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1
Department of Radiology, Mayo Clinic, East-2B, 200 First St., S.W., Rochester,
MN 55905.
2
Present address: Department of Internal Medicine, Walter Reed Army Medical
Center, 6900 Georgia Ave., N.W., Washington, DC 20307-5001.
3
Division of Gastroenterology and Hepatology and Internal Medicine, Mayo
Clinic, Rochester, MN 55905.
4
Division of Colon and Rectal Surgery, Mayo Clinic, Rochester, MN 55905.
5
Section of Biostatistics, Mayo Clinic, Rochester, MN 55905.
Received June 15, 2001;
accepted after revision August 28, 2001.
Supported by Fraternal Order of the Eagles cancer grant 180 and Mayo
Foundation CR program grant 509-019-9904.
Abstract
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MATERIALS AND METHODS. Fifty patients with a history of resected invasive colorectal carcinoma underwent contrast-enhanced CT colonography and colonoscopy. Colonic distention was graded for different colonic segments. Two radiologists evaluated for the presence of local recurrence, metachronous disease, and metastatic disease. Results were compared with colonoscopy, histology, and clinical follow-up.
RESULTS. Most patients had adequate colonic inflation (37/50, 74%). Eleven of 13 patients with inadequate distention had collapse in the sigmoid colon, usually associated with ileocolic anastomoses. Contrast-enhanced CT colonography detected local recurrences with an accuracy of 94% (95% confidence interval, 83-99%). The accuracy of contrast-enhanced CT colonography for metachronous lesions greater than or equal to 1 cm was 92% (95% confidence interval, 80-98%), but there was only one such lesion, which was missed on initial colonoscopy. Stool, granulation tissue, and inflammation can mimic the CT appearance of local recurrence or metachronous disease and account for false-positive examinations. Contrast-enhanced CT colonography identified five patients with metastatic disease.
CONCLUSION. Suboptimal sigmoid distention can be seen on contrast-enhanced CT colonography, predominantly in patients with right hemicolectomies. Contrast-enhanced CT colonography is a promising method for detecting local recurrence, metachronous disease, and distant metastases in patients with prior invasive colorectal carcinoma. The technique can also serve as a useful adjunct to colonoscopy by detecting local recurrences or metachronous disease that are endoscopically obscure or by serving as a full structural colonic examination when endoscopy is incomplete.
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Recurrent colorectal carcinoma can be classified as local recurrence, metachronous disease, or distant recurrence (metastases). Local recurrence includes mucosal disease or extramucosal disease (perineural, serosal, or nodal) near the site of primary resection. Metachronous disease refers to other cancers or adenomas located at different sites in the colon. Distant recurrence includes metastases to the liver, lung, lymph nodes, and peritoneum. Patients with potentially curative colonic resections for invasive colorectal carcinoma are at risk for developing all types of recurrent colorectal carcinoma.
A large array of screening tests currently exist for recurrent colorectal cancer, but each test has limitations, and the follow-up of patients with invasive carcinoma after surgical resection is nonstandard [10, 11]. CT colonography has recently shown promise in detecting colonic neoplasia with a high degree of accuracy [12,13,14,15]. Like CT colonography, contrast-enhanced CT colonography is performed after an air enema and uses a narrow collimation and reconstruction interval to detect colonic lesions. Contrast-enhanced CT colonography, theoretically, has the ability to examine both the colonic mucosa and the pericolonic tissues for local recurrence. The administration of IV contrast material has recently been shown to improve the sensitivity of CT colonography for subcentimeter polyps that are 5 mm or greater [14] and should consequently aid in the detection of metachronous lesions. The use of standard dose settings and IV contrast material in contrast-enhanced CT colonography permits optimal examination of the solid organs for metastatic disease. Contrast-enhanced CT colonography thereby has the potential to be a single test that could display both mucosal and extramucosal local recurrence, metachronous polyps and cancers, and hepatic and peritoneal metastases. One potential problem with contrast-enhanced CT colonography in patients with prior colonic resections is increased reflux of air into the small bowel because the ileocecal valve has been removed and replaced with widely patent anastomoses in patients with right hemicolectomies. Luminal collapse can lead to false-negative examinations on CT colonography [16]. In a population of patients with a history of invasive colorectal carcinoma, the purpose of our study was to determine whether colonic anastomoses prohibited adequate colonic distention on contrast-enhanced CT colonography and to estimate the performance of contrast-enhanced CT colonography in detecting local recurrence and metachronous disease.
