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Breast Imaging |
1 From the Iris Cantor Center for Breast Imaging, Department of Radiological Sciences, UCLA School of Medicine, 200 UCLA Medical Plaza, Rm 165-49, Los Angeles, CA 90095-6952 (G.R., A.C.S., J.S.P., J.W.S., L.W.B.); the Department of Radiology, Olive View-UCLA Medical Center, Sylmar, Calif (G.C.H.); the West Los Angeles Veterans Administration Medical Center, Calif (M.L.M.); and the Department of Radiology, Indiana University School of Medicine, Indianapolis (H.E.R., V.P.J.). From the 1996 RSNA scientific assembly. Received August 4, 1998; revision requested September 4; final revision received March 16, 1999; accepted July 1. Address reprint requests to L.W.B.
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Abstract |
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MATERIALS AND METHODS: One hundred sixty-two consecutive solid masses with a tissue diagnosis were reviewed. Three radiologists reviewed the masses without knowledge of clinical history or histologic examination results.
RESULTS: US features that most reliably characterize masses as benign were a round or oval shape (67 of 71 [94%] were benign), circumscribed margins (95 of 104 [91%] were benign), and a width-to–anteroposterior (AP) dimension ratio greater than 1.4 (82 of 92 [89%] were benign). Features that characterize masses as malignant included irregular shape (19 of 31 [61%] were malignant), microlobulated (four of six [67%] were malignant) or spiculated (two of three [67%] were malignant) margins, and width-to–AP dimension ratio of 1.4 or less (28 of 70 [40%] were malignant). If the three most reliable criteria had been strictly applied by each radiologist, the overall cancer biopsy yield would have increased (from 23% to 39%) by 16%. When US images and mammograms were available, the increase in biopsy yield contributed by US was not statistically significant (2%, P = .73). However, in independent reviews, one to three reviewers interpreted four carcinomas as benign at US.
CONCLUSION: The data confirm that certain US features can help differentiate benign from malignant masses. However, practice and interpreter variability should be further explored before these criteria are generally applied to defer biopsy of solid masses.
Index terms: Breast, US, 00.12981, 00.12985 • Breast neoplasms, diagnosis, 00.12981, 00.12985, 00.30 • Breast neoplasms, radiography, 00.11, 00.30 • Breast neoplasms, US, 00.12981, 00.12985, 00.30 • Breast radiography, comparative studies, 00.11
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Introduction |
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In the 1970s, use of US decreased the number of biopsies for benign masses 25%–35% by enabling reliable identification of simple cysts (4,5). In the 1980s, investigators reported US features that occurred more frequently in benign solid breast masses and other features that occurred more frequently in malignant masses (6–8). However, in subsequent studies, US results were not yet reliable enough to determine whether biopsy should be performed on a solid mass (9–11). Nonetheless, investigators continued to pursue US features that would be typical of either benign or malignant lesions (12).
Improvements in US equipment have prompted more recent studies (13) with findings that describe reliable signs for differentiating benign from malignant masses. However, it is important to determine if these results are reproducible when applied to practices with different US equipment, operator experience, interpreting physicians, and patient populations. It is also important to establish the interobserver variability in the assessment of these features, since to our knowledge this has not been reported.
Furthermore, the additional contribution of US needs to be determined for women in whom mammography has been performed (14). To investigate the general applicability and interobserver variability of US features to distinguish benign from malignant solid masses in other practices, we conducted a retrospective analysis of 162 consecutive cases in which patients underwent breast US followed by tissue diagnosis at two institutions. We also evaluated the additional contribution of US for those women with available mammograms.
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MATERIALS AND METHODS |
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In 50 cases in which results of the core-needle or fine-needle biopsy were either positive for malignancy or not definitive, surgical excision was performed, as is our usual protocol. A needle biopsy result was considered not definitive if the imaging and histologic findings were discordant or if needle biopsy results indicated insufficient sampling. The examinations were performed at two hospitals with different staff and physicians; one is a university outpatient center and the other is a county facility in a different city of the same county.
The patients' age range was 22–75 years (mean age, 47 years). In our practices, US is routinely performed for palpable masses as an initial imaging examination in women younger than 30 years to better define a mammographically detected mass and to image a mass not visible at mammography. US is performed for nonpalpable, mammographically detected masses to rule out cysts or to determine whether the mass is amenable to US-guided tissue sampling.
