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Staging of Rectal Cancer: Diagnostic Potential of Multiplanar Reconstructions with MDCT

¹ Institute of Clinical Radiology, Ludwig-Maximilians University Grosshadern Munich, Munich, Germany.
² Present address: Department of Radiology, University of Vienna, Waehringer Guertel 18-20, AKH Vienna, Vienna A-1090, Austria.
³ Institute of Pathology, Ludwig-Maximilians University Grosshadern Munich, Munich, Germany.
⁴ Department of Surgery, Ludwig-Maximilians University Grosshadern Munich, Munich, Germany.

Received November 14, 2003; accepted after revision February 2, 2004.

 
Address correspondence to C. Kulinna (christianekulinn{at}netscape.net).

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. The purpose of this study was to evaluate whether multiplanar reconstructions (MPRs) of MDCT could improve local staging of rectal cancer.

CONCLUSION. Adding MPRs, on the basis of the MDCT data sets, provides definite improvements in the accurate local staging of rectal cancer compared with standard axial reconstructions alone.

Introduction

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Colorectal cancer is the second most common form of cancer in developed countries and is responsible for significant morbidity and mortality rates. The prognosis of rectal cancer directly relates to extramural tumor spread into the mesorectum [1, 2], the ability to achieve surgical clearance [3, 4], and the presence of occult hepatic and lymph node metastases. Two recent advances in therapy are reducing the frequency of local recurrence and improving survival: total mesorectal excision surgery and preoperative neoadjuvant radiochemotherapy in advanced tumor stages [5–7]. These advances have greatly increased the importance of accurate preoperative staging in providing information about tumor location, size, configuration, and local infiltration. One of the main objectives in staging is accurate identification of International Union Against Cancer (UICC) stages I and greater than I [8]. Knowledge of the exact UICC stage influences the selection of patients who benefit from preoperative radiochemotherapy.

The current role of CT in patients with rectal cancer is controversial. Early studies reported high accuracy rates for CT [9–11]. However, most patients in these early series had advanced disease [12]. In more recent reports, less satisfactory results have been obtained, with accuracy rates ranging between 41% and 82% [13–16] for helical CT staging because of limited collimation and insufficient reconstruction increments [17]. The introduction of MDCT allowed thin-collimation scanning, resulting in improved multiplanar reconstructions (MPRs) [18, 19]. These benefits may help to establish MDCT as an effective diagnostic technique in the evaluation of preoperative local staging of rectal cancer.

The aim of this study was to evaluate whether adding coronal and sagittal MPRs to axial slices rather than using axial slices alone could improve UICC staging.

Subjects and Methods

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In this prospective study, 55 patients (30 men and 25 women) with biopsy-proven rectal carcinoma were examined preoperatively with MDCT. The mean age of the patients was 69 years (range, 47–95 years). Written informed consent was obtained from each patient. Five minutes before the start of CT, the patients received a rectal enema with 500–1,000 mL of 2% methylcellulose solution [20]. Before rectal filling, the patients were asked to empty their rectums. No additional preparation followed. All patients underwent the same CT protocol using a Somatom Plus 4 Volume Zoom CT scanner (Siemens) with 1-mm collimation at a table feed of 6 mm/0.75-sec scanner rotation, table speed of 8 mm/sec, and pitch of 6. Each scan was obtained with a tube voltage of 120 kV and 180–250 mAs, depending on the patient's weight. All patients received 120 mL of nonionic IV contrast agent at a flow rate of 3 mL/sec (300 mg I/mL, Solutrast 300, Schering). The scanning was initiated after a delay of 65 sec. The acquisition time with this protocol was approximately 21 sec. Images were reconstructed in axial, coronal, and sagittal planes (5-mm slice thickness, 4-mm increment) from the row data for interactive multiplanar image viewing on a work-station and for documentation on axial planes for the surgeon.

MDCT scans were prospectively evaluated by a clinical instructor (reviewer 1) and a fellow (reviewer 2) in radiology. They were assessed for detectability of the tumor, location, and depth of tumor infiltration and regional lymph nodes. Our study protocol first provided the reviewers with axial images only, followed by a combined evaluation with axial plus sagittal and coronal reconstructions, using a cine mode technique on a PACS. One week elapsed between the evaluations, and the reviewers, blinded to patient identity, interpreted the images independently from each other. The studies were presented to the reviewers in a different order the second time.

