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How to Find an Isoechoic Lesion with Breast US1 Min Jung Kim, MD, PhD • Ji Youn Kim, MD • Jung Hyun Yoon, MD • Ji Hyun Youk, MD, PhD • Hee Jung Moon, MD • Eun Ju Son, MD, PhD Jin Young Kwak, MD, PhD • Eun-Kyung Kim, MD, PhD Breast ultrasonography (US) is recognized as a useful diagnostic tool for palpable or nonpalpable breast masses, but isoechoic lesions surrounded by fat can be a challenge for radiologists and can result in false-negative interpretations and a delayed diagnosis of breast cancer. Identifying isoechoic lesions surrounded with fat by using breast US requires meticulous evaluation with B-mode US in correlation with mammography. For correlation between mammography and US, the location, surrounding tissue, and lesion characteristics, including size, shape, and internal contents, must be considered. Complementary tools to B-mode US in the evaluation of isoechoic breast lesions include spatial compound imaging, tissue harmonic imaging, US elastography, color or power Doppler imaging, power Doppler vocal fremitus imaging, and contrast agent enhancement. Specimen radiography after breast biopsy can be helpful in evaluating the adequacy of tissue sampling and the appropriateness of lesion targeting and localization, evaluations that increase confidence in the findings from tissue acquisition. ©

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Abbreviations: CC = craniocaudal, MLO = mediolateral-oblique RadioGraphics 2011; 31:663–676 • Published online 10.1148/rg.313105038 • Content Codes: From the Department of Radiology, Research Institute of Radiological Science, Yonsei University Health System, 250 Seongsanno, Seodaemun-gu, Seoul 120-752, South Korea. Presented as an education exhibit at the 2009 RSNA Annual Meeting. Received March 3, 2010; revision requested April 14 and received September 19; accepted October 19. All authors have no financial relationships to disclose. Address correspondence to E.K.K. (e-mail: [email protected]). 1

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Introduction

Breast ultrasonography (US) is a useful diagnostic adjunct to mammography. Breast US offers the advantage of distinguishing cystic from solid lesions and can be used to determine whether partially obscured or indistinct lesion borders at mammography are caused by surrounding fibrous tissue or mass infiltration (1). Breast US is also helpful in determining whether mammographic abnormalities such as focal asymmetry are true lesions or summations. When a lesion is evident at breast US examination, US guidance for biopsy is preferred over stereotactic guidance because of the advantages of US-guided biopsy, which include ease of performance and lower cost (2–4). The ultimate success of a US-guided biopsy of an isoechoic mass depends on the meticulous identification of the mass at US to ensure that the mass indeed represents the same lesion that was identified at mammography. However, breast US may not reveal a definitive cause for the suspected mammographic abnormality in two specific instances. In the first instance, no US correlate is identified, the breast US evaluation is accurate, and the mammographic abnormality is a pseudolesion caused by summation of normal structures. In the second instance, breast US evaluation is unsuccessful in depicting the mammographic abnormality either because the wrong area was evaluated with US or because the abnormality on the mammogram was not conspicuous at breast US and was missed. In this second instance, the negative findings at breast US may give radiologists false confidence about the lack of a breast abnormality and thereby result in a false-negative finding that might delay the diagnosis of breast cancer. The internal echogenicity of a mass is assessed by its relationship to the echogenicity of fat in the breast, not by its relationship to the echogenicity of the fibroglandular tissue or generic surrounding tissue. Hypo- and hyperechoic lesions can usually be delineated easily, even if they are located in fat, by virtue of their contrasting echogenicity. However, by definition, isoechogenicity in the breast means echogenicity equal to that of fat. The absence of contrasting echogenicity makes definition of isoechoic lesions against a fatty background difficult (Fig 1) (5). This review examines examples of imaging techniques for the identification and characterization of isoechoic nodules in fat by using breast US. The purpose of this review is to describe the principles and useful techniques of identifying and characterizing isoechoic breast nodules in fat

Figure 1.  Definitions of isoechogenicity and hypoechogenicity. Transverse US image shows that isoechogenicity is echogenicity that is equal to that of fat (*) in subcutaneous and prepectoral breast tissue, and hypoechogenicity (arrow) is echogenicity that is less than that of fat.

at US. In this article, isoechogenicity in the breast is defined and detailed with regard to breast lesions. Then the methods to identify and characterize US nodules are presented, including the adjustment of US parameters and the use of the principles of US-mammographic correlation, as well as the use of other complementary methods to identify and characterize US nodules. Finally, techniques to confirm isoechoic nodules are presented, including mammography with marker or needle localization and specimen radiography.

