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(Radiology. 1999;211:743-746.)
© RSNA, 1999


Gastrointestinal Imaging

The Accordion Sign at CT: a Nonspecific Finding in Patients with Colonic Edema1

Michael Macari, MD, Emil J. Balthazar, MD and Alec J. Megibow, MD

1 From the Department of Radiology, NYU Medical Center, Tisch Hospital, 560 First Ave, Suite HW 202, New York, NY 10016. Received July 28, 1998; revision requested August 18; revision received September 2; accepted November 25. Address reprint requests to M.M.


    Abstract
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To determine whether the "accordion sign" is a specific computed tomographic (CT) sign of Clostridium difficile colitis.

MATERIALS AND METHODS: Fifty-seven patients with CT evidence of severe colitis, as judged by colonic wall thickening, an abnormal haustral pattern, the target sign, and stranding of the pericolic fat, were identified from a computerized CT database for 25 months. CT images were retrospectively evaluated for the presence of oral contrast material in the colon and for the accordion sign. The medical and laboratory records of all patients were reviewed and correlated with CT findings to establish the cause of colitis.

RESULTS: Oral contrast material had reached the colon in 35 of 57 patients at the time of the CT examination. The images in 15 of these patients demonstrated the accordion sign, and those in 20 patients did not. C difficile colitis was documented in four of the 15 cases displaying the accordion sign. In the remaining 11 patients, a different cause was documented. Oral contrast material had not reached the colon in the remaining 22 patients. Within this group with findings similar to the accordion sign, five patients had documented C difficile colitis, and four had colitis from other causes.

CONCLUSION: The accordion sign is indicative of severe colonic edema or inflammation, but it is not specific for C difficile colitis.

Index terms: Colitis, 75.2043, 75.261, 75.266, 75.269 • Computed tomography (CT), colon, 75.12112


    Introduction
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The accordion sign was originally defined as alternating edematous haustral folds separated by transverse mucosal ridges filled with oral contrast material, simulating the appearance of an accordion (1,2). This computed tomographic (CT) finding has been reported to be a specific sign of severe Clostridium difficile–related colitis (1,3). In cases of C difficile colitis, the high-attenuating oral contrast material is trapped between thickened edematous folds and pseudomembranes in the colonic mucosa. The degree of colonic wall thickening caused by the pseudomembranes and edematous tissues that develop in this condition has been suggested as the reason for the sign's specificity (1,3).

We have identified the accordion sign on CT scans obtained in patients with and those without C difficile colitis. Consequently, we performed a retrospective study to determine the frequency with which the accordion sign is identified on CT scans in patients with severe colitis and to determine its specificity for C difficile colitis.


    MATERIALS AND METHODS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
From April 1996 through May 1998, all patients with a CT-based diagnosis of severe colitis were retrospectively identified from a computerized CT database. CT cases consistent with colitis were entered into the database on the basis of the readers' assessment of findings that were indicative of severe inflammation. Cases with mild findings may not have been entered. Findings of "severe" colitis included marked colonic wall thickening, an abnormal haustral pattern, a "target" appearance of the colonic wall (ie, low attenuation in the submucosa surrounded by a hyperattenuating serosa), and pericolonic inflammatory changes.

All CT examinations were performed with HiSpeed Advantage machines (GE Medical Systems, Milwaukee, Wis). Helical CT of the abdomen and pelvis was performed by using the following parameters: 7-mm collimation, 7–10 mm/sec table speed with a 1.0:1.4 pitch, 120 kV, and 210–260 mA. Image acquisition began 60–80 seconds after the initiation of an intravenously administered bolus of contrast material (either 150 mL of iothalamate meglumine [Conray 60; Mallinckrodt Medical, St Louis, Mo] or 150 mL of iopromide [Ultravist; Berlex Laboratories, Wayne, NJ]) that was power injected through an arm vein at 1.0–2.5 mL/sec. In addition, 800 mL of dilute barium sulfate suspension (Readi-Cat 2; E-Z-EM, Westbury, NY) was ingested in small increments, beginning 1.0–1.5 hours before CT scanning began.

