British Journal of Radiology (2006) 79, 208-214
© 2006 British Institute of Radiology
doi: 10.1259/bjr/99126323
Comparison of Radiologists' confidence in excluding significant colorectal neoplasia with multidetector-row CT colonography compared with double contrast barium enema
S A Taylor, MD, MRCP, FRCR
S Halligan, MD, MRCP, FRCR
A Slater, MRCP, FRCR
D Burling, MRCP, FRCR
M Marshall, MRCP, FRCR
and
C I Bartram, FRCP, FRCS, FRCR
Department of Intestinal Imaging, St Mark's and Northwick Park Hospitals, Harrow, London HA1 3UJ, UK
Correspondence: Dr Stuart Taylor, Department of Specialist X-ray, Level 2, University College Hospital, 235 Euston Road, London NW1 2BU, UK.
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Abstract
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The aim of this study was to compare the confidence of experienced radiologists in excluding colonic neoplasia with CT colonography (CTC) compared with barium enema. 78 patients (median age 70 years, range 61–87 years, 44 women) underwent same day CTC and barium enema. Two radiologists experienced in reporting barium enema assessed whether the examination had excluded a polyp 6 mm or greater as "yes", "probably" or "no" for each of 6 colonic segments. Two different radiologists experienced in CTC independently performed the same assessment on the CT datasets. Responses were compared using a paired exact test. Formal barium enema and CT reports were compared with any endoscopic examination performed within 1 year. Studies reporting polyps 6 mm+ in patients not subsequently undergoing endoscopy were reviewed by two independent observers. Radiologists stated they had confidently excluded a significant lesion in 314 (71%) and 382 (86%) of 444 segments with barium enema and CTC, respectively (p<0.001). Confidence was significantly higher with CTC in the in the descending and ascending colon (p = 0.02 and p<0.001, respectively), and caecum (p<0.001). 22 patients underwent some form of endoscopy. Of five patients with proven colorectal neoplasia (including two with cancer), CTC and barium enema correctly identified five and three, respectively. In 56 patients not undergoing endoscopy, CTC reported 17 polyps 6 mm+, of which 16 were retrospectively classified as definite or probable. 11 could not be identified on the barium enema, even in retrospect. Confidence in excluding polyps 6 mm or larger is significantly greater with CT colonography particularly in the proximal colon.
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Introduction
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Symptoms of colorectal neoplasia are notoriously non-specific with the result that the majority of patients investigated do not harbour significant pathology. Even when applying defined symptom complexes, such as those specified in the recent "2 week wait" initiative [1], the prevalence of significant pathology is increased to no more than 10–15% [2]. Colonoscopy remains the reference standard whole colon examination but is technically demanding, invasive, and associated with a small morbidity and even mortality. Adverse effects are well documented, largely related to the cardiorespiratory effects of sedation [3–6], with some evidence of increased susceptibility amongst the elderly [7].
Radiological alternatives to colonoscopy, including both CT colonography and barium enema, are generally viewed as safer, less invasive investigations [8]. Barium enema remains the standard radiological investigation, although the day-to-day diagnostic performance in comparison with CT colonography has not been assessed in large-scale clinical trials of symptomatic patients. Advocates of CT colonography point to increased patient acceptability [9, 10] and extrapolated higher sensitivity for significant colonic pathology [11, 12]. However, given that most symptomatic patients will not harbour significant colonic neoplasia, one important, but often neglected, consideration is the degree of confidence with which the reporting radiologist can confirm normality and thus spare the patient further expensive and invasive investigations. If CT colonography is to become the standard radiological investigation, the incidence of inconclusive examinations should therefore be at least equal to, and preferably less than that of the barium enema in elderly symptomatic patients.
The purpose of this study was to compare the confidence of experienced radiologists in excluding significant colonic neoplasia with both CT colonography and barium enema in patients undergoing both examinations.
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Materials and methods
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Our local ethical review committee approved the study and all subjects gave informed written consent. All patients 60 years of age or older referred for double contrast barium enema between July 2002 and December 2003 were identified from clinical request cards sent to the Department of Radiology. Only those referred because of a clinical suspicion of colorectal neoplasia were eligible for inclusion. All eligible patients were then invited by letter to additionally undergo CT colonography immediately before barium enema. A total of 78 patients (median age 70 years, range 61–87 years, 44 women) were recruited. Reasons for referral were as follows: change in bowel habit (n = 60); iron deficiency anaemia (n = 10); palpable abdominal mass (n = 8).
