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Breast Imaging |
1 From the Departments of Radiology (W.K.M., J.G.I., Y.H.K.), Surgery (D.Y.N.), and Pathology (I.A.P.) and Clinical Research Institute, Seoul National University Hospital and the Institute of Radiation Medicine, SNUMRC, 28 Yongon-Dong, Chongno-Gu, Seoul 110-744, Korea. Received December 22, 1999; revision requested January 25, 2000; revision received February 29; accepted March 24. Address correspondence to W.K.M. (e-mail: moonwk@radcom.snu.ac.kr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Ninety-four patients with 100 mammographically detected microcalcification clusters prospectively underwent US with a 10- or 12-MHz transducer before mammographically guided presurgical hook-wire localization. The visibility of breast masses at US was correlated with histologic and mammographic findings.
RESULTS: Surgical biopsy revealed 62 benign lesions, 30 intraductal cancers, and eight invasive cancers. At US, breast masses associated with microcalcifications were seen in 45 (45%) of 100 cases. US depicted more breast masses associated with malignant (31 [82%] of 38) than with benign (14 [23%] of 62) microcalcifications (P < .001). In malignant microcalcification clusters larger than 10 mm, US depicted associated breast masses in all 25 cases. There was no statistically significant difference in shape and distribution of calcific particles, as well as in breast composition, at mammography between US visible and invisible groups.
CONCLUSION: Given a known mammographic location, US with a high-frequency transducer can depict breast masses associated with malignant microcalcifications, particularly clusters larger than 10 mm. US can be used to visualize large clusters of microcalcifications that have a very high suspicion of malignancy.
Index terms: Breast, US, 00.1298 • Breast neoplasms, calcifications, 00.3221, 00.3241 • Breast neoplasms, diagnosis, 00.1298, 00.301
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The advances in ultrasonographic (US) equipment and the refinement of breast imaging techniques enable radiologists to detect and characterize small lesions better (6–9) and to provide efficient and economical US guidance for percutaneous procedures (10,11). As practitioners gain hands-on experience using US in patients with nonpalpable lesions, both localization procedures and percutaneous biopsies are being performed with increasing frequency by means of US guidance as opposed to mammographic guidance (11–13). However, the low capability of US to depict microcalcifications remains a major limitation (14,15). Microcalcifications cannot be depicted with US when they are located inside echogenic, fibroglandular breast tissue because of the difficulty in differentiating them from the echogenic interfaces among tissues.
After using a high-frequency transducer, some investigators have reported that US depicted clustered microcalcifications in breast cancers (16–18). Calcifications associated with malignant tumors are more likely to be seen sonographically because most malignant calcifications occur within the masses as opposed to within echogenic breast parenchyma. A hypoechoic background of tumor enhances the ability of US to enable identification of the hyperechoic punctate calcifications. In contrast, benign calcifications, especially in fibrocystic diseases, are less likely to be seen at US because most benign calcifications do not occur within masses. Those studies were, however, retrospective in nature (16,18) and lacked reproducibility of the findings. In nonpalpable lesions, difficulties also arise in ensuring that a lesion that was visible at US was the same as that seen on the mammograms (13, 18). US demonstration of microcalcifications is considered by many to be unreliable if not impossible.
The objectives of this prospective study were to determine whether (a) US performed with a high-frequency transducer can demonstrate breast masses associated with mammographically detected clustered microcalcifications without mass density and (b) the visibility at US is different between benign and malignant lesions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mammography was performed by using a conventional screen-film technique and dedicated equipment (Senographe, 600T; GE Medical Systems, Milwaukee, Wis). Routine mediolateral oblique and craniocaudal mammograms were obtained in all patients, and additional spot compression magnification and true lateral images were available in all but two patients. Multicentric lesions were seen in four patients, and bilateral lesions were seen in two patients. Of 100 lesions, 48 lesions were in heterogeneously or extremely dense breasts and 52 lesions were in entirely or predominantly fatty breasts. According to the American College of Radiology (ACR) Breast Imaging Reporting and Data System (BI-RADS) (19), the final assessment was probably benign lesions (category 3) in four cases, suspicious lesions (category 4) in 67 cases, and highly suspicious lesions (category 5) in 29 cases. In four cases of probably benign lesions, the patient underwent biopsy because of patient or referring clinician preference based on clinical grounds (Fig 1).
