Breast MRI Using the VIBE Sequence: Clustered Ring Enhancement in the Differential Diagnosis of Lesions Showing Non-Masslike Enhancement

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Tozaki et al. Breast MRI Using the VIBE Sequence Tozaki et al.

W O M E N ’S IMAGING

Mitsuhiro Tozaki1,2 Takao Igarashi2 Kunihiko Fukuda2 Tozaki M, Igarashi T, Fukuda K

Breast MRI Using the VIBE Sequence: Clustered Ring Enhancement in the Differential Diagnosis of Lesions Showing Non-Masslike Enhancement OBJECTIVE. The purpose of this study was to assess the frequency of a finding in which minute ring enhancements are clustered (defined as clustered ring enhancement) in lesions showing non-masslike enhancement and to evaluate the clinical usefulness of this sign, in addition to that of the BI-RADS MRI descriptors, in the differentiation between benign and malignant lesions. 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. reast MRI has emerged as a highly sensitive technique for imaging of breast tumors, although its specificity remains variable, ranging from 30% to 80% [1–6]. To improve the specificity, detailed assessment of the lesion morphology using 3D MRI and of the kinetic patterns depicted using dynamic protocols may be useful [7]. 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 breathhold 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 find-

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Keywords: BI-RADS, breast, breast cancer, MRI, VIBE sequence DOI:10.2214/AJR.05.0881 Received May 24, 2005; accepted after revision August 17, 2005. 1Present address: Division of Diagnostic Imaging,

Breast Center, Kameda Medical Center, 929 Higashi-cho, Kamogawa, Chiba, Japan 296-8602. Address correspondence to M. Tozaki ([email protected]). 2Department

of Radiology, The Jikei University School of Medicine, 3-25-8 Nishi-Shimbashi, Minato-ku, Tokyo, Japan 105-8461.

AJR 2006; 187:313–321 0361–803X/06/1872–313 © American Roentgen Ray Society

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ing 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 nonmasslike 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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Tozaki et al. Fig. 1—54-year-old woman with suspicious microcalcifications on mammography. A, Coronal first contrastenhanced T1-weighted MR image of left breast shows regional enhancement in upper outer quadrant (arrow). Lesion indicates heterogeneous enhancement inside of which minute ring enhancements are seen clustered (clustered ring enhancement). B, Photomicrograph of histopathologic specimen shows ductal carcinoma in situ (DCIS) with intraluminal necrosis and microcalcifications. Clustered ring enhancement corresponds to periductal stroma. However, intraductal cancer cell involvement in enhancement cannot be ruled out.

Materials and Methods Patients From July 2000 to July 2004, breast MRI was performed in 568 patients at our institute. In this study, a retrospective review of 61 consecutive histopathologically diagnosed breast lesions showing non-masslike enhancement was performed. The patients ranged in age from 25 to 79 years, with a mean age of 48 years. 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.

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A

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 × 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 × 218; receiver bandwidth, 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

B

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. 1 and 2). The kinetic enhancement parameters were evaluated as exhibiting washout, plateau, or persistent characteristics. The findings were visually assessed by comparing the signal intensity on the first and third dynamic images, acquired at 60 seconds and 4 minutes, respectively [14]. By definition, any decline in signal intensity between 60 seconds and 4 minutes

AJR:187, August 2006

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Breast MRI Using the VIBE Sequence

A

B

Fig. 2—48-year-old woman who presented with bloody nipple discharge of left breast. No microcalcifications were detectable on mammography. A, Coronal first contrast-enhanced T1-weighted MR image shows segmental heterogeneous enhancement in lower region of left breast (arrow). B, Transverse third contrast-enhanced T1-weighted MR image shows clustered ring enhancement (arrow). C, Photomicrograph of histopathologic specimen shows ductal carcinoma in situ (DCIS) with micropapillary pattern. Clustered ring enhancement corresponds to periductal stroma.

