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Published online before print May 29, 2003, 10.1148/radiol.2281020950
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(Radiology 2003;228:152-156.)
© RSNA, 2003

Gastrointestinal Imaging

Colorectal Neoplasms: Role of Intravenous Contrast-enhanced CT Colonography1

Jacob Sosna, MD, Martina M. Morrin, FFRRCSI, FCRR, Jonathan B. Kruskal, MD, PhD, Richard J. Farrell, MD, MRCPI, Imad Nasser, MD and Vassilios Raptopoulos, MD

1 From the Departments of Radiology (J.S., M.M.M., J.B.K., V.R.), Gastroenterology (R.J.F.), and Pathology (I.N.), Beth Israel Deaconess Medical Center, Harvard Medical School, 330 Brookline Ave, Boston, MA 02215. Received August 1, 2002; revision requested September 23; revision received September 27; accepted November 22. Address correspondence to J.S. (e-mail: jsosna@caregroup.harvard.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate whether computed tomographic (CT) colonography with intravenously administered contrast material can help predict malignant differentiation of colorectal neoplasms (≥10 mm in diameter).

MATERIALS AND METHODS: Enhancement of 29 consecutive colorectal neoplasms on pre- and postcontrast CT colonographic images was retrospectively measured. The neoplasms were subsequently resected. Enhancement was calculated by subtraction of attenuation values (in Hounsfield units) obtained with precontrast and postcontrast 45-second-delay prone CT colonographic sequences. The neoplasms were graded as follows: grade 1, adenoma; grade 2, adenoma with high-grade dysplasia; grade 3, well-differentiated adenocarcinoma; grade 4, moderately differentiated adenocarcinoma; and grade 5, poorly differentiated adenocarcinoma. Correlation among size, histologic grade, and degree of enhancement was made with Pearson and Spearman coefficients. The ability of the degree of enhancement to help predict adenocarcinoma (histologic grade, ≥3) was calculated.

RESULTS: Histologic–CT colonographic correlation was performed in 29 neoplasms (mean diameter, 27.9 mm; range, 10–65 mm). There was no correlation between size and degree of enhancement, size and histologic grade (R = -0.17, P = .33), or histologic grade and degree of enhancement (R = 0.23, P = .23). However, increasing enhancement was noted between grades 2 and 5. When an enhancement threshold of 40 HU was used for the diagnosis of adenocarcinoma (grades 3–5), sensitivity was 92%, specificity was 20%, positive predictive value was 50%, and negative predictive value was 75%.

CONCLUSION: The degree of contrast enhancement on a 45-second-delay CT colonographic image does not correlate with size or degree of histologic differentiation, although increasing enhancement with lesser degrees of differentiation was noted.

© RSNA, 2003

Index terms: Colon, CT, 75.12112, 75.12114, 75.12115, 75.1282 • Colon neoplasms, 75.311, 75.321 • Colon neoplasms, CT, 75.12111, 75.12115, 75.1282 • Colonoscopy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Colorectal cancer is the second leading cause of cancer mortality in the United States. Most carcinomas arise from preexisting adenomas (1). Conventional endoscopic colonoscopy is currently the modality of choice for colorectal cancer screening (2). Since its first description in 1994 (3), several study findings have demonstrated a promising role of computed tomographic (CT) colonography as a minimally invasive test for detection of colorectal cancers and polyps. Various investigators have reported sensitivity between 85% and 100% in the detection of polyps larger than 10 mm in diameter and between 66% and 91% for polyps 6–9 mm in diameter (4–12). Conversely, other investigators (13–15) have reported sensitivities of 66% for polyps 10 mm or larger and 36% for polyps 6–9 mm in diameter.

Technical factors that may limit the ability of CT colonography to depict polyps include poor colonic distention and inadequate bowel preparation (16), where residual fluid may obscure a submerged polyp or adherent stool may mimic a polyp or a mass. The use of intravenously administered contrast material can significantly improve conspicuity of the colonic wall and detection of medium-sized colorectal polyps (17).