There were 118 palpable masses and 44 nonpalpable masses. Thirty-eight of the masses proved to be malignancies, of which 31 were infiltrating ductal carcinomas not otherwise specified, two were infiltrating lobular carcinomas, two were medullary carcinomas, two were malignant phyllodes tumors, and one was an infiltrating mucinous carcinoma. Mammograms were available for 133 cases, including 32 malignancies. Mammograms were not available for 29 cases, including cases in younger women who presented with a palpable mass and did not undergo mammography and in several women in whom mammography had been performed elsewhere and results could not be retrieved at the time of the study.
US Examination Technique
All US examinations were performed with either a model VST unit (Diasonics, Milpitas, Calif) with a 10-MHz linear-array transducer or a model 5200 unit (Acoustic Imaging, Phoenix, Ariz) with a 7-MHz linear-array transducer. The scanning protocol included both transverse and longitudinal real-time imaging of the solid masses, with representative hard-copy images acquired in each plane. Faculty radiologists specializing in breast imaging either performed the examinations themselves or supervised a specially trained radiologic technologist or a board-certified radiologist who was participating in breast imaging fellowship training.
Retrospective Evaluation of Cases
Three faculty radiologists (M.L.M., H.E.R., V.P.J.) experienced in breast imaging reviewed the hard-copy US images and the mammograms. The three reviewers were not from the facilities where the images were obtained and interpreted and had no previous knowledge of any of the cases or the original interpretations. The patients' clinical histories, previous imaging results, and tissue sampling results were not available to them.
Each of the radiologists was requested to review the cases independently in three different phases: In phase 1, the reviewers evaluated only the US scans. In phase 2, the reviewers evaluated only the mammograms for those patients in whom mammograms were available. In phase 3, the reviewers evaluated the US scans in conjunction with the mammograms. The interval between each of the three phases averaged 2–3 weeks.
US Image Review
For the US scans of the solid masses, the three reviewers were asked to assess the following criteria from the literature (12,13): shape (oval, round, lobulated, or irregular), margins (circumscribed, ill defined, spiculated, or microlobulated), width-to-anteroposterior (AP) dimension ratio, posterior echoes (enhanced, unaffected, or decreased), echogenicity (intensity of internal echoes), echotexture (homogeneity of internal echoes), presence of calcifications, presence of lateral edge refraction, and presence of a pseudocapsule.
Establishing a standardized final assessment for each case was important for categorization of the results and analysis of statistics. Therefore, by using the US findings, the reviewers were asked to provide a final assessment category modeled on the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS) (15) to indicate the probability of malignancy. Thus, each mass was further categorized as benign (negative, benign, or probably benign) or malignant (showing a suspicious abnormality or highly suggestive of malignancy).
To establish a baseline consensus in terminology, US diagnostic criteria, and final assessment categories, training sessions were held wherein the study readers evaluated images of 15 biopsy-proved masses. The 15 cases were selected from the study group because they represented a variety of benign and malignant masses. They were excluded from the final study set.
Mammogram Review
For the mammograms, the reviewers were asked to assess standard criteria including size, shape, margins, presence of microcalcifications, and presence of architectural distortion. On the basis of this evaluation, a BI-RADS final assessment category was assigned by each reader.
Mammogram and US Image Review
The reviewers evaluated the cases in which both US and mammography were performed and assigned a final assessment category that took into account the findings of each.
Analysis of Data
The statistical analysis of the data was supervised by a biostatistician (J.W.S.) experienced in imaging research. For the US evaluation phase of the study, each US characteristic was analyzed to determine its association with a benign versus malignant tissue diagnosis. For each reader, the final assessment categories were compared with the tissue diagnoses to determine sensitivity, specificity, and positive predictive value for US alone, mammography alone, and the two modalities used simultaneously. A 
2 test was used to determine statistical significance. Interobserver agreement was assessed for each US characteristic with the 
statistic (16).
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RESULTS |
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Some features that showed excellent correlation with a benign or malignant tissue diagnosis were too infrequent to be generally applicable. For example, a hyperechoic lesion was very reliable as a predictor of benignity but was reported in only 2% of the masses.
Table 2 reports on interobserver variability for specific lesion features. The readers' agreement was calculated with statistics and was generally considered excellent when the value was greater than 0.8 (16). The three reviewers had high agreement for most of the US features. Two features were potentially predictive of a benign tissue diagnosis but showed low interobserver agreement. These were the presence of a pseudocapsule (for agreement, = 0.713) and homogeneous echotexture ( = 0.604).
