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Gastrointestinal Imaging |
1 From the Department of Clinical Sciences and Bioimages, Section of Radiology (A.F., R.A., M.F., T.M., L.B.), and Department of Radiation Oncology (D.G.), SS Annunziata Hospital, G. D’Annunzio University, Via dei Vestini, 66013 Chieti, Italy. Received September 12, 2002; revision requested December 2; final revision received July 17, 2003; accepted August 6. Supported in part by a grant from CNR-MIUR. Address correspondence to A.F. (e-mail: a.filippone@rad.umich.it).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Forty-one patients with colorectal carcinoma underwent preoperative contrast-enhanced multi–detector row CT colonography. Images were obtained in the arterial (start delay of 35 seconds) and portal venous (start delay of 70 seconds) phases. The arterial phase was focused on the suspected region of neoplasm, whereas the venous phase included the whole abdomen and pelvis. Two radiologists independently evaluated the depth of tumor invasion into the colorectal wall (T) and regional lymph node involvement (N) on transverse CT images alone and in combination with multiplanar reformations (MPRs). Disagreements were resolved by means of consensus. CT findings were compared with pathologic results, which served as the reference standard. Sensitivity, specificity, accuracy, positive predictive value, and negative predictive value were assessed. Differences in accuracy for T and N staging were assessed by using the McNemar test.
RESULTS: In T staging, overall accuracy was 73% when transverse images were evaluated alone and 83% when they were evaluated in combination with MPRs. This difference was not significant. N staging was associated with an overall accuracy of 59% with transverse images alone and 80% with combined transverse and MPR images (P < .01).
CONCLUSION: Contrast-enhanced multi–detector row CT colonography is an accurate technique for preoperative local staging of colorectal tumors.
© RSNA, 2004
Index terms: Colon neoplasms, CT, 758.12112, 758.12114 • Colon neoplasms, staging
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The use of intravenously administered contrast material to enhance the bowel wall during CT is a relatively recent development in gastrointestinal imaging. To our knowledge, Amin et al (10,11) were the first to describe the use of intravenously administered contrast material during dynamic helical CT of an air-insufflated colon in the detection and staging of colorectal cancer.
Contrast material–enhanced CT colonography has the potential advantage of providing images of the bowel wall, extracolonic tissues, and liver in one setting (12,13). While this benefit may have limited relevance in a screening population, it may substantially improve the use of CT colonography to stage colorectal cancers by helping us assess the depth of involvement of a possible neoplasm; to identify pericolic spread, including lymph nodes; and to detect colorectal liver metastases.
In an effort to further improve the diagnostic accuracy of CT colonography, we evaluated the accuracy of dual phase contrast-enhanced multi–detector row CT colonography for preoperative staging of colorectal cancer.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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2 test) did not show a statistically significant difference in age distribution according to patient sex. Pathologic findings for depth of tumor invasion and nodal involvement served as the reference standard. The standard of reference for liver, peritoneum, and retroperitoneum metastases was histolopathologic examination, intraoperative hepatic US, or surface exploration results.
T and N staging was based on the international TNM classification (14), as follows: pT1, tumor invading submucosal layer; pT2, tumor invading muscularis propria or subserosa; pT3, tumor penetrating serosa and perivisceral fat; and pT4, tumor invading adjacent organs. Lymph nodes were likewise classified: N0, no regional lymph node metastasis; N1, metastasis in one to three perirectal lymph nodes; N2, metastasis in four or more perirectal lymph nodes; and N3, metastasis in pelvic lymph nodes.
CT Protocol
A Somatom Plus Volume Zoom CT scanner (Siemens, Forchheim, Germany) was used for this study. Each patient received orally administered colon-cleaning preparation (polyethylene glycol solution, Isocolan; Bracco, Milan, Italy) 12 hours prior to CT examination and ingested 500 mL of water orally shortly before scanning.
All patients were placed in the prone position on the CT table, and a 12-F balloon-tipped rectal tube was inserted. After intravenous injection of 1 mL of a spasmolytic agent (Joscine-N-Butilbromure; Boehringer Ingelheim, Berkshire, England), room air was gently insufflated into the colon by the same experienced radiologist to patient tolerance. A standard CT scout image was obtained to assess the degree of colonic distention, which was considered acceptable when all colonic segments, including cecum, ascending colon, transverse colon, descending colon, sigmoid colon, and rectum, were visualized and well distended. When necessary, further insufflation was performed to maximum patient tolerance before data acquisition.
