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Large bowel cancer in the setting of inflammatory bowel disease

Features and management with a focus on rectal cancer

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Summary

Background

Inflammatory bowel diseases (IBDs) are a well-known risk factor for the development of colorectal cancer (CRC). This risk relates to different aspects of the disease, such as the duration, activity, and extension, and tends to increase in the presence of associated conditions, such as family history of CRC or some extra-intestinal manifestations. Rectal cancer (RC) in IBD has been poorly investigated.

Methods

We reviewed the scientific literature for data on the features and management of RC in the setting of IBD. Here, we provide a practical insight into the diagnosis and management of the condition.

Results

Several genetic and environmental factors promote the development of CRC, including alterations of intestinal microflora and mutations in the genes responsible for the cell cycle and for DNA mismatch repair. Dysplasia is the main evidence of a clear conversion of normal epithelium to cancer. Dysplasia is often multifocal, in contrast to sporadic CRC, which explains the tendency toward the development of synchronous and metachronous CRC in patients with IBD. Other conditions that need attention are strictures, for which the threshold for surgery must be low. Treatment of RC in patients with IBD follows the same oncologic criteria as non-IBD-related RC, but patients are often diagnosed at more advanced stages, suggesting that this is frequently overlooked. This is ultimately associated with poorer outcomes in IBD patients.

Conclusion

There is a pressing need for more data on IBD-related RC. Implementing knowledge will result in optimization of survival for these patients.

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Abbreviations

5-ASA:

5-aminosalicylic acid

APE:

Abdominoperineal excision

CCFA:

Crohn’s and Colitis Foundation of America

CD:

Crohn’s disease

CI:

Confidence intervals

CIN:

Chromosomal instability

COX-2:

Cyclo-oxygenase-2

CRC:

Colorectal cancer

DALM:

Dysplasia-associated lesion or mass

FAP:

Familial adenomatous polyposis

HGD:

High-grade dysplasia

HNPCC:

Hereditary non-polyposis colorectal cancer syndrome

IBD:

Inflammatory bowel disease

IPAA:

Ileal pouch–anal anastomosis

LGD:

Low-grade dysplasia

MSI:

Micro satellites instability

NOS:

Nitric oxide synthase

OR:

Odds ratio

PSC:

Primary sclerosing cholangitis

RC:

Rectal cancer

RONS:

Reactive oxygen and nitrogen species

SIR:

Standardized incidence ratio

UC:

Ulcerative colitis

References

  1. Kulaylat MN, Dayton MT. Ulcerative colitis and cancer. J Surg Oncol. 2010;101:706–12.

    Article  PubMed  Google Scholar 

  2. Jess T, Loftus EV, Velayos FS, Harmsen WS, Zinsmeister AR, Smyrk TC, Schleck CD, Tremaine WJ, Melton LJ, Munkholm P, et al. Risk of intestinal cancer in inflammatory bowel disease:a population-based study from olmsted county,Minnesota. Gastroenterology. 2006;130:1039–46.

    Article  PubMed  Google Scholar 

  3. Sebastian S, Hernández V, Myrelid P, Kariv R, Tsianos E, Toruner M, Marti-Gallostra M, Spinelli A, Meulen-de Jong AE van der, Yuksel ES, Gasche C, Ardizzone S, Danese S. Colorectal cancer in inflammatory bowel disease: results of the 3rd ECCO pathogenesis scientific workshop (I). J Crohns Colitis. 2014;8(1):5–18.

    Article  PubMed  Google Scholar 

  4. Egan L, D’Inca R, Jess T, Pellino G, Carbonnel F, Bokemeyer B, Harbord M, Nunes P, Van der Woude J, Selvaggi F, Triantafillidis J. Non-colorectal intestinal tract carcinomas in inflammatory bowel disease: results of the 3rd ECCO Pathogenesis Scientific Workshop (II). J Crohns Colitis. 2014;8(1):19–30.

    Article  PubMed  Google Scholar 

  5. Selvaggi F, Pellino G, Canonico S, Sciaudone G. Systematic review of cuff and pouch cancer in patients with ileal pelvic pouch for ulcerative colitis. Inflamm Bowel Dis. 2014;20(7):1296–308.

    Article  PubMed  Google Scholar 

  6. Gyde SN, Prior O, Allan RN, et al. Colorectal cancer in ulcerative colitis:a cohort study of primary referrals from three centres. Gut. 1988;29:206–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Eaden J. Review article: colorectal carcinoma and inflammatory bowel disease. Aliment Pharmacol Ther. 2004;20:24–30.

    Article  PubMed  Google Scholar 

  8. Rutter MD, Saunders BP, Wilkinson KH, Rumbles S, Schofield G, Kamm MA, Williams CB, Price AB, Talbot IC, Forbes A. Thirty-year analysis ofa colonoscopic surveillance program for neoplasia in ulcerative colitis. Gastroenterology. 2006;130:1030–8.

