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Insight into Mucinous Colorectal Carcinoma: Clues from Etiology

  • Colorectal Cancer
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

The prognostic impact of mucinous carcinoma (MC) in colorectal cancer (CRC) has been subject to debate ever since the introduction of the classification of tumors according to their histological differentiation. MC is a distinct clinical and pathological entity within the spectrum of CRC and accounts for approximately 10–15 % of cases. Factors involved in MC development have not been completely understood, but clinical observations may lead to a better insight into the etiology of MC. In this article, we provide an in-depth review of the literature regarding etiological aspects of MC. We show that there are worldwide differences in the prevalence of MC, with low rates in Asian countries and higher rates in the western world. Moreover, MC is more commonly diagnosed in patients suffering from inflammatory bowel diseases or Lynch syndrome and an increased rate of MC is observed in patients with radiotherapy-induced CRCs. These findings are suggestive of a different oncogenic development. Identification of conditions that are associated with MC generates insight into the etiological pathways leading to the development of this special subtype.

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References

  1. Ferlay J, Shin HR, Bray F, et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127(12):2893–917.

    Article  CAS  PubMed  Google Scholar 

  2. Hyngstrom JR, Hu CY, Xing Y, et al. Clinicopathology and outcomes for mucinous and signet ring colorectal adenocarcinoma: analysis from the National Cancer Data Base. Ann Surg Oncol. 2012;19(9):2814–21.

    Article  PubMed Central  PubMed  Google Scholar 

  3. Hugen N, Verhoeven RH, Radema SA, et al. Prognosis and value of adjuvant chemotherapy in stage III mucinous colorectal carcinoma. Ann Oncol. 2013;24(11):2819–24.

    Article  CAS  PubMed  Google Scholar 

  4. Hugen N, van de Velde CJ, de Wilt JH, et al. Metastatic pattern in colorectal cancer is strongly influenced by histological subtype. Ann Oncol. 2014;25(3):651–7.

    Article  CAS  PubMed  Google Scholar 

  5. Mekenkamp LJ, Heesterbeek KJ, Koopman M, et al. Mucinous adenocarcinomas: poor prognosis in metastatic colorectal cancer. Eur J Cancer. 2012;48(4):501–9.

    Article  PubMed  Google Scholar 

  6. 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(8):1305–10.

    Article  CAS  PubMed  Google Scholar 

  7. 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(6):881–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Bosman FT. World Health Organization. International Agency for Research on Cancer. WHO classification of tumours of the digestive system. 4th edn. Lyon: International Agency for Research on Cancer, 2010.

  9. Song GA, Deng G, Bell I, et al. Mucinous carcinomas of the colorectum have distinct molecular genetic characteristics. Int J Oncol. 2005;26(3):745–50.

    CAS  PubMed  Google Scholar 

  10. Hanski C. Is mucinous carcinoma of the colorectum a distinct genetic entity? Br J Cancer. 1995;72(6):1350–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Du W, Mah JT, 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(1):78–85.

    Article  PubMed  Google Scholar 

  12. Sasaki S, Masaki T, Umetani N, et al. Characteristics in primary signet-ring cell carcinoma of the colorectum, from clinicopathological observations. Jpn J Clin Oncol. 1998;28(3):202–6.

    Article  CAS  PubMed  Google Scholar 

  13. Kanemitsu Y, Kato T, Hirai T, et al. Survival after curative resection for mucinous adenocarcinoma of the colorectum. Dis Colon Rectum. 2003;46(2):160–7.

    Article  PubMed  Google Scholar 

  14. Yamaguchi T, Taniguchi H, Fujita S, et al. Clinicopathological characteristics and prognostic factors of advanced colorectal mucinous adenocarcinoma. Histopathology. 2012;61(2):162–9.

    Article  PubMed  Google Scholar 

  15. Numata M, Shiozawa M, Watanabe T, et al. The clinicopathological features of colorectal mucinous adenocarcinoma and a therapeutic strategy for the disease. World J Surg Oncol. 2012;10:109.

    Article  PubMed Central  PubMed  Google Scholar 

  16. 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(3):294–8.

    Article  PubMed  Google Scholar 

  17. 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(14 Pt 1):4244–50.

    Article  CAS  PubMed  Google Scholar 

  18. 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(13):1486–91.

    PubMed  Google Scholar 

  19. Gao P, Song YX, Xu YY, et al. Does the prognosis of colorectal mucinous carcinoma depend upon the primary tumour site? Results from two independent databases. Histopathology. 2013;63(5):603–15.

