Download Pseudomembranous Colitis: Spectrum of Imaging Findings with

SCIENTIFIC EXHIBIT
Pseudomembranous
Colitis: Spectrum of
Imaging Findings with
Clinical and Pathologic
Correlation1
Satomi Kawamoto, MD
Karen M. Horton, MD
Elliot K. Fishman, MD
Pseudomembranous colitis (PMC) is a potentially life-threatening acute
infectious colitis caused by one or more toxins produced by an unopposed
proliferation of Clostridium difficile bacteria. PMC is characterized by the
presence of elevated, yellow-white plaques forming pseudomembranes
on the colonic mucosa. These plaques can be visualized at both pathologic
analysis and endoscopy. Plain radiography, contrast enema studies, and
computed tomography (CT) are useful in the evaluation of PMC. Plain
radiography of the abdomen can demonstrate polypoid mucosal thickening, “thumbprinting” (wide transverse bands associated with haustral
fold thickening), or gaseous distention of the colon. A toxic megacolon
with distention and occasionally pneumoperitoneum may be seen in the
most severe cases of PMC involving perforation. At contrast enema studies,
the primary finding in mild cases of PMC is small nodular filling defects
representing the mucosal plaques. With more extensive colonic involvement, the plaques are larger and coalesce to form an irregular bowel wall
margin. Mural thickening and wide haustral folds caused by intramural
edema may also be seen. A contrast enema study is contraindicated in
patients with severe PMC due to the danger of perforation. Common CT
findings include wall thickening, low-attenuation mural thickening corresponding to mucosal and submucosal edema, the “accordion sign,” the
“target sign” (“double halo sign”), pericolonic stranding, and ascites. Familiarity with these imaging characteristics may allow early diagnosis and
treatment and prevent progression to more serious pathologic conditions.
Abbreviation: PMC = pseudomembranous colitis
Index terms: Colitis, pseudomembranous, 75.2043, 75.263 • Colon, CT, 75.12112
RadioGraphics 1999; 19:887–897
1From
the Department of Radiology, Saitama Medical School, Saitama, Japan (S.K.), and The Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins Medical Institutions, Baltimore, Md (K.M.H., E.K.F.). Presented as a scientific exhibit at the 1998 RSNA scientific assembly. Received January 4, 1999; revision requested February
24 and received March 16; accepted March 19. Address reprint requests to E.K.F., Department of Radiology, Johns
Hopkins Hospital, 601 N Caroline St, Baltimore, MD 21287.
©RSNA,
1999
887
Figure 1. Gross specimen of the resected colon
from a 47-year-old woman with severe PMC that developed following antibiotic therapy shows multiple, widely distributed pseudomembranes.
Figure 2. Gross specimen of the resected colon
from a 72-year-old man with severe PMC that developed 1 week after the patient underwent prostatectomy shows confluent pseudomembranes (straight
arrows), marked submucosal edema, and mucosal ulceration (curved arrow).
■
■
INTRODUCTION
Pseudomembranous colitis (PMC) is an acute infectious colitis caused by toxins produced by an
unopposed proliferation of Clostridium difficile
bacteria in the colon (1). C difficile infection is
responsible for virtually all cases of PMC and for
up to 20% of cases of antibiotic-associated diarrhea without colitis (1). Over the past few decades, PMC has emerged as a significant medical problem, largely due to the increased use of
prophylactic and broad-spectrum antibiotics. The
prevalence of PMC continues to rise steadily in
the United States, with recent epidemic outbreaks
reported at a number of institutions (2).
PMC can result in significant patient morbidity
and mortality, especially if it is not diagnosed
early. Overall mortality rates from 1.1% to 3.5%
have been reported for patients with PMC (3,4).
It is important for radiologists to be aware of
this potentially life-threatening condition and its
imaging characteristics because they may be
the first to suggest the diagnosis.
In this article, we discuss and illustrate the
imaging appearances of PMC at plain radiography, contrast enema studies, and computed tomography (CT) and correlate these findings with
pathologic and endoscopic findings.
