Physicians Patient and Public Members Annual Meeting Industry DCR About Us
Home > Physicians > Education > Core Subjects > Surgical Therapy Of ...
Print

Surgical Therapy Of Crohn's Disease

Feza H. Remzi, M.D.
Staff Surgeon, Department of Colorectal Surgery
The Cleveland Clinic Foundation
Cleveland, Ohio

Crohn's disease is a chronic inflammatory condition of unknown etiology that may affect any part of the gastrointestinal tract. The typical presenting symptoms include abdominal pain, diarrhea and weight loss. However the anatomic location of Crohn's disease within the gastrointestinal tract determines the clinical features and the presentation of the disease. This is also true for the type of complications that may arise, and the type of procedures that would be employed when surgery is indicated. Inflammation of the terminal ileum and cecum is the most common subtype followed by disease confined to large intestine, small intestine and perineal disease. No medical or surgical therapy has been developed that is curative.

Operative Indications

Most patients with Crohn's disease ultimately require one or more surgeries in their lifetime. The reported probability of surgery after 20 and 30 years of disease symptoms was 78% to 90%, respectively. Surgery for Crohn's disease is done either for complications or failure of medical therapy. Operative indications are usually the same no matter where the disease manifests itself: These include

  1. Failure of medical therapy or steroid dependency
  2. Obstruction
  3. Fistula or abscess
  4. Hemorrhage
  5. Growth Retardation
  6. Carcinoma
  7. Extraintestinal Manifestations

Preparation of the Patient for Surgery

Patient preparation is similar no matter the location of the disease. Preoperative counseling regarding the nature and the course of the disease with discussion about the rationalization of the surgery, hospitalization, perioperative morbidity including the possibility of ileostomy and future implications of recurrence is important.

In addition to preoperative counseling comprehensive assessment with a through endoscopic and radiological evaluation of the small and large bowel is performed to define the road map of the diseased areas and the operative strategy.

Correction of the restorable metabolic defects such as anemia, electrolyte deficiencies, dehydration, and coagulation defects is important. Nutritional status is commonly suboptimal. Preoperative optimization with the use of total parenteral nutrition is controversial. Most reports are retrospective and uncontrolled and results on either side of the issue can be found. In our practice, we use preoperative hyperalimentation for 5 to 7 days, if surgery is elective or semielective and malnutrition is considered severe.

Cessation of immunosupressives such as azathioprine, 6-mercaptopurine, and cyclosporine 3-4 weeks prior to an elective procedure is advised because of concerns about tissue or anastomotic healing. However the data to support this belief is limited and controversial.

Bowel preparation either with polyethylene glycol (4L) or fleet phosphosoda (90 ml) is used on patients who do not have signs and symptoms of obstruction. However, many patients with Crohn's disease involving the small bowel will present with varying degrees of obstructive signs and symptoms. In these, a mechanical bowel preparation is modified or omitted. Partially obstructed patients are placed on dietary restrictions with an elemental diet given for 3-5 days with supplemental oral or intravenous fluids. In this situation magnesium citrate over several days may be tolerated better than polyethylene glycol and help cleanse the bowel. Patients with distended small bowel may require hospitalization prior to surgery for nasogastric decompression as well as hydration and correction of electrolyte inbalances. Despite the mechanical bowel preparation, our practice, for distal colon or anorectal surgery is to do intraoperative washout of the rectum through a large rectal (34 FR) catheter until effluent is clear.

Some patients may need either temporary or permanent stoma at the time of the procedure. If there is any indication that a stoma may be needed, preoperative marking is essential. The major factor influencing satisfactory rehabilitation of an ostomy patient is the correct location and construction of the stoma. The principles of stoma siting include the following

  1. The site is clearly visible to the patient
  2. The surrounding zone of skin is undisturbed for a distance of 5 cm
  3. The site is located at the summit of the infraumblical fat mound
  4. The surface marking is within the rectus abdominis muscle
  5. The site is away from bony prominences skin creases, or scars.

Stress dose steroids are administered perioperatively if the patient has been treated with steroids within 6 months prior to operation. Additional preparation includes intravenous antibiotics with postoperative antibiotic selection is based on operative findings, likely flora, pending cultures and sensitivity. After anesthesia, a nasogastric tube is passed and Foley catheter is placed in the bladder. Central venous lines and peripheral arterial lines may be placed on the likely difficulty and duration of the operation. Ureteric stents are not used routinely but can be helpful with reoperative pelvic surgery. Finally, prophylaxis against deep venous thrombosis is employed using pneumatic stockings with or without mini-dose heparin.

