CT Colonography versus Colonoscopy for the Detection of Advanced Neoplasia
David H. Kim, M.D., Perry J. Pickhardt, M.D., Andrew J. Taylor, M.D., Winifred K. Leung, M.D., Thomas C. Winter, M.D., J. Louis Hinshaw, M.D., Deepak V. Gopal, M.D., Mark Reichelderfer, M.D., Richard H. Hsu, M.D., and Patrick R. Pfau, M.D.
Background Advanced neoplasia represents the primary targetfor colorectal-cancer screening and prevention. We comparedthe diagnostic yield from parallel computed tomographic colonography(CTC) and optical colonoscopy (OC) screening programs.
Methods We compared primary CTC screening in 3120 consecutiveadults (mean [±SD] age, 57.0±7.2 years) with primaryOC screening in 3163 consecutive adults (mean age, 58.1±7.8years). The main outcome measures included the detection ofadvanced neoplasia (advanced adenomas and carcinomas) and thetotal number of harvested polyps. Referral for polypectomy duringOC was offered for all CTC-detected polyps of at least 6 mmin size. Patients with one or two small polyps (6 to 9 mm) alsowere offered the option of CTC surveillance. During primaryOC, nearly all detected polyps were removed, regardless of size,according to established practice guidelines.
Results During CTC and OC screening, 123 and 121 advanced neoplasmswere found, including 14 and 4 invasive cancers, respectively.The referral rate for OC in the primary CTC screening groupwas 7.9% (246 of 3120 patients). Advanced neoplasia was confirmedin 100 of the 3120 patients in the CTC group (3.2%) and in 107of the 3163 patients in the OC group (3.4%), not including 158patients with 193 unresected CTC-detected polyps of 6 to 9 mmwho were undergoing surveillance. The total numbers of polypsremoved in the CTC and OC groups were 561 and 2434, respectively.There were seven colonic perforations in the OC group and nonein the CTC group.
Conclusions Primary CTC and OC screening strategies resultedin similar detection rates for advanced neoplasia, althoughthe numbers of polypectomies and complications were considerablysmaller in the CTC group. These findings support the use ofCTC as a primary screening test before therapeutic OC.
Advanced neoplasia of the large intestine consists of both adenocarcinomasand a subgroup of benign neoplasms referred to as advanced adenomas.The advanced adenoma represents the optimal target lesion forstrategies to prevent colorectal cancer. This benign lesionis considered to be associated with a relatively high risk ofprogression to cancer.1 The advanced adenoma is specificallydefined as an adenoma that meets one or more of the followingcriteria: a size of at least 10 mm, the presence of a substantialvillous component, and the presence of high-grade dysplasia.1,2Removal of detected advanced adenomas effectively disrupts thepotential pathway to the development of cancer that is believedto be responsible for the majority of colorectal carcinomas.2,3,4
Most subcentimeter polyps are not adenomatous, and only a smallfraction of all adenomas are advanced, suggesting a need formore selective alternatives to the practice of universal polypectomy.3,5,6The purpose of this study was to compare computed tomographiccolonography (CTC) and optical colonoscopy (OC) when appliedto the same general screening population. Important outcomemeasures included detection rates for advanced adenomas andadenocarcinomas for various categories of polyp size and overallpolypectomy rates. These observations provided an assessmentof CTC as a selective filter for therapeutic OC in the detectionof advanced neoplasia.
Methods
Study Group
Our study, which complied with the guidelines of the HealthInsurance Portability and Accountability Act, was approved bythe institutional review board at the University of WisconsinMedical School. The requirement for informed consent was waived.The clinical databases from parallel CTC and OC colorectal screeningprograms at a single institution were analyzed to evaluate thediagnostic yield of each approach. We compared results from3120 consecutive patients enrolled in the CTC screening programduring a 25-month period with those from 3163 consecutive patientsseen at OC screening during a 17-month period (with partiallyoverlapping time periods). The two programs drew patients fromthe same general screening population and geographic region.
The patients in each program were referred by the same groupsof primary care providers for the indication of colorectal-cancerscreening. Exclusion criteria included polyp surveillance ora history of a bowel disorder, such as inflammatory bowel disease,polyposis syndromes, and the hereditary nonpolyposis colorectalcancer syndrome. The characteristics of the two groups are shownin Table 1. The majority of patients were asymptomatic and ataverage risk for colorectal cancer.
Table 1. Demographic Characteristics of the Patients.
