Mucinous subtype as prognostic factor in colorectal cancer: A systematic review and meta-analysis

Journal of Clinical Pathology

Volumn 65, Issue 5, 2012, Pages 381-388

  Verhulst, J ^a   Ferdinande, L ^a   Demetter, P ^b   Ceelen, W ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER PROGNOSIS; CANCER SURVIVAL; COLORECTAL CARCINOMA; COLORECTAL MUCINOUS ADENOCARCINOMA; GENDER AND SEX; HUMAN; META ANALYSIS; MICROSATELLITE INSTABILITY; MUCINOUS CARCINOMA; OVERALL SURVIVAL; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW;

ADENOCARCINOMA, MUCINOUS; AGE FACTORS; COLORECTAL NEOPLASMS; FEMALE; HUMANS; MALE; MUCINS; NEOPLASM STAGING; PROGNOSIS; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL;

EID: 84860740469     PISSN: 00219746     EISSN: 14724146     Source Type: Journal    
DOI: 10.1136/jclinpath-2011-200340     Document Type: Review

References (82)

1. Minsky BD. Clinicopathological impact of colloid in colorectal-carcinoma. Dis Colon Rectum 1990;33:714-19.
2. Jass JR, Sobin LH. Histologic Typing of Intestinal Tumours. 2nd edn. Berlin: Springer-Verlag, 1989.
3. Pande R, Sunga A, Levea C, et al. Significance of signet-ring cells in patients with colorectal cancer. Dis Colon Rectum 2008;51:50-5.
4. Papadopoulos VN, Michalopoulos A, Netta S, et al. Prognostic significance of mucinous component in colorectal carcinoma. Tech Coloproctol 2004;8(Suppl 1):s123-5. (Pubitemid 40394533)
5. Park ET, Gum JR, Kakar S, et al. Aberrant expression of SOX2 upregulates MUC5AC gastric foveolar mucin in mucinous cancers of the colorectum and related lesions. Int J Cancer 2008;122:1253-60. (Pubitemid 351287224)
6. Okudaira K, Kakar S, Cun L, et al. MUC2 gene promotor methylation in mucinous and non-mucinous colorectal cancer tissues. Int J Oncol 2010;36:765-75.
7. Park ET, Oh HK, Gum JR, et al. HATH1 expression in mucinous cancers of the colorectum and related lesions. Clin Cancer Res 2006;12:5403-10. (Pubitemid 44497254)
8. Song GA, Deng GR, Bell I, et al. Mucinous carcinomas of the colorectum have distinct molecular genetic characteristics. Int J Oncol 2005;26:745-50.
9. Tanaka H, Deng GR, Matsuzaki K, et al. BRAF mutation, CpG island methylator phenotype and microsatellite instability occur more frequently and concordantly in mucinous than non-mucinous colorectal cancer. Int J Cancer 2006;118:2765-71. (Pubitemid 43673355)
10. Messerini L, Vitelli F, DeVitis LR, et al. Microsatellite instability in sporadic mucinous colorectal carcinomas: Relationship to clinico-pathological variables. J Pathol 1997;182:380-4. (Pubitemid 27317201)
11. Hawkins N, Norrie M, Cheong K, et al. CpG island methylation in sporadic colorectal cancers and its relationship to microsatellite instability. Gastroenterology 2002;122:1376-87. (Pubitemid 34465180)
12. Kim DH, Kim JW, Cho JH, et al. Expression of mucin core proteins, trefoil factors, APC and p21 in subsets of colorectal polyps and cancers suggests a distinct pathway of pathogenesis of mucinous carcinoma of the colorectum. Int J Oncol 2005;27:957-64.
13. Zhang H, Evertsson S, Sun XF. Clinicopathological and genetic characteristics of mucinous carcinomas in the colorectum. Int J Oncol 1999;14:1057-61.
14. Enriquez JM, Diez M, Tobaruela E, et al. Clinical, histopathological, cytogenetic and prognostic differences between mucinous and nonmucinous colorectal adenocarcinomas. Rev Esp Enferl Dig 1998;90:568-72. (Pubitemid 128617919)
15. Akino F MH, Nakamura T, Ohtani Y, et al. High apoptotic activity and low epithelial cell proliferation with underexpression of p21(WAF1/CIP1) and p27(Kip1) of mucinous carcinomas of the colorectum - comparison with well-differentiated type. Am J Clin Pathol 2002;117:908-15. (Pubitemid 34564347)