888 ■
Scientific Exhibit
CAUSES OF PMC
C difficile infection is nosocomial and can be
epidemic or endemic in hospitals or nursing
homes (5). PMC usually occurs as a complication of antibiotic therapy but is also associated
with abdominal surgery, colonic obstruction,
uremia, or prolonged hypotension or hypoperfusion of bowel. It also occurs with increased
frequency in patients with severe debilitating
disease such as lymphoma, leukemia (6,7), and
advanced human immunodeficiency virus infection (8). PMC is a toxin-mediated disease that
requires production of two toxins by the C difficile
organisms for clinical expression. Toxin A is an
enterotoxin, whereas toxin B is a cytotoxin (5).
Although many laboratories assay for only one
of these toxins, both are present, and testing
for both increases sensitivity (9).
CLINICAL MANIFESTATION AND DIAGNOSIS
■
The clinical manifestations of C difficile infection include (in increasing order of severity) absence of symptoms, antibiotic-associated colitis
without pseudomembrane formation, PMC, and
fulminant colitis.
The majority of hospital inpatients infected
with C difficile are asymptomatic (1) or are only
mildly to moderately ill (10). The clinical features of PMC include diarrhea, abdominal tenderness, fever, dehydration, and leukocytosis.
Occasionally, patients with C difficile colitis
Volume 19
Number 4
resulting in the need for surgical intervention.
Today, PMC is essentially a “medical” disease
with less than 1% of patients requiring surgery
(10). However, in patients with a fulminant and
toxic form of PMC who fail to respond to medical therapy, surgical intervention (usually partial colectomy with a temporary diverting ileostomy) can be lifesaving (1,14).
■
Figure 3. Endoscopic images obtained in the same
patient as in Figure 1 show characteristic yellow
plaques representing pseudomembranes completely
involving the visualized segments of the colon circumferentially. The images (numbered 1 through 4)
were obtained in adjacent areas of the colon.
present with or progress to fulminant, life-threatening colitis. Such patients are acutely ill, with
signs and symptoms of lethargy, fever, tachycardia, and abdominal pain (1,11), and may progress
to toxic megacolon and colonic perforation resulting from full-thickness colonic necrosis (3).
Because its manifestations may vary, PMC is
not always recognized by the attending physician. For example, approximately 5% of patients
with PMC may present with signs and symptoms
suggestive of acute abdomen or abdominal sepsis (3,12), leading to unwarranted laparotomy
(3,13).
The diagnosis of PMC depends on the demonstration of C difficile toxins in the stool or of
characteristic adherent yellow plaques 2–10 mm
in diameter at proctosigmoidoscopy or colonoscopy (1).
■
TREATMENT
The treatment of PMC consists of oral administration of metronidazole or vancomycin, and
most patients respond well within 3–4 days (10).
In a study by Morris et al (3), medical therapy
failed in 22% of patients prior to initiation of
treatment with metronidazole or vancomycin,
July-August 1999
PATHOLOGIC FINDINGS
PMC caused by C difficile infection is restricted
to the colon except in patients with ileostomies
or defunctionalized loops of small bowel (5,15).
At gross examination, PMC is characterized by
multiple elevated, yellow-white plaques on the
colonic mucosa forming pseudomembranes (5)
(Fig 1). At histologic analysis, these pseudomembranes are typically seen to arise from a
point of superficial ulceration and are accompanied by an acute or chronic inflammatory infiltrate in the lamina propria. They are composed
of fibrin, mucin, sloughed mucosal epithelial
cells, and acute inflammatory cells and can vary
from a few millimeters to 20 mm in diameter.
With advanced disease, pseudomembranes may
coalesce and eventually slough to leave large areas of denudation (5).
In patients with severe acute PMC requiring
surgical resection, massive transmural edema
has also been observed extending through the
submucosa into the muscularis propria of the
colon (Fig 2). Although mural edema can be
present in acute colitis, it is typically confined
to the mucosa and submucosa (16). Therefore,
a marked degree of transmural edema involving
the colon is probably indicative of severe C
difficile colitis.