Contrast-enhanced multi–detector row CT colonography scans were obtained with the patient in the prone position after intravenous injection of 130 mL of iodinated contrast agent (Iomeron 400; Bracco) was administered at 3 mL/sec. CT acquisitions were performed in the arterial phase (start delay of 35 seconds) and in the portal venous phase (start delay of 70 seconds) by using the following protocol: collimation of 4 x 2.5 mm, rotation speed of 0.5 second, table feed of 12.5 mm per rotation, section width of 3 mm for the arterial phase and 5 mm for the venous phase, reconstruction increment of 1 mm for the arterial phase and 3 mm for the venous phase, field of view to fit, 180 mAs, and 120 kVp. At the time of CT scanning, the investigator knew the anatomic location of the carcinoma, which was necessary to restrict the arterial phase acquisition to the suspected region of the neoplasm.
The venous phase CT examination included the whole abdomen and pelvis, from the diaphragmatic dome to the anal verge. All CT data were transferred to a workstation (Volume Wizard; Siemens) for evaluation.
Image Analysis
Two abdominal radiologists (A.F., R.A.), who had at least 6 years of experience in abdominal CT and who were partially blinded to the endoscopic results and completely blinded to lesion size, macroscopic features, and stage of colorectal cancers, independently evaluated CT images on the workstation by using soft-tissue window settings. Differences in assessment were resolved by means of consensus.
Arterial phase contrast-enhanced transverse CT images were initially assessed separately, followed by a second review combining both arterial phase contrast-enhanced transverse images and multiplanar reformations (MPRs). Presence, site, and type (stricturing or not) of neoplasm were assessed, in addition to the depth of tumor invasion (T staging) and regional lymph node involvement (N staging). We did not use a three-dimensional endoluminal view; we used only transverse CT images combined with two-dimensional MPR images.
The assessment of extracolonic compartment metastases of the abdomen and pelvis was performed on 5-mm venous phase contrast-enhanced transverse images. Metastases were recorded as present, absent, or indeterminate. When the interpreting radiologists judged a metastasis as indeterminate, they reconstructed venous phase transverse images with a section width of 3 mm to enable them to record a definite opinion. Bowel wall thickening of more than 0.5 cm was considered to indicate the presence of a neoplasm.
Colorectal wall invasion was analyzed according to a modified T classification (Fig 1). In CT image analysis, the readers considered only three T stages (
T2, T3, or T4), instead of the normal four T stages as reported in the TNM system. T1 and T2 tumors were combined to represent one T stage, T2. This classification was used to address known limitations at CT in distinguishing T1 and T2 lesions.
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1 cm in long axis) was considered to be stage N3.
Statistical Analysis
Sensitivity, specificity, accuracy, positive predictive value, and negative predictive value were calculated for transverse images alone and in combination with MPRs for T and N staging.
Differences in accuracy for T and N staging were assessed by using the McNemar test. Statistical significance was inferred at a confidence level of 5%.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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With CT, tumors were located correctly in the rectum in 26 patients, in the sigmoid colon in eight, in the descending colon in three, and in the ascending colon in four.
Although there were 30 of 41 (73%) stricturing tumors, conventional colonoscopy enabled exploration of the entire colon lumen up to the hepatic flexure in 39 of 41 (95%) patients. In the remaining two patients, conventional colonoscopy failed to reach the right colon, owing to patient intolerance.
T Staging
At histopathologic examination, three of 41 (7%) neoplasms were staged as pT1, 10 of 41 (24%) as pT2, 25 of 41 (61%) as pT3, and three of 41 (7%) as pT4.
The overall accuracy of contrast-enhanced multi–detector row CT colonography was 73% (30 of 41 patients) when transverse images were evaluated alone. Overall accuracy improved to 83% (34 of 41 patients) when transverse and MPR images were evaluated in combination (Fig 4). However, these differences were not statistically significant. Over- and understaging by using transverse images occurred in nine of 41 (22%) patients and two of 41 (5%) patients, respectively. With transverse images and MPRs combined, over- and understaging occurred in five of 41 (12%) patients and two of 41 (5%) patients, respectively.