Study Design
We identified all pathologically proven neoplasms that weredetected by each screening method from the pool of resectedpolyps. From this group, the advanced neoplasms were extracted.Large polyps were defined as measuring at least 10 mm in size,small polyps as measuring 6 to 9 mm, and diminutive lesionsas measuring 5 mm or less. Prospective assignment of polyp characteristicsat both CTC and OC screening included size, morphologic characteristics,and anatomical location. The morphologic characteristics ofthe polyps were classified as sessile, pedunculated, or flat;frankly invasive masses were considered as a separate category.The location of the polyp was originally assigned accordingto anatomical segment but, for the purpose of this study, wascondensed into proximal and distal locations, relative to thesplenic flexure. Adenomas were classified histologically astubular, tubulovillous (25 to 75% villous component), villous,or serrated subtypes. Invasive carcinoma was defined as malignantspread beyond the muscularis mucosa.
We compared the prevalence of high-grade dysplasia, invasiveadenocarcinoma, and overall advanced neoplasia in each studygroup. The rates of positive results for both screening testswere calculated at various thresholds of polyp size. A testwas considered to be positive at a given size threshold whenone or more polyps of that size or greater were detected.
CTC Protocol
Referral by a physician was required for primary CTC screening.Bowel preparation for CTC involved both a cathartic agent andoral contrast tagging agents.7 A single 45-ml dose of sodiumphosphate was used for catharsis in most patients8; magnesiumcitrate or, rarely, polyethylene glycol was substituted in aminority of patients with renal or cardiac conditions. Singledoses of 2% barium (250 ml) and diatrizoate (60 ml) were givento tag residual stool and fluid, respectively. No sedating orspasmolytic agents were given. Colonic distention was achievedwith automated low-pressure delivery of carbon dioxide (PROTOCO2L,E-Z-EM). A multidetector 8-channel or 16-channel computed tomographic(CT) scanner was used (LightSpeed Series, General Electric MedicalSystems). The CT technique involved the use of 1.25-mm collimationand scanner settings of 120 kVp and 25 to 75 mAs with the patientin both supine and prone positions. The imaging data were reviewedon a dedicated three-dimensional CTC workstation (V3D Colon,Viatronix).
The CTC examinations were immediately interpreted by one offive gastrointestinal radiologists who were experienced in CTC.Polyp size was determined on the optimal CTC view with the useof electronic calipers.9 Colonic and extracolonic findings onCT were classified according to designations of CTC Reportingand Data System (C-RADS).10 For all polyps of at least 6 mm,the patient was offered same-day therapeutic OC, unless theprocedure was contraindicated. Patients with only one or twopolyps of 6 to 9 mm were given the option of CTC surveillance.10Potential diminutive lesions (5 mm) were not reported.5,11 AfterCTC, patients resumed their regular activities but remainedin a fasting state to allow for same-day OC, if necessary. FinalCTC results were relayed to patients within 2 hours after theprocedure.
OC Protocol
Primary OC screening operates as an open-access system. Bowelpreparation was usually accomplished with polyethylene glycol(4 liters), although some patients instead received two 45-mldoses of sodium phosphate. Moderate sedation was accomplishedwith intravenous midazolam and fentanyl. The OC examinationswere performed with the use of standard colonoscopes (EC-3872LKand EC-3470LK, Pentax) by 1 of 10 experienced gastroenterologists.OC after a positive CTC study was performed in a fashion similarto that of primary OC, with the exception that the physicianhad knowledge of CTC polyp findings before performing the OCstudy.
The colonoscope was advanced to the cecum; examination for polypswas performed on both insertion and withdrawal of the scope.Polyps that were identified during OC were removed with standardtechniques. Polyp size was based on in vivo OC estimation beforepolypectomy. Detected polyps, including diminutive lesions,were generally removed at OC evaluation, regardless of whetherthe study was performed as a primary screening test or afterCTC.
Statistical Analysis
Primary comparisons were made between the patients enrolledin the CTC screening program and those in the OC screening program.The two groups were compared with the use of the Student's t-testfor independent samples for continuous outcomes and Pearson'schi-square test for categorical outcomes. A two-sided P valueof less than 0.05 was considered to indicate statistical significance.
Results
The diagnostic yields from primary CTC and primary OC screeningare summarized in Table 2. The total number of advanced neoplasmsand the prevalence in patients were similar for the two screeningapproaches. No statistical difference between the groups wasseen in the number of large or small advanced adenomas thatwere removed. However, the number of polypectomies performedto achieve these similar outcomes differed significantly betweenthe two groups, with more than four times as many polyps removedin the OC group as in the CTC group.