■
ENDOSCOPIC FINDINGS
Endoscopy can help establish the diagnosis of
PMC by demonstrating the characteristic adherent yellow plaques (Fig 3). The rectum and sigmoid colon are typically involved, but in approximately 10% of cases colitis is confined to
the more proximal colon and may be missed at
sigmoidoscopy (17). In fulminant colitis, sigmoidoscopy or colonoscopy should not be performed due to the risk of perforation. However,
proctoscopy with minimal insufflation of air may
be a useful diagnostic tool (1).
Kawamoto et al ■
RadioGraphics ■
889
4.
Figures 4–6. (4) Plain radiograph obtained
in the same patient as in Figure 1 shows diffuse
nodular haustral thickening and polypoid mucosal thickening (arrows). (5) Plain radiograph
obtained in a 37-year-old woman with PMC
shows gaseous distention of the transverse colon associated with haustral thickening (arrows).
(6) Plain radiograph obtained in a 47-year-old
woman with PMC shows mild to moderate
haustral thickening associated with contour irregularity limited to the distal transverse and
proximal descending colon (arrows). However,
CT performed the same day demonstrated
thickening of the entire colon (cf Fig 12).
■
RADIOLOGIC FINDINGS
With the increased use of radiologic examinations today, it is important that the radiologist
be aware of the spectrum of imaging findings in
PMC and help determine and direct the correct
course of patient management. Imaging is typically not the method of choice in the diagnosis
of PMC. However, radiologic studies including
plain radiography, barium enema studies, and
CT may suggest the diagnosis.
●
Plain Radiography
Plain radiographic findings in PMC vary depending on the severity and extent of disease. Boland
et al (18) reported radiographic abnormalities
in 32% of 152 hospitalized patients with a positive stool toxin assay, including colonic ileus
(32%), small bowel ileus (20%), ascites (7%), and
890 ■
5.
Scientific Exhibit
6.
nodular haustral thickening (18%). “Thumbprinting” (unusual, wide transverse bands associated with thickening of the haustral folds) and
gaseous distention of the colon have also been
identified (19–22) (Figs 4, 5). Segmental dilatation of the colon may or may not occur in the
same area as the thumbprinting (20). In severe
cases, abdominal radiographs can demonstrate
polypoid mucosal thickening, presumably representing the plaquelike pseudomembranous
plaques protruding into the air-containing lumen (Fig 4). Toxic megacolon with distention
(20) and even colonic perforation (22) with pneumoperitoneum may be seen in the most severe
cases.
Volume 19
Number 4
7.
8.
Figures 7, 8. (7) Image from a double-contrast barium enema study of a patient with PMC demonstrates multiple nodular filling defects throughout the colon (arrows) representing pseudomembranous plaques. (8) Image from a single-contrast barium enema study of a patient with PMC demonstrates
marked haustral thickening and thumbprinting of the colon, most prominently in the transverse and
descending colon. The distal ileum is normal.
Although plain radiography may suggest the
diagnosis of PMC, it is not sensitive. Furthermore, even when radiographs are positive for
PMC, the extent and severity of disease may be
underestimated (23) (Fig 6).
●
Contrast Enema Studies
Since the advent of cross-sectional imaging,
contrast enema studies have played a limited
role in the diagnosis of PMC (24).
Findings at contrast enema studies also vary
depending on the severity and extent of disease. In mild cases, the primary finding is small
nodular filling defects representing the mucosal
plaques (Fig 7). With more extensive colonic involvement, the plaques are larger and coalesce
to form an irregular bowel wall margin (6,7,25).
The serrated outline of the barium column represents barium interposed between the plaquelike
membranes rather than true ulceration with
surrounding edema (26). Mural thickening and
wide haustral folds due to intramural edema may
also be seen (19,21) (Fig 8). An enema study is
contraindicated in patients with severe PMC
due to the danger of perforation (6,25). It may
be performed only in patients in whom clinical
and radiographic findings are equivocal or misleading (25).
