Changes In Surgical Technique
Thomas E. Read, MD
Assistant Professor of Surgery
Section of Colon and Rectal Surgery
Washington University School of Medicine
St. Louis, MO
There have been many technical developments in colon and rectal surgery during the past 5-10 years, including the application of laparoscopic techniques to intestinal surgery. Rather than attempt to outline all the changes in surgical technique, three areas that have been somewhat controversial and apply to a fairly large number of patients will be reviewed: total mesorectal excision for rectal cancer; proctectomy and colonic pouch-anal anastomosis; and the double-stapled technique for ileal pouch-anal anastomosis.
Total Mesorectal Excision for Rectal Cancer
In 1990, the National Institutes of Health released a consensus statement advocating adjuvant chemotherapy and external beam radiation therapy for T3 and N1 (Stage II and III) rectal adenocarcinoma.(1) These recommendations were based, at least in part, on local recurrence rates of 25% to 35% in most of the cooperative trials.(2) Since that time, there has been renewed interest in the technical aspects of proctectomy for rectal cancer, as wide surgeon-to-surgeon variability has been demonstrated for both local recurrence and survival rates following curative excision of rectal cancer.(3-5) William Heald (Basingstoke, UK) and others advocated a technique termed "total mesorectal excision" as a method to reduce local recurrence rates to 4% to 8% following proctectomy for rectal cancer, without the use of adjuvant therapy.(6-10) This spawned considerable controversy regarding the definition of "total" mesorectal excision and its value in rectal cancer surgery.
Total mesorectal excision has focused attention on two critical components of oncologic proctectomy: the lateral (radial) margin and the distal margin of mesorectal excision. As noted by Dukes in 1943, rectal cancers are much more likely to spread laterally by direct extension and involvement of the mesorectum than distally in the intramural plane.(11) Cure and avoidance of local recurrence depend on the adequacy of lateral pelvic clearance and the removal of mesorectal tissue in its fascial envelope.(6, 12, 13) This is not a new concept, and local recurrence rates as low as 8% have been achieved in large numbers of patients undergoing anterior resection for rectal cancer in the 1960's.(14) The success of mesorectal excision depends on sharp dissection under direct vision in the presacral space posterior to the mesorectum. This plane can be identified by opening the plane just posterior to the superior hemorrhoidal artery and extending the dissection distally over the sacral promontory. No major blood vessels should be encountered in the posterior midline in this space from the origin of the inferior mesenteric artery at the aorta to the anal canal. Laterally, the peritoneum is incised just medial to the ureter on either side and proceeds along the sidewalls of the pelvis. Blunt tearing maneuvers and "coning down" on the mesorectum should be avoided. It is crucial to have the operative specimen retrieved by the pathologist and have the radial margins inked prior to opening the specimen. The presence of a positive radial margin is a strong predictor of local recurrence. Although these concepts are neither novel nor controversial, the recent discussion regarding total mesorectal excision has served to emphasize their importance in rectal cancer surgery.
