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(Radiology. 2000;214:503-508.)
© RSNA, 2000

Gastrointestinal Imaging

MR Imaging for the Preoperative Planning of Sphincter-saving Surgery for Tumors of the Lower Third of the Rectum: Use of Intravenous and Endorectal Contrast Materials1

Michael Urban, MD, Harald R. Rosen, MD, Nikolaus Hölbling, MD, Wolfgang Feil, MD, Gerhard Hochwarther, MD, Walter Hruby, MD and Rudolf Schiessel, MD

1 From the Department of Radiology, Ludwig Boltzmann Institute of Digital Radiography and Interventional Radiology (M.U., W.H.) and the Ludwig Boltzmann Institute of Surgical Oncology (H.R.R., N.H., W.F., G.H., R.S.), Danube Hospital/SMZ-Ost, Langobardenstrasse 122, A-1220 Vienna, Austria. Received March 23, 1998; revision requested June 17; final revision received May 28, 1999; accepted July 30. Address reprint requests to M.U. (e-mail: Michael.Urban@SMZ.magwien .gv.at).


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate the value of magnetic resonance (MR) imaging with a flexible surface coil in predicting the resectability of tumors in the lower rectum and the feasibility of sphincteral salvage.

MATERIALS AND METHODS: In a prospective study, 61 patients with histologically proved primary adenocarcinoma of the lower or middle third of the rectum (<12 cm from the pectinate line) were examined at double-contrast-material–enhanced MR imaging with a circular polarized flexible surface coil.

RESULTS: Assessment of anal sphincteral infiltration at MR imaging was excellent, with a specificity of 98% and a sensitivity of 100%. In the determination of tumor infiltration into adjacent organs (T4), the specificity was 100%, and the sensitivity was 90%, with surgical and histologic findings as the standards. While MR imaging showed negative nodes in 40 patients (stage N0 at MR imaging), histologic examination showed negative nodes in 27 patients and positive nodes in 34. At MR imaging, sensitivity was 68%, and specificity was 24%.

CONCLUSION: While preoperative staging at MR imaging according to the TNM system still has limited value and accuracy, MR imaging provides the surgeon with valuable information regarding the presence of sphincteral invasion and the surrounding structures in patients with cancers in the lower third of the rectum.

Index terms: Rectum, MR, 757.121411, 757.12143, 757.321 • Rectum, neoplasms, 757.121411, 757.12143, 757.321 • Rectum, surgery, 757.321, 757.451


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Carcinoma of the rectum is one of the most common malignant lesions in the Western world (1). The cure for the cancer and the preservation of sphincteral function are the major goals of modern rectal surgery. In addition to radical surgery, which includes standardized mesorectal excision, sphincter-preserving procedures have gained importance in the treatment of this disease to guarantee the patient an acceptable quality of life after surgery (2–8).

While anterior resection is the standard treatment for tumors in the upper third of the rectum, it is sometimes difficult to predict the feasibility of sphincteral salvage with resection in the middle and lower thirds. Tumors of the lower rectum that are confined to the rectal wall or those that infiltrate the internal anal sphincter can be radically treated with sphincteral preservation (very low rectal or intersphincteral rectal resection with coloanal anastomosis), although infiltration of the external anal sphincter and/or puborectalis muscle has led to abdominoperineal resection of the cancer (2-8). Since magnetic resonance (MR) imaging has been shown to be a valuable tool in the depiction of the pelvic structures, including the rectum and anal canal, we studied its value in the prediction of sphincter-saving surgery for tumors of the lower rectum.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Sixty-one consecutive patients with histologically proved primary adenocarcinoma in the middle or lower third of the rectum (<12 cm from the pectinate line, as determined with a rigid proctoscope) were included in a prospective study that was approved by our institutional review board. All patients provided written informed consent for the MR imaging examination and for the administration of contrast media. Patients with emergency conditions and those not scheduled for radical surgery because of known systemic metastases or poor general health were excluded. Forty-one male and 20 female patients with a median age of 69.5 years (mean age, 64.5 years ± 11 [SD]; age range, 43–82 years) underwent staging at MR imaging. None of the patients had received preoperative radiation therapy or any other local treatment in the rectum besides the endoscopic biopsy.