    Article  PubMed  Google Scholar 

  9. Lakatos L, Mester G, Erdelyi Z, David G, Pandur T, Balogh M, Fischer S, Vargha P, Lakatos PL. Risk factors for ulcerative colitis-associated colorectal cancer ina Hungarian cohort of patients with ulcerative colitis: results ofa population-based study. Inflamm Bowel Dis. 2006;12:205–11.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kim BJ, Yang SK, Kim JS, Jeen YT, Choi H, Han DS, Kim HJ, Kim WH, Kim JY, Chang DK. Trends of ulcerative colitis-associated colorectal cancer in Korea: A KASID study. J Gastroenterol Hepatol. 2009;24:667–71.

    Article  PubMed  Google Scholar 

  12. Söderlund S, Brandt L, Lapidus A, Karlén P, Broström O, Löfberg R, Ekbom A, Askling J. Decreasing time-trends of colorectal cancer ina large cohort of patients with inflammatory bowel disease. Gastroenterology. 2009;136:1561–1157, quiz 1818–9.

    Article  PubMed  Google Scholar 

  13. Jess T, Horváth-Puhó E, Fallingborg J, Rasmussen HH, Jacobsen BA. Cancer risk in inflammatory bowel disease according to patient phenotype and treatment:a Danish population-based cohort study. Am J Gastroenterol. 2013;108:1869–76.

    Article  CAS  PubMed  Google Scholar 

  14. Potack J, Itzkowitz SH. Colorectal Cancer in Inflammatory Bowel Disease. Gut Liver. 2008;2:61–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ekbom A, Helmick C, Zack M, Adami HO. Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med. 1990;323:1228–33.

    Article  CAS  PubMed  Google Scholar 

  16. Gupta RB, Harpaz N, Itzkowitz S, Hossain S, Matula S, Kornbluth A, Bodian C, Ullman T. Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study. Gastroenterology. 2007;133:1099–105.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Smith MP, Loe RH. Sclerosing cholangitis. Review of recent case reports and associated diseases and four new cases. Am J Surg. 1965;110:239–46.

    CAS  PubMed  Google Scholar 

  18. Askling J, Dickman PW, Karlén P, Broström O, Lapidus A, Löfberg R, Ekbom A. Colorectal cancer rates among first-degree relatives of patients with inflammatory bowel disease:a population-based cohort study. Lancet. 2001;357:262–6.

    Article  CAS  PubMed  Google Scholar 

  19. Velayos FS, Loftus EV, Jess T, Harmsen WS, Bida J, Zinsmeister AR, Tremaine WJ, Sandborn WJ. Predictive and protective factors associated with colorectal cancer in ulcerative colitis: a case-control study. Gastroenterology. 2006;130:1941–9.

    Article  PubMed  Google Scholar 

  20. Ekbom A, Helmick C, Zack M, Adami HO. Increased risk of large-bowel cancer in Crohn’s disease with colonic involvement. Lancet. 1990;336:357–9.

    Article  CAS  PubMed  Google Scholar 

  21. Jess T, Winther KV, Munkholm P, Langholz E, Binder V. Intestinal and extra-intestinal cancer in Crohn’s disease: follow-up of a population-based cohort in Copenhagen County, Denmark. Aliment Pharmacol Ther. 2004;19:287–93.

    Google Scholar 

  22. Jess T, Gamborg M, Matzen P, Munkholm P, Sørensen TI. Increased risk of intestinal cancer in Crohn’s disease:a meta-analysis of population-based cohort studies. Am J Gastroenterol. 2005;100:2724–9.

    Article  PubMed  Google Scholar 

  23. Friedman S, Rubin PH, Bodian C, Harpaz N, Present DH. Screening and surveillance colonoscopy in chronic Crohn’s colitis: results ofa surveillance program spanning 25 years. Clin Gastroenterol Hepatol. 2008;6:993–8.

    Article  PubMed  Google Scholar 

  24. Canavan C, Abrams KR, Meta-analysis MJ. colorectal and small bowel cancer risk in patients with Crohn’s disease. Aliment Pharmacol Ther. 2006;23:1097–104.

    Article  CAS  PubMed  Google Scholar 

  25. Roon AC von, Reese G, Teare J, Constantinides V, Darzi AW, Tekkis PP. The risk of cancer in patients with Crohn’s disease. Dis Colon Rectum. 2007;50:839–55.

    Article  Google Scholar 

  26. Laukoetter MG, Mennigen R, Hannig CM, et al. Intestinal cancer risk in Crohn’s disease:a meta-analysis. J Gastrointest Surg. 2011;15:576–83.

    Article  PubMed  Google Scholar 

  27. Selvaggi F, Pellino G. Pouch-related fistula and intraoperative tricks to prevent it. Tech Coloproctol. 2015;19:63–7.