Isoechogenicity of Breast Lesions Definition of Isoechogenicity Fatty tissue appears in the center of the grayscale spectrum of echogenicities of normal breast tissue and pathologic breast lesions (6). At one end of the spectrum, dense fibrous tissue, calcium, and skin are hyperechoic, and at the opposite end of the spectrum, simple cysts are anechoic. All women, regardless of their age and breast parenchymal pattern, have subcutaneous fatty tissue that can be used as the reference point in defining the echo pattern of the remaining breast tissue or lesion(s). Therefore, the American College of Radiology recommends that fatty tissue should be used as the reference tissue for comparison of echogenicity at breast US (5) and should set the standard for “isoechogenicity” within a breast. In addition to fat, isoechogenicity can be seen in loose stromal fibrous tissue and in terminal ductolobular units in normal breast tissues (6).

Breast Lesions Showing Isoechogenicity at US Isoechogenicity itself is not classified as a suspicious finding for malignancy but is considered an indeterminate finding (7–9). Hong et al (10)

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Figure 2.  Mucinous carcinoma in a 55-year-old woman with a palpable mass in the right breast. (a) Craniocaudal (CC) view shows a 1.5-cm round high-density indistinct mass (arrows) abutting the anterior mammary fascia in the medial portion of the right breast. (b) Transverse US image shows an oval isoechoic nodule (arrows) compressing the surrounding tissue inferiorly (arrowheads).

reported that isoechogenicity is not uncommon in benign breast lesions, manifesting in 16% (41 of 262 lesions) of benign lesions, and is not common in malignant lesions (5.7%; eight of 141 lesions). However, interobserver variability of observations of echogenicity is reported to be relatively high (k = 0.29–0.37), so that lesions categorized as isoechoic may, in practice, also include slightly hypoechoic lesions because the boundaries between these designations are, at best, blurry (5,11–13). Given this combination of facts, isoechogenicity, including slight hypoechogenicity, is common in breast lesions, being reported in 84% (527 of 625 breast lesions) of benign nodules and 30% (38 of 125 lesions) of malignant lesions. Thus, about onethird of breast cancers may be defined as isoechoic in actual clinical practice (7). Isoechogenicity can be seen in usual ductal hyperplasia, atypical ductal hyperplasia, papillary apocrine metaplasia, adenosis, debris and floating cells of complex cysts in the fibrocystic and benign proliferative conditions, fibroadenoma, and papilloma, as well as in about one-third of breast carcinomas (Fig 2) (8,9). Kopans (14) reported that more than 70% of breast cancers develop at the periphery of glandular tissue, just anterior to the retromammary fat, or beneath the subcutaneous fat. On the basis of geometry, more than 50% of the parenchyma is in this zone, so it would not be uncommon to define a breast cancer either projecting within or abutting fatty tissue (14). As a result, radiologists using breast US may often encounter breast lesions and breast cancers that are surrounded by fat. Should the echogenicity

of the lesion or cancer be similar to that of fat (ie, be isoechoic to fat), defining the lesion at US examination may be challenging.

Methods to Identify and Characterize US Nodules Adjustment of US Parameters Above all, for proper comparison with fat tissue as the standard of isoechogenicity, it is important to set the US parameters, such as the dynamic range, total gain, and time-gain compensation curve, appropriately for comparison (6,9). If the dynamic range is too narrow, hypoechoic lesions will appear anechoic, and if the dynamic range is too wide, lesions may appear isoechoic and be undetectable with US. The optimal dynamic range is usually recommended to be 55–70 dB, but real-time adjustment is required. Total gain can accentuate the effects of an inappropriate dynamic range. The time-gain compensation curve should be adjusted to increase gradually with increasing depth and to equalize fatty tissues at all breast tissue depths. The subcutaneous fat within the premammary zone should demonstrate the same midlevel gray echogenicity as fat tissues in both the mammary parenchymal zone and the retromammary zone (5,6) (Fig 3). Recently, automatic tissue optimization has been developed, in which dynamic imaging processing remaps the gray scale over the range of gray shades actually depicted within the image (15).

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Figure 3.  Transverse US image demonstrates that to generate an appropriate time-gain compensation curve, fatty tissue at all breast tissue depths should be equalized for the midlevel gray echogenicity, including the subcutaneous fat within the premammary zone (arrowhead), the mammary zone, and the retromammary zone (arrow). Figure 4.  Superficial breast lesion location. (a, b) Drawings illustrate that if a lesion (black circle) involves or abuts the anterior mammary fascia on the mammogram (a), the lesion should also abut the anterior mammary fascia on the US image (b). (c, d) Mucinous carcinoma in a 40-yearold woman with a mammographic mass in the left breast. (c) MLO view shows an 8-mm lobular highdensity mass (arrow) in the anterior portion of the breast. (d) On the transverse US image, the mammographic mass is depicted as an oval microlobulated isoechoic mass (arrows) in the superficial portion of the breast.

