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1 All authors: Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
revised November 11, 2001;
accepted after revision December 21, 2001.
Presented at the annual meeting of the American Roentgen Ray Society,
Atlanta, April-May 2002.
Abstract
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MATERIALS AND METHODS. Retrospective review was performed of 100 consecutive solitary MR imaging—detected breast lesions that had MR imaging—guided needle localization and surgical excision. We described lesions, using terms found in a proposed breast MR imaging lexicon. Histologic findings were reviewed.
RESULTS. Carcinoma was identified in 25 lesions (25%), including ductal carcinoma in situ (DCIS) in 13 (52%) and infiltrating carcinoma in 12 (48%). Carcinoma was found in 15 (25%) of 60 masses versus 10 (25%) of 40 nonmass lesions; most malignant masses (73%) were infiltrating carcinoma, whereas most malignant nonmass lesions (90%) were DCIS. The features with the highest PPV were spiculated margin (80% carcinoma), rim enhancement (40% carcinoma), and irregular shape (32% carcinoma) for mass lesions and segmental (67% carcinoma) or clumped linear and ductal enhancement (31% carcinoma) for nonmass lesions. Visually assessed kinetic patterns were not significant predictors of carcinoma, but washout was present in 70% of infiltrating carcinomas versus 9% of DCIS lesions (p < 0.01). Carcinoma was present in 17 (19%) of 88 lesions classified as suspicious versus eight (67%) of 12 lesions classified as highly suggestive of malignancy (p = 0.001).
CONCLUSION. Among MR imaging—detected breast lesions referred for biopsy, carcinoma was found in 25%, of which half were DCIS. Features with the highest PPV were spiculated margin, rim enhancement, and irregular shape for mass lesions and segmental or clumped linear and ductal enhancement for nonmass lesions. Final assessment categories were significant predictors of carcinoma.
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Patient, Lesion, and Breast Characteristics
These 100 lesions that had MR imaging—guided needle localization
occurred in 97 women of median age of 49 years (range, 28-75 years). Median
lesion size was 1.3 cm (range, 0.2-6.3 cm). Directed sonography failed to show
a sonographic correlate to the MR imaging findings in 63 lesions. In the
remaining 37 lesions, directed sonography was not performed at the discretion
of the interpreting radiologist and treating clinician. Hence, none of these
100 lesions had a known sonographic correlate. Mammographic parenchymal
density [5] was class 4 (dense)
in 21 lesions (21%), class 3 (moderately dense) in 59 (59%), class 2 (mildly
dense) in 19 (19%), and class 1 (fatty) in one (1%).
Breast MR Imaging Technique
At our institution, diagnostic MR imaging was 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 sequence included a localizing sequence followed by a sagittal
fat-suppressed T2-weighted sequence (TR/TE, 4000/85). A T1-weighted
three-dimensional fat-suppressed fast spoiled gradient-echo (17/2.4; flip
angle, 35°; bandwidth, 31.25 MHz) sequence was 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 contrast material injection and saline bolus. Images were obtained sagittally, for an acquisition time per volumetric acquisition of less than 2 min each. Total imaging time per breast, including three enhanced acquisitions, was approximately 15 min. Section thickness was 2 mm without a gap, using a matrix of 256 x 192 and a field of view of 16-18 cm. Frequency was in the anteroposterior direction. After the examination, the unenhanced images were subtracted from the first enhanced images on a pixel-by-pixel basis.
Interpretation of Breast MR Imaging in Clinical Practice
In our practice, MR imaging examinations were interpreted by breast imaging
specialists 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 (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).
MR imaging—detected lesions referred for biopsy primarily included masses with spiculated or irregular margins, irregular shape, or heterogeneous or rim enhancement and nonmass lesions showing linear or segmental enhancement. Other lesions were referred for biopsy at the discretion of the interpreting radiologist in conjunction with clinical history and other imaging studies. Tiny (1-mm) foci of enhancement or diffuse stippled enhancement generally did not prompt biopsy. Classification was based primarily on lesion morphology; however, kinetic features were visually assessed on the three enhanced image acquisitions, with quantitative kinetic curves generated in specific cases at the request of the interpreting radiologist.