July-August 1999
●
CT Scanning
CT has been used increasingly in recent years
for the evaluation of acute abdominal disease
and has proved useful in the diagnosis of PMC
(27–31), especially when the disease is not suspected clinically. In a study of 26 patients with
PMC, Fishman et al (31) found abnormal CT
findings in 23 patients. Common CT findings include wall thickening, low-attenuation mural
thickening corresponding to mucosal and submucosal edema, the “accordion sign,” the “target sign” (“double halo sign”), pericolonic
stranding, and ascites. Although the accordion
sign is highly suggestive of PMC, other findings
such as wall thickening, pericolonic stranding,
and ascites are not very specific and can be
seen in a variety of inflammatory or infectious
diseases of the colon (32). In addition, approximately 5% of patients with PMC present with
signs and symptoms suggestive of acute abdomen or abdominal sepsis (3,12). In these cases,
CT can help suggest the diagnosis and thus
avoid unwarranted laparotomy.
Kawamoto et al ■
RadioGraphics ■
891
9.
10.
11a.
11b.
Figures 9–11. CT scan obtained in a 28-year-old woman with acquired immunodeficiency syndrome who developed PMC following antibiotic therapy for pneumonia shows circumferential thickening of the edematous
wall of the ascending and sigmoid colon. Note the enhancement of the luminal surface (arrowheads), a finding
that indicates mucosal hyperemia. Extensive ascites is also seen. (10) CT scan obtained in a 46-year-old woman
with myeloproliferative disorder who developed PMC following antibiotic therapy for pneumonia demonstrates
eccentric thickening of the colon with relative sparing of the anterior wall of the transverse colon. (11a) CT
scan obtained in a 39-year-old man with a history of pancreatitis with pseudocyst who developed PMC shows
eccentric thickening of the transverse colon (arrow) with relative sparing of the anterior wall. (11b) CT scan
shows more severe involvement of the ascending colon than of the transverse or descending colon. Note the
moderate pericolonic stranding around the ascending colon.
Wall Thickening.—The most common CT finding in patients with PMC is colonic wall thickening, which usually ranges from 3 mm to 32
mm in diameter (mean, 14.7 mm) (31). Mural
892 ■
Scientific Exhibit
thickening may be circumferential (Fig 9), eccentric (Figs 10, 11), smooth, irregular, or polypoid. At CT, wall thickening is often more irregular and shaggy than the typically symmetric
and homogeneous thickening seen in Crohn
disease (31).
Volume 19
Number 4
12a.
12b.
13a.
13b.
Figures 12, 13. (12) Unenhanced (a) and contrast-enhanced (b) CT scans obtained in the same patient as in
Figures 1 and 6 demonstrate a thickened colon wall that enhances markedly after administration of contrast material. Note the presence of ascites and diffuse subcutaneous edema. (13) CT scans obtained in a 23-year-old man
with cystic fibrosis who developed PMC following antibiotic therapy for pneumonia demonstrate marked thickening of the colon wall with intense enhancement of the mucosa and thickened, low-attenuation submucosa
(target sign).
Inflammation of the mucosa and colon wall
may enhance markedly following intravenous
bolus administration of contrast material (Fig 12).
The target sign, which consists of two or three
concentric rings of different attenuation, was
originally described in ulcerative colitis and
Crohn disease and has also been reported in
July-August 1999
PMC (33) (Fig 13). The target sign indicates mucosal hyperemia and submucosal edema or inflammation (34). The rings of varying attenuation are better appreciated during the arterial
phase of enhancement.
Kawamoto et al ■
RadioGraphics ■
893
a.
b.
Figure 15. (a) On a CT scan obtained in a 36-year-old man with chronic renal failure who developed PMC following antibiotic therapy, the accordion sign is best appreciated in the ascending colon. (b) CT scan shows diffuse thickening of the transverse colon and descending colon.
Accordion Sign.—The accordion sign is seen
when orally administered contrast material becomes trapped between markedly thickened
haustral folds, giving the appearance of alternating bands of high attenuation (contrast material)
and low attenuation (edematous haustra) (31,
35) (Figs 14, 15a). The accordion sign is highly
suggestive of PMC, although it is usually seen
only in advanced cases. Its appearance may vary
depending on the degree of edema of the haustral folds and the amount of contrast material
trapped between the folds (35). With significant
fold enlargement, barium that is deeply entrapped
between markedly thickened folds may simulate
intramural tracts (23).