Principles of USMammographic Correlation Before performing US, the radiologist must confirm that the mammographic abnormality is a true lesion by using routine, and possibly additional, mammographic views. If the abnormality appears to be a true lesion requiring further investigation, the radiologist should next determine its location within the breast (1,16). Other mammographic features, including the number, size, shape, and presence of calcifications and the nature and appearance of adjacent tissues, should also be noted—findings that will aid in first locating and then characterizing the lesion at US. US

is then performed for further characterization of the lesion and for determining the convenience of intervention with US guidance. Location.—The description of the location of a

lesion should include the breast quadrant, the clockface direction, and the distance from the nipple (1,16). The CC view provides a better reference for localization than does the mediolateral-oblique (MLO) view because (a) the CC view is easily reproduced at US by scanning in a

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Kim et al  667 Figure 5.  Deep breast lesion location. (a, b) Drawings illustrate that if a lesion (black circle) abuts or is deep to the posterior mammary fascia within the retromammary fat (stippled area) on the mammogram (a), the lesion may appear to abut the chest wall on the US image (b). At US performed with the patient supine, the retromammary fat is compressed, so it is often invisible. (c, d) Invasive ductal carcinoma in a 66- year-old woman with a mammographic mass in the right breast. (c) CC view shows a 5-mm round microlobulated isodense nodule (arrow) surrounded by retromammary fat. (d) On the transverse US image, the lesion is depicted as a microlobulated isoechoic nodule (calipers) abutting the chest wall (arrows).

straight transverse plane and (b) the application of mammographic compression has a much smaller rotational component on the CC view than on the MLO view. With the patient in the supine or supine oblique position with the ipsilateral side elevated so as to position the nipple in the center of the breast, the breast is scanned at US in a cephalocaudal sweep from the top to the bottom of the breast, with the use of the CC mammographic lesion location as a guide. The MLO view assesses the quadrant and the clockface direction of the lesion location. This assessment may be difficult because the mammographic plane of obliquity is between 30° and 60°. Given this variability, the exact effect of the angle at which the MLO view was exposed on determining the true location of the lesion can only be estimated in most cases. Thus care should be taken in locating the lesions with US. If a true lateral view is available, estimating the located quadrant and clockface direction is easier. The relationship of the MLO view and US is affected by the

x-ray beam passing from the upper medial to the lower outer portion of the breast in the MLO view. Therefore, a lesion that appears to lie exactly at the level of the nipple on an MLO view may actually lie within the upper inner quadrant or within the lower outer quadrant. The distance above or below the posterior nipple line at which a structure projects onto the MLO mammographic view varies with the angle of obliquity and the location of the lesion (17,18). The distance from the nipple can be correlated between mammograms and US images, although this may be hindered by positional differences. Radiologists must be aware that the distance from the nipple to the lesion tends to be accentuated on mammograms because the breast is pulled out and then compressed during mammographic examination. Surrounding Tissues.—Surrounding tissue density

is another consideration in US-mammographic correlation. The depth of the lesion relative to the surrounding tissue is important for identifying lesions at breast US. The location of the lesion relative to the mammary parenchymal zone or the proximity of the lesion to the anterior or posterior mammary fascia should be considered. If a lesion involves or abuts the anterior mammary fascia, the lesion should also abut the anterior mammary fascia on the US image (Fig 4). If a lesion is more posterior than the posterior mammary fascia or abuts the fascia on the mammogram, the lesion will likely abut the chest wall on the US image because in a US image obtained with the patient supine, the retromammary fat is compressed to the extent that it is often markedly thinned, if not invisible (Fig 5). When the lesion is located in

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Figure 6.  Compression affecting the shape of lesions. (a) Drawing illustrates that because of the different directions of compression applied, the shape of the lesion tends to be stretched at mammography. (b, c) Drawings illustrate the shape of the lesion with the patient in the supine position (b) and show how lesions are flattened because of compression by the US probe (c).

the mammary parenchymal zone on both MLO and CC views, the lesion is usually located in the mammary parenchymal zone on the US image. Lesion Characteristics.—For identification and

characterization of an isoechoic mass with US, the shape and size of the lesion on the mammogram should be considered. Because of positioning differences between mammograms and US images, the shape and size of lesions at US examination may be different from their appearances on mammograms (Fig 6). The dimensions of lesions en face are affected by compression forces from the mammography paddles, as is the perpendicular direction of lesions compressed by the US probe. Therefore, a lesion on a US image tends to be oval or elliptical, even though a lesion on mammograms is round. For similar mechanical reasons, the sizes of lesions can differ between mammograms (Fig 6a) and US images (Fig 6c).

