A Comparison of Virtual and Conventional Colonoscopy for the Detection of Colorectal Polyps
Helen M. Fenlon, M.B., David P. Nunes, M.B., Paul C. Schroy, M.D., M.P.H., Matthew A. Barish, M.D., Peter D. Clarke, M.D., and Joseph T. Ferrucci, M.D.
Background Virtual colonoscopy is a new method of imaging thecolon in which thin-section, helical computed tomography (CT)is used to generate high-resolution, two-dimensional axial images.Three-dimensional images of the colon simulating those obtainedwith conventional colonoscopy are then reconstructed off-line.We compared the performance of virtual and conventional colonoscopyfor the detection of colorectal polyps.
Methods We prospectively studied 100 patients at high risk forcolorectal neoplasia (60 men and 40 women; mean age, 62 years).We performed virtual colonoscopy immediately before conventionalcolonoscopy. We inserted a rectal tube and insufflated the colonwith air to the maximal level that the patient could tolerate.We administered 1 mg of glucagon intravenously immediately beforeCT scanning to minimize the degree of smooth-muscle spasm andperistalsis and to reduce the patient's discomfort.
Results The entire colon was clearly seen by virtual colonoscopyin 87 patients and by convention-al colonoscopy in 89. Fifty-onepatients had normal findings on conventional colonoscopy. Inthe other 49, we identified a total of 115 polyps and 3 carcinomas.Virtual colonoscopy identified all 3 cancers, 20 of 22 polypsthat were 10 mm or more in diameter (91 percent), 33 of 40 thatwere 6 to 9 mm (82 percent), and 29 of 53 that were 5 mm orsmaller (55 percent). There were 19 false positive findingsof polyps and no false positive findings of cancer. Of the 69adenomatous polyps, 46 of the 51 that were 6 mm or more in diameter(90 percent) and 12 of the 18 that were 5 mm or smaller (67percent) were correctly identified by virtual colonoscopy. Althoughdiscomfort was not specifically recorded, none of the patientsrequested that virtual colonoscopy be stopped because of discomfortor pain.
Conclusions In patients at high risk for colorectal neoplasia,virtual and conventional colonoscopy have similar efficacy forthe detection of polyps 6 mm or more in diameter.
Colorectal cancer is the second leading cause of cancer-relateddeath in the United States. A total of approximately 129,000new cases of carcinoma of the colon will be diagnosed in 1999,and 56,600 patients will die of the disease.1 Screening andsurveillance are cost-effective strategies for reducing boththe incidence of and mortality due to colorectal cancer.2,3,4,5,6To date, however, implementation of these procedures has beenlimited, partly because of the lack of an optimal screeningstrategy that is safe and acceptable to patients and that provideshigh diagnostic accuracy at low cost.
Virtual colonoscopy is a new method of imaging the colon inwhich thin-section, helical computed tomography (CT) is usedto generate high-resolution, two-dimensional axial images. Three-dimensionalimages of the colon, simulating those obtained with conventionalcolonoscopy, are then reconstructed off-line.7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27Studies suggest that this technique may be an attractive alternativeto existing screening tests for colorectal cancer, since itis relatively safe and minimally invasive. The diagnostic accuracyof virtual colonoscopy remains unknown. We conducted a prospectivestudy of the diagnostic performance of virtual colonoscopy,as compared with conventional colonoscopy performed on the sameday, in a group of patients at high risk for colorectal neoplasia.
Methods
Study Group
Between March 1997 and January 1999, we recruited 100 patientsat high risk for colorectal neoplasia (60 men and 40 women;mean age, 62 years; range, 50 to 77 years). Patients were consideredto be at high risk if they were 50 years of age or older andif they had a history of adenomatous polyps, recent sigmoidoscopicevidence of one or more polyps, a positive finding on fecaloccult-blood testing, or a history of colorectal cancer in oneor more first-degree relatives. Exclusion criteria were clinicalor radiologic evidence of large-bowel obstruction or ischemia;colonic biopsy or polypectomy within the previous 14 days; retainedbarium on a scout film; colostomy; a known allergy to glucagon;known glucagonoma, insulinoma, or pheochromocytoma; and pregnancy.Logistical constraints (e.g., scheduling conflicts) and theavailability of endoscopy without the requirement of a priorconsultation precluded the use of a consecutive-enrollment scheme.The study protocol was approved by the institutional reviewboard of the Boston Medical Center, and written informed consentwas obtained from all participants.