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Accuracy for each T stage by using transverse and combined transverse and MPR images, respectively, was as follows: T2, 90% and 93%; T3, 85% and 90%; and T4, 80% and 98% (Table 1).
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The overall accuracy of the assessment of lymph node involvement on contrast-enhanced multi–detector row CT colonographic images was 59% (24 of 41 patients). Over- and understaging occurred in 12 of 41 (29%) patients and five of 41 (12%) patients, respectively.
The overall accuracy of the assessment of lymph nodes on transverse images in combination with MPRs was 80% (33 of 41 patients). Over- and understaging occurred in five of 41 (12%) patients (Fig 5) and three of 41 (7%) patients, respectively. The difference between transverse images plus MPRs and transverse images alone was statistically significant (P < .01). Nodal metastases were detected in 16 of 20 (80%) patients by using transverse images alone and in 18 of 20 (90%) patients by using transverse images combined with MPRs.
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Contrast-enhanced multi–detector row CT colonography showed a peritoneal metastasis located within mesenteric fat (2 cm in size) in one patient with stage T3 sigmoid colon cancer. This finding was confirmed at surgery.
Interobserver Agreement
We used blinded consensus reading to resolve disagreements between interpreting radiologists. In the overall assessment of T staging, there was agreement in 38 of 41 (93%) patients when evaluating transverse images alone and in 40 of 41 (98%) patients when evaluating combined transverse and MPR images. In the assessment of lymph node involvement, there was agreement in 37 of 41 (90%) patients when transverse images were evaluated alone and in 39 of 41 (97%) patients when transverse and MPR images were used in combination. When considering extracolonic metastases, the readers showed agreement in all patients except one, who had peritoneal metastasis.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Most authors agree that laparoscopy-assisted colectomy should be performed in patients who have colorectal cancer with mucosal (T1) or submucosal (T2) invasion (17), while it is preferable to treat more advanced cancers with open surgery. Moreover, it has been suggested that the extent of laparoscopic lymph node dissection can be modified according to tumor stage (18).
As shown for colonic neoplasm, accurate staging of rectal cancer is necessary to indicate the most appropriate management. An early small rectal cancer confined to submucosa (T1 stage) can be excised locally, whereas preoperative chemotherapy and radiation therapy can be recommended for advanced rectal cancer for downstaging. Compared with surgery alone, preoperative neoadjuvant therapy plus surgery for advanced rectal cancer (T3, T4) results in better survival rates, better local control, and comparable or better toxicity compared with standard postoperative adjuvant regimens (19–21). Accurate staging is therefore crucial in the selection of patients for trials on the evaluation of neoadjuvant treatment. In our patient population, there was an increased prevalence of rectosigmoid neoplasms owing to the presence of a surgeon with extensive experience in rectal disease at our hospital.
Furthermore, an accurate evaluation of liver, peritoneum, and retroperitoneum is recommended to identify metastases while curative resection is still possible. Patients with colorectal cancer and liver metastases may be treated with colorectal surgery and intraoperative radiofrequency ablation of liver lesions.
To select the optimal treatment modality, accurate preoperative staging is necessary, which will benefit patients with colorectal cancer in terms of cure and quality of life. Therefore, the main purpose of this study was to evaluate the overall diagnostic accuracy of contrast-enhanced multi–detector row CT colonography in staging of colorectal neoplasms to help choose the optimal treatment modality for each case.
The CT colonography protocol we used represents the technique currently used at some centers performing CT colonography (13,22,23). We preferred to use only transverse and MPR images without acquiring endoluminal views. For staging purposes, the endoluminal views are of little value, and cross-sectional techniques that demonstrate the extraluminal depth of invasion through the bowel walls are really the crux of the assessment. In CT colonography, the combined use of supine and prone positions is useful for detection of polyps, and, since the main aim was to stage an already known tumor, we preferred to use only the prone position, which improves colorectal distention (24).
CT colonography is most likely used for colorectal cancer screening (22). Our results showed that an important benefit inherent in CT colonography is the ability to be not only a screening tool but also a tool to differentiate early colorectal carcinoma (T2) and advanced cancer (T3, T4).