Fifty-seven patients (40 women, 17 men; mean age, 40 years; age range, 20–99 years) were identified, and their CT studies were retrieved and reviewed. The CT studies were retrospectively reviewed by two experienced gastrointestinal radiologists (M.M., E.J.B.), together and by consensus, for the presence of (a) an appearance consistent with the accordion sign, (b) oral contrast material in the colon, and (c) a thickened, low-attenuating colonic wall. Retrospective evaluation of the CT studies was performed without knowledge of the final diagnosis.

Subsequently, the cause of the colitis in each patient was documented by reviewing the endoscopic biopsy and laboratory results in 54 patients and the surgical results in three patients. All three patients who underwent surgery had ischemic colitis. Confirmation of C difficile colitis was based on a stool assay positive for C difficile cytotoxin. In those patients with stool assays that were negative for C difficile cytotoxin, an alternate diagnosis was made on the basis of a combination of laboratory, endoscopic, and clinical findings in all but two patients. A specific diagnosis was not established in the two patients despite laboratory, endoscopic, and clinical findings. These two patients were considered to have "nonspecific colitis."


    RESULTS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In 35 of 57 patients, oral contrast material was present in the colon at the time of the CT examination. In 22 patients, the oral contrast material had not reached the colon. The accordion sign was present on the images obtained in 15 (six men and nine women) of the 35 patients with contrast material in the colon (Table 1). In these patients, the accordion sign was identified diffusely (n = 6) or segmentally (n = 9) within the colon at CT. The accordion sign was owing to the following entities with colonic edema: cirrhosis in four patients, C difficile in four patients, ischemia in two patients, nonspecific colitis in two patients, and Campylobacter species, Salmonella species, and Shigella species in one patient each. The appearance of the accordion sign was similar regardless of its cause (Figs 13). The remaining 20 patients with oral contrast material in the colon but without the accordion sign were six men and 14 women. In these patients, the cause of the colitis was C difficile in 10 patients, ulcerative colitis in four patients, ischemia in two patients, granulomatous (or Crohn) colitis in two patients, neutropenia in one patient, and cytomegalovirus in one patient.


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TABLE 1. Cases of Colonic Edema with the Accordion Sign
 


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Figure 1. Accordion sign in a 50-year-old woman with C difficile colitis. Marked submucosal edema (arrows) is present in the right colon. Oral contrast material (arrowhead) is trapped within the lumen.

 


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Figure 2a. Accordion sign in 44-year-old man with C difficile colitis. (a) Initial CT scan demonstrates markedly thickened and edematous submucosa (short arrow). On this image, the oral contrast material has not yet reached the colon. However, the enhancing mucosa (long arrow) simulates the accordion sign even though oral contrast material is not present. (b) On the follow-up CT scan obtained in the same patient 3 days later, the accordion sign is again depicted with edematous submucosa (arrow). Oral contrast material (arrowhead) is trapped within the lumen. In this case, the accordion sign was identified both with and without oral contrast material in the colon.

 


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Figure 2b. Accordion sign in 44-year-old man with C difficile colitis. (a) Initial CT scan demonstrates markedly thickened and edematous submucosa (short arrow). On this image, the oral contrast material has not yet reached the colon. However, the enhancing mucosa (long arrow) simulates the accordion sign even though oral contrast material is not present. (b) On the follow-up CT scan obtained in the same patient 3 days later, the accordion sign is again depicted with edematous submucosa (arrow). Oral contrast material (arrowhead) is trapped within the lumen. In this case, the accordion sign was identified both with and without oral contrast material in the colon.