CT colonography
CT colonography was performed immediately prior to same day barium enema. Patients underwent the standard bowel purgation regimen used at our institution, consisting of 24 h of a clear liquid diet together with two sachets of sodium picosulphate/magnesium citrate (Picolax; Ferring Pharmaceuticals, Berkshire, UK). No tagging agents were used. All but two patients received 20 mg of intravenous hyoscine butylbromide (Buscopan; Boehringer Ingelheim, Bracknell, UK) prior to gas insufflation. The remaining two patients received intravenous glucagon (Nova Nordisk Pharmaceuticals, Crawley, UK) because of a contraindication to hyoscine butylbromide (both due to recent acute cardiovascular events). Colonic insufflation was performed with carbon dioxide using an automatic insufflator (Protocol; E-Z-EM, Westbury, NY). Insufflation occurred at a rate of 1–2 l min–1 with a maximum intracolonic pressure of 25 mmHg, set using the pump controls, and was continued until patient discomfort, or if distension was deemed adequate by the supervising radiologist from the CT scout image. Patients were then scanned in the supine position using a four detector row CT scanner (Lightspeed plus; General Electric Medical Systems, Milwaukee, WI) and the following parameters: 2.5 mm collimation; pitch of 1.5; 120 kVp; 50 mA; 50% slice overlap. Patients were turned prone and further gas insufflated if a second scout image suggested areas of collapse. A scan in the prone position was then performed using identical CT parameters. Intravenous contrast was not administered.
Barium enema
After CT colonography was complete, patients were escorted from the CT scanner to the fluoroscopy suite. Appointment times were such that there was at least 1 h between completion of CT colonography and commencement of barium enema. Barium enemas were performed by either one of three experienced radiographers (68 patients), or by a radiology trainee (10 patients) according to a standard protocol consisting of multiple digital fluoroscopic spot views of the double-contrasted colon followed by two lateral decubitus over-couch radiographs. The barium preparation (94% w/w, PolibarTM; E-Z-EM, Westbury, NY) was diluted with 700 ml water and instilled via a rectal catheter. Colonic distension was achieved with carbon dioxide introduced by manual compression of the gas-filled enema bag. Patients received a second identical dose of the spasmolytic that had been administered for CT colonography (either hyoscine butylbromide or glucagon) prior to the barium enema.
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Image analysis: CT colonography
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Image analysis was performed using a dedicated workstation with proprietary software (Advantage Windows 4.0 and Colonography; GE Medical Systems, Milwaukee, WI). Two radiologists experienced in CT colonography (defined by prior reading of at least 150 CT colonographic datasets with full endoscopic correlation) independently analysed the CT datasets. Reader one read the first 36 patients and reader two the second 42 patients. Analysis was performed using primary analysis of two-dimensional (2D) axial supine and prone images with multiplanar reformats and 3D endoluminal views reserved for problem solving. For the purpose of the study the colon was divided into six segments using previously published criteria [13]. Readers noted the presence of diverticular disease or colonic neoplasia in each of the six segments on a study sheet designed for the trial. Colorectal neoplasia and diverticular disease were defined using previously well-established criteria [14, 15]. A formal CT report was also generated for the referring clinician as per usual practice.
Readers additionally independently assessed each colonic segment as to whether they could answer the clinical question "has the test excluded a significant colonic lesion?" For the purposes of the trial, a significant colonic lesion was defined as a polyp 6 mm or larger. The readers graded their response for excluding a significant lesion as "yes", "probably" or "no". If the response was "probably" or "no", readers listed reason for non-exclusion as "fluid", "poor distension" or "faecal residue". A significant lesion was by definition not excluded (i.e. "no") if such a lesion was reported as being present in that particular segment.