MR Imaging—Guided Needle Localization Technique
Localization was performed using previously described methods
[6]. Informed consent was
obtained for all needle localization procedures. The patient was positioned
prone with both breasts in a dedicated surface breast coil (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 No. NMR NI 160, MRI Devices) or a slightly modified
design of the commercially available model.
An axial localizing T1-weighted sequence was performed. The volume of interest was selected to include the compression device, and a vitamin E marker was placed over the expected lesion site. Gadopentetate dimeglumine, 0.1 mmol/L per kilogram of body weight, was injected IV as a rapid bolus injection through an indwelling IV catheter, and acquisition of sagittal images started immediately after contrast injection. Time of acquisition, usually less than 1 min, varied with breast size and area covered.
After we reviewed images at the console, a cursor was placed over the lesion on the monitor. The spatial relationships between the skin surface, vitamin E marker, and lesion were determined, and the skin entry site and lesion depth were calculated. The patient was then withdrawn from the magnet, a mark was made on the skin overlying the lesion, and the skin was cleansed with alcohol and anesthetized with 1-2 mL of 1% lidocaine hydrochloride (Xylocaine; Astra USA, Westborough, MA).
A needle guide (Biopsy-System No. NMR NI 160, MRI Devices) was inserted into the grid hole overlying the anesthetized area, and an MR-compatible needle and hookwire (Tumor Localizer, 18 or 20 gauge, Daum Medical, Schwerin, Germany; MRI Breast Lesion Marking System, 20 gauge, E-Z-EM, Westbury, NY; MReye Modified Kopans Spring Hook Localization Needle, 20 gauge, Cook, Bloomington, IN) were placed into the needle guide and advanced to the desired depth, approximately 0.5-1.0 cm deep in relation to the lesion. Sagittal contrast-enhanced T1-weighted images were obtained to document the location of the needle, which was evident as a low-signal-intensity structure with adjacent susceptibility artifact.
After the needle tip was accurately positioned, the wire was deployed by advancing the wire to the mark indicating that the tip had emerged from the needle. The needle was then removed, leaving the wire in place, and a final series of T1-weighted contrast-enhanced images were obtained to document the wire position. After localization, a two-view mammogram was obtained. These films were labeled, a labeled diagram was drawn, and the patient took the films and diagram to the operating suite for use during surgery. Specimen radiography, performed in 17 lesions, showed retrieval of the localizing wire in all cases.
Lesion retrieval was confirmed by imaging—histologic correlation in all cases and by postoperative MR imaging in selected cases. Postoperative MR imaging was performed in 24 lesions (18 benign lesions and six MR imaging—detected cancers) at a median of 5 months (range, 1-13 months) after surgery. Postoperative MR imaging confirmed lesion retrieval in all 18 benign lesions and in five of six MR imaging—detected cancers. In one lesion yielding ductal carcinoma in situ (DCIS) at MR imaging—guided needle localization, postoperative MR imaging findings suggested partial excision with possible residual disease; reexcision showed residual microscopic DCIS at the biopsy site.
Data Collection and Analysis
For this study, diagnostic breast MR imaging for 100 consecutive, solitary,
mammographically occult nonpalpable lesions that underwent MR
imaging—guided needle localization were reviewed by one radiologist with
11 years of experience as a breast imaging specialist, who had previously
interpreted approximately 300 clinical breast MR imaging examinations. The
institution at which the study was performed is an academic center where more
than 30,000 mammograms, 500 breast MR imaging examinations, and 1000 new
breast cancer cases were evaluated annually during the study period.
T2-weighted images, T1-weighted unenhanced images, and T1-weighted images obtained within the first 2 min after IV contrast injection in all cases were posted by a breast imaging fellow on the PACS (picture archiving and communication system) workstation (General Electric Medical Systems) for review by the radiologist. In 78 cases, two subsequent enhanced T1-weighted images were also available and posted for review. The radiologist was not provided with pathologic outcome, 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 workstation.
Data recorded included lesion size, signal intensity on T2-weighted images (hyperintense vs not hyperintense), and other morphologic features and final assessment categories as described in the proposed breast MR imaging lexicon (Table 1). In the 78 cases with a total of three enhanced T1-weighted images available, visual analyses of the time course of enhancement in these three images were performed and categorized in accordance with lexicon terminology as "progressive" (increasing signal intensity throughout the dynamic period), "plateau" (stabilized enhancement without change in signal intensity between the initial and subsequent enhanced images), or "washout" (abrupt decline in signal intensity after the initial enhanced images) [4, 7,8,9] (Table 1).