    Article  CAS  PubMed  Google Scholar 

  28. Söderlund S, Granath F, Broström O, Karlén P, Löfberg R, Ekbom A, et al. Inflammatory bowel disease confersa lower risk of colorectal cancer to females than males. Gastroenterology. 2010;138((5):1697–703.

    Article  PubMed  Google Scholar 

  29. Gillen CD, Walmsley RS, Prior P, Andrews HA, Allan RN. Ulcerative colitis and Crohn’s disease:a comparison of the colorectal cancer risk in extensive colitis. Gut. 1994;35:1590–2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Canavan C, Abrams KR, Mayberry J. Meta-analysis: colorectal and small bowel cancer risk in patients with Crohn’s disease. Aliment Pharmacol Ther. 2006;23:1097–104.

    Article  CAS  PubMed  Google Scholar 

  31. Stahl TJ, Schoetz DJ, Roberts PL, et al. Crohn’s disease and carcinoma: Increasing justification for surveillance? Dis Colon Rectum. 1992;35:850–6.

    Article  CAS  PubMed  Google Scholar 

  32. Greenstein AJ, Sachar D, Pucillo A, Kreel I, Geller S, Janowitz HD, Aufses A Jr. Cancer in Crohn’s disease after diversionary surgery. A report of seven carcinomas occurring in excluded bowel. Am J Surg. 1978;135:86–90.

    CAS  PubMed  Google Scholar 

  33. Connell WR, Sheffield JP, Kamm MA, Ritchie JK, Hawley PR, Lennard-Jones JE. Lower gastrointestinal malignancy in Crohn’s disease. Gut. 1994;35:347–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lovasz BD, Lakatos L, Golovics PA, David G, Pandur T, Erdelyi Z, et al. Risk of colorectal cancer in Crohn’s disease patients with colonic involvement and stenosing disease in a population-based cohort from Hungary. J Gastrointestin Liver Dis. 2013;22(3):265–8.

    PubMed  Google Scholar 

  35. Hamilton SR. Colorectal carcinoma in patients with Crohn’s disease. Gastroenterology. 1985;89:398–407.

    Article  CAS  PubMed  Google Scholar 

  36. Triantafillidis JK, Nasioulas G, Kosmidis PA. Colorectal cancer and inflammatory bowel disease: epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. Anticancer Res. 2009;29:2727–37.

    PubMed  Google Scholar 

  37. Kraus S, Arber N. Inflammation and colorectal cancer. Curr Opin Pharmacol. 2009;9:405–10.

    Article  CAS  PubMed  Google Scholar 

  38. Green S, Stock RG, Greenstein AJ. Rectal cancer and inflammatory bowel disease: natural history and implication for radiation therapy. Int J Radiol Oncol Biol Phys. 1999;44:835–40.

    Article  CAS  Google Scholar 

  39. Ullman TA, Itzkowitz SH. Intestinal inflammation and cancer. Gastroenterology. 2011;140:1807–16.

    Article  CAS  PubMed  Google Scholar 

  40. Slater G, Greenstein A, Aufses AH Jr.. Anal carcinoma in patients with Crohn’s disease. Ann Surg. 1984;199:348–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Befrits R, Hammarberg C, Rubio C, Jaramillo E, Tribukait B. DNA aneuploidy and histologic dysplasia in long-standing ulcerative colitis. A 10-year follow-up study. Dis Colon Rectum. 1994;37:313–9, discussion 319-320.

    Article  CAS  PubMed  Google Scholar 

  42. Willenbucher RF, Zelman SJ, Ferrell LD, Moore DH, Waldman FM. Chromosomal alterations in ulcerative colitis-related neoplastic progression. Gastroenterology. 1997;113:791–801.

    Article  CAS  PubMed  Google Scholar 

  43. Lyda MH, Noffsinger A, Belli J, et al. Micro satellite instability and k‑ras mutations in patients with ulcerative colitis. Hum Pathol. 2000;31(6):655–71.

    Article  Google Scholar 

  44. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol. 2004;287(1):G7–G17.

    Article  CAS  PubMed  Google Scholar 

  45. Hardy RG, Meltzer SJ, Jankowski JA. ABC of colorectal cancer. Molecular basis for risk factors. BMJ. 2000;321:886–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lakatos PL, Lakatos L. Risk for colorectal cancer in ulcerative colitis: changes, causes and management strategies. World J Gastroenterol. 2008;14:3937–47.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Itzkowitz S. Colon carcinogenesis in inflammatory bowel disease: applying molecular genetics to clinical practice. J Clin Gastroenterol. 2003;36:70–4, discussion S94–96.

    Article  Google Scholar 

  48. Leedham SJ, Graham TA, Oukrif D, McDonald SA, Rodriguez-Justo M, Harrison RF, et al. Clonality, founder mutations, and field cancerization in human ulcerative colitis-associated neoplasia. Gastroenterology. 2009;36(2):542–50.