C after the injection of contrast material is considered a washout enhancement pattern. Plateau enhancement was considered to be stabilized enhancement without change in signal intensity between 60 seconds and 4 minutes. Persistent enhancement was considered to be an increase in signal intensity throughout the dynamic period. Each lesion was characterized according to the strongest enhancement pattern visible over the entire lesion. 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.

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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.

Results Table 1 shows the frequencies of the morphologic parameters, including clustered ring enhancement and the kinetic patterns. The most frequent morphologic finding among the malignant lesions was heterogeneous internal enhancement (69%) (p = 0.003), followed in frequency by a 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) (Figs. 3 and 4). Regarding the kinetic enhancement, the most frequent pattern observed in the malignant lesions was a washout pattern (49%); alternately, 88% of the benign lesions (p < 0.001) exhibited a persistent pattern (Fig. 5). The features with the highest positive predictive value for carcinoma were a segmental distribution (100%), clustered ring enhancement (96%), and a washout pattern (94%).

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Tozaki et al. Fig. 3—42-year-old woman with suspicious density on mammography. A, Sagittal multiplanar reconstruction of first contrast-enhanced T1weighted MR image shows focal enhancement in upper region of left breast (arrow). B, Transverse multiplanar reconstruction of first contrast-enhanced T1weighted MR image shows nonenhancing internal septations (arrow). C, Transverse third contrast-enhanced T1weighted MR image shows heterogeneous internal enhancement with clustered ring enhancement (arrows). Histologic evaluation of lumpectomy specimen revealed 20-mm ductal carcinoma in situ (DCIS) within 5-mm invasive ductal carcinoma. Nonenhancing internal septations corresponded to normal gland tissue.

B

A

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 (Fig. 6). Furthermore, the washout pattern was observed in 55% of the malignant lesions showing clustered ring enhancement (12/22). 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 use-

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ful 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). Discussion Breast MRI has emerged as a highly sensitive technique for the diagnosis of breast tumors [15–20]. During the past 15 years, substantial research has been conducted to identify the most significant features on MR images of the breast useful for the diagnosis of breast cancer [10, 12, 13, 21–27]. According to the recently published BI-RADS MRI lexicon [11], the lesion configuration classified as mass enhancement (space-occupying lesion) or non-masslike enhancement is determined first. Many cases of DCIS are detected as non-masslike enhancement and show segmental or ductal distribution and a clumped internal architecture [12, 13].

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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 MorakkabatiSpitz 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 en-

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Breast MRI Using the VIBE Sequence

A

B Fig. 4—38-year-old woman with microcalcifications on mammography. A, Coronal first contrast-enhanced T1-weighted MR image of right breast shows focal enhancement in upper outer quadrant (arrow). B, Coronal first contrast-enhanced T1-weighted MR image of right breast shows clustered ring enhancement (arrow). C, Coronal third contrast-enhanced T1-weighted MR image shows persistent pattern (arrow). Lesion shows aggregate of enhancing foci in cobblestone pattern (clumped enhancement), and enhancing foci constitute ringlike enhancement pattern. This type of clustered ring enhancement is thought to be subtype of clumped enhancement. Histologic evaluation of excisional biopsy specimen revealed fibrocystic disease. Clustered ring enhancement corresponded to dilated ducts within microcalcifications.

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hancement (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 nonmasslike enhancement. The discrepancy may

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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 (Fig. 3). In this study, a washout pattern was observed in 49% of the malig-

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Tozaki et al.

B

A

C

Fig. 5—43-year-old woman with microcalcifications on mammography. A, Coronal first contrast-enhanced T1-weighted MR image of right breast shows regional heterogeneous enhancement (arrows). B, Transverse multiplanar reconstruction of first contrast-enhanced T1-weighted MR image shows regional heterogeneous enhancement without clustered ring enhancement (arrows). C, Transverse third contrast-enhanced T1-weighted MR image shows persistent enhancing region without clustered ring enhancement (arrows). Histologic evaluation of excisional biopsy specimen revealed fibrocystic disease.