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Image analysis: barium enema
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All barium enemas were reported on the day they were performed by one of two experienced readers (defined as a radiologist with a declared subspecialty interest in gastrointestinal radiology with at least 5 years experience of reporting more than 4 barium enema examinations per week). These readers were different from the radiologists analysing the CT scans and were blinded to the CT report. Individual readers single read the barium enema studies as they appeared on their clinical lists and a formal report was generated for the referring clinician as per usual practice. Readers one and two read 40 and 38 studies, respectively.
For the purposes of the trial, the colon was again divided into six segments using the same criteria as for CT colonography. Readers noted the presence of diverticular disease or colonic neoplasia in each of the six segments on a study sheet designed for the trial, identical to that for the CT readers. As for the CT, readers additionally independently assessed each colonic segment as to whether they could answer the clinical question "has the test excluded a significant colonic lesion?" (polyp 6 mm or larger), listing their response as "yes", "probably" or "no". If the response was "probably" or "no", readers listed reason for non-exclusion as "poor barium coating", "poor distension", "barium pool" or "faecal residue". Again, a significant lesion was by definition not excluded (i.e. "no") if such a lesion was reported by the radiologist for that particular segment.
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Endoscopic correlation
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After trial completion, a non-observer searched the local endoscopic database to ascertain if patients had undergone any form of endoscopy within 1 year of the barium enema and CT scan (either before or after). There was a time period of 6 months between the CT/barium enema of the last patient recruited and the database search. The trial study sheets were then correlated with the endoscopic report to derive the CT and barium enema sensitivity and false positive rate for colorectal neoplasia. A radiologically detected polyp was deemed true positive if a corresponding polyp was found in the same segment at endoscopy and if the estimated size of the polyp agreed as follows; for polyps less than 6 mm at endoscopy radiological measurement was within ±90%, for polyps 6–9 mm radiological measurement was within ±70%, and for polyps 10 mm or greater radiological measurement was within ±50%. A radiologically detected polyp was deemed false positive if either no polyp was found in the corresponding segment during subsequent endoscopy or if the measured size fell outside the above criteria. If endoscopy had preceded imaging, endoscopically removed polyps were excluded from the comparison. All readers were blinded to the endoscopic data.
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Radiological review
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All cases where a lesion at least 6 mm had been reported on either the CT colonography, or barium enema and yet the patient had not subsequently been referred for endoscopy were identified and reviewed. An independent observer, experienced in CT colonography with audited performance in line with the published literature, reviewed the CT colonography datasets, and another expert gastrointestinal radiologist reviewed the barium enema, both unblinded to the original study reports. If the lesion(s) had been reported on CT colonography alone, the abnormality was found in the CT colonography dataset and classified as "definite", "probable" or "likely false positive" by the independent CT observer. The barium enema was then carefully reviewed to see if the lesion was in retrospect "definitely present", "probably present" or "not identified". If the lesion(s) was identified on barium enema alone, the same process was undertaken in reverse. Lesions reported on both CT colonography and barium enema were classified as "definite", "probable" or "likely false positive" by the independent observers for each modality.
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Statistical analysis
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For the purposes of analysis of radiologist confidence at excluding a significant colonic lesion, the "no" and "probably" responses were combined into a single group and compared with the "yes" responses. The first set of analyses were performed for each segment of the colon separately using a paired exact test (binomial based exact test).
The effect of patient age (categorised into 65 or less versus greater than 65) upon radiologist confidence was also examined using Fisher's Exact test separately for the two procedures. The effects of individual readers on confidence scores were then compared for both barium enema and CT, and any effect on who had performed the barium enema (radiographer or radiology registrar) was sought.
Confidence scores from all six segments were then combined into a single analysis. Because segments in individual patients are not wholly independent of each other, logistic regression with robust standard errors was used for the analysis and any effect of patient age, who performed test and who reported the test was sought by adding each factor to the basic regression model.
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Results
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Radiologist confidence
A total of four patients did not tolerate one of the two tests (four failed barium enema and one also failed CT colonography) and were excluded. Two of the four patients were intolerant of colonic distension (including the one who failed CT colonography) and two were insufficiently mobile to undergo barium enema. A total of 74 patients were thus left for analysis.
Overall, the reporting radiologists stated they had confidently excluded a significant lesion in 314 of 444 segments (71%) with barium enema and in 382 of 444 segments (86%) with CT colonography (p<0.001).