T Staging
In our study, the accuracy rate for the depth of tumor invasion obtained with contrast-enhanced multi–detector row transverse CT images alone (73%) was comparable to that in other studies in which single–detector row helical CT was used (4,10–12). However, the rate in our study was superior to that in reports in which conventional CT was used (25–35). A possible explanation for the better performance of helical CT is that the shorter examination time at helical CT results in optimal enhancement of neoplastic tissue following intravenous contrast material administration. Morrin et al (12) found that the use of intravenously administered contrast material during CT colonography proved useful in the assessment of patients suspected of having extensive colorectal cancer; it permitted identification of invasion of pericolic fat planes and adjacent organs with an overall accuracy (81%) similar to that in our study.
The utility of the contrast-enhanced arterial phase acquisition for tumor detection has been demonstrated by Hundt et al (4), who reported a sensitivity of 97.2% during the arterial phase and 81.6% during the venous phase. In their series of 37 patients who underwent helical CT for colon neoplasms, arterial phase imaging allowed better differentiation between the tumor and the adjacent organs and tissues, whereas contrast enhancement during the venous phase resulted in a more homogeneous enhancement of the neoplasm and the adjacent normal tissue. In the same way, in the staging of local extension of colorectal tumors, Hundt et al (4) achieved an accuracy rate of 81.0% for the arterial phase and 64.8% for the venous phase.
Contrast-enhanced multi–detector row CT colonography provides the additional capability of using thin collimation (4 x 2.5 mm) during the arterial phase of contrast enhancement. Thin collimation results in improved quality of MPRs and better spatial resolution. Despite thin sections, however, an intrinsic limitation of CT is the lack of visualization of the individual wall layers. As a result, it is not possible to differentiate T1 tumors from T2 tumors. In our series, three colorectal cancers staged as pT1 at histopathologic examination were evaluated at contrast-enhanced multi–detector row CT colonography as T2 tumor (one of three) and T4 tumor (two of three) on transverse images alone and as T2 tumor (three of three) on transverse images in combination with MPRs.
Although T1 tumors may benefit from limited surgical resection and transanal endoscopic microsurgery, the clinical value of such a conservative approach is limited by the impossibility of performing a complete intraoperative staging of nodal sites (36). For this reason, differentiation between T1 and T2 tumors may be of little clinical consequence in the care of patients with rectal cancer.
By using combined transverse and MPR images, good preoperative prediction of stage T2, T3, and T4 lesions is possible. In differentiating T2 from T3 tumors, the crucial criterion is infiltration of pericolonic fat. We based the CT diagnosis of T3 lesions on the presence of tumor extending into the perirectal fat with a broad-based bulging configuration, as described by Brown et al (15) for MR imaging. The presence of spiculation within the fat may be caused by fibrosis alone, and use of this CT criterion to stage T3 tumors may lead to a high rate of overstaging (34). In a previous study (37), two-thirds of transrectal US staging errors were due to overstaging of T2 tumors, mainly as a result of extramural fibrosis and inflammatory reaction at the advancing edge of the tumor. It is important to remember that an inflammatory reaction at the expanding tumor margin occurs in about 25% of rectal cancers (38). In our series, the CT criterion of nodular advancing margin allowed us to correctly identify 22 of 25 (88%) pT3 colorectal cancers, with one false-positive case and two false-negative cases. In this way, we obtained good specificity (94%) without a relevant reduction of the sensitivity rate (88%) for prediction of stage T3 tumors (Table 1). The only tumor erroneously staged as T3 was determined to be pT2 at histopathologic examination, whereas the false-negative cases were represented as neoplasms staged as pT2 at contrast-enhanced CT colonography. The two latter tumors proved to be borderline T3-T2 tumors at histopathologic examination. As noted by other authors, differentiation between minimal T3 tumor infiltration and T2 tumors is probably of relatively little consequence for patient treatment, because patients with minimal T3 infiltration into perivisceral fat are at low risk of surgical failure from circumferential excision margin involvement (39,40).
In the differentiation of T3 and T4 tumors, the crucial criterion is infiltration of adjacent viscera. The CT criterion for T4 stage was the obliteration of fat planes between tumor and adjacent organs. Transverse images combined with MPRs were superior to the use of transverse images alone in the staging of T4 tumors (Table 1). Improvement in accuracy was mainly due to a reduction in overstaging. The use of MPRs allowed the reader to identify a thin fat plane between tumor and adjacent organs, regardless of the optimal imaging plane.
