Risk of dysplasia and adenocarcinoma following restorative proctocolectomy for ulcerative colitis

Colorectal Disease

Volumn 9, Issue 1, 2007, Pages 15-27

  Das, P ^a   Johnson, M W ^a   Tekkis, P P ^b   Nicholls, R Johnstella ^a  

^a ST MARK S HOSPITAL   (United Kingdom)

^b ST MARY S HOSPITAL   (United Kingdom)

Author keywords

Cancer; Dysplasia; Pouchitis; Restorative proctocolectomy; Surveillance; Ulcerative colitis

Indexed keywords

ANEUPLOIDY; ANORECTAL DISEASE; CARCINOGENESIS; CELL TRANSFORMATION; CHROMOSOME 17P; CHROMOSOME 18Q; CHROMOSOME 5Q; COLON ADENOCARCINOMA; COLON BIOPSY; COLON DISEASE; COLON DYSPLASIA; COLON POUCH; COLUMNAR EPITHELIUM; CROHN DISEASE; DISEASE DURATION; DISEASE SURVEILLANCE; DYSPLASIA; ENTERITIS; FOLLOW UP; HETEROZYGOSITY LOSS; HISTOPATHOLOGY; HUMAN; ILEITIS; ILEORECTAL ANASTOMOSIS; ILEOSTOMY; ILEUM MUCOSA; LITERATURE; LYMPHOMA; MEDLINE; MORPHOGENESIS; MUCOSA INFLAMMATION; ONCOGENE K RAS; PRIORITY JOURNAL; PROCTOCOLECTOMY; REVIEW; RISK ASSESSMENT; SCLEROSING CHOLANGITIS; SQUAMOUS CELL CARCINOMA; SURGICAL RISK; SURGICAL STAPLING; TUMOR SUPPRESSOR GENE; ULCERATIVE COLITIS;

ADENOCARCINOMA; CELL TRANSFORMATION, NEOPLASTIC; COLITIS, ULCERATIVE; HUMANS; INTESTINAL MUCOSA; INTESTINAL NEOPLASMS; POSTOPERATIVE COMPLICATIONS; POUCHITIS; PROCTOCOLECTOMY, RESTORATIVE;

EID: 33845343978     PISSN: 14628910     EISSN: 14631318     Source Type: Journal    
DOI: 10.1111/j.1463-1318.2006.01148.x     Document Type: Review

References (96)