Table 2. Diagnostic Yield of Primary CTC and Primary OC Screening.
Overall, 246 of 3120 patients in the CTC group (7.9%) were referredfor therapeutic OC (Figure 1). Of note, the numbers of polypsin the primary CTC group do not reflect the 193 unresected polypsof 6 to 9 mm in 158 patients undergoing continuing surveillance.On the basis of previous experience with CTC screening, approximately60% of polyps of 6 to 9 mm detected by CTC would be expectedto be adenomatous,12 and approximately 3% of CTC-detected adenomasof 6 to 9 mm contain advanced histologic findings.6 Therefore,we estimated that CTC surveillance would yield three to fouradvanced adenomas (193x0.6x0.03), resulting in a yield of advancedneoplasias among small lesions that was very similar to theyield associated with OC.
Figure 1. Enrollment and Outcomes of Patients Undergoing CTC.
The detection of polyps of 6 mm or more was considered to be a positive finding. The detection of diminutive polyps was classified as a negative finding.
Limited follow-up data regarding these polyps are available.The majority of these patients are awaiting interval CTC examination.Of the patients with 1 or 2 polyps of 6 to 9 mm who are undergoingcontinuing surveillance, 54 have returned for follow-up CTCwith findings of 70 small polyps. In this group, 67 polyps (96%)have remained stable or decreased in size at follow-up. Threepolyps grew at least 1 mm but did not cross the 10-mm threshold;these polyps were all removed. Histologic examination revealedtubular adenomas without high-grade dysplasia for all threepolyps.
The rates of positive test results for the two screening strategiesare shown in Table 3. The rates for CTC and OC were similarat the 10-mm and 6-mm thresholds, but there was a disparityin overall positivity rates, reflecting the different handlingof diminutive lesions.
Table 3. Rates of Positive Screening Results, According to Threshold of Polyp Size.
Characteristics of advanced neoplasia, including size, histologicand morphologic characteristics, and anatomical location, aresummarized in Table 4. The great majority of lesions could beclassified as advanced on the basis of size alone, including117 of 123 (95.1%) in the primary CTC group and 107 of 121 (88.4%)in the primary OC group. A total of 15 of the 6283 patientsin the combined groups (0.2%) had subcentimeter advanced neoplasias.As noted above, several additional small advanced adenomas maybe among the unresected polyps in the CTC surveillance group.Of the 20 subcentimeter advanced adenomas in these 15 patients,16 of 20 (80%) had tubulovillous histologic characteristicswithout high-grade dysplasia; four lesions in three patientscontained high-grade dysplasia. All proven adenocarcinomas werelarge, with a mean (±SD) size of 34.9±14.6 mm.Of 18 invasive cancers, 15 were more than 2 cm in size, and3 were 1 to 2 cm.
Tubular and tubulovillous histologic characteristics were commonamong the advanced adenomas from both groups, whereas villousand serrated histologic characteristics were relatively rare(Table 4). High-grade dysplasia without carcinoma was also quiterare and was seen in only 14 of 6283 patients (0.2%). In theCTC group, 12 of 3120 patients (0.4%) had invasive adenocarcinoma,as compared with 4 of 3163 (0.1%) in the OC group. Most advancedadenomas in both groups were characterized as either sessileor pedunculated (Figure 2), with few flat lesions. Advancedadenomas were distributed throughout the large intestine.
Figure 2. CTC in a Man at Average Risk for Colorectal Cancer.
In Panel A, an endoluminal three-dimensional CTC image shows a 33-mm lobulated rectal polyp (arrow), as well as a 13-mm polyp (arrowhead) near the rectosigmoid junction. Two-dimension coronal (Panel B) and sagittal (Panel C) CTC images confirm the presence and soft-tissue composition of the larger polyp (arrows). In Panel D, a digital photograph from same-day optical colonoscopy shows the endoscopic capture of the polyp immediately before resection. Pathological evaluation revealed a large tubulovillous adenoma with high-grade dysplasia. The second lesion also had benign tubulovillous histologic characteristics but without high-grade dysplasia.
Extracolonic findings detected on CTC and classified accordingto C-RADS criteria10 are shown in Table 5. Such classificationallows for uniform reporting and indicates which imaging findingsmay require further evaluation. Overall, eight extracoloniccancers were seen in the CTC cohort, accounting for a prevalenceof 0.3%.
