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Original Report |
1 Department of Radiology, Ege University Hospital, Bornova, 35100, Izmir,
Turkey.
2 Department of Pathology, Ege University Hospital, Izmir, Turkey.
Received October 22, 2001;
accepted after revision March 11, 2002.
Address correspondence to I. Günhan-Bilgen.
Abstract
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CONCLUSION. Invasive micropapillary carcinoma of the breast usually manifests as a firm, immobile mass. Findings on mammography are of a spiculated, irregular or round, high density mass with or without associated microcalcifications. On sonography, the common findings are of a homogeneously hypoechoic, irregular or microlobulated mass with posterior acoustic shadowing or normal sound transmission. Axillary lymph nodes are frequently involved. Although these findings are not specific and may be seen with other breast malignancies, invasive micropapillary carcinoma should be included in the differential diagnosis for breast masses with these imaging features. Also, radiologic findings may help in the histopathologic differentiation of cases that are difficult to diagnose, such as metastatic tumors.
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All 16 patients underwent routine diagnostic imaging workup with mammography and sonography. Mammography was performed on a Senographe Senix 600T (General Electric, Issy Les Moulineaux, France) or Mammomat 3000 (Siemens, Solna, Sweden). Sonography was performed in all patients with a 7.5-MHz transducer (SAL 70, Toshiba, Tokyo, Japan; or Sonoline Adara, Siemens, Erlangen, Germany) or a broadband 5- to 11-MHz transducer (HDL 1000; Advanced Technology Laboratories, Bothell, WA).
Two radiologists who are specialists in breast imaging retrospectively reviewed all mammograms and evaluated the findings in consensus. These radiologists were unaware of patient information from physical examinations or sonographic records, but they were aware of each patient's histopathologic diagnosis. Each mammographic lesion was characterized according to size, mass characteristics (shape, margins, density, size, and location), presence and type of microcalcifications, associated architectural distortion, and skin changes using the criteria given by the American College of Radiology's Breast Imaging Reporting and Data System (BI-RADS) [7]. Parenchymal patterns were categorized as fatty, heterogeneously dense, and extremely dense using BI-RADS criteria [7].
The sonographic prints and records of each patient were reviewed after the mammograms during the same evaluation session. Sonograms were assessed for lesion shape, margin, echotexture, echogenicity, and posterior acoustic phenomena. All lesions were surgically excised. In one patient, the nonpalpable lesion (retroareolar microcalcifications) was preoperatively localized by the mammography-guided needle-wire localization system.
The microscopic slides of each patient were reviewed and evaluated in consensus by two pathologists who are specialists in breast pathology. Fine-needle-aspiration smears of the breast lesions (n = 14) were stained with both H and E and May-Grünwald Giemsa stain. The surgical specimens from all of the cases (n = 16) were fixed in formalin, and paraffin-embedded tissues were stained with H and E. All of the tumors had invasive micropapillary carcinoma with characteristic histologic features.
Finally, the mammographic and sonographic findings were correlated with the histopathologic results. Size, predominant findings, and lymph node status were obtained from surgical pathology reports.
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All patients underwent mammography. Parenchymal patterns were extremely dense in three, heterogeneously dense in eight, and fatty in five breasts. The distribution of mammographic findings in 15 of the 16 patients were as follows: mass in eight (50%), isolated microcalcifications in two (12.5%), and mass associated with microcalcifications in five patients (31.3%). In one patient whose mammogram revealed no abnormalities, invasive micropapillary carcinoma presented as a palpable mass. Associated findings in our study group included skin retraction in one patient and axillary lymphadenopathy in one patient.
Of the 13 mammographic masses, nine were in the upper outer quadrant, two were in the upper inner quadrant, and two were in the lower inner quadrant. The mean diameter of these masses was 2.2 cm (range, 1-5 cm). All masses were of high density. Seven masses (53.8%) were round to ovoid, and six (46.2%) were irregular. The margins of the masses were obscured and spiculated in one (7.7%), spiculated in eight (61.5%) (Fig. 1A), indistinct in two (15.4%), and microlobulated in two (15.4%) patients.