1. Veress B, Reinholt FP, Lindquist K, Lofberg R, Liljeqvist L. Long-term histomorphological surveillance of the pelvic ileal pouch: Dysplasia develops in a subgroup of patients. Gastroenterology 1995; 109: 1090-7.
2. Thompson-Fawcett MW, Marcus V, Redston M, Cohen Z, McLeod RS. Risk of dysplasia in long-term ileal pouches and pouches with chronic pouchitis. Gastroenterology 2001; 12: 275-81.
3. Tarroni D, Wilkinson KH, Saunders B, Talbot I, Nicholls RJ. Long-term histological assessment of the ileal reservoir following restorative proctocolectomy for ulcerative colitis for inflammation and dysplasia. Dis Colon Rectum 2002; 45: A7.
4. Shepherd NA, Jass JR, Duval I, Moskowitz RL, Nicholls RJ, Morson BC. Restorative proctocolectomy with ileal reservoir: Pathological and histochemical study of mucosal biopsy specimens. J Clin Pathol 1987; 40: 601-7.
5. Herbst F, Ciclitira PJ, Talbot IC, Nicholls RJ. Early changes of ileoanal pouch mucosa in patients with ulcerative colitis. Eur J Gastroenterol Hepatol 2000; 12: 899-905.
6. Goldberg PA, Talbot IC, Nicholls RJ. Ileo-anal pouch histology. Int J Colorectal Dis 1993; 8: 226.
7. Setti Carraro P, Talbot IC, Nicholls RJ. Longterm appraisal of the histological appearances of the ileal reservoir mucosa after restorative proctocolectomy for ulcerative colitis. Gut 1994; 35: 1721-7.
8. Apel R, Cohen Z, Andrews CW Jr, McLeod R, Steinhart H, Odze RD. Prospective evaluation of early morphological changes in pelvic ileal pouches [see comment]. Gastroenterology 1994; 107: 435-43.
9. Arai K, Fukushima T, Sugita A, Shimada H. Urinary changes in patients following restorative proctocolectomy. Surgery 1997; 27: 801-5.
10. Arai K, Koganei K, Kimura H, Akatani M, Kitoh F, Sugita A, Fukushima T. Incidence and outcome of complications following restorative proctocolectomy. Am J Surg 2005; 190: 39-42.
11. de Silva HJ, Millard PR, Kettlewell M, Mortensen NJ, Prince C, Jewell DP. Mucosal characteristics of pelvic ileal pouches. Gut 1991; 32: 61-5.
12. Kuisma J, Mentula S, Luukkonen P, Jarvinen H, Kahri A, Farkkila M. Factors associated with ileal mucosal morphology and inflammation in patients with ileal pouch-anal anastomosis for ulcerative colitis. Dis Colon Rectum 2003; 46: 1476-83.
13. Roediger WE. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 1982; 83: 424-9.
14. Roediger WE, Heyworth M, Willoughby P, Piris J, Moore A, Truelove SC. Luminal ions and short chain fatty acids as markers of functional activity of the mucosa in ulcerative colitis. J Clin Pathol 1982; 35: 323-6.
15. Roediger WE, Rae DA. Trophic effect of short chain fatty acids on mucosal handling of ions by the defunctioned colon. Br J Surg 1982; 69: 23-5.
16. Rolandelli RH, Koruda MJ, Settle RG, Rombeau JL. Effects of intraluminal infusion of short-chain fatty acids on the healing of colonic anastomosis in the rat. Surgery 1986; 100: 198-204.
17. Roediger WE. Anaerobic bacteria, the colon and colitis. Aust N Z J Surg 1980; 50: 73-5.
18. Shepherd NA, Hulten L, Tytgat GN et al. Pouchitis. Int J Colorectal Dis 1989; 4: 205-29.
19. Nicholls RJ, Belliveau P, Neill M, Wilks M, Tabaqchali S. Restorative proctocolectomy with ileal reservoir: A pathophysiological assessment. Gut 1981; 22: 462-8.
20. Moskowitz RL, Shepherd NA, Nicholls RJ. An assessment of inflammation in the reservoir after restorative proctocolectomy with ileoanal ileal reservoir. Int J Colorectal Dis 1986; 1: 167-74.
21. Veress B, Reinholt FP, Lindquist K, Liljeqvist L. Different types of mucosal adaptation in the ileal reservoir after restorative proctocolectomy. A two-year follow-up study. Apmis 1990; 98: 786-96.