    Article  Google Scholar 

  49. Fogt F, Vortemeyer AO, Goldman H, Giordano TJ, Merino MJ, Zhuang Z. Comparison of genetic alterations in colonic adenoma and ulcerative colitis-associated dysplasia and carcinoma. Hum Pathol. 1998;29(2):131–6.

    Article  CAS  PubMed  Google Scholar 

  50. Hussain SP, Amstad P, Raja K, Ambs S, Nagashima M, Bennett WP, 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 

  51. Romano M, Cuomo A, Tuccillo C, Salerno R, Rocco A, Staibano S, Mascolo M, Sciaudone G, Mucherino C, Giuliani A, Riegler G, Nardone G, Del Vecchio BC, Selvaggi F. Vascular endothelial growth factor and cyclooxygenase-2 are overexpressed in ileal pouch-anal anastomosis. Dis Colon Rectum. 2007;50(5):650–9.

    Article  PubMed  Google Scholar 

  52. Svrcek M, El-Bchiri J, Chalastanis A, Capel E, Dumont S, Buhard O, Oliveira C, Seruca R, Bossard C, Mosnier JF, et al. Specific clinical and biological features characterize inflammatory bowel disease associated colorectal cancers showing microsatellite instability. J Clin Oncol. 2007;25:4231–8.

    Article  CAS  PubMed  Google Scholar 

  53. Schulmann K, Mori Y, Croog V, Yin J, Olaru A, Sterian A, et al. Molecular phenotype of inflammatory bowel disease-associated neoplasm with microsatellite instability. Gastroenterology. 2005;129(1):74–85.

    Article  CAS  PubMed  Google Scholar 

  54. Issa JP, Ahuja N, Toyota M, Bronner MP, Brentnall TA. Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Res. 2001;61(9):3573–7.

    CAS  PubMed  Google Scholar 

  55. Fleisher AS, Esteller M, Harpaz N, Leytin A, Rashid A, Xu Y, et al. Microsatellite instability in inflammatory bowel disease-associated neoplastic lesion is associated with hypermethylation and diminished expression of DNA mismatchrepair gene, hMLH1. Cancer Res. 2000;60(17):4864–8.

    CAS  PubMed  Google Scholar 

  56. Hsieh CJ, Klump B, Holzmann K, Borchard F, Gregor M, Porschen R. Hypermethylation of the p16INK4a promoter in colectomy specimens of patients with long-standing and extensive ulcerative colitis. Cancer Res. 1998;58:3942–5.

    CAS  PubMed  Google Scholar 

  57. Azer SA. Overview of molecular pathways in inflammatory bowel disease associated with colorectal cancer development. Eur J Gastroenterol Hepatol. 2013;25:271–81.

    Article  CAS  PubMed  Google Scholar 

  58. Elzagheid A, Emaetig F, Alkikhia L, Buhmeida A, Syrjänen K, El-Faitori O, Latto M, Collan Y, Pyrhönen S. High cyclooxygenase-2 expression is associated with advanced stages in colorectal cancer. Anticancer Res. 2013;33:3137–43.

    PubMed  Google Scholar 

  59. Marnett LJ, DuBois RN. COX-2:a target for colon cancer prevention. Annu Rev Pharmacol Toxicol. 2002;42:55–80.

    Article  CAS  PubMed  Google Scholar 

  60. Atreya R, Mudter J, Finotto S, Müllberg J, Jostock T, Wirtz S, et al. Blockade of interleukin 6 trans signalling suppresses T‑cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat Med. 2000;6:583–8.

    Article  CAS  PubMed  Google Scholar 

  61. McLoughlin RM, Witowski J, Robson RL, Wilkinson TS, Hurst SM, Williams AS, et al. Interplay between IFN-gamma and IL-6 signaling governs neutrophil trafficking and apoptosis during acute inflammation. J Clin Invest. 2003;112:598–607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Li Y, Haar C de, Chen M, Deuring J, Gerrits MM, Smits R, et al. Disease-related expression of the IL6/STAT3/SOCS3 signalling pathway in ulcerative colitis and ulcerative colitis-related carcinogenesis. Gut. 2010;59(2):227–32.

    Article  PubMed  CAS  Google Scholar 

  63. Glocker EO, Kotlarz D, Boztung K, Gertz EM, Schäffer AA, Noyan F, et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med. 2009;361:2033–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Kimura H, Hokari R, Miura S, Shigematsu T, Hirokawa M, Akiba Y, Kurose I, Higuchi H, Fujimori H, Tsuzuki Y, et al. Increased expression of an inducible isoform of nitric oxide synthase and the formation of peroxynitrite in colonic mucosa of patients with active ulcerative colitis. Gut. 1998;42:180–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Rachmilewitz D, Stamler JS, Bachwich D, Karmeli F, Ackerman Z, Podolsky DK. Enhanced colonic nitric oxide generation and nitric oxide synthase activity in ulcerative colitis and Crohn’s disease. Gut. 1995;36:718–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Swidsinski A, Kilkin M, Kerjaschki D, Schreiber S, Ortner M, Weber j, et al. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology. 1998;115(2):281–6.