Surgical Strategy

Small intestine is a non-renewable resource. Major resections can lead to disability from malabsorption, including short bowel syndrome. Thus, small bowel conservation in Crohn's disease is imperative to minimize the risk of excessive bowel resection. For this reason, segments of small bowel affected by nonobstructing, nonhemorrhaging Crohn's disease do not warrant resection. We should be treating only the problem in hand. Bowel economy is practiced as emphasized. However some exceptions to this philosophy exist. One modification of this principle involves jejunal and ileal strictures. If a stricture is identified at operation, even if it is not felt to be symptomatic at that time it should be addressed. We believe complications of strictureplasty in these situations are negligible, yet reoperation following strictureplasty is more likely to be necessary for new symptomatic strictures than for an old strictureplasty site. In addition to this any out circuit bowel such as rectal stump or small bowel should be considerate for excision due to cancer risk.

Important to the concept of conservation in surgery is the issue of resected margins. Recent evidence in a randomized controlled trial of patients (N=152) undergoing limited (2-cm) versus wide (12-cm) margins of resection beyond macroscopically diseased bowel showed that extended resection margins are unnecessary and has no advantage in reducing cumulative recurrence rates. This is of some importance in that minute aphthous ulcers may be seen within the intestine at sites remote from the resected specimen. These ulcers can be ignored, as there is no evidence that leaving such lesions in situ adversely affects recurrence rates. This is especially true in-patients with foreshortened intestine (<200 cm) where it is acceptable to join segments that are involved or even inflamed with Crohn's disease as long as there is no stricturing or deep ulceration present.

As for reoperation, surgery is deferred for any elective indication until at least three months-preferably six months since last laparotomy. Otherwise formidable adhesions may be encountered making for increased risks of inadvertent enterotomy. A small window of time (7 to 12 days) exists following laparotomy during which reoperation for complications such as enterocutaneous fistula can be attempted with reasonable success. Reoperation is justifiable for complications of intestinal ischemia, peritonitis and major hemorrhage between 12 to 90 days after the initial laparotomy. If the surgeon reoperates within 12 to 90 day post-operative period without an absolute indication he does so at the patient's peril. For patients with postoperative ileus/ bowel obstruction, it is safer to provide long-term TPN and a percutaneous gastrostomy than to risk enteric injury, fistulas or substantial loss of intestinal length in a well-intentioned, but dangerous venture. If an enterocutaneous fistula complicated with intra-abdominal sepsis or pouching and skin excoriation problems occur during the high risk period, a small laparotomy in the left upper quadrant with a proximal high loop jejunostomy isolates the septic source. Home TPN is continued for 4 to 6 months to maintain nutrition, pending restoration to correct the fistula and restore intestine continuity.

Use of temporary ostomy may be indicated in situations where anastomotic healing is compromised such as excessive blood loss during a long operation, severe hypoalbuminemia, incompletely drained sepsis or when a phlegmonous pyogenic membrane is in proximity to an anastomosis. These are not necessarily absolute indications or even the only indications for such diversion, but in the examples mentioned, temporary ostomies appear reasonable.

Vertical midline incisions are preferred to preserve potential ostomy sites. At the completion of operation the peritoneal cavity is thoroughly irrigated with warm saline. Drains are used if a septic pyogenic membrane is left behind, or if presacral mobilization of rectum has been done (sump suction drainage catheters). In our practice we prefer Latex rubber drains placed over residual septic focus rather than silastic drains where these are removed over two to three weeks to prevent premature healing which can cause an abscess to reform. If the focal site is remote from the skin surface and a residual cavity possible, a small (14 F to 16 F) mushroom or Pezzer catheter is substituted for a further 3 to 6 weeks. Prior to removal of such catheters, sinography is recommended to ensure collapse of the cavity and confirm fistula eradication.

SURGICAL PROCEDURES

Several types of operations are used in the surgery of Crohn's disease. These may be classified as resection with or without anastomosis, bypass procedures (internal and external such as gastroduoedenal bypass or ileostomy) and strictureplasty. As would be expected the surgical procedure depends on the site of the disease.