Tumors on MDCT were classified by a modified TNM stage: tumors confined to the bowel wall were classified as T1 or T2. An indistinct or spiculated border between the outer rectal wall and the surrounding fat at the level of the tumor was considered as evidence of perirectal invasion (T3). Tumor infiltration into adjacent organs was considered stage T4. Lymph nodes were considered to be positive for metastases if at least one perirectal lymph node with a short-axis diameter of more than 3 mm was found.

The ultimate surgical classification of rectal cancer to establish the correct treatment of patients is based on the UICC [8] classification. Patients underwent surgery if tumors were staged as UICC stage I; if tumors were staged at a UICC stage greater than I, patients underwent radiotherapy before surgery. If patients underwent radiotherapy, the second MDCT, performed after radiotherapy, was included in the study.

CT staging was compared with pathologic UICC staging. The sensitivity, specificity, positive predictive valve (PPV), negative predictive value (NPV), and accuracy rates, including confidence intervals, were calculated for the reviewing of axial images only versus the combination of axial, sagittal, and coronal images. Sensitivity, specificity, PPV, NPV, and accuracy rates were used in the context of identifying UICC stage I versus UICC stages greater than I. To analyze the ratings for the question—"Is there a statistically significant improvement in staging supplementing axial with coronal and sagittal reconstructions?"—we performed a McNemar test for paired nonparametric data. A p value of less than 0.05 was considered a statistically significant difference.

The Cohen's kappa test was performed to assess interobserver reliability. Negative kappa values express discordance of the observations, values higher than 0.75 are considered excellent, and kappa values between 0.4 and 0.7 correspond to good interobserver agreement.

Results

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Histopathologic examination showed stage pT2 tumors in 24 patients, stage pT3 tumors in 30 patients, and a stage pT4 tumor in one patient. N staging showed 36 patients without lymph node metastases, whereas 16 patients were classified with stage pN1 and three patients were classified with stage pN2. Twenty-three patients with UICC stage I and 32 patients with UICC stages greater than I were found histologically.

Interobserver variability was good to excellent (Fig. 1). The lowest interobserver variability was found for UICC staging in sagittal reconstructions ( = 0.881). The highest interobserver variability, but still good agreement, was present on coronal reconstructions in N staging ( = 0.606).

View larger version (13K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. —Bar graph shows interobserver variability between reviewers 1 and 2 as indicated by kappa values. UICC = International Union Against Cancer 2002 [8], T = T staging, N = N staging, ax = axial reconstructions, cor = coronal reconstructions, sag = sagittal reconstructions.

T Staging
With regard to axial reconstructions, the sensitivity for axial slices was 81% versus 77% (reviewer 1 vs reviewer 2), 98% versus 88% for additional coronal slices, and 98% versus 90% with additional sagittal slices. The specificity for axial reconstructions was 58% versus 67%, 75% versus 62% for coronal slices, and 83% versus 79% for sagittal slices. The overall accuracy was 71% versus 72% for axial slices, 89% versus 76% for additional coronal slices, and 93% versus 85% for additional sagittal slices. There were statistically significant differences between axial and coronal reconstructions (p = 0.006) and between axial and sagittal (p = 0.02) reconstructions for reviewer 1 (Table 1).

N Staging
The sensitivity for axial slices was 84% versus 80%, 98% versus 90% for additional coronal slices, and 97% versus 98% for additional sagittal slices. The specificity was 67% versus 67% with axial slices, 86% versus 61% with coronal slices, and 94% versus 70% with sagittal slices. The accuracy rate of N staging was 73% versus 71% (reviewer 1 vs reviewer 2) with axial slices, 91% versus 71% with additional coronal slices, and 96% versus 80% with additional sagittal views. There were statistically significant differences between axial and coronal reconstructions (p = 0.006) and between axial and sagittal (p = 0.01) reconstructions for reviewer 1 (Table 2).

UICC Staging
With regard to axial reconstructions, the sensitivity for axial slices was 78% for both reviewers, 98% versus 87% (reviewer 1 vs reviewer 2) for additional coronal slices, and 98% versus 97% with additional sagittal slices. The specificity for axial reconstructions was 39% versus 52%, 74% versus 52% for coronal slices, and 87% versus 78% for sagittal slices. The overall accuracy was 62% versus 67% for axial slices, 89% versus 73% for additional coronal slices, and 95% versus 89% for additional sagittal slices. Statistically significant differences were observed between axial and coronal (p = 0.01) and between axial and sagittal (p = 0.01) slices for reviewer 1 and reviewer 2 (p = 0.04 vs 0.012) (Table 3).