Figure 7.  Ductal carcinoma in situ in a 64-year-old woman with a mammographic mass in the right breast. (a) Transverse US image shows a 9-mm oval isoechoic mass (arrowheads) in the area corresponding to the mammographic abnormality. The cystic portion (arrow) of the mass is noted in the periphery of the nodule and indicates an isoechoic nodule surrounded by fat. (b) Spot compression view with a skin marker (white dot) corresponding to the US lesion confirms that the nodule identified on the US image is identical to that seen on the mammogram.

On mammograms, breast lesions are measured from border to border because the capsule surrounding the lesion is indistinguishable from the lesion. Therefore, to correlate the US and mammographic measurements of a lesion, methods that include the thickness of the capsule and the hyperechoic halo on US images should be used. Additional findings that may or may not be depicted at mammography can also be clues to finding an isoechoic lesion. These additional findings include intralesional cyst(s) (Fig 7), hyperechoic foci such as microcalcifications (Fig 8) or necrosis, and a hyperechoic halo surrounding the mass (Fig 9).

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Figure 8.  Microcalcifications. (a, b) Correlation of the locations of microcalcification clusters in the left breast on an MLO view (a) and a transverse US image (b). On the MLO view, the microcalcification cluster (black arrow) noted in a superficial location at the 12 o’clock position was depicted as an isoechoic mass with micro-calcifications at US (image not shown). Another micro-calcification cluster (white arrow) in the retromammary fat at the 4 o’clock position on the mammogram is depicted as an isoechoic nodule with hyperechoic foci (circle) on the transverse US image. US-guided vacuum-assisted biopsy was performed, and the results of histopathologic examination disclosed a fibroadenoma with microcalcifications. (c) Specimen radiograph shows several microcalcifications. (d) Follow-up MLO view shows disappearance (white arrow) of the microcalcifications that were previously subjected to biopsy but persistence of the superficially located microcalcifications (black arrow).

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Figure 9.  Invasive ductal carcinoma in a 70-year-old woman with a mammographic mass in the left breast. (a) CC view shows a 5-mm irregular spiculated isodense nodule (arrow) surrounded by fatty tissue. (b) On the transverse US image, the mammographic nodule correlates with a microlobulated isoechoic nodule (arrow) with a hyperechoic halo (arrowheads), which was depicted as spiculations on the mammogram. (c) Tissue harmonic image accentuates the isoechoic nodule (arrow) because the surrounding fatty tissue appears less dark than the targeted lesion.

Complementary Methods to Identify and Characterize US Nodules Spatial Compound Imaging Spatial compound imaging allows the acquisition of multiple coplanar images of the same object from different angles and combines them into a single compound image for display. Spatial compound imaging gives high contrast and high spatial resolution and reduces artifactual echoes within cysts and solid masses compared with those on conventionally obtained US images (15). Moreover, the critical angle phenomenon, which is a common problem at the lateral edges of a breast mass with conventional imaging, is reduced. Keep in mind, however, that shadowing at the lateral edges can be used to help identify isoechoic masses in fat (Fig 10). Thus, radiologists should be prepared to turn these complementary techniques on and off during the examination.

Tissue Harmonic Imaging Tissue harmonic imaging uses nonlinear sound propagation. For image production, tissue har-

monic imaging processes only the returned highfrequency harmonic signals and rejects echoes from the fundamental frequencies. This technique improves lesion conspicuity with high image contrast and lateral resolution (19,20). Moreover, surrounding fatty tissue appears less dark than the targeted lesion with tissue harmonic imaging. Thus, an isoechoic mass on the fundamental US image will appear hypoechoic compared with surrounding fatty tissue at tissue harmonic imaging (Figs 9, 11). However, if the “mass” is a simply a fat lobule, no appreciable difference in echogenicity will be identified (Fig 12). If a mammographic mass is located in fatty tissue and not depicted at fundamental US, the lesion is isoechoic. In that case, tissue harmonic imaging is useful for surveying the area that is suspicious on the basis of the mammographic findings and may assist in defining the isoechoic mass. In our experience,

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Figure 10.  Posterior shadowing. (a) The conventional transverse US image shows marked posterior shadowing (arrows) along the lateral edges of the breast mass because of the critical angle phenomenon. (b) On the spatial compound image, the posterior shadowing is minimal (arrows).

