Skip to main content
Top
Published in: Diagnostic Pathology 1/2011

Open Access 01-12-2011 | Research

Nuclear beta-catenin overexpression in metastatic sentinel lymph node is associated with synchronous liver metastasis in colorectal cancer

Authors: Hongxia Cheng, Hui Liang, Yejun Qin, Ying Liu

Published in: Diagnostic Pathology | Issue 1/2011

Login to get access

Abstract

Background

Beta-catenin, a component of the Wingless/Wnt signaling pathway, can activate target genes linking with the adenomatous polyposis coli (APC) gene in colorectal cancer. The purpose of this study is to investigate whether nuclear beta-catenin overexpression in metastatic sentinel lymph node(s) [SLN(s)] is associated with synchronous liver metastasis.

Methods

Clinicopathological data from 355 patients (93 cases with liver metastasis and 262 cases without liver metastasis) were reviewed. Beta-catenin expression in metastatic SLN(s) and liver metastatic lesions was examined by immunohistochemistry. The association of nuclear beta-catenin expression in metastatic SLN(s) and liver metastatic lesions was evaluated, and the relationship between nuclear beta-catenin expression and clinicopathological characteristics was analyzed. Finally, univariate and logistic multivariate regression analyses were adopted to discriminate the risk factors of liver metastasis.

Results

Nuclear beta-catenin overexpression in metastatic SLN(s) was observed in 70 patients with liver metastasis and 31 patients without liver metastasis (75.3% vs. 11.8%; P < 0.001). Nuclear beta-catenin expression was noted in all the metastatic lesions. Spearman rank correlation analysis demonstrated that nuclear beta-catenin expression in metastatic SLN(s) had a positive correlation with that in metastatic lesions (r = 0.425, P < 0.001). Univariate and multivariate analyses indicated that nuclear beta-catenin overexpression in metastatic SLN(s) correlated with liver metastasis.

