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1 Department of Radiology, Abdominal Imaging, NYU Medical Center, Tisch
Hospital, 560 First Ave., Ste. HW 207, New York, NY 10016.
2 Department of Medicine, Division of Gastroenterology, NYU Medical Center, New
York, NY 10016.
Received November 3, 2003;
accepted after revision January 30, 2004.
Address correspondence to M. Macari
(michael.macari{at}med.nyu.edu).
Abstract
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SUBJECTS AND METHODS. One hundred eighty-six men (age range, 40–87 years; mean, 62.3 years) underwent CT colonography immediately before conventional colonoscopy. All polyps detected on CT colonography were measured and imaged, and their segmental location was documented. All polyps detected on colonoscopy were measured, photographed, biopsied, and histologically analyzed. Results of CT colonography and conventional colonoscopy were compared with the final pathology reports. Conventional colonoscopy was used as the gold standard unless CT colonography showed a lesion measuring 10 mm or more that was not detected on conventional colonoscopy and had characteristics of a polyp. In these cases, follow-up conventional colonoscopy was offered.
RESULTS. One hundred ninety-one polyps were detected on conventional colonoscopy. CT colonography prospectively detected 53 polyps. Histologic analysis of the polyps not detected on CT colonography showed that of those 5 mm or smaller, 58.1% were not adenomas, and of those measuring 6–9 mm, 42.8% were not adenomas. Both missed polyps at CT colonography of 10 mm or more were adenomas. Of the 22 polyps measuring 10 mm or more, three were not detected on conventional colonoscopy. Of these three, CT colonography showed a lesion having characteristics of a polyp, follow-up endoscopy confirmed the presence of the lesion, and histologic analysis showed a villous adenoma, a tubulovillous adenoma, and a tubular adenoma.
CONCLUSION. If CT colonography shows no abnormality, follow-up screening in 5 years is recommended. If CT colonography detects a lesion smaller than 5 mm, follow-up imaging in 3–5 years is recommended. If CT colonography detects a lesion measuring 6 mm or more, endoscopy and polypectomy should be offered unless contraindicated.
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5 mm) is 10–67%
[2–9].
The sensitivity of the examination for larger raised polyps—10 mm or
more—is approximately 75–90%. Currently, the American
Gastroenterological Association (AGA) states that CT colonography is a
promising technique for colorectal screening but not yet ready for
"prime-time" screening. A major concern is that CT colonography
performs poorly for detecting small polyps. However, many small colonic protrusions are normal colonic mucosa or hyperplastic polyps at pathologic evaluation [5]. These lesions have no clinical potential to become carcinoma. Although small adenomas are not uncommon, their clinical significance has been questioned [10–15]. One study found that of 357 adenomas smaller than 10 mm, only 11 showed severe dysplasia, and in only two was carcinoma found [10]. In neither case was the lesion smaller than 5 mm.
Although it is generally agreed that most colorectal carcinomas develop from precursor adenomatous polyps, the dwell time and growth rate for these small polyps to become carcinoma is very long, estimated to be greater than 10 years [11, 12]. If colorectal screening is performed at routine intervals, detecting growth in these lesions should be possible.
The purpose of this study was twofold: first, to determine the histology and clinical significance of small polyps missed at CT colonography when compared with colonoscopy; and second, to propose an algorithm for follow-up screening, surveillance, and intervention based on various findings at CT colonography.
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CT Colonography Technique
On the day before the study, one of two bowel preparations was
administered, either oral hydration with two 45-mL doses of Phospho-Soda
([sodium phosphate] prep 1, Fleet Pharmaceuticals) or 4 L of polyethylene
glycol and electrolytes solution (GoLYTELY, Braintree Laboratories). On site
and immediately before CT colonography, the patient evacuated any residual
fluid from the rectum.
CT colonography was performed on a Plus 4 Volume Zoom MDCT system (Siemens Medical Solutions). A flexible rubber catheter was inserted into the rectum and the colon was insufflated with room air to patient tolerance by an experienced technologist or nurse practitioner. CT colonography was performed with the patient in the supine and prone positions and encompassed the entire colon and rectum.