Ileocolic Disease

Ileocolic disease is the anatomic site most often involved with Crohn's disease affecting 40% of patients undergoing surgery. The typical patient with this disease will present with symptoms suggestive of perforation or obstruction. In particular, patients exhibiting stricturing disease, extraintestinal manifestations, or more than 5 years of recognized disease symptoms are likely to fail to respond to medical treatment, and early surgical intervention should be considered. Resection of the diseased bowel with ileoascending anastomosis is the preferred method of surgical treatment. If disease is associated with perforation and peritonitis creation of diverting ileostomy proximal to the ileocolic anastomosis decreases the morbidity associated with the next procedure. As much as normal right colon as possible is preserved for increased water absorption and avoiding anastomosis sitting over the duodenum with the risk of fistula development. Wrapping the anastomosis with omentum may avoid this problem. Unilateral exclusion bypass is done less in recent years for the apparently fixed ileocecal mass densely attached to the iliac vessels or retroperitoneum. Definitive resection is intended 6 months later.

Jejunoileal Disease

Approximately 10 to 20% will have jejunoileal disease. The most common surgical procedure is resection. Because Crohn's disase is panintestinal surgical therapy has shifted toward conservative approaches. Strictureplasty has become a valuable option for surgeon dealing with small bowel Crohn's disease. Since its initial application in Crohn's disease by Lee and Papaioannou, the safety and efficacy of the technique in general have been proven by several large studies that reported outcomes similar to those of resective surgery.

Heinecke-Mikulicz strictureplasty, which is the most commonly used one, is suitable for short strictures up to 10 cm. Longer strictures re treated by Finney type of strictureplasty. One of the concerns previously indicated regarding a Finney strictureplasty is that of bacterial overgrowth in the resultant large, diverticulum-like sac that extends from the intestine. Three variations have been proposed that deal with the concern of the Finney type of diverticulum. Fazio and Tjandra described a modification to treat multiple strictures in a small segment. Sasaki et all also reported a similar technique. The most effective technique for long strictures to prevent this diverticulum-like sac problem was described by Michelassi et al. He used a side to side isoperistaltic hand-sewn strictureplasty where this technique effectively eliminated the diverticulum produced by Finney method.

In general the situations for which strcitureplasty is considered are as follows:

  1. Diffuse involvement of the small bowel with multiple strictures
  2. Stricture(s) in a patient who has undergone previous major resection(s) of small bowel (more than 100 cm)
  3. Rapid recurrence of Crohn's disease manifested as obstruction.
  4. Stricture in a patient with short bowel syndrome
  5. Nonphlegmonous fibrotic stricture

The contraindications to strictureplasty are as follows:

  1. Free or contained perforation of the small bowel
  2. Phlegmomous inflammation, internal fistula, or external fistula involving the affected site
  3. Multiple strictures within a short segment
  4. Stricture in close proximity to a site chosen for resection
  5. Colonic strictures
  6. Hypoalbuminemia (less than 2.0 g/dl)
  7. Rigid thickened non supple bowel segments either short or long
  8. Extensive ulceration of mesenteric margin especially bleeding or friable
  9. Suspicion of cancer in a strictured segment

A retrospective review of 314 patients undergoing 1124 strictureplasty procedure for obstructing small bowel Crohn's disease at the Cleveland Clinic between 1984 and 1999 showed overall morbidity of 18% with septic complications occurring in 5% of patients. Intraabdominal abscess were comprised in seven patients (2%), anastomotic leak or enterocutaneous fistula in six patients (2%), and wound infection in four patients (1%). The most common complication was luminal bleeding requiring transfusion. This developed in 23 patients (7%) and was almost always self-limited. In two cases angiography with vasopressin infusion was needed. A number of factors were examined to determine their influence on postoperative morbidity. Only older age and preoperative weight loss were significantly associated with morbidity. Previously reported of increased septic complications associated in patients with serum albumin values less than 3.0 g/dl was not seen in the most recent report from our institution. This is high likely related to the practice that we have adopted after the initial study where strictueplasty was avoided in patients with low albumin levels or these patients were proximally diverted.

In this most recent from the Cleveland Clinic within 1 to 6 months of operation, 98% of patients were without obstructive symptoms, and only 19% of patients remained on prednisone. After a mean length of follow-up of 7.7 years, 116 (37%) suffered recurrence of their Crohn's disease that required operation. The indication for reoperation was obstruction in 92% of the patients. Strictureplasty was performed again, either alone or in combination with resection, in 54% of patients. Multiple factors were analyzed to determine their effect on recurrence. The primary factors found to correlate with recurrence time were age, duration of disease, and years since previous resection.

