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Differentiation of Benign from Malignant Solid Breast Masses: Conventional US versus Spatial Compound Imaging¹

¹ From the Dept of Radiology, Seoul Municipal Boramae Hosp, Seoul, Korea (J.H.C.); Dept of Radiology and Clinical Research Inst, Seoul National Univ Hosp and the Inst of Radiation Medicine, 28, Yongon-dong, Chongno-gu, Seoul 100-744, Korea (W.K.M., N.C., S.Y.C., G.C., J.G.I.), Dept of Radiology, Univ of Ulsan College of Medicine, Asan Medical Ctr, Seoul, Korea (S.H.P.); Dept of Radiology, College of Medicine, Iowa Univ, Iowa City, Iowa (J.M.P.); Dept of Radiology, Samsung Medical Ctr, Sungkyunkwan Univ School of Medicine, Seoul, Korea (B.K.H., Y.H.C.). Received Aug 26, 2004; revision requested Oct 29; revision received Dec 17; accepted Jan 20, 2005. Supported by grant 05-2003-0060 from Seoul National University Hospital Research Fund. Address correspondence to W.K.M. (e-mail: moonwk{at}radcom.snu.ac.kr).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To compare prospectively the diagnostic performance of radiologists who used conventional ultrasonography (US) with that of radiologists who used spatial compound imaging for the differentiation of benign from malignant solid breast masses.

MATERIALS AND METHODS: The study was approved by the institutional review board, and informed consent was obtained. Before excisional or needle biopsy was performed, conventional US and spatial compound images were obtained in 67 patients (age range, 25–67 years; mean age, 45 years) with 75 solid breast masses (21 cancers and 54 benign lesions). Three experienced radiologists who did not perform the examinations independently analyzed US findings and indicated the probability of malignancy. Results were evaluated with statistics and receiver operating characteristic (ROC) analysis.

RESULTS: For US findings, the presence of calcifications was the most discordant feature ( = 0.372) between conventional US and spatial compound imaging, followed by echotexture ( = 0.439), boundary echo ( = 0.496), orientation ( = 0.518), echogenicity ( = 0.523), shape ( = 0.526), margin ( = 0.569), and posterior acoustic transmission ( = 0.669). The area under the ROC curve for conventional US was 0.79 for reader 1, 0.88 for reader 2, and 0.82 for reader 3, and the area under the ROC curve for spatial compound imaging was 0.85 for reader 1, 0.88 for reader 2, and 0.89 for reader 3. The partial area index for conventional US was 0.29 for reader 1, 0.69 for reader 2, and 0.39 for reader 3, and the partial area index for spatial compound imaging was 0.29 for reader 1, 0.65 for reader 2, and 0.39 for reader 3. The difference between the diagnostic performances of the two techniques was not significant (P > .05).

CONCLUSION: The performance of the radiologists with respect to the characterization of solid breast masses was not significantly improved with spatial compound imaging.

© RSNA, 2005

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
In addition to facilitating the distinction of cysts and solid breast tumors, ultrasonography (US) can be used to help differentiate benign from malignant solid lesions. Stavros et al (1) described a classification model with a reported 98.4% (123 of 125 lesions) sensitivity, 67.8% (424 of 625 lesions) specificity, and 99.5% (424 of 426 lesions) negative predictive value. The US findings that were used to characterize a solid breast mass included shape, orientation, margin, echogenicity, echotexture, posterior acoustic transmission, boundary echo, and the presence of calcifications. US, however, is operator dependent, and considerable observer variabilities in terms of radiologists' descriptions and assessments of breast lesions have been described in the literature (2,3). For example, with conventional US, a number of inherent artifacts, such as speckle, clutter, acoustic shadowing, and acoustic enhancement, can compromise image quality and are in part responsible for the inconsistent and inaccurate interpretation of breast images.