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Patients underwent a standard colonoscopic bowel preparation consisting of 4 L of polyethylene glycol solution and two 5-mg bisacody tablets. After the insertion of a rectal tube and the administration of 1-mg IV glucagon, the colon was inflated with carbon dioxide to patient tolerance. Adequate colonic distention was checked with a CT scout. Contrast-enhanced CT colonography was performed using 150 mL of Isovue-300 (Bracco Diagnostics, Princeton, NJ) IV contrast medium injected at a rate of 3-5 mL/sec, with images acquired after a 70-sec delay. Multidetector CT examinations were obtained using LightSpeed Plus and LightSpeed QX/i CT scanners (General Electric Medical Systems, Milwaukee, WI). The CT technique included the following parameters: a dose of 152 mAs, a slice thickness of 5 mm, and a reconstruction interval of 3 mm. Technologists could increase the dose for the supine examination, depending on patient body habitus. The examination was repeated with the patient in the prone position after the insufflation of additional air, using a dose of 40 mAs.
Colonic distention was recorded on a 4-point scale for each colonic segment (rectum, sigmoid, descending, transverse, and ascending colon/cecum) and for each supine or prone scan as follows: 0 = no distention (complete collapse), 1 = inadequate distention (partial collapse), 2 = submaximal but acceptable distention, and 3 = maximal distention. As we sought to ascertain whether distention allowed a confident review of the entire luminal surface, each colonic segment was graded by the most collapsed region in that segment. For example, if all of the sigmoid colon was distended on the supine images except for a collapsed rectosigmoid junction, the sigmoid distention was graded 0. An example of each grade of distention is given in Figure 1A,1B,1C,1D. After supine and prone scans were individually graded, the distention of each segment of the colon was compared between the supine and prone scans to assess the complementary inflation of different regions in the colon with dual positioning. The least distended region in each segment using dual positioning was then graded with the 4-point scale. In this manner, we were able to determine whether any portion of the colon was inadequately visualized with supine and prone positioning. The degree of distention was compared with the location of the segment containing the colonic anastomosis. Patients with a prior low anterior resection presented a problem with the classification of the colonic segment proximal to their anastomosis (as either sigmoid or descending colon) because various lengths of sigmoid colon were left in place following resection. The classification of this segment proximal to the anastomosis in these patients was left to the discretion of the interpreting radiologist.
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Two gastrointestinal radiologists with experience in CT colonography (each having interpreted over 300 examinations) individually analyzed volumetric CT datasets using a specialized computer workstation that displayed axial two-dimensional multiplanar reformatted and three-dimensional endoluminal images and allowed for comparison of supine and prone data sets. The radiologists were unaware of the results of all other examinations. Polyp presence, size, and location were recorded. Local recurrence was rated as present, absent, or indeterminate. Local recurrence was rated as present when the characteristic appearance of local recurrence on routine CT was present (i.e., an enhancing, predominately extracolonic mass or masses at or near the surgical anastomosis with or without adjacent adenopathy). We classified predominantly intraluminal abnormalities at the anastomosis as indeterminate for local recurrence. The liver, peritoneum, retroperitoneum, lung bases, and lymph nodes were evaluated for the presence of metastatic disease. The location of metastases was also recorded as present, absent, or indeterminate. Disagreements were resolved by consensus before any unblinding and comparison with gold standards.