Extent of Disease.—CT may reveal pancolitis
or segmental colitis. In the study by Fishman et
al (31), abnormal bowel wall thickening most
commonly involved the entire colon (12 of 26
patients) (Fig 15b) but also manifested as disease
limited to the sigmoid colon (3 of 26) (Figs 16,
17) or either the right or the transverse colon
(7 of 26) (Fig 18). More localized involvement
of PMC may also be encountered (Fig 19). By
helping determine the extent and location of
colonic involvement, CT can aid the endoscopist. For example, if the disease is not present
in the rectosigmoid colon, proctoscopy and sigmoidoscopy may fail to allow diagnosis.
894 ■
Scientific Exhibit
Figure 14. CT scan obtained in a 34-year-old woman
who developed PMC 5 weeks after undergoing heart
transplantation demonstrates the accordion sign in
the rectosigmoid colon. The thickened, low-attenuation colon wall indicates submucosal edema. Limited
ascites is also seen.
Pericolonic Stranding.—Pericolonic stranding may be identified (Fig 20) but is usually
mild, reflecting the primary mucosal and submucosal nature of PMC (24). The relative paucity of pericolonic inflammation in PMC in combination with marked colonic wall thickening
helps differentiate this disorder from other
colitides (29).
Volume 19
Number 4
16.
17.
Figures 16, 17. (16) CT scan obtained in a 67-year-old man who developed PMC 1 week after undergoing surgery for spine infection shows thickening of the colon wall and haustral folds limited to the rectosigmoid colon.
(17) CT scan obtained in a 78-year-old woman who developed PMC following antibiotic therapy shows nodular
wall thickening limited to the rectosigmoid colon (arrows).
18.
19.
Figures 18, 19. (18) CT scan obtained in a 37-year-old man with acquired immunodeficiency syndrome who
developed PMC following antibiotic therapy demonstrates thickening of the ascending and proximal transverse
colon with an irregular luminal surface. The distal transverse colon and the descending colon have been spared.
(19) CT scan obtained in a 63-year-old man who presented with signs and symptoms of colon obstruction and
had a history of sigmoid colon diverticulitis that had been treated with antibiotics shows a well-defined focal
thickening of the sigmoid colon simulating colon cancer (arrows). Sigmoidectomy was performed, and pathologic findings were consistent with PMC. After sigmoid colon resection, PMC progressed to involve the entire
colon, and the patient underwent partial colectomy.
Ascites.—Ascites is occasionally a direct complication of PMC and tends to occur in severe
cases (Fig 9). However, it may also be due to
coexisting conditions such as portal hypertension, congestive heart failure, and sepsis (36)
(Fig 13). Because ascites is uncommon in other
July-August 1999
inflammatory bowel disease, it may be a helpful
clinical finding. However, ascites has also been
reported in patients with Crohn disease, infectious colitis, and vasculitis and is therefore not
specific for PMC (32).
Kawamoto et al ■
RadioGraphics ■
895
a.
b.
Figure 20. (a) CT scan obtained in the same patient as in Figure 2 demonstrates wall thickening and pericolonic
stranding involving the entire colon. The accordion sign is seen in the ascending colon. (b) CT scan shows bilateral pleural effusions. Some thickening of the colon is seen near the splenic flexure (arrow).
Other CT Findings.—Colonic intramural gas
or pneumatosis coli with or without air in the
intrahepatic portal vein has been reported in severe cases (12,30). Small pleural effusions (Fig
20) and subcutaneous edema are also commonly
seen in patients with severe PMC, although both
findings may be related to the primary disease
or to the patient’s debilitated state.
■
PITFALLS AND CAUTIONS
Radiologic studies including plain radiography,
barium enema studies, and CT may suggest the
diagnosis of PMC. However, imaging findings in
PMC are not specific and may be simulated by
other disorders that also cause focal or diffuse
bowel wall thickening. For example, PMC can
be confused with the acute stage of ulcerative
and granulomatous colitis, inflammatory colitides,
and ischemic colitis. Entities that cause thickening of the colon unrelated to colitis (eg, hemorrhage, colonic lymphangiectasia, leukemic infiltration, diverticulitis) should also be considered
as part of the differential diagnosis (24).