 


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Figure 3a. Accordion sign in the right colon in a 42-year-old man with cirrhosis. (a) CT scan of the colon demonstrates the accordion sign with edematous submucosa (arrow). Oral contrast material (arrowhead) is trapped within the lumen. (b) CT scan of the liver demonstrates cirrhosis and a transjugular intrahepatic portosystemic shunt (arrow). Results of endoscopy in this patient demonstrated a normal mucosa, and the stool was negative for C difficile cytotoxin.

 


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Figure 3b. Accordion sign in the right colon in a 42-year-old man with cirrhosis. (a) CT scan of the colon demonstrates the accordion sign with edematous submucosa (arrow). Oral contrast material (arrowhead) is trapped within the lumen. (b) CT scan of the liver demonstrates cirrhosis and a transjugular intrahepatic portosystemic shunt (arrow). Results of endoscopy in this patient demonstrated a normal mucosa, and the stool was negative for C difficile cytotoxin.

 
Of the 22 patients without oral contrast material in the colon, nine (five women and four men) had colonic edema with a marked low-attenuating thickening of the colonic wall (Table 2). In these patients, the accordion sign was identified diffusely (n = 8) or segmentally (n = 1) throughout the colon at CT. The stretched enhancing mucosa in these nine cases had an appearance similar to the accordion sign despite the lack of oral contrast material in the colon (Figs 4,5). The colitis in these patients was caused by C difficile in five patients and by cytomegalovirus, ischemia, cryptosporidiosis, and lupus vasculitis in one patient each. In the remaining 13 patients without oral contrast material in the colon, the colitis was caused by ulcerative colitis in four patients, granulomatous (or Crohn) colitis in three patients, ischemia in three patients, and cytomegalovirus, lupus vasculitis, and Salmonella species in one patient each.


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TABLE 2. Cases of Massive Colonic Edema without Oral Contrast Material in the Colon
 


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Figure 4. Accordion sign in a 43-year-old man with cryptosporidiosis. CT scan of the transverse colon demonstrates the accordion sign without oral contrast material present. The enhancing mucosa (arrowhead) is stretched around markedly thickened submucosal folds (arrow).

 


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Figure 5. Accordion sign in a 50-year-old woman with ischemic colitis. CT scan of the transverse colon demonstrates the accordion sign without oral contrast material present. The enhancing mucosa (arrowhead) is stretched around markedly thickened submucosal haustral folds (arrow). Findings at surgery confirmed ischemic colitis.

 
By combining the two groups—that is, the 15 patients with the accordion sign and oral contrast in the colon and the nine patients with findings similar to the accordion sign but without oral contrast in the colon—a total of 24 patients with massive colonic wall edema (ie, with the accordion sign) were identified. In nine of these 24 patients, C difficile was the cause of the accordion sign. The sensitivity and specificity of C difficile as the cause of the accordion sign were 38% (nine of 24 patients) and 61% (14 of 23 patients), respectively.


    DISCUSSION
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
C difficile is a gram-positive anaerobic bacillus that can cause a spectrum of enteric diseases ranging from mild diarrhea to fulminant life-threatening colitis (4). Almost all cases of pseudomembranous colitis are associated with recent antibiotic therapy (35). Infrequently, a prior history of antibiotic use is not a factor in a documented case of C difficile colitis. Almost all antibiotics, and some antineoplastic agents, have been implicated as factors leading to C difficile colitis (5). By altering the normal colonic flora, antibiotic use allows C difficile to proliferate, which results in the clinical disease (5). Earlier recognition and treatment of C difficile–related colitis with appropriate antibiotics decreases the prevalence of fulminant colitis that may develop in these patients (5).

The CT findings in patients with C difficile colitis have been reported previously (14,6). The results of a study involving 64 patients with stools positive for C difficile cytotoxin, who also underwent CT within 3 days of the positive stool assay, demonstrated poor correlation between the clinical findings and severity of disease as depicted at CT (4). Thirty-nine percent of patients with stools positive for the cytotoxin had no colonic disease detected at CT. However, the patients who demonstrated a nodular haustral pattern or the accordion sign did have a more severe clinical course than did the patients without these findings.