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After we recorded these data, histologic findings were reviewed and correlated with MR imaging interpretations. Data were entered into a computerized spreadsheet (Excel; Microsoft, Redmond, WA). Statistical analysis was performed using computerized statistics software (Epi-Info; Centers for Disease Contro and Prevention, Atlanta, GA) with the chi-square and Fisher's exact tests.
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Lesions were masses in 60 (60%) and nonmass enhancement in 40 (40%). Carcinoma was found in 15 (25%) of 60 masses versus 10 (25%) of 40 nonmass enhancing lesions (p = 0.81). Eleven (73%) of 15 malignant masses were infiltrating carcinomas, whereas nine (90%) of 10 malignant nonmass lesions were DCIS (p < 0.004). Among 13 MR imaging—detected DCIS lesions, nine (69%) were evident as nonmass enhancement, and four (31%) were evident as masses. Eleven (92%) of 12 MR imaging—detected infiltrating carcinomas were evident as masses, and one (8%) was evident as a nonmass enhancement.
Masses
Among masses, the features with the highest PPV were spiculated margin (80%
carcinoma), rim enhancement (40% carcinoma), and irregular shape (32%
carcinoma) (Table 2 and Figs.
1 and
2). There was a significantly
higher frequency of carcinoma among masses with spiculated rather than
nonspiculated margins (80% vs 20%, p = 0.01). The spiculated mass
yielding benign histologic findings represented a radial scar at surgery.
Carcinoma was present in 22% of masses with irregular margins and in 17% of
smoothly marginated masses.
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The frequency of carcinoma was higher among masses with irregular as opposed to lobular shape (32% vs 13%, p = 0.17) and among masses with rim enhancement as opposed to other patterns of enhancement (40% vs 24%, p = 0.59), but these differences did not achieve statistical significance.
Nonmass Enhancement
Among nonmass enhancing lesions, the PPV was highest for segmental
enhancement (67% carcinoma) (Fig.
3) and clumped linear and ductal enhancement (31% carcinoma)
(Fig. 4)
(Table 3). There was a
significantly higher frequency of carcinoma among nonmass lesions described as
clumped compared with those that were not clumped (9/22 = 41% vs 1/18 = 6%,
p = 0.01) (Table 3).
Clumped enhancement was present in eight (62%) of 13 MR imaging—detected
DCIS lesions and in eight (89%) of nine DCIS cases identified in nonmass
lesions (Table 3 and Figs.
3,4,5).
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Visual Assessment of Kinetic Patterns
Among 78 lesions with kinetic data available, the most common pattern was
plateau, present in 64% (Table
4). Carcinoma was present in 33% of lesions that showed washout
versus 24% of lesions that had other kinetic patterns (p = 0.33)
(Table 4). Infiltrating
carcinoma was present in 29% of lesions with washout versus 6% of lesions
without washout (p < 0.01). DCIS was present in 4% of lesions with
washout versus 19% of lesions without washout (p = 0.16). A washout
pattern was present in 70% of infiltrating carcinomas versus 9% of DCIS
lesions (p < 0.01) (Table
4).
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Lesion Size
Carcinoma was present in 29% of lesions measuring 1 cm or larger at maximal
diameter versus 18% of lesions smaller than 1 cm (p = 0.34)
(Table 5). The proportion of
cancers that were infiltrating did not differ significantly for lesions that
were 1 cm or larger as opposed to smaller lesions (39% vs 71%, p =
0.20).
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T2-Weighted Images
Carcinoma was present in 16% of lesions that were hyperintense on
T2-weighted images versus 28% of lesions that were not hyperintense on
T2-weighted images (p = 0.35)
(Table 5). No significant
difference was observed in the proportion of cancers that were infiltrating
among lesions that were hyperintense as opposed to those that were not
hyperintense on T2-weighted images (75% vs 43%, p = 0.32).
Final Assessment Categories
Carcinoma was present in 19% of lesions classified as suspicious versus 67%
lesions classified as highly suggestive of malignancy (p = 0.001)
(Table 5). A designation of
"highly suggestive of malignancy" was given to 42% of infiltrating
carcinomas versus 23% DCIS lesions (p = 0.41).