The necessity of the second component of total mesorectal excision, the removal of the entire mesorectum distal to the tumor, is not as well supported by the available evidence and may not be appropriate for all patients with rectal cancer. Careful pathologic studies have shown that distal spread of rectal adenocarcinoma (either in the wall of the rectum or mesorectum) greater than 2-3 cm is rare, and when it occurs it is associated with advanced lesions and poor prognosis.(11, 15-20) Although total mesorectal excision may be appropriate for all distal and most middle rectal cancers, the need to extend mesorectal excision more than 5 cm beyond a proximal rectal cancer has not been proven, and may increase morbidity. Heald et al. reported a high anastomotic leak rate (17%) following low anterior resection, which may be a result of leaving devascularized rectum distal to the anastomosis.(21) This high leak rate prompted the Basingstoke group to perform routine diverting stomas, and others to perform complete proctectomy with coloanal anastomosis in all patients undergoing total mesorectal excision. However, temporary diverting stomas necessitate a second operation and have their own morbidity, and functional outcome after sphincter-sparing operation worsens as the distance of the anastomosis from the pelvic floor decreases.(22, 23) A more reasonable approach may be to mobilize the mesorectum in its fascial envelope for a distance of 3 to 5 cm distal to the tumor, transect the mesorectum (and rectum) perpendicularly at that level, and perform the anastomosis there. The Mayo Clinic group has termed this approach "tumor-specific" mesorectal excision, and have reported similar local recurrence rates with lower morbidity.(12) In its most recent report, the Basingstoke group acknowledges performing a similar procedure for patients with proximal rectal cancer.(7) Although it could be argued by experienced pelvic surgeons that a policy of "tumor-specific" mesorectal excision is neither novel nor controversial, the recent attention to surgical technique is warranted given the widely divergent local recurrence rates reported in the literature.(24)
Proponents of total mesorectal excision have argued that the low local recurrence rates achieved by meticulous technique may obviate the need for adjuvant external beam radiation therapy for non-fixed tumors.(7, 10, 12) The data from some series are difficult to evaluate in this regard because of the inclusion of patients who received external beam radiation, or the potential selection bias introduced by the exclusion of patients who received external beam radiation for potentially more aggressive tumors. Regardless, the hypothesis that external beam radiation, which has been shown to reduce local recurrence rates in multiple trials,(25, 26) would be ineffective when combined with "total" or "tumor specific" mesorectal excision has yet to be prospectively evaluated. Local recurrence rates of 11% and 13% after low anterior resection for stage II and III disease in a recent large series of patients treated with surgery alone(12) would indicate that there may be a continued role for adjuvant external beam radiotherapy in the treatment of rectal cancer.
Proctectomy with Colonic Pouch-Anal Anastomosis
The overwhelming majority of patients undergoing coloanal anastomosis suffer from carcinoma of the rectum. Until recently, most patients with mid or distal rectal cancers underwent abdomino-perineal resection. Technical issues non-withstanding, surgeons were loath to consider preservation of the distal rectum or anal canal in these patients because of their concern of distal intramural spread of tumor. As noted above, pathologic studies have shown that distal spread of rectal adenocarcinoma greater than 2 cm is rare, and it is the radial extension of tumor into the mesorectum or pelvic sidewall that is of critical importance.(11, 13, 15-20) Preservation of anal sphincter function is thus possible following proctectomy for mid and distal cancers, provided that the distal margin of the tumor is several centimeters above the anorectal muscular ring.(6, 12)
Precise definition of coloanal anastomosis is lacking. Removal of the rectum to the level of the levators with anastomosis in, or just above, the anal canal is considered to be a coloanal anastomosis by some surgeons. Others have a more rigorous definition, requiring anastomosis at the dentate line, and refer to the former as an ultra-low colorectal anastomosis. Regardless of technique, the concept of removal of the rectum and mesorectum with restoration of intestinal continuity in the region of the anal sphincter complex remains constant.
Construction of a neorectum using a colonic pouch has received considerable attention recently. Stool frequency, urgency, and irregular transit (stool "clustering") are reduced compared to straight coloanal anastomosis, probably because of increased reservoir capacity.(27-36) The advantage of the pouch-anal anastomosis over a straight coloanal anastomosis appears to be most pronounced in the first 1-2 years following construction. The typical colonic pouch is constructed in a J-fashion using a 6-10 cm limb length. Larger pouches (10 cm limb length) may impair emptying,(37, 38) although the functional differences emphasized in some studies of pouch limb length may be negated by changes in pouch volume over time.
Patient Evaluation and Details of Operation
Patients with rectal cancer should undergo evaluation with digital rectal examination, rigid proctoscopy, and transrectal ultrasound (TRUS). Invasion of the anorectal muscular ring precludes restoration of intestinal continuity. Before considering coloanal anastomosis, sphincter function should be assessed. A detailed continence history and physical examination by an experienced surgeon are probably the most predictive of postoperative function.(39) However, anal manometry may help in equivocal cases. Despite the enthusiasm of many patients to restore intestinal continuity at all costs, it should be remembered that an abdominal colostomy is preferable to a perineal colostomy in cases where sphincter function is impaired.