Discussion

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Multiplanar reformatting is a reconstruction algorithm implemented in medical imaging devices such as CT or MRI. This technique allows rendering of a volume data set, acquired in one direction, into desired planes. It also permits reconstructed images to be displayed in any plane or arbitrary orientation (e.g., sections along curved lines). Although ordinary 2D image data may be used for MPRs, slice misregistration cannot be avoided when reconstructing images in planes other than the plane in which the data were acquired. In practice, a prerequisite for high-quality MPR is near-isotropic voxels. With the advent of MDCT, near-isotropic volume imaging is feasible because of the wide coverage using 1-mm collimation within one breath-hold. Although it means additional time and manpower, MPRs from CT data are currently routinely used for applications involving trauma, CT angiography, and the lung [18, 21–24] but are not widely used for rectal examinations to date. In our study, the CT procedure, including rectal filling and reconstructing and reviewing the images, took approximately 15–20 min.

In this age of market-driven health care, expensive diagnostic procedures must be justified by their impact on treatment selection. Because of the introduction and the proven benefit of preoperative radiochemotherapy for advanced tumor stages [7] and total mesorectal excision, accurate preoperative staging for rectal cancer is critical.

Although initial studies reported that CT is an excellent technique for preoperative staging of colorectal cancer, recent studies have failed to reproduce those results. CT studies from the last decade showed accuracy rates of 41–82% in T staging [13–16]; however, all these examinations were performed before 1999 without MDCT. In our study, MDCT had an accuracy rate of only 81% versus 77% (reviewer 1 vs reviewer 2) for axial evaluation and 98% versus 90% for combined evaluation with MPR in T staging. In UICC staging, our main objective, the accuracy rate for axial slices, was 78% versus 78% and 98% versus 97% with combined evaluations.

These results surpassed those previously reported. In our opinion, two important elements of our study contributed to these superior outcomes: an adequate filling of the rectum and the technical advantages of MDCT, in particular, thin-slice high-resolution imaging combined with high-resolution MPRs. The advantage of increased speed and spatial resolution, with near-isotropic voxel imaging, is improved multiplanar imaging capability. For high-quality sagittal and coronal reformations, one must acquire CT data using the narrowest collimation for volume data acquisition supported by the scanner (e.g., 4 x 1 mm collimation in 4-MDCT). In case further reconstruction procedures are necessary, reconstructions of 1.25-mm sections with a 1-mm increment can serve as the basis for further post-processing without stair-stepping artifacts. This technique can be used in problematic cases to visualize better the anatomic complex, the extent of the disease, and the location of a suspected mass or other abnormality.

Axial sections are still the primary mode of evaluation for local staging of rectal carcinoma. They serve as an adjunct to most other indications: axial sections are important as a control mode to check findings detected on 3D displays. In addition, axial sections are used to evaluate the scan for the presence of collateral findings or unexpected disease. Adding MPRs serves as a cross-sectional technique that optimally displays the longitudinal extent, intraluminal disease, and intramural involvement of rectal disease. Optimal sections through the tumor are obtained with sagittal and coronal reconstructions (Figs. 2A, 2B, and 2C). Both reviewers confirmed that sagittal reconstructions are helpful in exact T staging, whereas coronal slices are important to identify enlarged lymph nodes.

View larger version (147K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —MDCT scans of 55-year-old woman with stage T2 N0 tumor. Transverse CT slice shows possible small-tumor strands (arrow) infiltrating perirectal fat.

View larger version (155K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —MDCT scans of 55-year-old woman with stage T2 N0 tumor. Multiplanar reconstructions in coronal (B) and sagittal (C) views show no neoplastic involvement of perirectal fat in well-distended rectum. No enlarged lymph nodes are visible. Tumor was correctly staged as T2 N0.

View larger version (151K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —MDCT scans of 55-year-old woman with stage T2 N0 tumor. Multiplanar reconstructions in coronal (B) and sagittal (C) views show no neoplastic involvement of perirectal fat in well-distended rectum. No enlarged lymph nodes are visible. Tumor was correctly staged as T2 N0.

The rectum must be sufficiently distended to achieve a sharp contrast between the rectal wall and the lumen [20]. Adequate distention and filling with a negative contrast agent ensures that feces within a partial collapsed rectum do not impair exact tumor delineation. Exact tumor delineation within the rectal wall is critical to identify small strands of tumor tissue extending beyond the external surface, indicative of neoplastic involvement of the perirectal fat or the serosa (Figs. 3A, 3B, and 3C).

