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Original Research |
1 Present address: Division of Diagnostic Imaging, Breast Center, Kameda Medical
Center, 929 Higashi-cho, Kamogawa, Chiba, Japan 296-8602.
2 Department of Radiology, The Jikei University School of Medicine, 3-25-8
Nishi-Shimbashi, Minato-ku, Tokyo, Japan 105-8461.
Received May 24, 2005;
accepted after revision August 17, 2005.
Address correspondence to M. Tozaki
(e-tozaki{at}keh.biglobe.ne.jp).
Abstract
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MATERIALS AND METHODS. Retrospective review was performed of 61 consecutive lesions showing non-masslike enhancement. MRI was performed on a 1.5-T system using the volumetric interpolated breath-hold examination (VIBE) sequence. The kinetic parameter was visually assessed as follows: washout, plateau, and persistent.
RESULTS. The most frequent morphologic finding among the malignant lesions was heterogeneous internal enhancement (69%) (p = 0.003), followed in frequency by segmental distribution (54%) (p < 0.001); whereas, stippled internal enhancement was the most frequent finding in benign lesions (50%) (p < 0.001). The presence of clustered ring enhancement was found in 63% of the malignant lesions and only 4% of the benign lesions (p < 0.001). The features with the highest positive predictive value for malignancy were a segmental distribution (100%), clustered ring enhancement (96%), and a washout pattern (94%). The specificity of clustered ring enhancement was 96% (25/26). In cases showing focal and regional enhancement, the combination of clumped internal architecture and clustered ring enhancement showed a statistically significant association with malignant lesions (p < 0.001).
CONCLUSION. Clustered ring enhancement is thought to be a useful sign to differentiate between benign and malignant lesions, in addition to the BI-RADS MRI descriptors.
Keywords: BI-RADS • breast • breast cancer • MRI • VIBE sequence
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The development of new MRI protocols of the breast has enabled simultaneous acquisition of high spatial and high temporal resolution images. One of the representative advanced protocols is a 3D fat-suppressed gradient-recalled echo technique with volumetric interpolation, first described by Rofsky et al. [8]. We previously reported the usefulness of the volumetric interpolated breath-hold examination (VIBE) sequence for evaluation of the extent of breast cancer and of the lesion characteristics [9, 10]. With the use of the high-spatial-resolution sequence, a finding in which minute ring enhancements are clustered (defined as "clustered ring enhancement") was detected in some cases of ductal carcinoma in situ (DCIS).
The recent BI-RADS [11] published by the American College of Radiology includes the first edition of MRI lexicon in relation to breast imaging. Many cases of DCIS are reported to exhibit non-masslike enhancement [12]. In regard to the patterns of internal enhancement among the lesions showing non-masslike enhancement, it was reported that a clumped internal architecture is more frequent in DCIS than in benign lesions [12, 13].
The goal of the current study was to assess the frequency of occurrence of clustered ring enhancement in lesions showing non-masslike enhancement and to evaluate the clinical usefulness of this evaluation, in addition to that of the BI-RADS MRI descriptors, in the differentiation between benign and malignant lesions.
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The histopathologic diagnosis was established by core biopsy (n = 19), excisional biopsy (n = 5), or examination of lumpectomy or mastectomy specimens (n = 37). There were 35 cases of carcinoma and 26 benign lesions. The histologic types of carcinoma included invasive ductal carcinoma with DCIS (n = 4), DCIS (n = 30), and lobular carcinoma in situ (n = 1); and the 26 benign lesions included atypical ductal hyperplasia (n = 5), intraductal papilloma (n = 2), fibrocystic disease (n = 18), and duct ectasia (n = 1). The breast carcinoma had an average tumor size of 41.8 mm, ranging from 5 to 110 mm. The Van Nuys system is a histopathlogic classification of DCIS. On the basis of the Van Nuys system, the DCIS is classified as high (3), intermediate (2), and low (1) grade. In this study, 15 low-grade DCISs, eight intermediate-grade DCISs, and seven high-grade DCISs were included.
MRI
MRI was performed using a 1.5-T system (Symphony, Siemens Medical
Solutions; maximum gradient field strength, 30 mT/m). All patients were
examined in a prone position using a double breast array coil. A transverse
fat-suppressed T2-weighted fast spin-echo sequence was performed with the
following parameters: TR/TE, 3,500/78; field of view, 20 cm; matrix size, 256
x 256; slice thickness, 5 mm with a 1-mm gap. T2*-weighted
first-pass perfusion images were obtained in the transverse plane before,
during, and after the bolus injection of 0.1 mmol gadopentetate dimeglumine
per kilogram of body weight at a rate of 3 mL/s, followed by a 20-mL saline
flush using an automatic injector.