The gold standard for metachronous adenomatous polyps and cancers was colonoscopy in 48 patients. Forty-five patients had the gold standard colonoscopy examination performed the same day, whereas two patients had colonoscopy within 4 days of the CT examination. One patient had a second colonoscopy performed within 3 weeks of the initial colonoscopy to reexamine suspicious colonoscopic findings at a surgical anastomosis. This examination was used as the gold standard in this patient. The second colonoscopy 3 weeks later serendipitously discovered a metachronous 4.0-cm tubulovillous adenoma in the cecum that had been overlooked. Two patients with rectosigmoid strictures precluding complete endoscopic assessment were excluded from the analysis of metachronous disease.
The gold standard for local recurrence was histologic evidence of recurrence (from colonoscopic or surgical biopsy, n = 1) or clinical progression of disease (n = 1). In cases in which contrast-enhanced CT colonography was indeterminate or positive and colonoscopy was negative, a follow-up CT and colonoscopy were performed in one year to ascertain the truth.
Metastases were considered to be present if there was histologic confirmation (n = 4) or if there was clinical progression of disease (n = 1). We did not follow patients without metastases because this study did not aim to estimate the accuracy of contrast-enhanced CT colonography in detecting metastases.
Estimates of sensitivity, specificity, and accuracy were calculated for each patient for local recurrence, metachronous polyps greater than or equal to 1 cm, and metachronous polyps between 0.5 and 0.9 cm. Examinations that were indeterminate for local recurrence on contrast-enhanced CT colonography but were negative according to the gold standard were counted as false-positive examinations in the statistical analysis. Three patients had multiple polyps between 0.5 and 0.9 cm, and a per polyp calculation was performed only for the estimate of sensitivity. Two patients had no gold standard assessment for metachronous polyp detection and were not included in the analyses for metachronous disease. The positive predictive value for metastases was calculated on a per patient basis, but sensitivity and specificity were not calculated because not all patients were followed over time. Our purpose did not include estimating the sensitivity for extracolonic metastases for this CT examination because true-negative examinations could not be ascertained with certainty. Exact 95% confidence intervals (CIs) were also calculated for the previously mentioned estimates.
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Figure 2 displays the percentage of patients with adequate colonic distention on supine, prone, and combined supine and prone scanning for each colonic segment. Most patients had adequate colonic inflation (i.e., grade 2 or 3 distention) throughout the entire colon (37/50, 74%). However, if the sigmoid colon had been excluded, nearly all patients (48/50) would have had adequate colonic distention with combined supine and prone scanning. Complete or partial sigmoid collapse accounted for 85% (11/13) of the cases with inadequate colonic distention. Interestingly, most of these patients (7/11, 64%) had right hemicolectomies with ileocolic anastomoses. Overall, one third of the patients with right hemicolectomies had a portion of the colon inadequately distended on supine and prone CT colonography (8/24). A minority of patients with inadequate sigmoid distention had a low anterior resection (3/11), and only 18% (3/17) of those patients with a low anterior resection had any colonic segment that was incompletely distended.
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The performance of contrast-enhanced CT colonography and colonoscopy in detecting different types of recurrent colorectal carcinoma is summarized in Table 1.