Spatial compound imaging is a method in which US information is obtained from several different angles of insonation; this information is then combined to produce a single image at real-time frame rates. Because images are averaged from multiple angles of insonation, spatial compound imaging can reduce the image artifacts that are inherent to conventional US (4–6). Moreover, results of previous studies have shown that, compared with conventional US, spatial compound imaging considerably improves the image quality of breast lesions (7–10). Spatial compound imaging has also been shown to reduce speckle artifacts, improve the conspicuity of low-contrast lesions, enhance the delineation of tumor margins, and improve the depiction of the internal architecture of solid lesions and microcalcifications. Conversely, the posterior echo pattern (ie, shadowing and enhancement) was less clear with spatial compound imaging than with conventional US. Although the potential benefits of spatial compound imaging for the differentiation of solid breast masses have been emphasized, previous studies have not address whether these improvements affect the final diagnostic assessment of lesions and allow better selection of patients for biopsy.

Thus, the purpose of our study was to compare prospectively the diagnostic performance of radiologists who used conventional US with that of radiologists who used spatial compound imaging for the differentiation of benign from malignant solid breast masses.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patients
Between January and March 2001, 71 consecutive patients who were scheduled to undergo excisional or percutaneous needle biopsy owing to suspicious mammographic or physical findings were examined with US. A total of 75 solid breast masses in 67 patients (age range, 25–67 years; mean age, 45 years) were visualized with US and were included in this study. Four patients with clustered microcalcifications that were detected at mammography were excluded from the study because the mass that was associated with the microcalcifications was not seen at US. The study was approved by the institutional review board of our institution, and informed consent was obtained from all patients.

Lesions manifested as clinically occult mammographic lesions in 44 instances, as palpable masses in 19 instances, as nipple discharge in six instances, and as incidental lesions in six instances. Mammograms were available in 60 patients with 65 lesions and demonstrated a mass in 36 instances, a mass with microcalcifications in 10 instances, an asymmetric density in three instances, and an architecture distortion in one instance. No mammographic abnormality was found for 15 (23%) of 65 lesions. Before biopsy, the 75 solid breast masses were assessed by using the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS) (11). A BI-RADS category 3 (probably benign) was assigned in ten (13%) of 75 masses, a BI-RADS category 4 (suspicious) in 55 (73%) of 75 masses, and a BI-RADS category 5 (highly suggestive of malignancy) in ten (13%) of 75 masses.

The nature of all masses seen at US was confirmed with histopathologic results after surgical excision (n = 21) or US-guided percutaneous core needle biopsy (n = 54), both of which were performed within 24 hours of the US examinations. Of the 75 masses, 21 (28%) were cancerous and 54 (72%) were benign. Malignant masses included infiltrating ductal carcinomas (n = 16), infiltrating lobular carcinomas (n = 2), and ductal carcinoma in situ (DCIS) (n = 3). Benign lesions included fibrocystic changes (n = 24), papillomas (n = 3), radial scars (n = 1), and fibroadenomas (n = 26). All benign lesions except five fibroadenomas were followed up for more than 1 year, and lesion stability was confirmed. The histologic diameter of the lesions was 5–25 mm (mean, 12.5 mm) for invasive cancer, 6–23 mm (mean, 13.3 mm) for DCIS, and 4–24 mm (mean, 12.1 mm) for benign lesions. The diameter of the mass at US was 4–9 mm for 37 lesions, 10–19 mm for 23 lesions, and 20–25 mm for 15 lesions.

US Examinations
All US images were obtained by using a US scanner (HDI 5000; Advanced Technology Laboratories, Bothell, Wash) with a 5–12-MHz linear array. Images were obtained by using both conventional US and spatial compound imaging, which were performed by one experienced breast radiologist (W.K.M.). The target mode, which consisted of nine frames obtained from different viewing angles, was used to produce spatial compound images in all cases. The scanning protocol included both transverse and longitudinal real-time imaging of the solid masses, and a split-screen imaging mode was used to obtain identical images with conventional US and spatial compound imaging. The images were obtained in an identical plane without changing depth, focus position, or gain settings. The order of the image acquisitions (ie, either spatial compound imaging first or conventional US first) was determined randomly. Representative transverse and longitudinal images of solid masses at conventional US and spatial compound imaging were saved in a picture archiving and communications system and were printed on film. The images were then cut apart so that the readers looked at only one image or the other. Image sets were masked and randomized.

