S, Oka S, et al. Management of T1 colorectal carcinoma with special reference to criteria for curative endoscopic resection. J Gastroenterol Hepatol. 2012;27:1057–62.PubMedCrossRef Nakadoi K, Tanaka S, Kanao H, Terasaki M, Takata S, Oka S, et al. Management of T1 colorectal carcinoma with special reference to criteria for curative endoscopic resection. J Gastroenterol Hepatol. 2012;27:1057–62.PubMedCrossRef
47.
Zurück zum Zitat Hamilton SR, Bosman FT, Boffetta P, Ilyas M, Morreau H, Nakamura S-I, et al. Carcinoma of the colon and rectum. In: Bosman FT, Carneiro F, Hruban RH, et al., editors. WHO classification of tumours of the digestive system. Lyon: International Agency for Research on Cancer (IARC); 2010. p. 134–46. Hamilton SR, Bosman FT, Boffetta P, Ilyas M, Morreau H, Nakamura S-I, et al. Carcinoma of the colon and rectum. In: Bosman FT, Carneiro F, Hruban RH, et al., editors. WHO classification of tumours of the digestive system. Lyon: International Agency for Research on Cancer (IARC); 2010. p. 134–46.
48.
Zurück zum Zitat Jass JR, O’Brien MJ, Riddell RH, Snover DC. Recommendations for the reporting of surgically resected specimens of colorectal carcinoma. Hum Pathol. 2007;38:537–45.PubMedCrossRef Jass JR, O’Brien MJ, Riddell RH, Snover DC. Recommendations for the reporting of surgically resected specimens of colorectal carcinoma. Hum Pathol. 2007;38:537–45.PubMedCrossRef
49.
51.
Zurück zum Zitat 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.PubMedCentralPubMedCrossRef 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.PubMedCentralPubMedCrossRef
52.
Zurück zum Zitat Ishikawa Y, Akishima-Fukasawa Y, Ito K, Akasaka Y, Yokoo T, Ishii T. Histopathologic determinants of regional lymph node metastasis in early colorectal cancer. Cancer. 2008;112:924–33.PubMedCrossRef Ishikawa Y, Akishima-Fukasawa Y, Ito K, Akasaka Y, Yokoo T, Ishii T. Histopathologic determinants of regional lymph node metastasis in early colorectal cancer. Cancer. 2008;112:924–33.PubMedCrossRef
53.
Zurück zum Zitat Ogawa T, Yoshida T, Tsuruta T, Tokuyama W, Adachi S, Kikuchi M, et al. Tumor budding is predictive of lymphatic involvement and lymph node metastases in submucosal invasive colorectal adenocarcinomas and in non-polypoid compared with polypoid growths. Scand J Gastroenterol. 2009;44:605–14.PubMedCrossRef Ogawa T, Yoshida T, Tsuruta T, Tokuyama W, Adachi S, Kikuchi M, et al. Tumor budding is predictive of lymphatic involvement and lymph node metastases in submucosal invasive colorectal adenocarcinomas and in non-polypoid compared with polypoid growths. Scand J Gastroenterol. 2009;44:605–14.PubMedCrossRef
54.
Zurück zum Zitat Horcic M, Koelzer VH, Karamitopoulou E, Terracciano L, Puppa G, Zlobec I, et al. Tumor budding score based on 10 high-power fields is a promising basis for a standardized prognostic scoring system in stage II colorectal cancer. Hum Pathol. 2012 (Epub ahead of print). Horcic M, Koelzer VH, Karamitopoulou E, Terracciano L, Puppa G, Zlobec I, et al. Tumor budding score based on 10 high-power fields is a promising basis for a standardized prognostic scoring system in stage II colorectal cancer. Hum Pathol. 2012 (Epub ahead of print).
55.
Zurück zum Zitat Puppa G, Senore C, Sheahan K, Vieth M, Lugli A, Zlobec I, et al. Diagnostic reproducibility of tumour budding in colorectal cancer: a multicentre, multinational study using virtual microscopy. Histopathology. 2012 (Epub ahead print). Puppa G, Senore C, Sheahan K, Vieth M, Lugli A, Zlobec I, et al. Diagnostic reproducibility of tumour budding in colorectal cancer: a multicentre, multinational study using virtual microscopy. Histopathology. 2012 (Epub ahead print).
Metadaten
Titel
Novel risk factors for lymph node metastasis in early invasive colorectal cancer: a multi-institution pathology review
verfasst von
Hideki Ueno
Kazuo Hase
Yojiro Hashiguchi
Hideyuki Shimazaki
Shinji Yoshii
Shin-ei Kudo
Masafumi Tanaka
Yoshito Akagi
Takeshi Suto
Shinji Nagata
Keiji Matsuda
Koji Komori
Kazuhiko Yoshimatsu
Yasuhiko Tomita
Shozo Yokoyama
Eiji Shinto
Takahiro Nakamura
Kenichi Sugihara
Publikationsdatum
01.09.2014
Verlag
Springer Japan
Erschienen in
Journal of Gastroenterology / Ausgabe 9/2014
Print ISSN: 0944-1174
Elektronische ISSN: 1435-5922
DOI
https://doi.org/10.1007/s00535-013-0881-3

Weitere Artikel der Ausgabe 9/2014

Journal of Gastroenterology 9/2014 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.