The presence of unresectable metastases makes coloanal anastomosis ill-advised. If a temporary diverting stoma is constructed, the patient may never be fit enough to have the stoma closed. Even if the patient does not require a diverting stoma, the initial 6-18 months following coloanal anastomosis are often marked by frequent loose stools and occasional incontinence. The patient may not survive long enough to benefit from the gradual improvement in function of the neorectum. If the patient is treated with chemotherapy postoperatively, the risk of diarrhea and fecal incontinence are increased further. Low anterior resection with Hartmann closure of the rectal stump is a more prudent option for these patients. Similarly, if tumor invasion of pelvic structures makes complete resection impossible, low anastomosis should be abandoned because of the high risk of persistent tumor growth in the pelvis.
Complete mobilization of the splenic flexure, division of the inferior mesenteric artery at its origin from the aorta, and division of the inferior mesenteric vein adjacent to the ligament of Treitz will allow the descending colon to reach into the deep pelvis in most patients. The descending colon is preferable for pelvic anastomoses because the sigmoid colon is often narrow and has muscular hypertrophy. In addition, if preoperative external beam radiation has been used, the sigmoid may have been included in the radiation field.
Division of the anal canal or very distal rectum can usually be accomplished through the abdomen using a linear stapler. The site of division should be below the tail of mesorectum so that all mesorectal tissue accompanies the specimen. Some surgeons are enthusiasts of the combined transanal-transabdominal resection procedure, where the distal margin is defined and the distal dissection is performed from a transanal approach. If the tumor is so low that division in the proximal anal canal would not provide an adequate distal margin, then perhaps an abdomino-perineal procedure would be safer from an oncologic standpoint. There may be a few patients who, because of a narrow pelvis or other aspect of body habitus, might benefit from such a technique.
Although a colonic pouch and pouch-anal anastomosis may be constructed entirely with suture, most surgeons perform this technique using surgical staplers. The proximal colon is usually divided with a linear cutting stapler. The colon is then folded into a J-configuration with a 6-8 cm limb length. The apex of the pouch is opened and a linear cutting stapler is used to create the pouch. Usually a single fire of a 75 or 90 mm stapler will create adequate pouch length. A pursestring suture is placed around the opening at the pouch apex and the anvil of the end-to-end stapler inserted. Alternatively, if the distal margin of resection has been determined by transanal dissection, the pouch can be passed to the anus and a handsewn anastomosis performed.
Although prospective randomized data are lacking, many surgeons feel that the risk of anastomotic or pouch leak with pelvic sepsis and subsequent fibrosis of the neorectum outweighs the benefits of avoiding temporary fecal diversion.(40) In addition, the majority of patients undergoing proctectomy and coloanal anastomosis for rectal cancer will have Stage II or III lesions. Most of these patients will be treated with postoperative chemotherapy, and chemotherapy-induced diarrhea in a patient first adapting to a neorectum can cause fecal incontinence. Temporary fecal diversion may also be prudent in cases where neoadjuvant chemoradiation is used. Although dramatic reductions in tumor size can be achieved with the use of preoperative chemoradiation, it may predispose to anastomotic problems in patients not undergoing temporary diversion at the time of proctectomy and coloanal anastomosis.(41) The most commonly used diverting stoma is the loop ileostomy, because its construction and subsequent takedown are straightforward, and the colonic mesentery is not threatened by such manipulation.