Figure 11.  Isoechoic lesion defined with tissue harmonic imaging. (a) On the conventional transverse US image, the nodule (black arrows) shows similar echogenicity to that of the adjacent fatty tissue (white arrows). (b) On the tissue harmonic image, the nodule (black arrows) is hypoechoic compared with the adjacent fatty tissue (white arrows). This nodule was diagnosed as a phyllodes tumor at core-needle biopsy, and surgical excision was performed.

Figure 12.  Tissue harmonic imaging for isoechoic lesions. The transverse tissue harmonic image shows an isoechoic “lesion” (arrows) with the same echogenicity as that of the adjacent fatty tissue. Core biopsy was performed, and the findings from histopathologic examination disclosed that the nodule was fatty tissue.

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Figure 13.  Isoechoic nodule analyzed with US elastography: invasive ductal carcinoma detected at screening US in a 57-year-old woman. An 8-mm irregular isoechoic mass (white arrow) depicted on the screening transverse US image demonstrated hardness (black arrow) on the US elastographic image (EUB-7500; Hitachi Medical, Tokyo, Japan), a finding that was suggestive of possible malignancy.

tissue harmonic imaging is one of most important complementary techniques of US for depicting isoechoic lesions in fatty tissue.

US Elastography US elastography is a tool that reflects the hardness of a lesion by mapping the strain in tissue elements subjected to external compression. This technique is based on the theory that cancer tissue is harder than the surrounding normal parenchyma. Tissue hardness can be another characteristic, in addition to the morphologic features depicted at US, that may be used in the differential diagnosis of various breast lesions (Fig 13) (21). Depending on the manufacturer of the US equipment, different color spectra are available for marking degrees of tissue hardness, for example, red to blue or white to black, and there are various semiquantitative scoring systems, such as the area ratio or fat-lesion ratio, that can be used (21–23). US elastography is not recommended for searching the breast for an isoechoic lesion, but it can be useful for determining the hardness of a lesion once it has been de-

tected. Even when US elastography demonstrates negative findings, one cannot be certain that the indicated tissue is fat. Breast malignancy should be suspected and biopsy recommended if US elastographic findings are positive for a mass and B-mode US shows no typically benign findings.

Color or Power Doppler Imaging Because neovascularization appears to be an essential event in the development and growth of malignant tumors (24), color or power Doppler imaging has been used as a complementary method to B-mode US (25). Color Doppler imaging is a procedure to depict the mean intravascular frequency shift caused by the Doppler effects of flowing blood corpuscles, and power Doppler imaging presents the intensities or energies of Doppler signals within a time period. On US images, malignant tumors tend to demonstrate hypervascularity (92.9%), irregular vessels (73.2%), and rich vascularization (vesselmass ratio > 10% in 54.2% of cases) and have more than one vascular pole (26). Typical color Doppler signs of malignancy are intratumoral vessels that are central (86% in malignancy vs 51% in benignity), penetrating (65% vs 34%), branching (56% vs 22%), and disordered (42%

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Figure 14.  Isoechoic nodule analyzed with power Doppler imaging. Transverse power Doppler image (same patient as in Fig 7) shows increased vascularity with a penetrating pattern (arrows), a finding that increased confidence in the diagnosis of an abnormality. This lesion was diagnosed as ductal carcinoma in situ.

Figure 15.  Isoechoic nodule analyzed with power Doppler vocal fremitus imaging. Transverse power Doppler vocal fremitus image (same patient as in Fig 9) shows artifact defect (arrow) in the area corresponding to the isoechoic lesion on the conventional US image (Fig 9b).

vs 8%) (27). Because power Doppler imaging can be used to depict a significant intratumoral increase in blood flow (P ≤ .0001) compared with the flow in normal breast tissue (28), an increased vascularity on power Doppler images in the area of a possible isoechoic nodule in fat increases confidence that the finding indicates an abnormality (Fig 14). However, such a finding is not useful until the presence of a focal isoechoic mass is suspected. False-negative findings at B-mode US screening of the breast are not improved by using Doppler imaging (25).

observation was not accurate. Defects caused by vibrational artifacts during power Doppler vocal fremitus US were reported to indicate only differences in tissue components from those of the surrounding tissue at the same depth. Nonetheless, Kim et al (32) found that power Doppler vocal fremitus US can be useful in differentiating isoechoic tumors from fatty tissue and for distinguishing between isoechoic glandular tissue and fat lobules (Fig 15). Occasionally, power Doppler vocal fremitus images may be helpful in detecting multifocal isoechoic disease (32).