A 3D fat-suppressed VIBE sequence was obtained before and 60 seconds, 100 seconds, and 4 minutes after the start of the IV administration. The MRI parameters for the VIBE sequence were as follows: TR/TE, 3.7/1.7; flip angle, 25°; field of view, 27 cm; matrix, 256 x 218; receiver band-width, 490 Hz/pixel; mean partition thickness, 1.2 mm; and time of acquisition, 35 seconds. The section thickness varied, depending on the size of the breast, and ranged from 1 to 1.5 mm without a gap. The affected single breast was examined on the first- and third-phase dynamic images, acquired at 60 seconds and 4 minutes, respectively, and both the breasts were examined on images obtained in the second phase at 100 seconds. If incidental suspicious enhancement was detected in the contralateral breast during the second phase, additional images of both breasts were obtained immediately during the subsequent third phase.
Image Interpretation
Two experienced breast radiologists evaluated all cases retrospectively and
arrived at a consensus; the radiologists were unaware of any clinical
information or the histopathologic diagnosis.
The morphologic parameters evaluated consisted of distribution modifiers (linear, ductal, focal, regional, segmental, multiple-region, diffuse) and pattern of internal enhancement (homogeneous, heterogeneous, stippled, clumped, reticular). In addition to the BI-RADS MRI descriptors, the presence of clustered ring enhancement was evaluated in the enhancing lesions (positive or negative) (Figs. 1A, 1B, 2A, 2B, and 2C).
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All the morphologic characteristics were analyzed on the coronal images and on transverse and sagittal multiplanar reformations, acquired at 60 seconds and 4 minutes. The final decision on the pattern of internal enhancement was made in images acquired during the third phase, at 4 minutes.
Statistical Analysis
For analysis of group differences from dichotomous variables, the
chi-square test and Fisher's exact test were used. A p value of less
than 0.05 was considered to indicate a statistically significant
difference.
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The features with the highest positive predictive value for carcinoma were a segmental distribution (100%), clustered ring enhancement (96%), and a washout pattern (94%). The specificity of clustered ring enhancement is 96% (25/26).
Table 2 shows the frequencies of observation of clustered ring enhancement according to the BI-RADS MRI descriptors of the lesions. Twenty-one lesions showing clustered ring enhancement exhibited a heterogeneous internal architecture (91%), and the remaining two cases showed clumped internal enhancement (9%). However, among the cases showing a heterogeneous internal architecture, clustered ring enhancement was observed in only those lesions that were malignant. Among the malignant lesions, 88% exhibiting heterogeneous enhancement showed the presence of clustered ring enhancement, whereas only 10% of those showing clumped enhancement showed the presence of this finding (Figs. 6A and 6B). Furthermore, the washout pattern was observed in 55% of the malignant lesions showing clustered ring enhancement (12/22).
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Table 3 shows the frequencies of the morphologic and kinetic patterns in cases showing focal and regional enhancement. None of the morphologic patterns showed any independent statistically significant association with benign or malignant lesions; that is, they were not useful for differentiating between malignant and benign lesions. However, the combination of clumped internal architecture and clustered ring enhancement showed a statistically significant association with malignant lesions (p < 0.001). The most frequently observed kinetic pattern in the malignant lesions was a washout pattern (p = 0.012), whereas the most frequently observed kinetic pattern in benign lesions was a persistent pattern (p < 0.001).
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Regarding the distribution patterns, all the cases that showed segmental enhancement were malignant lesions, whereas multiple regions of enhancement and diffuse enhancement were observed only in benign lesions. Morakkabati-Spitz et al. [13] reported that segmental or linear enhancement was the most frequent manifestation of DCIS on dynamic MRI; however, the overall positive predictive value of this sign was only moderate (34%). The apparently higher positive predictive value of segmental enhancement in our study as compared with that reported by Morakkabati-Spitz et al. may be related to the difference in the plane of the MR images. We assessed the morphologic characteristics using the coronal, transverse, and sagittal images; based on the assessment in these three planes, an apparently triangular region of enhancement, with the apex pointing toward the nipple, was defined as "segmental." In particular, we relied on images from the coronal plane because the distribution of the ductal system can be precisely evaluated on coronal images.
In our study, the most frequent morphologic pattern encountered among the malignant lesions was heterogeneous internal enhancement (69%). In regard to the internal architecture, Liberman et al. [12] reported that the feature with the highest positive predictive value for malignancy was clumped internal enhancement in lesions showing non-masslike enhancement. The discrepancy may also be attributable to two other major factors: difference in the slice thickness—we used images with a higher spatial resolution (mean slice thickness, 1.2 mm)—and evaluation of the internal enhancement on images acquired during the delayed phase at 4 minutes. If the lesion shows a strong enhancement effect during the early phase and a washout pattern, the pattern of internal enhancement was usually assessed as "heterogeneous" during the delayed phase (Figs. 3A, 3B, and 3C). In this study, a washout pattern was observed in 49% of the malignant lesions. We thus surmised that the pattern could depend on the spatial resolution and the time of acquisition of the images.