CT parameters included 4 x 1 mm detector configuration, 120 kV, 0.5-sec gantry rotation, and 50 effective mAs in a 30-sec breath-hold. CT images were reconstructed as 1.25-mm-thick sections with a 1-mm reconstruction interval.
CT Colonography Data Interpretation
All CT examinations were interpreted by a single abdominal radiologist who
had 5 years of experience with CT colonography interpretation. The radiologist
was not informed of the patient's history, risk factors, or other demographic
information. CT colonography data were networked to a Vitrea 2 workstation
(Vital Images). The presence, location, size, and morphology of colorectal
polyps were assessed over six colonic segments (cecum, ascending colon,
transverse colon, descending colon, sigmoid, and rectum), to facilitate
polyp-to-polyp mapping with conventional colonoscopy. The evaluation time was
recorded. The presence or absence of polyps or cancers was recorded.
Assessment was made in this fashion because the implication of a positive
result (polyp or cancer) would be that follow-up colonoscopy would be
required, depending on the size of the abnormality.
Colonoscopy
Colonoscopy was performed, without knowledge of CT colonography findings,
by a board-certified gastroenterologist or a senior gastroenterology fellow
under the direct supervision of the attending gastroenterologist. All polyps
identified at colonoscopy were photographed, biopsied or removed by snare
polypectomy, and sent for histologic analysis. Polyps were measured in
millimeters using an open biopsy forceps technique. The location of each polyp
was mapped within the same six colonic segments used in the CT analysis.
CT Colonography and Colonoscopy Data Comparison
Biweekly, the radiologist and the gastroenterologist reviewed the findings
in each patient. For purposes of CT colonography analysis, a finding was
defined as true-positive when the CT colonography data and the conventional
colonoscopy data both depicted a lesion in the same anatomic segment with
similar morphology and size. A finding was defined as true-negative when both
CT colonography and colonoscopy revealed no abnormalities in the same segment.
A finding was defined as false-positive when CT colonography detected an
abnormality measuring less than 10 mm that was not present in the same segment
on colonoscopy. A finding was defined as false-negative when a lesion was
detected in a segment on colonoscopy but not on CT colonography. If CT
colonography and conventional colonoscopy both detected a lesion in the same
segment with similar morphology but with a slight difference in the estimation
of polyp size ( 3 mm), these were considered to be the same polyp. In
these cases, the radiologist and gastroenterologist carefully reviewed the
images of the polyp in an attempt to determine the actual size.
If CT colonography detected a lesion measuring 10 mm or more that was not seen on conventional colonoscopy but showed morphology and attenuation characteristics consistent with a polyp, the patient was offered follow-up colonoscopy. If a polyp was subsequently confirmed, the reasons for initial nonobservation on colonoscopy were evaluated.
Histologic Analysis
In all cases in which a polyp was present at colonoscopy, a pathologist
reviewed the biopsy material. The pathology report from this biopsy material
was reviewed to determine the histology of all biopsied polyps. In all cases
in which a polyp was present on colonoscopy but not prospectively identified
on CT colonography, the histology of the missed polyp was documented in an
attempt to determine its clinical significance.
Statistical Analysis
The sensitivity and specificity of CT colonography were assessed using
conventional colonoscopy as the gold standard. A bootstrap resampling method
was used to generate 95% confidence intervals (CIs) for the sensitivity of CT
colonography in detecting polyps measuring 5 mm or less, 6–9 mm, and 10
mm or more. An exact 95% confidence interval for the specificity of CT
colonography was obtained using the binomial as the reference
distribution.
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CT colonography detected 21 of 143 lesions 5 mm or smaller (95% CI, 9.1–22.2%), 12 of 26 between 6 and 9 mm (95% CI, 26.2–67.2%), and 20 of 22 polyps measuring 10 mm or more (95% CI, 70.9–99.1%) (Table 1).
