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Gastrointestinal Imaging |
1 From the Departments of Academic Radiology (D.M.K., G.B., J.E.H.) and Medical Statistics (A.R.N.), Royal Marsden Hospital, Downs Rd, Sutton SM2 5PT, England; Departments of Pathology (L.T.) and Surgery (A.R., P.T.), Epsom General Hospital, England; and Department of Surgery, St Helier’s Hospital, St Helier, England (N.B.). From the 2002 RSNA scientific assembly. Received January 28, 2003; revision requested April 15; final revision received July 9; accepted August 6. Supported by a grant from the Royal College of Radiologists, United Kingdom. Address correspondence to D.M.K. (e-mail: dowmukoh@icr.ac.uk).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Mesorectal lymph nodes in 12 patients with adenocarcinoma of the rectum were evaluated with USPIO and high-spatial-resolution MR imaging. Appearance and signal intensity of lymph nodes at T2- and T2*-weighted imaging were recorded before and after USPIO administration. Two radiologists visually assessed pattern of enhancement; interobserver agreement was tested with the 
statistic. After total mesorectal excision, MR imaging of surgical specimens was performed, and it enabled node-by-node correlation with histopathologic findings.
RESULTS: Appearances of 74 nodes at in vivo MR imaging were compared with histopathologic findings. Sixty-eight nodes were nonmalignant (34 were normal, 34 showed reactive changes); six nodes were malignant. Four patterns of USPIO uptake were demonstrated at T2*-weighted imaging: uniform low signal intensity, central low signal intensity, eccentric high signal intensity, and uniform high signal intensity. Two radiologists showed good interobserver agreement ( = 0.88, P < .01) in classification of nodes into these four categories. Sixty-five (96%) of 68 nonmalignant nodes showed uniform or central low-signal-intensity patterns; 16 (47%) of 34 reactive nodes showed central low-signal-intensity patterns. Compared with uniform low-signal-intensity pattern, central low-signal-intensity pattern was more commonly observed in reactive nodes (P < .01, 
2 test; positive predictive value, 67%; 95% CI: 47%, 87%). Eccentric and uniform high-signal-intensity patterns were observed in lymph nodes that contained metastases larger than 1 mm in diameter.
CONCLUSION: Mesorectal lymph nodes can be characterized by using USPIO and T2*-weighted MR imaging. Uniform and central low-signal-intensity patterns are features of nonmalignant nodes. Reactive nodes frequently show central low signal intensity at T2*-weighted imaging.
© RSNA, 2004
Index terms: Iron • Magnetic resonance (MR), contrast media, 757.12143 • Neoplasms, staging • Rectum, MR, 757.121411, 757.121412 • Rectum, neoplasms, 757.321
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Nodal uptake of ultrasmall particles of iron oxide (USPIO) has been proposed as a method for enabling accurate identification of normal and metastatic nodes; in some studies, researchers have already evaluated nodal staging with this method in lung, head and neck, and pelvic malignancies (5–11). In these studies, researchers have shown that a normal node will darken uniformly and homogeneously at T2- and T2*-weighted magnetic resonance (MR) imaging after USPIO administration (5–11). However, to our knowledge, USPIOs have not previously been employed to help characterize mesorectal lymph nodes in rectal cancer.
The specimen removed at total mesorectal excision comprises the rectum and mesorectum and contains the local draining lymph nodes, and this anatomic package provides an excellent opportunity to characterize and compare individual nodes with their histologic counterparts. The aim of this study was to compare the histopathologic findings with the appearances of mesorectal nodes at MR imaging with USPIO in patients with rectal cancer.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Patient Characteristics
Twelve patients with histopathologically verified adenocarcinoma of the rectum who were candidates for primary total mesorectal excision and who had nodes visible within the mesorectum but were judged to be node negative or to have N1 (TNM classification) disease at T2-weighted high-spatial-resolution MR staging with 3-mm section thickness (12) were recruited to undergo further MR imaging with USPIO. By using morphologic criteria, a node was deemed to be positive if it showed an irregular outline or internal signal intensity heterogeneity at high-spatial-resolution T2-weighted MR imaging with 3-mm section thickness (12).