MR Imaging Technique
The MR imaging examinations were performed on a 1.0-T Magnetom Expert MR system (Siemens Medical Systems, Erlangen, Germany). The preparation of the patients included a cleansing enema, which was performed on the ward. All patients received an enema with 400 mL of a superparamagnetic iron solution (Abdoscan; Nycomed, Oslo, Norway). The enema tube was left in place to mark the lumen of the anal canal.

The patients were then placed in the supine position on a circular polarized flexible surface coil. Turbo fast low-angle shot scout images were obtained in three orthogonal planes by using the body coil. These scout images were used only for the planning of the following sequences. By using the body coil again, transverse T1-weighted spin-echo images (510/14 [repetition time msec/echo time msec], three signals acquired) and T2-weighted turbo spin-echo images (5,400/132, three signals acquired) were obtained to cover the whole pelvis. These images were used to stage the lymph nodes and to determine the level of the tumor.

Subsequently, contrast material (0.1 mmol of gadodiamide [Omniscan; Nycomed] per kilogram of body weight) was intravenously administered by hand as a bolus injection. Transverse, coronal (Fig 1), and sagittal T1-weighted spin-echo images (420/14, four signals acquired) were then obtained by using the flexible surface coil as a receiver. A field of view of 220 mm, a three-quarters rectangular field of view, a 40% phase oversampling, and a matrix of 192 x 256 yielded a pixel size of 0.86 x 0.86 mm. The section thickness was 4 mm, with an intersection gap of 0.4 mm. For the sagittal sequence, a presaturation slab was ventrally placed to cover the femoral vessels to avoid pulsation artifacts. This technique, described by Wallengren and co-workers (9), was used to show the hypointensity of the tumor compared with the strong enhancement of the mucosa and muscles of the rectum (Fig 2). No fat suppression was used to better delineate the tumor against the perirectal fat. Since only the tumors of the lower two-thirds of the rectum were studied, the use of drugs was not necessary to diminish movement in the small bowel.



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  		Figure 1a. (a) Coronal and (b) transverse T1-weighted spin-echo images (510/14) show the following normal anatomy of the sphincter: internal anal sphincter (arrowheads), external anal sphincter (straight solid arrows), levator ani muscle (curved solid arrows in a), mucosa and submucosa (open arrows in a), and anal canal (* in a).

 


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  		Figure 1b. (a) Coronal and (b) transverse T1-weighted spin-echo images (510/14) show the following normal anatomy of the sphincter: internal anal sphincter (arrowheads), external anal sphincter (straight solid arrows), levator ani muscle (curved solid arrows in a), mucosa and submucosa (open arrows in a), and anal canal (* in a).

 


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  		Figure 2a. (a) Coronal and (b) transverse T1-weighted spin-echo images (510/14) show a rectal carcinoma without sphincteral infiltration. The tumor (straight solid arrows) is hypointense to the normal mucosa (curved solid arrows). The external (open arrows in b) and internal (arrowheads in b) anal sphincters are both intact.

 


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  		Figure 2b. (a) Coronal and (b) transverse T1-weighted spin-echo images (510/14) show a rectal carcinoma without sphincteral infiltration. The tumor (straight solid arrows) is hypointense to the normal mucosa (curved solid arrows). The external (open arrows in b) and internal (arrowheads in b) anal sphincters are both intact.

 
After MR imaging, the staging was assessed by the radiologist (M.U.) according the following criteria: infiltration of adjacent organs and infiltration of the external anal sphincter and/or levator ani muscle. Lymph nodes larger than 1 cm were regarded as highly suspicious for tumorous disease, while local nodes smaller than 1 cm were described as negative. All MR images were interpreted by two experienced radiologists (M.U., W.H.). Staging and the decision about the possible surgical procedure were made on a consensus basis; findings on images and written reports were discussed with the surgeon (H.R.R., N.H., W.F., G.H., R.S.).