Technique
The patients underwent bowel preparation with either 4 litersof a polyethylene glycol–electrolyte solution or a 48-hourliquid diet combined with two 8-oz (240-ml) doses of magnesiumcitrate, after which a commercially available bisacodyl andsodium phosphate enema was administered. All virtual colonoscopicexaminations were performed immediately before conventionalcolonoscopy.
Virtual colonoscopic examinations were performed according toa previously described protocol.13,21,22,23,24,25 A rectal tubewas inserted, and the colon was gently insufflated with roomair to the maximal level tolerated by the patient. One milligramof glucagon was given immediately before helical CT imagingof the abdomen and pelvis in order to minimize the degree ofsmooth-muscle spasm and peristalsis and to reduce discomfort.A standard CT scout film of the abdomen and pelvis was acquiredto assess the degree of colonic distention, and additional airwas insufflated as required.
All CT examinations were performed with the use of a helicalCT scanner (model PQ-5000, Picker International, Cleveland).Images were acquired with the use of 5-mm collimation, a tablespeed of 6.25 mm per second at 110 mA and 110 kV, and a matrixof 512 by 512. Images were obtained during a single breath-holdingsession when possible in order to visualize the entire colon.Images were reconstructed at 2-mm intervals, with a 3-mm sliceoverlap. The procedure was first performed with the patientin the supine position and then repeated with the patient inthe prone position.
The CT data were downloaded to a workstation (Voxel Q, PickerInternational) equipped with software for three-dimensionalrendering (epi-Scope 3.4 and Voyager 3.4, Picker International).Using this software, a single radiologist, who was unaware ofthe results of conventional colonoscopy, generated both antegradeand retrograde endoluminal virtual endoscopic navigations ofthe colon.
Interpretation
The axial two-dimensional CT images and endoluminal three-dimensionalreconstructions were reviewed by two experienced gastrointestinalradiologists who were unaware of the results of conventionalcolonoscopy and all previous evaluations, including flexiblesigmoidoscopy. Axial CT images, obtained with the patient lyingboth supine and prone, were viewed at a window level of –1000Hounsfield units and a window width of 500 Hounsfield units.The endoluminal images were reviewed on a 17-in. (43-cm) monitor(Voxel Q) at a rate of 5 to 30 frames per second. Final interpretationswere based on a combined evaluation of the axial CT images andthe endoluminal images. The radiologists reviewed the studiesjointly and arrived at a consensus.
Conventional Colonoscopy
Conventional colonoscopy was performed by an experienced gastroenterologistimmediately after virtual colonoscopy, with the use of a standardendoscope (model CFQ-140L, Olympus, Lake Success, N.Y.). Theendoscopists were not aware of the results of virtual colonoscopy.In cases in which the conventional colonoscopic examinationwas incomplete, the endoscopist's best estimate of the depthof inspection was recorded. The location of each lesion wasdocumented, and the size was measured by comparison with anopen biopsy forceps.28
Statistical Analysis
We regarded the results of conventional colonoscopy as the goldstandard against which the results of virtual colonoscopy werecompared. The results of virtual colonoscopy were analyzed ona per-polyp basis. Analysis included an evaluation of the agreementbetween the two methods of colonoscopy with respect to boththe size and the location of the polyp. For the purpose of determininglocation, the colon was divided into six segments: rectum, sigmoidcolon, descending colon, transverse colon, ascending colon,and cecum. For a true positive result, the lesion identifiedon virtual colonoscopy had to have been matched according tolocation, size, and morphologic features to a lesion found onconventional colonoscopy. In the per-patient evaluation, a resultwas considered to be truly positive only when at least one polypidentified on virtual colonoscopy was matched to a lesion seenon conventional colonoscopy. All other results were consideredto be false positive. The chi-square test was used to determinesignificant differences.
Results
Conventional Colonoscopy
Of the 100 patients, 51 had normal findings on conventionalcolonoscopy. A total of 115 polyps and 3 carcinomas were identifiedin 49 patients. Fifty-three of the 115 polyps (46 percent) were1 to 5 mm in diameter, 40 (35 percent) were 6 to 9 mm, and 22(19 percent) were 10 mm or larger. Of the 115 polyps identified,101 (88 percent) were successfully removed and examined histologically;69 were adenomatous and 32 were hyperplastic. Hyperplastic polyps(32 percent of the polyps retrieved) tended to be smaller thanadenomatous polyps (P=0.001) and were predominantly on the leftside of the colon, whereas adenomatous polyps were more evenlydistributed (P=0.02) (Table 1). All three of the adenocarcinomaswere sessile; one was located in the sigmoid colon (35 mm),one in the transverse colon (25 mm), and one in the cecum (25mm).