Conclusions

Nuclear beta-catenin overexpression in metastatic SLN(s) is strongly associated with liver metastasis and may contribute to predict liver metastasis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Jemal A, Tiwari RC, Murray T, Ghafoor A, Samuels A, Ward E: Cancer statistics 2004. CA Cancer J Clin. 2004, 54: 8-29. 10.3322/canjclin.54.1.8.CrossRefPubMed Jemal A, Tiwari RC, Murray T, Ghafoor A, Samuels A, Ward E: Cancer statistics 2004. CA Cancer J Clin. 2004, 54: 8-29. 10.3322/canjclin.54.1.8.CrossRefPubMed
2.
go back to reference Laffer UT, Metzger U: Intraportal chemotherapy for colorectal hepatic metastases. World J Surg. 1995, 19: 246-51. 10.1007/BF00308634.CrossRefPubMed Laffer UT, Metzger U: Intraportal chemotherapy for colorectal hepatic metastases. World J Surg. 1995, 19: 246-51. 10.1007/BF00308634.CrossRefPubMed
3.
go back to reference Barozzi C, Ravaioli M, D'Errico A, Grazi GL, Poggioli G, Cavrini G, et al.: Relevance of biologic markers in colorectal carcinoma: a comparative study of a broad panel. Cancer. 2002, 94: 647-57. 10.1002/cncr.10278.CrossRefPubMed Barozzi C, Ravaioli M, D'Errico A, Grazi GL, Poggioli G, Cavrini G, et al.: Relevance of biologic markers in colorectal carcinoma: a comparative study of a broad panel. Cancer. 2002, 94: 647-57. 10.1002/cncr.10278.CrossRefPubMed
4.
go back to reference Chen Z, Li M, Yuan Y, Wang Q, Yan L, Gu J: Cancer/testis antigens and clinical risk factors for liver metastasis of colorectal cancer: a predictive panel. Dis Colon Rectum. 2010, 53: 31-8. 10.1007/DCR.0b013e3181bdca3a.CrossRefPubMed Chen Z, Li M, Yuan Y, Wang Q, Yan L, Gu J: Cancer/testis antigens and clinical risk factors for liver metastasis of colorectal cancer: a predictive panel. Dis Colon Rectum. 2010, 53: 31-8. 10.1007/DCR.0b013e3181bdca3a.CrossRefPubMed
5.
go back to reference Iwaya K, Oikawa K, Semba S, Tsuchiya B, Mukai Y, Otsubo T, et al.: Correlation between liver metastasis of the colocalization of actin-related protein 2 and 3 complex and WAVE2 in colorectal carcinoma. Cancer Sci. 2007, 98: 992-9. 10.1111/j.1349-7006.2007.00488.x.CrossRefPubMed Iwaya K, Oikawa K, Semba S, Tsuchiya B, Mukai Y, Otsubo T, et al.: Correlation between liver metastasis of the colocalization of actin-related protein 2 and 3 complex and WAVE2 in colorectal carcinoma. Cancer Sci. 2007, 98: 992-9. 10.1111/j.1349-7006.2007.00488.x.CrossRefPubMed
6.
go back to reference Kaio E, Tanaka S, Kitadai Y, Sumii M, Yoshihara M, Haruma K, et al.: Clinical significance of angiogenic factor expression at the deepest invasive site of advanced colorectal carcinoma. Oncology. 2003, 64: 61-73. 10.1159/000066511.CrossRefPubMed Kaio E, Tanaka S, Kitadai Y, Sumii M, Yoshihara M, Haruma K, et al.: Clinical significance of angiogenic factor expression at the deepest invasive site of advanced colorectal carcinoma. Oncology. 2003, 64: 61-73. 10.1159/000066511.CrossRefPubMed
7.
go back to reference Sasaki A, Iwashita Y, Shibata K, Matsumoto T, Ohta M, Inomata M, et al.: Risk factors for early extrahepatic metastasis in patients with liver metastasis from colorectal carcinoma. Hepatogastroenterology. 2005, 52: 1840-4.PubMed Sasaki A, Iwashita Y, Shibata K, Matsumoto T, Ohta M, Inomata M, et al.: Risk factors for early extrahepatic metastasis in patients with liver metastasis from colorectal carcinoma. Hepatogastroenterology. 2005, 52: 1840-4.PubMed
8.
go back to reference Talbot IC, Ritchie S, Leighton MH, Hughes AO, Bussey HJ, Morson BC: The clinical significance of invasion of veins by rectal cancer. Br J Surg. 1980, 67: 439-42. 10.1002/bjs.1800670619.CrossRefPubMed Talbot IC, Ritchie S, Leighton MH, Hughes AO, Bussey HJ, Morson BC: The clinical significance of invasion of veins by rectal cancer. Br J Surg. 1980, 67: 439-42. 10.1002/bjs.1800670619.CrossRefPubMed
9.
