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Original Report |
1 Department of Radiology, Hospital Clínic and University of Barcelona
Medical School, Villarroel, 170, 08036 Barcelona, Spain.
2 Department of Radiotherapy Oncology, Hospital Clínic and University of
Barcelona Medical School, 08036 Barcelona, Spain.
3 Department of Obstetrics and Gynecology, Hospital Clínic and University
of Barcelona Medical School, 08036 Barcelona, Spain.
4 Department of Pathology, Hospital Clínic and University of Barcelona
Medical School, 08036 Barcelona, Spain.
Received March 17, 2004;
accepted after revision July 1, 2004.
Supported by grants from the Spanish Health Ministry (FIS PI 020534 and
01/1519).
Abstract
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CONCLUSION. Metaplastic carcinoma of the breast shows high signal intensity on T2-weighted MRI. This finding is related to the necrotic component of the tumor and may be useful for preoperative diagnosis of metaplastic carcinoma of the breast, although it must be differentiated from mucinous carcinoma and, less frequently, necrotic infiltrating ductal carcinoma.
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The objective of this study was to describe the MRI findings of metaplastic carcinoma of the breast and to compare those findings with the underlying histopathologic features.
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All patients presented with a single palpable firm mass without skin changes or nipple retraction. Axillary enlargement was absent in all cases. The average age of the patients was 56.5 years (range, 39-82 years). Ten patients underwent conservative surgery and radiation therapy; modified radical mastectomy was performed in two patients. Axillary lymphadenectomy was performed in 10 patients and sentinel node biopsy was undertaken in two patients. At present, all patients except one are alive at follow-up and free of locoregional disease.
Mammography was performed using a Senographe DMR unit (GE Healthcare). Each mammographic lesion was evaluated and categorized using the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS) classification [7]. All lesions were classified as BI-RADS category 5, highly suggestive of malignancy.
B-mode and duplex power Doppler sonography were performed in eight patients included in a study protocol on vascularization in breast cancer. Informed consent was obtained from all patients. Sonography was performed using a PowerVision SSA-380 (Toshiba) with a 7.5-MHz linear transducer and Doppler frequency of 5 MHz. Sonograms were assessed for lesion shape, margins, size, echogenicity, and vascularity. The resistive index (peak systolic velocity - peak end diastolic velocity / peak systolic velocity) was determined for each tumor artery. The maximum resistive index for each tumor was considered.
All MR examinations were performed on a 1-T unit (Magnetom Impact, Siemens AG). A dedicated double breast surface coil was used and bilateral scans were obtained. Before the examination, a needle was inserted into a cubital vein for IV administration of the contrast agent, and the patient was in a comfortable prone position.
The MR examination was performed on all patients without interslice gaps in five steps: Step 1: A T1-weighted spin-echo localizer sequence (TR/effective TE, 90/15; slice thickness, 10 mm; field of view, 400) provided axial, coronal, and sagittal images of both breasts. Step 2: A turbo spin-echo sequence of coronal T2-weighted imaging (TR/TE, 8,256/132; flip angle, 180°; slice thickness, 4 mm; matrix, 120 x 256 pixels; and field of view, 350 mm) was performed. Step 3: A coronal T1-weighted 3D fast low-angle shot (FLASH) sequence (TR/TE, 14/7; flip angle, 25°; matrix, 96 x 256 pixels; slice thickness, 2 mm; field of view, 350 mm; slices, 64; measurement time, 87 sec) was performed before and after enhancement with gadopentetate dimeglumine (Magnevist, Schering) using a dose of 0.16 mmol/kg of body weight without moving the patient, followed by an injection of saline. Step 4: Visual evaluation was supported by automated subtraction of the appropriate unenhanced and contrast-enhanced images. Step 5: Multiplanar reconstruction of the data sets facilitated visualization of 3D anatomy.
One patient had claustrophobia during the examination and only a turbo spin-echo T2-weighted sequence could be performed.
Morphologic and kinetic features were evaluated. The enhanced areas were quantitatively analyzed by drawing regions of interest on unenhanced and contrast-enhanced images. Normalized signal increase (NSI) was calculated on the basis of the technique described by Heywang-Köbrunner [8]. NSI of less than 500 normalized units (NU) was considered to be no or minimal enhancement; between 500 and 1000 NU, intermediate enhancement; and greater than 1,000 NU, strong enhancement. Time-signal intensity curves of the lesions were recorded and classified on the basis of their shape as steady (type 1), plateau (type 2), or washout (type 3) [9]. The morphology of all enhanced lesions was evaluated using the following criteria: size; shape (round, oval, lobulated); margin (well-circumscribed, irregular, spiculated, internal structure); presence of septation or cavities; and enhancement (ring, centripetal, or other).
All imaging studies were evaluated in consensus interpretations by radiologists who were experienced in breast imaging.
Preoperative fine-needle aspiration cytology was performed in all patients using a 20-gauge, 1.5-inch needle. The tumors were submitted for routine histopathologic examination. They were fixed in 10% buffered formalin, embedded in paraffin, sectioned at 3 µm, and stained with H and E. The cases were classified according to the World Health Organization classification [10]. Immunohistochemical analysis was used to confirm myxochondroid differentiation and included the use of anti-S100 and antiactin antibodies. Expression of estrogen receptor, progesterone receptor, protein p53, and protooncogene c-erbB-2 was also analyzed with the Envision (Dako) method and monoclonal antibodies. In seven patients the p53 status was determined, and in 11 patients the expression of c-erbB-2 gene was considered. All pathology studies were reviewed by a breast pathology specialist.
