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1 Breast Imaging Section, Memorial Sloan-Kettering Cancer Center, 1275 York
Ave., New York, NY 10021.
2 Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY
10021.
Received December 18, 2002;
accepted after revision January 22, 2003.
Address correspondence to L. Liberman
(libermal{at}mskcc.org).
Abstract
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MATERIALS AND METHODS. Retrospective review was performed of 427 nonpalpable, mammographically occult lesions that had MR imaging–guided needle localization and surgical biopsy. Lesions were reviewed by one radiologist who was unaware of the histologic outcomes and were classified according to a standardized lexicon. MR imaging and histologic findings of ductal enhancing lesions were reviewed.
RESULTS. Ductal enhancement accounted for 88 (21%) of 427 lesions and 88 (59%) of 150 nonmass lesions. Histologic finding in these 88 lesions were ductal carcinoma in situ (DCIS) in 18 (20%); infiltrating carcinoma in five (6%), including three with DCIS; lobular carcinoma in situ (LCIS) in nine (10%); atypical ductal hyperplasia in eight (9%); and benign in 48 (55%). Among the 48 benign lesions, the dominant histologic findings were fibrocystic change (n = 16); ductal hyperplasia (n = 8); fibrosis (n = 8); postbiopsy change (n = 5); benign breast tissue (n = 3); sclerosing adenosis (n = 2); and single cases of fibroadenoma, fibroadenomatoid change, lymph node, mastitis, papilloma, and radial scar. Factors associated with a trend toward a higher frequency of carcinoma included clumped enhancement (p = 0.05) and synchronous ipsilateral cancer (p = 0.07).
CONCLUSION. Ductal enhancement accounted for 21% of MR imaging–detected lesions that had biopsy and had a positive predictive value of 26%. Differential diagnosis of ductal enhancement includes carcinoma (usually DCIS); atypical ductal hyperplasia; LCIS; and benign findings such as fibrocystic change, ductal hyperplasia, and fibrosis.
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Ductal enhancement is nonmass enhancement in a line that points toward the nipple and may have branching, conforming to a breast duct [5]. Ductal enhancement may be seen in carcinoma, particularly ductal carcinoma in situ (DCIS) [6, 7]. This study was undertaken to determine the prevalence of ductal enhancement among MR imaging–detected lesions that had biopsy and to assess the histologic findings associated with ductal enhancement.
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Histologic findings in these 427 lesions were DCIS in 49 (11%), infiltrating carcinoma in 45 (10%), atypical ductal hyperplasia in 36 (8%), lobular carcinoma in situ (LCIS) in 35 (8%) (including six with atypical ductal hyperplasia), and benign in 262 (61%).
Breast MR Imaging Technique
At our institution, diagnostic MR imaging examinations were performed with
the patient prone in a 1.5-T commercially available system (Signa, General
Electric Medical Systems, Milwaukee, WI) using a dedicated surface breast
coil. Our imaging protocol includes a localizing sequence followed by a
sagittal T2-weighted fat-suppressed sequence (TR/TE, 4000/85). A
three-dimensional T1-weighted fat-suppressed fast spoiled gradient-echo
sequence (17/2.4; flip angle, 35°; bandwidth, 31.25 MHz) is then performed
before and three times after a rapid bolus injection of 0.1 mmol/L of
gadopentetate dimeglumine (Magnevist, Berlex, Wayne, NJ) per kilogram of body
weight, delivered through an indwelling IV catheter.
Image acquisition started after injection of contrast material and a saline bolus. Images were obtained sagittally for an acquisition time per volumetric acquisition under 3 min each. The total imaging time per breast including three acquisitions after contrast enhancement was approximately 20 min. Section thickness was between 2 and 3 mm without a gap using a matrix of 256 x 192 and a field of view of 18–22 cm. Frequency was in the anteroposterior direction. After the examination, the unenhanced images were subtracted from the first contrast-enhanced images on a pixel-by-pixel basis.
Interpretation of MR Imaging Examinations of the Breast in Clinical
Practice
In our practice, MR imaging examinations were interpreted by breast imaging
specialists using previously described criteria
[7,
8] in conjunction with clinical
history and other breast imaging studies, including mammograms and sonograms
when available. Level of suspicion was reported on a scale of 0–5 as
follows: 0, needs additional imaging evaluation; 1, no abnormal enhancement;
2, benign enhancement; 3, probably benign, recommend short-term follow-up
(specified as either at a different time in the patient's menstrual cycle or
in 6 months); 4, suspicious; or 5, highly suggestive of malignancy
[5].