Double Stapled Ileal Pouch-Anal Anastomosis
Total proctocolectomy with creation of an ileal pouch-anal anastomosis (IPAA) has been performed since the late 1970's and has become the most commonly performed procedure for mucosal ulcerative colitis and familial adenomatous polyposis.(42, 43) The procedure was initially performed with a transanal mucosectomy beginning at the dentate line. Mucosectomy theoretically removes all columnar epithelium from the upper anal canal, thereby preventing inflammation in this area and eliminating the risk of dysplasia or carcinoma developing in residual rectal mucosa. However, mucosectomy is a time-consuming and technically demanding technique. Sphincter stretch and damage during the procedure may result in fecal seepage and soilage, and removal of the anal transitional zone may ablate the rectoanal inhibitory reflex and impair rectal sensation. Because of these technical and functional considerations, there has been a recent trend toward performing IPAA using a double-stapled technique.
Double-stapled IPAA, first introduced in the late 1980's, involves proctectomy from the abdominal approach, with division of the distal rectum between the levators usually 1-2 cm proximal to the dentate line using a linear stapler.(44) After the anvil of the stapler is inserted into the pouch, the anastomosis is constructed by placing the stapler per anus. In addition to avoiding prolonged retraction of the anal canal, this technique preserves the distal internal anal sphincter muscle and anal transitional zone, both of which may contribute to improved continence.(45, 46) Although there are exceptions,(47, 48) the majority of investigators have demonstrated functional advantages of the double-stapled technique when compared to mucosectomy, including increased anal resting pressure, preservation of the rectoanal inhibitory reflex, and improved continence.(49-53) Double-stapled IPAA has also been shown, in one large series, to have fewer septic complications than the handsewn technique.(54)
When the double-stapled IPAA was introduced, concerns were voiced regarding persistent inflammation in the retained strip of retained rectal and transitional zone mucosa, as well as the risk of developing dysplasia and carcinoma in the same area. Few patients undergoing double-stapled IPAA for ulcerative colitis have needed treatment for symptomatic inflammation of the anal canal, and most respond to simple topical medication.(55) Dysplasia in the anal transitional zone is extremely rare when there is no evidence of dysplasia or carcinoma in the colon and rectum, and develops in very few patients post-operatively.(56, 57) The Cleveland Clinic group found low-grade dysplasia in 3 percent of 254 patients who underwent double-stapled IPAA for ulcerative colitis and were followed with annual postoperative biopsies of the anal transitional zone.(57) They advocated completion mucosectomy when the dysplasia persisted on follow-up biopsy.
Mucosectomy has been advocated as the preferred technique for patients with familial adenomatous polyposis and those with ulcerative colitis who have dysplasia or carcinoma elsewhere in the colon or rectum. However, residual nests of rectal mucosa have been found either outside the ileal pouch or adjacent to the pouch-anal anastomosis in up to 21% of patients undergoing mucosectomy.(58) There have been at least three reports of patients developing rectal carcinoma after mucosectomy.
References
1. NIH consensus conference. Adjuvant therapy for patients with colon and rectal cancer. JAMA 1990;264(11):1444-50.
2. McCall JL. Total mesorectal excision: evaluating the evidence. Aust N Z J Surg 1997;67(9):599-602.
3. Holm T, Johansson H, Cedermark B, Ekelund G, Rutqvist LE. Influence of hospital- and surgeon-related factors on outcome after treatment of rectal cancer with or without preoperative radiotherapy. Br J Surg 1997;84(5):657-63.
4. Porter GA, Soskolne CL, Yakimets WW, Newman SC. Surgeon-related factors and outcome in rectal cancer. Annals of Surgery 1998;227(2):157-67.
5. Dahlberg M, Pahlman L, Bergstrom R, Glimelius B. Improved survival in patients with rectal cancer: a population-based register study. Br J Surg 1998;85(4):515-20.
6. Heald RJ, Ryall RD. Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1986;1(8496):1479-82.
7. Heald RJ, Moran BJ, Ryall RD, Sexton R, MacFarlane JK. Rectal cancer: the Basingstoke experience of total mesorectal excision, 1978-1997. Arch Surg 1998;133(8):894-9.
