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Staging of Rectal Cancer after Polypectomy: Usefulness of Endorectal US¹

¹ From the Departments of Radiology (J.B.K., R.A.K.) and Colorectal Surgery (S.M.S.), Beth Israel Deaconess Medical Center, One Deaconess Rd, Boston, MA 02215. From the 1996 RSNA scientific assembly. Received June 1, 1998; revision requested July 22; revision received August 5; accepted October 6. J.B.K. supported by the RSNA Research and Education Foundation as an RSNA Scholar. Address reprint requests to J.B.K.

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To determine the usefulness of endorectal ultrasonography (US) in staging rectal cancer discovered at polypectomy.

MATERIALS AND METHODS: Before surgical resection, endorectal US was performed in 18 consecutive patients with adenocarcinoma discovered in polypectomy specimens. A rotating 7–10-MHz endoprobe with an inflatable balloon was used in all cases. The precise depth of penetration (T stage) was determined with endorectal US and correlated with the histopathologic findings.

RESULTS: For detection of residual tumor after polypectomy, endorectal US had a sensitivity of 100%, specificity of 44%, positive predictive value of 64%, and negative predictive value of 100%. Although the precise T stage was correctly predicted with endorectal US in only eight patients (44%), endorectal US was able to demonstrate whether the tumor was limited to the bowel wall in 16 patients (89%).

CONCLUSION: Endorectal US is an accurate technique for localizing tumors to or beyond the rectal wall in patients who have undergone diagnostic polypectomy. Although inaccuracies in determining the specific T stage may occur, endorectal US facilitates surgical planning in the vast majority of patients and should therefore remain the local staging technique of choice in this specific patient population.

Index terms: Rectum, neoplasms, 757.3211 • Rectum, surgery, 757.126, 757.45 • Rectum, US, 757.12989

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Endorectal ultrasonography (US) is currently the best method of preoperatively staging rectal tumors. Usually, endorectal US is performed after identification of a rectal tumor with digital rectal examination or endoscopy. At our institution, endorectal US is used to assess whether local full-thickness resection is feasible (stage T1 or T2) or not feasible (stage T3) (1) and to facilitate surgical planning, since the depth of tumor invasion is directly related to outcome and prognosis (2). In these cases, both the degree of tumor invasion and the presence or absence of lymphadenopathy can be assessed with endorectal US. The accuracy of endorectal US in predicting the depth of tumor invasion is reported to be 81%–92% (3).

Benign-appearing rectal polyps may be identified and removed during endoscopy. If adenocarcinoma is identified in these polyps, then staging these tumors is important for clinical decision making. Unfortunately, the results of staging with endorectal US after polypectomy are unknown, to our knowledge. Irradiation and surgery may result in overestimation of the depth of tumor invasion with endorectal US (4), but the effects of prior polypectomy, if any, are unknown.

We compared the results of endorectal US staging of rectal cancer after polypectomy with the histopathologic findings after surgery to determine whether endorectal US is useful for preoperative staging and surgical planning in this specific subset of patients.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patients were included in the study only if they underwent endorectal US at our institution within 1 month after polypectomy and underwent subsequent surgical excision of a rectal cancer. The US results were then compared with the histopathologic findings in the resected specimens. A total of 18 patients were referred for preoperative staging of rectal adenocarcinoma with endorectal US after undergoing diagnostic polypectomy. To avoid bias, all postpolypectomy patients sequentially referred for endorectal US who subsequently underwent surgery were included in this retrospective study. All lesions appeared benign to the endoscopist at the time of polypectomy and were therefore removed in their entirety. The histopathologic findings were unexpected in all 18 patients.

Polypectomy was performed endoscopically in 13 patients; in five patients, polypectomy was performed surgically by means of transanal excision. In general, endorectal US was performed 3–4 weeks after polypectomy. All endorectal US studies were performed in a similar manner by one radiologist (R.A.K.), who staged each tumor at the time of the study. The endorectal US scans were reinterpreted by two gastrointestinal radiologists (R.A.K., J.B.K.) experienced in the technique of endorectal US. These radiologists were blinded to the histopathologic findings and reached a consensus about the tumor stage.