Imaging Review
Three breast radiologists (J.M.P., B.K.H., Y.H.C.) who did not perform the US examinations and who were blinded to the image acquisition technique independently analyzed US images of the transverse and longitudinal scans without physical examination or mammographic information. The radiologists were from two academic centers other than the institution where US examinations were performed, and their level of experience in breast US varied (range, 5–12 years; mean 8.3 years). Two radiologists had no experience in spatial compound imaging, and one radiologist had only 2 weeks of experience in spatial compound imaging.

A total of 150 sets of US images (75 conventional US images and 75 spatial compound images) were divided into two groups that comprised 75 images each. Images were reviewed after a 1-month interval. For both techniques, the readers described the shape (round, oval, lobulated, or irregular), orientation (wider than tall or taller than wide), margin (circumscribed, microlobulated, ill defined, or spiculated), echogenicity (hyperechoic, isoechoic, mildly hypoechoic, or markedly hypoechoic), echotexture (homogeneous or heterogeneous), posterior acoustic transmission (unaffected, enhanced, or shadowing), boundary echo (absent, thin pseudocapsule, or thick echogenic halo), and calcifications (absent or present). Readers also provided a BI-RADS final assessment category to indicate the probability of malignancy (1,11). Each lesion was further categorized as benign (ie, benign or probably benign) or malignant (ie, suspicious or highly suggestive of malignancy). For management, follow-up was recommended for lesions that were either benign or probably benign, and biopsy was recommended for lesions that were either suspicious or highly suggestive of malignancy.

Statistical Analysis
Agreement between the two US techniques and agreement between the three readers for each US technique (ie, interobserver agreement) was calculated by using statistics. Agreement was evaluated for all US findings, including shape, orientation, margin, echogenicity, echotexture, posterior acoustic transmission, boundary echo, and the presence of calcifications within masses, as well as for BI-RADS final assessment categories. A value of 0.20 or greater was considered slight agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, substantial agreement; and 0.81–1.00, almost perfect agreement (12). By using the calcifications observed at mammography as a reference standard, we calculated the sensitivity and specificity of calcification detection for conventional US and spatial compound imaging. Sensitivity and specificity were then compared between the two US techniques by using the McNemar test.

Receiver operating characteristic (ROC) analysis was conducted to assess and compare the performance of each reader for the characterization of solid breast masses with conventional US and spatial compound imaging. To analyze performance, we calculated and compared parametric estimates of the area under the ROC curve (A_z) and the partial area index (_0.90 A'_z) (ie, the area under the ROC curve between 90% and 100% sensitivity) for the two techniques by using the ROCKIT algorithm (C. Metz, University of Chicago, Chicago, Ill) and the method described by McClish and Jiang et al (13–16). In addition, the sensitivities, specificities, and positive and negative predictive values of the two techniques were calculated for each reader and were compared by using the McNemar test. Two-tailed P values of less than .05 were considered to indicate a statistically significant difference. Statistical analyses other than ROC analysis were performed by using a commercially available statistical software program (SPSS, version 10 for Windows; SPSS, Chicago, Ill).