During the study period, a total of 140 patients with newly diagnosed rectal cancer were referred to our institution; of these, 14 patients fitted our inclusion criteria for the study. Of the 14 suitable patients, 12 consented to take part in the study. Another 12 patients were also candidates for primary total mesorectal excision but had no visible mesorectal nodes at T2-weighted MR imaging with 3-mm section thickness; hence, the nodes were unlikely to be detected by using USPIO with MR imaging. The remaining 114 patients had received prior neoadjuvant treatment and were not eligible for inclusion.
There were seven men (mean age, 62 years; range, 53–75 years) and five women (mean age, 54 years; range, 52–56 years). The mean age of all patients was 59 years (range, 52–75 years). None of the patients received preoperative chemotherapy or radiation therapy.
Of the 12 patients, one had stage T1 (TNM classification) tumor, six had stage T2 tumor, and five had stage T3 tumor. Two had poorly differentiated adenocarcinoma, five had moderately differentiated adenocarcinoma, and five had well-differentiated adenocarcinoma. Two of 12 tumors were located in the lower rectum, seven were in the midrectum, and three were in the upper rectum. The morphology of the rectal tumors included annular (four), polypoidal (three), and eccentric wall thickening (five).
MR Imaging
MR imaging was performed with a 1.5-T system (Magnetom Vision; Siemens, Erlangen, Germany) and a wraparound pelvic phased-array surface coil, with the patient in the supine position. MR imaging was performed before and 24–36 hours after the intravenous administration of USPIO. Total mesorectal excision was performed within 7 days from the day of USPIO administration (mean, 4 days; range, 2–7 days).
Prior to the administration of USPIO, sagittal T2-weighted MR images (repetition time msec/echo time msec, >5,000/128; echo train length, 16; section thickness, 3 mm; field of view, 350 cm; matrix, 512 x 512; number of signals acquired, three; imaging duration, 4 minutes) of the rectum were first obtained to enable planning of the transverse sections. Contiguous transverse 3-mm-thick images of the pelvis were acquired in a plane perpendicular to the rectal wall, from the anorectal junction to at least 2 cm proximal to the tumor along the length of the mesorectum. T2-weighted turbo spin-echo (>5,000/128; echo train length, 16; section thickness, 3 mm; field of view, 185 mm; matrix, 256 x 256; number of signals acquired, three; imaging duration, 3–12 minutes) and T2*-weighted two-dimensional spoiled gradient-echo multiecho MR images (630/25.8; flip angle, 30°; section thickness, 3 mm; field of view, 185 mm; matrix, 256 x 256; number of signals acquired, two; imaging duration, 6–24 minutes) were obtained. The range of imaging duration reflects the number of oblique transverse acquisitions required to evaluate the entire mesorectum.
Three patients could not tolerate the long examination and became restless while in the imaging unit. As a result, the superior 3 cm of the mesorectum was not imaged in these three patients. The total MR imaging examination time was approximately 1 hour.
After the precontrast MR imaging study, USPIO contrast medium (Sinerem; Guerbet Laboratories, Roissy, France) was administered to the patient. The drug was supplied as a powder in a glass vial and was reconstituted by using 10 mL of normal saline. A dose of 0.13 mL per kilogram of body weight of the reconstituted solution (equivalent to a dose of 2.6 mg of iron per kilogram) in 100 mL of normal saline was administered intravenously through a microfilter during approximately 30 minutes. During infusion, patients were monitored closely for any adverse effects.
Postcontrast MR imaging was performed 24–36 hours after USPIO contrast medium administration by using the same imaging sequences, planes, and parameters as were used in the precontrast study.
Image Analysis
All image analysis was completed prior to surgery and before the pathologic results were known.
The images were analyzed by two radiologists. One (D.M.K.) had 8 years experience and the other (G.B.) had 10 years experience in the interpretation of pelvic MR imaging studies. The images were assessed independently and with consensus. All images were analyzed with a workstation (Workstation, version VB33A; Siemens, Erlangen, Germany), but a hard copy of the images was also made on film for the purpose of annotation. Images were magnified two to three times for optimal visualization of the mesorectal nodes and were assessed for nodal size, patterns of nodal enhancement after USPIO administration, and nodal signal intensity ratio.