go back to reference Yamazoe Y, Maetani S, Onodera H, Nishikawa T, Tobe T: Histopathological prediction of liver metastasis after curative resection of colorectal cancer. Surg Oncol. 1992, 1: 237-44. 10.1016/0960-7404(92)90070-2.CrossRefPubMed Yamazoe Y, Maetani S, Onodera H, Nishikawa T, Tobe T: Histopathological prediction of liver metastasis after curative resection of colorectal cancer. Surg Oncol. 1992, 1: 237-44. 10.1016/0960-7404(92)90070-2.CrossRefPubMed
10.
go back to reference Adachi Y, Inomata M, Kakisako K, Sato K, Shiraishi N, Kitano S: Histopathologic characteristics of colorectal cancer with liver metastasis. Dis Colon Rectum. 1999, 42: 1053-6. 10.1007/BF02236702.CrossRefPubMed Adachi Y, Inomata M, Kakisako K, Sato K, Shiraishi N, Kitano S: Histopathologic characteristics of colorectal cancer with liver metastasis. Dis Colon Rectum. 1999, 42: 1053-6. 10.1007/BF02236702.CrossRefPubMed
11.
go back to reference De Jong KP, Stellema R, Karrenbeld A, Koudstaal J, Gouw AS, Sluiter WJ, et al.: Clinical relevance of transforming growth factor alpha, epidermal growth factor receptor, p53, and Ki67 in colorectal liver metastases and corresponding primary tumors. Hepatology. 1998, 28: 971-9.CrossRefPubMed De Jong KP, Stellema R, Karrenbeld A, Koudstaal J, Gouw AS, Sluiter WJ, et al.: Clinical relevance of transforming growth factor alpha, epidermal growth factor receptor, p53, and Ki67 in colorectal liver metastases and corresponding primary tumors. Hepatology. 1998, 28: 971-9.CrossRefPubMed
12.
go back to reference Nanashima A, Yamaguchi H, Sawai T, Yasutake T, Tsuji T, Jibiki M, et al.: Expression of adhesion molecules in hepatic metastases of colorectal carcinoma: relationship to primary tumours and prognosis after hepatic resection. J Gastroenterol Hepatol. 1999, 14: 1004-9. 10.1046/j.1440-1746.1999.01991.x.CrossRefPubMed Nanashima A, Yamaguchi H, Sawai T, Yasutake T, Tsuji T, Jibiki M, et al.: Expression of adhesion molecules in hepatic metastases of colorectal carcinoma: relationship to primary tumours and prognosis after hepatic resection. J Gastroenterol Hepatol. 1999, 14: 1004-9. 10.1046/j.1440-1746.1999.01991.x.CrossRefPubMed
13.
go back to reference Fujita S, Taniguchi H, Yao T, Shimoda T, Ueno H, Hirai T, et al.: Multi-institutional study of risk factors of liver metastasis from colorectal cancer: correlation with CD10 expression. Int J Colorectal Dis. 2010, 25: 681-6. 10.1007/s00384-010-0913-x.CrossRefPubMed Fujita S, Taniguchi H, Yao T, Shimoda T, Ueno H, Hirai T, et al.: Multi-institutional study of risk factors of liver metastasis from colorectal cancer: correlation with CD10 expression. Int J Colorectal Dis. 2010, 25: 681-6. 10.1007/s00384-010-0913-x.CrossRefPubMed
14.
go back to reference Ohji Y, Yao T, Eguchi T, Yamada T, Hirahashi M, Iida M, et al.: Evaluation of risk of liver metastasis in colorectal adenocarcinoma based on the combination of risk factors including CD10 expression: multivariate analysis of clinicopathological and immunohistochemical factors. Oncol Rep. 2007, 17: 525-30.PubMed Ohji Y, Yao T, Eguchi T, Yamada T, Hirahashi M, Iida M, et al.: Evaluation of risk of liver metastasis in colorectal adenocarcinoma based on the combination of risk factors including CD10 expression: multivariate analysis of clinicopathological and immunohistochemical factors. Oncol Rep. 2007, 17: 525-30.PubMed
15.
go back to reference Brabletz S, Schmalhofer O, Brabletz T: Gastrointestinal stem cells in development and cancer. J Pathol. 2009, 217: 307-17. 10.1002/path.2475.CrossRefPubMed Brabletz S, Schmalhofer O, Brabletz T: Gastrointestinal stem cells in development and cancer. J Pathol. 2009, 217: 307-17. 10.1002/path.2475.CrossRefPubMed
16.
go back to reference Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T: Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005, 5: 744-9. 10.1038/nrc1694.CrossRefPubMed Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T: Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005, 5: 744-9. 10.1038/nrc1694.CrossRefPubMed