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Histologic analysis of the 122 lesions measuring 5 mm or less that were not detected at CT colonography showed that 30 were normal colonic mucosa, 37 were hyperplastic polyps, 43 were tubular adenomas, seven were tubulovillous adenomas, one was a villous adenoma, and four were unknown pathology. Of the 122 lesions of 5 mm or smaller that were not detected on CT colonography, 58.1% (95% CI, 48.5–68.1%) were not adenomas (Figs. 1,2,3) (Table 2).
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Histologic analysis of the 14 lesions measuring 6–9 mm that were not detected on CT colonography showed that one was colonic mucosa, three were hyperplastic polyps, seven were tubular adenomas, one was a tubulovillous adenoma, and two were unknown pathology. Of the 14 lesions measuring 6–9 mm, 42.8% (95% CI, 17.7–71.1%) were not adenomas. Histologic analysis of the two lesions of 10 mm or greater that were not detected on CT colonography showed that one was a tubular adenoma and one was a tubulovillous adenoma.
In the remaining 89 patients, conventional colonoscopy showed no abnormality. Seventy-four of these 89 patients showed no abnormality on CT colonography, for an overall per patient specificity of 83.1% (95% CI, 73.7–90.2%). A total of 28 lesions detected on CT colonography were not matched according to size, location, or morphology with findings at conventional colonoscopy. Therefore, these 28 lesions were considered false-positive. Seventeen (60.7%) were 5 mm or smaller, eight (28.6%) measured 6–9 mm, and three (10.7%) were 10 mm or larger. On further review, the three lesions that measured 10 mm or greater on CT colonography and were not detected on conventional colonoscopy showed homogeneous attenuation and morphologic characteristics that were consistent with polyps. All three of these patients underwent repeated colonoscopy that confirmed the presence of a colorectal polyp at the expected location, as shown on CT colonography.
In these three cases, the reasons for not visualizing the lesion at initial endoscopy were investigated. In the first patient, CT colonography showed a 12-mm lesion in the sigmoid colon that was probably obscured by an interhaustral fold during endoscopy (Fig. 4A, 4B, 4C, 4D). Follow-up colonoscopy and polypectomy showed a villous adenoma. In the second patient, a 10-mm lesion in the sigmoid colon was in an area of severe diverticular disease (Fig. 5A, 5B, 5C). Follow-up colonoscopy and polypectomy showed a 10-mm tubulovillous adenoma. In the third patient, colonoscopy was completed only to the transverse colon because of difficulty obtaining adequate sedation; at CT colonography a 17-mm lesion was seen in the ascending colon. Follow-up colonoscopy was completed to the cecum and confirmed a 17-mm tubular adenoma (Fig. 6A, 6B, 6C).
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When considering what constitutes a clinically significant colorectal polyp, three factors are of special importance: histology, gross morphology, and size [12].
Most imaging studies cannot predict the histology of colorectal lesions with the exception of lipomas. Likewise, visual inspection of a colorectal polyp at conventional colonoscopy usually cannot differentiate among normal colonic mucosal protrusions, lymphoid aggregates, hyperplastic polyps, and adenomas [10, 16].
The gross morphology of polyps is occasionally helpful in predicting histology. Polyps that are flat, sessile, or irregular, especially lesions that are ulcerated, tend to have a more advanced histology, such as tubular or villous adenomas. Polyps that are pedunculated tend to have a more benign histology and include hyperplastic and inflammatory polyps and tubular adenomas [12]. However, gross morphology alone cannot be used to determine clinical significance because some sessile lesions are hyperplastic and some pedunculated lesions contain villous histology [16, 17].
The imaging criterion that has primarily been used to determine clinical significance is size [12]. Size has been shown to be the most simple and practical indicator of polyp abnormalities and is closely related to the degree of dysplasia in the lesion [17]. However, some controversy exists about when to consider a colorectal polyp clinically significant on the basis of size alone [11, 13, 18]. In a study of 1,048 colorectal polyps measuring up to 6 mm, Waye et al. [18] found that 61% were neoplastic (adenomas); the remainder were divided equally between hyperplastic polyps and normal colonic mucosa [18]. In that cohort of polyps, the incidence of carcinoma was extremely low, 0.1%. Nevertheless, the authors recommended that all diminutive polyps be resected because most were adenomas.