Serious adverse events during primary OC screening includedcolonic perforation in seven patients (0.2%); in four of thepatients, surgical repair was required. During primary CTC screening,there were no perforations or other serious complications relatedto either the CTC examination or subsequent therapeutic OC.
Discussion
Colorectal cancer is a major cause of cancer-related mortalityin the United States, accounting for approximately 55,000 deathsper year.13 However, because this cancer has an identifiableprecursor lesion, there is a genuine opportunity for preventionrather than cancer detection alone.3,4 In particular, targeteddetection and removal of advanced adenomas may be the most effectiveapproach to cancer prevention.1 OC is an effective screeningtool for the detection and removal of advanced colorectal neoplasiaand is widely regarded as part of the preferred screening strategy.4,14,15Our results suggest that primary CTC with selective OC alsodeserves consideration as a preferred screening strategy becauseit appears to achieve the same goals of detection and preventionbut with the use of substantially fewer resources in terms ofOC procedures and polypectomies. Thus, CTC may provide a moretargeted screening approach for detection of advanced neoplasia.
In our study, the coexistence of parallel CTC and OC screeningprograms at a single institution allowed for substantive comparisonof diagnostic yields and the use of resources. We observed similardetection rates for advanced adenomas during both CTC and OCscreenings. The diagnostic yield for advanced neoplasia wassimilar in the two groups, despite the fact that small lesions(5 mm) were not reported during CTC. In addition, a subgroupof patients with unresected polyps of 6 to 9 mm were undergoingCTC surveillance, and the frequency of a family history of colorectalcancer was higher in the OC screening cohort. The differenthandling of diminutive lesions largely accounts for the discrepanciesin the overall rates of positive test results (12.9% in theCTC group vs. 37.6% in the OC group) and in the numbers of polypectomies(561 vs. 2434).
Overall, 2006 polypectomies were performed to remove diminutivepolyps, which yielded four advanced lesions (0.2%). Such observationsreinforce the scarcity of diminutive and small advanced neoplasticlesions and the potential benefits of filtering strategies duringCTC. In fact, Markov modeling of large cohorts has shown thatthe strategy of not reporting diminutive polyps detected duringCTC screening is a cost-effective approach that can substantiallyreduce the rate of polypectomy and complications without anysacrifice with respect to cancer prevention.16
Beyond these differences, however, there were also some strikingsimilarities between the two screening strategies. For example,the rates of positive test results at the thresholds of 6 mmand 10 mm were similar, and the characteristics of the advancedadenomas were also quite similar.
Polyps of at least 10 mm appear to represent a very useful surrogatefor advanced adenomas, accounting for the great majority ofall advanced lesions in our study. Large polyp size has alreadybeen singled out by some observers as the most important criterionfor advanced neoplasia.1 Only 20 subcentimeter polyps in ourstudy were histologically advanced, which corresponded to anoverall prevalence of 0.2% (15 of 6283 patients). Only fouradvanced adenomas were identified in the diminutive category.Furthermore, only 3 patients had four subcentimeter polyps withhigh-grade dysplasia (0.05%), and there were no subcentimetercancers in more than 6000 patients. These observations suggestthat a 10-mm threshold for polypectomy at asymptomatic screeningwould probably capture the vast majority of clinically relevantlesions.
The overall prevalence of advanced neoplasia in this healthyscreening cohort of 6283 adults was 3.3%, which is somewhatlower than the prevalence of 4 to 6% reported in several otherstudies5,15,17,18,19 and substantially lower than the prevalenceof 10.5% in a population of male veterans.14 These differencesare probably multifactorial, but variations in age, sex, ethnicbackground, family history, and frequency of symptoms may allplay a role. A recent colonoscopy study showed that the prevalenceof advanced neoplasia was less than 3% in certain low-risk cohorts.20In our study, the frequency of advanced histologic findingsamong subcentimeter lesions, particularly high-grade dysplasiaand invasive carcinoma, was also generally lower than previouslyreported.2,21,22,23 However, the inclusion of 10-mm lesionsin the category of small polyps in some previous studies substantiallyincreased the reported prevalence.22,23 Furthermore, a recentcolonoscopy series evaluating a large screening population reportedlow cancer rates among resected adenomas measuring 6 to 9 mm(0.07%) and 1 to 2 cm (2.4%).24 In our study, the exclusionof a subgroup of patients who had small, unresected polyps andwere undergoing CTC surveillance probably had only a small effecton the prevalence of advanced adenomas.