N Staging
In the present study, readers were more sensitive and specific when using combined transverse and MPR images than transverse images alone for N staging. A more accurate measurement of lymph node diameter and better differentiation between lymph nodes and small perirectal vessels was possible with the use of MPRs.
Our results showed good correlation between pathologic and CT findings in N staging, with an overall accuracy and sensitivity rate superior to that in previous reports (28,30–35). This difference is likely due to the added MPR images and to the CT criteria used.
The CT criteria included not only nodal size (a regional node 1 cm in diameter) but also the number of lymph nodes, regardless of their size. If a whole node is replaced by tumor and the node is enlarged secondary to it, detection is more likely. If only a small deposit or a micrometastasis is present, however, the characteristics of the node are unlikely to be sufficiently altered to allow detection.
On the basis of studies in which up to 20% of patients have involved nodes smaller than 3 mm (41,42), some authors (28) recommend consideration of any visualized regional lymph node. The use of size criteria alone would improve specificity but reduce sensitivity.
In our opinion, high sensitivity is more important than specificity, since understaging of lymph node involvement is dangerous to patients with colorectal cancer because it can lead to undertreatment. Our results showed an overall sensitivity of 90% with 77% specificity.
Contrast-enhanced CT colonography showed acceptable values of accuracy for local staging of colorectal cancer and has several advantages over alternative existing tests. A number of investigators have reported the usefulness of endoscopy with US for staging of colorectal cancer (28,43–45); however, it has several disadvantages, including the high cost of equipment, limited maneuverability, and the failure of the endoscope to traverse tight stenoses and reach the cecum. Transrectal US and MR imaging with an endorectal coil have superior accuracy to that of multi–detector row CT colonography; unfortunately, both techniques are limited by the inability to examine the bulky stricturing or high rectal tumors that occur in approximately 20% of cases (46,47).
Brown et al (15) demonstrated excellent preoperative prediction of local stage of rectal carcinoma by using a thin-section MR technique and body phased-array coil. With respect to MR imaging, multi–detector row CT colonography has the potential to be a faster single test for staging of local, liver, and peritoneal extension of rectal cancer.
Extracolonic Compartment Metastases
Early detection of liver, peritoneal cavity, and retroperitoneal metastases, especially before surgery, is extremely important for patient survival because it enables planning of a combined treatment of primary and secondary disease.
Although assessment of the accuracy of contrast-enhanced multi–detector row CT colonography in the detection of distant metastases was not the primary goal of our study, we were able to correctly identify six of seven hepatic lesions and the only peritoneal metastasis.
As shown in the literature, contrast-enhanced MR imaging with ferumoxides or gadolinium chelates provides excellent results in the preoperative staging of hepatic metastases (48,49). However, MR imaging is more expensive than CT and is not as widely available. Furthermore, a recent study (50) showed that the use of 5-mm venous phase contrast-enhanced helical CT scans as the only preoperative imaging technique in the assessment of colorectal cancer metastases allowed accurate preoperative staging (sensitivity, 85.1%; positive predictive value, 96.1%). In addition, 112 (94.1%) of the 119 patients who were considered to be candidates for surgical treatment underwent successful curative resection. On the basis of these results, the authors recommended helical CT as the routine preoperative imaging technique in patients who are candidates for hepatic resection because of the noninvasive nature of the examination, its wide availability, and its ability to depict extrahepatic disease.
Our CT scanning protocol, including a dual phase study of the abdomen with the arterial phase focused on the colorectal cancer and the portal venous phase extended to the entire abdomen, allowed us to optimize the local staging of colorectal cancer and the detection of extracolonic compartment metastases of the abdomen and pelvis.
In conclusion, contrast-enhanced multi– detector row CT colonography enables accurate preoperative assessment of T, N, and abdominal M staging in patients with colorectal cancer.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, L.B.; study concepts, A.F., R.A., D.G.; study design, A.F., R.A.; literature research, M.F., T.M.; clinical studies, A.F., D.G.; experimental studies, R.A., M.F.; data acquisition, R.A., M.F., T.M.; data analysis/interpretation, A.F., R.A.; statistical analysis, A.F.; manuscript preparation, A.F., R.A.; manuscript definition of intellectual content, A.F.; manuscript editing, T.M., M.F.; manuscript revision/review, A.F., L.B.; manuscript final version approval, L.B.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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