    PubMed  Google Scholar 

  20. Kaw LL Jr, Punzalan CK, Crisostomo AC, et al. Surgical pathology of colorectal cancer in Filipinos: implications for clinical practice. J Am Coll Surg. 2002;195(2):188–95.

    Article  PubMed  Google Scholar 

  21. Thomas RM, Sobin LH. Gastrointestinal cancer. Cancer. 1995;75(1 Suppl):154–70.

    Article  CAS  PubMed  Google Scholar 

  22. Kang H, 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(6):1161–8.

    Article  PubMed  Google Scholar 

  23. 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(4):1109–15.

    Article  PubMed  Google Scholar 

  24. Morikawa T, Kuchiba A, Qian ZR, et al. Prognostic significance and molecular associations of tumor growth pattern in colorectal cancer. Ann Surg Oncol. 2012;19(6):1944–53.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Engeland A, Tretli S, Austad G, et al. Height and body mass index in relation to colorectal and gallbladder cancer in two million Norwegian men and women. Cancer Causes Control. 2005;16(8):987–96.

    Article  PubMed  Google Scholar 

  26. Erichsen R, Baron JA, Stoffel EM, et al. Characteristics and survival of interval and sporadic colorectal cancer patients: a nationwide population-based cohort study. Am J Gastroenterol. 2013;108(8):1332–40.

    Article  PubMed  Google Scholar 

  27. Nitsche U, Zimmermann A, Spath C, et al. Mucinous and signet-ring cell colorectal cancers differ from classical adenocarcinomas in tumor biology and prognosis. Ann Surg. 2013;258(5):775–83.

    Article  PubMed Central  PubMed  Google Scholar 

  28. Papadopoulos VN, Michalopoulos A, Netta S, et al. Prognostic significance of mucinous component in colorectal carcinoma. Tech Coloproctol. 2004;8(Suppl 1):s123–5.

    Article  PubMed  Google Scholar 

  29. Benatti P, Gafa R, Barana D, et al. Microsatellite instability and colorectal cancer prognosis. Clin Cancer Res. 2005;11(23):8332–40.

    Article  CAS  PubMed  Google Scholar 

  30. Safaee A, Moghimi-Dehkordi B, Fatemi SR, et al. Characteristics of colorectal mucinous adenocarcinoma in Iran. Asian Pac J Cancer Prev. 2010;11(5):1373–5.

    PubMed  Google Scholar 

  31. Veruttipong D, Soliman AS, Gilbert SF, et al. Age distribution, polyps and rectal cancer in the Egyptian population-based cancer registry. World J Gastroenterol. 2012;18(30):3997–4003.

    Article  PubMed Central  PubMed  Google Scholar 

  32. Day FL, Jorissen RN, Lipton L, et al. PIK3CA and PTEN gene and exon mutation-specific clinicopathologic and molecular associations in colorectal cancer. Clin Cancer Res. 2013;19(12):3285–96.

    Article  CAS  PubMed  Google Scholar 

  33. Bray F, Ren JS, Masuyer E, et al. Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer. 2013;132(5):1133–45.

    Article  CAS  PubMed  Google Scholar 

  34. Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut. 2001;48(4):526–35.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Lutgens MW, van Oijen MG, van der Heijden GJ, et al. Declining risk of colorectal cancer in inflammatory bowel disease: an updated meta-analysis of population-based cohort studies. Inflamm Bowel Dis. 2013;19(4):789–99.

    Article  PubMed  Google Scholar 

  36. Gyde SN, Prior P, Macartney JC, et al. Malignancy in Crohn’s disease. Gut. 1980;21(12):1024–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Savoca PE, Ballantyne GH, Cahow CE. Gastrointestinal malignancies in Crohn’s disease. A 20-year experience. Dis Colon Rectum. 1990;33(1):7–11.

    Article  CAS  PubMed  Google Scholar 

  38. Sugita A, Greenstein AJ, Ribeiro MB, et al. Survival with colorectal cancer in ulcerative colitis. A study of 102 cases. Ann Surg. 1993;218(2):189–95.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Choi PM, Zelig MP. Similarity of colorectal cancer in Crohn’s disease and ulcerative colitis: implications for carcinogenesis and prevention. Gut. 1994;35(7):950–4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Connell WR, Talbot IC, Harpaz N, et al. Clinicopathological characteristics of colorectal carcinoma complicating ulcerative colitis. Gut. 1994;35(10):1419–23.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Rubio CA, Befrits R. Colorectal adenocarcinoma in Crohn’s disease: a retrospective histologic study. Dis Colon Rectum. 1997;40(9):1072–8.