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Contrast-enhanced CT colonography detected both patients with local recurrences for a sensitivity of 100% (CI, 16-100%; Table 1). The specificity for local recurrence was 94% (45/48; CI, 92-100%). The overall accuracy of contrast-enhanced CT colonography for local recurrence was 94% (CI, 83-99%). One of the patients with local recurrence had an extracolonic local recurrence with local nodal metastases and soft tissue adjacent to the surgical clips near the anastomosis (Fig. 3A,3B,3C). The other patient had a stricture with friable mucosa at the anastomosis on colonoscopy, prompting a biopsy that showed recurrent adenocarcinoma (Fig. 4). This patient underwent abdominoperineal resection for recurrent rectal carcinoma. Although there were no false-positive examinations for recurrent carcinoma, contrast-enhanced CT colonography classified three patients as being indeterminate for local recurrence, and these indeterminate examinations were counted as false-positive examinations for statistical purposes. All of these patients were reexamined after one year with both contrast-enhanced CT colonography and colonoscopy, and in all cases, the anastomosis looked normal, and no local recurrence was found. All three patients had either intraluminal soft tissue or intramural soft-tissue thickening at the anastomosis on CT (Fig. 5A,5B). Colonoscopy revealed a benign ulcer in one patient, polypoid lymphoid hyperplasia and inflammation in the second, and inflammation and architectural distortion consistent with an anastomotic site in the third. Six additional patients without local recurrence had inflammation or other suspicious findings, prompting biopsy of their colonic anastomoses on colonoscopy, but contrast-enhanced CT colonography showed normal-appearing anastomoses in these patients. All cases of local recurrence and anastomotic inflammation were first detected using only axial images.
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There was only one metachronous lesion greater than or equal to 1 cm: a 4-cm tubulovillous adenoma in the cecum (Table 1). The initial colonoscopy failed to identify this lesion, which was seen on contrast-enhanced CT colonography as a large flat lesion along the lateral wall of the cecum (Fig. 6A,6B). The lesion was subsequently identified during a repeat colonoscopy 3 weeks later, and the patient has undergone photoablation and close interval surveillance. The overall accuracy for polyps greater than or equal to 1 cm was 92% (CI, 80-98%). The sensitivity and specificity for metachronous polyps greater than or equal to 1 cm were 100% (1/1; no CI) and 91% (43/47; CI, 80-98%), respectively. Contrast-enhanced CT colonography identified two of four polyps between 0.5 and 0.9 cm, for a sensitivity of 50% (CI, 7-93%). The specificity and accuracy for polyps of this size calculated on a per patient basis were 84% (38/45; CI, 71-94%) and 83% (CI, 70-93%), respectively. Both of the missed polyps in this category were in a single patient who had residual particulate stool throughout his colon.
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There were four false-positive contrast-enhanced CT colonographic examinations for metachronous adenomatous polyps greater than or equal to 1 cm. One examination revealed a 1.5-cm hyperplastic polyp. The colorectal surgeon performing the endoscopy in this patient stated that the hepatic flexure was examined several times before this polyp could be identified and removed. All of the other false-positive examinations incorrectly identified 1-cm polyps. Two lesions were due to adherent stool, whereas another was due to the appearance of a polyp at the ileocolic anastomosis (Fig. 7A,7B).
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There were two patients with incomplete colonoscopies who were excluded from our analysis. Contrast-enhanced CT colonography in both of these patients was of diagnostic quality and negative for metachronous disease.
Contrast-enhanced CT colonography identified five patients with metastatic disease, all of whom were subsequently confirmed to have distant recurrence (positive predictive value, 100%; CI, 48-100%; Table 1). Three of these patients had hepatic metastases, whereas two had nodal metastases and one had pulmonary metastasis. Potential curative resection was undertaken in three of these patients. Contrast-enhanced CT colonography identified another patient with diffuse colonic wall thickening, who was diagnosed with ischemic colitis on the basis of the clinical assessment and colonoscopic biopsy.
We used a blinded consensus reading to resolve disagreements between the interpreting radiologists. There was agreement on the presence or absence of local recurrence in 47 (94%) of 50 patients. The interpreting radiologists agreed on the presence or absence of polyps greater than or equal to 1 cm in 49 (98%) of 50 patients and on the presence or absence of polyps between 5 and 9 mm in 39 (78%) of 50 patients. There was agreement in 45 (90%) of 50 patients with distant metastatic disease.
There was no significant correlation between any form of recurrent
colorectal carcinoma and the stage of the initial invasive cancer at the time
of resection or at the time between resection and the contrast-enhanced CT
colonographic examination (
36 months vs > 36 months).