Colonic Disease

Colonic disease affects 20-30 of patients. The choice of operation for Crohn's disease affecting large intestine depends on multiple variables, including age, disease distribution, extent of involvement, previous resections, rectal compliance and adequacy of fecal continence. Segmental resection with ileocolic or colocolic anastomosis and abdominal colectomy with ileoproctostomy are the procedures most commonly performed for Crohn's colitis.

In patients with pancolitis a total proctocolectomy with permanent ileostomy is the usual operative choice. Although isolated centers are offering proctocolectomy and ileal pouch-anal anastomosis with reasonable results, patients requiring surgical treatment of proctitis with or without accompanying colitis usually undergo proctocolectomy and end ileostomy. When a proctectomy is done for Crohn's disease, the initial dissection starting at the pelvic brim is done in a similar manner for other rectal dissections. Since the operation is not typically done for cancer, the removal of the anus does not have to be radical. Either amputating the rectum at the level of the anorectal ring and doing an anal canal mucosectomy and sewing the anal sphincter complex or removing the anorectal complex with intersphincteric dissection and primary closure of the perineal wound may avoid an unhealed perineal wound. The resultant unhealed perineal wound is often difficult to manage, notorious for poor healing and significantly compromises the affected patient's quality of life. Complex tissue flap closure of the perineal wound utilizing different muscle flaps is generally successful. Alternatively omentoplasty effectively treats a persistent perineal sinus.

In toxic patient or those with severe perineal disease and sepsis, a colectomy without proctectomy and with ileostomy is done. In these circumstances it may be beneficial to staple the colon in the mid to distal sigmoid colon level and then sew it in the distal aspect of the incision. Therefore if the staple line breaks down, the patient is left initially with a wound infection and later colocutaneous out-of-circuit fistula instead of peritonitis from the leaking stump.

For patients with rectal sparing, a colectomy with ileorectal anastomosis prevents or delays the need of permanent ileostomy. For this operation to be optimal, anal sphincters should be normal and there should be no or minimal anal disease. In an effort to better select individuals suitable for ileoproctostomy measuring maximum tolerated rectal volume of not less than 150 ml and subjective evidence of rectal compliance as indicated by distention with proctoscopic air insufflation may be helpful.

Surgery for large bowel disease has always generated debate as to whether bowel conversation should be practiced with the understanding that recurrence rates may be increased with lesser procedures. Bernell et al retrospectively evaluated 833 patients who underwent surgery for Crohn's colitis and reported cumulative 10 year risk for symptomatic recurrence were as follows: segmental colectomy with anastomosis, 47%; total colectomy with ileoproctostomy, 58%; total colectomy with ileostomy, 24%; and proctocolectomy with ileostomy, 37%. Similar favorable results for segmental resection was reported by Andersson et al where patients with segmental resection had fewer symptoms, more formed stools, and better anorectal function and similar recurrence rates as individuals undergoing total colectomy. Multivariate analysis revealed that the number of excised colonic segments was the strongest predictor of postoperative symptoms, and anorectal dysfunction. This operation is particularly considered in older patients and patients who have had a significant amount of small bowel resected.

Perineal Disease

The perianal abnormalities associated with Crohn's disease include edematous skin tags or hemorrhoids, cyanotic, discoloration, fissures or canal ulceration, abscesses, fistulas, and anorectal stricture. Patients with colonic disease are more likely to have perianal manifestations than those with ileocolic or small bowel disease patterns. Surgery is reserved for symptomatic problems. If the patient is too uncomfortable for an adequate evaluation, a well-conducted examination under anesthesia is mandated. Simple incision and drainage of the abscess will adequately relieve the acute symptoms and allow resolution of the inflammation. A small 12-14 Fr mushroom-tipped catheter placed into the abscess cavity allows continued drainage for several days.