    Article  CAS  PubMed  Google Scholar 

  42. Mayer R, Wong WD, Rothenberger DA, et al. Colorectal cancer in inflammatory bowel disease: a continuing problem. Dis Colon Rectum. 1999;42(3):343–7.

    Article  CAS  PubMed  Google Scholar 

  43. Svrcek M, Cosnes J, Beaugerie L, et al. Colorectal neoplasia in Crohn’s colitis: a retrospective comparative study with ulcerative colitis. Histopathology. 2007;50(5):574–83.

    Article  CAS  PubMed  Google Scholar 

  44. Brackmann S, Andersen SN, Aamodt G, et al. Two distinct groups of colorectal cancer in inflammatory bowel disease. Inflamm Bowel Dis. 2009;15(1):9–16.

    Article  PubMed  Google Scholar 

  45. Higashi D, Futami K, Ishibashi Y, et al. Clinical course of colorectal cancer in patients with ulcerative colitis. Anticancer Res. 2011;31(7):2499–504.

    PubMed  Google Scholar 

  46. Watanabe T, Konishi T, Kishimoto J, et al. Ulcerative colitis-associated colorectal cancer shows a poorer survival than sporadic colorectal cancer: a nationwide Japanese study. Inflamm Bowel Dis. 2011;17(3):802–8.

    Article  PubMed  Google Scholar 

  47. Hussain SP, Amstad P, Raja K, et al. Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: a cancer-prone chronic inflammatory disease. Cancer Res. 2000;60(13):3333–7.

    CAS  PubMed  Google Scholar 

  48. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883–99.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Gasche C, Chang CL, Rhees J, et al. Oxidative stress increases frameshift mutations in human colorectal cancer cells. Cancer Res. 2001;61(20):7444–8.

    CAS  PubMed  Google Scholar 

  50. Aust DE, Terdiman JP, Willenbucher RF, et al. The APC/beta-catenin pathway in ulcerative colitis-related colorectal carcinomas: a mutational analysis. Cancer. 2002;94(5):1421–7.

    Article  CAS  PubMed  Google Scholar 

  51. Sanchez JA, Dejulius KL, Bronner M, et al. Relative role of methylator and tumor suppressor pathways in ulcerative colitis-associated colon cancer. Inflamm Bowel Dis. 2011;17(9):1966–70.

    Article  PubMed  Google Scholar 

  52. Brentnall TA, Crispin DA, Rabinovitch PS, et al. Mutations in the p53 gene: an early marker of neoplastic progression in ulcerative colitis. Gastroenterology. 1994;107(2):369–78.

    CAS  PubMed  Google Scholar 

  53. Zhang H, Evertsson S, Sun X. Clinicopathological and genetic characteristics of mucinous carcinomas in the colorectum. Int J Oncol. 1999;14(6):1057–61.

    CAS  PubMed  Google Scholar 

  54. 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(9):1275–83.

    Article  PubMed  Google Scholar 

  55. Hanski C, Bornhoeft G, Shimoda T, et al. Expression of p53 protein in invasive colorectal carcinomas of different histologic types. Cancer. 1992;70(12):2772–7.

    Article  CAS  PubMed  Google Scholar 

  56. Brentnall TA, Crispin DA, Bronner MP, et al. Microsatellite instability in nonneoplastic mucosa from patients with chronic ulcerative colitis. Cancer Res. 1996;56(6):1237–40.

    CAS  PubMed  Google Scholar 

  57. Edwards RA, Witherspoon M, Wang K, et al. Epigenetic repression of DNA mismatch repair by inflammation and hypoxia in inflammatory bowel disease-associated colorectal cancer. Cancer Res. 2009;69(16):6423–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Chang CL, Marra G, Chauhan DP, et al. Oxidative stress inactivates the human DNA mismatch repair system. Am J Physiol Cell Physiol. 2002;283(1):C148–54.

    Article  CAS  PubMed  Google Scholar 

  59. Iwashita J, Sato Y, Sugaya H, et al. mRNA of MUC2 is stimulated by IL-4, IL-13 or TNF-alpha through a mitogen-activated protein kinase pathway in human colon cancer cells. Immunol Cell Biol. 2003;81(4):275–82.

