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Gastrointestinal Imaging |
1 From the Departments of Gastroenterology and Hepatology (J.T.E., N.M.F., G.M.F.) and Diagnostic and Interventional Radiology (R.M.M., C.W., D.M.), Royal Perth Hospital, Box X2213 GPO Perth, Western Australia 6000; and Departments of Public Health (L.F.), Medicine (G.M.F.), and Surgery (R.M.M.), University of Western Australia, Perth. Supported by the Health Department of Western Australia. Received November 3, 2002; revision requested January 13, 2003; final revision received June 3; accepted June 25. Address correspondence to J.T.E. (e-mail: john.t.edwards@health.wa.gov.au).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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MATERIALS AND METHODS: CT colonography for colorectal neoplasia screening was offered to 2,000 subjects aged 50–54 and 65–69 years. Only asymptomatic subjects at average risk of colorectal neoplasia were enrolled. Participants underwent CT colonography followed by colonoscopy if CT colonography findings showed any polyps. Acceptability was measured with a 100-point (0, most favorable; 100, least favorable) visual analogue scale (VAS). 
2 statistic was used to compare participation rates among subgroups. Safety of CT colonography was evaluated by recording all important adverse events.
RESULTS: A total of 1,452 subjects were eligible for screening. The adjusted participation rate was 28.4%. Participation was higher in younger subjects and in those from a high socioeconomic region. Major reasons for nonparticipation were insufficient time and perceived good health. Median VAS scores for pain, general satisfaction, embarrassment, and willingness to repeat screening were 13, 6, 8, and 5, respectively. Most subjects found CT colonography better than (60%) or same as (32%) expected. Ninety-three (27.4%) of 340 subjects were referred for colonoscopy, with polyps found in 67 (positive predictive value, 0.73). By adopting criteria that a positive finding at CT colonography is that of a single polyp larger than 5 mm or multiple polyps larger than 2 mm, 14% of CT examinations would have led to colonoscopy; 5.7% of CT findings were false-positive, with no significant impairment in large polyp detection. There were no important adverse events related to CT colonography, although four subjects had syncope or presyncope related to bowel preparation.
CONCLUSION: Community-based colorectal neoplasia screening with CT colonography was accompanied by a participation rate that compares favorably with that of similar screening programs. CT colonography was highly acceptable to participants.
© RSNA, 2003
Index terms: Colon, CT, 75.12115, 75.12117, 75.12119 • Colon neoplasms, 75.3111, 75.3113 • Computed tomography (CT), image processing, 75.12117, 75.12119
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Computed tomographic (CT) colonography is an emerging technology that depicts the mucosal aspect of the whole colon. Findings of studies in symptomatic subjects show that sensitivities of 85% for polyps larger than 5 mm in diameter and of 91% for polyps larger than 10 mm can be achieved by using current technology (6–9). CT colonography has several advantages as a screening tool: It is minimally invasive, is quick for the patient, and does not require sedation. To date, however, data are lacking on the overall applicability of CT colonography to an asymptomatic population at average risk for colorectal neoplasia, and controversy exists regarding such issues as the appropriate polyp size threshold (10).
The purpose of this study was to evaluate CT colonography as a screening tool for average-risk asymptomatic subjects in a community with regard to participation, acceptability, and safety.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Subjects
Names of 2,000 subjects were randomly drawn from the Western Australian Electoral Commission database by allocating identification numbers at random and then choosing the lowest numbers, with equal distribution according to sex, age group (50–54 and 65–69 years), and socioeconomic region (high, middle, and low). Two age groups were used to facilitate determination of the influence of age on participation. This cohort represented 22% of the eligible population in the catchment region. Socioeconomic status was assigned by using an urban index of residential postcode developed by the Australian Bureau of Statistics and known as the Socio-Economic Indices for Areas, or SEIFA, (11). The SEIFA Urban Index of Advantage is an indicator of well-being in each geographic region based on census data such as high income, tertiary education, home ownership, and skilled occupations.
Recruitment
A total of 2,000 letters of invitation to undergo CT colonography were sent to subjects in the community. Letters were accompanied by an explanatory brochure regarding bowel cancer screening, CT colonography, and colonoscopy. Subjects were randomly assigned to the following three groups of planned follow-up in the event there was no response to the initial invitation: group A, telephone call at 7 days; group B, telephone call at 21–28 days; and group C, follow-up letter at 21–28 days. Exclusion criteria were personal history of colonic polyps or cancer or history of a first-degree relative with colorectal cancer (ie, at above average risk for bowel cancer [3]); colonoscopy or barium enema examination within the past 5 years; history of rectal bleeding, change in bowel habit, or weight loss within the previous 12 months; or severe medical illness precluding bowel preparation. Subjects were also excluded when the letter was returned because of wrong address and when at telephone contact the subject was unable to speak English. Nonresponders to the screening invitation were offered questionnaires by mail or telephone to determine the reasons for nonparticipation. Subjects completed the questionnaire as to the acceptability of the processes after CT colonography was complete. Acceptability was assessed by using a 100-point visual analogue scale questionnaire (score 0, most favorable; score 100, least favorable).