    Article  CAS  PubMed  Google Scholar 

  67. Darfeuille-Michaud A, Neut C, Lederman E, Di Martino P, Desreumaux P, et al. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn’s disease. Gastroenterology. 1998;115(6):1405–13.

    Article  CAS  PubMed  Google Scholar 

  68. Riddell RH. Premalignant and early malignant lesions in the gastrointestinal tract. Definitions, terminology, and problems. Am J Gastroenterol. 1996;91:864–72.

    CAS  PubMed  Google Scholar 

  69. Lim CH, Dixon MF, Vail A, Forman D, Lynch DA, Axon AT. Ten year follow up of ulcerative colitis patients with and without low grade dysplasia. Gut. 2003;52:1127–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Odze RD, Tomaszewski JE, Furth EE, Feldman MD, Diallo R, Poremba C, et al. Variability in the diagnosis of dysplasia in ulcerative colitis by dynamic telepathology. Oncol Rep. 2006;16:1123–9.

    PubMed  Google Scholar 

  71. Odze RD, Goldblum J, Noffsinger A, Alsaigh N, Rybicki LA, Fogt F. Interobserver variability in the diagnosis of ulcerative colitis-associated dysplasia by telepathology. Mod Pathol. 2002;15:379–86.

    Article  PubMed  Google Scholar 

  72. Rubin CE, Haggitt RC, Burmer GC, et al. DNA aneuploidy in colonic biopsies predicts future development of dysplasia in ulcerative colitis. Gastroenterology. 1992;103:1611–20.

    Article  CAS  PubMed  Google Scholar 

  73. Itzkowitz SH, Present DH. Consensus conference: Colorectal cancer screening and surveillance in inflammatory bowel disease. Inflamm Bowel Dis. 2005;11:314–21.

    Article  PubMed  Google Scholar 

  74. Bernstein CN, Shanahan F, Weinstein WM. Are we telling patients the truth about surveillance colonoscopy in ulcerative colitis? Lancet. 1994;343:71–4.

    Article  CAS  PubMed  Google Scholar 

  75. Farraye FA, Odze DR, Eaden J, Itzkowitz SH. AGA technical review on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease. Gastroenterology. 2010;138:746–74.

    Article  PubMed  Google Scholar 

  76. Thomas T, Abrams KA, Robinson RJ, et al. Meta-analysis: cancer risk of low-grade dysplasia in chronic ulcerative colitis. Aliment Pharmacol Ther. 2007;25:657–68.

    Article  CAS  PubMed  Google Scholar 

  77. Ullman T, Croog V, Harpaz N, et al. Progression of flat low-grade dysplasia to advanced neoplasia in patients with ulcerative colitis. Gastroenterology. 2003;125:1311–9.

    Article  PubMed  Google Scholar 

  78. Choi CH, Ignjatovic-Wilson A, Askari A, Lee GH, Warusavitarne J, Moorghen M, Thomas-Gibson S, Saunders BP, Rutter MD, Graham TA. Hart AL Low-grade dysplasia in ulcerative colitis: risk factors for developing high-grade dysplasia or colorectal cancer. Am J Gastroenterol. 2015;110:1461–71.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Choi CH, Rutter MD, Askari A, Lee GH, Warusavitarne J, Moorghen M, Thomas-Gibson S, Saunders BP, Graham TA, Hart AL. Forty-year analysis of colonoscopic surveillance program for neoplasia in ulcerative colitis: an updated overview. Am J Gastroenterol. 2015;110:1022–34.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Ullman TA, Croog V, Harpaz N, et al. Progression to colorectal neoplasia in ulcerative colitis: effect of 5‑aminosalicylic acid. Clin Gastroenterol Hepatol. 2008;6(11):1225–30.

    Article  CAS  PubMed  Google Scholar 

  81. Itzkowitz SH, Present DH. Consensus conference: Colorectal cancer screening and surveillance in inflammatory bowel disease. Inflamm Bowel Dis. 2005;11:314–21.

    Article  PubMed  Google Scholar 

  82. Kelly JK, Gabos S. The pathogenesis of inflammatory polyps. Dis Colon Rectum. 1987;30:251–4.

    Article  CAS  PubMed  Google Scholar 

  83. Rutter MD, Saunders BP, Wilkinson KH, Rumbles S, Schofield G, Kamm MA, Williams CB, Price AB, Talbot IC, Forbes A. Cancer surveillance in longstanding ulcerative colitis: endoscopic appearances help predict cancer risk. Gut. 2004;53:1813–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Loftus EV, Harewood GC, Loftus CG, Tremaine WJ, Harmsen WS, Zinsmeister AR, Jewell DA, Sandborn WJ. PSC-IBD: a unique form of inflammatory bowel disease associated with primary sclerosing cholangitis. Gut. 2005;54:91–6.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Soetikno RM, Lin OS, Heidenreich PA, Young HS, Blackstone MO. Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis:a meta-analysis. Gastrointest Endosc. 2002;56:48–54.

