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DOI: 10.1148/radiol.2233010757
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(Radiology 2002;223:620-624.)
© RSNA, 2002

Gastrointestinal Imaging

Diagnostic Yield of Barium Enema Examination after Incomplete Colonoscopy1

Alice Chong, BAS, Janak N. Shah, MD, Marc S. Levine, MD, Stephen E. Rubesin, MD, Igor Laufer, MD, Gregory G. Ginsberg, MD, William B. Long, MD and Michael L. Kochman, MD

1 From the Departments of Radiology (A.C., M.S.L., S.E.R., I.L.) and Medicine (J.N.S., G.G.G., W.B.L., M.L.K.), Hospital of the University of Pennsylvania, 3400 Spruce St, Philadelphia, PA 19104. Received April 9, 2001; revision requested May 29; revision received September 11; accepted October 10. Address correspondence to M.S.L. (e-mail: levine@oasis.rad.upenn.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To determine the diagnostic yield of barium enema examination for neoplastic lesions larger than 1 cm in diameter in the nonvisualized portion of the colon after incomplete colonoscopy.

MATERIALS AND METHODS: A review of computerized gastroenterology and radiology databases identified 355 patients who underwent incomplete colonoscopy; 158 (44.5%) underwent subsequent barium enema examination (125 double-contrast and 33 single-contrast barium enema examinations). The radiographic reports were reviewed and compared with the endoscopic reports by one author to identify neoplastic lesions larger than 1 cm in the nonvisualized colon after incomplete colonoscopy. Six such lesions were found. In all six cases, the images from the barium enema examinations were reviewed together by two authors to determine the size, location, and morphologic features (polypoid, ulcerated, or annular) of the lesions. Medical, endoscopic, and surgical records were subsequently reviewed by one author to determine whether these represented true- or false-positive radiographic findings.

RESULTS: Barium enema examination depicted six possible lesions in the nonvisualized colon after incomplete colonoscopy; five were found to be true-positive radiographic findings, and one was found to be a false-positive finding. The five true-positive findings included two annular lesions (both adenocarcinomas) and three polypoid lesions (all tubulovillous adenomas, with high-grade dysplasia in one). Thus, neoplastic lesions larger than 1 cm were found on barium enema images in the nonvisualized colon in five (3.2%) of 158 patients after incomplete colonoscopy.

CONCLUSION: Barium enema examination had a diagnostic yield of 3.2% for neoplastic lesions larger than 1 cm in the nonvisualized colon after incomplete colonoscopy.

© RSNA, 2002

Index terms: Barium enema examination, 758.1281, 758.1282 • Colon neoplasms, 752.321, 752.3291 • Colonoscopy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
As an increasing number of colonoscopic examinations are performed, physicians and patients are increasingly faced with the dilemma of an incomplete colonoscopy. Even an experienced endoscopist may be unable to intubate the colon in its entirety to the cecum for a variety of reasons, including a redundant or tortuous colon, marked diverticulosis or circular muscle thickening, obstructing masses or strictures, angulation or fixation of colonic loops, spasm, or poor colonic preparation (1). The reported rate of incomplete colonoscopic examinations has ranged from 4% to 25% (2–5).

When colonoscopy is incomplete, a barium enema examination (preferably a double-contrast barium enema examination) is often performed as the next diagnostic test to evaluate the portion of colon not visualized at colonoscopy. A recent letter to the editor in the New England Journal of Medicine cast doubt on the validity of this policy of performing a barium enema examination to complete the evaluation of the colon after incomplete colonoscopy (6). To our knowledge, however, little data are available in the medical literature about the diagnostic yield of barium enema examination for neoplastic lesions in the nonvisualized portion of the colon when colonoscopy cannot be completed.

The purpose of our investigation, therefore, was to determine the diagnostic yield of barium enema examination for neoplastic lesions larger than 1 cm in diameter in the nonvisualized portion of the colon after incomplete colonoscopy.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A review of the computerized gastroenterology database at our university hospital revealed 3,859 colonoscopic examinations that had been performed by three experienced endoscopists during a 3.5-year period from May 1996 to September 2000.