We hypothesized that the degree of polyp enhancement will inversely correlate with the differentiation. Thus, the purpose of our study was to evaluate whether intravenous contrast material–enhanced CT colonography can help predict malignant differentiation of colorectal neoplasms 10 mm or larger in diameter.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
The study protocol was approved by our institutional review board, and informed consent was obtained from the patients. A retrospective evaluation was performed of all CT colonographic studies performed between November 1997 and March 2002. During that period, 642 patients underwent CT colonography at our institution, 321 (50%) of whom had received intravenously administered contrast material. Polyps were detected in 110 (34%) of 321 patients, 58 of whom had lesions 10 mm or larger in diameter. Twenty-four patients were excluded because of nonavailability of histologic correlation at our institution (n = 15), nonavailability of CT colonographic studies (n = 6), and diagnosis of benign lesions (lipomas) that were not resected (n = 3). Radiologic-histologic correlation was available for 35 lesions in 34 of the 58 patients. Six masses in six patients were resected but were noncancerous and were therefore not included in our study. The masses were an inverted appendiceal stump; a prolapsed mucosa; and four inflammatory masses, two from diverticulitis and two from Crohn disease of the colon. In 28 patients (14 women, 14 men; age range, 28–84 years; mean age, 62.5 years), 29 lesions were assigned a specific histologic grade. These patients constitute the case material for this study. All 29 lesions were removed either at colonoscopy (n = 15, 52%) or at subsequent laparotomy (n = 14, 48%) performed within a month of CT colonography.

CT Colonographic Technique
All patients underwent standard bowel preparation 24–48 hours prior to colonoscopy with either a standard barium enema preparation (Fleet Prep Kit 1; Fleet Pharmaceutical, Lynchburg, Va) or a balanced polyethylene glycol solution (GoLYTELY; Braintree Laboratories, Braintree, Mass). Patients undergoing elective colonoscopy or surgery for known colorectal cancers underwent CT colonography prior to conventional colonoscopy or laparotomy, respectively. Patients were placed on the CT table in the right lateral decubitus position. A 12-F balloon-tipped rectal tube was inserted, and room air was gently insufflated into the colon according to patient tolerance. A standard CT scout scan was obtained with the patient in the supine position to assess the degree of colonic distention. All patients were first scanned in the supine position and then turned to the prone position for further scanning. We used a single breath-hold acquisition to obtain images of the entire colon. Prone images were acquired following intravenous administration of 150 mL of ioversol (Optiray 320; Mallinckrodt, St Louis, Mo) at a rate of 3 mL/sec after a delay of 45 seconds.

CT examinations were performed by using a HiSpeed (GE Medical Systems, Milwaukee, Wis) (six scans), a LightSpeed QX/I (GE Medical Systems) (21 scans), or a Somatom Plus 4 (Siemens Medical Systems, Iselin, NJ) (one scan) helical CT scanner. The scanning parameters were 3-mm collimation, 6 mm/sec (pitch of 2) table speed, 120 mA, 120 kVp, and 512 x 512 matrix. Transverse images were reconstructed at 1.5-mm intervals with a 1.5-mm section overlap. The following parameters were used for scans obtained with the multisection LightSpeed scanner: 2.5–5.0-mm section thickness, 11.25–15.0-mm table speed per rotation with a high-speed mode, 1.25–2.5-mm image spacing, 100–200 mA, 120 kVp, and an average scanning time of 22 to 30 seconds.

Acquired CT data were transferred to a workstation (Advantage Windows, version 3.1; GE Medical Systems) equipped with navigator software, which permits the radiologist to obtain multiplanar reformations of the air-distended colon, as well as an endoluminal perspective through the distended colonic lumen. As routinely performed, magnified transverse images were viewed in rapid cine sequence and in three-dimensional projection. Surface-shaded endoluminal images were generated in areas of the bowel that could not be confidently evaluated with magnified transverse sequences alone.