    Article  PubMed  Google Scholar 

  86. Kornfeld D, Ekbom A, Ihre T. Is there an excess risk for colorectal cancer in patients with ulcerative colitis and concomitant primary sclerosing cholangitis? A population based study. Gut. 1997;41:522–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Sokol H, Cosnes J, Chazouilleres O, Beaugerie L, Tiret E, Poupon R, Seksik P. Disease activity and cancer risk in inflammatory bowel disease associated with primary sclerosing cholangitis. World J Gastroenterol. 2008;14:3497–503.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Thackeray EW, Charatcharoenwitthaya P, Elfaki D, Sinakos E, Lindor KD. Colon neoplasms develop early in the course of inflammatory bowel disease and primary sclerosing cholangitis. Clin Gastroenterol Hepatol. 2011;9:52–6.

    Article  PubMed  Google Scholar 

  89. Gumaste V, Sachar DB, Greenstein AJ. Benign and malignant colorectal strictures in ulcerative colitis. Gut. 1992;33:938–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Lindström L, Lapidus A, Ost Å, Bergquist A. Increased risk of colorectal cancer and dysplasia in patients with Crohn’s colitis and primary sclerosing cholangitis. Dis Colon Rectum. 2011;54((11):1392–7.

    Article  PubMed  Google Scholar 

  91. Broden B, Halliday J, Aryasingha S, Sharifi Y, Checchin D, Warren BF, et al. Risk for colorectal neoplasia in patients with colonic Crohn’s disease and concomitant primary sclerosing cholangitis. Clin Gastroenterol Hepatol. 2012;10((3):303–8.

    Article  Google Scholar 

  92. Korelitz BI, Lauwers GY, Sommers SC. Rectal mucosal dysplasia in Crohn’s disease. Gut. 1990;12:1382–6.

    Article  Google Scholar 

  93. Igarashi T, Akimoto S, Otasiro Y, Hanyu F, Nagasako K. Precancerous lesions of the colon and rectum. Gan Kagaku Ryoho. 1989;16:1639–44.

    CAS  Google Scholar 

  94. Richards ME, Rickert RR, Nance FC. Crohn’s diseaseassociated carcinoma. A poorly recognized complication of inflammatory bowel disease. Ann Surg. 1989;209:764–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Petras RE, Mir-Madjlessi SH, Farmer RG. Crohn’s disease and intestinal carcinoma:a report of 11 cases with emphasis on associated epithelial dysplasia. Gastroenterology. 1987;93:1307–14.

    Article  CAS  PubMed  Google Scholar 

  96. Rutter MD, Saunders BP, Wilkinson KH, et al. Most dysplasia in ulcerative colitis is visible at colonoscopy. Gastrointest Endosc. 2004;60:334–9.

    Article  PubMed  Google Scholar 

  97. Engelsgjerd M, Farraye FA, Odze RD. Polypectomy may be adequate treatment for adenoma-like dysplastic lesions in chronic ulcerative colitis. Gastroenterology. 1999;117:1288–94, discussion 1488–1491.

    Article  CAS  PubMed  Google Scholar 

  98. Odze RD, Farraye FA, Hecht JL, et al. Long-term follow-up after polypectomy treatment for adenoma-like dysplastic lesions in ulcerative colitis. Clin Gastroenterol Hepatol. 2004;2:534–41.

    Article  PubMed  Google Scholar 

  99. Rubin PH, Friedman S, Harpaz N, et al. Colonoscopic polypectomy in chronic colitis: conservative management after endoscopic resection of dysplastic polyps. Gastroenterology. 1999;117:1295–300.

    Article  CAS  PubMed  Google Scholar 

  100. Winawer S, Fletcher R, Rex D, et al. Colorectal cancer screening and surveillance: clinical guidelines and rationale-update based on new evidence. Gastroenterology. 2003;124:544–60.

    Article  PubMed  Google Scholar 

  101. Kiran RP, Khoury W, Church JM, Lavery IC, Fazio VW, Remzi FH. Colorectal cancer complicating inflammatory bowel disease: similarities and differences between Crohn’s disease and ulcerative colitis based on three decades of experience. Ann Surg. 2010;252(2010):330–5.

    Article  PubMed  Google Scholar 

  102. Rieder F, Bruyn JR de, Pham BT, Katsanos K, Annese V, Higgins PD, Magro F, Dotan I. Results of the 4th scientific workshop of the ECCO (Group II): markers of intestinal fibrosis in inflammatory bowel disease. J Crohns Colitis. 2014;1;8(10):1166–78, Oct.