22. Gullberg K, Lindforss U, Zetterquist H, Stalberg D, Reinholt FP, Veress B, Tribukait B, Olivecrona H, Lofberg R. Cancer risk assessment in long-standing pouchitis. DNA aberrations are rare in transformed neoplastic pelvic pouch mucosa. Int J Colorectal Dis 2002; 17: 92-7.
23. Stahlberg D, Gullberg K, Liljeqvist L, Hellers G, Lofberg R. Pouchitis following pelvic pouch operation for ulcerative colitis. Incidence, cumulative risk, and risk factors. Dis Colon Rectum 1996; 39: 1012-8.
24. Achkar JP, Al-Haddad M, Lashner B, Remzi FH, Brzezinski A, Shen B, Khandwala F, Fazio V. Differentiating risk factors for acute and chronic pouchitis. Clin Gastroenterol Hepatol 2005; 3: 60-6.
25. Lohmuller JL, Pemberton JH, Dozois RR, Ilstrup D, van Heerden J. Pouchitis and extraintestinal manifestations of inflammatory bowel disease after ileal pouch-anal anastomosis [see comment]. Ann Surg 1990; 211: 622-7; discussion: 627-9.
26. Penna C, Dozois R, Tremaine W, Sandborn W, LaRusso N, Schleck C, Ilstrup D. Pouchitis after ileal pouch-anal anastomosis for ulcerative colitis occurs with increased frequency in patients with associated primary sclerosing cholangitis. Gut 1996; 38: 234-9.
27. Aitola P, Matikainen M, Mattila J, Tomminen T, Hiltunen KM. Chronic inflammatory changes in the pouch mucosa are associated with cholangitis found on peroperative liver biopsy specimens at restorative proctocolectomy for ulcerative colitis. Scand J Gastroenterol 1998; 33: 289-93.
28. Stahlberg D, Veress B, Tribukait B, Broome U. Atrophy and neoplastic transformation of the ileal pouch mucosa in patients with ulcerative colitis and primary sclerosing cholangitis: A case control study. Dis Colon Rectum 2003; 46: 770-8.
29. Nuako KW, Ahlquist DA, Sandborn WJ, Mahoney DW, Siems DM, Zinsmeister AR. Primary sclerosing cholangitis and colorectal carcinoma in patients with chronic ulcerative colitis: A case-control study. Cancer 1998; 82: 822-6.
30. Broome U, Lofberg R, Veress B, Eriksson LS. Primary sclerosing cholangitis and ulcerative colitis: Evidence for increased neoplastic potential [see comment]. Hepatology 1995; 22: 1404-8.
31. Brentnall TA, Haggitt RC, Rabinovitch PS et al. Risk and natural history of colonic neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis [see comment]. Gastroenterology 1996; 110: 331-8.
32. Nagengast FM, Grubben MJ, van Munster IP. Role of bile acids in colorectal carcinogenesis. Eur J Cancer 1995; 31A: 1067-70.
33. Marchesa P, Lashner BA, Lavery IC, Milsom J, Hull TL, Strong SA, Church JM, Navarro G, Fazio VW. The risk of cancer and dysplasia among ulcerative colitis patients with primary sclerosing cholangitis. Am J Gastroenterol 1997; 92: 1285-8.
34. O'Connell PR, Pemberton JH, Weiland LH, Beart RW Jr, Dozois RR, Wolff BG, Telander RL. Does rectal mucosa regenerate after ileoanal anastomosis ? Dis Colon Rectum 1987; 30: 1-5.
35. Lavery IC, Sirimarco MT, Ziv Y, Fazio VW. Anal canal inflammation after ileal pouch-anal anastomosis. The need for treatment. Dis Colon Rectum 1995; 38: 803-6.
36. Thompson-Fawcett MW, Mortensen NJ, Warren BF. "Cuffitis" and inflammatory changes in the columnar cuff, anal transitional zone, and ileal reservoir after stapled pouch-anal anastomosis. Dis Colon Rectum 1999; 42: 348-55.
37. Lofberg R, Liljeqvist L, Lindquist K, Veress B, Reinholt FP, Tribukait B. Dysplasia and DNA aneuploidy in a pelvic pouch. Report of a case. Dis Colon Rectum 1991; 34: 280-3 ; discussion 283-4.
38. Hulten L, Willen R, Nilsson O, Safarani N, Haboubi N. Mucosal assessment for dysplasia and cancer in the ileal pouch mucosa in patients operated on for ulcerative colitis - a 30-year follow-up study. Dis Colon Rectum 2002; 45: 448-52.
39. Duff SE, O'Dwyer ST, Hulten L, Willen R, Haboubi NY. Dysplasia in the ileoanal pouch. Colorectal Dis 2002; 4: 420-9.