A retrospective study of 64 patients with C
difficile infection and 30 control subjects with
diarrhea who tested negative for C difficile infection revealed that the sensitivity and specificity of CT in the detection of colonic abnormalities were 85% and 48%, respectively (37).
Although CT findings do not necessarily correlate with clinical severity and negative CT findings do not exclude PMC (38), it is important to
896 ■
Scientific Exhibit
be suspicious for the disease because increased
mortality has been associated with delay in diagnosis. Once PMC is suspected, diagnosis can
be confirmed by the presence of toxins in stool
assays and by direct visualization of the pseudomembranous plaques at endoscopy.
■
CONCLUSIONS
PMC is an acute infectious colitis caused by one
or more toxins produced by an unopposed proliferation of C difficile bacteria and usually occurs as a complication of antibiotic therapy.
The clinical manifestation of C difficile infection varies from absence of symptoms to fulminant colitis. Because imaging is being used increasingly in the evaluation of patients with abdominal pain, it is important to recognize the
imaging features of PMC that may suggest the
diagnosis. Early diagnosis and treatment are essential for preventing progression to more serious pathologic conditions.
■ REFERENCES
1. Kelly CP, Pothoulakis C, LaMont JT. Clostridium
difficile colitis. N Engl J Med 1994; 330:257–262.
2. Rubin MS, Bodenstein LE, Kent KC. Severe
clostridium difficile colitis. Dis Colon Rectum
1995; 38:350–354.
3. Morris JB, Zollinger RM Jr, Stellato TA. Role of
surgery in antibiotic-induced pseudomembranous enterocolitis. Am J Surg 1990; 160:535–
539.
4. 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.
Volume 19
Number 4
5. Bartlett JG. Pseudomembranous enterocolitis
and antibiotic-associated colitis. In: Sleisenger
MH, Fordtran JS, eds. Gastrointestinal disease.
5th ed. Philadelphia, Pa: Saunders, 1993; 1174–
1189.
6. Stanley RJ, Melson GL, Tedesco FJ. The spectrum
of radiographic findings in antibiotic-related
pseudomembranous colitis. Radiology 1974; 111:
519–524.
7. Shimkin PM, Link RJ. Pseudomembranous colitis: a consideration in the barium enema differential diagnosis of acute generalized ulcerative
colitis. Br J Radiol 1973; 46:437–439.
8. Cappell MS, Philogene C. Clostridium difficile
infection is a treatable cause of diarrhea in patients with advanced human immunodeficiency virus infection: a study of seven consecutive
patients admitted from 1986 to 1992 to a university teaching hospital. Am J Gastroenterol
1993; 88:891–897.
9. Kader HA, Piccoli DA, Jawad AF, McGowan KL,
Maller ES. Single toxin detection is inadequate
to diagnose Clostridium difficile diarrhea in pediatric patients. Gastroenterol 1998; 115:1329–
1334.
10. Lipsett PA, Samantaray DK, Tam ML, Bartlett
JG, Lillemoe KD. Pseudomembranous colitis: a
surgical disease? Surgery 1994; 116:491–496.
11. Triadafilopoulos G, Hallstone AE. Acute abdomen as the first presentation of pseudomembranous colitis. Gastroenterology 1991; 101:685–
691.
12. Chatila W, Manthous CA. Clostridium difficile
causing sepsis and an acute abdomen in critically ill patients. Crit Care Med 1995; 23:1146–
1150.
13. Medich DS, Lee KK, Simmons RL, Grubbs PE,
Yang HC, Showalter DP. Laparotomy for fulminant pseudomembranous colitis. Arch Surg 1992;
127:847–853.
14. Bradley SJ, Weaver DW, Maxwell NP, Bouwman
DL. Surgical management of pseudomembranous
colitis. Am Surg 1988; 54:329–332.
15. Kralovich KA, Sacksner J, Karmy-Jones RA,
Eggenberger JC. Pseudomembranous colitis
with associated fulminant ileitis in the defunctionalized limb of a jejunal-ileal bypass: report
of a case. Dis Colon Rectum 1997; 40:622–624.