Screening Program
The primary aim of this study was to assess participation, acceptability, and safety of CT colonography screening. Hence, the protocol reflects a true screening program; that is, subjects undergoing CT colonography were referred for colonoscopy only if findings at CT colonography were abnormal. Participating subjects were scheduled for CT colonography at enrollment, were provided with bowel preparation, and underwent CT colonography in the morning. Subjects with positive CT colonography findings were offered colonoscopy later that same morning or were given a subsequent appointment if desired. Subjects with negative CT colonography findings were given verbal and written information regarding national colorectal cancer screening guidelines (3) and were referred back to their general practitioner.
CT Colonography Technique and Interpretation
All participants underwent bowel preparation with low-residue diet followed by either a polyethylene glycol (Colonlytely; Dendy Pharmaceuticals, East Brighton, Australia)/sodium picosulfate (Picolax; Dendy Pharmaceuticals) (n = 259) or magnesium citrate (equivalent to 3 g magnesium oxide; Pharmatel, Thornleigh, Australia)/sodium picosulfate (n = 82) preparation the evening prior to CT colonography. A rectal examination was performed in all subjects by a trained nurse, followed by insertion of a 28-F Foley catheter into the rectum. The catheter was connected by means of an Oro1H (Pall, Cheltenham, Australia) gas filter to a gas insufflator (UHI-2; Olympus, Tokyo, Japan), with flow rate adjustable with adjustable pressure limits. Twenty milligrams of hyoscine butylbromide (Buscopan; Boehringer Ingelheim, North Ryde, Australia) was administered intravenously if no contraindications (history of glaucoma or arrhythmia or symptoms of urinary outflow obstruction) were present. Carbon dioxide was delivered at 1–2 L/min until 2.5 L was administered or until the patient experienced discomfort. CT scout images were used to check bowel inflation and were followed by further insufflation as required. CT scanning was performed with a helical scanner (CTi; GE Medical Systems, Milwaukee, Wis). The following two protocols were used according to body habitus: 5-mm collimation, pitch of 1.5:1, and 70 mAs or 3-mm collimation, pitch of 2.0:1, and 96 mAs. Reconstruction intervals were 1 mm for supine and 2 mm for prone scans. A standard algorithm was used. Tube rotation time was 0.8 second. The total radiation dose for both protocols was calculated to be less than 5 mSv (total effective body dose)2 Transverse images were examined by using a dual-monitor workstation (Advantage Windows version 3.1; GE Medical Systems), and multiplanar reformations and three-dimensional endoluminal views (Navigator 2.0 and later colonography version 2 software; GE Medical Systems) were used for problem-solving.
Two physicians (J.T.E., R.M.M.) experienced with CT colonography (>120 examinations each) provided a consensus report for each scan. A positive CT colonography finding was defined by the presence of any polyp 2 mm or larger on transverse images. This inclusive definition was used because there are no current data in average-risk screening populations from which to determine more restrictive size thresholds in defining a positive CT colonography finding. Polyps were measured on two-dimensional images by using the longest axis across the polyp. Soft-tissue window settings were also used to examine the transverse images for colonic wall thickening and infiltrative cancers.
Colonoscopy
Colonoscopy was performed by one of four experienced (>1,000 colonoscopies each) gastroenterologists (including J.T.E., G.M.F.) who were aware of the CT colonography results so as to minimize the risk of missing lesions at colonoscopy that were seen at CT colonography. Conscious sedation was induced with intravenous midazolam hydrochloride (Midazolam; Pharmacia, Rydalmere, Australia) and pethidine hydrochloride (Pethidine; AstraZeneca, North Ryde, Australia) or fentanyl citrate (Fentanyl; AstraZeneca). All lesions found were recorded. A lesion at colonoscopy was deemed to coincide with a lesion at CT colonography if the lesion was in the same bowel segment and the size estimates did not differ by more than 30%. Polyps were measured at colonoscopy by comparing the polyp diameter with the diameter of open-biopsy forceps.