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In their actual evaluation of the cases, by using the US diagnostic criteria to determine which women should undergo tissue sampling, the readers would have increased the overall positive predictive value for these cases (number of cancers detected divided by number of biopsies recommended) from 23% (original assessments) to 34% (mean of responses of the three reviewers).
On the basis of the readers' overall impressions, four cancers were categorized as benign at US by at least one of the reviewers (Table 3). These cases did not show typical features of malignancy; however, they did not meet all of the criteria of benignity defined in the strictest sense when viewed in retrospect and with knowledge of the biopsy results.
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In the last case, one reader assessed the cancer as benign on US images but correctly identified it as malignant on mammograms and at the combined US image and mammogram evaluation.
Five malignancies were either not visible or were interpreted as benign on mammograms by at least one of the readers (Table 3). Three of these malignancies were correctly assessed as suspicious by the same readers when they had access to the US images. One of the five malignancies was incorrectly identified as benign by all three observers on US images. The remaining malignancy was identified as benign by one observer but was correctly identified as suspicious by the other two.
Results of the evaluation of the 133 cases in which both mammography and US were performed are shown in Table 4. When both examinations were performed, there was a trend toward increased sensitivity, positive predictive value, and negative predictive value, but the increases were not statistically significant.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Since only cases with positive results were evaluated, our study does not address detectability. In addition, the role of US in differentiating benign from malignant solid masses is still evolving. The investigators in several studies in the past (6–8,12) have described specific US findings to determine if a solid mass is benign or malignant. The features of masses that are usually analyzed are shape, margins, and echogenicity. A recent investigation by Stavros et al (13) has renewed interest in the potential value of these US diagnostic criteria. However, in the latter investigation, one highly experienced radiologist obtained and interpreted the images, so the accuracy might not be reproducible in general practice.
The purpose of our study was to investigate the general applicability and interobserver variability of US features in differentiating benign from malignant solid breast masses. Our results were not as encouraging as those of Stavros et al (13) in that we encountered false-negative interpretations and interobserver variability in the characterization of features and in the final assessments.
For an individual US characteristic to be deemed to have practical applicability in the differentiation of benign from malignant lesions, we concluded that it must (a) be present frequently, (b) help reliably distinguish benign from malignant lesions, and (c) have high interobserver agreement. For example, although a hyperechoic lesion was a reliable predictor of benignity if present, it was infrequently observed in our cases and therefore not generally applicable. The effect of a mass on posterior echoes was not reliable for differentiating benign from malignant masses. The identification of a pseudocapsule lacked utility because of high interobserver variability. Overall, the least useful US features in our retrospective study were echogenicity, presence of a pseudocapsule, posterior echo intensity, presence of calcifications, and echotexture.
In our study, we identified three features described in the literature that best met the criteria of frequency, reliability, and interobserver agreement. These three features were the shape, margins, and width–to-AP dimension ratio of the mass (Table 1). While a width-to–AP dimension ratio greater than 1.4 would seem to be the most objective of these criteria for benignity, there were 25 cases in which the width-to–AP dimension ratio was 1.4–1.6. In these 25 cases, where the ratio was close to but just greater than 1.4 cm, variability in placement of the cursors by the operator and selection of images for measurements by the reviewer were factors that could have affected the determination of benignity versus malignancy.
It is important to emphasize that the criteria for differentiating benign from malignant solid masses should be strictly applied, as emphasized by Stavros et al (13). In our study, we found another requirement: that all three observers agree on the presence of the benign criteria. There were 26 masses in which all three reviewers agreed that the criteria of benignity were met for each of these three features. All of these masses were benign. Therefore, we conclude that these characteristics could be strictly applied to predict a diagnosis of benignity. Our retrospective analysis of the data showed that use of these three features alone, when agreed on by all three observers, to identify masses that did not require biopsy could have improved the overall positive predictive value (biopsy yield of carcinoma) by 16% (from 23% to 39%).
However, in most practices, only one observer interprets the features of a case, and subjectivity often enters into the final assessment, which leads to the possibility of a false-negative interpretation. In our series, one cancer was interpreted subjectively to be benign on US images by all three reviewers. In retrospect, this mass did not strictly meet the criterion of circumscribed margins, since portions of the lateral and inferior margins were ill defined (Fig 3).