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A lexicon is being developed for breast MR imaging [4], but few data address the PPV of MR imaging features. In previous studies, the MR imaging features with the highest PPV were spiculated margin (77-95% cancer), irregular shape (80-83% cancer), linear and ductal enhancement (67-86% carcinoma), and rim enhancement in the presence of central lesion enhancement (79-92%) [9, 13,14,15,16]. Smooth borders were associated with benignity in 97-100% of cases in these prior reports [9, 13,14,15,16]. A limitation of these studies is that they included patients with mammographic or palpable abnormalities, potentially representing a biased sample.
Our study is the first, to our knowledge, to present the PPV of features in lesions detected solely on breast MR imaging. Carcinoma was found in 25% of our MR imaging—detected lesions. This 25% PPV is within the 9-47% range of PPVs reported for mammographically guided needle localization [17] and may have been higher if we had included lesions with mammographic or sonographic correlates [18]. Among our MR imaging—detected lesions referred for biopsy, 60% were masses, and 40% were nonmass enhancing lesions. Both masses and nonmass lesions had a 25% frequency of carcinoma, but most malignant masses were infiltrating carcinoma, whereas most malignant nonmass lesions were DCIS. These findings are analogous to those of prior reports of suspicious mammographic lesions, in which most malignant masses represented infiltrating carcinoma, whereas most malignant calcifications represented DCIS [10].
The feature with the highest PPV for malignancy in our study was spiculated margins, which had a PPV of 80%: four of five spiculated masses represented carcinoma, all four of which were infiltrating cancers. This finding is consistent with the 70-80% frequency of carcinoma among spiculated mammographically detected masses referred for biopsy [10]. Although there was a higher frequency of carcinoma among masses with spiculated as opposed to nonspiculated borders, spiculated margins were present in only four (27%) of 15 malignant masses; irregular margins were present in eight (53%) of 15 and smooth margins in three (20%) of 15 malignant masses.
We found carcinoma in 17% of smoothly marginated masses (Fig. 6A,6B). Smooth margins, associated with a 2% likelihood of cancer on mammography [19, 20], may not be a reliable indicator of benignity on MR imaging for several reasons. First, the patient population undergoing MR imaging is at high risk [2]. Second, the perception of margin smoothness on MR imaging is dependent on technical factors, including spatial resolution and window and level settings [21]. Third, the histologic correlate of the visually perceived margin is different for mammography (in which the margin represents the interface between the lesion and the adjacent parenchyma) than for contrast-enhanced MR imaging (in which the margin represents the interface between the area of vascularity and the surrounding tissue) [22, 23]. We therefore cannot assume that "probably benign" mammographic features such as smooth margins will necessarily be "probably benign" on breast MR imaging.
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Mass shape and internal enhancement patterns were not significant predictors of the likelihood of carcinoma. We found, as did Nunes et al. [13, 14], that irregular shape and rim enhancement were associated with a higher frequency of carcinoma than other shape and enhancement features, but these differences did not achieve statistical significance. Nonenhancing internal septations were present in one of our cases, which contained a fibroadenoma at surgery. Nonenhancing internal septations, described in 40-64% of fibroadenomas, correlate with collagenous bands at histologic analysis [24]. Although nonenhancing internal septations suggest fibroadenoma, they may be seen in carcinoma, particularly in a mass with irregular margins [14].
Among nonmass lesions, the frequency of carcinoma was highest in segmental enhancement (67% carcinoma) and clumped linear and ductal enhancement (31% carcinoma). Previous studies of breast MR imaging have reported PPVs of 67-86% for linear enhancement [13, 14] and 58% for segmental or linear enhancement [25]. These findings are analogous to results with nonmass (calcification) lesions identified on mammography, in which the frequency of carcinoma was highest for segmental distribution (74% carcinoma) and linear distribution (68% carcinoma) [10]. We found that the MR imaging pattern of "clumped" enhancement had a high PPV: nine (41%) of 22 lesions described as clumped were carcinoma, of which eight (89%) were DCIS. The clumped pattern of beaded or cobblestonelike enhancement in a duct may represent irregularly heaped-up tumor cells expanding a duct containing DCIS.