Power Doppler Vocal Fremitus Imaging

Contrast Agent Enhancement

Sohn et al (29) first described power Doppler vocal fremitus imaging, which is the controlled manipulation of power Doppler artifacts. When a patient speaks during a power Doppler examination, acoustic vibrations from the chest wall create color artifacts in normal tissue but not within the tumor. Color power Doppler vocal fremitus US was reported to be able to be used to differentiate between benign and malignant masses in preliminary cases (30), but Stavros et al (31) and Kim et al (32) have demonstrated that this

Although the vascularity of tumors can be determined noninvasively by using color Doppler imaging, differentiation between Doppler signals and background disturbances is not easy in small vessels with slow flow and few reflectors (33). Depiction of tumor vascularization can, however, be improved by using US contrast agents. Moreover, contrast agent enhancement can accentuate Doppler signals and improve diagnostic accuracy (34).

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Figure 16.  US-guided needle localization of the isoechoic nodule shown in Figure 9. The transverse US image (a) and the CC view (b) show that a US-guided needle (arrowheads in a) penetrates the mammographic nodule (arrow), which confirmed that the isoechoic US nodule depicted in Figure 9b and 9c was identical to the mammographic lesion in Figure 9a. Precise correlation between mammographic and US abnormalities can be demonstrated by using needle localization.

Techniques to Confirm Isoechoic Nodules Mammography with Marker or Needle Localization Skin markers are a widely popular tool for mammography, allowing radiologists to find a palpable mass, or for correlating US findings with mammographic findings. If, after US, a question remains as to whether the lesion noted at mammography and the US lesion are one and the same, a marker can be placed on the skin overlying the lesion at US, and then orthogonal mammographic images of the breast with the marker exposed can be obtained. Proximity of the marker to the mammographic mass would thus confirm that the mammographic lesion has been correctly identified at US (Fig 7b). However, if the correlation between US and mammographic lesions before a biopsy or excision is uncertain, needle localizations can be performed to confirm whether the US lesions are identical to those seen on the mammogram (Fig 16). The combination

of placing a metallic clip at the biopsy site after a US-guided core biopsy and then comparing the postbiopsy mammogram with the prebiopsy images provides assurance that the sampled lesion was, in fact, the mass originally observed mammographically (35).

Specimen Radiography Specimen radiography is a well-established procedure for assessing the adequacy of calcifications retrieved in specimens (Fig 8c) (36). Berg et al (37) reported that a specimen radiograph of cores of tissue obtained from a noncalcified breast mass can determine the adequacy of sampling, unless the breast parenchyma is extremely dense. Specimen radiography can also be useful in assessing the radiographic density of the targeted lesion when an isoechoic lesion targeted with a biopsy procedure cannot be distinguished as a fat lobule or a solid mass in fatty tissue (Fig 17). Specimen radiography provides information on the adequacy of sampling and on characterization of the lesion as a fat lobule or a nonfatty mass. Even when the mammographic

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Kim et al  675 Acknowledgment.—The authors are grateful to DongSu Jang, MA, medical illustrator (Medical Research Support Section, Yonsei University College of Medicine, Seoul, Korea), for his help with the figures.

References

Figure 17.  Specimen radiograph shows five core samples (rectangle) from the noncalcified isoechoic US nodule that was depicted in Figure 7. The core samples from the mass are more dense than the specimen core from the adjacent fatty tissue (oval), which is included for comparison. By using specimen radiography, appropriate US-guided biopsy of the dense nodule depicted on the mammogram can be confirmed.

abnormality is obviously located within fatty tissue, US-guided biopsy is preferred as long as the lesion is depicted with US, because this method is faster and more comfortable for the patient. In cases of a low-density specimen radiograph of an isoechoic lesion, radiologists should assess postbiopsy mammographic images to confirm whether the lesion was depicted and targeted appropriately at US. Specimen US after surgical excision of an isoechoic mass may also be helpful to confirm excision of the target lesion.

Conclusions

Breast US is a useful diagnostic tool for palpable and nonpalpable breast masses. However, using breast US to identify isoechoic lesions surrounded by fat can be challenging. Meticulous evaluation with B-mode US is important for finding isoechoic lesions that correlate with mammographic lesions. For correlating mammographic and US lesions, the location, the surrounding tissue, and the lesion characteristics, including size, shape, and internal contents, should be considered. Complementary tools to B-mode US for evaluating isoechoic breast lesions include spatial compound imaging, tissue harmonic imaging, elastography, Doppler imaging, power Doppler vocal fremitus imaging, and contrast agent enhancement.