MR Imaging–Guided Needle Localization Technique
Localization was performed using previously described methods
[9] with a dedicated surface
breast coil (OBC, MRI Devices, Waukesha, WI). The breast undergoing
localization was placed in a dedicated biopsy compression device using a
commercially available grid-localizing system (Biopsy-System [model no. NMR NI
160], MRI Devices, Waukesha, WI) with an MR-compatible needle and hookwire
(Tumor Localizer [18- or 20-gauge], Daum Medical, Schwerin, Germany; MRI
Breast Lesion Marking System [20-gauge], E-ZEM, Westbury, NY; or MReye
Modified Kopans Spring Hook Localization Needle [20-gauge], Cook, Bloomington,
IN).
Review of MR Images
For this study, diagnostic breast MR imaging examinations for 427
consecutive mammographically occult nonpalpable lesions that underwent MR
imaging–guided needle localization were reviewed by one radiologist with
12 years of experience as a breast imaging specialist who had previously
interpreted approximately 500 clinical breast MR imaging examinations. The
institution at which the study was performed is an academic center where more
than 30,000 mammograms, 1000 breast MR imaging examinations, and 1000 new
breast cancer cases were evaluated annually during the study period.
T2-weighted images, T1-weighted images obtained before injection of IV contrast material, T1-weighted images obtained within the first 2 min after IV contrast injection, and delayed images after IV contrast injection were posted by a breast imaging fellow on a PACS (picture archiving and communication system) monitor (General Electric Medical Systems) for review by the radiologist. The radiologist was not provided with the pathologic outcomes, clinical information, quantitative kinetic curves, or other breast imaging studies. The sagittal image best showing the lesion was presented to the radiologist, but the radiologist could page back and forth through sequential slices and adjust the window and level settings at the monitor.
Data recorded included lesion type (mass or nonmass), size, and signal intensity on T2-weighted images (hyperintense or not hyperintense). Visual analysis of the time course of enhancement after contrast injection was categorized as persistent (continued increase in signal over time), plateau (flat; signal intensity did not change over time after its initial rise), or washout (signal intensity decreased after its highest point from its initial rise) [2, 5, 10–12]. For ductal enhancing lesions, the internal enhancement pattern was classified as clumped (cobblestone-like enhancement, with occasional confluent areas), heterogeneous (non-uniform enhancement), or homogeneous (confluent, uniform enhancement) [5].
Patient, Lesion, and Breast Characteristics
Eighty-eight lesions were classified as ductal enhancement and constitute
the basis of this article. These 88 ductal enhancing lesions occurred in 80
women with a median age of 51 years (range, 33–79 years). Directed
sonography failed to show a sonographic correlate to the MR imaging finding in
45 lesions. In the remaining 43 lesions, directed sonography was not performed
at the discretion of the interpreting radiologist and treating clinician.
Hence, none of these lesions had a known sonographic correlate.
The median interval between mammography and diagnostic MR imaging was 22 days (range, 0–100 days); none of these 88 lesions had a mammographic correlate. Mammographic parenchymal density [13] was class 4 (dense) in 18 (20%), class 3 (heterogeneously dense) in 57 (65%), class 2 (scattered fibroglandular densities) in 12 (14%), and class 1 (predominantly fat) in one (<1%).
Data Collection and Analysis
Histologic findings of ductal enhancing lesions were reviewed and
correlated with MR imaging interpretations. Results of postoperative imaging,
when available, were reviewed. Data were entered into spreadsheet software
(Excel, Microsoft, Redmond, WA). Statistics were analyzed using statistical
software (Epi-Info, Centers for Disease Control and Prevention, Atlanta, GA)
with the chisquare and Fisher's exact tests.