    Article  CAS  PubMed  Google Scholar 

  60. Okudaira K, Kakar S, Cun L, et al. MUC2 gene promoter methylation in mucinous and non-mucinous colorectal cancer tissues. Int J Oncol. 2010;36(4):765–75.

    CAS  PubMed  Google Scholar 

  61. Ng SC, Bernstein CN, Vatn MH, et al. Geographical variability and environmental risk factors in inflammatory bowel disease. Gut. 2013;62(4):630–49.

    Article  PubMed  Google Scholar 

  62. Kountouras J, Zavos C. Recent advances in the management of radiation colitis. World J Gastroenterol. 2008;14(48):7289–301.

    Article  PubMed Central  PubMed  Google Scholar 

  63. Slaughter DP, Southwick HW. Mucosal carcinomas as a result of irradiation. AMA Arch Surg. 1957;74(3):420–9.

    Article  CAS  PubMed  Google Scholar 

  64. Smith J. Carcinoma of the rectum following irradiation of carcinoma of the cervix. Proc R Soc Med. 1962;55:701–2.

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Black WC 3rd, Ackerman LV. Carcinoma of the large intestine as a late complication of pelvic radiotherapy. Clin Radiol. 1965;16:278–81.

    Article  PubMed  Google Scholar 

  66. Pemberton M, Lendrum J. Squamous-cell carcinoma of the caecum following ovarian adenocarcinoma. Br J Surg. 1968;55(4):273–6.

    Article  CAS  PubMed  Google Scholar 

  67. DeCosse JJ, Rhodes RS, Wentz WB, et al. The natural history and management of radiation induced injury of the gastrointestinal tract. Ann Surg. 1969;170(3):369–84.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Localio SA, Stone A, Friedman M. Surgical aspects of radiation enteritis. Surg Gynecol Obstet. 1969;129(6):1163–72.

    CAS  PubMed  Google Scholar 

  69. MacMahon CE, Rowe JW. Rectal reaction following radiation therapy of cervical carcinoma: particular reference to subsequent occurrence of rectal carcinoma. Ann Surg. 1971;173(2):264–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  70. Castro EB, Rosen PP, Quan SH. Carcinoma of large intestine in patients irradiated for carcinoma of cervix and uterus. Cancer. 1973;31(1):45–52.

    Article  CAS  PubMed  Google Scholar 

  71. Cunningham MP, Wilhoite R. Radiation-induced carcinoma of the transverse colon: report of a case. Dis Colon Rectum. 1973;16(2):145–8.

    Article  CAS  PubMed  Google Scholar 

  72. Qizilbash AH. Radiation-induced carcinoma of the rectum. A late complication of pelvic irradiation. Arch Pathol. 1974;98(2):118–21.

    CAS  PubMed  Google Scholar 

  73. Burri B, Mosimann R. A propos de quatre tumeurs malignes colo-rectales et du péritoine apparues après irradiation pelvienne. Helv Chir Acta. 1978;45:101–4.

    CAS  PubMed  Google Scholar 

  74. Greenwald R, Barkin JS, Hensley GT, et al. Cancer of the colon as a late sequel of pelvic irradiation. Am J Gastroenterol. 1978;69(2):196–8.

    CAS  PubMed  Google Scholar 

  75. O’Connor TW, Rombeau JL, Levine HS, et al. Late development of colorectal cancer subsequent to pelvic irradiation. Dis Colon Rectum. 1979;22(2):123–8.

    Article  PubMed  Google Scholar 

  76. Sabio H, Teja K, Elkon D, et al. Adenocarcinoma of the colon following the treatment of Wilms tumor. J Pediatr. 1979;95(3):424–6.

    Article  CAS  PubMed  Google Scholar 

  77. Martins A, Sternberg SS, Attiyeh FF. Radiation-induced carcinoma of the rectum. Dis Colon Rectum. 1980;23(8):572–5.

    Article  CAS  PubMed  Google Scholar 

  78. Tan BC, Chia KB. Radiation induced cancer: a report of ten cases. Ann Acad Med Singapore. 1981;10(3):267–76.

    CAS  PubMed  Google Scholar 

  79. Jao SW, Beart RW Jr, Reiman HM, et al. Colon and anorectal cancer after pelvic irradiation. Dis Colon Rectum. 1987;30(12):953–8.

    Article  CAS  PubMed  Google Scholar 

  80. Hareyama M, Okubo O, Oouchi A, et al. A case of carcinoma of the rectum after radiotherapy for carcinoma of the cervix. Radiat Med. 1989;7(4):197–200.