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Microcalcifications were present in seven patients. In five patients, microcalcifications were accompanying a mass, and in two patients they were without a mass. The two patients with isolated microcalcifications had dense breasts. In one of these patients, the punctate, clustered microcalcifications were localized by a mammography-guided needle-wire system; histopathologic examination revealed an invasive micropapillary carcinoma of 1 cm. In the other patient, the palpable mass, which was revealed on sonography, was in a different quadrant than the microcalcifications. At histopathologic examination, the palpable mass was diagnosed as invasive micropapillary carcinoma, and the microcalcifications were diagnosed as ductal carcinoma in situ (Fig. 2A).
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All patients underwent sonography. A solid mass was detected in 15 of 16 patients; the mean longest diameter was 2 cm (range, 1-6 cm). Only one mass was longer than 2.5 cm. All masses were hypoechoic. The margins were irregular in eight (53.3%), microlobulated in five (33.3%), well-circumscribed in one (6.7%) (Fig. 2B), and spiculated in one patient (6.7%). The shape of the mass was irregular in seven (46.7%), round in five (33.3%), and ellipsoid in three patients (20%). The echotexture of masses were mostly (93.3%) homogeneous. In one patient (6.7%), calcifications seen as bright punctate echoes inside the mass caused a heterogeneous echogenicity. Nine masses (60.0%) had posterior acoustic shadowing (Fig. 1B), whereas six masses (40.0%) showed normal sound transmission (no acoustic phenomena). Axillary lymphadenopathy was detected in six patients (37.5%).
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Aspiration biopsy cytology of the breast lesions was performed in 14 patients and disclosed malignant epithelial tumors. Two lesions were recorded as malignant epithelial tumors consistent with invasive micropapillary carcinoma.
Twelve patients underwent modified radical mastectomy, and four patients underwent lumpectomy. The histopathologic findings in all patients showed abundant invasive epithelial cell nests within clear spaces. The epithelial cell groups and surrounding clear spaces were set within a fine reticular to collagenous stroma (Fig. 1C). The mean size of invasive micropapillary carcinoma was 2.1 cm (range, 1-6 cm). In one patient, inflammatory breast carcinoma of invasive micropapillary type (6 cm) was present. In another patient with a 1.5-cm palpable mass of invasive micropapillary carcinoma in the lower outer quadrant (Fig. 2C), ductal carcinoma in situ of comedo type was present in the upper outer quadrant (multicentric malignancy). Axillary dissection was performed in 14 of 16 patients; malignant adenopathy was present in six (42.9%). Positive lymph nodes were associated only with invasive micropapillary carcinoma masses that were equal to or greater than 2 cm at largest diameter.
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Invasive micropapillary carcinoma is an uncommon tumor with a reported incidence of 1.2-2.7% of breast cancers [1, 4, 5]. In our study, the incidence is lower (0.9%, 16/1845). A number of reasons account for this difference. First, because we would be describing the imaging findings for the first time, we included only the cases of pure invasive micropapillary carcinoma. Second, this is a retrospective study concerning the past 15 years, and the patients discussed were diagnosed in the past 6 years (time interval, 1-66 months; mean, 27.5 months). It is likely that this recently described entity had been underestimated. Moreover, the incidence given as 1.2-2.7% is from the pathology, not the radiology, literature.
The role of breast imaging in establishing a diagnosis of invasive micropapillary carcinoma remains uncertain. Experience is limited, and so far no specific mammographic, sonographic, or MR imaging characteristics have been identified [5]. We know of only one report in the literature that describes physical examination and imaging findings of invasive micropapillary carcinoma, a case report on the aspiration biopsy cytology of invasive micropapillary carcinoma. It describes only the MR imaging findings because neither mammography nor sonography was performed. In that report, Wong et al. [5] presented an 80-year-old patient with a firm, nontender mass of 4 cm in the upper outer quadrant of the left breast. MR imaging revealed asymmetric enlargement of the left breast with a 3.2-cm irregular mass that was highly suggestive of malignancy because of its signal characteristics and contrast enhancement pattern [5]. In our study, a palpable mass was present in 93.8% (15/16) of the patients. The mass showed similar physical examination characteristics. Although MR imaging was not performed in our study, all patients underwent mammography and sonography.
In most of the patients (81.3%) in our series, the tumor presented on mammography as a mass (with or without microcalcifications). All masses were of high density. The shape of the mass was round to ovoid in approximately half of the patients (53.8%) and irregular in the others. The margins were commonly spiculated (72.7%); however, in approximately one third of the patients, indistinct or microlobulated margins were seen. Microcalcifications, either isolated or associated with a mass, were present in 43.8% of patients. The morphology of the microcalcifications was pleomorphic or punctate or both, and their distribution was clustered or segmental. On sonography, all masses were hypoechoic, and 93.3% showed homogeneous echotexture. Their margins were mostly (86.6%) irregular or microlobulated. Posterior acoustic shadowing was seen in 60.0% of the masses, whereas the other masses showed normal sound transmission.