All patients underwent surgery within 1 week of the imaging studies. The surgical protocol established at this institution for patients with rectal cancer is illustrated in Table 1.


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  		TABLE 1. Surgical Protocol for Curative Resection of Rectal Cancer
 
In brief, all tumors without infiltration of the external anal sphincter that were either well-differentiated or moderately differentiated (G1–2, as determined at preoperative biopsy) were resected by means of very low anterior resection or intersphincteral resection. Restoration of continuity was performed by means of a double-stapling technique or coloanal anastomosis. Tumors that invaded the external anal sphincter or poorly differentiated tumors (G3) closer than 4 cm to the pectinate line were treated by means of abdominoperineal resection with total anorectal reconstruction and dynamic graciloplasty, as previously reported (8).

In patients with nonresectable tumors, a Hartmann procedure was performed with terminal sigmoidostomy and closure of the rectal stump. In all patients, a detailed histologic evaluation of the surgical specimens was performed, and the results were correlated with the findings at MR imaging.

Statistical Methods
The results of MR imaging (infiltration of adjacent organs, infiltration of the external anal sphincter or levator ani muscle, and lymph node enlargement) were compared with the surgical findings (sphincteral preservation vs abdominoperineal resection) and with the histologic status of the lymph nodes. Sensitivity and specificity were calculated for MR imaging with regard to the preoperative assessment of infiltration of the tumor into the sphincteral muscles and/or adjacent organs and lymph node status (N stage).


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
The staging of sphincteral infiltration at MR imaging revealed an involvement of the internal anal sphincter in four patients (7%) and an infiltration of the external sphincter in eight patients (13%) (Fig 3). A tumor confined to the rectal wall was described in 49 patients (80%). Possible sphincteral salvage was predicted in 52 patients (85%). In the eight patients with external sphincteral infiltration, we predicted abdominoperineal resection. One patient showed extensive infiltration of pelvic organs and the sacrum, so a palliative Hartmann procedure seemed to be the only possibility (Fig 4).



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  		Figure 3a. (a) Coronal and (b) transverse T1-weighted images (510/14) obtained in a patient with a T3 tumor in the low rectum shows tumor infiltration of the levator ani muscle and the external anal sphincter on the right side (arrows). Image in b was obtained at the plane of the tumor infiltration.

 


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  		Figure 3b. (a) Coronal and (b) transverse T1-weighted images (510/14) obtained in a patient with a T3 tumor in the low rectum shows tumor infiltration of the levator ani muscle and the external anal sphincter on the right side (arrows). Image in b was obtained at the plane of the tumor infiltration.

 


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  		Figure 4a. (a) Coronal and (b) transverse T1-weighted spin-echo images (510/14) of a large, grade T4 tumor (arrowheads) show perforation of the tumor with abscess formation (straight arrows) and infiltration of the external and internal anal sphincters on the right (curved arrows in a).

 


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  		Figure 4b. (a) Coronal and (b) transverse T1-weighted spin-echo images (510/14) of a large, grade T4 tumor (arrowheads) show perforation of the tumor with abscess formation (straight arrows) and infiltration of the external and internal anal sphincters on the right (curved arrows in a).

 
A stage T4 tumor was diagnosed in nine patients (15%) altogether, and resectability as far as the sphincteral apparatus was concerned was predicted in eight of these patients. An evaluation of the surgical results showed that abdominoperineal resection was performed in 13 patients (21%). Histologic evaluation of the resected specimens showed an infiltration of the sphincteral muscles in only seven patients. One MR image was false-positive and showed no differentiation between the tumor and the levator ani muscle (Fig 5). The tumor proved to be clearly distinguishable at surgery and was completely resectable (Table 2).



