Colon: Non Neoplastic Disease: CT Evaluation of the Colon: Inflammatory Disease
Karen M. Horton MD , Frank M. Corl MS and Elliot K. Fishman, MD
Introduction
The utility of Computed Tomography (CT) in patients with suspected colonic pathology has been well documented. A unique imaging feature of CT is its ability to accurately visualize the bowel wall as well as the pericolonic soft tissues and adjacent structures. Therefore, abdominal CT provides a highly sensitive method for the detection of intramural pathology as well as extraluminal extension of colonic diseases.
CT is particularly valuable for detection and characterization of many inflammatory conditions of the colon including appendicitis, typhlitis, infectious colitis, diverticulitis and inflammatory bowel disease. This article reviews a wide variety of inflammatory conditions that affect the colon and stresses important distinctive imaging patterns that may help to distinguish specific diseases.
Technique
Routine abdominal CT is usually performed after the administration of intravenous and oral contrast. At our institution, the patient routinely drinks approximately 1000-1250cc of a 3% oral Hypaque solution (Nycomed Amersham, Princetom NJ) 60-90 minutes before the scan.
If specific colonic pathology is suspected, it is important to adequately opacify the entire colon. Therefore, oral contrast can be administered the night before the study as well as just prior to the scan. This insures that the contrast has reached the colon and is essential for optimal visualization. Alternatively, in urgent cases, or in patients in whom limited rectosigmoid disease is suspected, positive contrast agents such as Hypaque can be administered per rectum. The use of air and/or water administered through a rectal tube to distend the colon has also been reported to be helpful1, 2. Unlike positive agents, air and water do not interfere with virtual colonoscopy or 3D CT angiography.
Although the administration of intravenous contrast is not essential for the diagnosis of many colonic conditions, it is often helpful, especially if extracolonic extension of disease is also suspected. At our institution we routinely administer 100-120 cc of Omnipaque 350, at a rate of 2-3 cc/sec.
The abdomen should be routinely imaged from the level of the diaphragm through the symphysis pubis. Using spiral CT, 5 collimation is usually adequate, using a table speed of 8 mm/sec and reconstruction of the dtata at 5 mm intervals.
Normal Colon
The colon can usually be distinguished from small bowel by its location, appearance and the presence of haustra . The colon normally frames the abdomen and is surrounded by homogeneous fat.
Variations in colon position are not uncommon, and are usually of little clinical significance. For example, there is significant variation in cecal position depending on the length of its mesentery and extent of retroperitonealization. In addition, the colon can be redundant, resulting the drooping of the transverse colon into the lower abdomen or extension of the sigmoid out of the pelvis into the lower abdomen. Chilaiditi's syndrome is an anatomic variant where there is interposition of the hepatic flexure and transverse colon between the liver and right hemidiaphragm . This is usually an incidental finding, is often transient but can rarely causes symptoms from obstruction or volvulus. Another common variant is seen when the colon occupies and empty renal fossa secondary to nephrectomy, renal agenesis, or pelvic kidney .
The transverse diameter of the colon varies. The cecum, the largest portion of the colon, should measure less than 9 cm in diameter. The transverse colon usually measures less than 6 cm in diameter, and the descending/sigmoid colon is usually slightly smaller in caliber. The wall of the colon is very thin and should measure less than 3 mm3. In fact, it should be barely perceptible if the colon is well distended with contrast. Gas, feces, and minimal fluid are normally present within the colon.
Inflammatory Conditions
Appendicitis
Acute appendicitis is a common cause of right lower quadrant pain. It occurs when the appendiceal lumen becomes occluded, resulting in an accumulation of fluid, appendiceal dilation, inflammation, ischemia and eventually perforation with possible abscess formation . Reported accuracy rates of helical CT for the diagnosis of appendicitis are as high as 98%4.
The normal appendix can be often reliably identified on routine CT scan of the abdomen4. It appears as a small thin walled tubular structure arising from the cecum between the ileocecal valve and the cecal tip . The appendix can be variable in length, measuring up to 20 cm. Usually the appendix lies anterior and inferior to the cecum although a retrocecal appendix occurs in up to 25% of patients. The normal appendix is surrounded by homogeneous low density fat.
There is continued debate in the literature regarding the optimal technique for CT examination of patients with suspected appendicitis. Some investigators advocate a dedicated focused appendiceal examination which is more cost efficient then a full abdominal and pelvis CT5, although this may limit the ability to establish alternative diagnoses. Also there is controversy regarding the need for oral, rectal and or IV contrast4.
