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Original Research |
1 Department of Radiology and Center for Imaging Science, Samsung Medical
Center, Sungkyunkwan University School of Medicine, 50 Irwon-dong, Gangnam-ku,
Seoul 135-710, Korea.
2 Department of Radiology, Inje University College of Medicine, Busan Paik
Hospital, Busan, Korea.
3 Department of Radiology, Catholic University of Daegu, College of Medicine,
Daegu, Korea.
4 Department of Pathology, Samsung Medical Center, Sungkyunkwan University
School of Medicine, Seoul, Korea.
Received July 12, 2007;
accepted after revision March 21, 2008.
Address correspondence to E. Y. Ko
(claudel{at}skku.edu).
Abstract
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MATERIALS AND METHODS. One hundred eighty-nine synchronous nodules in 147 breast cancer patients were surgically excised after localization, and 412 synchronous nodules in 191 patients were observed or biopsied or excised without localization. Among a total of 601 synchronous nodules, 372 nodules were ipsilateral and 229 were contralateral to a primary malignant tumor. Two radiologists retrospectively reviewed sonograms of these nodules and determined the sonographic BI-RADS category without clinical information or pathologic results. For each nodule, the preoperative BI-RADS category and pathologic or follow-up results were compared.
RESULTS. Four hundred eighty-two nodules were classified category 3; 112 nodules, category 4; and seven nodules, category 5. Fifty-five (11.4%) of the category 3 nodules and 57 (47.9%) of the category 4 and 5 nodules were confirmed malignant. Thirty-six (21.2%) of 170 category 3 synchronous nodules in the same quadrant as the primary tumor were confirmed malignant, as were 12 (9.8%) of 122 nodules in a different quadrant and eight (4.2%) of 190 nodules in the contralateral breast.
CONCLUSION. For assessment of synchronous nodules in breast cancer patients, application of conventional screening sonographic BI-RADS categories may not account for possible increased risk of malignancy in synchronous nodules, especially those in the same quadrant of the breast as the index malignant tumor.
Keywords: BI-RADS • breast cancer • sonography • synchronous
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Breast sonography has been suggested as an adjunct to mammography in the preoperative evaluation of patients with breast cancer [5–7]. The American College of Radiology has applied its BI-RADS to sonography [8]. To our knowledge, however, little has been discussed regarding application of the current sonographic BI-RADS to assessment of synchronous nodules in breast cancer patients. This study was designed to evaluate the applicability of the current sonographic BI-RADS to synchronous breast nodules other than the primary malignant tumor in breast cancer patients.
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In cases of synchronous nodules in the same quadrant of the ipsilateral breast, clinicians excised nodules easily with minimal extension of the surgical margin. Especially in women with small, thin breasts, breast-conserving surgery is not markedly different from quadrantectomy in many cases. Therefore, synchronous nodules in the same quadrant usually were excised with the main tumor. Synchronous nodules in a different quadrant of the ipsilateral breast or in the contralateral breast were selectively excised to confirm the safety of breast-conserving surgery, in consideration of the patient's anxiety, in cases of high risk of breast cancer, or according to the surgeon's preference.
We retrospectively evaluated pathologic results or clinical course (corresponding to synchronous nodules larger than 5 mm in diameter not excised with localization) by reviewing results of a comparative analysis between radiologic and pathologic results or follow-up sonographic images. For excised nodules, we sorted the pathologic findings into benign and malignant lesions. Malignancy was suggested when there was precise matching of sonographic findings and pathologic results, including size and direction and distance from main mass. Other nodules were considered benign unspecified. Patients who had multiple malignant masses without a dominant one were excluded from the study.
We used sonographic units (HDI 5000, Advanced Technology Laboratories; iU22, Philips Healthcare; Logiq 700, GE Healthcare) equipped with 12- to 5-MHz linear-array transducers. All sonographic examinations were performed or supervised by experienced board-certified breast radiologists with at least 5 years of experience in breast sonography. We routinely reviewed mammograms before performing sonography; therefore, radiologists performed sonography with knowledge of the mammographic findings.