The accordion sign has been detected at CT in 4%–19% of patients with documented C difficile colitis, and it has been described as a sign that is specific for the diagnosis of C difficile–related pseudomembranous colitis (1,2,4,6). Although they were not specifically identified as the accordion sign, massive colonic wall thickening and a similar colonic mucosal pattern have been documented in previous CT reports of colitis from other causes (7).

In our series of 57 patients with CT evidence of severe colitis, the accordion sign was detected in 15 patients. However, an additional nine patients had massive colonic wall thickening at CT. In these patients, the oral contrast material had not yet reached the colon. If the CT examination had been delayed, oral contrast material would have been present in the colon, and the accordion sign, as defined, presumably would have been present (Fig 2). If we include these nine patients, a total of 24 patients (15 with and nine without contrast material in the colon) demonstrated the accordion sign. In nine (38%) of these 24 patients, C difficile was the cause of the colitis. Although this was the largest single causative factor in the development of this sign, 15 (63%) patients in whom the sign was present had other causes. Within this group, cirrhosis with colonic edema (n = 4) and ischemic colitis (n = 3) were most common.

There are several limitations to our study. The frequency with which the accordion sign was identified in this series (in 24 [42%] of 57 patients) was greater than that previously reported (2,4,6). The high frequency with which the accordion sign was identified in the patients in our study is probably related to the selection bias that is inherent with the entering of severe cases in the database as opposed to cases with minimal or no findings. Therefore, we are unable to give a true sensitivity of the presence of the accordion sign in cases of C difficile colitis. However, this study was undertaken to examine the specificity of this sign in C difficile colitis. The pathophysiologic changes that result in the accordion sign are almost always the result of severe colitis. We believe the fact that this finding was present in the cases of severe colitis within this group, irrespective of the cause, supports our contention that the accordion sign has little cause-related specificity.

A second limitation to this study is its retrospective design. A prospective study in which all cases of the accordion sign were identified would have allowed a better understanding of the frequency with which various colitides are the cause.

In conclusion, the results of our study demonstrate that although the accordion sign may be detected in a variety of edematous and inflammatory conditions that affect the colon, it has no cause-related specificity. It may be related to infectious conditions (often C difficile colitis) or inflammatory and ischemic colitis, and it may even be present in patients with edema related to cirrhosis. When the accordion sign is identified on CT studies, it should be viewed as a sign indicative of severe colonic edema of uncertain cause. Correlation with the clinical and laboratory findings should be performed to determine the exact cause.


    Footnotes
 
Author contributions: Guarantor of integrity of entire study, M.M.; study concepts and design, M.M., E.J.B., A.J.M.; definition of intellectual content, M.M.; literature research, M.M.; clinical studies, M.M.; data acquisition and analysis, M.M., E.J.B., A.J.M.; manuscript preparation, editing, and review, M.M., E.J.B., A.J.M.


    References
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. O'Sullivan SG. The accordion sign. Radiology 1998; 206:177-178.[Free Full Text]
  2. Fishman EK, Kavuru M, Jones B, et al. Pseudomembranous colitis: CT evaluation of 26 cases. Radiology 1991; 180:57-60.[Abstract/Free Full Text]
  3. Ros PR, Buetow PC, Pantograg-Brown L, Forsmark CE, Sobin LH. Pseudomembranous colitis. Radiology 1996; 198:1-9.[Free Full Text]
  4. 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.[Medline]
  5. Bartlett JG. Antibiotic-associated diarrhea. Clin Infect Dis 1992; 15:673-581.
  6. 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.[Abstract/Free Full Text]
  7. Balthazar EJ, Megibow AJ, Fazzini E, Opulencia JF, Engel I. Cytomegalovirus colitis in AIDS: radiographic findings in 11 patients. Radiology 1985; 155:585-589.[Abstract/Free Full Text]



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