8. MacFarlane JK, Ryall RD, Heald RJ. Mesorectal excision for rectal cancer. Lancet 1993;341(8843):457-60.
9. Enker WE, Thaler HT, Cranor ML, Polyak T. Total mesorectal excision in the operative treatment of carcinoma of the rectum. J Am Coll Surg 1995;181(4):335-46.
10. Arenas RB, Fichera A, Mhoon D, Michelassi F. Total mesenteric excision in the surgical treatment of rectal cancer: a prospective study. Arch Surg 1998;133(6):608-11.
11. Dukes C. The surgical pathology of rectal cancer. Proc R Soc Med 1943;37:131.
12. Zaheer S, Pemberton JH, Farouk R, Dozois RR, Wolff BG, Ilstrup D. Surgical treatment of adenocarcinoma of the rectum. Ann Surg 1998;227(6):800-11.
13. Quirke P, Durdey P, Dixon MF, Williams NS. Local recurrence of rectal adenocarcinoma due to inadequate surgical resection. Histopathological study of lateral tumour spread and surgical excision. Lancet 1986;2(8514):996-9.
14. Wilson SM, Beahrs OH. The curative treatment of carcinoma of the sigmoid, rectosigmoid, and rectum. Ann Surg 1976;183(5):556-65.
15. Quer E, Dahin D, Mayo C. Retrograde intramural spread of carcinoma of the rectum and rectosigmoid. Surg Gynecol Obstet 1953;96:24-30.
16. Grinnell R. Distal intramural spread of rectal carcinoma. Surg Gynecol Obstet 1954;99:421-30.
17. Black U, Waugh J. The intramural extension of carcinoma of the descending colon, sigmoid and rectosigmoid. A pathological study. Surg Gynecol Obstet 1948;1948:457-64.
18. Scott N, Jackson P, al JT, Dixon MF, Quirke P, Finan PJ. Total mesorectal excision and local recurrence: a study of tumour spread in the mesorectum distal to rectal cancer. Br J Surg 1995;82(8):1031-3.
19. Williams NS, Dixon MF, Johnston D. Reappraisal of the 5 centimetre rule of distal excision for carcinoma of the rectum: a study of distal intramural spread and of patients' survival. Br J Surg 1983;70(3):150-4.
20. Goligher J, Dukes C, Bussey H. Local recurences after sphincter saving excisions for carcinoma of the rectum and rectosigmoid. Br J Surg 1951;39:199-211.
21. Karanjia ND, Corder AP, Bearn P, Heald RJ. Leakage from stapled low anastomosis after total mesorectal excision for carcinoma of the rectum. Br J Surg 1994;81(8):1224-6.
22. Karanjia ND, Schache DJ, Heald RJ. Function of the distal rectum after low anterior resection for carcinoma. Br J Surg 1992;79(2):114-6.
23. Lewis WG, Holdsworth PJ, Stephenson BM, Finan PJ, Johnston D. Role of the rectum in the physiological and clinical results of coloanal and colorectal anastomosis after anterior resection for rectal carcinoma. Br J Surg 1992;79(10):1082-6.
24. McCall JL, Cox MR, Wattchow DA. Analysis of local recurrence rates after surgery alone for rectal cancer. Int J Colorectal Dis 1995;10(3):126-32.
25. Improved survival with preoperative radiotherapy in resectable rectal cancer. Swedish Rectal Cancer Trial. N Engl J Med 1997;336(14):980-7.
26. Fleshman JW, Myerson RJ. Adjuvant radiation therapy for adenocarcinoma of the rectum. Surg Clin North Am 1997;77(1):15-25.
27. Lazorthes F, Chiotasso P, Gamagami RA, Istvan G, Chevreau P. Late clinical outcome in a randomized prospective comparison of colonic J pouch and straight coloanal anastomosis. Br J Surg 1997;84(10):1449-51.