16. Sarli L, Bottarelli L, Azzoni C, et al. Two subtypes of mucinous adenocarcinoma of the colorectum: clinicopathological and genetic features (vol. 15, pg 1429, 2008). Ann Surg Oncol 2008;15:3326.
17. Kondo T, Masuda H, Abe Y, et al. Two subtypes in colorectal mucinous carcinoma in relation to microsatellite instability. Hepatogastroenterology 2002;49:660-3. (Pubitemid 34615322)
18. Liu XP, Sato T, Oga A, et al. Two subtypes of mucinous colorectal carcinoma characterized by laser scanning cytometry and comparative genomic hybridization. Int J Oncol 2004;25:615-21.
19. You JF, Hsieh LL, Changchien CR, et al. Inverse effects of mucin on survival of matched hereditary nonpolyposis colorectal cancer and sporadic colorectal cancer patients. Clin Cancer Res 2006;12:4244-50.
20. Melis M, Hernandez J, Siegel EM, et al. Gene expression profiling of colorectal mucinous adenocarcinomas. Dis Colon Rectum 2010;53:936-43.
21. Green JB, Timmcke AE, Mitchell WT, et al. Mucinous carcinoma - just another colon cancer. Dis Colon Rectum 1993;36:49-54. (Pubitemid 23019444)
22. Kanemitsu Y, Kato T, Hirai T, et al. Survival after curative resection for mucinous adenocarcinoma of the colorectum. Dis Colon Rectum 2003;46:160-7. (Pubitemid 36222614)
23. Consorti F, Lorenzotti A, Midiri G, et al. Prognostic significance of mucinous carcinoma of colon and rectum: a prospective case-control study. J Surg Oncol 2000;73:70-4. (Pubitemid 30123728)
24. Farhat MH, Barada KA, Tawil AN, et al. Effect of mucin production on survival in colorectal cancer: a case-control study. World J Gastroenterol 2008;14:6981-5.
25. Catalano V, Loupakis F, Graziano F, et al. Mucinous histology predicts for poor response rate and overall survival of patients with colorectal cancer and treated with first-line oxaliplatin- and/or irinotecan-based chemotherapy. Br J Cancer 2009;100:881-7.
26. Negri FV, Wotherspoon A, Cunningham D, et al. Mucinous histology predicts for reduced fluorouracil responsiveness and survival in advanced colorectal cancer. Ann Oncol 2005;16:1305-10. (Pubitemid 41158475)
27. Sengul N, Wexner SD, Woodhouse S, et al. Effects of radiotherapy on different histopathological types of rectal carcinoma. Colorectal Dis 2006;8:283-8.
28. Tierney JF, Stewart LA, Ghersi D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials 2007;8:16.
29. Higgins J, Thompson S, Deeks J, et al. Measuring inconsistency in meta-analysis. Br Med J 2003;327:557-60.
30. Goi T, Obata S, Inoue T, et al. Clinicopathological study of the colorectal mucinous carcinomas. Int Surgery 2006;91:352-7.
31. King-Yin Lam A, Ong K, Ho YH. Colorectal mucinous adenocarcinoma: The clinicopathologic features and significance of p16 and p53 expression. Dis Colon Rectum 2006;49:1275-83. (Pubitemid 44401375)
32. Suma KS, Nirmala V. Mucinous component in colorectal-carcinoma prognostic-significance - a study in a south Indian population. J Surg Oncol 1992;51:60-4.
33. Manxhuka-Kerliu S, Telaku S, Ahmetaj H, et al. Prognostic values. Bosnian J Basic Med 2009;9:19-24.
34. Maksinovic S. Surivall rates in patients with mucinous adenocarcinoma of the colorectum. Med Arh 2007;63:114-16.
35. Adell RME. Is mucinous colorectal cancer a distinct entity? Gastroenterol Hepatol 2002;25:534-40.
36. Duarte I, Zuniga A, Rahmer A, et al. Analysis of 1071 large bowel adenocarcinomas resected in 978 patients. Revista Medica De Chile 1996;124:681-7.
37. Coco C, Magistelli P. [The prognostic role of anatomo-pathologic factors in colorectal cancer: an univariate analysis] (In italian). Ann Ital Chir 1991;62:355-62.
38. Sun XF, Carstensen JM, Stal O, et al. Interrelations of clinicopathologic variables and their prognostic value in colorectal adenocarcinoma. APMIS 1996;104:35-8. (Pubitemid 26083438)
39. Umpleby HC, Ranson DL, Williamson RCN. Peculiarities of mucinous colorectal-carcinoma. Br J Surg 1985;72:715-18.