Nodal size.—The maximum and minimum bidimensional length in the orthogonal plane of each mesorectal node was measured to the nearest millimeter on the transverse images by one radiologist (D.M.K.) with the caliper tool on the workstation. Each node was numbered and annotated accordingly on the image.
Patterns of nodal enhancement after USPIO administration.—The pattern of enhancement of each node on the T2- and T2*-weighted MR images after USPIO administration was recorded independently by the two radiologists. This allowed evaluation of the interobserver agreement of the visual assessment. In cases of disagreement, repeat assessment of the images was performed with consensus between the two radiologists for a final classification. The patterns of enhancement detected at in vivo MR imaging with USPIO were compared with the histopathologic findings.
Nodal signal intensity ratio.—The signal intensity ratio of each node was expressed as the signal intensity of the node divided by the signal intensity of muscle. The signal intensity of the node was determined by using a region of interest that encompassed the node (typically 0.1–0.3 cm2). The signal intensity of muscle was obtained with placement of a region of interest of similar size over the gluteus medius or gluteus maximus muscle. The signal intensity measurement was made over the same muscle region before and after contrast medium administration. All regions of interest were drawn by one radiologist (D.M.K.). Two measurements were made for each, and the average was recorded. The signal intensity ratio was computed before and after USPIO administration for both the T2- and T2*-weighted studies.
Before and after USPIO administration, the signal intensity ratios of all nodes on T2- and T2*-weighted MR images were compared. The signal intensity ratios of malignant versus nonmalignant nodes on T2- and T2*-weighted MR images were evaluated. The signal intensity measurements of the gluteus muscle before and after contrast medium administration were also assessed.
Nodal Matching and Radiologic-Pathologic Comparison
Surgery and pathologic processing.—Total mesorectal excision was performed by one of three dedicated colorectal surgeons (A.R., P.T., N.B.), and the specimens were transported directly to the pathology laboratory either fresh or in buffered formalin saline. The specimens were opened anteriorly to the upper border of the mesorectum and at least 20 mm above the tumor. Each specimen was pinned to corkboard and immersed in a tank of buffered formalin saline for at least 72 hours for fixation.
Specimen MR imaging.—Three-millimeter-thick contiguous images of the specimen were obtained from the distal resection margin along the length of the mesorectum. Imaging was performed in the transverse plane with the same imaging parameters as those used to perform the in vivo studies.
Nodal matching between specimen MR imaging and in vivo MR imaging.—Because both in vivo and specimen MR imaging were performed with the same imaging parameters and planes, it was possible to match the lymph nodes detected at in vivo imaging with those nodes detected at specimen MR imaging (D.M.K., G.B.) by correlating each node for the position of the node in relation to the rectum, the shape of the node, the size of the node, the appearance of the tumor and/or rectum at the level of the node, and the position of the blood vessels within the mesorectum at the level of the node (Fig 1). Individual nodes seen at in vivo MR imaging but not visible at specimen MR imaging and vice versa were noted.
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The pathologic evaluation was performed by a pathologist (L.T.) with 25 years experience in the presence of a radiologist (D.M.K. or G.B.). The total mesorectal excisional specimen was sectioned transversely stepwise from distal to proximal ends at 3-mm intervals by using a 3-mm ruled template as a guide. The tissue sections were laid out and numbered sequentially from distal to proximal ends. The slices were then photographed. Each tissue slice was then matched to a corresponding specimen MR image.
In each pathologic tissue slice, a careful search for lymph nodes was made by the pathologist. Each lymph node found at tissue dissection was matched to a corresponding node visible on the specimen MR images by studying the position of the node in relation to the rectum, the shape and size of the node, the appearance of the tumor and/or rectum at the level of the node, and the position of the blood vessels within the mesorectum at the level of the node (Fig 1). Instances where nodal matching was not possible were recorded as such. In this way, it was possible to compare individual mesorectal nodes visible at in vivo imaging with histopathologic findings.
The nodes harvested from each tissue section were placed in individual trays for processing, and the tray numbers were annotated against the nodes on the specimen MR images.
All nodes obtained were sliced and processed according to standard methods and stained with hematoxylin-eosin. The nodes were individually reported according to the tray numbers in which they were placed. The lymph nodes were reported by the pathologist (who was blinded to the radiologic findings) as normal, reactive (follicular or sinusoidal hyperplasia), or malignant. If a node showed concomitant tumor infiltration and reactive changes, it was classified as a malignant node for the purpose of analysis. For lymph nodes that were malignant, the location and size of the metastatic foci were recorded.
