DOI:10.2214/AJR.05.0881
AJR 2006; 187:313-321
© American Roentgen Ray Society
Breast MRI Using the VIBE Sequence: Clustered Ring Enhancement in the Differential Diagnosis of Lesions Showing Non-Masslike Enhancement
Mitsuhiro Tozaki1,2,
Takao Igarashi2 and
Kunihiko Fukuda2
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
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.
Keywords: BI-RADS • breast • breast cancer • MRI • VIBE sequence
Introduction
Breast 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 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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Fig. 1A —54-year-old woman with suspicious microcalcifications on
mammography. Coronal first contrast-enhanced 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).
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Fig. 1B —54-year-old woman with suspicious microcalcifications on
mammography. 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.
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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.
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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Fig. 2A —48-year-old woman who presented with bloody nipple discharge
of left breast. No microcalcifications were detectable on mammography. Coronal
first contrast-enhanced T1-weighted MR image shows segmental heterogeneous
enhancement in lower region of left breast (arrow).
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Fig. 2B —48-year-old woman who presented with bloody nipple discharge
of left breast. No microcalcifications were detectable on mammography.
Transverse third contrast-enhanced T1-weighted MR image shows clustered ring
enhancement (arrow).
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Fig. 2C —48-year-old woman who presented with bloody nipple discharge
of left breast. No microcalcifications were detectable on mammography.
Photomicrograph of histopathologic specimen shows ductal carcinoma in situ
(DCIS) with micropapillary pattern. Clustered ring enhancement corresponds to
periductal stroma.
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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 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.
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.
3A,
3B,
3C,
4A,
4B, and
4C). 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 (Figs.
5A,
5B, and
5C).
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Fig. 3A —42-year-old woman with suspicious density on mammography.
Sagittal multiplanar reconstruction of first contrast-enhanced T1-weighted MR
image shows focal enhancement in upper region of left breast
(arrow).
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Fig. 3B —42-year-old woman with suspicious density on mammography.
Transverse multiplanar reconstruction of first contrast-enhanced T1-weighted
MR image shows nonenhancing internal septations (arrow).
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Fig. 3C —42-year-old woman with suspicious density on mammography.
Transverse third contrast-enhanced T1-weighted 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.
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Fig. 4A —38-year-old woman with microcalcifications on mammography.
Coronal first contrast-enhanced T1-weighted MR image of right breast shows
focal enhancement in upper outer quadrant (arrow).
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Fig. 4C —38-year-old woman with microcalcifications on mammography.
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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Fig. 5B —43-year-old woman with microcalcifications on mammography.
Transverse multiplanar reconstruction of first contrast-enhanced T1-weighted
MR image shows regional heterogeneous enhancement without clustered ring
enhancement (arrows).
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Fig. 5C —43-year-old woman with microcalcifications on mammography.
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.
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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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Fig. 6A —40-year-old woman who presented with bloody nipple discharge
of left breast. No microcalcifications were detectable on mammography.
Transverse multiplanar reconstruction of first contrast-enhanced T1-weighted
MR image shows segmental enhancement with clumped internal architecture
(arrows).
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Fig. 6B —40-year-old woman who presented with bloody nipple discharge
of left breast. No microcalcifications were detectable on mammography.
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.
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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).
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].
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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Abstract
Introduction