Outcome Measures and Statistical Analysis
Participation.—Crude participation was calculated as the number of subjects agreeing to participate divided by the number of subjects invited and not known to be ineligible. The adjusted participation rate was calculated with the assumption that of those nonparticipants who did not respond, a similar percentage as that of the responders were ineligible. The adjusted rate also accounts for the three subjects who commenced bowel preparation for CT colonography but who did not complete screening because of adverse events during bowel preparation.
Participation was compared in the subgroups of the sample according to age group (50–54 vs 65–69 years), sex, recruitment strategy, and socioeconomic region (low, medium, and high). Differences between proportions were tested with a 2 statistic, and P value of .05 was considered to indicate statistically significant difference.
Performance characteristics.—The protocol design permitted evaluation of certain performance characteristics of CT colonography in this clinical setting. The overall positive predictive value (PPV) of CT colonography was determined on a per-person basis as the proportion of subjects with a positive CT colonography finding who had a lesion confirmed at colonoscopy. The PPV was also calculated on a lesion-specific basis both for finding any polyps (including adenomatous, hyperplastic, and other polyps) and for finding any adenomatous polyps or cancer. The false-positive rate was calculated by using a range of different size thresholds, between 2 and 9 mm, for a positive finding at CT colonography. The overall sensitivity of CT colonography in polyp detection could not be assessed because subjects with only positive CT colonography findings underwent colonoscopy. However, for the polyps identified at colonoscopy, we were able to determine the proportion correctly identified at the preceding CT colonography. By accepting that currently CT colonography has limited accuracy for polyps smaller than 5 mm, the CT colonographic scans of all false-negative polyps larger than 5 mm were reviewed by the reporting physicians, and a consensus judgment was made as to the likely cause of the false-negative results. The CT colonographic scans and colonoscopy reports were reviewed in similar fashion for all false-positive lesions larger than 5 mm.
Acceptability.—The acceptability of CT colonography as perceived by subjects was assessed by using a 100-point visual analogue scale questionnaire (score 0, most favorable; score 100, least favorable) that was completed after CT colonography but prior to the revelation of results. Subjects were also asked if the procedure was better, worse, or similar than expected and what was the worst part of the screening process.
Adverse Events.—Clinically important adverse events at CT colonography were recorded for each subject. These were defined as an adverse clinical problem that required specific evaluation by nursing or medical staff.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Participation in Screening
The overall participation was 343 of 1,452 subjects, or 23.6% (17.1% response to initial letter of invitation and 6.5% additional response after follow-up), and the adjusted participation rate was 28.4% (340 of 1,197). The adjusted participation rate assumes a similar percentage of exclusions (not counting undeliverable mail) from the nonparticipants who did not respond to postal or telephone questionnaires (ie, of 687 subjects who did not respond, 255 were assumed to be ineligible). The adjusted rate also accounts for the three subjects who commenced bowel preparation for CT colonography but who did not complete screening because of adverse events during bowel preparation. Participation was significantly higher in the younger age group and in those from a high socioeconomic region, but there were no differences with respect to sex and recruitment strategy (Table 1).
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Acceptability of CT Colonography
Results of the 100-point visual analogue scale questionnaire are listed in Table 2. Participants reported a high level of acceptability and a high likelihood of undergoing repeat CT colonography.
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Adverse Events
Adverse events associated with the CT colonography procedure itself, such as mild nausea with gas insufflation (n = 3), postprocedural abdominal pain requiring short bed rest (n = 2), and flushing and sweating during CT (n = 2), were generally minor. However, four of 82 subjects who received the magnesium citrate/sodium picosulfate bowel preparation had syncopal (n = 3) or presyncopal episodes during the bowel preparation, which were judged to be caused by relative dehydration. This bowel preparation was therefore abandoned. No such episodes were encountered with the use of polyethylene glycol/sodium picosulfate. One subject developed a migraine headache while undertaking the low-residue diet and did not complete the bowel preparation.
Findings at CT Colonography
Of 340 CT colonography examinations, 93 (27.4%) had positive findings, and hence the subjects were referred for colonoscopy (92 subjects complied: 89 on the same day and three at subsequent dates). Colonoscopy was completed to the cecum in all subjects. In the 92 subjects, 123 lesions were seen at CT colonography; 68 lesions were confirmed at colonoscopy in 67 subjects (PPV per-polyp basis, 0.55). The PPVs (on a per-person basis) of CT colonography in helping to predict the presence of any polyp or adenoma and/or carcinoma were 0.73 (67 of 92) and 0.55 (51 of 92), respectively. That is, in 73% of subjects with a positive CT colonography finding, at least one lesion was depicted at colonoscopy; in 55% of subjects with a positive CT colonography finding, at least one adenoma or carcinoma was depicted. Overall, 7.4% (25 of 339) of CT colonography findings were false-positive for any polyp, and 12.1% (41 of 339) were false-positive for adenomatous polyps.