    CAS  PubMed  Google Scholar 

  81. Levitt MD, Millar DM, Stewart JO. Rectal cancer after pelvic irradiation. J R Soc Med. 1990;83(3):152–4.

    CAS  PubMed Central  PubMed  Google Scholar 

  82. Shirouzu K, Isomoto H, Morodomi T, et al. Clinicopathologic characteristics of large bowel cancer developing after radiotherapy for uterine cervical cancer. Dis Colon Rectum. 1994;37(12):1245–9.

    Article  CAS  PubMed  Google Scholar 

  83. Kimura T, Iwagaki H, Hizuta A, et al. Colorectal cancer after irradiation for cervical cancer–case reports. Anticancer Res. 1995;15(2):557–8.

    CAS  PubMed  Google Scholar 

  84. Morita H, Koyama N, Tamura Y. Development of flat adenoma and superficial rectal cancer after pelvic radiation. J Clin Gastroenterol. 1998;26(3):171–4.

    Article  CAS  PubMed  Google Scholar 

  85. Minami K, Matsuzaki S, Hayashi N, et al. Immunohistochemical study of p53 overexpression in radiation-induced colon cancers. J Radiat Res. 1998;39(1):1–10.

    Article  CAS  PubMed  Google Scholar 

  86. Tamai O, Nozato E, Miyazato H, et al. Radiation-associated rectal cancer: report of four cases. Dig Surg. 1999;16(3):238–43.

    Article  CAS  PubMed  Google Scholar 

  87. Nakao A, Iwagaki H, Yoshino T, et al. Immunohistochemical studies of colorectal cancers that developed following pelvic irradiation. Surg Today. 2000;30(2):117–21.

    Article  CAS  PubMed  Google Scholar 

  88. Yokoyama S, Takifuji K, Arii K, et al. Radiation-induced rectal cancer originating from a rectocutaneous fistula: report of a case. Surg Today. 2004;34(8):706–9.

    Article  PubMed  Google Scholar 

  89. Denman DL, Kirchner FR, Osborne JW. Induction of colonic adenocarcinoma in the rat by X-irradiation. Cancer Res. 1978;38(7):1899–905.

    CAS  PubMed  Google Scholar 

  90. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.

    Article  CAS  PubMed  Google Scholar 

  91. Shamsuddin AK, Elias EG. Rectal mucosa. Malignant and premalignant changes after radiation therapy. Arch Pathol Lab Med. 1981;105(3):150–1.

    CAS  PubMed  Google Scholar 

  92. Asayama N, Ikehara H, Yano H, et al. Endoscopic submucosal dissection of multiple flat adenomas in the radiated rectum. World J Gastrointest Endosc. 2013;5(3):128–31.

    Article  PubMed Central  PubMed  Google Scholar 

  93. Bourguignon MH, Gisone PA, Perez MR, et al. Genetic and epigenetic features in radiation sensitivity Part I: cell signalling in radiation response. Eur J Nucl Med Mol Imaging. 2005;32(2):229–46.

    Article  PubMed  Google Scholar 

  94. Sharp C, Cox R. Genetic susceptibility to radiation effects: possible implication for medical ionising radiation exposures. Eur J Nucl Med. 1999;26(4):425–8.

    Article  CAS  PubMed  Google Scholar 

  95. Nakatsuka H, Shimizu Y, Yamamoto T, et al. Colorectal cancer incidence among atomic bomb survivors, 1950–80. J Radiat Res. 1992;33(4):342–61.

    Article  CAS  PubMed  Google Scholar 

  96. Babior BM. Oxygen-dependent microbial killing by phagocytes (second of two parts). N Engl J Med. 1978;298(13):721–5.

    Article  CAS  PubMed  Google Scholar 

  97. Valko M, Rhodes CJ, Moncol J, et al. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact. 2006;160(1):1–40.

    Article  CAS  PubMed  Google Scholar 

  98. Troll W, Wiesner R. The role of oxygen radicals as a possible mechanism of tumor promotion. Annu Rev Pharmacol Toxicol. 1985;25:509–28.

    Article  CAS  PubMed  Google Scholar 

  99. Feinendegen LE. Evidence for beneficial low level radiation effects and radiation hormesis. Br J Radiol. 2005;78(925):3–7.

    Article  CAS  PubMed  Google Scholar 

  100. Haton C, Francois A, Vandamme M, et al. Imbalance of the antioxidant network of mouse small intestinal mucosa after radiation exposure. Radiat Res. 2007;167(4):445–53.