A subsequent review of the endoscopic reports by two authors (A.C., J.N.S.) revealed that 355 (9.2%) of these 3,859 patients underwent incomplete colonoscopic examinations, in which the endoscopist failed to intubate the colon in its entirety to the cecum. Of the 355 patients who underwent incomplete colonoscopy, the farthest level the endoscope was believed to have reached was the ascending colon in 87 patients (24%), the hepatic flexure in 46 (13%), the transverse colon in 56 (16%), the splenic flexure in 28 (8%), the descending colon in 42 (12%), the sigmoid colon in 81 (23%), and the rectum in five (1%). In the remaining 10 patients (3%), the extent of colonic intubation was not specified. The reasons for incomplete colonoscopy are summarized in Table 1.


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  		TABLE 1. Reasons for Incomplete Colonoscopy in 355 Patients

 
A subsequent review of our computerized radiology database revealed that 158 (44.5%) of these 355 patients underwent barium enema examination, including 125 double-contrast examinations and 33 single-contrast examinations (which were performed if patients were too old, sick, or debilitated to tolerate a double-contrast barium enema or if colonic obstruction was suspected), within 3 months after incomplete colonoscopy. These 158 patients comprised our study group. The group included 50 men and 108 women, with a mean age of 63.7 years (range, 18–91 years). The indications for colonoscopy in these 158 patients are summarized in Table 2. In 157 (99.4%) of the 158 cases, the radiographic reports indicated that the entire colon from the rectum to the cecum had been visualized with barium enema examination. In the remaining case, the proximal colon was not visualized with barium enema examination because of an obstructing carcinoma of the sigmoid colon.


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  		TABLE 2. Indications for Colonoscopic Examination in 158 Patients Who Underwent Barium Enemas after Incomplete Colonoscopy

 
The radiographic reports for these 158 patients were reviewed and compared with the endoscopic reports by one author (A.C.) to identify barium enema examination–diagnosed neoplastic lesions larger than 1 cm in diameter in the area stated to be the nonvisualized colon after incomplete colonoscopy. A size of 1 cm was used as the threshold for these lesions because polyps smaller than 1 cm have a minimal risk of harboring cancer (on the order of 1%), whereas polypoid lesions larger than 1 cm have a risk of 10% or more of harboring invasive cancer (7). These neoplasms larger than 1 cm are therefore recognized as the clinically important lesions that warrant endoscopic or surgical removal (8). A total of six such lesions were found in five double-contrast barium enema examinations and in one single-contrast barium enema examination. In all six patients, the images from the barium enema examinations were reviewed together by two authors (A.C., M.S.L.) to determine the size, location, and morphologic features (polypoid, ulcerated, or annular) of the lesions. There were no disagreements between the radiographic reports and review of the images for these six cases.

Medical, endoscopic, and surgical records were subsequently reviewed by one author (A.C.) to determine whether the lesions represented true- or false-positive radiographic findings. If repeat colonoscopy and/or surgery confirmed the presence of neoplastic lesions larger than 1 cm in the nonvisualized colon at initial colonoscopic examination, the radiographic findings were considered to be true-positive findings. If, however, repeat colonoscopy and/or surgery failed to confirm the presence of neoplastic lesions larger than 1 cm in the nonvisualized colon at initial colonoscopic examination, the radiographic findings were considered to be false-positive findings. The diagnostic yield of the barium enema examination was defined as the number of positive cases (ie, cases with pathologically proved neoplastic lesions larger than 1 cm in the nonvisualized colon after incomplete colonoscopy) divided by the total number of cases.

Our institutional review board approved all aspects of this retrospective study and did not require informed consent from patients whose records were included in the study.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Barium enema examinations depicted six possible lesions in the nonvisualized portion of the colon after incomplete colonoscopy. With use of the surgical findings (five cases) and/or endoscopic findings at repeat colonoscopy to the cecum (two cases) as the criterion standard, five lesions were found to have true-positive radiographic findings and one was found to have a false-positive radiographic finding.