    Article  Google Scholar 

  103. Rieder F, Latella G, Magro F, et al. European Crohn’s and Colitis Organisation Topical Review on Prediction, Diagnosis and Management of Fibrostenosing Crohn’s Disease. J Crohns Colitis. doi:10.1093/ecco-jcc/jjw055.

  104. Winawer S, Fletcher R, Rex D, et al. Colorectal cancer screening and surveillance: clinical guidelines and rationale-update based on new evidence. Gastroenterology. 2003;124:544–60.

    Article  PubMed  Google Scholar 

  105. Pellino G, Selvaggi F. From colon-sparing techniques to pelvic ileal pouch: history and evolution of surgery for ulcerative colitis. Eur Surg. 2015;47:81–90.

    Article  Google Scholar 

  106. McLeod RS, Baxter NN. Quality of life of patients with inflammatory bowel disease after surgery. World J Surg. 1998;22:375–81.

    Article  CAS  PubMed  Google Scholar 

  107. Seidel SA, Newman M, Sharp KW. Ileoanal pouch versus ileostomy: is therea difference in quality of life? Am Surg. 2000;66:540–6.

    CAS  PubMed  Google Scholar 

  108. Feroci F, Lenzi E, Baraghini M, Cantafio S, Scatizzi M. General surgeons’ views on Oncologic Multidisciplinary Group meetings as part of colorectal cancer care. Updates Surg. 2012;64(4):273–8.

    Article  PubMed  Google Scholar 

  109. Wibe A, Syse A, Andersen E, Tretli S, Myrvold HE, Soreide O. Oncological outcomes after total mesorectal excision for cure for cancer of the lower rectum: anterior vs. abdominoperineal resection. Dis Colon Rectum. 2004;47:48–58.

    Article  PubMed  Google Scholar 

  110. Schroen AT, Cress RD. Use of surgical procedures and adjuvant therapy in rectal cancer treatment:a population-based study. Ann Surg. 2001;234:641–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Selvaggi F, Fucini C, Pellino G, Sciaudone G, Maretto I, Mondi I, Bartolini N, Caminati F, Pucciarelli S. Outcome and prognostic factors of local recurrent rectal cancer:a pooled analysis of 150 patients. Tech Coloproctol. 2015;19:135–44.

    Article  CAS  PubMed  Google Scholar 

  112. Frykholm GJ, Glimelius B, Pahlman L. Preoperative or postoperative irradiation in adenocarcinoma of the rectum: final treatment results ofa randomized trial and an evaluation of late secondary effects. Dis Colon Rectum. 1993;36:564–72.

    Article  CAS  PubMed  Google Scholar 

  113. Glimelius B, Gronberg H, Jarhult J, Wallgren A, Cavallin-Stahl E. A systematic overview of radiation therapy effects in rectal cancer. Acta Oncol. 2003;42:476–92.

    Article  PubMed  Google Scholar 

  114. Kapiteijn E, Marijnen CA, Nagtegaal ID, Putter H, Steup WH, Wiggers T, Rutten HJ, Pahlman L, Glimelius B, Krieken JH van, Leer JW, Velde CJ van de. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001;345:638–46.

    Article  CAS  PubMed  Google Scholar 

  115. Snelgrove R, Brown CJ, O’Connor BI, Huang H, Victor JC, et al. Proctocolectomy for colorectal cancer – is the ileal pouch anal anastomosisa safe alternative to permanent ileostomy? Int J Colorectal Dis. 2014;29:1485–91.

    Article  PubMed  Google Scholar 

  116. Merchea A, Wolff BG, Dozois EJ, Abdelsattar ZM, Harmsen WS, Larson DW. Clinical features and oncologic outcomes in patients with rectal cancer and ulcerative colitis:a single-institution experience. Dis Colon Rectum. 2012;55:881–5.

    Article  PubMed  Google Scholar 

  117. Gorfine SR, Harris MT, Bub DS, Bauer JJ. Restorative proctocolectomy for ulcerative colitis complicated by colorectal cancer. Dis Colon Rectum. 2004;47:1377–85.

    Article  PubMed  Google Scholar 

  118. Radice E, Nelson H, Devine RM, Dozois RR, Nivatvongs S, Pemberton JH, Wolff BG, Fozard BJ, Ilstrup D. Ileal pouchanal anastomosis in patients with colorectal cancer: long-term functional and oncologic outcomes. Dis Colon Rectum. 1998;41:11–7.

    Article  CAS  PubMed  Google Scholar 

  119. Pellino G, Selvaggi F. Outcomes of Salvage Surgery for Ileal Pouch Complications and Dysfunctions. The Experience ofa Referral Centre and Review of Literature. J Crohns Colitis. doi:10.1093/ecco-jcc/jjv066.