However, retrospective analyses do not reflect actual everyday practice. Three additional cancers were misinterpreted as benign by individual observers, which verified the variability among observers in making a final assessment.
In women younger than 30 years, in whom mammography is less useful, US is often considered the modality of choice to initiate the evaluation of a palpable mass (20,22). In our study, the younger women who underwent US but not mammography would have benefited the most from the application of US criteria for benign versus malignant solid masses. Use of the diagnostic criteria would have eliminated the need for five (17%) of 29 biopsies in the women who did not have mammograms, but this P value (P = .75) does not indicate statistical significance because of the small number of subjects examined.
In women who underwent mammography, the overall contribution of US was less. In these patients, who were usually older (mean age, 47 years), the application of the US diagnostic criteria improved the sensitivity, positive predictive value, and negative predictive value, but the improvements were not statistically significant (Table 4). For example, the positive predictive value was improved by only 2% by applying the US diagnostic criteria in addition to the mammographic findings in these patients. However, US did not result in an improvement in specificity (number of negative interpretations that were truly benign lesions at tissue diagnosis).
On the basis of our case material, US is unlikely to contribute substantially to the differentiation of benign versus malignant solid masses in women in whom mammography adequately depicted a solid mass. However, US does contribute to the differentiation of benign versus malignant if the mass is not visible or is partially obscured at mammography.
We believe that our study has several strengths. First, we have evaluated the contribution of US in women who underwent mammography. To our knowledge, this has not been addressed in other articles on the use of US to define benign versus malignant masses. Second, US examinations were performed by several operators, including specially trained radiologic technologists, rather than one highly experienced operator. We believe that the use of several operators is more representative of radiology practices in general. Finally, by using three interpreting physicians in our study we were able to address interobserver variability in the recognition and application of diagnostic criteria.
We also recognize some limitations of our study. These include the fact that the evaluation of the cases was retrospective, that the sample size was relatively small, and that there was unavoidable case-selection bias. For example, patients with obviously malignant findings on mammograms usually did not undergo US unless imaging-guided biopsy was planned, which resulted in relatively fewer malignant masses in our study than if US had been performed on all mammographically detected masses.
Another case-selection bias involved exclusion of cases in which US failed to show a clinically or mammographically detected cancer. The latter selection bias reduced the US false-negative rate. Another limitation was that certain unusual-appearing masses might have been identified at US because they had already been detected at mammography.
When assessing the general usefulness of these US diagnostic criteria as a method of avoiding unnecessary excisional biopsy, it is also important to remember that there are other options for determining whether a solid mass is benign or malignant. For example, fine-needle aspiration biopsy with cytologic analysis is a relatively inexpensive, minimally invasive procedure that many experienced radiologists find useful in the evaluation of solid masses (23). Core-needle biopsy is now widely used for the evaluation of nonpalpable solid masses and is readily adaptable to US guidance (18,19).
Some women and their physicians will insist on excisional biopsy of a palpable mass because of fear, physician uncertainty, or traditional standard-of-care protocols despite improvements in diagnostic criteria for determining whether a solid mass is benign or malignant.
In conclusion, the results of our study were encouraging in that we were able to identify the most applicable US features for differentiating benign from malignant solid masses. These features have the potential to help decrease the number of biopsies performed for benign solid masses. However, we also found interobserver variability in the evaluation of these features and in the final assessments. This led to a number of false-negative interpretations of malignant solid masses in our study.
Therefore, our conclusion is that these diagnostic US features should not be generally applied to defer the biopsy of a solid mass until additional investigations are undertaken. The additional investigations should further explore issues of reproducibility of specific criteria in a variety of practices and among interpreters.
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, L.W.B.; study concepts, L.W.B.; study design, L.W.B., A.C.S., G.R., G.C.H.; definition of intellectual content, L.W.B., G.R.; literature research, G.R., A.C.S., G.C.H.; clinical studies, G.R., A.C.S., G.C.H.; experimental studies, G.R., A.C.S.; data acquisition, all authors; data analysis, G.R., A.C.S., J.S.P.; statistical analysis, G.R., J.W.S.; manuscript preparation, L.W.B., G.R., V.P.J.; manuscript editing, L.W.B., V.P.J., G.R.; manuscript review, all authors.
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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