Table 1. Histologic Classification of 101 Retrieved Polyps According to Size and Location.
Eighty-nine percent of the conventional colonoscopic examinationswere complete, with visualization to the cecum. Reasons forincomplete colonoscopy included inadequate bowel preparation,tortuosity, and lack of cooperation on the part of the patient.The only documented complication of conventional colonoscopywas a perforation of the sigmoid colon in a patient with sigmoiddiverticular disease. This patient was admitted to the hospitalfor observation but did not require surgery.
Virtual Colonoscopy
Table 2 shows the performance of virtual colonoscopy for thedetection of polyps, according to size and histologic type.Eighty-two of the 115 polyps (71 percent) seen on conventionalcolonoscopy were correctly identified on the basis of locationand size. An example is shown in Figure 1. The sensitivity ofvirtual colonoscopy was related to the size of the polyp. Only29 of 53 polyps between 1 and 5 mm in diameter (55 percent)were correctly identified on virtual colonoscopy. The sensitivityfor the detection of polyps that were 6 to 9 mm and those thatwere 10 mm or larger was significantly higher (82 percent and91 percent, respectively; P=0.001). The performance of virtualcolonoscopy was also related to histologic type. The sensitivityof virtual colonoscopy for the detection of hyperplastic polyps1 to 5 mm in diameter was significantly lower than that forthe detection of adenomatous polyps of the same size (48 percentvs. 67 percent, P=0.003). The sensitivity of virtual colonoscopywas 71 percent for the detection of hyperplastic polyps 6 to9 mm in diameter and 90 percent for adenomatous polyps of thesame size. All three cancers were identified on virtual colonoscopy;an example is shown in Figure 2.
An 8-mm polyp was identified on an axial two-dimensional CT image of the colon (Panel A, arrow) and on an endoluminal three-dimensional reconstruction (Panel B, arrow). The polyp was confirmed on conventional colonoscopy performed the same day (Panel C, arrow). Histologic examination revealed an adenomatous polyp.
A 25-mm sessile carcinoma was identified on an axial two-dimensional CT image of the cecum (Panel A, arrow). The same image shows a 6-mm polyp on the opposite wall of the cecum (arrowhead). The endoluminal three-dimensional image showed the carcinoma (Panel B, arrow), as well as the polyp (not shown). A normal ileocecal valve was also seen. Conventional colonoscopy performed on the same day confirmed the carcinoma (Panel C, arrow) and the polyp (not shown). Histologic examination of the polyp revealed that it was adenomatous and that the cancer was an adenocarcinoma.
There were 19 false positive findings of polyps on virtual colonoscopy;9 were 1 to 5 mm in diameter, 8 were 6 to 9 mm, and 2 were 10mm or more (Table 2). Nine of the false positive findings werein segments of colon containing residual solid stool, and eightwere in segments of colon (particularly the sigmoid colon) withdiverticular disease and poor distention, where thickened andcomplex haustral folds were misinterpreted as polyps; the othertwo were in clean, well-distended areas of colon. There wereno false positive reports of cancer on virtual colonoscopy.
Of the 33 polyps that were not detected on virtual colonoscopy,24 (73 percent) were between 1 and 5 mm in diameter. Retrospectiveanalysis of the images did not result in the identificationof many of these polyps, despite adequate distention and preparationof the colon. Limited image resolution probably accounts formost of these false negative results. False negative resultsfor the seven polyps that were 6 to 9 mm in diameter and thetwo that were 10 mm or larger were due to the misinterpretationof polyps as stool (two polyps) or as folds (three) or to inadequatevisualization because of retained intraluminal fluid and poorcolonic distention (four). Of the two false negative resultsinvolving polyps that were 10 mm or more in diameter, one wasdue to inadequate distention of the sigmoid colon, and the otherwas due to an error in interpretation. The latter polyp, a 25-mmmass located in the proximal sigmoid colon, was the largestpolyp missed (Figure 3). Although the mass was identified onvirtual colonoscopy, the dramatic difference in its positionon the two films obtained with the patient in the prone andsupine positions was interpreted as indicating the presenceof stool rather than a polyp on a very long stalk.