	RESULTS

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Observer Agreement
Table 1 shows the level of agreement between the two US techniques for the eight US findings and BI-RADS final assessment of solid breast masses. The three readers showed fair to substantial agreement for US findings by using the two techniques. For US findings, the presence of calcifications was the most discordant feature ( = 0.372), followed by echotexture ( = 0.439), boundary echo ( = 0.496), orientation ( = 0.518), echogenicity ( = 0.523), shape ( = 0.526), margin ( = 0.569), and posterior acoustic transmission ( = 0.669). Ten lesions (eight cancers and two benign lesions) were found to have a mass with calcifications at mammography, but readers 1, 2, and 3 reported that seven, six, and seven lesions, respectively, at conventional US and six, six, and six lesions, respectively, at spatial compound imaging demonstrated calcification (Fig 1). The mean sensitivity and specificity for depicting calcifications were 67% (20 of 30 lesions) and 87% (144 of 165 lesions), respectively, for conventional US and 60% (18 of 30 lesions) and 82% (152 of 165 lesions), respectively, for spatial compound imaging. These differences were not significant (P > .05). Of the 45 lesions that were described as having accompanying posterior acoustic enhancement at conventional US, 13 were described differently at spatial compound imaging by at least one reader (Fig 2 ). Twelve lesions were described as unaffected, and one lesion demonstrated shadowing. Of the 17 lesions that were described as having accompanying posterior acoustic shadowing at conventional US, six were described differently at spatial compound imaging by at least one reader. Four lesions were described as unaffected, and two were described as enhanced. For the BI-RADS final assessment of solid breast masses, fair to moderate agreement was found between the two techniques; values were 0.506 (standard error, 0.078) for reader 1, 0.384 (standard error, 0.083) for reader 2, and 0.594 (standard error, 0.106) for reader 3.

View larger version (128K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. US images obtained in 40-year-old woman with infiltrating ductal carcinoma. Comparison between (a) transverse spatial compound image and (b) conventional US image demonstrates enhanced delineation of tumor margin owing to speckle reduction and disappearance of posterior acoustic shadowing (*) on spatial compound image. Both images show punctate echogenic dots (arrows) within a hypoechoic mass that correspond to microcalcifications seen at mammography. Final assessment by all readers was "highly suggestive of malignancy" at both spatial compound imaging and conventional US.

View larger version (134K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. US images obtained in 40-year-old woman with infiltrating ductal carcinoma. Comparison between (a) transverse spatial compound image and (b) conventional US image demonstrates enhanced delineation of tumor margin owing to speckle reduction and disappearance of posterior acoustic shadowing (*) on spatial compound image. Both images show punctate echogenic dots (arrows) within a hypoechoic mass that correspond to microcalcifications seen at mammography. Final assessment by all readers was "highly suggestive of malignancy" at both spatial compound imaging and conventional US.

View larger version (156K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. US images obtained in 34-year-old woman with fibroadenoma. Comparison between (a) transverse spatial compound image and (b) conventional US image demonstrates enhanced delineation of tumor margin owing to speckle reduction on spatial compound image. Posterior acoustic enhancement (*) is reduced on spatial compound image. Final assessment by all readers was "probably benign" at both spatial compound imaging and conventional US.

View larger version (166K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. US images obtained in 34-year-old woman with fibroadenoma. Comparison between (a) transverse spatial compound image and (b) conventional US image demonstrates enhanced delineation of tumor margin owing to speckle reduction on spatial compound image. Posterior acoustic enhancement (*) is reduced on spatial compound image. Final assessment by all readers was "probably benign" at both spatial compound imaging and conventional US.

ROC Analysis
For the three readers, mean A_z values at conventional US and spatial compound imaging were 0.83 ± 0.05 (standard deviation) and 0.87 ± 0.02, respectively (Table 2). The A_z value for conventional US was 0.79 for reader 1, 0.88 for reader 2, and 0.82 for reader 3. The A_z value for spatial compound imaging was 0.85 for reader 1, 0.88 for reader 2, and 0.89 for reader 3. These differences were not statistically significant. The _0.90A'_z value for conventional US was 0.29 for reader 1, 0.69 for reader 2, and 0.39 for reader 3. The _0.90A'_z value for spatial compound imaging was 0.29 for reader 1, 0.65 for reader 2, and 0.39 for reader 3. These differences were not statistically significant. The sensitivity, specificity, and positive and negative predictive values of conventional US and spatial compound imaging for the three readers are summarized in Table 2. Differences were not statistically significant.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
In this study, three readers described the specific US findings of solid breast masses and provided a BI-RADS final assessment category by using conventional US and spatial compound imaging. This differs from previous studies, which graded or scored the quality of the findings by using these two techniques. As a result, we found fair to substantial agreement between the two techniques in terms of the description of US findings and the final assessment of the masses. For the three readers, diagnostic performance (ie, the area under the ROC curve [A_z], partial area index at 90% sensitivity [_0.90 A'_z], sensitivity, and specificity) was not significantly different between conventional US and spatial compound imaging. Interobserver agreement between the readers in terms of the description of the US findings and mass assessment were also similar for conventional US and spatial compound imaging.