Endorectal US Technique
Endorectal US was performed with a commercially available US scanner (B & K Medical, Naerum, Denmark) equipped with a 7–10-MHz mechanical rotating endoprobe (type 1850) with a focal zone of 2–4 cm, an axial resolution of 0.4 mm, and a lateral resolution of 1.0 mm. A 360° display of the rectal wall and surrounding tissue was provided. A latex balloon was attached to the end of the probe over the lubricated transducer. After administration of a cleansing enema (Fleet, Lynchburg, Va), the patient was placed in the left lateral decubitus position. A digital rectal examination was performed to exclude clinically important anal stenosis and to lubricate the anal canal, then the probe was gently inserted. The balloon was inflated with 40 mL of degassed water, and images were recorded with a digital capture device (Eastman Kodak, Rochester, NY).

Interpretation of Endorectal US Scans
The following data were collected: presence or absence of a mass in the rectal wall, depth of tumor invasion, size and location of the tumor, distance of the tumor from the anal verge, and percentage of the rectal wall circumference involved by the tumor. Lesions less than 4 cm in diameter, less than 10 cm from the anal verge, and with no evidence of distant metastases or invasion into perirectal fat are usually eligible for local excision (1). The presence or absence of lymph nodes and nodal involvement by tumor were not included in the data analysis because these factors were not consistently evaluated at surgery. The US classification of tumor depth into the bowel wall corresponds to the pathologic classification of the TNM system (5). Each tumor was assigned a T stage, with T1 indicating a tumor in the mucosal or submucosal layer, T2 a tumor extending into but not beyond the muscularis propria layer, and T3 a tumor extending beyond the muscularis propria layer into perirectal tissue and fat. Each tumor was also assigned a Dukes stage (6), with stage A indicating a tumor confined to the bowel wall and stage B indicating tumor extension through the bowel wall.

Histopathologic Study
Specimens were fixed, prepared, and stained with standard techniques. The depth of tumor invasion was classified according to the pathologic TNM classification: T1, tumor confined to the submucosa; T2, tumor confined to the muscularis propria; and T3, tumor that has penetrated the rectal wall into the perirectal fat or subserosa. The histopathologic data were the standard of reference for comparison with the endorectal US findings.

Statistical Analyses
The significance of differences between endorectal US and histopathologic results was measured with the Wilcoxon signed rank test, and ordinal data were correlated with the Spearman correlation. Because samples were not independent, a ² calculation was made with the McNemar correlated proportions test. The agreement between endorectal US and histopathologic results was determined with a weighted value because T-stage data represented ordered categories with no linear relationship between numbers. Standard statistical techniques were used to determine diagnostic accuracy (sensitivity, specificity, and predictive values) (7).

	RESULTS

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Eighteen consecutive patients met all of the inclusion criteria. The T stage was correctly predicted with endorectal US in eight patients (44%). Seven tumors (39%) were overstaged with endorectal US, and three tumors (17%) were understaged. However, when lesions were assigned a Dukes stage, endorectal US allowed correct prediction of whether the tumor was confined to the bowel wall (stage A) or extended through the bowel wall (stage B) in 16 patients (89%). Of the two tumors with incorrect Dukes stages, one tumor was overstaged and the other was understaged. When used to predict the more surgically relevant Dukes stage, endorectal US had a sensitivity of 94%, specificity of 50%, accuracy of 89%, positive predictive value of 94%, and negative predictive value of 50%.

When lesions were assigned a T stage, there was only moderate agreement between endorectal US and histopathologic results (weighted = 0.44). This agreement did not reach statistical significance (P = .126). No statistically significant difference was found between endorectal US and histopathologic results when lesions were assigned a Dukes stage (² = 0.5).