Until now, the severe technical constraints of MR units have made it necessary to choose between temporal and spatial resolution. Dynamic breast MRI, popular in European countries, attempts to distinguish between benign and malignant lesions according to the enhancement kinetics at a high temporal resolution. Static breast MRI, popular in the United States, attempts to achieve the same goal by evaluating the morphologic patterns at a high spatial resolution. However, Orel and Schnall [20] predicted that acquisition of both high spatial and high temporal resolution images might ultimately dominate MRI protocols for the breast. Recently, the development of new imaging protocols has enabled high spatial and high temporal resolution images to be acquired simultaneously. Because the morphologic appearance of the ductal system on MRI depends on spatial resolution [11], the 3D VIBE sequence, which allows high-spatial-resolution images with near-isotropic voxels to be obtained, is thought to be a useful sequence for breast MRI [9, 10].
The presence of clustered ring enhancement was found in 63% of the malignant lesions and only 4% of the benign lesions in this study. The positive predictive value of this sign for malignancy was 96%. "Clustered ring enhancement" describes a finding in which minute ring enhancements are clustered. "Clumped enhancement" of lexion BI-RADS MRI is defined as an aggregate of enhancing masses or foci in a cobblestone pattern that may be occasionally confluent. Our study has two types of clustered ring enhancement: One shows a clumped enhancement with the enhancing masses or foci constituting a ringlike enhancement pattern (Figs. 4A, 4B, 4C, 6A, and 6B); in the other, the lesion indicates heterogeneous enhancement inside of which minute ring enhancements are seen clustered (Figs. 1A, 1B, 2A, 2B, 2C, 3A, 3B, and 3C). Almost all cases (91%) belonged to the latter group. Among the former, some show the ringlike enhancement pattern early (Figs. 4A, 4B, and 4C); in others, washout produces the ringlike enhancement pattern (Figs. 6A and 6B). To avoid confusion in terminology, it makes more sense to call the former a subtype clumped enhancement and the latter, clustered ring enhancement. The terminology should be differentiated from "clumped" or "heterogeneous." Moreover, because a washout pattern was observed in 55% of malignant lesions showing clustered ring enhancement (Figs. 3A, 3B, 3C, 6A, and 6B), it is thought that dynamic studies can be useful for evaluation of the vascularity of intraductal carcinoma. One physiopathologic explanation for clustered ring enhancement is that an intraductal carcinoma with an abundant blood supply exhibits a washout pattern, and the contrast medium that accumulated in the periductal stroma or ductal wall contributes to this phenomenon.
In contrast to segmental and ductal enhancement [12, 13, 27], the usefulness of focal and regional enhancement as BI-RADS descriptors remains unknown. We found no statistically significant independent association of any of the morphologic BI-RADS descriptors or clustered ring enhancement with benign and malignant lesions; this evaluation is not useful for differentiating between malignant and benign lesions. However, the presence of a combination of clumped internal architecture and clustered ring enhancement was statistically significant for the diagnosis of malignancy (p < 0.001). On the basis of these results, we suggest that the presence of clumped internal architecture and clustered ring enhancement should first be evaluated in cases showing localized nonsegmental enhancement because the presence of these signs may be indicative of malignant dilated ducts. In addition to the morphologic assessment, the detection of a washout pattern was useful for the diagnosis of malignancy.
In our study, the positive predictive value of the washout pattern for the diagnosis of malignancy was 94%. However, Liberman et al. [12] reported that visually assessed kinetic features were not significant predictors of breast carcinoma. The reasons for these discrepant observations cannot be confirmed; however, they are possibly related to differences in the protocols used for the dynamic scanning. We assessed the kinetic characteristics of the tumor visually by comparing the signal intensity on dynamic scans obtained during the first and third phases [10]. The scans of the third phase were acquired at 4 minutes after the start of IV administration of the contrast material. This short period until the delayed phase might explain the infrequent observation of a washout pattern in benign lesions. Therefore, we concluded that an interval of 4 minutes for obtaining scans of the delayed phase was not too short to evaluate the hemodynamics of hypervascular tumors.
Our study has several limitations. First, only a relatively small group of 26 benign lesions was evaluated. Second, this study was a retrospective review of histopathologically proven lesions; it did not include histopathologically unproven cases under follow-up. Therefore, further investigations and evaluations are needed to refine the diagnostic usefulness of clustered ring enhancement reported in this study. Third, clustered ring enhancement is believed to be an enhancement effect of the periductal stroma and ductal wall but a possibility that intraductal cancer cells are involved in the enhancement cannot be ruled out. Contrasting pathologic studies are warranted in this area in the future.
In conclusion, the features with the highest positive predictive value for the diagnosis of malignancy were segmental distribution, clustered ring enhancement, and a washout pattern in lesions showing non-masslike enhancement. Clustered ring enhancement is thought to be a useful sign to differentiate between benign and malignant lesions, in addition to the BI-RADS MRI descriptors. Moreover, we found that the combination of a clumped internal architecture and clustered ring enhancement might also be a useful predictor of malignancy in lesions showing focal and regional enhancement.
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