40. Yamamoto S, Mochizuki H, Hase K, et al. Assessment of clinicopathological features of colorectal mucinous adenocarcinoma. Am J Surg 1993;166:257-61. (Pubitemid 24046429)
41. Pihl E, Nairn RC, Hughes ES, et al. Mucinous colorectal carcinoma: immunopathology and prognosis. Pathology 1980;12:439-47. (Pubitemid 10025249)
42. Wu CS, Tung SY, Chen PC, et al. Clinicopathological study of colorectal mucinous carcinoma in Taiwan: a multivariate analysis. J Gastroenterol Hepatol 1996;11:77-81.
43. Okuno M, Ikehara T, Nagayama M, et al. Mucinous colorectal-carcinoma - clinical pathology and prognosis. Am Surg 1988;54:681-5. (Pubitemid 19015546)
44. Song W, Wu SJ, He YL, et al. Clinicopathologic features and survival of patients with colorectal mucinous, signet-ring cell or non-mucinous adenocarcinoma: experience at an institution in southern China. Chin Med J (Engl) 2009;122:1486-91.
45. Secco GB, Fardelli R, Campora E, et al. Primary mucinous adenocarcinomas and signet-ring cell carcinomas of colon and rectum. Oncology 1994;51:30-4. (Pubitemid 24008637)
46. Hill DA, Furman WL, Billups CA, et al. Colorectal carcinoma in childhood and adolescence: a clinicopathologic review. J Clin Oncol 2007;25:5808-14.
47. Chen HS. Curative resection of colorectal adenocarcinoma: multivariate analysis of 5-year follow-up. World J Surg 1999;23:1301-6.
48. Connelly JH, Robeycafferty SS, Cleary KR. Mucinous carcinomas of the colon and rectum - an analysis of 62 stage-b and stage-c lesions. Arch Pathol Lab Med 1991;115:1022-5.
49. Sultan I, Rodriguez-Galindo C, El-Taani H, et al. Distinct features of colorectal cancer in children and adolescents a population-based study of 159 cases. Cancer 2010;116:758-65.
50. Kang HJ, O'Connell JB, Maggard MA, et al. A 10-year outcomes evaluation of mucinous and signet-ring cell carcinoma of the colon and rectum. Dis Colon Rectum 2005;48:1161-8. (Pubitemid 40897859)
51. Higgins JPT, Green S. (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org
52. Arai T, Kasahara I, Sawabe M, et al. Microsatellite-unstable mucinous colorectal carcinoma occurring in the elderly: comparison with medullary type poorly differentiated adenocarcinoma. Pathol Int 2007;57:205-12. (Pubitemid 46279949)
53. Kakar S, Aksoy S, Burgart LJ, et al. Mucinous carcinoma of the colon: correlation of loss of mismatch repair enzymes with clinicopathologic features and survival. Mod Pathol 2004;17:696-700. (Pubitemid 38715493)
54. Leopoldo S, Lorena B, Cinzia A, et al. Two subtypes of mucinous adenocarcinoma of the colorectum: clinicopathological and genetic features. Ann Surg Oncol 2008;15:1429-39.
55. Messerini L, Ciantelli M, Baglioni S, et al. Prognostic significance of microsatellite instability in sporadic mucinous colorectal cancers. Hum Pathol 1999;30:629-34. (Pubitemid 29266720)
56. Kazama Y, Watanabe T, Kanazawa T, et al. Mucinous colorectal cancers with chromosomal instability - a biologically distinct and aggressive subtype. Diagn Mol Pathol 2006;15:30-4.
57. Nozoe T, Anai H, Nasu S, et al. Clinicopathological characteristics of mucinous carcinoma of the colon and rectum. J Surg Oncol 2000;75:103-7.
58. Sasaki O, Atkin WS, Jass JR. Mucinous carcinoma of the rectum. Histopathology 1987;11:259-72. (Pubitemid 17038274)
59. Symonds DA, Vickery AL. Mucinous carcinoma of colon and rectum. Cancer 1976;37:1891-900.
60. Gafa R, Maestri I, Matteuzzi M, et al. Sporadic colorectal adenocarcinomas with high-frequency microsatellite instability - pathobiologic features, hMLH1 and hMSH2 expression, and clinical outcome. Cancer 2000;89:2025-37.
61. Kim YH, Min BH, Choi HK, et al. Sporadic colorectal carcinomas with low-level microsatellite instability in Korea: do they form a distinct subgroup with distinguished clinicopathological features? J Surg Oncol 2009;99:351-5.