In 67 subjects, 136 polyps or cancers were found at colonoscopy (Table 3). Of the nine polyps larger than 9 mm found at colonoscopy, all had been detected at CT colonography. Thirty (70%) of 43 polyps 6–9 mm and 31 (37%) of 84 polyps smaller than 6 mm had also been detected at CT colonography. These data do not represent true sensitivities, as negative findings at CT colonography did not proceed to the performance of colonoscopy.
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There were 19 false-positive lesions larger than 5 mm. In retrospect, 11 of these were believed to be caused by feculent material, two were likely prominent folds, one was feculent sludge on a prominent fold, one was a particularly bulbous ileocecal fold, and four were indeterminate.
Modification of the definition of what constitutes a positive finding at screening CT colonography according to various polyp sizes resulted in a downward adjustment of the proportion of false-positive findings. The Figure shows that the proportion of false-positive findings decreases with increasing polyp size as the threshold for defining a positive finding at CT colonography. Use of a polyp size threshold larger than 5 mm results in 5.0% (17 of 340) of CT colonographic findings being false-positive (for adenomatous polyps) and 11.8% (40 of 340) of CT colonographic findings requiring colonoscopy. When a positive CT colonography finding was defined as that of a polyp larger than 5 mm or two or more polyps larger than 2 mm, 5.3% (18 of 340) of CT colonography findings were false-positive and 14% (48 of 340) required colonoscopy; of adenomas detected in this study, 74% (20 of 27) 6–9 mm and all (eight of eight) larger than 9 mm would have been detected.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Participation in a screening program is an important determinant of the cost-effectiveness of any colon cancer screening test (13,14). Participation rates with use of FOBT (23%–50%) (15–19) and flexible sigmoidoscopy (23%–47%) (20–22) have varied greatly. Participation is generally facilitated by the involvement of general practitioners and a publicity campaign (19,21,23), neither of which our program had used. Despite this, the participation rate of 28.4% compares favorably with previous rates of Australian (23%) (15) and French (26%–34%) (16) FOBT trials and Australian flexible sigmoidoscopy programs (23%) (20) of similar design.
Compliance with follow-up colonoscopy for a positive test (99%) was higher for CT colonography than was previously noted in some flexible sigmoidoscopy programs (76%) (20) (although not in others [96%] [22]) and FOBT trials (85%) (17,18,24). Same-day colonoscopy is achieved with a bowel preparation suitable for both CT colonography and colonoscopy, but it requires a coordinated approach from both a radiologist and an endoscopist to ensure maximum compliance following a positive finding at CT colonography.
The high acceptability and strong willingness of subjects to undergo CT colonography again is encouraging for a screening test that will likely be performed first when a subject reaches 50 years of age, with subsequent testing over the next 25 years, during which time cancer risk increases (25). If compliance decreases with subsequent screening visits, as was noted with FOBT (16,17,19) and flexible sigmoidoscopy (26), participation will be lowest at the time the cancer risk is highest. We have found, as have others (19,27), that older age groups and those from low to medium socioeconomic regions were less likely to participate. The most frequent reason given for nonparticipation among the older subjects was good health and/or no need, which suggests that poorer understanding of the concept of cancer screening when the patient is asymptomatic may in part be responsible for the lower participation rate.
The acceptability results compare favorably with those obtained with flexible sigmoidoscopy. Although most subjects who undergo screening flexible sigmoidoscopy experience only mild or moderate discomfort, 15%–25% experience great discomfort (28). Authors of one study (20) reported that pain led to an incomplete examination in 26% of subjects. In our cohort, only 10% of subjects reported a pain score of greater than 50 out of a total of 100, and only 6% said the procedure was more uncomfortable than expected. The acceptability data are similar to those from a previous study (29) by our group of symptomatic or high-risk patients. Other workers (30) have reported that patients had a less satisfactory experience with CT colonography than with colonoscopy, although overall both tests had good acceptability. Efforts to optimize the subjective experience of CT colonography are clearly important, particularly in the context of a screening program.
The bowel preparation and the associated dieting were the major reasons for a negative experience for participating subjects, and lack of time was the major reported impediment to participation. These data suggest that fecal tagging or "virtual preparation" techniques should enhance the attractiveness of CT colonography as a screening modality (31). First, bowel preparation would be limited and, hence, more acceptable. Second, the patient could leave immediately after scanning and before the results are obtained. Compliance with late follow-up colonoscopy for subjects with positive CT colonography findings may, however, be lower than that observed with immediate colonoscopy.