Anal fistulas represent one of the most challenging dilemmas in the treatment of Crohn's disease. As in most components of Crohn's disease, therapy is directed at alleviating symptoms while avoiding side effects. The treatment is usually based upon fistula's location and complexity, the presence or absence of concomitant proctitis, and the severity of accompanying anal canal disease. Most low-lying fistulas can be managed by fistulotomy. If the fistula is high and fecal incontinence is a concern a chronic non cutting seton may ensure adequate drainage. The soft nonreactive nature of Silastic vessel loops makes them an ideal seton material for longterm fistula management. As with any chronic fistula the risk of malignant generation has been described and therefore the patient should be examined periodically.

For patients with limited rectal inflammation, no cavitating ulceration or anal stenosis the advancement flap may be used. Temporary fecal diversion is not necessary unless the patient is undergoing a repeat advancement flap procedure or an excessive amount of fibrosis was encountered during flap mobilization. In the event that the situation is complicated by anal canal ulceration or stricturing sleeve advancement flap with loop ilestomy may be helpful.

Rectovaginal fistulas typically originate from an anterior ulcer eroding into the vagina. The associated disease dictates whether a simple transanal, transvaginal advancement flap can be used or if a sleeve of rectum will need to be advanced.

Controversy exits in controlling the proximal disease will improve perianal disease. However overall the proximal disease component of a patient with perianal Crohn's disease appears to merit treatment only if intestinal disease is independently symptomatic or obviously interrelated to the perianal component.

As there is no cure for Crohn's disease, the primary treatment goals are amelioration of symptoms and prevention of future complications. One recalls an Alexander- Williams aphorism that informs us that patients are more likely to be made incontinent by aggressive surgery than by aggressive Crohn's disease.

Duodenal Crohn's Disease

Among patients with Crohn's disease, the duodenum is affected in 1 to 2% of cases. The most common problem is stricture leading to obstructive symptoms. Most patients with Crohn's disease affecting the duodenum can be managed successfully with medical therapy. Surgical approaches are used when obstructive symptoms remain disabling despite medical therapy. Gastrojejunostomy is the simplest and most widely used operation for relief of obstruction. The issue of adding either a truncal or parietal cell vagotomy remains unsettled. Because reoperation after gastrojejunostomy is common in the long term and dumping and reflux may occur, duodenal strictureplasty has been successfully used in selected cases. No randomized trial has yet been done comparing duodenal strictureplasty and gastrojejeunostomy.

Laparascopy

Laparascopy continues to be a very good tool in selective cases. . At many centers, laparascopic resection is commonly used in this setting with reasonable conversion rates and acceptable outcomes. As with all laparascopic bowel surgery, the comfort of the surgeon with laparascopic surgery continues to be the deciding factor along with associated problems like extensive adhesions in redo surgery, abscesses, and internal fistulas.

Conclusion

Crohn's disease is a complex disease incurable disease. Advances in technology, such as interventional radiology, nutritional therapy and anesthesia, just to name a few, provide valuable tools or adjuncts to our overall care of patient requiring surgery for Crohn's disease. Important advances in pharmacologic management such as Remicaid may change the indications and surgical procedures done in the future. Yet the modern management of the patient with Crohn's disease requires the close collaboration of many members of a team. This involves the skills of the gastroenterologist, nutritionist, enterostomal therapist, radiologist, and the anesthesia and surgical personnel.

Surgery for Crohn' s disease continues to evolve and remains largely empiric. Until the cause and cure of Crohn's disease is found, it seems to us that the challenges for the next millennium will be to review and test critically the array of surgical and medical options in current use with strategic goal of obtaining and preserving maximum function and least disability for our patients.