28. Mortensen NJ, Ramirez JM, Takeuchi N, Humphreys MM. Colonic J pouch-anal anastomosis after rectal excision for carcinoma: functional outcome. Br J Surg 1995;82(5):611-3.
29. Hallbook O, Pahlman L, Krog M, Wexner SD, Sjodahl R. Randomized comparison of straight and colonic J pouch anastomosis after low anterior resection. Ann Surg 1996;224(1):58-65.
30. Hallbook O, Sjodahl R. Comparison between the colonic J pouch-anal anastomosis and healthy rectum: clinical and physiological function. Br J Surg 1997;84(10):1437-41.
31. Seow-Choen F, Goh HS. Prospective randomized trial comparing J colonic pouch-anal anastomosis and straight coloanal reconstruction. Br J Surg 1995;82(5):608-10.
32. Ho YH, Tan M, Seow CF. Prospective randomized controlled study of clinical function and anorectal physiology after low anterior resection: comparison of straight and colonic J pouch anastomoses. Br J Surg 1996;83(7):978-80.
33. Ortiz H, De MM, Armendariz P, Rodriguez J, Chocarro C. Coloanal anastomosis: are functional results better with a pouch? Dis Colon Rectum 1995;38(4):375-7.
34. Nicholls RJ, Lubowski DZ, Donaldson DR. Comparison of colonic reservoir and straight colo-anal reconstruction after rectal excision. Br J Surg 1988;75(4):318-20.
35. Dehni N, Tiret E, Singland JD, Cunningham C, Schlegel RD, Guiguet M, et al. Long-term functional outcome after low anterior resection: comparison of low colorectal anastomosis and colonic J-pouch-anal anastomosis. Dis Colon Rectum 1998;41(7):817-22.
36. Hallbook O, Nystrom PO, Sjodahl R. Physiologic characteristics of straight and colonic J-pouch anastomoses after rectal excision for cancer. Dis Colon Rectum 1997;40(3):332-8.
37. Lazorthes F, Gamagami R, Chiotasso P, Istvan G, Muhammad S. Prospective, randomized study comparing clinical results between small and large colonic J-pouch following coloanal anastomosis. Dis Colon Rectum 1997;40(12):1409-13.
38. Hida J, Yasutomi M, Fujimoto K, Okuno K, Ieda S, Machidera N, et al. Functional outcome after low anterior resection with low anastomosis for rectal cancer using the colonic J-pouch. Prospective randomized study for determination of optimum pouch size. Dis Colon Rectum 1996;39(9):986-91.
39. Church JM, Saad R, Schroeder T, Fazio VW, Lavery IC, Oakley JR, et al. Predicting the functional result of anastomoses to the anus: the paradox of preoperative anal resting pressure. Dis Colon Rectum 1993;36(10):895-900.
40. Dehni N, Schlegel RD, Cunningham C, Guiguet M, Tiret E, Parc R. Influence of a defunctioning stoma on leakage rates after low colorectal anastomosis and colonic J pouch-anal anastomosis. Br J Surg 1998;85(8):1114-7.
41. Hyams DM, Mamounas EP, Petrelli N, Rockette H, Jones J, Wieand HS, et al. A clinical trial to evaluate the worth of preoperative multimodality therapy in patients with operable carcinoma of the rectum: a progress report of National Surgical Breast and Bowel Project Protocol R-03. Diseases of the Colon & Rectum 1997;40(2):131-9.
42. Meagher AP, Farouk R, Dozois RR, Kelly KA, Pemberton JH. J ileal pouch-anal anastomosis for chronic ulcerative colitis: complications and long-term outcome in 1310 patients. Br J Surg 1998;85(6):800-3.
43. Fazio VW, Ziv Y, Church JM, Oakley JR, Lavery IC, Milsom JW, et al. Ileal pouch-anal anastomoses complications and function in 1005 patients. Ann Surg 1995;222(2):120-7.