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On sonography, 75% (6/8) of the lesions showed complex echogenicity with solid and cystic components. On duplex power Doppler sonography, 75% (6/8) of lesions were highly vascularized. The average resistive index was 0.83 (range, 0.71-0.96).
On MRI, all lesions were expressed as a mass of irregular contour with spiculations. The signal intensity on T2-weighted images was highly variable; it was greater than or equal to the signal intensity of the surrounding fibroglandular tissue. On the basis of T2 signal intensity, the metaplastic tumors were grouped into three signal patterns: homogeneous intratumoral hypersignal (Fig. 2) similar to the hypersignal visible on simple cysts, which was observed in 16% (2/12) of cases; a mottled pattern (Fig. 3) with areas of intratumoral hypersignal combined with areas of hyposignal or isosignal, which was observed in 75% (9/12); and an isointense pattern (Fig. 4) equivalent to that of fibroglandular tissue, which was seen in 8% (1/12) of cases. All lesions showed contrast uptake (one case not available). The uptake morphology was ring-like in 72% (8/11) of cases (Fig. 5A) and was completely homogeneous and centripetal in the remaining 27% (3/11). In the quantitative analysis, intermediate uptake was found in 63% of cases (7/11) and high uptake in the remaining 36% (4/11). Enhancement speed showed type 1 time-signal intensity curve in 18% (2/11) of cases, type 2 in 45% (5/11), and type 3 in the remaining 36% (4/11).
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In only one patient, squamous metaplastic carcinoma was found in the fine-needle aspiration cytology. In the remainder, the cytology was compatible with ductal carcinoma. The mean size of the lesions at the pathologic examination was 25.9 mm (range, 12-45 mm). Central necrosis comprising more than 50% of the tumor was observed in 66% (8/12) of cases (Figs. 5B, 5C, 5D). Axillary metastasis was observed in 25% (3/12). Two of these cases were squamous metaplastic cancers and one was carcinoma with chondroid metaplasia. The average number of nodes that underwent excision was 13.2 (range, 8-22).
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In our series, all patients had negative estrogen receptor and progesterone receptor status. In five patients, overexpression of the p53 protein was observed. The c-erbB-2 oncogene was intensely positive in two cases, moderately positive in two cases, slightly positive in five cases, and negative in two cases.
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Metaplastic carcinomas usually present in women older than 50 years as fast-growing palpable masses with an average size generally larger than that of breast carcinoma, and no predilection for the left or right breast. Metaplastic breast carcinoma can be diagnosed with aspiration cytology or at core biopsy. Nevertheless, excisional biopsy is preferred to avoid diagnostic errors resulting from inadequate samples in cases with extensive necrosis. In our series, cytology suggested the correct diagnosis in only one case.
Depending on the series, axillary node involvement is in the range of 25-40% [2, 6]. In our series, 25% of the patients with axillary lymphadenectomy had metastatic nodes. Metaplastic carcinomas of the breast rarely express immunoreactivity to the estrogen and progesterone receptors, as confirmed in our series. Treatment of these tumors is not any different from that of the usual ductal carcinomas.
The mammographic appearance of metaplastic carcinoma of the breast has been previously described as a predominantly circumscribed mass with irregular contours, or with spiculations without calcification. In some studies, distortion is associated with the nodular lesion [5, 6]. In our series, most of the tumors were polylobulated, with ill-defined contours in more than 50%, with no evidence of associated distortion. Microcalcifications were observed in 25% of the cases, with greater frequency in the carcinomas with chondroid metaplasia. In our series, we found that radiologic manifestations of metaplastic breast carcinoma are similar to those of other invasive breast carcinomas when expressed on mammography as a mass.
On B-mode sonography, Park et al. [5] observed complex internal echogenicity with solid and cystic components in six of 16 lesions, and Günhan-Bilgen et al. [6] in one of eight cases. These findings are associated with the presence of necrosis and cystic degeneration in the histologic analysis. In our series, all tumors showed complex echogenicity. On power duplex Doppler sonography, the average resistive index was high (0.83), a finding similar to the indexes found in the usual breast carcinoma [11].
On breast MRI, the intensity of the signal for the lesions in the T1-weighted image sequence was generally isointense or hypointense when compared with normal glandular tissue, as occurs in other histologic types of invasive breast carcinoma. Nevertheless, an increase in the signal on T2-weighted images was detected in 91% of cases. The T2 hypersignal is related to the necrotic component of the tumor, a frequent finding in this type of tumor, which in our series was observed in all cases but one. Nevertheless, histologic analysis showed an elevated necrotic component.
The T2 hypersignal is also observed in carcinomas with mucoid content and, more rarely, in infiltrating ductal carcinoma with an abundant necrotic component [12]. Therefore, the T2 hypersignal is useful in differentiating these tumors from other histologic types of invasive carcinoma.
The most frequent uptake morphology was ringlike, which can be partially explained by the extensive central necrosis observed in these tumors. The most frequent time-signal intensity curves were types 2 and 3, which is not a special characteristic of this type of tumor.
In summary, the high signal intensity on T2-weighted MRI appears to be useful for preoperative diagnosis of metaplastic carcinoma of the breast, although differentiating from mucinous carcinoma and, less frequently, necrotic infiltrating ductal carcinoma is required.
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