1. Stavros AT. Targeted indication: mammographic abnormality. In: Stavros AT. Breast ultrasound. Philadelphia, Pa: Lippincott Williams & Wilkins, 2003; 124–146. 2. Harvey JA, Moran RE, DeAngelis GA. Technique and pitfalls of ultrasound-guided core-needle biopsy of the breast. Semin Ultrasound CT MR 2000;21 (5):362–374. 3. Liberman L. Percutaneous image-guided core breast biopsy. Radiol Clin North Am 2002;40(3): 483–500, vi. 4. Youk JH, Kim EK, Kim MJ, Lee JY, Oh KK. Missed breast cancers at US-guided core needle biopsy: how to reduce them. RadioGraphics 2007;27 (1):79–94. 5. American College of Radiology. Breast Imaging Reporting and Data System® (BI-RADS®). 4th ed. Reston, Va: American College of Radiology, 2003. 6. Stavros AT. Breast anatomy: the basis for understanding sonography. In: Stavros AT. Breast ultrasound. Philadelphia, Pa: Lippincott Williams & Wilkins, 2003; 56–108. 7. Stavros AT, Thickman D, Rapp CL, Dennis MA, Parker SH, Sisney GA. Solid breast nodules: use of sonography to distinguish between benign and malignant lesions. Radiology 1995;196(1):123–134. 8. Stavros AT. Ultrasound of solid breast nodules: distinguishing benign from malignant. In: Stavros AT. Breast ultrasound. Philadelphia, Pa: Lippincott Williams & Wilkins, 2003; 445–527. 9. Berg WA. Lesion imaging characteristics. In: Berg WA, Birdwell RA, Gombos E, et al. Diagnostic imaging: breast. Salt Lake City, Utah: Amirsys, 2006; IV:1–IV:152. 10. Hong AS, Rosen EL, Soo MS, Baker JA. BI-RADS for sonography: positive and negative predictive values of sonographic features. AJR Am J Roentgenol 2005;184(4):1260–1265. 11. Lazarus E, Mainiero MB, Schepps B, Koelliker SL, Livingston LS. BI-RADS lexicon for US and mammography: interobserver variability and positive predictive value. Radiology 2006;239(2):385–391. 12. Lee HJ, Kim EK, Kim MJ, et al. Observer variability of Breast Imaging Reporting and Data System (BIRADS) for breast ultrasound. Eur J Radiol 2008;65 (2):293–298. 13. Park CS, Lee JH, Yim HW, et al. Observer ��������������� agreement using the ACR Breast Imaging Reporting and Data System (BI-RADS): ultrasound, first edition (2003). Korean J Radiol 2007;8(5):397–402.

676  May-June 2011 14. Kopans DB. Interpreting the mammogram. In: Kopans DB. Breast imaging. 3rd ed. Philadelphia, Pa: Lippincott Williams & Wilkins, 2006; 365–480. 15. Stavros AT. Breast ultrasound equipment requirements. In: Stavros AT. Breast ultrasound. Philadelphia, Pa: Lippincott Williams & Wilkins, 2003; 16–41. 16. Park JM, Franken EA Jr. Triangulation of breast lesions: review and clinical applications. Curr Probl Diagn Radiol 2008;37(1):1–14. 17. Sickles EA. Practical solutions to common mammographic problems: tailoring the examination. AJR Am J Roentgenol 1988;151(1):31–39. 18. Rose GH. Medial or lateral mammographic lesions: down and out is down and out ... sometimes. Radiology 1998;209(1):276–278. 19. Desser TS, Jeffrey RB. Tissue harmonic imaging techniques: physical principles and clinical applications. Semin Ultrasound CT MR 2001;22(1):1–10. 20. Rosen EL, Soo MS. Tissue harmonic imaging sonography of breast lesions: improved margin analysis, conspicuity, and image quality compared to conventional ultrasound. Clin Imaging 2001;25(6): 379–384. 21. Itoh A, Ueno E, Tohno E, et al. Breast disease: clinical application of US elastography for diagnosis. Radiology 2006;239(2):341–350. 22. Sohn YM, Kim MJ, Kim EK, Kwak JY, Moon HJ, Kim SJ. Sonographic elastography combined with conventional sonography: how much is it helpful for diagnostic performance? J Ultrasound Med 2009;28 (4):413–420. 23. Zhu QL, Jiang YX, Liu JB, et al. Real-time ultrasound elastography: its potential role in assessment of breast lesions. Ultrasound Med Biol 2008;34(8): 1232–1238. 24. Srivastava A, Hughes LE, Woodcock JP, Laidler P. Vascularity in cutaneous melanoma detected by Doppler sonography and histology: correlation with tumour behaviour. Br J Cancer 1989;59(1):89–91. 25. Schroeder RJ, Bostanjoglo M, Rademaker J, Maeurer J, Felix R. Role of power Doppler techniques and ultrasound contrast enhancement in the differential diagnosis of focal breast lesions. Eur Radiol 2003; 13(1):68–79.