On CT, an abnormal appendix will appear dilated (>6mm) and unopacified with a thickened wall that may homogeneously enhance after the administration of intravenous contrast . The appendix may be filled with fluid or debris. An appendicolith can be detected in up to 25%-40% of cases6. The presence of an appendicolith along with pericecal inflammation or mass is considered diagnostic for appendicitis .
A hallmark of acute appendicitis is the presence of varying degrees of inflammatory thickening in the fat surrounding the diseased appendix. Stranding of the pericecal fat has a reported sensitivity of 100%, with an 80% specificity7. The presence of pericecal inflammatory changes, without definite identification of an abnormal appendix is suspicious for acute appendicitis, but not diagnostic, as many other conditions such as Crohn's disease or cecal diverticulitis may have inflammatory changes. However, the presence of a dilated thickened appendix, even without pericolonic inflammation, is suggestive of possible appendicitis. Less specific signs such as cecal wall thickening, paracolic gutter fluid, and phlegmon may also be present7.
Perforation is a potential complication of appendicitis and appears as small pockets of extraluminal air or pneumoperitoneum. Appendiceal abscesses appear as a pericecal fluid collection which may contain air or necrotic debris and is surrounded by inflammatory changes . Less common complications include hepatic abscess or small bowel obstruction.
Diverticulitis
Diverticulosis is a common condition in Western society, affecting between 5- 10 percent of the population over 45 years of age8. Diverticula can occur anywhere throughout the colon but are most common in the sigmoid. They represent small outpouching of the colonic mucosa through the muscular layers of the wall. Diverticula usually range in size from 2-3 mm up to 2 cm .
Acute diverticulitis occurs when the neck of a diverticulum is occluded by stool, inflammation or food particles resulting in a microperforation of the diverticula and surrounding pericolonic inflammation. Left sided diverticula more commonly lead to diverticulitis, while right sided diverticula more frequently bleed.
CT is well suited for the evaluation of diverticular disease, as it is able to image the wall of the colon as well as the surrounding pericolonic fat. On CT, diverticulosis appears as small air filled outpouchings of the wall of the colon, most abundant in the sigmoid colon . The wall of the colon may appear thickened due to muscular hypertrophy.
Diverticulitis appears as segmental wall thickening and hyperemia with inflammatory changes in the pericolonic fat . An abscess can be seen in up to 30% of cases and appears as a fluid collection with surrounding inflammatory changes9 . The center of the collection may contain air or air fluid levels or have low attenuation representing necrotic debris.
CT also allows detection of other complications of diverticulitis such as colovesical fistula or perforation and is more sensitive than contrast enema10, 11. Colovesical fistula is suspected when air is seen in the bladder and there is thickening of the bladder wall adjacent to a diseased segment of bowel (usually sigmoid) 10 . Focal contained perforations appear as small extraluminal pockets of air or extravasation oral contrast material. CT also provides guidance for percutaneous drainage of diverticular abscesses, which can eliminate the need for emergent surgery, thus permitting an elective single-stage resection, after proper patient preparation12 .
One potential pitfall of the CT diagnosis of diverticulitis is overlapping imaging findings in diverticulitis and colon cancer . In a study by Padidar et al of 69 patients with sigmoid diverticulitis and 29 patients with sigmoid colon cancer, the presence of fluid in the root of the sigmoid mesentery and engorgement of adjacent sigmoid mesenteric vasculature favor the diagnosis of diverticulitis13. However, in some cases it may not be possible to distinguish diverticulitis from colon cancer with CT alone, and histologic samples will be required.
Typhlitis
Typhlitis, also known as neutropenic enterocolitis, is a condition which occurs in neutropenic patients undergoing treatment for a malignancy, most frequently in patients with acute leukemia on chemotherapy14. However, It has also been reported in patients with aplastic anemia, lymphoma, after kidney transplantation, and in patients with AIDS15. Typhlitis is characterized by edema and inflammation of the cecum, ascending colon and sometimes terminal ileum. The inflammation can be so severe that transmural necrosis, perforation and death can result. The etiology of the condition is not known but probably represents a combination of ischemia, infection (especially CMV), mucosal hemorrhage and perhaps neoplastic infiltration15. Treatment consists of antibiotics and aggressive fluid and electrolyte replacements.
