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Breast Imaging |
1 From the Departments of Radiology (W.K.M., J.G.I.) and Surgery (D.Y.N.), Clinical Research Institute, Seoul National University Hospital and the Institute of Radiation Medicine, Seoul National University Medical Research Center, 28 Yongon-Dong, Chongno-Gu, Seoul 110-744, Korea. From the 2000 RSNA scientific assembly. Received July 18, 2001; revision requested September 11; revision received October 9; accepted November 12. Supported by grant HMP-00-P-14-006 from the Korea Health 21 R&D Project, Ministry of Health and Welfare, Republic of Korea. 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 METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Two hundred one patients who had newly diagnosed breast cancer or who were suspected of having breast cancer underwent US examination of the ipsilateral and contralateral breasts with a 10-, 12-, or 13-MHz transducer. All solid lesions found at US alone were classified according to level of suspicion and were selected for biopsy. The US results were compared with mammographic findings. Sensitivity, specificity, and positive and negative predictive values were calculated.
RESULTS: In ipsilateral breasts, US depicted 194 (97%) of 201 foci of invasive cancer and 52 (75%) of 69 foci of ductal carcinoma in situ (DCIS), whereas mammography and physical examination depicted 173 (86%) foci of invasive cancer and 56 (81%) foci of DCIS. In the contralateral breast, US depicted 11 (92%) of 12 foci of invasive cancer and four (57%) of seven foci of DCIS, whereas mammography and physical examination depicted six (50%) foci of invasive cancer and five (71%) foci of DCIS. Overall, US depicted mammographically and clinically unsuspected multifocal or multicentric cancers in 28 patients (14%) and contralateral cancer in eight patients (4%). On the basis of these US findings, therapy was correctly changed in 32 patients (16%). The sensitivity, specificity, and positive and negative predictive values of prospective classification of 77 solid lesions detected at US alone were 100% (36 of 36), 51% (21 of 41), 64% (36 of 56), and 100% (21 of 21), respectively.
CONCLUSION: Bilateral whole-breast US complements mammography in the preoperative evaluation of patients with breast cancer.
© RSNA, 2002
Index terms: Breast neoplasms, 00.31, 00.32, 00.81 • Breast neoplasms, diagnosis, 00.31, 00.32, 00.81 • Breast neoplasms, staging • Breast neoplasms, US, 00.1298
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The ability of physician-performed ultrasonography (US) to depict mammographically occult cancer (14) has recently led to the investigation of US as a tool for staging breast cancer in dense breasts. In a study of 40 patients known or highly suspected to have breast cancer, Berg and Gilbreath (15) found that nine (14%) of 64 malignant foci were seen only at US. On the basis of US findings, three (15%) of the 20 patients suspected of having unifocal disease at mammography required wider excision. This study showed the potential of US as an adjunctive imaging modality to mammography in the preoperative evaluation of patients with breast cancer. The study, however, focused only on the ipsilateral breast and was limited by its small study population. To our knowledge, little has been published regarding the detection and appearance of synchronous bilateral breast cancers at US.
The purpose of our study was to evaluate the efficacy of preoperative bilateral whole-breast US in the detection of additional multifocal, multicentric, and contralateral cancers and the effect of US information on therapeutic decisions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Imaging and Image Evaluation
Mammography was performed with 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 obtained in 130 patients (65%) for evaluation of the lesions and the extent of disease. Of the 201 patients, 71 (35%) had scattered fibroglandular tissues in fatty breasts (BI-RADS grade 2), 76 (38%) had heterogeneously dense breasts (grade 3), and 54 (27%) had extremely dense breasts (grade 4). On mammograms, the index lesion was seen as a mass in 60 (30%) patients, as a mass with microcalcifications in 62 (31%) patients, as microcalcifications in 29 (14%) patients, as an asymmetric density in 16 (8%) patients, and as architecture distortion in three (1%) patients. No mammographic abnormality was observed in 31 (15%) patients.
All US examinations were performed by one experienced radiologist (W.K.M.) with knowledge of the clinical and mammographic findings. A 10- or 12-MHz linear-array probe (HDI 3000 or HDI 5000; Advanced Technology Laboratories, Bothell, Wash) was used in 157 patients and a 13-MHz linear-array probe (LOGIQ 700; GE Medical Systems) was used in 44 patients. US examinations were performed with the patient in the supine position with the arms raised. If necessary, the patient was shifted into an appropriate contralateral posterior oblique position so that the lateral and inferior parts of the breast could be scanned. US was targeted first to the index lesion and the surrounding breast tissue in the same quadrant, then to the remainder of the ipsilateral breast, and then to the contralateral breast. Additional foci were considered to exist and were documented when they appeared more than 2 cm from the index lesion at US. Scanning was performed in the radial and antiradial planes, as well as in the longitudinal and transverse planes (17). The examination took approximately 20 minutes (range, 15–45 minutes).