The T stage was incorrectly predicted with endorectal US in 10 patients, with seven tumors overstaged and three tumors understaged. Two T2 tumors were understaged as T1 with endorectal US, and no change in surgical management occurred (Fig 1). One T3 tumor was understaged as T2 with endorectal US due to microinvasion beyond the muscularis propria layer (Fig 2). Such microinvasion is difficult to distinguish from tumor-induced nodularity of the muscularis propria layer (Fig 3) (4). This understaging error did not alter the choice of surgical management, but the patient did receive additional radiation therapy.

View larger version (144K): [in this window] [in a new window]   Figure 1. T2 tumor understaged as T1. Endorectal US scan shows focal thickening of the hypoechoic muscularis mucosa layer (white arrows) in the anterior rectal wall. The hyperechoic submucosal layer clearly separates the tumor from the hypoechoic muscularis propria layer (black arrows). However, histopathologic analysis demonstrated tumor extension into the muscularis propria.

View larger version (164K): [in this window] [in a new window]   Figure 2. T3 tumor understaged as T2. Endorectal US scan shows a large tumor (T) in the left side of the anterior rectal wall. The tumor clearly extends into the hypoechoic muscularis propria layer (short arrow), with a focal area of nodularity (long arrow) abutting the perirectal fat. Nodularity or focal asymmetric thickening of the muscularis propria layer is frequently identified during endorectal US of rectal tumors and is thought to be due to tumor-induced desmoplasia of the muscularis propria. Histopathologic analysis demonstrated tumor extension into the perirectal fat.

View larger version (166K): [in this window] [in a new window]   Figure 3. T2 tumor. Endorectal US scan shows marked thickening of the muscularis mucosa (small arrow) and muscularis propria (arrowhead) layers with focal nodularity (large arrows) that appears to extend into the perirectal fat. Histopathologic analysis demonstrated no extension into the perirectal fat, unlike the case shown in Figure 2.

View larger version (126K): [in this window] [in a new window]   Figure 4. Rectal wall scarring misinterpreted as a T1 tumor. Endorectal US scan shows focal thickening of the muscularis mucosa layer (white arrows) in the left lateral rectal wall. The hyperechoic submucosal layer is clearly seen outside the tumor immediately beneath the hypoechoic muscularis propria layer (black arrow). No residual tumor was identified at histopathologic analysis.

View larger version (143K): [in this window] [in a new window]   Figure 5. Rectal wall scarring misinterpreted as a T2 tumor. Endorectal US scan shows focal thickening of the muscularis mucosa (large arrow, margins indicated by +) and muscularis propria (small arrows) layers. This finding was considered to indicate a T2 tumor, but histopathologic analysis demonstrated rectal wall scarring with no residual tumor. In retrospect, the hyperechoic submucosal layer is clearly intact and separates the muscularis mucosa and muscularis propria layers.

View larger version (160K): [in this window] [in a new window]   Figure 6. T1 tumor overstaged as T2. Endorectal US scan shows marked thickening of the hypoechoic muscularis mucosa layer (long arrows), with a clearly defined hyperechoic band (short arrow) separating the tumor from the muscularis propria layer, which is not well defined on this image. Such focal thickening of the muscularis mucosa layer is consistent with a T1 tumor, which was demonstrated at histopathologic analysis. + = depth of tumor, x = width of tumor.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
At our institution, patients with rectal cancers that involve the bowel wall (T1, T2, or Dukes stage A tumors) undergo transanal excision with or without chemoradiation therapy (1). However, when the tumor has extended beyond the rectal wall (T3 or Dukes stage B tumor), abdominoperineal resection of the rectum with colostomy or proctectomy with coloanal anastomosis is recommended. The choice of surgical management depends largely on the depth of tumor invasion, which is currently determined with preoperative endorectal US. In our study, endorectal US after polypectomy did not allow accurate distinction between T1 and T2 tumors; however, endorectal US did allow accurate prediction of the more clinically relevant Dukes stage in 89% of patients. Because the choice of surgical management is stratified according to the Dukes stage (6), an accuracy of 89% is of greater clinical use to our colorectal surgeons than the incorrect staging of tumors according to the T-stage system.