CT is the study of choice for the diagnosis of typhlitis, due to the risk of bowel perforation with colonoscopy or contrast enema. CT demonstrates cecal distention and circumferential thickening of the wall, which may have low attenuation secondary to the edema16 (Fig. 16). Inflammatory stranding of the adjacent mesenteric fat is a common finding. Complications such as pneumatosis, pneumoperitoneum, or pericolonic fluid collections can also be present16. CT is also helpful to assess response to treatment, and to identify patients in need of surgical resection (intramural air)15.
Due to its involvement of the cecum, differentiation of typhlitis from appendicitis or Crohn's disease can be difficult, although the clinical presentation and history are usually distinct.
Radiation Colitis
Radiation therapy can result in injury to colon. More than half of patients receiving more than 3000cGy radiation therapy to the pelvis will experience an acute proctitis manifested by pain, diarrhea, tenesmus and rectal bleeding17. This is typically treated symptomatically, is self limited and does not require imaging.
Chronic radiation injury of the colon and rectum can lead to a variety of complications, with most patients presenting between 6 and 24 months after the completion of therapy18. The sigmoid and rectum are most commonly affected, as radiation therapy is often given for pelvic pathology19. CT findings include nonspecific wall thickening, typically in the rectum, increased pelvic fat accumulation and thickening of the perirectal fibrous tissue are also seen 20. Stricturing and fistula are possible complications. The clinical history is the key to suggesting the diagnosis, as the CT findings can be very nonspecific.
Inflammatory Bowel Disease
Although classic barium contrast studies remain the principle tools for the diagnosis and evaluation of suspected inflammatory bowel disease, CT can sometimes aid in differentiating Crohn's disease and Ulcerative colitis (UC) when barium studies are equivocal. In addition, CT plays an important role in detection of complications of inflammatory bowel disease.
There may considerable overlap of the CT findings in Crohn's disease and ulcerative colitis. However, there are often certain features present which may help distinguish the two. Extensive involvement of right colon and small bowel more common in Crohn's, although involvement of the left colon and rectosigmoid does occur . In contrast, UC is typically left sided or diffuse, and only rarely involves the right colon exclusively19 . On CT, the most frequent finding in both Crohn's disease and ulcerative colitis is wall thickening. The mean wall thickness in Crohn's colitis( 11-13 mm) is usually greater than in UC (7.8 mm) 19, 21. Wall thickening in UC may be diffuse and symmetric, while wall thickening in Crohn's may be eccentric. The asymmetry of the disease involvement in Crohn's disease can result in the formation of pseudodiverticula which appear as outpouching of the colonic formedopposite eccentric regions of scarring and fibrosis. This discontinuous appearance ("skip areas") is an important feature which distinguishes Crohn's disease from ulcerative colitis, which usually appears confluent, continuous and circumferential.
The halo sign, a low attenuation ring in the bowel wall due to deposition of submucosal fat, is seen more commonly in UC than Crohn's colitis. In Crohn's disease, the bowel wall tends to enhance homogeneously, although edema within the wall may result in low attenuation19. Proliferation of mesenteric fat is seen almost exclusively in Crohn's, while the proliferation of perirectal fat is nonspecific and can be present in Crohn's, UC, Pseudomembranous colitis, or radiation colitis .
The presence of mesenteric lymphadenopathy suggests Crohn's rather than UC, although is certainly not specific for inflammatory bowel disease. Complications of IBD can be imaged with CT, and, in the case of Crohn's disease has been shown to effect patient management in 28% of cases21. Abscess formation is detected almost exclusively in Crohn's, not UC19, 22. Abscesses can be confined to the bowel wall and pericolonic fat, or can involve adjacent structures such as the bladder, psoas muscle, or pelvic sidewall (Fig 22).
Fistulae can also be reliably detected with CT. Enterovesical, enterocutaneous, perianal, rectovaginal fistulae have all been detected with CT. If enterovesical fistula is suspected, it is often helpful to perform the CT with oral/rectal contrast but no intravenous contrast. If positive contrast is detected in the bladder, it originated from the bowel and therefore enterocutaneous fistula is confirmed. If intravenous contrast is administered, positive contrast can reach the bladder via the ureters or bowel. Other CT findings of enterovesical fistula include air within the bladder and or focal bladder wall thickening adjacent to a diseased loop of bowel. Enterocutaneous, perianal and rectovaginal fistulae may be diagnosed by detecting oral or rectal contrast within the actual fistulous tract. Alternatively, for greater sensitivity, positive contrast can be injected into the fistula and its connection to the bowel can be determined. In our experience, this technique is usually more successful under real time fluosocopy rather than CT, as it usually requires probing and repositioning of the catheter during injection. However, in difficult cases, the tract can be injected under fluosocopy and then a non contrast CT can be performed, if necessary.