All solid lesions detected at US were prospectively analyzed and assessed in consensus by two radiologists (including W.K.M.). At US, the solid lesions were described according to their shape as round, lobular, or irregular; according to their orientation as wider than tall or taller than wide; according to their echogenicity as hyperechoic, isoechoic, mildly hypoechoic, or markedly hypoechoic; according to their echotexture as homogeneous or heterogeneous; according to their margin as well defined, microlobulated, ill defined, or spiculated; according to their acoustic transmission as shadowing, enhancing, or normal; and according to their boundary echo as having a pseudocapsule or a thick echogenic rim (17,18). The size of each lesion was measured along the widest dimension. All solid lesions detected at US alone were categorized according to BI-RADS final assessment categories (16). Each lesion was further categorized as benign (ie, benign or probably benign) or malignant (ie, suspicious or highly suggestive for malignancy). Diagnostic accuracy, including sensitivity, specificity, and positive and negative predictive values, was calculated for the detection of lesions at US.
In patients with additional cancers seen only at US, the mammograms were retrospectively analyzed by the same radiologist who performed the US examinations to determine why the cancers were not detected at mammography. In each case, the failure to detect additional cancers was attributed to one of the four known factors (poor mammographic technique, interpretation error, anatomic area not included at routine mammography, and presence of obscuring dense parenchyma) (19). The density of tissue at the tumor site was recorded if the tumor was included on the mammogram.
Biopsy and Surgery
All solid lesions detected at US were sampled for biopsy with a 14-gauge automatic biopsy gun and US guidance or after US-guided needle localization. In 24 patients, instead of core needle biopsy, surgical excision after US-guided needle localization was used for histologic confirmation of additional foci because the US examination was performed the day before the operation. A radiograph of the specimen was obtained in all patients. US of the specimen was performed in 16 patients at the surgeon’s request because excision of the lesion was uncertain or out of concern that the hook wire may not have been located in the center of the mass.
All patients underwent surgery within 1 week of US examination. In our institution, most patients with a tumor larger than 3 cm and patients with multicentric cancers undergo mastectomy instead of conservation surgery. The patient’s preference and the size of the breast was considered in all cases. After lumpectomy or mastectomy, serial 10-mm slices were evaluated by pathologists, and additional slices were prepared from any grossly suspicious areas. Multifocal cancer was defined as the presence of two or more foci of cancer in one quadrant that were separated by 2 cm of normal parenchyma. Multicentric cancer was classified as the presence of two or more foci of cancer in different quadrants. All cases were reviewed at a multidisciplinary conference that included a comparison of the imaging and histopathologic findings. If there was a change in the care of the patient after US, it was recorded at the conference.
Statistical Analysis
To determine whether the detection rate of mammographically and clinically occult cancer at US was related to the size and palpability of the index lesion or to breast composition, statistical analysis was performed with a statistical software program (SAS for Windows, version 6.12; SAS Institute, Cary, NC). Index lesions seen at US were separated into two groups according to size: those 2 cm or smaller and those larger than 2 cm. Each breast was classified into one of the two following groups according to its composition: fatty (grade 2) and dense (grades 3 and 4). The Fisher exact and 
2 tests were used; findings with a P value less than .05 were considered statistically significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Of patients with malignant disease, 113 (56%) had a single tumor, 43 (21%) had multifocal cancer, and 30 (15%) had multicentric cancer in the same breast. Fifteen (7%) patients had bilateral breast cancer. Of the 15 patients with bilateral breast cancer, nine also had multifocal or multicentric tumors in the ipsilateral breast. Of patients with benign lesions, 19 (33%) had a benign lesion in the ipsilateral breast, 28 (48%) had a benign lesion in the contralateral breast, and 11 (19%) had benign lesions in both breasts. The average lesion size was 18 mm (median, 20 mm; range, 4–76 mm) for malignant tumors and 17 mm (median, 19 mm; range, 3–87 mm) for benign lesions. Of the 201 patients with breast cancer, 19 (9%) had stage 0 (DCIS) cancer, 56 (28%) had stage I cancer, 97 (48%) had stage II cancer, and 29 (14%) had stage III cancer. For treatment of ipsilateral cancer, mastectomy was performed in 161 (80%) patients; breast conservation therapy was performed in 40 (20%). For treatment of the 15 patients with bilateral cancer, contralateral mastectomy was performed in five (33%) patients; breast conservation therapy was performed in 10 (67%).