nant 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

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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-spatialresolution 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 clus-

tered. “Clumped enhancement” of lexion BIRADS 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. 4 and 6); in the other, the lesion indicates heterogeneous enhancement inside of which minute ring enhancements are seen clustered (Figs. 1, 2, and 3). Almost all cases (91%) belonged to the latter group. Among the former, some show the ringlike enhancement pattern early (Fig. 4); in others, washout produces the ringlike enhancement pattern (Fig. 6). To avoid confusion in terminology, it makes

AJR:187, August 2006

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Breast MRI Using the VIBE Sequence

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B

Fig. 6—40-year-old woman who presented with bloody nipple discharge of left breast. No microcalcifications were detectable on mammography. A, Transverse multiplanar reconstruction of first contrast-enhanced T1-weighted MR image shows segmental enhancement with clumped internal architecture (arrows). B, Transverse third contrast-enhanced T1-weighted MR image shows clustered ring enhancement after washout (arrows). This type of clustered ring enhancement is thought to be subtype of clumped enhancement. Histologic evaluation of mastectomy specimen revealed ductal carcinoma in situ (DCIS). One physiopathologic explanation is that intraductal carcinoma with abundant blood supply exhibits washout pattern and contrast medium that accumulates in periductal stroma or ductal wall contributes to this phenomenon.

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. 3 and 6), 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.

TABLE 1: Frequency of MRI Parameters in Non-Masslike Enhancement Benign (n = 26)

Malignant (n = 35)

pa

4 (15)

7 (20)

NS

Focal area

7 (27)

5 (14)

NS

Regional

5 (19)

4 (11)

NS

Segmental

0

19 (54)

< 0.001

Multiple regions

3 (12)

0

NS

Diffuse

7 (27)

0

0.003

Descriptor Distribution modifiers Ductal

Internal enhancement Homogeneous

2 (8)

1 (3)

NS

Heterogeneous

7 (27)

24 (69)

0.003

Stippled, punctate Clumped Clustered ring enhancement

13 (50)

0

< 0.001

4 (15)

10 (29)

NS

1 (4)

22 (63)

< 0.001

Kinetic pattern Persistent

23 (88)

10 (29)

< 0.001

Plateau

2 (8)

8 (23)

NS

Washout

1 (4)

17 (49)

< 0.001

Note—Numbers in parentheses are percentages. NS = not significant. a Chi-square test and Fisher’s exact test were used.

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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

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Tozaki et al. TABLE 2: Frequency of Clustered Ring Enhancement Descriptor

Benign (n = 26)

Malignant (n = 35)

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Internal enhancement Ductal Homogeneous

2

1

Clumped

2

6

Focal area

Benign (n = 12)

Malignant (n = 9)

pa

Heterogeneous

6

6

NS

Stippled, punctate

5

0

NS

Clumped

1

3

NS

1

5

NS

Descriptor Internal enhancement

Clustered ring enhancement Combination of internal enhancements

Heterogeneous

2

2 [2]

Heterogeneous enhancement with clustered ring enhancement

0

5

0.012

Stippled, punctate

4

0

Clumped enhancement and clustered ring enhancement

1

8

< 0.001

Clumped

1 [1]

3

12

1

< 0.001

Heterogeneous

4

4 [3]

Plateau

0

3

NS

Stippled, punctate

1

0

Washout

0

5

0.012

Regional

Heterogeneous

0

18 [16]

Clumped

0

1 [1]

Heterogeneous

1

0

Stippled, punctate

2

0

Multiple regions

Diffuse Stippled, punctate

6

0

Clumped

1

0

Kinetic pattern Persistent

Kinetic pattern Persistent

Segmental

23 [1]

10 [8]

Plateau

2

8 [2]

Washout

1

17 [12]

Note—Numbers in brackets indicate number of cases of clustered ring enhancement.

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 duc-

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TABLE 3: Frequency of MRI Parameters in Focal and Regional Enhancement

Note—NS = not significant. a Chi-square test and Fisher’s exact test were used.

tal 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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