Walsh and Bleiweiss [1] have stated that, given the obvious predilection of invasive micropapillary carcinoma of the breast for lymphatic and lymph node spread, identification of this entity as a distinct variant of breast cancer with a potentially aggressive behavior seems prudent. In the histopathologic differential diagnosis of invasive micropapillary carcinoma, other breast carcinomas, such as rare invasive papillary carcinoma and colloid carcinoma, must be considered [1]. Knowing the imaging findings of these tumors may be of value in the differential diagnosis. Invasive papillary carcinoma, which occurs infrequently, may be seen as solitary masses or as a cluster of well-defined, circumscribed nodules confined to one breast quadrant on mammography [8]. Sonography usually reveals solid masses, although complex cystic and solid masses also can be identified [8]. The characteristic colloid carcinoma growth is smoothly marginated, sometimes also lobulated. In invasive micropapillary carcinoma, as described in this study, 69.2% of masses showed spiculated margins, and none had well-circumscribed margins on mammography. All masses in our study appeared solid on sonography, and none had cystic components. Therefore, imaging findings are likely to be useful for differential diagnosis, also. Further studies in this respect are needed.
Metastatic tumors from ovarian serous papillary adenocarcinoma and the micropapillary variant of transitional cell carcinoma of the bladder, although rare, must also be considered in the differential diagnosis [1, 9, 10]. Both of these tumors may exactly mimic the histologic appearance of primary invasive micropapillary carcinoma of the breast. A thorough and accurate clinical history, the use of immunohistochemical markers, and the presence of associated ductal carcinoma in situ will aid in the correct diagnosis of primary invasive micropapillary carcinoma of the breast [1, 10]. Again, imaging findings might help in the differential diagnosis. Focal metastases are generally visualized on mammography as round, sharply outlined lesions, frequently with no significant marginal indistinctness, spiculation, or other signs of desmoplastic response that characterize many primary carcinomas [11, 12]. The perfectly round shape is particularly suggestive of a focal metastatic tumor. Aside from coarse calcifications involving necrotic areas, calcifications are extremely rare and are only described as amorphous calcifications in ovarian carcinoma [11]. On sonography, metastatic breast masses usually have distal acoustic enhancement or acoustic shadowing [11]. As a result, imaging findings of metastatic tumors and invasive micropapillary carcinoma, as described in this study, are different, and this may be helpful in the differential diagnosis.
To our knowledge, only three cases of aspiration biopsy cytology of invasive micropapillary carcinoma have been reported in the literature [5, 10]. The diagnosis of invasive micropapillary carcinoma can be suggested based on some cytomorphologic findings [10]. Differentiation of invasive micropapillary carcinoma from other papillary lesions and malignancies by aspiration biopsy cytology may be possible, but more experience is needed because the number of reported cases remains limited [5]. In our series, aspiration biopsy cytology was performed in 14 patients and disclosed malignant epithelial tumors. Two of the lesions were reported as malignant epithelial tumors consistent with invasive micropapillary carcinoma. More experience is needed before it is possible to make a definitive diagnosis with confidence on the basis of fine-needle aspiration smears. The core-biopsy technique is a better alternative, because it can provide more definitive histopathologic data.
Follow-up studies on patients with invasive micropapillary carcinoma have been limited by small patient numbers, short duration of follow-up, and lack of multivariate analyses [3]. Follow-up data are present in only two of the patients in our study, one of whom has remained disease-free for 2 years and one, for 3 years.
In conclusion, invasive micropapillary carcinoma of the breast usually manifests on mammography as a firm, immobile, spiculated, irregular or round, high-density mass with or without associated microcalcifications. Common findings on sonography include a homogeneously hypoechoic, irregular or microlobulated mass with posterior acoustic shadowing or normal sound transmission. Axillary lymph nodes are frequently involved, especially if the mass is greater than 2 cm. Although these findings are not specific and may be seen in other types of breast malignancies, invasive micropapillary carcinoma should be included in the differential diagnosis for breast masses with these imaging features. Also, radiologic findings may help in the histopathologic differentiation of cases that are difficult to diagnose, such as metastatic tumors.
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