Figure 3. False Negative Finding on Virtual Colonoscopy.
An axial CT image obtained with the patient supine showed a 25-mm mass in the descending colon (Panel A, arrow). A portion of the normal ileocecal valve is also shown (arrowhead). With the patient in the prone position, the mass apparently moved distally into the sigmoid colon and was located at the opposite wall (Panel B, arrow). The mass was misinterpreted as stool because of the difference in its position in the two images. On conventional colonoscopy, the mass proved to be a 25-mm pedunculated, adenomatous polyp in the descending colon (Panel C, arrow) on a 5-cm stalk (Panel D, arrow).
When the results of virtual colonoscopy were analyzed on a per-patientbasis, the performance was improved. If the detection of polypsof all sizes was regarded as important, the results of 42 virtualcolonoscopic examinations would have been classified as truepositive results, 41 as true negative results, 8 as false positiveresults, and 9 as false negative results. Therefore, when polypsof all sizes were included, the per-patient sensitivity of virtualcolonoscopy was 82 percent, and the specificity was 84 percent.The positive and negative predictive values were 82 and 84 percent,respectively. The per-patient performance improved as the sizeof the polyps increased; virtual colonoscopy had a sensitivityof 94 percent and a specificity of 92 percent for the detectionof polyps between 6 and 9 mm in diameter, with positive andnegative predictive values of 92 and 94 percent, respectively.At 10 mm, the sensitivity, specificity, and positive and negativepredictive values for virtual colonoscopy were each 96 percent.It should be noted that in the per-patient analysis, only lesionsthat had been matched with polyps seen on conventional colonoscopywere regarded as true positive findings.
The entire colon was clearly seen on virtual colonoscopy in87 of the 100 patients, as compared with 89 on conventionalcolonoscopy. In 13 patients, virtual colonoscopic evaluationwas incomplete because of a combination of inadequate distentionof the colon and retained intraluminal fluid or stool. On average,the time required for virtual colonoscopy was just under 20minutes for CT scanning, 30 minutes for image manipulation,and 10 minutes for interpretation.
Air insufflation was performed to the maximal level toleratedby the patient. Although discomfort was not specifically recorded,none of the patients requested that the procedure be stoppedbecause of discomfort or pain. The patients who reported discomfortdescribed it as mild bloating or cramping. After the injectionof intravenous glucagon, several patients reported nausea.
Discussion
Since its description in 1994,7 virtual colonoscopy has emergedas a promising method of colorectal evaluation. Although investigatorshave used a variety of terms and scanning techniques,7,8,9,10,11,12,16,17,18,22,23,24,25,26the same basic imaging principles apply: thin-section, helicalCT of the air-distended, clean colon, with interpretation ofdata based on both axial two-dimensional images of the colonicmucosa and computer-generated, three-dimensional, reconstructedimages. This technique has been evaluated in in vitro studies,10,11,16,17in studies of patients with proven carcinoma of the colon,21,24,25and in studies of small numbers of patients with colorectalpolyps.8,16 Data from these preliminary studies suggested asensitivity of more than 75 percent and a specificity of morethan 90 percent for large colorectal polyps (those more than10 mm in diameter) and cancers. These studies also demonstratedseveral technical advantages of virtual colonoscopy over conventionalcolonoscopy, including visualization of the colon next to anobstructing lesion24 and ease of inspection of both antegradeand retrograde sides of haustral folds, resulting in the identificationof large lesions missed on endoscopy.25
As expected, the performance of virtual colonoscopy was highlydependent on the size of the lesion. As demonstrated in thein vitro models, the threshold for the reliable detection ofsmall lesions was approximately 5 mm.15,17 However, the rateof detection of larger polyps, and adenomatous polyps in particular,was much better and approached the reported rate for the detectionof adenomatous polyps 6 mm or larger by conventional colonoscopy.29The lower sensitivity for the detection of hyperplastic polypsmay reflect the tendency of these polyps to be effaced whenthe colon is distended with air.30
Care must be taken in reporting false positive results withvirtual colonoscopy. Although conventional colonoscopy was usedas the gold standard in this study, between 10 and 20 percentof colonic polyps and up to 5 percent of colorectal cancersmay be missed on conventional colonoscopy.29,31,32,33 We havefound that virtual colonoscopy can identify large colonic polyps(adenomas of 5 mm or larger) not seen on initial conventionalcolonoscopy. Consequently, it is possible that the true specificityand positive predictive value of virtual colonoscopy are higherthan those reported here.