17.
go back to reference Fodde R, Brabletz T: Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol. 2007, 19: 150-8. 10.1016/j.ceb.2007.02.007.CrossRefPubMed Fodde R, Brabletz T: Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol. 2007, 19: 150-8. 10.1016/j.ceb.2007.02.007.CrossRefPubMed
18.
go back to reference Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, et al.: Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci USA. 2001, 98: 10356-61. 10.1073/pnas.171610498.PubMedCentralCrossRefPubMed Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, et al.: Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci USA. 2001, 98: 10356-61. 10.1073/pnas.171610498.PubMedCentralCrossRefPubMed
19.
go back to reference Harris TJ, Peifer M: Decisions, decisions: beta-catenin chooses between adhesion and transcription. Trends Cell Biol. 2005, 15: 234-7. 10.1016/j.tcb.2005.03.002.CrossRefPubMed Harris TJ, Peifer M: Decisions, decisions: beta-catenin chooses between adhesion and transcription. Trends Cell Biol. 2005, 15: 234-7. 10.1016/j.tcb.2005.03.002.CrossRefPubMed
20.
go back to reference van EJH, Barker N, Clevers H: You Wnt some, you lose some: oncogenes in the Wnt signaling pathway. Curr Opin Genet Dev. 2003, 13: 28-33. 10.1016/S0959-437X(02)00012-6.CrossRef van EJH, Barker N, Clevers H: You Wnt some, you lose some: oncogenes in the Wnt signaling pathway. Curr Opin Genet Dev. 2003, 13: 28-33. 10.1016/S0959-437X(02)00012-6.CrossRef
21.
go back to reference Bandapalli OR, Dihlmann S, Helwa R, Macher-Goeppinger S, Weitz J, Schirmacher P, et al.: Transcriptional activation of the beta-catenin gene at the invasion front of colorectal liver metastases. J Pathol. 2009, 218: 370-9. 10.1002/path.2539.CrossRefPubMed Bandapalli OR, Dihlmann S, Helwa R, Macher-Goeppinger S, Weitz J, Schirmacher P, et al.: Transcriptional activation of the beta-catenin gene at the invasion front of colorectal liver metastases. J Pathol. 2009, 218: 370-9. 10.1002/path.2539.CrossRefPubMed
22.
go back to reference Bagaria SP, Faries MB, Morton DL: Sentinel node biopsy in melanoma: technical considerations of the procedure as performed at the John Wayne Cancer Institute. J Surg Oncol. 2010, 101: 669-76. 10.1002/jso.21581.PubMedCentralCrossRefPubMed Bagaria SP, Faries MB, Morton DL: Sentinel node biopsy in melanoma: technical considerations of the procedure as performed at the John Wayne Cancer Institute. J Surg Oncol. 2010, 101: 669-76. 10.1002/jso.21581.PubMedCentralCrossRefPubMed
23.
go back to reference van AAC, Voit CA, Verhoef C, Eggermont AM: New developments in sentinel node staging in melanoma: controversies and alternatives. Curr Opin Oncol. 2010, 22: 169-77. 10.1097/CCO.0b013e328337aa78.CrossRef van AAC, Voit CA, Verhoef C, Eggermont AM: New developments in sentinel node staging in melanoma: controversies and alternatives. Curr Opin Oncol. 2010, 22: 169-77. 10.1097/CCO.0b013e328337aa78.CrossRef
24.
go back to reference Kelley MC, Hansen N, McMasters KM: Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Am J Surg. 2004, 188: 49-61. 10.1016/j.amjsurg.2003.10.028.CrossRefPubMed Kelley MC, Hansen N, McMasters KM: Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Am J Surg. 2004, 188: 49-61. 10.1016/j.amjsurg.2003.10.028.CrossRefPubMed
25.
go back to reference Newman EA, Newman LA: Lymphatic mapping techniques and sentinel lymph node biopsy in breast cancer. Surg Clin North Am. 2007, 87: 353-64. 10.1016/j.suc.2007.01.013. viiiCrossRefPubMed Newman EA, Newman LA: Lymphatic mapping techniques and sentinel lymph node biopsy in breast cancer. Surg Clin North Am. 2007, 87: 353-64. 10.1016/j.suc.2007.01.013. viiiCrossRefPubMed
26.