The clinical management of small polyps of 6 to 9 mm that aredetected during CTC is controversial. One approach is to offerOC for polypectomy to all patients with CTC-detected polypsof at least 6 mm.25 However, an option of short-term CTC surveillancefor patients with one or two small CTC-detected polyps has alsobeen suggested.10 Short-term CTC surveillance for small polypsallows for more efficient detection and removal of the uncommonadvanced neoplasms because only the enlarging lesions are removed.As discussed previously, potential benefits include the decreaseduse of resources, procedural risks, and cost. Potential drawbacksmainly involve the possibility of following a polyp that harborsa focus of cancer or transforms to cancer during the surveillanceperiod, resulting in a lost opportunity for cancer prevention.The presumed low risk for this subgroup of polyps is echoedby the low prevalence of subcentimeter lesions harboring high-gradedysplasia or invasive carcinoma in the population we studied.In addition, the limited natural-history data from several olderlongitudinal studies that monitored lesions with the use ofbarium enema and endoscopic examination support the practiceof short-term CTC follow-up.26,27,28,29 Ultimately, more investigationwill be needed to determine which strategy is more beneficialduring CTC. Such a surveillance strategy for small polyps thatare detected during primary OC would clearly be less appealingbecause the scope is already in place and the only incrementalcosts and risks that are incurred are related to the polypectomyitself.
Adverse events were uncommon during OC screening, and no seriouscomplications were reported in the CTC group. The perforationrate of 0.2% (7 of 3163 patients) in the OC group was withinthe expected range reported in previous colonoscopy series.30,31The absence of perforations in the CTC screening group was largelydue to both the minimally invasive nature of CTC32 and the decreasednumbers of OC studies and polypectomies, as compared with theprimary OC group. Concern has been raised regarding the potentialrisks associated with radiation exposure from CTC. Some observerscontend that the risk is too small to quantify.33 Proponentsof the linear, no-threshold model argue that a small risk exists,but even members of this group agree that the benefits of screeningfor colorectal cancer appear to outweigh these small theoreticalrisks.34
A major limitation of our study was the lack of randomization.Thus, a potential exists for selection bias affecting the compositionof the study population for each program, leading to differentprevalences of advanced adenomas. Although most patients inboth cohorts were being screened for the first time, it is possiblethat some of them had undergone previous colorectal screeningelsewhere. However, the groups were similar in several importantrespects, including a relatively young age and a predominanceof women. Age and sex have been shown to be strong predictivefactors for the prevalence of adenomas and high-grade dysplasias.1,35The percentage of patients with a positive family history washigher in the OC group, which should have resulted in more advancedadenomas in that group. The fact that similar numbers of advancedadenomas were seen in the two groups further reinforces thepotential of CTC for screening.
In conclusion, CTC and OC screening methods resulted in similardetection rates for advanced neoplasias within the same generalpopulation. This finding is important because advanced neoplasmsrepresent the primary target of colorectal screening and cancerprevention. The marked decrease in the use of OC and total ratesof polypectomies in the CTC group suggests that this techniqueis a safe, clinically effective, and cost-effective filter fortherapeutic OC. Furthermore, by combining primary CTC and primaryOC screening efforts, with the choice between tests driven bypatient preference, the overall screening compliance for totalcolonic examination could substantially increase.
Dr. Kim reports serving on the medical advisory board for C.B.Fleet and receiving lecture fees from Viatronix; Dr. Pickhardt,receiving consulting fees from C.B. Fleet, Viatronix, Medicsight,and Philips Medical Systems; and Dr. Gopal, receiving lecturefees from AstraZeneca. No other potential conflict of interestrelevant to this article was reported.
We thank Holly C. Casson, R.N., B.S.N., clinical program coordinatorfor CTC; Stephanie Schiro, CTC program assistant; and Cara H.Olsen of the Biostatistics Consulting Center, Bethesda, MD,for statistical-analysis support.
Source Information
From the Department of Radiology (D.H.K., P.J.P., A.J.T., W.K.L., T.C.W., J.L.H.) and the Section of Gastroenterology and Hepatology (D.V.G., M.R., R.H.H., P.R.P.), University of Wisconsin Medical School, Madison.
Address reprint requests to Dr. Kim at the Department of Radiology, University of Wisconsin Medical School, E3/311 Clinical Science Center, 600 Highland Ave., Madison, WI 53792-3252, or at dkim{at}uwhealth.org.
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5 mm) were not reported.5,11 After CTC, patients resumed their regular activities but remained in a fasting state to allow for same-day OC, if necessary. Final CTC results were relayed to patients within 2 hours after the procedure. 
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