When the result of the histopathologic analysis was known, the tissue from a reactive node that showed central low signal intensity was selected for further staining with Perls Prussian blue stain to demonstrate the location of iron oxide particles within the node.
Statistical Analysis
Statistical analysis was performed with software (SPSS for Windows, version 10.0.5; SPSS, Chicago, Ill). The pattern of enhancement observed in lymph nodes by two observers was tested for interobserver agreement with the test. Before and after USPIO administration, the signal intensity ratios of nodes on T2- and T2*-weighted MR images were compared by using the Student t test. The T2- and T2*-weighted signal intensity ratios of nonmalignant versus malignant nodes after administration of USPIO were compared by using the Mann-Whitney U test because of nonnormal distribution of the values. The signal intensities obtained over the gluteus muscle before and after contrast medium administration were also compared by using the Student t test.
No significant difference was found in the distribution of the signal intensity ratio between male and female patients or between older and younger (defined as older or younger than the median age of 56 years, respectively) patients in our study group (P > .05, Mann-Whitney U test). Hence, the statistical analysis for signal intensity ratio was not adjusted for age- or sex-related differences.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Of the 74 lymph nodes detected at in vivo imaging that were matched to histopathologic findings, 68 were nonmalignant and six were malignant. Of the 68 nonmalignant nodes, 34 were normal and 34 revealed reactive changes, which included follicular hyperplasia (n = 30) and sinusoidal hyperplasia (n = 4). Four of 43 mesorectal nodes that were not matched to in vivo MR images were malignant, but these were 2 mm and were found in one patient in whom two other malignant nodes were correctly identified.
The results that follow refer to the 74 mesorectal nodes seen on in vivo MR images that were compared with histopathologic findings.
Nodal Size
The mean short- and long-axis nodal sizes were 4.0 mm (range, 2–8 mm) and 5.0 mm (range, 3–13 mm), respectively, at in vivo MR imaging.
Patterns of Nodal Enhancement after USPIO Administration
No discernible change in the appearance of lymph nodes was recognized on T2-weighted images after USPIO administration. However, the appearance of the nodes on T2*-weighted images obtained with the T2*-weighted two-dimensional spoiled gradient-echo multiecho sequence after contrast medium administration could be classified into four main patterns: uniform low signal intensity, central low signal intensity, eccentric high signal intensity, and uniform high signal intensity (Fig 3).
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There was very good interobserver agreement ( = 0.88, P < .01) in classification of the appearance of mesorectal nodes on T2*-weighted images into these categories by two radiologists who reviewed the images independently (Table 1). Disagreement occurred with regard to five nodes. In three of these, the chemical shift artifact surrounding the node resulted in perception of a central low-signal-intensity pattern instead of a uniform low-signal-intensity pattern. In the other two nodes that showed subtle central low signal intensity, one observer spuriously classified the pattern in these as uniform high signal intensity. Subsequent repeated review of these nodes at the workstation with further magnification enabled the reclassification of these nodes with consensus.
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2 test) and had a positive predictive value of 67% (95% CI: 47%, 87%) for reactive nodes. Perls Prussian blue staining of a section obtained from one such node with follicular hyperplasia demonstrated distribution of the iron oxide particles in macrophages predominantly within the medullary sinus (Fig 6).
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No significant difference was found in a comparison of the signal intensity ratio of nonmalignant versus malignant lymph nodes after USPIO administration at T2-weighted (median, 3.2 and 2.4, respectively; P = .77, Mann-Whitney U test) or T2*-weighted (median, 1.1 and 0.7, respectively; P = .78, Mann-Whitney U test) MR imaging.
There was also no significant difference in the signal intensity measured over the gluteus muscles before and after USPIO administration at T2-weighted (mean, 109 and 109, respectively; P = .94, paired t test) and T2*-weighted (mean, 183 and 181, respectively; P = .82, paired t test) MR imaging, which was employed in the calculation of the signal intensity ratio of the lymph nodes.