Data Collection
Magnified transverse images were evaluated by two abdominal radiologists (J.S., M.M.M) experienced (2 and 6 years of experience, respectively) in CT colonography; all differences in assessment were resolved with consensus. Images were viewed with colonoscopy-adjusted window settings (window level, 80 HU; window width, 4,000 HU), as well as with abdominal window settings (window level, 40 HU; window width, 400 HU). Unenhanced supine images were compared with the corresponding enhanced prone images. Enhancement values for each lesion were measured by calculating the mean of three attenuation values (in Hounsfield units) of at least a 1-cm2 (range, 1.0–2.6 cm2) region of interest obtained before and after contrast enhancement. The net change was then calculated as the enhancement. Lesion size was measured by using electronic calipers according to their maximal diameter on the source transverse images, and the lesion location was recorded.

Histologic Grading
For the purpose of this study, each colorectal lesion was assigned one of five histologic grades based on the interpretation by a pathologist who was unaware of the CT findings or the degree of enhancement. The following grading scale was used: grade 1, adenoma; grade 2, adenoma with evidence of high-grade dysplasia; grade 3, well-differentiated adenocarcinoma; grade 4, moderately differentiated adenocarcinoma; and grade 5, poorly differentiated adenocarcinoma.

Statistical Analysis
The statistical analysis was performed by our institutional statistical service. Correlation between the degree of polyp enhancement and size and between the degree of enhancement and the histologic grade was made by using Pearson and Spearman correlation coefficients, respectively. We also analyzed the correlation between the size and the histologic grade. The sensitivity, specificity, and positive and negative predictive values for the identification of adenocarcinoma (histologic grade ≥3) were calculated for enhancement thresholds of 40, 50, and 60 HU.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
The mean diameter of the neoplasms was 27.9 mm (range, 10–65 mm). The regional distribution of the masses was as follows: rectum (n = 4), sigmoid colon (n = 10), descending colon (n = 3), hepatic flexure (n = 1), ascending colon (n = 6), and cecum (n = 5). Table 1 demonstrates the detailed findings in each case; enhancement values after contrast material administration ranged from 7 to 210 HU, with a mean of 63 HU (Figure). Adenoma (grade 1) constituted the largest group (n = 12), and moderately differentiated adenocarcinoma (grade 4) constituted the next largest group (n = 9). One case with a single lesion with an absolute enhancement value of 210 HU was excluded from statistical analysis since this outlier was beyond 3 SDs greater than the second highest level of 103 HU and would skew the results.


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  		TABLE 1. Data on Size, Histologic Grade, and Enhancement Value of Colorectal Lesions

 


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  		Figure a. CT colonographic scans obtained in an 84-year-old woman with cirrhosis and rectal bleeding. (a) Nonenhanced transverse scan obtained with the patient in the supine position shows a 2.5-cm pedunculated mass (arrow) in the ascending colon. (b) Contrast-enhanced scan with the patient in the prone position shows that the mass (arrow) enhanced by 99.7 HU. At surgery, a moderately differentiated adenocarcinoma was found and excised.

 


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  		Figure b. CT colonographic scans obtained in an 84-year-old woman with cirrhosis and rectal bleeding. (a) Nonenhanced transverse scan obtained with the patient in the supine position shows a 2.5-cm pedunculated mass (arrow) in the ascending colon. (b) Contrast-enhanced scan with the patient in the prone position shows that the mass (arrow) enhanced by 99.7 HU. At surgery, a moderately differentiated adenocarcinoma was found and excised.

 
The size distribution varied, with the largest number of lesions (n = 8) being 10–14 mm in diameter, while seven masses were 5 cm or larger. There was no significant correlation between the size and enhancement (Pearson correlation coefficient, R = -0.17; P = .33). There was also no correlation between the size of the lesion and the histologic grading. The enhancement values of polyps were compared with their histologic grade (Table 2). The Spearman correlation coefficient between histologic differentiation, grade, and enhancement was 0.23 (P = .23). An increasing enhancement was noted between grades 2 and 5 (enhancement values of 45 and 85 HU, respectively), but it did not reach statistical significance.