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In all 100 cases, hook-wire localization was performed by using a fenestrated compression plate and a 21-gauge hook-wire needle (Kopans spring hook localization needle; Cook, Bloomington, Ind). All procedures were carefully done to avoid tissue damage or bleeding in the breast. Final wire placement mammograms in craniocaudal, oblique, and true lateral projections were obtained with a radiopaque marker at the wire entry point on the skin. The localizing wire was placed within 2 mm of the lesions in 89 lesions and within 5 mm in 11 lesions. After placement of the hook wire, the patient moved to the US room for the second US examination. Postlocalization US was performed to confirm that the lesion seen at prelocalization US was correct. In nonpalpable lesions, difficulties can arise in ensuring that a lesion that is visible at US is the same as that seen on the mammograms. US scans obtained after hook-wire localization were not used for image analysis. All patients underwent surgery within 24 hours of the US examinations. Mammography of the specimen was performed in all patients, and microcalcifications were confirmed in all 100 lesions.
The 100 clusters of microcalcifications were categorized into two groups according to the visibility at US: sonographically visible lesions and invisible lesions. The lesion was considered to be sonographically visible when a mass with or without sonographically visible microcalcification was definitely seen at the suspicious area determined at mammography and confirmed at US after needle localization. We did not attempt to sonographically identify microcalcifications without an associated US mass.
All mammographic and US images were assessed preoperatively by means of consensus between the two radiologists. At mammography, the size of the calcific cluster was measured at the greatest dimension. The shape and distribution of microcalcifications were described according to the ACR BI-RADS (19). At US, the lesions were described according to size, shape, orientation, echogenicity, echotexture, margin, boundary echo, acoustic transmission, and US evidence of calcifications (6). The US maximum diameter of the mass was defined as the size of the lesion. The shape of masses was classified as round, lobular, or irregular. The orientation of masses was classified as wider than tall or taller than wide according to the anteroposterior to transverse dimension ratio. The echogenicity of masses was compared with that of the subcutaneous fat and classified as hyperechoic, isoechoic, mildly hypoechoic, markedly hypoechoic, or anechoic. The echotexture of masses was classified as homogeneous or heterogeneous. Mass margins were classified as well defined, microlobulated, ill defined, or spiculated. If an echogenic boundary was seen, it was defined as a thin capsule or thick halo. Posterior shadowing or enhancement was considered to be present when an area had relatively less or more through transmission of sound than was present in the surrounding tissue at the same depth. If punctate echogenic dots suggestive of calcifications were seen within the mass, they were reported. The two radiologists who performed the US examinations also correlated US findings with histologic and mammographic findings.
To determine whether the visibility at US is affected by the pathologic condition (benign or malignant disease), breast composition (fatty or dense breast), and/or mammographic findings (size, shape, and distribution of microcalcifications), statistical analysis was performed with a statistical software system (SAS for Windows, version 6.12; SAS Institute, Cary, NC). The Fisher exact test and 
2 test were used for independent samples, and the Mann-Whitney U test was used for the variables with nonnormal distributions. Findings with a P value of less than .05 were considered as statistically significant. By using the presence of the mass at US as the diagnostic criterion for malignancy in ACR BI-RADS category 4 or 5 microcalcifications, a diagnostic accuracy, including sensitivity, specificity, and positive and negative predictive values, was calculated. Because the number of cases in which we used the 12-5–MHz transducer was small, the results of US performed with 10-5–MHz and with 12-5–MHz transducers were reported together.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Of 31 malignancies found at US, 23 cases were DCIS and eight cases were infiltrating ductal carcinomas (Table 1). All of the malignant lesions were seen as solid masses with heterogeneous echotexture but with variable findings. At US, a lobular shape (n = 14), mild hypoechogenicity (n = 16), ill-defined margin (n = 13), normal acoustic transmission (n = 18), and lack of associated calcifications (n = 13) were more commonly seen in DCIS (Fig 2), whereas an irregular shape (n = 6) and calcifications within the mass (n = 7) were more frequently seen in invasive cancers (Table 3).
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By using the presence of a US mass as the diagnostic criterion for malignancy in ACR BI-RADS category 4 (n = 67) or 5 (n = 29) microcalcifications, the sensitivity, specificity, and positive and negative predictive values of US were 82% (31 of 38), 83% (48 of 58), 76% (31 of 41), and 87% (48 of 55). For ACR BI-RADS category 4 (n = 40) or 5 (n = 22) lesions larger than 10 mm, the sensitivity, specificity, and positive and negative predictive values of US were 100% (31 of 31), 84% (31 of 37), 81% (25 of 31), and 100% (31 of 31).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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US is less sensitive for demonstration of microcalcifications than is mammography (20,21). The smaller the calcifications, the lower the sensitivity of US for depicting them. The low capability to visualize microcalcifications remains a major limitation for using US as a screening or diagnostic tool for breast cancers. However, the currently used high-frequency transducers can yield a higher percentage of mammographically visible calcifications than could the previously used lower-frequency transducers (22,23). With use of high-frequency, correctly focused 10–12-MHz probes, tiny echogenic spots without acoustic shadowing that correspond to the mammographic image findings can be seen.