Ischemic colitis
Ischemic colitis is a common cause of abdominal pain in the elderly and results when blood flow to the colon is compromised, usually as a result of hypoperfusion in the inferior mesenteric artery distribution. Most patients are over 70 years of age and many have a history of heart disease23. The extent and severity of the affected colon vary with etiology (hypoperfusion vs. thrombus vs. trauma). Most cases of transient ischemia result in full resolution. Strictures are common complications of more serous episodes. If severe, ischemic bowel may become infarcted, which is a life threatening condition requiring immediate surgical resection.
Radiologic assessment of potential ischemia, traditionally consisted of plain films of the abdomen, barium studies and angiography. However, with continued technologic advancement, CT is being used with increasing frequency in the evaluation of patients with suspected colonic ischemia.
In patients with colonic ischemia, CT typically demonstrates circumferential, symmetric wall thickening with fold enlargement . A double halo or target sign may also be present. Inflammatory changes in the pericolonic fat may also be present24. Ischemic colitis can be diffuse or segmental . Watershed areas of the colon,(splenic flexure and rectosigmoid) are most commonly effected. Right sided colonic ischemia and necrosis has been reported as a complication of hemorrhagic shock after blunt or penetrating trauma25.
Pneumatosis with or without air in the mesenteric vessels or portal vein is an ominous finding in patients with colonic ischemia and suggesting necrosis . CT is more sensitive than plain film for the detection of pneumatosis and can sometimes identify the etiology26. However, the CT findings of pneumatosis coli is not pathognomonic for colonic ischemic and has been reported in benign conditions, including as a late manifestation in patients with AIDS27. Thus, CT can only suggest the diagnosis of ischemic colitis in the appropriate clinical setting.
Graft vs. Host Disease
Graft versus host disease (GVHD) is a complication of allogenic bone marrow transplantation which occurs when the donor lymphocytes in the graft mount an immunologic attack against the host. The skin, liver and gastrointestinal tract (predominantly the ileum and colon) are the primary organs affected.
Findings on CT include small bowel and colonic wall thickening which may result in luminal narrowing and separation of bowel loops . Prolonged contrast coating of the both the small bowel and colon has been reported in patients with severe mucosal disease. In these cases, the barium can actually become incorporated into the bowel wall as the mucosal ulcerations heal28 . This intramural contrast agent is not pathognomonic for graft versus host disease, as it has been described in other conditions which cause severe mucosal ulceration such as ischemic colitis29.
Other CT findings include the presence of a halo of decreased attenuation within the wall, as well as inflammatory changes in the mesentery30 . As opposed to processes like Crohn's disease or radiation enteritis, the length of small bowel involvement in GVHD is more extensive. Once again, the clinical history is most helpful in making the specific diagnosis.
Infectious Colitis
There are many causes of infectious colitis. Bacterial infections include Shigella, Salmonella, Yersinia, Campylobacter, Staphylococcus, and Chlamydia trachomatis. Fungal infection such as histoplasmosis, mucormycosis, and actinomycosis can involve the colon. Viral causes of colitis include herpes, CMV, and Rotavirus. Amebiasis, a protozoan causes a colitis that can resemble inflammatory bowel disease. TB is another cause of colitis. In general, the infectious colidities are typically diagnosed clinically and do not rely on CT for detection or differential diagnosis. They may, however, be identified on CT incidentally or in cases where the patient's clinical symptoms are not straight forward.
On CT, patients with infectious colitis, of any etiology, typically demonstrate wall thickening, which usually displays homogenous enhancement . Low attenuation may be detected within the wall, representing edema. Ascites or inflammation of the pericolic fat may be present19. Multiple air fluid levels may be present in the colon due to increased fluid and fluid feces. Although there is considerable overlap of the appearances of infectious colitis on CT and laboratory studies are necessary for definitive diagnosis, the portion os colon affected may help suggest a specific organism.
For instance, most infectious colitis is limited to involvement of the right colon (Shigella, Salmonella), although diffuse involvement also occurs (CMV, E.coli)15. In contrast, Gonorrhea, herpes and Chlamydia Trachomatis (lymphogranuloma venereum) typically involve the rectosigmoid colon. In addition, schistosomiasis, involvement is usually confined to the descending and sigmoid colon, as the adult worm have a tendency to enter the inferior mesenteric vein.