  120. Pellino G, Sciaudone G, Candilio G, De Fatico GS, Landino I, Canonico S, Selvaggi F. Restorative proctocolectomy with ileal pouch-anal anastomosis is safe and effective in selected very elderly patients suffering from ulcerative colitis. Int J Surg. 2014;12(Suppl 2):S56–9.

    PubMed  Google Scholar 

  121. Pellino G, Sciaudone G, Miele E, Candilio G, De Fatico GS, Riegler G, Staiano A, Canonico S, Selvaggi F. Functional outcomes and quality of life after restorative proctocolectomy in paediatric patients:a case-control study. Gastroenterol Res Pract. 2014;2014:340341 doi:10.1155/2014/340341.

    Article  PubMed  PubMed Central  Google Scholar 

  122. Selvaggi F, Pellino G, Canonico S, Sciaudone G. Is omitting pouchography before ileostomy takedown safe after negative clinical examination in asymptomatic patients with pelvic ileal pouch? An observational study. Tech Coloproctol. 2012;16:415–20.

    Article  CAS  PubMed  Google Scholar 

  123. Pellino G, Sciaudone G, Canonico S, Selvaggi F. Role of ileostomy in restorative proctocolectomy. World J Gastroenterol. 2012;18:1703–7.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Greenstein AJ. Cancer in inflammatory bowel disease. Mt Sinai J Med. 2000;67:227–40.

    CAS  PubMed  Google Scholar 

  125. Fornaro R, Secco GB, Picori E, Stabilini C, Frascio M, Ricci B, Mandolino F, De Salvo L, Gianetta E. Surgical treatment of Crohn’s disease complications. Our experience. G Chir. 2006;27:21–6.

    CAS  PubMed  Google Scholar 

  126. Fornaro R, Frascio M, Stabilini C, Sticchi C, Barberis A, Denegri A, Ricci B, Mandolino F, Lazzara F, Gianetta E. Crohn’s disease surgery: problems of postoperative recurrence. Chir Ital. 2008;60:761–81.

    PubMed  Google Scholar 

  127. Fornaro R, Frascio M, Denegri A, Stabilini C, Imperatore M, Mandolino F, Lazzara F, Gianetta E. Crohn’s disease and cancer. Ann Ital Chir. 2009;80:119–25.

    PubMed  Google Scholar 

  128. Selvaggi F, Sciaudone G, Limongelli P, Di Stazio C, Guadagni I, Pellino G, De Rosa M, Riegler G. The effect of pelvic septic complications on function and quality of life after ileal pouch-anal anastomosis:a single center experience. Am Surg. 2010;76:428–35.

    PubMed  Google Scholar 

  129. Pellino G, Sciaudone G, Selvaggi F, Riegler G. Delayed diagnosis is influenced by the clinical pattern of Crohn’s disease and affects treatment outcomes and quality of life in the long term:a cross-sectional study of 361 patients in Southern Italy. Eur J Gastroenterol Hepatol. 2015;27:175–8.

    Article  PubMed  Google Scholar 

  130. Pellino G, Selvaggi F, Ghezzi G, Corona D, Riegler G, Delaini GG. A think tank of the Italian society of colorectal surgery (SICCR) on the surgical treatment of inflammatory bowel disease using the Delphi method: Crohn’s disease. Tech Coloproctol. 2015;19(10):639–51. doi:10.1007/s10151-015-1368-4.

    Article  CAS  PubMed  Google Scholar 

  131. Selvaggi F, Pellino G, Ghezzi G, Corona D, Riegler G, Delaini GG. A think tank of the Italian Society of Colorectal Surgery (SICCR) on the surgical treatment of inflammatory bowel disease using the Delphi method: ulcerative colitis. Tech Coloproctol. 2015;19(10):627–38. doi:10.1007/s10151-015-1367-5.

    Article  CAS  PubMed  Google Scholar 

  132. Cacciola NA, Calabrese C, Malapelle U, et al. UbcH10 expression can predict prognosis and sensitivity to the antineoplastic treatment for colorectal cancer patients. Mol Carcinog. 2015;27 doi:10.1002/mc.22322.

  133. Riegler G, Bossa F, Caserta L, Pera A, Tonelli F, Sturniolo GC, Oliva L, Contessini Avesani E, Poggioli G, IG-IBD Group. Colorectal cancer and high grade dysplasia complicating ulcerative colitis in Italy. A retrospective co-operative IG-IBD study. Dig Liver Dis. 2003;35:628–34.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Francesco Selvaggi MD.

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G. Pellino, R. Marcellinaro, G. Sciaudone, A. Reginelli, P. Esposito, G. Riegler, S. Canonico, V. Villanacci, and F. Selvaggi declare that they have no competing interests.

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Pellino, G., Marcellinaro, R., Sciaudone, G. et al. Large bowel cancer in the setting of inflammatory bowel disease. Eur Surg 48, 191–202 (2016). https://doi.org/10.1007/s10353-016-0434-0

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