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —MDCT scans of 74-year-old man with stage T3 N1 tumor. Transverse CT image shows nodular and spiculated configuration of tumor margin (arrow).

View larger version (134K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —MDCT scans of 74-year-old man with stage T3 N1 tumor. In corresponding coronal (B) view and especially in sagittal (C) view, delineation of rectal wall also seems to be irregular and shows infiltration into perirectal fat (white arrows). Lymph node larger than 3 mm on short-axis diameter can also be seen (black arrows). Histopathology confirmed stage T3 N1.

View larger version (152K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —MDCT scans of 74-year-old man with stage T3 N1 tumor. In corresponding coronal (B) view and especially in sagittal (C) view, delineation of rectal wall also seems to be irregular and shows infiltration into perirectal fat (white arrows). Lymph node larger than 3 mm on short-axis diameter can also be seen (black arrows). Histopathology confirmed stage T3 N1.

Similar strands can be caused by scarring, inflammation, or congestive changes; therefore, we acknowledge the slight tendency toward overstaging in our study. In three of five patients (reviewer 2) and three of three patients (reviewer 1) who were overstaged and examined after radiotherapy, radiogenic fibrosis was mis-interpreted as tumor. In previous studies [25], a peritumoral reaction, comprising fibrosis and inflammation, was described as an important cause of overstaging. In our experience, using MPRs improves differentiation of peritumoral reaction from the tumor itself. The sagittal slices, in particular, help to differentiate the nodular or spiculated configuration of an advanced tumor margin from the smooth opacities of postradiation fibrosis or inflammation in the perirectal fat (Figs. 4A and 4B). Axial slices often show only a smooth spiculation, which can sometimes be a partial volume effect.

View larger version (165K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —MDCT scans obtained after preoperative neoadjuvant radiochemotherapy in 66-year-old woman with stage T2 N0 tumor. Axial reconstruction shows nodular and spiculated appearance (arrow), suggestive of infiltration of perirectal fat.

View larger version (188K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —MDCT scans obtained after preoperative neoadjuvant radiochemotherapy in 66-year-old woman with stage T2 N0 tumor. On sagittal image, these changes were interpreted as smooth opacities of postradiation fibrosis and partial volume effects. Dorsal wall of rectum shows sharp delineation (arrow). Tumor was correctly staged as T2 N0.

MPRs (i.e., sagittal images) also have major implications for improving the delineation of the tumor as opposed to adjacent organs or vessels. Although only one of our patients had a T4 tumor, this improvement is representative of our experience with a consecutive series at our institution. However, stage T4 also includes the infiltration of the visceral peritoneum, which is not visible on MDCT. Although it usually has no implications for therapy, this characteristic of stage T4 should be taken into account when classifying a tumor as stage T3 because the visceral peritoneum usually extends down to the upper part of the rectum.

Lymph node involvement is also important for prognosis and treatment planning of rectal cancer. Thin collimation and MPRs enable better delineation of the size and localization of the lymph nodes, which are important signs for the differentiation of lymph node metastases from reactive lymph nodes. In our study, we focused on the size and number of perirectal lymph nodes. Our results indicate that MDCT provides more accuracy in the diagnosis and staging of lymph node metastases and that combining axial slices with MPRs is superior to using axial slices alone. Another helpful diagnostic tool, especially for N staging, is the capability of cine mode viewing on PACS, particularly for differentiation of small lymph nodes from small vessels. Cine mode viewing and semiautomatic PACS are also necessary for the increased number of images that result from thin-collimation scanning. A data set of 1-mm slices reconstructed with a 40% overlap easily contains more than 200 slices for the examination of the pelvis alone, which exceeds the capacity of film prints. This high number of images raises the question of which technique has the most efficient reporting system. The availability of workstations that can load and handle the larger data sets will help solve this issue. Using the cine mode technique on PACS proved highly useful for analyzing MDCT examinations of the pelvis in patients with rectal cancer.

Daily clinical routine has taught us that more instructive, accessible image information helps the surgeon to be more confident in planning and performing surgery. MPRs proved very useful in assessing rectal wall invasion, infiltration of the mesorectum, and infiltration of the adjacent organs or vessels; thus, postprocessing services are becoming key ingredients in successful radiologic practice and communication.

Near-isotropic volume MDCT with MPR significantly improves staging in rectal cancer compared with axial reconstructions alone. Therefore, MDCT protocols using 1-mm collimation or thinner are generally recommended to allow high-quality MPR.

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