40. Herline AJ, Meisinger LL, Rusin LC, Roberts PL, Murray JJ, Coller JA, Marcello PW, Schoetz DJ. Is routine pouch surveillance for dysplasia indicated for ileoanal pouches ? Dis Colon Rectum 2003; 46: 156-9.
41. Borjesson L, Willen R, Haboubi N, Duff SE, Hulten L. The risk of dysplasia and cancer in the ileal pouch mucosa after restorative proctocolectomy for ulcerative proctocolitis is low: A long-term term follow-up study. Colorectal Dis 2004; 6: 494-8.
42. Gullberg K, Stahlberg D, Liljeqvist L, Tribukait B, Reinholt FP, Veress B, Lofberg R. Neoplastic transformation of the pelvic pouch mucosa in patients with ulcerative colitis. Gastroenterology 1997; 112: 1487-92.
43. Barrett M, Schoetz D, Semple J, Rusin L, Cohen J, Roberts P, Murray J, Coller J. Long-term risk of neoplastic changes in ileoanal pouches in patients with ulcerative colitis. Dis Colon Rectum 1998; 41: A26.
44. Seow-Choen F, Ho YH, Goh HS. The ileo-anal reservoir: Results from an evolving use of stapling devices. J R Coll Surg Edinb 1994; 39: 13-6.
45. Thompson-Fawcett MW, Warren BF, Mortensen NJ. A new look at the anal transitional zone with reference to restorative proctocolectomy and the columnar cuff. Br J Surg 1998; 85: 1517-21.
46. Tsunoda A, Talbot IC, Nicholls RJ. Incidence of dysplasia in the anorectal mucosa in patients having restorative proctocolectomy. Br J Surg 1990; 77: 506-8.
47. Ziv Y, Fazio VW, Sirimarco MT, Lavery IC, Goldblum JR, Petras RE. Incidence, risk factors, and treatment of dysplasia in the anal transitional zone after ileal pouch-anal anastomosis. Dis Colon Rectum 1994; 37: 1281-5.
48. O'Riordain MG, Fazio VW, Lavery IC, Remzi F, Fabbri N, Meneu J, Goldblum J, Petras RE. Incidence and natural history of dysplasia of the anal transitional zone after ileal pouch-anal anastomosis: Results of a five-year to ten-year follow-up. Dis Colon Rectum 2000; 43: 1660-5.
49. Remzi FH, Fazio VW, Delaney CP et al. Dysplasia of the anal transitional zone after ileal pouch-anal anastomosis: Results of prospective evaluation after a minimum of ten years. Dis Colon Rectum 2003; 46: 6-13.
50. Thompson-Fawcett MW, Rust NA, Warren BF, Mortensen NJ. Aneuploidy and columnar cuff surveillance after stapled ileal pouch-anal anastomosis in ulcerative colitis. Dis Colon Rectum 2000; 43: 408-13.
51. Coull DB, Lee FD, Henderson AP, Anderson JH, McKee RF, Finlay IG. Risk of dysplasia in the columnar cuff after stapled restorative proctocolectomy. Br J Surg 2003; 90: 72-5.
52. Haray PN, Amarnath B, Weiss EG, Nogueras JJ, Wexner SD. Low malignant potential of the double-stapled ileal pouch-anal anastomosis. Br J Surg 1996; 83: 1406.
53. Gilchrist KW, Harms BA, Starling JR. Abnormal rectal mucosa of the anal transitional zone in ulcerative colitis. Arch Surg 1995; 130: 981-3.
54. Schmitt SL, Wexner SD, Lucas FV, James K, Nogueras JJ, Jagelman DG. Retained mucosa after double-stapled ileal reservoir and ileoanal anastomosis. Dis Colon Rectum 1992; 35: 1051-6.
55. Stern H, Walfisch S, Mullen B, McLeod R, Cohen Z. Cancer in an ileoanal reservoir: A new late complication? [see comment]. Gut 1990; 31: 473-5.
56. Lee SW, Sonoda T, Milsom JW. Three cases of adenocarcinoma following restorative proctocolectomy with hand-sewn anastomosis for ulcerative colitis: A review of reported cases in the literature. Colorectal Dis 2005; 7: 591-7.
57. Rodriguez-Sanjuan JC, Polavieja MG, Naranjo A, Castillo J. Adenocarcinoma in an ileal pouch for ulcerative colitis. Dis Colon Rectum 1995; 38: 779-80.
58. Vieth M, Grunewald M, Niemeyer C, Stolte M. Adenocarcinoma in an ileal pouch after prior proctocolectomy for carcinoma in a patient with ulcerative pancolitis. Virchows Arch 1998; 433: 281-4.