Other studies evaluating the significance of small colorectal polyps have reached different conclusions. One study evaluating diminutive polyps measuring 3 mm or less found that 90% were hyperplastic [19]. Aldridge and Simson [10], in a review of 1,228 colorectal polyps measuring less than 10 mm, found that 657 were adenomas. In that series, only two carcinomas were detected, and in neither case was the carcinoma in a polyp smaller than 5 mm. On the basis of those observations, the authors recommended removal of all polyps greater than 5 mm, although surveillance could be performed if a polyp is smaller than 5 mm. In a larger review of 20,000 polyps, Nusko et al. [14] found that colorectal polyp size was the most important factor in determining malignancy. In that series, invasive carcinoma was not present in any of the 5,027 small adenomas measuring 5 mm or less.
Most colorectal cancers progress through the adenoma–carcinoma sequence [10, 12, 16, 20]. As many as 90% of all colorectal cancers develop from benign adenomas through a series of genetic alterations [10, 17]. However, most diminutive adenomas never progress through this complete sequence of events. As a result, attention should be shifted away from identifying and removing all diminutive polyps and toward strategies that will allow reliable detection of the less common, but more dangerous, advanced adenomas [13].
Moreover, those diminutive adenomas that do progress to carcinoma, do so very slowly [12, 21]. Analysis of data from the National Polyp Study shows that an average of 5.5 years is required for the transformation of a large adenomatous polyp into cancer. An average of 10 years is needed for the smallest polyps to develop into cancer [20]. Muto et al. [12] concluded that it takes an average of 10–15 years for most adenomas to become cancer [12].
The current screening recommendations of the AGA for colorectal cancer include a yearly fecal occult blood test with sigmoidoscopy or double-contrast barium enema every 5 years or colonoscopy every 10 years [22, 23]. The AGA considers CT colonography a potentially promising tool yet states it is not yet ready to be used for widespread screening [23]. However, in clinical practice patients undergo CT colonography for a variety of reasons, including incomplete colonoscopy, medical conditions that make conventional colonoscopy risky, and patient refusal to undergo other screening tests. CT colonography is therefore being performed with increasing frequency.
Because of the natural history of most colorectal polyps, the findings in this study, and the previously reported sensitivity of CT colonography for detecting colorectal polyps, if an appropriate screening and surveillance interval were established for CT colonography, adenomas that are missed and subsequently increase in size should be detected on follow-up studies before they reach the stage of invasive cancer. The following algorithm for patient follow-up and management is predicated on the interpretation of a well-prepared and well-distended colon by an experienced observer.
In patients with normal findings on CT colonography examinations, follow-up imaging is recommended in 5 years. This recommendation takes into account the facts that many diminutive polyps will not be detected and that some larger lesions measuring more than 6 mm may also be missed. Although this is a limitation of CT colonography, the gold standard—conventional colonoscopy—is also imperfect in the detection of colorectal polyps [24]. Miss rates of up to 25% for diminutive polyps have been reported for colonoscopy, and occasionally larger lesions are also missed. In our study, three of the confirmed lesions that measured 10 mm or more were not prospectively detected on conventional colonoscopy. Taking into account the differences in sensitivity of conventional colonoscopy and CT colonography, a 5-year followup after negative CT colonography findings would seem reasonable.
The current AGA-recommended screening interval for both sigmoidoscopy and double-contrast barium enema is 5 years. This is similar to our recommendation for CT colonography even though the sensitivity of CT colonography appears to be superior to that of the double-contrast barium enema, and CT colonography has the advantage of complete colonic evaluation when compared with flexible sigmoidoscopy [25–29].