As a means of detecting colonic polyps and as a potential screeningtool, virtual colonoscopy must be measured against other diagnosticapproaches, including fecal occult-blood testing, sigmoidoscopy,and double-contrast barium enema. Because it allows for directvisualization of the entire colon, virtual colonoscopy has advantagesover both fecal occult-blood testing2,3,4,34,35,36,37 and sigmoidoscopy.38,39In the only direct comparison to date, virtual colonoscopy wasmore sensitive than single-contrast barium enema for the detectionof polyps.11 Our data also suggest that virtual colonoscopyis superior to double-contrast barium enema, which has a reportedsensitivity of 65 to 75 percent for the detection of polypslarger than 7 mm in patients undergoing surveillance examinationsbecause of a history of colorectal adenomas.40,41 Furthermore,the results of double-contrast barium enema are highly dependenton the skill of the operator.42,43 Improvements in the meansof acquisition of CT data (multidetector systems) and in softwareare likely to improve the results of virtual colonoscopy andtheir reproducibility, in terms of both the quality of the imagesand the interpretation of the data. Together, these improvementsmay reduce the cost of the procedure by decreasing the amountof time required for both scanning and three-dimensional reconstruction.
Virtual colonoscopy is relatively simple and is less invasivethan conventional colonoscopy. Although full preparation ofthe colon is required, the procedure takes considerably lesstime than conventional colonoscopy and does not require sedation.Most patients experience some abdominal discomfort as a resultof air insufflation, but the examination may be more acceptableto patients than conventional colonoscopy.13,44
An important question is whether the low rate of sensitivityfor the detection of polyps between 1 and 5 mm in diameter isacceptable. There is controversy about what constitutes a clinicallysignificant polyp with regard to size.45,46,47 Although manywould argue for the removal of all adenomatous polyps, whatevertheir size, the prevalence of polyps less than 10 mm in diameterin people over 50 years of age is high (30 to 50 percent).3,48Removal of all such polyps for the prevention of colorectalcarcinoma would be a formidable challenge. Moreover, in thesubgroup of patients with adenomatous polyps that are 10 mmor smaller, the probability of cancer is low, and the likelihoodof any single lesion progressing to cancer is also small.49On the basis of these data, Glick et al.50 have suggested thata policy of identifying and removing only polyps above a specificthreshold for size, as opposed to a policy of universal polypectomy,could result in a similar reduction in mortality but at lowerrisk and lower cost.
Our study has several limitations. First, the diagnostic accuracyof virtual colonoscopy in this study of high-risk patients maybe an overestimation of its performance in persons with averagerisk. Hence the validity of this technique as a screening testneeds to be confirmed. Second, our highly selective patient-recruitmentscheme precluded a meaningful assessment of whether patientswill find virtual colonoscopy acceptable. Similarly, our studydesign did not allow us to compare virtual colonoscopy and conventionalcolonoscopy with respect to tolerance of the procedure, sideeffects, patients' preference, or cost. Furthermore, we didnot address the reproducibility of our results in terms of variabilitybetween observers and between centers. Further studies are neededto address each of these limitations before widespread use ofvirtual colonoscopy can be recommended.
Supported in part by a grant from the Research and EducationFund of the Radiological Society of North America.
Source Information
From the Departments of Radiology (H.M.F., M.A.B., P.D.C., J.T.F.) and Gastroenterology (D.P.N., P.C.S.), Boston University School of Medicine, Boston Medical Center, Boston.
Address reprint requests to Dr. Barish at the Department of Radiology, Boston University School of Medicine, Boston Medical Center, Boston, MA 02118, or at mbarish{at}virtualcolonoscopy.net.
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Virtual Colonoscopy
Mackenzie S., Vallance R., O'Dwyer P. J., Glick S. N., Anderson J. C., Pollack B. J., Shaw R. D., Morrin M. M., Farrell R. J., Kruskal J. B., Silverman C., Fenlon H. H., Barish M. A., Ferrucci J. T., Bond J. H.
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Full Text
N Engl J Med 2000;
342:737-739, Mar 9, 2000.
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A correction has been published: N Engl J Med 2000;342(7):524.
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