Diminished visibility of posterior acoustic shadowing with spatial compound imaging was considered a limitation in terms of the characterization of solid breast masses because posterior acoustic shadowing is an important clue for the diagnosis of breast cancer at conventional US (6,9). The results of our study, however, showed that this change did not negatively affect the evaluation of solid breast masses with spatial compound imaging, and no malignancy was misclassified as benign with spatial compound imaging owing to the disappearance of posterior acoustic shadowing. This was probably because malignant masses with posterior acoustic shadowing often had other suspicious findings, such as an irregular shape, taller-than-wide orientation, or a spiculated margin (17). Of the eight US findings, posterior acoustic transmission was the most concordant between spatial compound imaging and conventional US in the present study. In contrast to findings from previous reports on the better visualization of microcalcifications with spatial compound imaging (6), our results demonstrated no difference in the sensitivity and specificity of the two techniques for the detection of microcalcifications (P > .05). In this study, we used a 12-MHz linear transducer, and microcalcifications associated with malignancy were frequently seen as punctate echogenic dots within a hypoechoic mass (18,19).

In terms of distinguishing malignant from benign solid breast masses at conventional US, the mean A_z and _0.90A'_z values were 0.83 ± 0.05 and 0.46 ± 0.21, respectively, for the three readers. This level of performance for the characterization of solid breast masses with US is comparable with the level of performance previously reported in similar patient populations (20). The three DCIS lesions that were included in the present study lowered the readers' sensitivity because the DCIS lesions were seen as subtle hypoechoic masses and were misclassified as probably benign at conventional US and spatial compound imaging. The readers were blinded to the mammographic information, and this probably lowered the radiologists' performance. We used only two static images (transverse and longitudinal) of solid breast masses for evaluation rather than real-time assessment at conventional US and spatial compound imaging. All three readers had limited experience with spatial compound imaging prior to the trial, which could be a limitation. The small sample size of our study could also be a limitation. The US lexicon described and defined by Stavros et al (1) was used in this study. The use of the new US lexicon for BI-RADS assessment (21) may increase the consistency and reproducibility of the US evaluation of solid breast masses. Because it is easy to switch from one technique to the other, both conventional US and spatial compound imaging can be used for breast imaging (6,9). We did not evaluate the complementary role of spatial compound imaging and conventional US. Further studies should be performed to evaluate the usefulness of combining conventional US and spatial compound imaging for the characterization of solid breast masses.

In conclusion, a difference was found between US findings for conventional US and for spatial compound imaging. The performance of radiologists with respect to the characterization of solid breast masses, however, did not improve significantly with spatial compound imaging.

	FOOTNOTES

 

Abbreviations: A_z = area under the ROC curve • BI-RADS = Breast Imaging Reporting and Data System • DCIS = ductal carcinoma in situ • ROC = receiver operating characteristic

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, W.K.M.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, J.H.C., W.K.M., N.C., S.Y.C., J.M.P., B.K.H.; clinical studies, J.H.C., W.K.M., N.C., J.M.P., B.K.H., Y.H.C.; statistical analysis, J.H.C., W.K.M., S.H.P., G.C.; and manuscript editing, J.H.C., W.K.M., N.C., S.Y.C., J.G.I.

	References

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 

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