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Among the 18 DCIS lesions evident as ductal enhancement, nuclear grade was low in five, intermediate in nine, and high in four. Histologic type was cribriform (n = 3), cribriform and papillary (n = 3), cribriform and apocrine (n = 2), cribriform and solid (n = 2), cribriform and micropapillary (n = 2), papillary (n = 1), papillary and solid (n = 1), apocrine (n = 1), micropapillary (n = 1), micropapillary and clinging (n = 1), and flat (n = 1). Necrosis was absent in 10, minimal in four, moderate in three, and extensive in one.
Among the 48 benign ductal enhancing lesions, dominant histologic findings were fibrocystic changes (n = 16); ductal hyperplasia (n = 8); fibrosis (n = 8); postbiopsy change (n = 5); benign breast tissue (n = 3); sclerosing adenosis (n = 2); and single cases of fibroadenoma, fibroadenomatoid change, lymph node, mastitis, papilloma, and radial scar.
Lesion Characteristics
Prevalence and positive predictive value of lesion characteristics in the
88 ductal enhancing lesions are shown in
Table 1. There was a trend
toward high frequency of carcinoma in ductal enhancing lesions that were
clumped as opposed to those that were not clumped (35% vs 14%, p =
0.05). The likelihood of cancer in ductal enhancing lesions did not differ
significantly as a function of visual kinetic pattern, T2 signal intensity,
lesion size, or mammographic parenchymal density
(Table 1).
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Clinical Features
Prevalence and positive predictive value of clinical features for these 88
ductal enhancing lesions are shown in Table
2. There was a trend toward higher frequency of carcinoma among
ductal enhancing lesions in women with synchronous ipsilateral cancer than in
women without synchronous ipsilateral cancer (50% vs 22%, p = 0.07).
The likelihood of cancer in ductal enhancing lesions did not differ
significantly as a function of family history of breast cancer, indication for
MR imaging, menopausal status, or personal history of breast cancer
(Table 2).
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Follow-Up
Postoperative MR imaging was performed to evaluate 37 (42%) of 88 lesion
sites at a median of 16 weeks (range, 3–61 weeks) after surgery. An
additional 15 (17%) of 88 lesion sites had subsequent mastectomy as treatment
for the malignant ductal enhancing lesion (n = 11) or for a
synchronous ipsilateral cancer (n = 4). Among the four women with
benign ductal enhancing lesions who had subsequent mastectomy, none had cancer
found at the site of the ductal enhancing lesion. In an additional 16 (18%) of
88 lesion sites, follow-up mammograms obtained at a median of 10 months
(range, 6–22 months) showed no suspicious findings. The remaining 20
(23%) of 88 lesion sites had neither imaging nor mastectomy follow-up.
Postoperative MR imaging suggested lesion retrieval or sampling in 36 (97%) of 37 lesion sites. The histologic findings in these 36 lesions, in which biopsy was confirmed by postoperative MR imaging, were comparable to those in all 88 lesions in the study (Table 3). In one 64-year-old woman who presented with occult left breast cancer in an axillary lymph node, MR imaging–guided needle localization and surgical biopsy of an area of clumped ductal enhancement yielded benign breast tissue with fibrosis. Postoperative MR imaging indicated that the lesion had not been removed. Repeated MR imaging–guided needle localization yielded ductal hyperplasia, fibrocystic change, and metastatic cancer in an intramammary lymph node.
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Few studies address the positive predictive value of ductal enhancement among MR imaging–detected breast lesions. Morakkabati et al. [18] reported ductal enhancement in five (1%) of 500 MR imaging examinations; among these five ductal enhancing lesions, biopsy revealed DCIS in one (20%) and benign findings in four (80%), including fibrocystic change in three and papilloma in one. In a study of MR imaging–detected lesions that underwent biopsy, ductal enhancement had a positive predictive value of 24% [7]. All malignant ductal enhancing lesions in these two prior reports were DCIS (Table 3) [7, 18].
In our study of lesions that had MR imaging–guided localization and surgical biopsy, we found that ductal enhancement had a prevalence of 21% and a positive predictive value of 26%. The 26% positive predictive value of ductal enhancement in our study should be interpreted in the context of the previously reported 30–68% positive predictive values of ductal distribution of calcifications on mammography [15, 16] and 51% positive predictive value of ductal extension on sonography [17]. The 26% positive predictive value of ductal enhancement in our study is comparable to the 20–24% range of positive predictive values for ductal enhancement in previous reports of breast MR imaging [7, 18] (Table 3).