Two radiologists with 5 and 2 years of experience in breast imaging retrospectively reviewed the preoperative sonographic images of each synchronous nodule and in consensus divided the nodules into categories according to the sonographic BI-RADS classification [8–10]. Cate gory 1 was no abnormality; category 2, benign finding, such as simple cyst or nodule with intense homogeneous hyperechogenicity; and category 3, solid hypoechoic oval or gently lobulated mass with circumscribed margins and an orientation parallel to the skin (possible fibroadenoma) or complicated cysts or clustered microcysts. We looked for suspicious sonographic findings, such as irregular shape, complex echogenicity, posterior shadowing, spiculated margins, microlobulated margins, nonparallel orientation, microcalcifi cations, and duct extension. Nodules with any suspicious findings were classified category 4. Nodules with three or more suspicious findings were classified category 5. The reviewers were aware that all of the patients had breast cancer. They were blinded to other clinical information, initial sonographic report or diagnosis, and the pathologic results on synchronous nodules.
Review of sonographic images was performed with digitalized images on the 5,000-pixel monochrome liquid crystal display monitor (ME551i2-B/C, Totoku) of a PACS. Only images of the synchronous nodules concerned were presented to reviewers. We compared sono graphic BI-RADS category and postoperative pathologic result for each nodule. Visualization of synchronous nodules on mammograms and the palpability of these nodules were correlated through survey of radiologic reports and medical records. We also evaluated the pathologic results or clinical course (corresponding to synchronous nodules larger than 5 mm not excised with localization) by reviewing results of a comparative analysis of radiologic and pathologic results or follow-up sonographic images. Institutional re view board approval was not required for this retrospective study at our institution.
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One hundred eighty-nine synchronous nodules in 147 patients were excised after sonographically guided tattooing localization during surgery for the main mass. All 147 patients were women (mean age, 47 years; range, 24–77 years). The mean size of nodules measured on sonography was 8.2 mm (range, 2.3–21.4 mm). All 189 synchronous nodules were not palpable and necessitated sonographically guided localization for excision. The final pathologic results for all 189 nodules are described in Table 1.
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The synchronous nodules not preoperatively localized were excised incidentally during the operation in cases of nodules in the same quadrant or in cases of mastectomy (n = 235), biopsied in cases of a palpable lesion (n = 9), or not excised but followed up (n = 318). Some nodules (n = 112) were too small (< 5 mm) to match with the pathologic result or follow-up sonographic images, and some nodules were not followed up (n = 23). We excluded category 2 nodules (n = 121) from analysis, because numerous cysts might have been passed over and not described during the preoperative sonographic examination. The mean follow-up period was 22 months (range, 5–49 months). The follow-up period was shorter than 12 months for 26 nodules and shorter than 24 months for 150 nodules. Nodules that did not change in size or became smaller were considered benign.
The locations of synchronous nodules in relation to primary malignant tumors are shown in Table 2. The incidence of benign and malignant findings according to each category is shown in Table 3. The incidence of malignancy according to location in each category is shown in Table 4. The rate of malignancy among the 482 category 3 nodules was 11.4%. Among 143 category 3 nodules excised after localization, 37 (25.9%) of the nodules were malignant (Fig. 2A, 2B). Among 339 category 3 nodules followed up or excised without localization, 18 (5.3%) of the nodules were malignant. Fifty-seven (47.9%) of the total 119 category 4 and 5 nodules were malignant, and 62 (52.1%) were benign (Fig. 3). Ipsilateral category 3 nodules were more likely to be malignant than were contralateral nodules, 48 (16.4%) of 292 versus eight (4.2%) of 190 (Fig. 4A, 4B, 4C). Among category 3 ipsilateral nodules, nodules in the same quadrant were more likely to be malignant than were nodules in another quadrant, 36 (21.2%) of 170 versus 12 (9.8%) of 122 (Fig. 5A, 5B, 5C).
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Mammograms were available for 185 of 189 synchronous nodules excised after localization. Among 185 nodules on mammograms, 27 synchronous nodules, including five malignant nodules and 22 benign nodules, were found before sonography. Overall, 49 (90.7%) of 54 malignant nodules and 109 (83.2%) of 131 benign nodules were mammographically occult.
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Sonographic BI-RADS was introduced more recently than BI-RADS for mammography, and radiologists have relatively little experience with it. Only a few publications [9–12] have dealt with sonographic BI-RADS, and the studies involved only small numbers of patients. Hong et al. [11] reported high positive and negative predictive values of features in the sonographic BI-RADS lexicon for evaluating solid masses. Lazarus et al. [12] reported good interobserver agreement among radiologists using the sonographic BI-RADS lexicon. Those reports, however, concerned only the primary mass. To our knowledge, there has been no study of the evaluation of satellite nodules around the main mass with sonographic BI-RADS. Probability of malignancy differs according to BI-RADS category [8, 13]. In category 2, there is almost no risk of cancer; category 3, very low risk (< 2%) of malignancy; category 4, 3–94% probability of malignancy; and category 5, more than 95% probability of malignancy.