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  		Figure 5. Coronal T1-weighted spin-echo image (510/14) obtained in the false-positive case shows suspected infiltration in the left levator ani muscle (arrow). At surgery, the tumor was distinguished from the pelvic floor and was resected with salvage of the sphincter.

 

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  		TABLE 2. Sphincter and/or Organ Infiltration
 
In five patients (8%) without histologically proved sphincteral infiltration, the diagnosis of a poorly differentiated tumor (G3) led to the decision to proceed with abdominoperineal resection. MR imaging correctly showed no tumorous involvement of the anal sphincter in these patients. In four patients, infiltration was restricted to parts of the internal anal sphincter, as diagnosed at MR imaging. This gave us the opportunity to perform an intersphincteral resection of the low rectum with subsequent reconstruction by means of coloanal anastomosis.

Tumors that infiltrated the adjacent organs and/or sacrum (T4) were seen in 10 patients (16%). In seven patients, curative resection was possible with either resection of the small bowel, partial resection of the bladder, or extirpation of the uterus. In three patients, the advanced stage of the tumor made it nonresectable, which necessitated a fecal diversion (Hartmann procedure) followed by chemotherapy and radiation therapy. The tumor in one of these patients was not correctly staged at MR imaging because infiltration of the bladder dome and small bowel was missed in the small field of view.

The determination of the lymph node status revealed that 27 patients (44%) had negative lymph nodes. MR imaging showed no signs of enlarged lymph nodes in 40 patients. Histologic evaluation revealed that 34 patients (56%) had diseased nodes. Positive nodes were found in 21 patients at MR imaging. At MR imaging, the sensitivity was 68%, and the specificity was 24%.


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Preoperative knowledge of the local spread of rectal cancer is essential in the determination of the therapeutic strategy for this disease. Several surgical options have been described, and these help the surgeon to preserve the anal sphincter and the patient's continence and, therefore, to provide an acceptable quality of life for the patient. The decision in favor of or against surgery is primarily influenced by the surgeon's awareness of the biologic aggressiveness of the tumor (determined at histologic grading), the preexisting sphincteral function of the patient (assessed at preoperative anal manometry), and the local infiltration of the cancer in the lower and middle thirds of the rectum.

While computed tomographic (CT) scanning provides only limited information regarding the local spread of rectal tumors (10,11), in the recent past, newer techniques such as endoscopic ultrasonography (US) and MR imaging have led to promising results regarding the prediction of the stage of the local tumor (12–15). In particular, the use of rectal coils has shown excellent results in the depiction of the sphincteral structures (16).

MR imaging at 1.0 T has been described as being accurate in the depiction of the extent of rectal carcinomas for staging (13,17). Findings from both of these studies showed a high degree of correlation with the histologic findings in patients with macroscopic infiltration of the tumor into the perirectal fat. Double-contrast-material–enhanced MR imaging of the rectum was reported to better delineate tumors against the lumen and the normal mucosa that enhanced (9). However, regarding the depiction of the intramural tumor spread in the rectum (T stage) and the lymph node involvement (N stage), the results at MR imaging were still disappointing. The same was true with our technique, so the main aim of this prospective study was not to provide exact T staging but to assess the relationship of the tumors to the sphincteral apparatus.

Only patients who had not undergone preoperative radiation therapy were included in this study. In this context, it is noteworthy that other authors (13) have described the reactive changes caused by preoperative radiation therapy, which made it impossible to delineate the spread of the tumor into the surrounding tissue.

Endoanal imaging of rectal tumors has been performed with great sensitivity both at US and at MR imaging. Because endorectal US depicts five layers of the rectal wall, it can be used for staging with the TNM criteria. The reported accuracy rates range from 64% to 93%, but they most commonly lie between 80% and 90% (18–20). Most diagnostic errors are made because of overstaging; this specially occurs in T2 tumors, in which the fibrosis and/or inflammation around the tumor cannot be distinguished from the spread of the tumor. Understaging also occurs, but it is less common. Detection of the perirectal lymph nodes is somewhat more problematic; reported accuracy rates range from 52% to 83% (and are mostly between 70% and 80%) (19,20).