At review of the signal intensity and signal intensity ratios of all nodes that showed the central low-signal-intensity pattern, none of these nodes demonstrated a paradoxical increase in signal intensity after USPIO administration (5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The most widely evaluated lymphographic MR imaging contrast agent is USPIO, which is administered intravenously. Once in the circulation, the particles are transferred by a process of transcytosis from capillaries into the interstitial space (13) and then via lymphatic vessels into lymph nodes. The iron particles, which are phagocytosed by nodal macrophages (13), produce susceptibility effects and result in signal intensity loss in normal nodes on T2- or T2*-weighted MR images. In nodes that are totally or partially replaced by tumor, the macrophage-depleted tumor-bearing areas demonstrate little susceptibility effect and remain with relatively high signal intensity (5–11).
The ability to detect uptake of USPIO into small mesorectal nodes requires an imaging sequence that is capable of high spatial resolution and that produces images with sensitivity to the susceptibility effects of the USPIO. However, increased sensitivity to the susceptibility effects can limit spatial resolution, since excessive low signal intensity resulting from the USPIO can obscure adjacent nodal details.
For the identification of nodes within the mesorectum, we found T2-weighted MR imaging to be superior to T2*-weighted MR imaging, since nodes were readily distinguished from blood vessels. Conversely, the T2*-weighted two-dimensional spoiled gradient-echo multiecho sequence, which is more sensitive to the susceptibility effects of iron, was more successful in characterizing the uptake of USPIO into nodes. The T2*-weighted two-dimensional spoiled gradient-echo multiecho sequence employs signal averaging from five echo times, thus reducing movement and chemical shift artifacts. However, as both lymph nodes and vessels were similarly high in signal intensity on T2*-weighted images before administration of USPIO, they may be mistaken for one another. Hence, we suggest that both T2- and T2*-weighted imaging should be performed for the assessment of mesorectal lymph nodes.
With a section thickness of 3 mm, nodes that were 3 mm or larger could be confidently identified in the transverse plane. Use of a 256 x 256 matrix and a small field of view (185 mm) enabled achievement of an in-plane resolution of approximately 0.7 x 0.7 mm. However, micrometastases 1 mm or smaller would still be difficult or impossible to detect at this resolution.
In our study, we found that nonmalignant nodes usually had one of two appearances on T2*-weighted images after USPIO administration: uniform low signal intensity or central low signal intensity. Uniform low signal intensity at T2*-weighted MR imaging has been used as a criterion for normal nodes in other studies with USPIO (5–11). However, to our knowledge, central low signal intensity, the pattern frequently encountered in reactive lymph nodes in our study, has not been previously described.
We believe the pattern of central low signal intensity at T2*-weighted MR imaging may be related to the distribution of macrophages that contain the iron particles within lymph nodes. In a normal node, the majority of the macrophages are distributed within the medullary sinus and, to a lesser extent, within the subcapsular sinus (14,15). This distribution is visible at high-field-strength (9.4-T) imaging of nodes after USPIO administration (15). The lymphoid follicles, which are located in the cortex, are scant in macrophages and appear relatively high in signal intensity compared with the signal intensity of the medulla (15).
When lymph nodes undergo reactive enlargement, there is frequently cortical or paracortical hyperplasia, which results in an increase in size of the lymphoid follicles and the nodal cortical thickness. Since the macrophages remain predominantly within the medullary sinus, the susceptibility effects of USPIO in a reactive lymph node can appear confined to the center of the node, and this appearance gives rise to the pattern of central low signal intensity. Although the normal distribution of USPIO within a node is not perceptible when evaluated at 1.5 T, the exaggeration of the nodal cortical thickness in the presence of nodal hyperplasia, combined with the use of high-spatial-resolution imaging, has probably enabled us to perceive this differential distribution of USPIO within the reactive nodes. This observation is important, because if we had applied criteria derived from previous studies with USPIO (5–11), we would have classified these nodes as suspicious or malignant.
Malignant nodes that harbor focal metastases larger than 1 mm in diameter demonstrated uniform or eccentric high signal intensity in our study. The eccentric high-signal-intensity pattern is potentially useful since it reflects the behavior of nodal metastasis. Lymphatic metastases are carried via lymphatic trunks to nodes, where they usually settle within the subcapsular sinus (14) or along the sinusoids within the medulla. From the intranodal site, the tumor cells proliferate and subsequently replace the lymph node. However, because a small nodal deposit is usually focal, this may be recognized at T2*-weighted MR imaging after USPIO administration as an eccentric area of high signal intensity adjacent to the low-signal-intensity normal nodal tissue.