Reasons for non-exclusion (other than reporting a lesion) with barium enema were residue: 41%, poor coating: 12%, barium pools: 32% and poor distension: 15%. Reasons for non-exclusion (other than reporting a lesion) with CT colonography were residue: 35%, fluid pools: 20% and poor distension: 45%.
The number of individual segments in which a lesion was confidently excluded is shown in Table 1
. Radiologists reporting CT colonography were significantly more likely to confidently exclude a significant lesion in the descending and ascending colon (p = 0.02 and p<0.001, respectively) and caecum (p<0.001) compared with those reporting barium enema. There was no significant effect of who had performed the barium enema (p = 0.27), or individual reader (p = 0.35) on overall confidence scores for the barium enema. Similarly there was no significant difference between confidence scores for the two CT colonography readers (p = 0.72).
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Table 1. Radiologist confidence at excluding a significant colonic lesion for barium enema and CT colonography according to colonic segment
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Confidence at excluding a significant lesion was not significantly affected by patient age on an individual segmental basis for either test, or overall for barium enema. However, overall confidence was significantly higher with CT colonography for patients 65 or less compared with those over 65 (odds of excluding a lesion 0.42 (confidence interval 0.20 to 0.89), p = 0.02).
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Endoscopic correlation
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Of the cohort of 78 patients, a total of 22 underwent some form of endoscopy within 1 year of the CT and barium enema. Of the 22 patients 10 underwent colonoscopy as a result of reported positive findings on CT colonography and/or barium enema. Of these 10, 2 colonoscopies were incomplete proximal to the reported abnormality (small polyps up to 8 mm) and have not been repeated. The results of the eight completed endoscopies in comparison with the radiological findings are shown in Table 2. All radiologically detected polyps fell within the size criteria listed above for positive correlation with the endoscopic findings. On a per patient basis, CT colonography correctly identified all four patients with endoscopically proven polyps (one with a single 12 mm sigmoid polyp, one with a rectal cancer and 10 mm ascending colon polyp, and two with several small polyps less than 5 mm) whereas barium enema detected two of the four (missing the two patients with polyps up to 5 mm). CT colonography correctly identified a histologically confirmed rectal cancer, although the same lesion was reported as a polyp on barium enema (Figure 1). In the four patients with confirmed neoplasia there were two presumed CT false positives (10 mm and 6 mm). CT colonography did however suggested a total of six polyps (three 6–9 mm and three 1–5 mm) in four patients in whom both the barium enema and subsequent colonoscopy were reported as normal and were therefore classified as false positives for CT (Figure 2).
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Table 2. Findings of complete colonoscopy performed as a result of reported abnormal radiological(CT colonography or barium enema) findings
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Figure 1. Spot view from a double contrast barium enema demonstrates a large filling defect(arrows) classified as a polyp by the reader. Subsequent histology confirmed invasive carcinoma.
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Figure 2. Presumed CT colonographic false positive.(a) Axial view and (b) CT colonographic endoluminal view demonstrates a 6 mm filling defect (arrows) reported as a polyp but not found on subsequent colonoscopy.
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The remaining 12 of the 22 patients underwent either an incomplete colonoscopy or a flexible sigmoidoscopy prior to the barium enema, which was requested by the clinician to assess the non-visualized colon. In 10 of these patients the limited endoscopy, subsequent barium enema and CT colonography were all reported as normal. In one patient with colonoscopy complete to the distal transverse colon, a caecal cancer was correctly diagnosed by both barium enema and CT colonography, the latter revealing multiple liver metastasis. In the remaining patient with long-standing Crohn's disease and weight loss, CT colonography and barium enema both confirmed a mid transverse colon stricture. Whereas barium enema confidently diagnosed a Crohn's stricture, CT colonography was unable to exclude cancer (Figure 3). Subsequent biopsy excluded malignancy.
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Figure 3. Transverse colonic Crohn's stricture. (a) Double contrast barium enema demonstrated the stricture (arrows) correctly classified as benign by the reader. (b) Axial CT colonographic image shows the short thick walled stricture (arrows) reported as a possible cancer by the reader.