Endorectal US remains the most accurate technique for determining the depth of tumor invasion, with reported accuracies of 81%–92% (8–10). However, over- and understaging of rectal tumors continues to be a problem in staging with US due to a variety of well-documented causes (4). To our knowledge, the precise role of US after polypectomy, if any, has not been determined, and determining this role was the purpose of our study. All of our patients had rectal malignancies and were imaged before surgical resection. The inability to identify absence of tumor (stage T0) with endorectal US is important when US is used to identify the presence of residual tumor. However, in patients with known malignancies scheduled for surgery, endorectal US has an important role in predicting tumor extension beyond the rectal wall and therefore in planning surgery.

Accurate staging of rectal cancer has become very important in recent years. First, the survival of patients with rectal cancer is directly proportional to the tumor stage (3). Second, local resection is becoming increasingly popular for treatment of early rectal cancer with or without adjuvant chemoradiation therapy (3). Perhaps equally important, objective assessment of the depth of wall invasion of a rectal neoplasm has provided a means by which local excisional techniques for early rectal cancer may be reported and objectively compared (1).

Errors in interpretation that may result in overstaging may be caused by peritumoral inflammation, effects of preoperative irradiation, or hemorrhage into the bowel wall after biopsy (3,4). Like rectal tumors, these conditions are typically hypoechoic and can therefore lead to overestimation of the depth of tumor invasion. Because of the more anechoic appearance of peritumoral tissue reaction, this condition can be differentiated from tumor with endorectal US (11). However, after polypectomy, as in our patients, or after biopsy, tissue changes may occur that limit accurate demonstration of the depth of tumor invasion. The present study was therefore performed to determine whether polypectomy affects tumor staging and whether the sensitivity of staging with endorectal US after polypectomy differs from that of such staging before polypectomy. There may be clinical consequences of overstaging or understaging of which both radiologists and surgeons should be aware (4). Local excision only of an understaged tumor may compromise the possibility of cure after subsequent more radical surgery.

Overstaging of rectal tumors clearly has major clinical consequences. Numerous factors are responsible for such overstaging, including tumor-induced desmoplasia, lack of operator experience, and local biopsy. When a tumor is understaged and the patient undergoes local excision, additional surgery can be performed for complete rectal excision, if necessary. However, overstaging of T2 tumors as T3 may result in patients undergoing complete rectal excision when local excision may have been adequate management. Numerous studies have evaluated such overstaging (12). In a detailed analysis of 209 cases, Solomon et al (13) found that overstaging occurred in 12% of tumors; usually, histopathologically determined T2 tumors were overstaged as T3 with endorectal US. This result reflects the well-recognized difficulty in differentiating tumor invasion into the muscularis propria from growth beyond the muscularis propria (3).

We reevaluated the digital images of all of our cases that were incorrectly staged. Of the three understaged cases, two T2 tumors were staged as T1 with US and one T3 tumor was staged as T2 with US. This latter case demonstrated microscopic invasion beyond the muscularis propria. In retrospect, we would not have changed our initial staging interpretation in any of these three cases. Of the seven overstaged cases, five demonstrated no residual tumor after surgical resection. However, in each case, focal hypoechoic abnormalities were identified at the biopsy site; these abnormalities could not be distinguished from residual tumor, even in retrospect. Histopathologic analysis of the abnormal areas demonstrated fibrous tissue, desmoplasia, and hemorrhage, none of which can be reliably distinguished from residual tumor at endorectal US. Of the remaining two overstaged tumors, one occurred high in the rectum at the rectosigmoid junction, which is a recognized site that produces overstaging (4).