Endorectal MR imaging is at least as accurate as endorectal US in the local staging of rectal carcinoma, with accuracy rates for MR imaging between 70% and 92% (17,21–24). Endoanal MR imaging can excellently depict sphincteral anatomy (16), but it offers less information regarding the spread of the tumor into the pelvis. In patients with severely stenosed tumors, placement of anal MR imaging coils can be impossible.

In agreement with other authors, we found that the predictive value of our technique in the detection of lymph node invasion is poor. Because the diagnosis is made primarily on the basis of lymph node size, infiltrated nodes with normal sizes are missed with these criteria. Even with a retrospective evaluation of form and fat content, the results were not improved substantially.

On the other hand, one must mention that since mesorectal excision will lead to a locally radical clearance of all tumors that are confined to the rectum and/or the perirectal fat and regional lymph nodes, the issue of exact TNM staging is less important than the relationship of the tumor to the structures in the sphincter.

Physiologic imaging of the lymph nodes with use of iron oxide contrast material (25,26) may be important in the staging of lymph node involvement in the future. The technique is based on the fact that different cells show different uptake of the ultrasmall iron oxide particles. Because tumorous lymph nodes contain fewer macrophages than do normal nodes, they show diminished uptake of the ultrasmall iron oxide particles and, therefore, higher signal intensity on T2-weighted images after the administration of such agents.

Compared with the distant lateral radiographs that were previously obtained in a standard fashion (27) in all of our patients, MR images offer the advantage of more accurate depiction of the inner end of the anal canal.

Due to the limited signal-to-noise ratio of our coil at the ventral rectal wall, the use of pelvic phased-array coils or double coils, as described by de Lange (13), would be preferable in obese patients with tumors of the ventral wall. The underestimation of one T4 tumor in our series occurred in a patient with infiltration of the bladder dome and a large tumor that extended from the lower third of the rectum to the rectosigmoid junction. In all other patients, the infiltration of the tumor into the adjacent organs was correctly assessed at preoperative MR imaging.

The fact that we preoperatively discussed the MR imaging results with the surgeon may seem to have led to a bias. However, the T stage and sphincteral infiltration were intraoperatively and histologically proved or excluded, so the results were not altered. Furthermore, the surgical approach was determined before the MR imaging examination and was not changed.

Reliable preoperative knowledge of the presence of a tumor that infiltrates the adjacent organs is helpful in avoiding an unnecessary laparotomy. Patients with locally advanced disease such as this could profit from preoperative chemotherapy and radiation therapy to achieve a possible decrease in the size of the tumor while still maintaining the option of subsequent radical tumor resection.

Information about sphincteral involvement is (together with tumor grade) of the utmost importance in choosing the appropriate surgical procedure (anterior resection, intersphincteral resection, abdominoperineal resection). The resolution of the internal and external sphincteral structures in our setting has been sufficient in most of our patients to prove or to exclude tumor infiltration.

The results show that the staging of low-rectal cancer at MR imaging with a flexible surface coil is a good method for providing the surgeon with information regarding the infiltration of the anal sphincter. Therefore, while T staging and lymph node staging are limited, MR imaging is recommended as a feasible, reproducible, and noninvasive tool for the evaluation of sphincteral infiltration; it allows the surgeon to plan sphincter-preserving surgical techniques.


   Footnotes
 
Author contributions: Guarantors of integrity of entire study, M.U., H.R.R., R.S., W.H.; study concepts, M.U., H.R.R., R.S.; study design, M.U., H.R.R.; definition of intellectual content, M.U., H.R.R., R.S.; literature research, M.U., H.R.R.; clinical studies, M.U., H.R.R., R.S.; data acquisition, M.U., H.R.R., N.H., W.F., R.S., G.H.; data analysis, M.U., H.R.R.; statistical analysis, H.R.R.; manuscript preparation and editing, M.U., H.R.R., N.H., R.S.; manuscript review, R.S., W.H.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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