Pseudomembranous Colitis
Pseudomembranous colitis (PMC) results from toxins produced by an overgrowth of the organism Clostridium difficile and results in a profuse watery diarrhea with abdominal pain and fever. 31. Although first described as a complication of antibiotic therapy, pseudomembranous colitis has also been described with hypotensive episodes, chemotherapeutic agents, following abdominal surgery, and proximal to a large bowel obstruction.
Histologically the condition is characterized by pseudomembranes which represent exudate of necrotic cells from the denuded mucosa . The diagnosis is typically made with stool assay for the C. difficile toxin or by stool culture, but the clinical presentation is often nonspecific. Radiologists should be familiar with the CT findings, as the diagnosis may not be suspected clinically and if not treated aggressively, can result in significant patient morbidity and mortality. 32, 33. Treatment with metronidazole and vancomycin is usually effective. However, some in patients with a fulminant form of PMC may not respond to medical therapy, and therefore will require surgical intervention such as colectomy31, 34.
The most common, but nonspecific CT finding in patients with PMC is thickening of the colonic wall which may be circumferential or eccentric. In one series the average wall thickness was 14.7 mm, significantly greater than wall thickening seen in other inflammatory conditions, such as Crohn's disease35. The bowel wall by be low attenuation due to edema, or may enhance significantly after intravenous contrast secondary to hyperemia . The "target sign" originally described in ulcerative colitis and Crohn's disease has also been reported in PMC. When haustral folds are significantly thickened, they can appear as broad transverse bands which may trap oral contrast. This is known as the "accordion pattern"35 . The accordion sign is very suggestive of PMC, but typically only occurs in severe cases and is therefore not sensitive.
Although PMC is classically a pancolitis, isolated involvement of segments of the colon and rectum has also been reported35 . Ascites has been reported to occur in patients with PMC, both as a direct complication of the infection and due to coexisting conditions such as portal hypertension36. As ascites is not common in other inflammatory bowel disease, it may be a helpful CT finding to suggest the diagnosis of PMC.
Conclusions
Computed tomography (CT) plays an important role in the evaluation of patients with a variety of colonic diseases due to its unique ability to accurately demonstrate the bowel wall as well as adjacent structures. If colonic disease is suspected, careful attention to technique is required for optimal evaluation. With the advent of even faster spiral CT scanners, it is likely that CT will continue to play a significant role in the imaging of colonic pathology.
References
1. Amin Z, Boulos PB, Lees WR. Technical report: spiral CT pneumocolon for suspected colonic neoplasms. Clin Radiol 1996; 51:56-61.
2. Gazelle GS, Gaa J, Saini S, Shellito P. Staging of colon carcinoma using water enema CT. J Comput Assist Tomogr 1995; 19:87-91.
3. Fisher JK. Abnormal colonic wall thickening on computed tomography. J Comput Assist Tomogr 1983; 7:90-97.
4. Rao PM, Rhea JT, Novelline RA, Mostafavi AA, Lawrason JN, McCabe CJ. Helical CT combined with oral contrast material administered only through the colon for imaging of suspected appendicitis. AJR 1997; 169:1275-1280.
5. Rhea JT, Rao PM, Novelline RA, McCabe CJ. A focused appendiceal CT technique to reduce the cost of caring for patients with clinically suspected appendicitis. AJR 1997; 169:113-118.
6. Balthazar EJ, Megibow AJ, Hulnick D, Gordon RB, Naidich DP, Beranbaum ER. CT of appendicitis. AJR 1986; 147:705-710.
7. Rao PM, Rhea JT, Novelline RA. Sensitivity and specificity of the individual CT signs of appendicitis: experience with 200 helical appendiceal CT examinations. J Comput Assist Tomogr 1997; 21:686-692.
8. Ferzoco LB, Raptopoulos V, Silen W. Acute diverticulitis. New Engl J Med 1998; 338:1521-1526.
9. Hulnick DH, MegibowAJ, Balthazar EJ, Naidich DP, Bosniak MA. Computed tomography in the evaluation of diverticuluitis. Radiology 1984; 152:491-495.
10. Labs JD, Sarr MG, Fishman EK, Siegelman SS, Cameron JL. Complications of acute diverticulitis of the colon: improved early diagnosis with computerized tomography. Am J Surg 1988; 155:331-336.
11. Jarrett TW, Vaughan ED Jr. Accuracy of compterized tomography in the diagnosis of colovesical fistula secondary to diverticular disease. J Urol 1995; 153:44-46.