Among the pitfalls we found in our evaluation was the presence of chemical shift artifact, which results in a thin high-signal-intensity line along one side of an otherwise uniformly low-signal-intensity node. This may result in misinterpretation as central low signal intensity and was a cause of interobserver discordance in our study. Difficulty may also be encountered in distinguishing between nodes that show central low signal intensity and those that exhibit uniform high signal intensity. This is because the area of central nodal darkening may be small or irregular. In such a situation, imaging in another plane or further magnification of the image may be useful in distinguishing between the two.
In our study, we could normalize the signal intensity of nodes to the signal intensity of the gluteus muscles, since the signal intensity of muscle did not show any significant change following contrast medium administration. However, we found that the use of the signal intensity ratio was unhelpful in discrimination between benign and malignant lymph nodes. This was not surprising, since a substantial proportion of benign nodes in our patients exhibited a central low-signal-intensity pattern, while the partially infiltrated nodes demonstrated an eccentric high-signal-intensity pattern at T2*-weighted MR imaging.
The sensitivity, specificity, and diagnostic accuracy of MR imaging with USPIO in the nodal staging of rectal carcinoma needs to be verified with a larger population study, as the number of malignant nodes was small in this initial series. A larger prospective study is currently being undertaken at our institution to validate these observations and the use of these criteria.
There were limitations to our study. First, because of time constraints or patient compliance, it was not always possible to image the entire mesorectum in vivo. This accounted for the relatively low rate (57%) of matching between nodes seen in vivo and the total number of mesorectal nodes harvested at pathologic analysis. It has been shown that the majority (98%) of positive nodes are located in the mesorectum at the level of the tumor (16), and it may be hard to justify a prolonged examination that may be poorly tolerated by the patient in order to detect "skipped" nodal metastases.
Second, lymph nodes proximal to the mesorectum along the superior rectal vessels up to the level of surgical transection were not evaluated. Node-by-node histopathologic correlation for these nodes would be difficult because they lie outside the mesorectum in a loose mobile mesentery, thus preventing accurate spatial localization.
Third, because of the limits of spatial resolution, small metastases of 1 mm or smaller cannot be identified by using the technique. This may not be a significant limitation, as the detection of an occult micrometastasis (defined as smaller than 1 mm) remains controversial and appears to be of limited clinical value. Andreola et al (17) found that the presence of small (5-mm) metastatic lymph nodes, vascular invasion, positive distal margin of the rectum, and positive circumferential margin of the mesorectum were more important than occult (
1 mm) micrometastases in prediction of early recurrence of rectal cancer.
Fourth, as all patients in our study had operable tumors and directly underwent surgery, we are uncertain as to what degree our findings may be generalized to other patients with higher stages of the disease.
Finally, because of the small number of malignant nodes in our series, the full spectrum of the appearances of malignant nodes is yet to be determined, and a larger prospective study is underway to ascertain the accuracy of the technique in detection of nodal metastases.
In conclusion, four distinct patterns of USPIO uptake at T2*-weighted MR imaging were observed in mesorectal lymph nodes, and these patterns could be applied in future studies with regard to the evaluation of diagnostic accuracy in nodal staging of rectal carcinoma. Uniform and central low-signal-intensity patterns were features of nonmalignant nodes. Reactive lymph nodes frequently demonstrated central low signal intensity, a pattern not previously described. Uniform high-signal-intensity and eccentric high-signal-intensity patterns may be useful in identification of a focal nodal metastasis larger than 1 mm.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, D.M.K.; study concepts and design, D.M.K., G.B.; literature research, D.M.K., G.B.; clinical studies, D.M.K., G.B., L.T., A.R., P.T., N.B.; data acquisition, D.M.K., G.B., L.T.; data analysis/interpretation, D.M.K., G.B., A.R.N.; statistical analysis, D.M.K., A.R.N.; manuscript preparation and definition of intellectual content, D.M.K., G.B.; manuscript editing and final version approval, D.M.K., G.B., J.E.H.; manuscript revision/review, all authors
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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