Of the 289 malignant tumors, 131 (45%) were clinically occult. Of these 131 lesions, 68 (52%) could be seen at mammography and US, 14 (11%) were seen at mammography alone, and 36 (27%) were detected on US images alone. The remaining 13 lesions (10%)—six foci of invasive cancer and seven foci of DCIS—were detected only at histopathologic analysis of the mastectomy specimen. The identification methods of 289 malignant foci are summarized in Table 1. Mammography with clinical examination and US revealed 173 (86%) of 201 invasive tumor foci and 56 (81%) of 69 foci of DCIS in ipsilateral breasts and six (50%) of 12 invasive tumor foci and five (71%) of seven foci of DCIS in contralateral breasts, whereas US depicted 194 (97%) invasive tumor foci and 52 (75%) foci of DCIS in ipsilateral breasts and 11 (92%) invasive tumor foci and four (57%) foci of DCIS in contralateral breasts. The 36 malignant foci in 36 patients that were seen only at US included 24 foci of infiltrating ductal carcinoma, four foci of infiltrating lobular carcinoma, and eight foci of DCIS (of which one was comedocarcinoma and seven were noncomedocarcinoma). Of the 36 malignant foci in 36 patients seen only at US, 28 (20 foci of infiltrating ductal carcinoma, two foci of infiltrating lobular carcinoma, and six foci of DCIS)—including 18 foci of multicentric cancers—were in ipsilateral breasts, and eight (four foci of infiltrating ductal carcinoma, two foci of infiltrating lobular carcinoma, and two foci of DCIS) were in contralateral breasts.
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Imaging findings and final assessment (according to BI-RADS categories) of 77 lesions in 73 patients seen with US alone are summarized in Tables 2 and 3. They proved to be 28 invasive and eight intraductal cancers, 32 cases of fibrocystic change (of which two were adenosis, five were papilloma, 22 were ductal hyperplasia without atypia, and three were atypical ductal hyperplasia), and nine fibroadenomas. The additional benign lesions found in 37 patients were in the ipsilateral breast in 12 patients, in the contralateral breast in 21 patients, and in both breasts in four patients. At US, a lobular shape (n = 5), mild hypoechogenicity (n = 5), ill-defined margin (n = 5), normal acoustic transmission (n = 7), and lack of associated pseudocapsule (n = 8) were more commonly seen in DCIS lesions (Fig 1), whereas an irregular shape (n = 18), marked hypoechogenicity (n = 18), spiculated margins (n = 12), posterior acoustic shadowing (n = 8), and thick echogenic halo (n = 5) were more frequently seen in invasive cancers (Figs 1 and 2).
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For the 36 additional cancers seen only at US, the failure to detect these cancers at mammography was attributed to poor mammographic technique in two cases (6%), interpretation error in five cases (14%), peripheral location of the tumor (ie, it was not included on the mammograms) in seven cases (19%), and presence of obscuring dense parenchyma in 22 cases (61%). In 29 cases with the tumor area included on the mammograms, the density of tissue at the tumor site was minimally dense in three cases, heterogeneously dense in nine cases, and extremely dense in 17 cases.
The therapeutic procedure was changed in 32 (16%) of the 201 patients because US depicted more extensive disease than was appreciated at mammography or at clinical evaluation. In eight of the 10 patients with multifocal lesions seen at US alone, a wider excision (two patients) or mastectomy (six patients) was performed instead of the planned lumpectomy. The remaining two patients underwent mastectomy anyway because the primary tumor was larger than 3 cm. In 16 of the 18 patients with multicentric lesions seen at US alone, mastectomy was performed instead of lumpectomy (Fig 1). The remaining two patients underwent mastectomy anyway because the primary tumor was larger than 3 cm. Of the eight patients with synchronous contralateral carcinoma seen at US alone, six underwent lumpectomy (Fig 2) and two underwent mastectomy in addition to ipsilateral surgical intervention. US alone demonstrated 20 false-positive lesions in 16 patients (8%). Three patients with atypical ductal hyperplasia detected at US underwent surgical excision. No patient underwent mastectomy on the basis of US findings that proved to be histologically benign.