44. Heald RJ, Allen DR. Stapled ileo-anal anastomosis: a technique to avoid mucosal proctectomy in the ileal pouch operation. Br J Surg 1986;73(7):571-2.
45. Deen KI, Williams JG, Grant EA, Billingham C, Keighley MR. Randomized trial to determine the optimum level of pouch-anal anastomosis in stapled restorative proctocolectomy. Dis Colon Rectum 1995;38(2):133-8.
46. Becker JM, LaMorte W, St MG, Ferzoco S. Extent of smooth muscle resection during mucosectomy and ileal pouch- anal anastomosis affects anorectal physiology and functional outcome. Dis Colon Rectum 1997;40(6):653-60.
47. McIntyre PB, Pemberton JH, Beart RJ, Devine RM, Nivatvongs S. Double-stapled vs. handsewn ileal pouch-anal anastomosis in patients with chronic ulcerative colitis. Dis Colon Rectum 1994;37(5):430-3.
48. Choen S, Tsunoda A, Nicholls RJ. Prospective randomized trial comparing anal function after hand sewn ileoanal anastomosis with mucosectomy versus stapled ileoanal anastomosis without mucosectomy in restorative proctocolectomy. Br J Surg 1991;78(4):430-4.
49. Tuckson WB, McNamara MJ, Fazio VW, Lavery IC, Oakley JR. Impact of anal manipulation and pouch design on ileal pouch function. J Natl Med Assoc 1991;83(12):1089-92.
50. Holdsworth PJ, Johnston D. Anal sensation after restorative proctocolectomy for ulcerative colitis. Br J Surg 1988;75(10):993-6.
51. Johnston D, Holdsworth PJ, Nasmyth DG, Neal DE, Primrose JN, Womack N, et al. Preservation of the entire anal canal in conservative proctocolectomy for ulcerative colitis: a pilot study comparing end-to-end ileo-anal anastomosis without mucosal resection with mucosal proctectomy and endo- anal anastomosis. Br J Surg 1987;74(10):940-4.
52. Lavery IC, Tuckson WB, Easley KA. Internal anal sphincter function after total abdominal colectomy and stapled ileal pouch-anal anastomosis without mucosal proctectomy. Dis Colon Rectum 1989;32(11):950-3.
53. Reilly WT, Pemberton JH, Wolff BG, Nivatvongs S, Devine RM, Litchy WJ, et al. Randomized prospective trial comparing ileal pouch-anal anastomosis performed by excising the anal mucosa to ileal pouch-anal anastomosis performed by preserving the anal mucosa. Ann Surg 1997;225(6):666-76.
54. Ziv Y, Fazio VW, Church JM, Lavery IC, King TM, Ambrosetti P. Stapled ileal pouch anal anastomoses are safer than handsewn anastomoses in patients with ulcerative colitis. Am J Surg 1996;171(3):320-3.
55. 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(8):803-6.
56. Tsunoda A, Talbot IC, Nicholls RJ. Incidence of dysplasia in the anorectal mucosa in patients having restorative proctocolectomy. Br J Surg 1990;77(5):506-8.
57. 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(12):1281-5.
58. O'Connell PR, Pemberton JH, Weiland LH, Beart RJ, Dozois RR, Wolff BG, et al. Does rectal mucosa regenerate after ileoanal anastomosis? Dis Colon Rectum 1987;30(1):1-5.
59. 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(3):257-60.
60. Rodriguez SJ, Polavieja MG, Naranjo A, Castillo J. Adenocarcinoma in an ileal pouch for ulcerative colitis [letter]. Dis Colon Rectum 1995;38(7):779-80.
61. Stern H, Walfisch S, Mullen B, McLeod R, Cohen Z. Cancer in an ileoanal reservoir: a new late complication? Gut 1990;31(4):473-5.
62. Sequens R. Cancer in the anal canal (transitional zone) after restorative proctocolectomy with stapled ileal pouch-anal anastomosis. Int J Colorectal Dis 1997;12(4):254-5.