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Our study also showed, however, that when a prior colonic anastomosis is present, approximately one quarter of CT colonography patients will have inadequate colonic distention in at least one portion of the colon. Eighty-five percent of our cases of inadequate distention occurred in the region of the sigmoid colon, predominantly in patients with right hemicolectomies and probably as a result of decompression through a widely patent ileocolic anastomosis. Conversely, a smaller number of patients had incomplete colonic distention after low anterior resection in the juxtaposed region of the proximal sigmoid or descending colon, possibly due to a lack of compliance from surgical scarring or radiation. Idiosyncratic positioning or additional air insufflation may improve colonic distention in collapsed regions of the sigmoid colon. We consequently dismiss patients only after both supine and prone examinations have been reviewed by a radiologist.
Contrast-enhanced CT colonography has several advantages over alternative existing tests for recurrent colorectal cancer. Carcino-embryonic antigen is the most specific serum marker for recurrent colorectal cancer, but the serum marker can be normal in up to 41% of patients with recurrence and can be elevated as a result of a large number of comorbid conditions [20, 21]. Additionally, an elevated serum carcinoembryonic antigen only triggers the search for locally recurrent or metastatic disease. Colonoscopy can detect intraluminal local recurrence, but most local recurrences are not intraluminal and will be endoscopically obscure [22, 23]. Routine CT may detect hepatic and peritoneal metastases, but CT is not a reliable indicator of local recurrence except in patients with a prior abdominoperineal resection [20].
Unlike these other tests, contrast-enhanced CT colonography directly displays the anastomosis, the luminal surface, the colonic wall, and the pericolonic tissues. This technique therefore has the potential to detect mucosal, intramural, and extracolonic local recurrence. When all patients with recurrent colorectal cancer in our study population were considered, contrast-enhanced CT colonography was able to identify all patients with local recurrence, metachronous lesions greater than or equal to 1 cm, and distant metastases (Table 1). Colonoscopy was unable to identify one of two patients with local recurrence and initially missed a large metachronous tubulovillous adenoma. Finally, contrast-enhanced CT colonography identified five patients with metastases (three with liver metastases). Elevated serum carcinoembryonic antigen levels were not elevated in two of the four patients with metastatic disease, and a subsequent examination would not have been triggered in these patients.
The appearance of local recurrence on contrast-enhanced CT colonography in our study was an enhancing mass occurring at the colonic anastomosis or local pericolonic recurrence. Given the small number of patients with local recurrence, our estimate of sensitivity, consequently, has a wide CI. Further experience with this technique will likely be needed to characterize the full spectrum of radiographic findings in patients with local recurrence.
Contrast-enhanced CT colonography may be particularly helpful to clinicians when a stricture or inflammation is present near the anastomosis on colonoscopy, but the contrast-enhanced CT colonography examination appears normal. Harvey et al. [19] have previously shown that contrast-enhanced CT colonography can be highly accurate in differentiating benign from malignant colonic strictures. Nine patients without local recurrence underwent anastomotic biopsy for suspicious findings on colonoscopy, and contrast-enhanced CT colonography appeared normal in six of these patients. A negative contrast-enhanced CT colonography may help to decrease the suspicion for recurrence when biopsies are negative, despite equivocal colonoscopic findings. Conversely, however, colonoscopic correlation is necessary when an enhancing soft-tissue mass is present on CT at the anastomotic site because contrast-enhanced CT colonography cannot distinguish between local recurrence and inflammation when enhancing soft tissue is present (Fig. 5A,5B).
Contrast-enhanced CT colonography promises to have a high sensitivity for polyps of considerable size, but our study population suffered from a low incidence of metachronous disease. The risk of metachronous colorectal cancer ranges from 0.6% to 10% and is increased by the presence of synchronous neoplasia at the time an index cancer is diagnosed [24, 25]. The use of IV contrast material will likely aid in the detection of metachronous lesions [14]. Contrast-enhanced CT colonography can be a helpful adjunct to colonoscopists, as evidenced by the fact that a large 4-cm tubulovillous adenoma was initially missed at colonoscopy but seen on colonography, and contrast-enhanced CT colonography aided in the detection of a 1.5-cm hyperplastic polyp. Although we counted this polyp as a false-negative examination for the purpose of our study, there is increasing evidence that some rightsided hyperplastic polyps may be premalignant [26, 27].