go back to reference Bembenek A, Gretschel S, Schlag PM: Sentinel lymph node biopsy for gastrointestinal cancers. J Surg Oncol. 2007, 96: 342-52. 10.1002/jso.20863.CrossRefPubMed Bembenek A, Gretschel S, Schlag PM: Sentinel lymph node biopsy for gastrointestinal cancers. J Surg Oncol. 2007, 96: 342-52. 10.1002/jso.20863.CrossRefPubMed
27.
go back to reference Dionigi G, Castano P, Rovera F, Boni L, Annoni M, Villa F, et al.: The application of sentinel lymph node mapping in colon cancer. Surg Oncol. 2007, 16 (Suppl 1): S129-32.CrossRefPubMed Dionigi G, Castano P, Rovera F, Boni L, Annoni M, Villa F, et al.: The application of sentinel lymph node mapping in colon cancer. Surg Oncol. 2007, 16 (Suppl 1): S129-32.CrossRefPubMed
28.
go back to reference Bilchik AJ, Giuliano A, Essner R, Bostick P, Kelemen P, Foshag LJ, et al.: Universal application of intraoperative lymphatic mapping and sentinel lymphadenectomy in solid neoplasms. Cancer J Sci Am. 1998, 4: 351-8.PubMed Bilchik AJ, Giuliano A, Essner R, Bostick P, Kelemen P, Foshag LJ, et al.: Universal application of intraoperative lymphatic mapping and sentinel lymphadenectomy in solid neoplasms. Cancer J Sci Am. 1998, 4: 351-8.PubMed
29.
go back to reference Dragan R, Nebojsa M, Dejan S, Ivan P, Dragos S, Damir J, et al.: Clinical application of sentinel lymph node biopsy for staging, treatment and prognosis of colon and gastric cancer. Hepatogastroenterology. 2009, 56: 1606-11.PubMed Dragan R, Nebojsa M, Dejan S, Ivan P, Dragos S, Damir J, et al.: Clinical application of sentinel lymph node biopsy for staging, treatment and prognosis of colon and gastric cancer. Hepatogastroenterology. 2009, 56: 1606-11.PubMed
30.
go back to reference He ZY, Wen H, Shi CB, Wang J: Up-regulation of hnRNP A1, Ezrin, tubulin beta-2C and Annexin A1 in sentinel lymph nodes of colorectal cancer. World J Gastroenterol. 2010, 16: 4670-6. 10.3748/wjg.v16.i37.4670.PubMedCentralCrossRefPubMed He ZY, Wen H, Shi CB, Wang J: Up-regulation of hnRNP A1, Ezrin, tubulin beta-2C and Annexin A1 in sentinel lymph nodes of colorectal cancer. World J Gastroenterol. 2010, 16: 4670-6. 10.3748/wjg.v16.i37.4670.PubMedCentralCrossRefPubMed
31.
go back to reference Greene FL, Page DL: AJCC Cancer Staging Manual. 2002, New York, NY: Springer-Verlag, 127-38. 6CrossRef Greene FL, Page DL: AJCC Cancer Staging Manual. 2002, New York, NY: Springer-Verlag, 127-38. 6CrossRef
32.
go back to reference Smith FM, Coffey JC, Khasri NM, Walsh MF, Parfrey N, Gaffney E, et al.: Sentinel nodes are identifiable in formalin-fixed specimens after surgeon-performed ex vivo sentinel lymph node mapping in colorectal cancer. Ann Surg Oncol. 2005, 12: 504-9. 10.1245/ASO.2005.08.019.CrossRefPubMed Smith FM, Coffey JC, Khasri NM, Walsh MF, Parfrey N, Gaffney E, et al.: Sentinel nodes are identifiable in formalin-fixed specimens after surgeon-performed ex vivo sentinel lymph node mapping in colorectal cancer. Ann Surg Oncol. 2005, 12: 504-9. 10.1245/ASO.2005.08.019.CrossRefPubMed
33.
go back to reference Romeo S, Bovee JV, Grogan SP, Taminiau AH, Eilers PH, Cleton-Jansen AM, et al.: Chondromyxoid fibroma resembles in vitro chondrogenesis, but differs in expression of signalling molecules. J Pathol. 2005, 206: 135-42. 10.1002/path.1782.CrossRefPubMed Romeo S, Bovee JV, Grogan SP, Taminiau AH, Eilers PH, Cleton-Jansen AM, et al.: Chondromyxoid fibroma resembles in vitro chondrogenesis, but differs in expression of signalling molecules. J Pathol. 2005, 206: 135-42. 10.1002/path.1782.CrossRefPubMed
34.
go back to reference Brembeck FH, Rosario M, Birchmeier W: Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr Opin Genet Dev. 2006, 16: 51-9. 10.1016/j.gde.2005.12.007.CrossRefPubMed Brembeck FH, Rosario M, Birchmeier W: Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr Opin Genet Dev. 2006, 16: 51-9. 10.1016/j.gde.2005.12.007.CrossRefPubMed
35.