According to the results of a phantom experiment with a 7.5-MHz transducer, US can depict and enable identification of minute glass beads even 100 mm in diameter, provided they are scattered in an ideal hypoechoic area (24). The visualization of typical malignant microcalcifications as small as 100–500 µm should increase with state-of-the-art US equipment and a higher frequency transducer (25). In our study, echogenic dots within the mass that were suggestive of calcifications were seen in 55% (17 of 31) of malignant cases. The assumption that US will more likely depict malignant rather than benign calcification was proved in the current study. However, the visibility of calcifications within a mass cannot be used to distinguish between benign and malignant disease; calcifications are sonographically visible in some benign lesions and invisible in some malignancies.
The main benefit of identifying a US abnormality in women with mammographically detected microcalcifications is to allow the use of US to guide interventional procedures, such as needle biopsy and needle localization (18,22). However, US cannot be routinely used to guide biopsy or needle localization of suspicious calcifications because it fails to depict the calcifications or an associated mass in many cases. Our study results showed that the majority of large malignant clusters of microcalcifications were visible at US, whereas small malignant clusters or benign clusters of any size were frequently invisible at US. Therefore, it would be reasonable to use US to try to visualize large (>10-mm) clusters of microcalcifications with a high suspicion of malignancy (estimated likelihood of malignancy 75% or higher, using mammographic assessment criteria). US-guided procedures are less expensive and faster than stereotactically guided procedures (11). In addition, for those institutions that do not have stereotactic equipment, the use of US in selected cases (large-area high-suspicion microcalcifications) would extend the role of percutaneous biopsy at these sites.
Common US features of invasive breast cancers include irregular shape, taller than wide orientation, marked hypoechogenicity, heterogeneous echotexture, spiculated margins, and posterior acoustic shadowing (6–9,26). Little is known about the US features of DCIS because this entity usually manifests as pure mammographic calcifications, which, to our knowledge, rarely have been evaluated with US. In our study, a lobular shape, mild hypoechogenicity, and normal acoustic transmission were the most common findings of DCIS, and these findings are consistent with those of previous reports about DCIS at US (27,28). Similar US findings were also seen in some benign lesions, such as sclerosing adenosis and atypical ductal hyperplasia, and were reported in a radial scar (29). Therefore, the US findings of DCIS seen in our study seem to be nonspecific. Abnormal distention of central ducts without an associated mass or intracystic papillary nodule, which is usually seen in patients with a nipple discharge or a palpable mass, was not observed in our series.
Benign US features were typically seen in some fibrocystic lesions and fibroadenomas. Multiple small cysts were seen in the area that corresponded to microcalcifications at mammography in three cases of ductal hyperplasia without atypia and in one case of microcysts, and a well-defined ellipsoid mass was seen in all fibroadenomas. On mammograms, the microcalcifications in these cases were of low to intermediate suspicion in all cases (Fig 1). Whether US can increase the specificity of mammography and helps to reduce the number of surgical or core biopsies performed in women with microcalcifications needs further investigation.
Our study seemed to include a smaller proportion of small DCIS lesions than expected; 37% (11 of 30) of DCIS lesions in our series were smaller than 10 mm compared with 72% (47 of 65) in the Sickles series (30). Thus, our overall results showed a larger percentage of DCIS lesions to be visible at US than would be observed in a practice that routinely detects DCIS at a smaller size. In our study, US visibility of mammographic calcifications in dense breasts (48% [23 of 48]) was higher than that in fatty breasts (42% [22 of 52]), but the difference was not statistically significant. We speculate that mammographic calcifications with subtle or small associated masses might be obscured by the dense parenchyma and misinterpreted as pure calcifications.
In summary, given a known mammographic location, US performed with a high-frequency transducer can depict breast masses associated with microcalcifications in a minority (45%) of cases. However, the visibility at US is much higher in malignant microcalcifications, particularly clusters larger than 10 mm, than in benign microcalcifications. Therefore, US can be used to visualize large clusters of microcalcifications that have a very high suspicion of malignancy. The potential benefit of US examination for suspicious breast microcalcifications is to identify a mass lesion associated with the calcifications and to guide the needle biopsy or hook-wire localization in cases for which stereotactic biopsy or localization cannot be performed or is unavailable.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, W.K.M.; study concepts, W.K.M., J.G.I., D.Y.N., Y.H.K.; study design, W.K.M., J.G.I., D.Y.N., I.A.P.; definition of intellectual content, W.K.M., J.G.I., Y.H.K.; literature research, W.K.M., Y.H.K.; clinical studies, W.K.M., Y.H.K.; data acquisition, W.K.M., Y.H.K.; data analysis, W.K.M., J.G.I., D.Y.N., I.A.P.; statistical analysis, W.K.M., Y.H.K.; manuscript preparation, W.K.M., J.G.I., D.Y.N., I.A.P.; manuscript editing, W.K.M., J.G.I.; manuscript review, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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