62. Borger ME, Gosens M, Jeuken JWM, et al. Signet ring cell differentiation in mucinous colorectal carcinoma. J Pathol 2007;212:278-86. (Pubitemid 47010061)
63. Bosset J, Mineur L, Maingon P, et al. Enhanced tumorocidal effect of chemotherapy with preoperative radiotherapy for ractal cancer: preliminary results-EORTC 22921. J Clin Oncol 2005;23:5620-7.
64. Nagtegaal I, Marijnen C, van de Velde C, et al. Morphological changes in tumour type after radiotherapy are accompanied by changes in gene expression profile but not in clinical behaviour. J Pathol 2004;204:183-92. (Pubitemid 39335292)
65. Kim HG, Jen J, Vogelstein B, et al. Clinical and pathological characteristics of sporadic colorectal carcinomas with DNA replication errors in microsatellite sequences. Am J Pathol 1994;145:148-56. (Pubitemid 24217493)
66. Chen JS, Hsieh PS, Hung SY, et al. Clinical significance of signet ring cell rectal carcinoma. Int J Colorectal Dis 2004;19:102-7.
67. Cusack JC, Giacco GG, Cleary K, et al. Survival factors in 186 patients younger than 40 years old with colorectal adenocarcinoma. J Am Coll Surg 1996;183:105-12. (Pubitemid 26260141)
68. Ponz de Leon M, Sant M, Micheli A, et al. Clinical and pathologic prognostic indicators in colorectal cancer: a population-based study. Cancer 1992;69:626-35.
69. Du WB, Mah JTL, Lee J, et al. Incidence and survival of mucinous adenocarcinoma of the colorectum: a population-based study from an Asian country. Dis Colon Rectum 2004;47:78-85. (Pubitemid 38040249)
70. Grillo-Ruggieri F, Mantello G, Berardi R, et al. Mucinous rectal adenocarcinoma can be associated to tumour downstaging after preoperative chemoradiotherapy. Dis Colon Rectum 2007;50:1594-603. (Pubitemid 47583365)
71. Hilska M, Collan Y, Roberts PJ, et al. Prognostic value of various staging and grading systems in proximal colon cancer. Eur J Surg 2002;168:84-90. (Pubitemid 34478211)
72. Lee WS, Chun HK, Lee WY, et al. Treatment outcomes in patients with signet ring cell carcinoma of the colorectum. Am J Surg 2007;194:294-8. (Pubitemid 47212047)
73. Min BS, Kim NK, Ko YT, et al. Clinicopathological features of signet-ring cell carcinoma of the colon and rectum: a case-matched study. Hepatogastroenterology 2009;56:984-8.
74. Purdie CA, Piris J. Histopathological grade, mucinous differentiation and DNA ploidy in relation to prognosis in colorectal carcinoma. Histopathology 2000;36:121-6. (Pubitemid 30113973)
75. Sugao Y, Yao T, Kubo C, et al. Improved prognosis of solid-type poorly differentiated colorectal adenocarcinoma: a clinicopathological and immunohistochemical study. Histopathology 1997;31:123-33. (Pubitemid 27357346)
76. Xie L, Villeneuve PJ, Shaw A. Survival of patients diagnosed with either colorectal mucinous or non-mucinous adenocarcinoma: a population-based study in Canada. Int J Oncol 2009;34:1109-15.
77. Chew MH, Koh PK, Ng KH, et al. Improved survival in an Asian cohort of young colorectal cancer patients: an analysis of 523 patients from a single institution. Int J Colorectal Dis 2009;24:1075-83.
78. Cerottini JP, Caplin S, Pampallona S, et al. Prognostic factors in colorectal cancer. Oncol Rep 1999;6:409-14.
79. Halvorsen TB, Seim E. Influence of mucinous components on survival in colorectal adenocarcinomas - a multivariate-analysis. J Clin Pathol 1988;41:1068-72.
80. Minsky BD, Mies C, Rich TA, et al. Colloid carcinoma of the colon and rectum. Cancer 1987;60:3103-12. (Pubitemid 18005891)
81. Spratt JS, Spjut HJ. Prevalence and prognosis of individual clinical and pathologic variables associated with colorectal carcinoma. Cancer 1967;20:1976-85.
82. Wolfman EF, Astler VB, Coller FA. Mucoid adenocarcinoma of the colon and rectum. Surgery 1957;42:846-52.