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The remaining 56 patients did not undergo any form of endoscopy either prior or subsequent to the radiological tests. Diverticular disease was reported in 26 on CT colonography and in 30 on barium enema.
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Radiological review
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In 56 patients, CT colonography reported 27 polyps in 19 patients (7: 10 mm+, 10: 6–9 mm and 10: 1–5 mm). Of the 17 polyps 6 mm+ reported on CTC, 10 were classified as definite, 6 as probable and 1 as a false positive, on retrospective review. Of the 16 polyps re-classified as probable or definite on review, 11 could not be identified on the barium enema, even in retrospect, including 4 of 7 polyps 10 mm+ (Table 3).
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Table 3. Retrospective independent observer classification of polyps 6 mm plus seen exclusively on CT colonography in patients without subsequent endoscopy
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Barium enema reported just one 6 mm polyp (not reported on CT, even on review) in the 56 patients.
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Discussion
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Radiological colonic imaging is generally regarded as safer and less invasive than total colonoscopy, particularly in patients with attendant comorbidity. Although, quite rightly, much emphasis is placed on the sensitivity of any particular technique, the ability of the test to confidently confirm normality is also an important consideration given that most symptomatic patients do not harbour significant pathology. Assuming it is technically complete, a normal barium enema or CT colonography is usually sufficient to spare the cost and risks of additional total colonoscopy in most patients with non-specific symptoms.
We found that experienced radiologists had significantly greater confidence in excluding a lesion 6 mm or larger with CT colonography than with barium enema, particularly in the proximal colon. Adequate visualization of the ascending colon and caecum is often difficult with barium enema, particularly in frail, immobile patients, mainly due to difficulties in barium filling and achieving the correct balance between adequate coating and unwanted liquid pools. Incomplete examinations are therefore relatively frequent in this patient group [16]. This difficultly is less apparent during CT colonography, when all that is required is gaseous distension of the proximal colon, something that can usually be achieved reliably [13, 17, 18]. The data suggest therefore that CT colonography is technically more "forgiving" than barium enema in older symptomatic patients. This has direct clinical implications, particularly as a combination of flexible sigmoidoscopy and barium enema has frequently been advocated in symptomatic patients [19, 20]. Our results suggest that experienced radiologists may be more confident when excluding significant pathology with CT colonography rather than barium enema in those undergoing limited endoscopy. Diagnostic confidence was almost identical in the sigmoid for barium enema and CT, suggesting this segment remains problematic, although recent data suggest CT colonography is as effective as flexible sigmoidoscopy for detecting significant lesions in patients presenting with rectal bleeding [21].
Residual fluid/barium or faecal residue generally decreased diagnostic confidence for CT and barium enema in similar proportion, although this affected more patients during barium enema overall. Interestingly, poor distension was the most common reason for inability to confidently exclude a significant lesion with CT colonography. The use of supine and prone imaging [17, 18] and spasmolytic [13] have all been shown to improve distension during CT colonography, but it is clear that any further improvements would still have significant impact on diagnostic confidence.
We did find evidence that referring clinicians consider a negative radiological test sufficiently reassuring to halt colonic investigation in symptomatic patients: no patient with a normal CT or barium enema went on to subsequent endoscopy. Indeed, 19 patients with abnormal CT reports (including 6 with suspected lesions at least 10 mm in size) have had no further colonic investigation. By way of explanation, all these patients had normal barium enema reports and the clinician may be more comfortable with this rather than the newer technology. However, it seems likely that two radiological investigations negative for cancer was enough to halt further investigation in elderly patients who were often frail.
The number of patients undergoing full colonoscopy was insufficient for any meaningful analysis of the diagnostic performance of CT colonography versus barium enema. CT identified all patients with colonic neoplasia on endoscopy whereas barium enema missed two (albeit with small and clinically insignificant polyps). However, of the two patients proven to have colorectal cancer (one of which was diagnosed only after incomplete colonoscopy), CT diagnosed both (and confirmed metastatic spread in one), whereas barium enema incorrectly classified a rectal cancer as a polyp. CT colonography did raise the possibility of a cancer in a patient with a Crohn's stricture, which was confidently reported as benign on barium enema, emphasising the benefit of barium enema for visualizing mucosal detail and the problems of using CT colonography in patients with inflammatory bowel disease.