radiographics.rsna.org 26. Giuseppetti GM, Baldassarre S, Marconi E. Color Doppler sonography. Eur J Radiol 1998;27(suppl 2):S254–S258. 27. Kook SH, Park HW, Lee YR, Lee YU, Pae WK, Park YL. Evaluation of solid breast lesions with power Doppler sonography. J Clin Ultrasound 1999;27(5): 231–237. 28. Milz P, Lienemann A, Kessler M, Reiser M. Evaluation of breast lesions by power Doppler sonography. Eur Radiol 2001;11(4):547–554. 29. Sohn C, Baudendistel A, Bastert G. Diagnosis of the breast tumor entity with “vocal fremitus” in ultrasound diagnosis [in German]. Bildgebung 1994;61 (4):291–294. 30. Sohn C, Baudendistel A. Differential diagnosis of mammary tumors with vocal fremitus in sonography: preliminary report. Ultrasound Obstet Gynecol 1995;6(3):205–207. 31. Stavros AT. Doppler evaluation of the breast. In: Stavros AT. Breast ultrasound. Philadelphia, Pa: Lippincott Williams & Wilkins, 2003; 920–946. 32. Kim MJ, Kim EK, Youk JH, Lee JY, Kim BM, Oh KK. Application of power Doppler vocal fremitus sonography in breast lesions. J Ultrasound Med 2006;25(7):897–906. 33. Ramos IM, Taylor KJ, Kier R, Burns PN, Snower DP, Carter D. Tumor vascular signals in renal masses: detection with Doppler US. Radiology 1988;168(3):633–637. 34. Clevert D, Jung EM, Jungius KP, Ertan K, Kubale R. Value of tissue harmonic imaging (THI) and contrast harmonic imaging (CHI) in detection and characterisation of breast tumours. Eur Radiol 2007; 17(1):1–10. 35. Feld RI, Rosenberg AL, Nazarian LN, et al. Intraoperative sonographic localization of breast masses: success with specimen sonography and surgical bed sonography to confirm excision. J Ultrasound Med 2001;20(9):959–966. 36. Gallager HS. Breast specimen radiography: obligatory, adjuvant and investigative. Am J Clin Pathol 1975;64(6):749–755. 37. Berg WA, Jaeger B, Campassi C, Kumar D. Predictive value of specimen radiography for core needle biopsy of noncalcified breast masses. AJR Am J Roentgenol 1998;171(6):1671–1678.

Teaching Points

May-June Issue 2011

How to Find an Isoechoic Lesion with Breast US Min Jung Kim, MD, PhD • Ji Youn Kim, MD • Jung Hyun Yoon, MD • Ji Hyun Youk, MD, PhD • Hee Jung Moon, MD • Eun Ju Son, MD, PhD Jin Young Kwak, MD, PhD • Eun-Kyung Kim, MD, PhD RadioGraphics 2011; 31:663–676 • Published online 10.1148/rg.313105038 • Content Codes:

Page 664 The internal echogenicity of a mass is assessed by its relationship to the echogenicity of fat in the breast, not by its relationship to the echogenicity of the fibroglandular tissue or generic surrounding tissue. Page 666 Other mammographic features, including the number, size, shape, and presence of calcifications and the nature and appearance of adjacent tissues, should also be noted—findings that will aid in first locating and then characterizing the lesion at US. Page 668 (Figure 7 on page 668, figure 8 on page 669, figure 9 on page 670) Additional findings that may or may not be depicted at mammography can also be clues to finding an isoechoic lesion. These additional findings include intralesional cyst(s) (Fig 7), hyperechoic foci such as microcalcifications (Fig 8) or necrosis, and a hyperechoic halo surrounding the mass (Fig 9). Page 670 If a mammographic mass is located in fatty tissue and not depicted at fundamental US, the lesion is isoechoic. In that case, tissue harmonic imaging is useful for surveying the area that is suspicious on the basis of the mammographic findings and may assist in defining the isoechoic mass. Page 675 Complementary tools to B-mode US for evaluating isoechoic breast lesions include spatial compound imaging, tissue harmonic imaging, elastography, Doppler imaging, power Doppler vocal fremitus imaging, and contrast agent enhancement.