12. Hachigian MP, Honickman S, Eisenstat TE, Rubin RJ, Salvati EP. Computed tomogphy in the inital management of acute left-sided diverticulitis. Dis Colon Rectum 1992; 35: 1123-1129.
13. Padidar AM, Jeffrey RB Jr, Mindelzun RE, Dolph JF. Differentiating sigmoid diverticulitis from carcinoma on CT scans: mesenteric inflammation suggests diverticulitis. AJR 1994; 163:81-83.
14. Wagner ML, Rosenberg HS, Fernbach DJ, Singleton EB. Typhlitis: a complication of leukemia in childhood. AJR 1970; 109:341-350.
15. Wall SD, Jones B. Gastrointestinal tract in the immunocompromised host: opportunistic infections and other complications. Radiology 1992; 185:327-335.
16. Frick MP, Maile CW, Crass JR, Goldberg ME, Delaney JP. Computed tomography of neutropenic colitis. AJR 1984; 143:763-765.
17. Otchy DP, Nelson H. Radiation injuries of the colon and rectum. Surg Clin North Am 1993; 73:1017-1035.
18. Gilinsky NH, Burns DG, Barbezat GO, et al. The natural history of radiation-induced proctsigmoiditis: an analysis of 88 of patients. Q J Med 1983; 52:40-53.
19. Philpotts LE, Heiken JP, Westcott MA, Gore RM. Colitis: use of CT findings in differential diagnosis. Radiology 1994; 190:445-449.
20. Frommhold W, Hubener KH. The role of computerized tomography in the after care of patients suffering from carcinoma of the rectum. J Comput Assist Tomogr 1981; 5:161-168.
21. Fishman EK, Wolf EJ, Jones B, et al. CT evalution of Crohn's disease, effect on patient management. AJR 1987; 148:537-540.
22. Gore RM, Marn CS, Kirby DF, Volgelzang RI. CT findings in ulcerative, granulomatous and indeterminate colitis. AJR 1984; 143:279-284.
23. Abel ME, Russell TR. Ischemic colitis: comparison of surgical and nonoperative management. Dis Colon Rectum 1983; 26:113-115.
24. Jones B, Fishman EK, Siegelman SS. Ischemic colitis demonstrated by computed tomography. J Comput Assist Tomogr 1982; 6:1120-1123.
25. Ludwig KA, Quebbeman EJ, Bergstein JM, Wallace JR, Wittmann DH, Aprahamian C. Shock-associated right colon ischemia and necrosis. J Trauma 1995; 39:1171-1174.
26. Connor R, Jones B, Fishman EK, Siegelman SS. Pneumatosis intestinalis: role of computed tomography in diagnosis and management. J Comput Assist Tomogr 1984; 8:269-275.
27. Wood BJ, Kumar PN, Cooper C, Silverman PM, RK. Z. Pneumatosis intestinalis in adults with AIDS: clinical significance and imaging findings. AJR 1995; 165:1387-1390.
28. Ma LD, Jones B, Lazenby AJ, Douglas T, Bulte JW. Persistent oral contrast agent lining the intestine in sever mucosal disease: elucidation of radiographic appearance. Radiology 1994; 191:747-749.
29. Greves JH 3rd, Bohlman TW, Frische LF, RM K. Intramural barium in ischemic colitis: a new radiographic finding. Am J Dig Dis 1976; 21:257-262.
30. Jones B, Fishman EK, Kramer SS, et al. Computed tomography of gastrointestinal inflammation after bone marrow transplant. AJR 1986; 146:691-695.
31. Kelly CP, Pothoulakis C, LaMont JT. Clostridium difficile colitis. N Engl J Med 1994; 330:257-262.
32. Jobe BA, Grasley A, Deveney KE, Deveney CW, Sheppard BC. Clostridium difficile colitis: an increasing hospital-acquired illness. Am J Surg 1995; 169:480-483.
33. Morris JB, Zollinger RM Jr, Stellato TA. Role of surgery in antibiotic-induced pseudomembranous enterocolitis. Am J Surg 1990; 160:535-539.
34. Bradley SJ, Weaver DW, Maxwell NP, Bouwman DL. Surgical management of pseudomembranous colitis. Am Surg 1988; 127:329-332.
35. Fishman EK, Kavuru M, Jones B, et al. Pseudomembranous colitis: CT evaluation of 26 cases. Radiology 1991; 180:57-60.
36. Jafri SF, Marshall LB. Ascites associated with antibiotic associated pseudomembranous colitis. South Med J 1996; 89:1014-1017.