59. Iwama T, Kamikawa J, Higuchi T, Yagi K, Matsuzaki T, Kanno J, Maekawa A. Development of invasive adenocarcinoma in a long-standing diverted ileal J-pouch for ulcerative colitis: Report of a case. Dis Colon Rectum 2000; 43: 101-4.
60. Heuschen UA, Heuschen G, Autschbach F, Allemeyer EH, Herfarth C. Adenocarcinoma in the ileal pouch: Late risk of cancer after restorative proctocolectomy. Int J Colorectal Dis 2001; 16: 126-30.
61. Bentrem DJ, Wang KL, Stryker SJ. Adenocarcinoma in an ileal pouch occurring 14years after restorative proctocolectomy: Report of a case [erratum appears in Dis Colon Rectum 2003; 46 (5): 628]. Dis Colon Rectum 2003; 46: 544-6.
62. Hassan C, Zullo A, Speziale G, Stella F, Lorenzetti R, Morini S. Adenocarcinoma of the ileoanal pouch anastomosis: An emerging complication? Int J Colorectal Dis 2003; 18: 276-8.
63. Knupper N, Straub E, Terpe HJ, Vestweber KH. Adenocarcinoma of the ileoanal pouch for ulcerative colitis - a complication of severe chronic atrophic pouchitis ? Int J Colorectal Dis 2006; 21: 478-82.
64. Puthu D, Rajan N, Rao R, Rao L, Venugopal P. Carcinoma of the rectal pouch following restorative proctocolectomy. Report of a case. Dis Colon Rectum 1992; 35: 257-60.
65. Sequens R. Cancer in the anal canal (transitional zone) after restorative proctocolectomy with stapled ileal pouch-anal anastomosis. Int J Colorectal Dis 1997; 12: 254-5.
66. Rotholtz NA, Pikarsky AJ, Singh JJ, Wexner SD. Adenocarcinoma arising from along the rectal stump after double-stapled ileorectal J-pouch in a patient with ulcerative colitis: The need to perform a distal anastomosis. Report of a case. Dis Colon Rectum 2001; 44: 1214-7.
67. Laureti S, Ugolini F, D'Errico A, Rago S, Poggioli G. Adenocarcinoma below ileoanal anastomosis for ulcerative colitis: Report of a case and review of the literature. Dis Colon Rectum 2002; 45: 418-21.
68. Baratsis S, Hadjidimitriou F, Christodoulou M, Lariou K. Adenocarcinoma in the anal canal after ileal pouch-anal anastomosis for ulcerative colitis using a double stapling technique: Report of a case. Dis Colon Rectum 2002; 45: 687-91 ; discussion 691-82.
69. Hyman N. Rectal cancer as a complication of stapled IPAA. Inflamm Bowel Dis 2002; 8: 43-5.
70. Bell SW, Parry B, Neill M. Adenocarcinoma in the anal transitional zone after ileal pouch for ulcerative colitis: Report of a case. Dis Colon Rectum 2003; 46: 1134-7.
71. Negi SS, Chaudhary A, Gondal R. Carcinoma of pelvic pouch following restorative proctocolectomy: Report of a case and review of the literature. Dig Surg 2003; 20: 63-5.
72. Hoehner JC, Metcalf AM. Development of invasive adenocarcinoma following colectomy with ileoanal anastomosis for familial polyposis coli. Report of a case. Dis Colon Rectum 1994; 37: 824-8.
73. von Herbay A, Stern J, Herfarth C. Pouch-anal cancer after restorative proctocolectomy for familial adenomatous polyposis. Am J Surg Pathol 1996; 20: 995-9.
74. Vuilleumier H, Halkic N, Ksontini R, Gillet M. Columnar cuff cancer after restorative proctocolectomy for familial adenomatous polyposis. Gut 2000; 47: 732-4.
75. Brown SR, Donati D, Seow-Choen F. Rectal cancer after mucosectomy for ileoanal pouch in familial adenomatous polyposis: Report of a case. Dis Colon Rectum 2001; 44: 1714-5.
76. Remzi FH, Church JM, Bast J et al. Mucosectomy vs. stapled ileal pouch-anal anastomosis in patients with familial adenomatous polyposis: functional outcome and neoplasia control. Dis Colon Rectum 2001; 44: 1590-6.
77. Bassuini MM, Billings PJ. Carcinoma in an ileoanal pouch after restorative proctocolectomy for familial adenomatous polyposis. Br J Surg 1996; 83: 506.