DCIS accounted for approximately half (52%) of the cancers encountered in our MR imaging—detected lesions. The high proportion of DCIS in our study likely reflects our high-risk patient population and the emphasis on morphologic rather than kinetic analysis. We found that visually assessed kinetic features were not significant predictors of carcinoma; furthermore, a washout kinetic pattern was present in 70% of infiltrating carcinomas but in only 9% of DCIS lesions. This result suggests that reliance on the presence of washout to diagnose cancer [26] may impair the ability to detect DCIS. The lower frequency of wash-out in DCIS than in infiltrating carcinoma may reflect differences in vascularity between in situ and invasive cancers (with perhaps less arteriovenous shunting in DCIS) [27,28,29] and should be confirmed and evaluated with rigorous quantitative analysis.
In the published literature, the reported sensitivity of MR imaging in the detection of DCIS has ranged from 40% to 100% [30]. In a study by Orel et al. [30] that included patients with mammographic or palpable abnormalities or with recently diagnosed breast cancer, 10 (77%) of 13 cases of histologically proven DCIS were identified on MR imaging: nine (90%) were evident as nonmass enhancement (linear and ductal in six and regional in three) and one (10%) as a peripherally enhancing mass. Among 13 MR imaging—detected DCIS lesions in our study, nine (69%) were nonmass lesions and four (31%) were masses. Mass lesions, uncommon in mammographically detected DCIS, may account for a higher proportion of DCIS lesions detected on MR imaging. Further work is necessary to determine the optimal breast MR imaging technique for the identification of DCIS and to further assess the sensitivity, patterns, and significance of DCIS detected on MR imaging.
Final assessment categories were significant predictors of carcinoma in MR imaging—detected breast lesions: carcinoma was present in 67% of lesions classified as highly suggestive of malignancy versus 19% of lesions classified as suspicious (p = 0.001). Among mammographically detected lesions, carcinoma has been reported in 81-94% of lesions classified as highly suggestive of malignancy versus 29-34% of lesions classified as suspicious [10, 31]. The apparent difference in PPV for these final assessment categories as a function of imaging modality may be a function of observer, patient population, experience, or the lexicon itself and should be assessed in future work.
T2 signal intensity was not a significant predictor of malignancy. This finding contrasts to a report of Kuhl et al. [32] of T2-weighted, non—fat-suppressed, turbo spin-echo images, in which high T2 signal intensity correlated with benign disease (perhaps because of the edematous extracellular matrix of fibroadenomas, particularly in patients younger than 50 years) and low T2 signal intensity correlated with carcinoma (perhaps because of dense cellularity, high nucleus-to-plasma ratio, absence of fat in cancers, and adjacent fibrosis). We observed no significant difference in the likelihood of malignancy among MR imaging—detected lesions measuring 1 cm or larger as opposed to smaller lesions.
Our study has several limitations. We examined a high-risk patient population and included only lesions referred for biopsy. The MR imaging examinations were evaluated by a single reviewer; there may be interobserver variability in the use of breast MR lesion descriptors [33]. Confirmation of lesion retrieval is difficult for MR imaging—guided surgical excision, because of the absence of a discrete target that can be identified on specimen imaging [34]; postoperative MR imaging, available in a minority of our patients, may be useful in this regard. Although the study included 100 lesions, some subgroups contained few or no lesions, a finding that limited conclusions that can be drawn about these features. The study focused on morphologic features, with only visual assessment of kinetic data. Finally, the breast MR imaging lexicon is a work in progress, and the terms assessed may not represent those in the finalized version [3].
In conclusion, we found carcinoma in 25 (25%) of MR imaging—detected lesions referred for biopsy, of which half were DCIS. Most malignant masses were infiltrating carcinoma, whereas most malignant nonmass lesions were DCIS. Features with the highest PPV were spiculated margin, rim enhancement, and irregular shape for masses and segmental or clumped linear and ductal enhancement for nonmass lesions. Final assessment categories were significant predictors of carcinoma. Further work with a larger series of cases including those interpreted as "benign" or "probably benign," multiple reviewers to assess interobserver variability, and inclusion of quantitative kinetic and morphologic analyses will be necessary as the breast MR imaging lexicon continues to evolve.
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