If CT colonography detects a lesion measuring 5 mm or less, should colonoscopy be offered? Probably not, for several reasons. First, many of these lesions will not be adenomas but hyperplastic polyps, normal colonic protrusions, or retained adherent fecal material. As pointed out, those that are adenomas will likely not progress to cancer within 5 years. Thus, if a diminutive lesion is detected at CT colonography, surveillance imaging in 3–5 years, depending on the patient's age and overall health status, could be offered to determine if the lesion is still present and if it has grown. However, this is a recommendation only. If a patient undergoing CT colonography is found to have a 5-mm lesion in the rectum that has characteristics of a polyp, and the patient is in otherwise good health, sigmoidoscopy and polypectomy could be performed. Obviously, significant cost issues are raised when considering the need to pursue such small lesions.
If CT colonography detects a lesion of 6 mm or greater, colonoscopy should probably be offered. However, in some circumstances endoscopy for a lesion of this size may not be justified. If the patient has severe cardiac or pulmonary dysfunction, has an allergy to sedatives, has a bleeding diathesis, or is of advanced age, short-interval imaging follow-up every 1–2 years may be warranted instead of polypectomy. As we have stated, not all large polyps will progress to cancer. Although most studies evaluating CT colonography, including this one, have divided colonic polyps into size categories of 5 mm or less, 6–9 mm, and 10 mm or greater, a recent report that evaluated polyps on the basis of size suggested that 8 mm may be an appropriate threshold at which to pursue a finding at CT colonography [29]. Although such a policy may prove to be cost-effective, one must consider the inherent variability in measurement of polyp size with both CT and conventional colonoscopy.
Our study has some limitations. All data were interpreted by a radiologist
with extensive experience with CT colonography. A less experienced interpreter
might have had a decreased detection rate for polyps measuring 10 mm or more.
However, when compared with other studies, overall detection rates for polyps
in this size range (
10 mm) by experienced interpreters range from 75% to
95% [1]. In the future,
computer-aided detection algorithms may become a reality and may increase the
sensitivity of the examination. Moreover, a trend exists toward training
radiologists in the interpretation of CT colonography. Ultimately, a quality
assurance program (similar to that implemented for mammography) may be helpful
in establishing certain minimum standards before one can interpret CT
colonography data sets.
A second limitation is that no truly flat adenomas were present. Flat lesions are difficult to detect on CT colonography, and flat adenomas tend to have a more aggressive histology than raised polyps. A flat lesion is defined as one which has a height of less than 50% of its width. However, these lesions should be considered broad-based and are usually readily detected on CT colonography. A truly flat adenoma is barely raised from the colonic surface and usually is only minimally discolored when compared with normal colonic mucosa at colonoscopy [29]. However, truly flat lesions appear to be rare in Western populations, as evidenced by our study of 186 patients in which none was detected. Further evidence that these truly flat adenomas are rare comes from a recent report of 1,233 asymptomatic individuals who underwent CT and conventional colonoscopy [30]. In that study, flat adenomas were not mentioned, and 93.8% of all adenomas measuring at least 10 mm were detected on CT colonography.
A third limitation is that our recommendations are based on the reported natural history of colorectal lesions and not on follow-up imaging studies. Therefore, future studies should be performed that would provide patient follow-up with CT colonography over time to verify the recommendations proposed in this study.
A final limitation is that our study did not evaluate the cost-effectiveness of CT colonography. Cost-effectiveness is an important consideration because CT colonography is not an inexpensive examination and would be performed more frequently than colonoscopy for screening. Colonoscopy clearly cannot be performed for every diminutive lesion detected on CT colonography. Whether it is a 6-, 7-, 8-, or 10-mm lesion that ultimately prompts colonoscopy is critical to the issue of cost-effectiveness of CT colonography. A cost assessment of CT colonography relative to other screening tests is clearly warranted.
In conclusion, CT colonography detects most large polyps but performs less well for smaller lesions. Because of the natural history of colorectal cancer and the adenoma–carcinoma sequence, missing these small lesions may not be clinically important if an appropriate screening interval is established. We propose follow-up in 5 years if CT colonography findings are normal, follow-up in 3–5 years if a diminutive lesion is detected, and conventional colonoscopy if a lesion measuring 6 mm or greater is detected.
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