There were no serious adverse events associated with the examination itself. To date, there have been no reports of bowel perforation associated with CT colonography. The risk of bowel perforation from barium enema examination is about one in 25,000 (32), and, contrary to our practice of CT colonography, it generally occurs when a rectal balloon is used to assist the retention of air and barium. One of the two bowel preparations used was associated with four syncopal or presyncopal episodes, which were probably related to the relative fluid depletion, and this preparation was abandoned after interim analysis of safety data.
Two reporters were used in our study; the performance data may potentially diminish slightly with one reporter, which is the likely situation in a true screening program. However, as experience with CT colonography grows over time, the performance of a highly experienced reporter may well approach that of two current reporters with moderate experience.
In this study, we were not able to accurately assess the sensitivity of CT colonography in polyp detection, as this requires that at least a subset of subjects undergo both CT colonography and colonoscopy. However, it is encouraging that in subjects with a positive finding at screening CT colonography who went on to undergo colonoscopy, very few medium and no large polyps were missed with CT colonography. This suggests that CT colonography was performed with reasonable rigor and that the acceptability outcomes are not artificially enhanced by suboptimal bowel preparation or inadequate colonic insufflation. Results from community-based studies that specifically address sensitivity and specificity are awaited.
The review of false-negative CT colonography findings suggests there is still room for improvement in the scanning technology; over half of the missed lesions were not seen at the review of CT colonography findings despite adequate inflation and bowel preparation. Multi–detector array CT scanners may improve sensitivity for medium to small polyps (33).
The review of false-positive CT colonography findings, however, suggests that attention to bowel preparation and efforts at fecal tagging will be the most effective technical measures to reduce false-positive results.
An important facet of a suitable screening test is a low percentage of false-positive findings and, hence, unnecessary procedures. Although our overall PPV was 0.73, colonoscopy was performed in a significant proportion (27.4%) of the total cohort, which reflects the reporting at CT colonography of any polyp larger than 2 mm. Restriction of the definition of a positive result (eg, a polyp > 5 mm or two or more polyps > 2 mm) improves false-positive and colonoscopy referral rates. How and if this approach can be implemented in the clinical setting should be a focus of further research.
In summary, this study provides data that support the continued development of CT colonography as an alternative screening tool in asymptomatic subjects who are at average risk for colorectal neoplasia.
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APPENDIX |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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To determine the exclusion rate applicable to nonresponders, subtract the number of exclusions because of wrong address (n = 97), because these should all be accounted for, from the total number of exclusions (n = 548): 548 - 97 = 451.
Determine the denominator for the exclusion rate to be applied to the nonresponders as follows: 1,313 - 97 = 1,216.
The exclusion rate is calculated as follows: 451 ÷ 1,216 = 0.3709.
If we assume the exclusion rate also applied to the nonresponders, there are 255 extra exclusions (0.3709 · 687).
The adjusted number for eligible subjects is 1,197 (2,000 - [548 + 255]).
Three of 343 participants did not complete the whole virtual colonoscopy process; therefore, the adjusted participation is 28.4% (340 of 1,197).
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, J.T.E.; study concepts, G.M.F., R.M.M., J.T.E., N.M.F.; study design, L.F., G.M.F., R.M.M., J.T.E., C.W., D.M.; literature research, J.T.E., N.M.F.; clinical studies, J.T.E., R.M.M., G.M.F., N.M.F., C.W., D.M.; data acquisition, J.T.E., R.M.M., D.M., C.W., N.M.F.; data analysis/interpretation, L.F., J.T.E.; statistical analysis, L.F.; manuscript preparation, J.T.E., G.M.F., R.M.M., L.F.; manuscript definition of intellectual content, J.T.E., G.M.F., R.M.M.; manuscript editing, L.F., G.M.F., R.M.M.; manuscript revision/review and final version approval, all authors
2 Dose estimation was based on experimental measurement of dose profiles through CT sections in a cylindrical water phantom. The average dose per section is calculated for given exposure factors and the profiles used to determine scatter to various organs. A computerized mathematic model based on adult anatomy is the basis of the calculations. Tissue weighting factors according to guidelines published in International Commission on Radiological Protection (ICRP) Publication 60 (12) are used to assess the effective dose to adult men and women. It is assumed that for spiral CT, the dose is equivalent to that obtained from a series of parallel sections separated by the pitch of the helix. 
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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