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  		TABLE 2. Mean Enhancement Values of Colorectal Masses with Respect to Histologic Grade

 
Different thresholds of enhancement were selected for the examination of sensitivity, specificity, positive predictive value, and negative predictive value for the diagnosis of adenocarcinoma (grades 3–5) (Table 3). When the threshold of polyp enhancement was selected at 40 HU, the sensitivity for detection of adenocarcinoma was calculated as 92%; specificity, as 20%; positive predictive value, as 50%; and negative predictive value, as 75%. When a threshold of 50 HU was selected, these values were 77%, 33%, 50%, and 62%, respectively. When a threshold of 60 HU was selected, the values were 62%, 40%, 48%, and 56%, respectively.


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  		TABLE 3. Lesion Discrimination with Enhancement Thresholds of 40, 50, and 60 HU for Diagnosis of Adenocarcinoma (Grades 3-5) and Adenoma (Grades 1 and 2)

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
The usefulness of intravenous contrast-enhanced dynamic helical CT of the air-insufflated colon for detecting and staging colorectal cancer has been shown (18,19), as it improved both reader confidence for detecting lesions and bowel wall conspicuity (17). Although dual positioning of the patient improves the accuracy of CT colonography, the problems and limitations associated with poor bowel preparation cannot always be overcome (17,20,21). An additional advantage of contrast-enhanced CT colonography is the ability to provide images of extracolonic tissues and the liver for staging colorectal cancers (18,19,22). In patients in whom CT colonography is performed as a screening examination, it is likely that contrast material will permit identification and characterization of additional unexpected abnormalities (23–25). Recently, contrast-enhanced CT colonography was extended to include patients undergoing surveillance after surgical removal of locally invasive colorectal carcinoma (26–27).

The significance of polyp enhancement must be further elucidated. There is evidence that neovascularization is an early critical event in primary colorectal tumorigenesis, reaching a maximum level early in the malignant process (28–29). Vascular branching counts, an indirect estimate of tumor angiogenic activity, are significantly higher in carcinomas than they are in adenomas (28–29). For colonic tumors, microvascular density, a direct measurement of angiogenic vessels in a solid tumor, is lower in the normal mucosa than in adenomas and is highest in carcinomas (29). Tumor vascularity evaluated at color Doppler ultrasonography is a good preoperative indicator of recurrence and patient survival in colon cancer (30). These findings have stimulated much interest in the use of intravenous contrast material as an adjunctive technique for improved in vivo characterization of polyps. We hypothesized that for polyps 10 mm or larger, the degree of enhancement would inversely correlate with differentiation.

In our study, we did not find a significant correlation between the size of the mass and its degree of enhancement or between the size of the mass and the grade of malignant differentiation. This is somewhat surprising, since it might be expected that larger lesions will enhance to a greater extent and be less differentiated. However, tumor perfusion is variable and unpredictable. After exclusion of the potential outlier, we did not demonstrate a significant correlation between the various histologic grades and the degree of enhancement. Although there seems to be a trend of increasing enhancement from adenoma with dysplasia (grade 2) into poorly differentiated adenocarcinoma (grade 5), it was not significant (Table 2).

With the technique we used, we measured enhancement after a standardized delay of 45 seconds from the start of contrast material injection. Although this delay may be useful for the assessment of bowel wall conspicuity, it may not be the optimal delay for the assessment of lesion characteristics. This single measurement in time may have caused underestimation of the microvascular characteristics. It is possible that other specific contrast agents targeted at angiogenic vessels, such as have been developed with gadolinium-loaded immunoliposomes targeted at very specific endothelial intergrins, may provide this important predictive data (31). The scanning time in our patients was between 22 and 30 seconds. With a delay of 45 seconds, a lesion was therefore scanned between 45 and 75 seconds after the start of injection. Calculation of the actual delay time for each lesion is complex and relates not only to the location but also to the blood vessel tortuosity and the patient’s overall medical status. Thus, further studies should be aimed at evaluating the timing of data acquisition to document whether this improves characterization. Perfusion measurements may be the optimal tool for evaluation of the vascular characteristics of colorectal cancers with perfusion maps and time-density curve analysis.