Contrast-enhanced CT colonography may also complete the structural examination of the colon when incomplete colonoscopy occurs (i.e., two patients in our study). We have also found contrast-enhanced CT colonography to be a useful method in examining the patient with an anal or low rectosigmoid stricture, which precludes endoscopic evaluation, outside of our study protocol. Further study is warranted regarding the ability of contrast-enhanced CT to detect metachronous polyps.
There are some drawbacks to contrast-enhanced CT colonography as a method for detecting metachronous disease in patients with a history of invasive colorectal cancer. The technique is limited by residual stool and currently suboptimally detects subcentimeter adenomatous polyps, particularly if stool is present. Interpreting radiologists disagreed on the presence of medium-sized polyps in 22% of patients and erroneously interpreted two examinations as positive for metachronous lesions (1 cm) because of retained stool. Additionally, polypoidshaped granulation tissue may also be present at colonic anastomoses and is not distinguishable from metachronous disease or local recurrence. For these reasons, we do not believe contrast-enhanced colonography is currently a sufficient means for evaluating metachronous disease when endoscopy can be performed in the absence of additional data. Further study is warranted, however, because additional images to inflate collapsed colonic segments and smaller collimation and reconstruction intervals afforded by multidetector CT scanners may improve detection and characterization of subcentimeter lesions and may also better discriminate them from adjacent stool.
We did not attempt to characterize the performance of contrast-enhanced CT colonography in detecting distant metastases but note that the technique had a positve predictive value of 100% for metastatic disease and identified five patients with metastases. As a technique for detecting small hepatic metastases, however, small collimation and reconstruction intervals, similar to those used in contrast-enhanced CT colonography, aid in the characterization of small hepatic lesions [28]. In this regard, contrast-enhanced CT colonography may detect small hepatic or pulmonary metastases while curative resection is still possible.
In conclusion, our study shows that contrast-enhanced CT colonography is a feasible method for detecting many types of recurrent colorectal cancer, including local recurrence, metachronous disease, and distant metastases. Contrast-enhanced CT colonography was the only screening test in our population to identify all patients with any type of recurrent disease (Table 1). No extra patient preparation is required if the patient is undergoing CT and colonoscopy for suspected recurrent disease, but the patient will need to be scheduled for contrast-enhanced CT colonography before colonoscopy. A radiologist should review the examination before the patient is dismissed to ensure that all regions of the colon can be evaluated. Contrast-enhanced CT colonography may be an inadequate test by itself to evaluate for the presence of metachronous disease, given potential suboptimal distention in patients with right hemicolectomies, retained stool and granulation tissue, or inflammation at anastomoses. However, contrast-enhanced CT colonography can improve the performance of colonoscopy alone in identifying local recurrence that is occult to colonoscopy (i.e., extracolonic) and metachronous disease that is endoscopically obscure. Contrast-enhanced CT colonography provides more information than the combination of routine surveillance CT (i.e., obtained without colonic distention or preparation) and colonoscopy by identifying metachronous disease, serving as a full structural examination in cases of incomplete colonoscopy, and showing colonic anastomoses in cases of stricture or inflammation on colonoscopy. Further studies examining the ability of contrast-enhanced CT colonography in larger populations are needed. If continuing technical developments improve contrast-enhanced CT colonography sufficiently, it could become the first-line test in patients with suspected recurrent colorectal cancer. Colonoscopy would then serve as an adjunct to contrast-enhanced colonography, being used for polypectomy and the biopsy of suspicious lesions.
Acknowledgments
We thank the Fraternal Order of the Eagles and the Mayo Foundation for
their financial support of this work. We also thank Jeanie Bard for her
efforts in assembling the manuscript.
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