We did not use color Doppler flow or pulsed Doppler imaging to evaluate the rectal wall tumors. In a recent study by Heneghan et al (14), color Doppler flow and pulsed Doppler imaging were most valuable in evaluating perirectal lymph nodes but did not help in better defining the T stage of residual tumors. In our experience (1,4) and that of others (3,15), endorectal US is sensitive in detection of perirectal nodes but insensitive in differentiation of inflammatory nodes from tumor-infiltrated nodes. Indeed, false-positive results occurred in the study of Beynon et al (15) when an increase in nodal size alone was used as a criterion for malignant involvement.

In the present study, we did not include data from cross-sectional imaging modalities such as computed tomography (CT) or magnetic resonance (MR) because surgeons at our institution currently rely solely on local staging data obtained with endorectal US. CT and MR imaging are accurate in assessing spread beyond the rectal wall, invasion of contiguous structures, spread to regional nodes, or distant metastases. However, CT and MR imaging currently lack the accuracy in determining depth of wall invasion required by the surgeon (3). CT has reported accuracies of approximately 70% in determining depth of wall invasion in patients who have not undergone local excision (16,17). Studies of MR imaging with and without use of endorectal receiver coils have found a good correlation between MR imaging and histologic findings (18). Although MR imaging would provide additional staging information, such as the presence of distant or hepatic metastases, limited studies that correlated endorectal MR imaging, histologic, and endorectal US findings have been performed (19) and no large, prospective comparisons between endorectal US and MR imaging findings have been published, to our knowledge.

Studies have shown that MR imaging does not allow differentiation between rectal carcinoma infiltrating the adjacent bowel wall and wall thickening caused by preoperative irradiation (20). In a large, multicenter, prospective comparison of staging with CT versus MR imaging, CT had a higher sensitivity (76%) than MR imaging (49%), particularly in demonstrating penetration of the muscularis propria by rectal cancer (21). The accuracies of CT and MR imaging in demonstrating the extramural extent of disease were equivalent. However, a body coil was used for MR imaging instead of an endorectal acquisition coil. It would have been interesting if the comparative performance of the most sensitive staging technique, endorectal US, had been evaluated in that study. In a recent study of contrast material–enhanced endorectal MR imaging, Vogl et al (22) demonstrated an approximately 87% correlation between MR imaging and histologic findings, and no tumors in the 35 patients were understaged. However, the authors noted difficulties in distinguishing the layers of the rectal wall due to pressure from the balloon compressing the layers of the wall together.

We analyzed potential limitations of the present study. It is possible that the peritumoral regions seen on the endorectal US scans did not correspond exactly to those examined histologically after rectal wall resection. However, in both cases, the areas of maximal tumor penetration were documented and subsequently compared. Also, the radiologists performing the studies were often aware of the approximate site where the polypectomy was performed. This awareness may have resulted in overstaging of some T0 lesions (ie, tumor completely removed with polypectomy) as subtle T1 lesions. However, this potential problem did not reduce the sensitivity of the technique when tumors were assigned a Dukes stage.

In summary, endorectal US is an accurate technique for localizing tumors to or beyond the rectal wall in patients who have undergone diagnostic polypectomy. Although inaccuracies in determining the specific T stage may occur, endorectal US facilitates surgical planning in the vast majority of patients and should therefore remain the local staging technique of choice in this specific patient population.

	Acknowledgments

 
The authors thank Hugh Wheeler, PhD, for performing the statistical analyses.

	Footnotes

 
Author contributions: Guarantors of integrity of entire study, J.B.K., S.M.S., R.A.K.; study concepts and design, J.B.K., S.M.S., R.A.K.; definition of intellectual content, J.B.K., S.M.S., R.A.K.; literature research, J.B.K., S.M.S., R.A.K.; clinical studies, J.B.K., S.M.S., R.A.K.; data acquisition and analysis, J.B.K., S.M.S., R.A.K.; statistical analysis, J.B.K., S.M.S.; manuscript preparation, J.B.K.; manuscript editing and review, J.B.K., S.M.S., R.A.K.

	References

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Kruskal, J. B. Articles by Kane, R. A. Search for Related Content PubMed PubMed Citation Articles by Kruskal, J. B. Articles by Kane, R. A.