    Article  CAS  PubMed  Google Scholar 

  101. Morgan WF. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res. 2003;159(5):567–80.

    Article  CAS  PubMed  Google Scholar 

  102. Prise KM, O’Sullivan JM. Radiation-induced bystander signalling in cancer therapy. Nat Rev Cancer. 2009;9(5):351–60.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  103. Lyng FM, Seymour CB, Mothersill C. Production of a signal by irradiated cells which leads to a response in unirradiated cells characteristic of initiation of apoptosis. Br J Cancer. 2000;83(9):1223–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  104. Morgan WF, Hartmann A, Limoli CL, et al. Bystander effects in radiation-induced genomic instability. Mutat Res. 2002;504(1–2):91–100.

    Article  CAS  PubMed  Google Scholar 

  105. Lewis DA, Mayhugh BM, Qin Y, et al. Production of delayed death and neoplastic transformation in CGL1 cells by radiation-induced bystander effects. Radiat Res. 2001;156(3):251–8.

    Article  CAS  PubMed  Google Scholar 

  106. Kruidenier L, Kuiper I, Van Duijn W, et al. Imbalanced secondary mucosal antioxidant response in inflammatory bowel disease. J Pathol. 2003;201(1):17–27.

    Article  CAS  PubMed  Google Scholar 

  107. Indaram AV, Visvalingam V, Locke M, et al. Mucosal cytokine production in radiation-induced proctosigmoiditis compared with inflammatory bowel disease. Am J Gastroenterol. 2000;95(5):1221–5.

    Article  CAS  PubMed  Google Scholar 

  108. Stoffel E, Mukherjee B, Raymond VM, et al. Calculation of risk of colorectal and endometrial cancer among patients with Lynch syndrome. Gastroenterology. 2009;137(5):1621–7.

    Article  PubMed Central  PubMed  Google Scholar 

  109. Boland CR, Goel A. Microsatellite instability in colorectal cancer. Gastroenterology. 2010;138(6):2073–87 e3.

    Google Scholar 

  110. Jass JR, Cottier DS, Jeevaratnam P, et al. Diagnostic use of microsatellite instability in hereditary non-polyposis colorectal cancer. Lancet. 1995;346(8984):1200–1.

    Article  CAS  PubMed  Google Scholar 

  111. Young J, Simms LA, Biden KG, et al. Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis. Am J Pathol. 2001;159(6):2107–16.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  112. Shia J, Ellis NA, Paty PB, et al. Value of histopathology in predicting microsatellite instability in hereditary nonpolyposis colorectal cancer and sporadic colorectal cancer. Am J Surg Pathol. 2003;27(11):1407–17.

    Article  PubMed  Google Scholar 

  113. Valle L, Perea J, Carbonell P, et al. Clinicopathologic and pedigree differences in Amsterdam I-positive hereditary nonpolyposis colorectal cancer families according to tumor microsatellite instability status. J Clin Oncol. 2007;25(7):781–6.

    Article  CAS  PubMed  Google Scholar 

  114. Jin HY, Liu X, Li VK, et al. Detection of mismatch repair gene germline mutation carrier among Chinese population with colorectal cancer. BMC Cancer. 2008;8:44.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  115. Chiang JM, Yeh CY, Changchien CR, et al. Mucinous adenocarcinoma showing different clinicopathological and molecular characteristics in relation to different colorectal cancer subgroups. Int J Colorectal Dis. 2010;25(8):941–7.

    Article  CAS  PubMed  Google Scholar 

  116. Konishi M, Kikuchi-Yanoshita R, Tanaka K, et al. Molecular nature of colon tumors in hereditary nonpolyposis colon cancer, familial polyposis, and sporadic colon cancer. Gastroenterology. 1996;111(2):307–17.

    Article  CAS  PubMed  Google Scholar 

  117. 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(5):1429–39.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Surgery, Radboud University Medical Center, HB, Nijmegen, The Netherlands

    Niek Hugen MD & Johannes H. W. de Wilt MD

  2. Department of Pathology, Radboud University Medical Center, HB, Nijmegen, The Netherlands

    Jasper J. P. van Beek BSc & Iris D. Nagtegaal MD

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  1. Niek Hugen MD
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Hugen, N., van Beek, J.J.P., de Wilt, J.H.W. et al. Insight into Mucinous Colorectal Carcinoma: Clues from Etiology. Ann Surg Oncol 21, 2963–2970 (2014). https://doi.org/10.1245/s10434-014-3706-6

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