US was more likely to depict mammographically and clinically occult cancer in women who had a larger index lesion or a palpable tumor than in women who had a smaller index lesion or a nonpalpable tumor. Of 36 additional cancers detected at US, 28 were found in the 96 women who had an index tumor larger than 2 cm (ie, 29% [28 of 96] of these women had additional cancer), whereas eight were found in the 105 women who had an index tumor of 2 cm or smaller (ie, 8% of these women had additional cancer) (P < .001). Thirty-one cancers were found in the 134 women who had a palpable mass (ie, 23% of these women had additional cancer), whereas five cancers were found in the 67 women who had a nonpalpable mass (ie, 7% of these women had additional cancer) (P < .01). Mammographically and clinically occult disease was more frequently found at US in patients with dense breasts than in patients with fatty breasts: 33 cancers were found in the 130 women with breasts with a density grade of 3 or 4 (ie, 25% of these women had additional cancer), and three cancers were found in the 71 women with breasts with a density grade of 2 (ie, 4% of these women had additional cancer) (P < .001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The results of two prospective studies (28,29) in an asymptomatic population have shown that US can play a role in the detection of mammographically and clinically occult carcinoma in dense breasts. In their study of 3,626 women with dense breasts (breast density grades 2 through 4), normal mammograms, and normal physical examinations, Kolb et al (28) found 11 (0.30%) cancers with screening US. Of these, nine (82%) were 1 cm or smaller. Overall cancer detection increased by 17%, and the number of tumors detected only with mammography and US increased by 37% (from 30 to 41 tumors). Two hundred four (5.6%) of all US screening patients had a solid mass that proved to be benign. Similar results were reported in a large series by Buchberger et al (29). In these two studies, US examination was performed by radiologists who specialized in breast US, and a 7.5- or 10-MHz linear transducer was used.
Once a probable cancer has been identified, the role of preoperative imaging in breast conservation surgery is to enable evaluation of the extent of the tumor, to help assess the contralateral breast for unsuspected synchronous breast cancer, and to guide excision of nonpalpable cancers. The results of our study show that US can depict invasive and noninvasive breast carcinomas that are both mammographically and clinically occult, offering the potential for more accurate breast cancer staging and optimized treatment planning. In our study, 12% (36 of 289) of all cancers were detected at US alone. US depicted additional multifocal or multicentric cancer in 5% (10 of 201) and 9% (18 of 201) of patients, respectively. Because of this information and the resulting changes in staging, the therapeutic procedure was changed from lumpectomy to wider excision or mastectomy in 86% (24 of 28) of these patients.
Additional contralateral carcinomas that were not palpable clinically and were not visible at conventional mammography were also depicted at US alone in 4% (eight of 201) of our patients. All of these patients underwent lumpectomy or mastectomy in addition to surgical intervention targeting the primary tumor. In patients with breast cancer, incidentally detected lesions in the contralateral breast, as well as lesions in the ipsilateral breast, are more likely to be malignant (15,30–32). In our series, with the exclusion of index lesions, of 77 lesions incidentally detected only at US, 36 (47%) were malignant. US-guided core biopsy and needle localization were used for histologic confirmation of the additional foci detected at US and provided valuable information in treatment planning. Further study is needed to investigate the clinical importance of additional foci of carcinoma, especially foci of DCIS, detected only at US imaging in patients with newly diagnosed breast cancer.
Compared with previous researchers (15,32–34), we detected more nonpalpable invasive cancers and DCIS lesions with US. Eight (11%) of 76 foci of DCIS were found at US alone. They represented 22% (eight of 36) of additional cancers detected at US. Our findings are largely a result of improved US technology and training on the part of the scanning physician (35,36). We used a 10-, 12-, or 13-MHz linear transducer. US scanning was performed in radial and antiradial planes, as well as in longitudinal and transverse planes. In our study, breast cancers that manifested as clusters of intermediate-concern microcalcifications (ie, American College of Radiology BI-RADS category 4 lesions) and breast cancers that occurred in entirely fatty breasts were excluded; this probably augmented the performance of US. The large size of the index tumors (average, 18 mm; median, 20 mm) and the more advanced stages of the tumors (62% of patients had stage II or stage III cancer) in our study could be a bias.