78. Palkar VM, deSouza LJ, Jagannath P, Naresh KN. Adenocarcinoma arising in "J" pouch after total proctocolectomy for familial polyposis coli. Indian J Cancer 1997; 34: 16-9.
79. Ooi BS, Remzi FH, Gramlich T, Church JM, Preen M, Fazio VW. Anal transitional zone cancer after restorative proctocolectomy and ileoanal anastomosis in familial adenomatous polyposis: Report of two cases. Dis Colon Rectum 2003; 46: 1418-23 ; discussion 1422-3.
80. Campos FG, Habr-Gama A, Kiss DR, da Silva EV, Rawet V, Imperiale AR, Perez R, da Silva JH, Sousa AH Jr, Gama-Rodrigues J. Adenocarcinoma after ileoanal anastomosis for familial adenomatous polyposis: Review of risk factors and current surveillance apropos of a case. J Gastrointest Surg 2005; 9: 695-702.
81. Kotanagi H, Kon H, Iida M, Ito M, Koyama K. Adenocarcinoma at the site of ileoanal anastomosis in Crohn's disease: Report of a case. Dis Colon Rectum 2001; 44: 1210-3.
82. Ben Temime L, Gherib BS, Daldoul S, Bel Hadj Salah R, Abdesselem Mel M, Zaouche A. Adenocarcinoma at the site of ileo-anal anastomosis in Crohn's disease: Report of a case. Tunis Med 2005; 83: 55-8.
83. Nyam DC, Pemberton JH, Sandborn WJ, Savcenko M. Lymphoma of the pouch after ileal pouch-anal anastomosis: Report of a case. Dis Colon Rectum 1997; 40: 971-2.
84. Frizzi JD, Rivera DE, Harris JA, Hamill RL. Lymphoma arising in an S-pouch after total proctocolectomy for ulcerative colitis: Report of a case. Dis Colon Rectum 2000; 43: 540-3.
85. Cox CL, Butts DR, Roberts MP, Wessels RA, Bailey HR. Development of invasive adenocarcinoma in a long-standing Kock continent ileostomy: report of a case. Dis Colon Rectum 1997; 40: 500-3.
86. Ravitch MM. The reception of new operations. Ann Surg 1984; 200: 231-46.
87. Schaffzin DM, Smith LE. Squamous-cell carcinoma developing after an ileoanal pouch procedure: Report of a case. Dis Colon Rectum 2005; 48: 1086-9.
88. Gyde SN, Prior P, Allan RN, Stevens A, Jewell DP, Truelove SC, Lofberg R, Brostrom O, Hellers G. Colorectal cancer in ulcerative colitis: A cohort study of primary referrals from three centres. Gut 1988; 29: 206-17.
89. Shelton AA, Lehman RE, Schrock TR, Welton ML. Retrospective review of colorectal cancer in ulcerative colitis at a tertiary center. Arch Surg 1996; 131: 806-10 ; discussion 810-11.
90. von Herbay A, Herfarth C, Otto HF. Cancer and dysplasia in ulcerative colitis: A histologic study of 301 surgical specimen. Z Gastroenterol 1994; 32: 382-8.
91. Giarnieri E, Giovagnoli MR, Montesani C, Nagar C, Pronio AM, Alderisio M, Ribotta G, Vecchione A. Image analysis in multisample biopsy after ileal pouch-anal anastomosis. Anticancer Res 1996; 16: 3207-11.
92. Giebel GD, Sabiers H. Ileal pouch-anal anastomosis for ulcerative colitis and polyposis coli: Is the risk of carcinoma formation conclusively averted ? Eur J Surg Oncol 1996; 22: 372-6.
93. Setti-Carraro P, Ritchie JK, Wilkinson KH, Nicholls RJ, Hawley PR. The first 10years'experience of restorative proctocolectomy for ulcerative colitis. Gut 1994; 35: 1070-5.
94. Sarigol S, Wyllie R, Gramlich T, Alexander F, Fazio V, Kay M, Mahajan L. Incidence of dysplasia in pelvic pouches in pediatric patients after ileal pouch-anal anastomosis for ulcerative colitis. J Pediatr Gastroenterol Nutr 1999; 28: 429-34.
95. Elkowitz D, Daum F, Markowitz J, Proccaccino J, Boas E, Cuomo J, Kahn E. Risk factors for carcinoma of the pelvic ileal pouch/anal canal in ulcerative colitis. Ann Clin Lab Sci 2004; 34: 143-9.
96. Hurlstone DP, Shorthouse AJ, Cross SS, Brown S, Sanders DS, Lobo AJ. High-magnification chromoscopic pouchoscopy: A novel in vivo technique for surveillance of the anal transition zone and columnar cuff following ileal pouch-anal anastomosis. Tech Coloproctol 2004; 8: 173-8 ; discussion 178.