References

  1. Farmer RG, Hawk WA, Turnbull RB. Clinical patterns in Crohn's disease: a statistical study of 615 cases. Gastroenterol 1975;68:627-635.
  2. Higgens CS, Keighley MRB, Allan RN. Impact of preoperative weight loss on postoperative morbidity. JR Soc Med 1981;74:571-5.
  3. Lee ECG, Papaioannou N. Minimal surgery for chronic obstruction in patients with extensive or universal Crohn's disease. Ann R Coll Surg Engl 1982;64:229.
  4. Whelan G, Farmer RG, Fazio VW, Goormastic M. Recurrence after surgery in Crohn's disease: relationship to location of disease (clinical pattern) and surgical indication. Gastroenterol 1985;88:1826-1833.
  5. Scammell BE, Keighley MRB. Delayed perineal wound healing after proctocolectomy for Crohn's colitis. Br J Surg 1986;73:150-2.
  6. Lashner BA, Evans AA, Hanauer SB. Preoperative total parenteral nutrition for bowel resection in Crohn's disease. Digestive Dis Science 1989;34:741-6.
  7. Fazio VW, Tjandra JJ, Lavery IC, Church JM, Milsom JW, Oakley JR. Long-term follow-up of strictureplasty in Crohn's disease. Dis Colon Rectum 1993;36:355-361.
  8. Fazio VW, Tjandra J. Strictureplasty for Crohn's disease with multiple long strictures. Dis Colon Rectum 1993;36:71.
  9. Ozuner G, Fazio VW. Management of gastrointestinal bleeding after strictureplasty for Crohn's disease. Dis Colon Rectum 1995;38:297-300.
  10. Fazio VW, Marchetti F, Church J, Goldblum J, Lavery I, Hull T, Milsom J, Strong S, Oakley J, Secic M. Effect of resection margins on the recurrence of Crohn's disease in the small bowel. A randomized controlled trial. Ann Surg 1996;224:563-573.
  11. Sasaki I, Funayama Y, Naito H, et al. Extended strictureplasty for multiple short skipped strictures of Crohn's disease. Dis Colon Rectum 1996;39:342.
  12. Ozuner G, Fazio VW, Lavery I, Milsom J, Strong S. Reoperative rates for Crohn's disease following strictureplasty. Dis Colon Rectum 1996;39:1199-1203.
  13. Michellasi F. Side-to side isoperistaltic strictureplasty for multiple Crohn's strictures. Dis Colon Rectum 1996;39:345.
  14. Hull TL, Fazio VW. Surgical approaches to low anovaginal fistula in Crohn's disease. Am J Surg 1997;173:95-8.
  15. Marchesa P, Hull TL, Fazio VW. Advancement sleeve flaps for treatment of severe perianal Crohn's disease. Br J Surg 1998;85:1695-1698.
  16. Fazio VW, Aufses AH Jr. Evolution of Surgery for Crohn's Disease: a century of progress. Dis Colon Rectum 1999;42:979-968.
  17. Worsey MJ, Hull TL, Ryland L, Fazio V. Strictureplasty is an effective option in the operative management of duodenal Crohn's disease. Dis Colon Rectum 1999;42:596-600
  18. Strong SA, Fazio VW. The surgical management of Crohn's disease. Inflammatory Bowel Disease, Fifth Edition. Kirsner JB, Hanauer SB (eds). Saunders Company, Orlando, Florida, 2000.
  19. Bemelman WA, Ivenski M, van Hogezand RA, et al.: How effective is extensive nonsurgical treatment of patients with clinically active Crohn's disease of the terminal ileum in preventing surgery? Dig Surg 2001;44:284-287.
  20. Wolf BG. Resection margins in Crohn's disease Br J of Surg 2001;88:771-772.
  21. Bernell O, Lapidus A, Hellers G. Recurrence after colectomy in Crohn's colitis. Dis Colon Rectum 2001:44:647-654.
  22. Regimbeau JM, Panis Y, Pocard M, et al. Long-term results of ileal pouch-anal anastomosis for colorectal Crohn's disease. Dis Colon Rectum 2001;44:769-778.
  23. Hurst RD, Gottlieb LJ, Crucitti P, et al. Primary closure of complicated perineal wounds with myocutaneous and fasciocutaneous flaps after proctectomy for Crohn's disease. Surgery 2001;130:767-772.
  24. Dietz DW, Laureti S, Strong SA, Hull TL, Church J, Remzi FH, Lavery IC, Fazio VW. safety and long-term efficacy of strictureplasty in 314 patients with obstructing small bowel Crohn's disease. J Am Coll Surg 2001;192:330-338.
  25. Schraut WH. The surgical management of Crohn's disease. Gastroenterol Clin N Am 2002;31:255-263.
  26. Strong SA. Surgical treatment of inflammatory bowel disease. Curr Opin Gastroenterol 2002;18: 441-446.
  27. Borley NR, Mortensen NJMcC, Chaudry MA, Mohammed S, Warren BF, George BD, Clark T, Jewell DP, Kettlewell MGW. Recurrence after abdominal surgery for Crohn's disease: relationship to disease site and surgical procedure. Dis Colon Rectum 2002;45:377-383.
  28. Anderson P, Olaison G, Hallbook O, et al. Segmental resection or subtotal colectomy in Crohn's colitis? Dis Colon Rectum 2002;45:47-53.