When a polyp is detected, the only reliable parameter influencing the diagnostic work-up is the size of the polyp (32). If contrast material perfusion characteristics were reliable in the prediction of tissue characterization, it would be helpful to study whether this would influence clinical decision making, specifically to avoid unnecessary procedures. When different thresholds of enhancement are applied for evaluation of the possibility of predicting different types of adenocarcinoma (grades 3–5), we found that a threshold of 40 HU results in a sensitivity of 92% but a low specificity of 20% for the diagnosis of carcinoma. When the threshold was increased to 60 HU, a trade-off between sensitivity and specificity was found, with a decrease in sensitivity to 62% and an increase in specificity to 40%. This clinical scenario is similar to that in CT lung screening, where nodule characterization with contrast material is used as a decision-making tool (27). The absence of significant lung nodule enhancement (15 HU) at CT is strongly predictive of benignity. Malignant nodules enhance more than do granulomas and benign neoplasms (33). A value below the threshold level of 40 HU is a relatively reliable indicator of the absence of tumor. The negative predictive value was 75% (Table 3). A potential benefit of this enhancement information may be in those patients in whom it may not be possible to reach a lesion except with a surgical approach. Enhancement patterns within the lesion that are below 40 HU might indicate a more benign lesion, therefore, allowing a more conservative approach.

Limitations of this study are data analysis that was retrospective with a small sample size. Bias may also have occurred, since we chose only patients with histologic proof of disease (34). Its magnitude, we believe, is small, since the decision to resect a lesion was not based on the contrast material injection. Comparison of polyp attenuation with the patient in the prone and in the supine positions might change the position of the lesion to a caudal or cephalad position and therefore to a thinner or thicker body part. This could theoretically change the Hounsfield units. Large lesions can have heterogeneous enhancement, with a different degree of enhancement in various regions. This could have affected the measurements, but we averaged three regions of interest that were at least 1 cm2 within the lesion. Perfusion maps of lesions may be more accurate in qualitative analysis of different parts of the lesion.

At our institution, we have been performing CT colonography for 6 years, with 642 studies performed until March of 2002. This represents the spectrum of polyps available for histologic correlation in which intravenous contrast material was used. Larger scale prospective studies might prove the reliability of CT colonography with intravenous contrast material as an adjunct to polyp characterization by making the trend found in this study statistically significant.

In conclusion, our provisional data suggest that there is no significant correlation between the size or malignant differentiation of a colorectal polyp and its enhancement values at CT colonography. Our hypothesis needs to be rejected, although there was increased enhancement with lesser degrees of colorectal cancer differentiation. We suggest that further studies be performed not only to increase the number of lesions being analyzed and compared but also to optimize perfusion parameters that can be measured for the in vivo characterization of tumor neovascularity.


   FOOTNOTES
 
Author contributions: Guarantors of integrity of entire study, M.M.M., V.R.; study concepts, M.M.M., J.S.; study design, J.S., M.M.M., J.R.K.; literature research, J.S.; clinical studies, J.S., I.N., R.J.F.; data acquisition and analysis/interpretation, J.S., M.M.M.; statistical analysis, J.S.; manuscript preparation, J.S., J.B.K., M.M.M.; manuscript definition of intellectual content, J.S., M.M.M., V.R.; manuscript editing and revision/review, J.B.K., V.R., R.J.F.; manuscript final version approval, J.S., V.R.


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RESULTS
 DISCUSSION
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R. E. van Gelder, H. W. Venema, J. Florie, C. Y. Nio, I. W. O. Serlie, M. P. Schutter, J. C. van Rijn, F. M. Vos, A. S. Glas, P. M. M. Bossuyt, et al.
CT Colonography: Feasibility of Substantial Dose Reduction--Comparison of Medium to Very Low Doses in Identical Patients
Radiology, August 1, 2004; 232(2): 611 - 620.
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