Among the malignant ductal enhancing lesions in our study, most either were pure DCIS (Figs. 1A, 1B, 2, 3) or had DCIS in association with infiltrating cancer. In prior reports, ductal enhancement was found in 38–60% of DCIS lesions seen at MR imaging [6, 7]. Although DCIS may present as ductal enhancement, other MR patterns have been described in DCIS, including segmental or regional nonmass enhancement in 30–31% and mass enhancement in 10–31% [6, 7]. Further work is necessary to determine the patterns of DCIS at MR imaging and to correlate these patterns with histologic subtype.
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More than half (55%) of our ductal enhancing lesions were benign without high-risk findings. Specific benign processes such as fibrocystic change, ductal hyperplasia, and fibrosis can occur along ducts and give a pattern of ductal enhancement (Figs. 4A, 4B, 5A, 5B, 6A, 6B). With the increasing use of MR imaging and MR imaging–guided biopsy, it is essential to recognize the specific histologic findings associated with different MR imaging patterns because imaging–histologic correlation is necessary to confirm lesion sampling [19]. Our data indicate that benign diagnoses such as fibrocystic change, ductal hyperplasia, and fibrosis, which are not common causes of ductal distribution of calcifications at mammography, may be concordant with a pattern of ductal enhancement at MR imaging.
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Among ductal enhancing lesions, 19% yielded high-risk findings including atypical ductal hyperplasia, LCIS, or both. Atypical ductal hyperplasia is a premalignant lesion that grows in a ductal distribution [20]. We found that atypical ductal hyperplasia may have MR imaging findings indistinguishable from cancer (Fig. 7A, 7B), just as it can have mammographic patterns indistinguishable from those of malignancy [21]. LCIS, a risk factor for subsequent development of cancer in either breast, is characterized histologically by a uniform population of small round cells that fills and expands the lobule [22]. LCIS may involve ducts, which can result in a pattern of ductal enhancement (Fig. 8A, 8B). Further study correlating MR imaging findings and histology in women with LCIS is needed.
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Carcinoma was more frequent among ductal enhancing lesions that were clumped (35% malignant) rather than not clumped (14% malignant). Clumped enhancement may correlate with irregular cell growth, suggestive of malignancy. Other lesion features such as lesion size, T2 signal intensity, and visual kinetic pattern could not be used to distinguish benign from malignant ductal enhancing lesions, reinforcing the necessity of biopsy to determine lesion histology. There was a trend toward a higher frequency of cancer among ductal enhancing lesions in women with synchronous ipsilateral cancer (50% malignant) than in women without such history (22% malignant), but no other clinical factors were significant predictors of carcinoma among ductal enhancing lesions in our high-risk women [23].
Our study has limitations. For women who did not have postoperative MR
imaging, lesion retrieval cannot be confirmed. Furthermore, the MR images were
reviewed by one radiologist; there is interobserver variability in describing
MR images [4], as has been
noted for mammograms [16,
24] and sonograms
[25]. Ikeda et al.
[4] evaluated reproducibility
of terms in an earlier version of the lexicon using the kappa statistic, with
a kappa value of 0–0.20, 0.21–0.4, 0.41–0.6, 0.61–0.8,
and 0.81–1.0 indicating slight, fair, moderate, substantial, and near
perfect agreement, respectively
[26]. Ikeda et al.
[4] found fair (
= 0.35)
agreement in use of the term "linear branching" but only slight
agreement in use of the term "linear." Assessment of interobserver
variability in use of the term "ductal enhancement" and other
terms in the current lexicon
[5] is necessary.
In conclusion, ductal enhancement accounted for 21% of MR imaging–detected lesions that had biopsy and had a positive predictive value of 26%. The differential diagnosis for ductal enhancement includes DCIS; infiltrating carcinoma; atypical ductal hyperplasia; LCIS; and benign findings such as fibrocystic change, ductal hyperplasia, and fibrosis. The frequency of cancer may be lower among lesions showing ductal enhancement at MR imaging than among lesions evident as ductal distribution of calcifications on mammography or ductal extension on sonography. Further study of specific histologic finding associated with different breast MR imaging patterns is necessary to refine our criteria for biopsy and enable appropriate imaging–histologic correlation to confirm lesion sampling if biopsy is performed.
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