In addition to cancers, many benign lesions are found at US performed for preoperative breast cancer staging. The identification of one or more additional solid lesions at a distance from the primary tumor or in the contralateral breast may require an increase in the amount of tissue excised or a second incision. To improve the specificity of interpretation of US findings, Stavros et al (17) used a strict classification scheme to predict the benignity of 750 solid masses detected at US. Of the 424 masses that were predicted to be benign, only two proved to be malignant. This result suggests that follow-up is a reasonable alternative to biopsy of lesions that are probably benign on the basis of US findings. In our study, no cancer was found in lesions that were classified at US as probably benign, and the sensitivity, specificity, and positive and negative predictive values of prospective US classification of solid masses were 100% (36 of 36), 51% (21 of 41), 64% (36 of 56), and 100% (21 of 21), respectively.
We tried to characterize a subgroup of patients who would most benefit from preoperative bilateral whole-breast US. Our results show that patients with large palpable tumors and those with dense breast parenchyma are most likely to have additional tumors detected at bilateral whole-breast US. Of 36 additional cancers detected at US, 78% were found in patients who had an index tumor larger than 2 cm, whereas 22% were found in patients who had an index tumor 2 cm or smaller; 92% of these cancers were found in patients with dense (grade 3 or 4) breasts, whereas 8% were found in patients with fatty (grade 2) breasts. Increasing size of the primary tumor has been known to correlate with the frequency of both multicentricity and bilaterality (37). In our study, 67% (134 of 201) of patients had a palpable mass, and the average tumor size was 18 mm. A family history of breast cancer, younger age, and lobular histologic type are also risk factors for bilateral breast cancer (38). Malignant lesions are more difficult to detect in mammographically dense breasts because of technical factors including reduced image contrast and sharpness and because many cancers have the same density as normal fibroglandular elements (5). Adjunctive preoperative imaging probably has a greater diagnostic role in the nonfatty breast.
Magnetic resonance (MR) imaging of the breast shows great promise as a preoperative planning procedure in defining the extent of cancer within the breast. Reported rates of mammographically and clinically occult multifocal or multicentric cancers that were detected at MR imaging have ranged from 16% to 37% (39–43); rates of contralateral cancers that were detected at MR imaging have ranged from 3.2% to 11% (43–45). According to the results of three studies comparing MR with mammography and US, contrast-enhanced MR imaging seems to be superior to US for the evaluation of the extent of disease, particularly in terms of sensitivity (43,46,47). The reported sensitivity of MR imaging for demonstration of invasive cancer has approached 100% in several series (41,42,46,48). However, the cost and difficulty of sampling lesions depicted only at MR imaging for biopsy have limited the clinical effectiveness of this modality (49,50). There is also no simple equivalent to radiography or US of specimens to confirm successful sampling.
Bilateral whole-breast US has limitations and should not replace mammography as the initial imaging procedure for staging of breast cancer. The mammogram is essential in providing a "road map" for US. Optimum mammographic film technique, including compression and penetration of dense tissue, is critical if subtle lesions are to be detected. In this study, additional views were obtained in only 65% (130 of 201) of patients; more use of additional views could have improved our detection of additional tumor foci at mammography. As physicians do at most breast imaging centers, we performed US as an adjunct to mammography with full knowledge of the clinical and mammographic findings. US of the specimen was not performed routinely in our institution; this could be a limitation to this study. US of the specimen can help verify the complete removal of nonpalpable tumors seen only at US (15,51).
In summary, preoperative bilateral whole-breast US depicted mammographically and clinically unsuspected multifocal, multicentric, and contralateral carcinomas in 18% (36 of 201) of patients with breasts grades 2 through 4 in density. On the basis of US findings, therapy was correctly changed in 16% (32 of 201) of patients. Mammographically and clinically occult cancer was more frequently found at US in patients with large (>2 cm) palpable masses and in patients with dense (grade 3 or 4) breasts than in patients with small (
2 cm) nonpalpable masses and in patients with fatty (grade 2) breasts. Bilateral whole-breast US can be complementary to mammography in the preoperative evaluation of breast cancer, particularly in patients with a large palpable mass and in those with dense breasts. Further study is needed to determine whether the use of breast US in staging and treatment planning leads to a decrease in the rate of tumor recurrence; the cost-effectiveness of this approach must also be determined.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, W.K.M.; study concepts and design, W.K.M., D.Y.N., J.G.I.; literature research, W.K.M.; clinical studies, W.K.M.; data acquisition and analysis/interpretation, W.K.M., D.Y.N.; statistical analysis, W.K.M.; manuscript preparation, definition of intellectual content, editing, revision/review, and final version approval, W.K.M., D.Y.N., J.G.I.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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