True-positive Radiographic Findings
True-positive neoplastic lesions larger than 1 cm were found on barium enema images in the nonvisualized colon in five (3.2%) of 158 patients after incomplete colonoscopy. The reasons for incomplete colonoscopy in these five patients included poor colonic preparation in two, a redundant colon in one, an obstructing mass lesion in one, and a radiation stricture in one. The five true-positive findings on barium enema images (from four double-contrast barium enema examinations and one single-contrast barium enema examination) after incomplete colonoscopy included two annular lesions (one in the sigmoid and one in the cecum) (Fig 1) and three polypoid lesions (two in the ascending colon and one in the descending colon) (Fig 2). The two annular lesions, which measured 7 and 5 cm in length, respectively, were both found to be poorly differentiated carcinomas at surgery. The three polypoid lesions, which had an average diameter of 2.6 cm (range, 1.2–4 cm), were found to be tubulovillous adenomas (with high-grade dysplasia in one) at repeat colonoscopy (two lesions) and/or surgery (three lesions).



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  		Figure 1. Supine oblique spot radiograph from a double-contrast barium enema examination in a 70-year-old woman with diarrhea shows an annular lesion in the cecum with shelflike borders (arrows). This patient underwent incomplete colonoscopy to the level of the ascending colon because of a tortuous, redundant colon. At surgery, the lesion was found to be a poorly differentiated carcinoma of cecum.

 


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  		Figure 2. Right lateral decubitus overhead radiograph from a double-contrast barium enema examination in a 76-year-old woman with rectal bleeding shows a 2.5-cm lobulated polyp (arrows) in the proximal descending colon. This patient underwent incomplete colonoscopy to the level of the distal sigmoid colon because of a colonic stricture secondary to radiation. At surgery, the lesion was found to be a tubulovillous adenoma.

 
False-positive Radiographic Findings
A false-positive neoplastic lesion larger than 1 cm was found on barium enema images in the nonvisualized colon in one (0.6%) of 158 patients after incomplete colonoscopy. The reason for incomplete colonoscopy in this patient was poor colonic preparation. This one false-positive finding was manifested on the double-contrast barium enema image by a polypoid lesion in the ascending colon that measured 1.1 cm in diameter (Fig 3). The lesion was not detected at repeat colonoscopy to the cecum, so it was assumed to be an artifact on the barium enema image that was related to the presence of adherent stool in the ascending colon.



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  		Figure 3. Supine oblique spot radiograph from a double-contrast barium enema examination in an 18-year-old man with rectal carcinoma shows a 1.1-cm ring shadow (arrows) in the proximal ascending colon that was thought to represent a sessile polyp. This patient underwent incomplete colonoscopy to the level of the splenic flexure because of inadequate preparation. However, the lesion was not detected at repeat colonoscopy to the cecum, so it was considered to be a false-positive radiographic finding, presumably related to presence of adherent stool.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Between 4% and 25% of patients who undergo colonoscopy have incomplete examinations because of a variety of factors that prevent intubation of the entire colon (2–5). The completion rate of colonoscopy can be improved by performing the examination with a thinner, more flexible enteroscope or pediatric colonoscope (9,10). When colonoscopic examinations are incomplete, a barium enema examination is often performed as an ancillary procedure to evaluate the portion of the colon that was not visualized at colonoscopy. However, little published data are available about the utility of barium enema examination as a follow-up diagnostic test after incomplete colonoscopy.

In our study, it was possible to visualize the colon in its entirety to the cecum on barium enema images in 157 (99.4%) of the 158 patients who underwent incomplete colonoscopy. Five (3.2%) of these patients were found to have neoplastic lesions larger than 1 cm in portions of the colon that had not been visualized at colonoscopy. Two patients with annular lesions (Fig 1) had poorly differentiated carcinomas, and three patients with polypoid lesions (Fig 2) had tubulovillous adenomas (with high-grade dysplasia in one). Thus, barium enema examination had a diagnostic yield of 3.2% for clinically important lesions in the nonvisualized portion of the colon after incomplete colonoscopy.

In the only comparable study, to the best of our knowledge, Hagenthau et al (11) found additional neoplastic lesions (including two adenocarcinomas) in the area not seen with colonoscopy in 11 (18%) of 60 patients who underwent double-contrast barium enema examination after incomplete colonoscopy. The higher diagnostic yield of the barium enema examination in this series is presumably related to the fact that lesions smaller than 1 cm were not excluded. In any case, these data provide additional support for the role of barium enema examination as a useful test for detecting neoplastic lesions in the nonvisualized colon after incomplete colonoscopy.