16. Schnitt SJ, Antonioli DA, Goldman H. Massive
mural edema in severe pseudomembranous
colitis. Arch Pathol Lab Med 1983; 107:211–213.
17. Tedesco FJ, Corless JK, Brownstein RE. Rectal
sparing in antibiotic-associated pseudomembranous colitis: a prospective study. Gastroenterol
1982; 83:1259–1260.
18. Boland GW, Lee MJ, Cats A, Mueller PR. Pseudomembranous colitis: diagnostic sensitivity of
the abdominal plain radiograph. Clin Radiol
1994; 49:473–475.
19. Stanley RJ, Melson GL, Tedesco FJ, Saylor JL.
Plain-film findings in severe pseudomembranous colitis. Radiology 1976; 118:7–11.
July-August 1999
20. Hutton L, Keown P. Pseudomembranous colitis
in renal transplant recipients: plain film findings. J Can Assoc Radiol 1981; 32:149–152.
21. Loughran CF, Tappin JA, Whitehouse GH. The
plain abdominal radiograph in pseudomembranous colitis due to Clostridium difficile. Clin
Radiol 1982; 33:277–281.
22. Snooks SJ, Hughes A, Horsburgh AG. Perforated colon complicating pseudomembranous
colitis. Br J Surg 1984; 71:291–292.
23. Jones B, Wall SD. Gastrointestinal disease in
the immunocompromised host. Radiol Clin
North Am 1992; 30:555–577.
24. Ros PR, Buetow PC, Pantograg-Brown L, Forsmark CE, Sobin LH. Pseudomembranous colitis.
Radiology 1996; 198:1–9.
25. Rubesin SE, Levine MS, Glick SN, Herlinger H,
Laufer I. Pseudomembranous colitis with rectosigmoid sparing on barium studies. Radiology
1989; 170:811–813.
26. Sherbon KJ. Radiology in pseudomembranous
colitis. Australas Radiol 1972; 16:66–72.
27. Brunner D, Feifarek C, McNeely D, Haney P.
CT of pseudomembranous colitis. Gastrointest
Radiol 1984; 9:73–75.
28. Megibow AJ, Streiter ML, Balthazar EJ, Bosniak
MA. Pseudomembranous colitis: diagnosis by
computed tomography. J Comput Assist Tomogr
1984; 8:281–283.
29. Merine D, Fishman EK, Jones B. Pseudomembranous colitis: CT evaluation. J Comput Assist
Tomogr 1987; 11:1017–1020.
30. Yankes JR, Baker ME, Cooper C, Garbutt J. CT
appearance of focal pseudomembranous colitis. J Comput Assist Tomogr 1988; 12:394–396.
31. Fishman EK, Kavuru M, Jones B, et al. Pseudomembranous colitis: CT evaluation of 26 cases.
Radiology 1991; 180:57–60.
32. Philpotts LE, Heiken JP, Westcott MA, Gore RM.
Colitis: use of CT findings in differential diagnosis. Radiology 1994; 190:445–449.
33. Gore RM. CT of inflammatory bowel disease.
Radiol Clin North Am 1989; 27:717–729.
34. Balthazar EJ. CT of the gastrointestinal tract:
principles and interpretation. AJR 1991; 156:23–
32.
35. O’Sullivan SG. The accordion sign. Radiology
1998; 206:177–178.
36. Jafri SF, Marshall JB. Ascites associated with antibiotic-associated pseudomembranous colitis.
South Med J 1996; 89:1014–1017.
37. Boland GW, Lee MJ, Cats AM, Gaa JA, Saini S,
Mueller PR. Antibiotic-induced diarrhea: specificity of abdominal CT for the diagnosis of
Clostridium difficile disease. Radiology 1994;
191:103–106.
38. Boland GW, Lee MJ, Cats AM, Ferraro MJ, Matthia AR. Mueller PR. Clostridium difficile colitis: correlation of CT findings with severity of
clinical disease. Clin Radiol 1995; 50:153–156.
Kawamoto et al ■
RadioGraphics ■
897