go back to reference Brabletz T, Jung A, Kirchner T: Beta-catenin and the morphogenesis of colorectal cancer. Virchows Arch. 2002, 441: 1-11. 10.1007/s00428-002-0642-9.CrossRefPubMed Brabletz T, Jung A, Kirchner T: Beta-catenin and the morphogenesis of colorectal cancer. Virchows Arch. 2002, 441: 1-11. 10.1007/s00428-002-0642-9.CrossRefPubMed
36.
go back to reference Canavese G, Bernardi A, Candelaresi G, Lovadina P, Amerio S, Rossetti V, et al.: Expression of the E-cadherin-catenins complex in sentinel node is related to tumor morphology but not to spread to nonsentinel nodes. Pathol Res Pract. 2007, 203: 517-23. 10.1016/j.prp.2007.03.003.CrossRefPubMed Canavese G, Bernardi A, Candelaresi G, Lovadina P, Amerio S, Rossetti V, et al.: Expression of the E-cadherin-catenins complex in sentinel node is related to tumor morphology but not to spread to nonsentinel nodes. Pathol Res Pract. 2007, 203: 517-23. 10.1016/j.prp.2007.03.003.CrossRefPubMed
37.
go back to reference Zhang B, Ougolkov A, Yamashita K, Takahashi Y, Mai M, Minamoto T: beta-Catenin and ras oncogenes detect most human colorectal cancer. Clin Cancer Res. 2003, 9: 3073-9.PubMed Zhang B, Ougolkov A, Yamashita K, Takahashi Y, Mai M, Minamoto T: beta-Catenin and ras oncogenes detect most human colorectal cancer. Clin Cancer Res. 2003, 9: 3073-9.PubMed
38.
go back to reference Baldus SE, Monig SP, Huxel S, Landsberg S, Hanisch FG, Engelmann K, et al.: MUC1 and nuclear beta-catenin are coexpressed at the invasion front of colorectal carcinomas and are both correlated with tumor prognosis. Clin Cancer Res. 2004, 10: 2790-6. 10.1158/1078-0432.CCR-03-0163.CrossRefPubMed Baldus SE, Monig SP, Huxel S, Landsberg S, Hanisch FG, Engelmann K, et al.: MUC1 and nuclear beta-catenin are coexpressed at the invasion front of colorectal carcinomas and are both correlated with tumor prognosis. Clin Cancer Res. 2004, 10: 2790-6. 10.1158/1078-0432.CCR-03-0163.CrossRefPubMed
39.
go back to reference da FLM, da LMM, Lacerda-Filho A, Cabral MM, da SRG: Colorectal carcinoma in different age groups: A histopathological analysis. Int J Colorectal Dis. 2011, da FLM, da LMM, Lacerda-Filho A, Cabral MM, da SRG: Colorectal carcinoma in different age groups: A histopathological analysis. Int J Colorectal Dis. 2011,
40.
go back to reference O'Connell JB, Maggard MA, Liu JH, Etzioni DA, Ko CY: Are survival rates different for young and older patients with rectal cancer. Dis Colon Rectum. 2004, 47: 2064-9. 10.1007/s10350-004-0738-1.CrossRefPubMed O'Connell JB, Maggard MA, Liu JH, Etzioni DA, Ko CY: Are survival rates different for young and older patients with rectal cancer. Dis Colon Rectum. 2004, 47: 2064-9. 10.1007/s10350-004-0738-1.CrossRefPubMed
41.
go back to reference Liang H, Wang XN, Wang BG, Pan Y, Liu N, Wang DC, et al.: Prognostic factors of young patients with colon cancer after surgery. World J Gastroenterol. 2006, 12: 1458-62.PubMedCentralPubMed Liang H, Wang XN, Wang BG, Pan Y, Liu N, Wang DC, et al.: Prognostic factors of young patients with colon cancer after surgery. World J Gastroenterol. 2006, 12: 1458-62.PubMedCentralPubMed
42.
go back to reference Savas N, Dagli U, Akbulut S, Yuksel O, Sahin OB: Colorectal cancer localization in young patients: should we expand the screening program. Dig Dis Sci. 2007, 52: 798-802. 10.1007/s10620-006-9432-6.CrossRefPubMed Savas N, Dagli U, Akbulut S, Yuksel O, Sahin OB: Colorectal cancer localization in young patients: should we expand the screening program. Dig Dis Sci. 2007, 52: 798-802. 10.1007/s10620-006-9432-6.CrossRefPubMed
Metadata
Title
Nuclear beta-catenin overexpression in metastatic sentinel lymph node is associated with synchronous liver metastasis in colorectal cancer
Authors
Hongxia Cheng
Hui Liang
Yejun Qin
Ying Liu
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Diagnostic Pathology / Issue 1/2011
Electronic ISSN: 1746-1596
DOI
https://doi.org/10.1186/1746-1596-6-109

Other articles of this Issue 1/2011

Diagnostic Pathology 1/2011 Go to the issue