The need to evaluate the colon for proximal neoplasms is influenced by the observation that there has been a gradual shift in the distribution of colorectal cancer toward the right side of the colon (12,13). In various series, as many as one-third to one-half of all colonic polyps and cancers have been located in the right side of the colon proximal to the splenic flexure (5,14). Investigators of recent studies have also found that patients with distal polyps, particularly adenomatous polyps, are more likely to have advanced proximal neoplasms than are patients without distal polyps (15,16). An age of 65 years or older has also been found to be an independent risk factor for advanced neoplasms in the proximal colon (17). Thus, it becomes even more important to evaluate the nonvisualized proximal colon after incomplete colonoscopy in patients who have adenomatous polyps or cancers in the visualized distal colon and in patients older than 65 years.

Apart from our five patients with true-positive radiographic lesions that were not detected at initial colonoscopic examination, one additional patient had a lesion larger than 1 cm on double-contrast barium enema images in the nonvisualized colon after incomplete colonoscopy (Fig 3). This lesion was found to be a false-positive radiographic finding at repeat colonoscopy to the cecum (a false-positive rate of 0.6%). In the past, false-positive rates of 5%–10% have been reported in the literature for polyps larger than 1 cm on double-contrast barium enema images (5,8). Because of the need for repeat colonoscopy when lesions are found on barium enema images in the nonvisualized colon, these false-positive findings unnecessarily increase the cost of the diagnostic work-up in a small percentage of patients. It may also be difficult to confirm the presence of radiographically diagnosed lesions in the proximal colon with repeat colonoscopy in patients who could not be intubated to the cecum at initial colonoscopic examination. If the endoscopist is unable to reach the area in question in the proximal colon on repeat examination, a follow-up barium enema examination or even surgery may be necessary as the next step, depending on the size and morphologic features of the lesion.

Our study is also limited by the fact that endoscopists are not always able to accurately assess the actual extent of colonic intubation after incomplete colonoscopy. It therefore is impossible to completely exclude the possibility that one or more lesions detected on barium enema images in the nonvisualized colon may have represented endoscopic errors (ie, false-negative endoscopic examinations) in portions of the colon that were visualized at colonoscopy.

When a barium enema examination is performed after incomplete colonoscopy, it is often not performed on the same day as the colonoscopic examination because of a sedated patient’s potential difficulty in cooperating for the procedure, as well as concern about excessive intraluminal air or fluid impeding colonic filling or mucosal coating during the barium enema examination. Recently, however, Brown et al (18) found that performing a double-contrast barium enema examination immediately after incomplete colonoscopy allowed evaluation of the entire colon in 94% of patients and revealed additional colonic lesions in 8%, including five malignant tumors not seen at colonoscopy. Unfortunately, it is not specified whether these lesions were in the nonvisualized colon or whether they represented endoscopic errors (ie, missed lesions) in the visualized colon. In any case, this study has shown that double-contrast barium enema examination is a technically feasible examination for evaluating the entire colon immediately after incomplete colonoscopy, avoiding the need for repeat bowel preparation.

Computed tomographic (CT) colonography has also been advocated as a rapid, well-tolerated, noninvasive alternative to barium enema examination that successfully images the entire colon after incomplete colonoscopy (including cases of occlusive colonic carcinoma) in most patients (19–21). This technique yields clinically useful information not only about colonic disease in the nonvisualized colon at colonoscopy but also about extracolonic abnormalities in the abdomen, such as abdominal aortic aneurysms, lymphadenopathy, and tumors (20). CT colonography is therefore another effective technique for evaluating the entire colon after incomplete colonoscopy.

In conclusion, barium enema examination had a diagnostic yield of 3.2% for neoplastic lesions larger than 1 cm in diameter in the nonvisualized portion of the colon after incomplete colonoscopy. Our findings indicate that barium enema examination is a useful test for detecting clinically important colorectal neoplasms in this group of patients.


   FOOTNOTES
 
Author contributions: Guarantor of integrity of entire study, M.S.L.; study concepts and design, A.C., J.N.S., M.S.L., M.L.K.; literature research, A.C.; clinical studies, A.C., J.N.S., M.S.L.; data acquisition, A.C., J.N.S.; data analysis/interpretation, A.C., J.N.S., M.S.L.; manuscript preparation, A.C., M.S.L.; manuscript definition of intellectual content, A.C., J.N.S., M.S.L., I.L., M.L.K.; manuscript editing, revision/review, and final version approval, all authors.


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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