In our study, the overall incidence of malignancy of category 3 nodules was higher (11.4%) than the generally accepted probability (< 3% in category 3) and much higher (21.2%) in the same quadrant of the ipsilateral breast. Probability of malignancy of category 3 nodules increased according to the location of the nodules relative to the primary breast malignant tumor. In order, the probabilities were same quadrant in ipsilateral breast, 21.2%; different quadrant in ipsilateral breast, 9.8%; and contralateral breast, 4.2%. Category 4 and 5 nodules had similar results. The incidence of malignancy of category 5 nodules was slightly less than expected because only four cases involved synchronous category 5 nodules.
The risk of malignancy associated with different BI-RADS categories in our study was quite different from that reported in previous studies [11–13]. We believe risk of malignancy in this limited population—breast cancer patients with synchronous nodules—may be different from that in a screening population. Category 3 nodules not excised or incidentally included in the surgical specimen without preoperative localization also had a higher rate of malignancy than is generally accepted, even though without definite matching of sonographic finding and pathologic satellite malignancy, most of them were classified benign unspecified. According to these results, in synchronous breast nodules detected on preoperative sonography in patients with breast cancer, agreement between probability of malignancy based on current sonographic BI-RADS categories and pathologic results was much lower than expected. The risk of malignancy in synchronous breast nodules was related to distance from the primary malignant tumor.
In our study, the rate of malignancy of mammographically occult nodules was slightly higher than that of mammographically visible nodules. However, the number of nodules found on mammography was small (27/185), and most of the patients were relatively young (mean age, 47 years) and had a higher rate of dense breasts. Therefore, we believe visualization on mammograms does not correlate with rate of malignancy and is much influenced by the size of synchronous nodules and the background breast composition.
There were limitations to our study. First, precise correlation with pathologic findings usually was impossible for synchronous nodules not tattooed and localized under sonographic guidance and incidentally included in the surgical specimen. In those cases, radiologic findings and pathologic results were carefully compared, but most of the nodules were classified benign unspecified. The exceptions were cases of obvious satellite malignant lesions precisely corresponding to the synchronous nodule on sonography. Because of the possibility of missing small foci of incidental malignant tumors not localized preoperatively during pathologic review, we might have underestimated the rate of malignancy of these synchronous nodules. The short follow-up period for nodules not excised and followed up also might have led to underestimation of the rate of malignancy. Another limitation was that all reviewers knew synchronous nodules can occur in patients with breast cancer. This factor might have resulted in overestimation of the sonographic BI-RADS category for each nodule.
Another limitation was that synchronous nodules excised after localization were more frequently malignant than were nodules not excised and followed up. This finding suggests that we must have preferably excised lesions that looked suspicious, even though they had been classified category 3. It also is possible that the difference in proportion of nodules according to location influenced the different rates of malignancy between the excision and preservation groups. Classifying as benign unspecified most of the synchronous nodules excised without preoperative localization also might have affected the results.
At our institution, we prefer sonographically guided tattooing localization and excision biopsy of synchronous nodules during surgery to additional biopsy for synchronous nodules after confirmation of the primary malignant tumor. Our purpose is to avoid additional preoperative biopsy to save time before surgery. Usually 1 week elapses between confirmation of primary malignancy and surgical treatment. However, we have a long waiting list for breast sonography and sonographically guided biopsy, and it can take as long as several days to obtain histologic results after biopsy. Therefore, surgical excision usually was performed for synchronous nodules without preoperative biopsy. However, it seems more prudent and desirable to perform preoperative biopsy of synchronous BI-RADS category 3 nodules than to excise them surgically.
For assessment of synchronous nodules in patients with breast cancer, uniform application of the current sonographic BI-RADS classification can lead to underestimation of the risk of malignancy, especially if the nodule is in same quadrant as the index lesion. Our results suggest that for accurate assessment of candidacy for breast-conserving surgery, biopsy is needed for synchronous nodules in the same quadrant as and maybe even in the same breast that contains a malignant tumor, even nodules considered probably benign according to conventional BI-RADS sonographic criteria.
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