CT colonography reported polyps in 29 (37%) patients compared with just 4 (5%) on barium enema. Although four patients had a subsequent normal colonoscopy suggesting CT false positives (although colonoscopy is an imperfect reference standard [22, 23]), the majority have not undergone endoscopic examination to confirm or refute the CT findings. All but one of the 17 polyps 6 mm plus initially reported on CT colonography in patients not undergoing endoscopy were classified as definite or probable on review by an independent observer, although only 4 were seen in retrospect on the barium enema. It could be argued that some of these additional polyps are false positives and if CT colonography were used alone could trigger unnecessary endoscopy. However, the prevalence of polyps even in an asymptomatic screening cohort over 50 is around 30–40% [24, 25], which perhaps gives some weight to the assertion that CT colonography was more sensitive than barium enema. Furthermore, there is increasing evidence of CT colonography's superior performance in polyp detection compared with barium enema [26]. Of course in the elderly symptomatic population, even sizeable polyps (over 1 cm) are likely incidental and a more sensitive test, such as CT colonography, does not always improve the outcome for patients (and indeed may worsen it if clinicians feel duty bound to "chase" incidental polyps reported on CT colonography in this vulnerable patient group). Conversely a 12 mm caecal polyp in a fit 70-year-old for example may well be highly significant for that individual. There needs to be a clear understanding between radiologist and referring clinician as to the lesion size threshold reported and the significance of findings in individual patients.
Our study does have weaknesses. It is possible that the prior CT colonography adversely affected the quality of subsequent barium enema. However carbon dioxide (which is readily absorbed through colonic mucosa) was used for CT colonography and there was at least 1 h between the two tests. Anecdotally those performing the enemas did not report additional problems in study patients, but we cannot exclude negative effects on the quality of the barium enemas. Different radiologists graded the barium enema and CT colonographic studies and it is possible that the confidence scores for excluding neoplasia were merely a reflection of the personalities of the individual radiologist rather than a comparison between the two tests. However, all radiologists had good experience of the technique they were reporting and importantly there were no statistically significant differences between levels of confidence for each of the two separate readers for each test, suggesting the scores reflected the procedure more than the radiologist. It would, however, be useful for further work to investigate intraobserver confidence in those trained in both CT colonography and barium enema. Although within the context of a trial we demonstrated greater confidence for excluding lesions 6 mm and over with CT colonography, it is clear that any level of uncertainty was often not reflected in the formal report sent to the referring clinician. In other words, even if the radiologist reported on the trial sheet that a significant lesion could not be excluded in, say, the caecum, this reduced confidence was not portrayed in the issued report. It is therefore questionable whether improved confidence with CT colonography would necessarily have a direct clinical impact in reducing unnecessary colonoscopy after technically imperfect barium enema. Such data will come from larger randomized trials currently in progress.
It is acknowledged that our definition of a significant lesion as anything 6 mm or larger is relatively wide and accept that there is a significant difference in not being able to exclude, say, an 8 mm polyp, compared with a 20 mm polyp. In essence our definition required the radiologist to be confident he/she could exclude a 6 mm lesion. However, detection of relatively small lesions is a reflection of the overall capabilities of the examination, especially when compared with endoscopy. Finally, as discussed above, CT colonography reported polyps in many more patients than barium enema and theoretically could actually act to increase endoscopic referral if the results are not viewed wisely in clinical context by clinicians. However, it must be remembered that a small but significant number of polyps around the centimetre mark will harbour cancer [27] and as life expectancy increases such lesions will assume greater importance in older individuals.
In conclusion, radiologist confidence in excluding polyps 6 mm or larger is significantly greater with CT colonography than barium enema, particularly in the proximal colon.
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Acknowledgments
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This research was supported by a research fellowship from the Royal College of Radiologists.
The authors would like to thank Paul Bassett for his statistical advice.
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Footnotes
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This research was supported by a research fellowship from the Royal College of Radiologists. 
Received for publication June 6, 2005.
Revision received July 13, 2005.
Accepted for publication July 15, 2005.
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BJR review of the year - 2006
Br. J. Radiol.,
March 1, 2007;
80(951):
147 - 151.
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Abstract
Introduction
