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Radiology Breast Imaging Wendie A. Berg, MD, PhD Cristina I. Campassi, MD2 Olga B. Ioffe, MD Index terms: Breast, biopsy, 00.1261, 00.1262 Breast, cysts, 00.721, 00.722, 00.723 Breast neoplasms, diagnosis, 00.311, 00.3115, 00.312, 00.319, 00.324, 00.327, 00.719 Breast neoplasms, US, 00.12982, 00.12985, 00.12989 Published online 10.1148/radiol.2272020660 Radiology 2003; 227:183–191 Abbreviations: CNB ⫽ core-needle biopsy DCIS ⫽ ductal carcinoma in situ IDC ⫽ invasive ductal carcinoma 1 From the Department of Radiology (W.A.B., C.I.C.), Greenebaum Cancer Center (W.A.B.), and Department of Pathology (O.B.I.), University of Maryland Medical Center, 419 W Redwood St, Suite 110, Baltimore, MD 21201. From the 2001 RSNA scientific assembly. Received May 31, 2002; revision requested June 27; final revision received September 23; accepted September 30. Address correspondence to W.A.B. (e-mail: [email protected]). Current address: Cystic Lesions of the Breast: Sonographic-Pathologic Correlation1 PURPOSE: To understand the pathologic basis for sonographic features of cystic lesions of the breast and determine appropriate assessment and management recommendations for these lesions based on sonographic appearance. MATERIALS AND METHODS: From a database of 2,072 image-guided procedures performed from July 1995 through September 2001, 150 cystic lesions were identified. Diagnosis was established with fine-needle aspiration (n ⫽ 55), 14-gauge core-needle biopsy (n ⫽ 81), or both (n ⫽ 14). Excision was performed for all malignant (n ⫽ 18) and atypical (n ⫽ 2) lesions and for 11 benign lesions, which recurred or enlarged at follow-up. Imaging follow-up was available for 92 of 119 benign lesions. Targeted sonography was performed with high-frequency (10-MHz center frequency) transducers. Imaging and histopathologic, cytologic, and/or microbiologic findings were reviewed. Lesions were categorized as simple cysts, complicated cysts (imperceptible wall, acoustic enhancement, low-level echoes), clustered microcysts, cystic masses with a thick (perceptible) wall and/or thick (ⱖ0.5 mm) septations, intracystic or mixed cystic and solid masses (at least 50% cystic), or predominantly solid masses with eccentric cystic foci. RESULTS: Of 150 lesions, 16 were simple cysts aspirated for symptomatic relief. Of 38 lesions characterized as complicated cysts and one cyst with thin septations, none proved malignant, nor did any of 16 lesions characterized as clustered microcysts. Of 23 masses with thick indistinct walls or thick septations, seven proved malignant. Of 18 intracystic or mixed cystic and solid masses, four proved malignant. Of 38 predominantly solid masses with eccentric cystic foci, seven proved malignant. 2 Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, Md. CONCLUSION: Symptomatic complicated cysts generally warrant aspiration. All clustered microcysts were benign, but further study is required. Cystic lesions with thick indistinct walls and/or thick septations (ⱖ0.5 mm), intracystic masses, and predominantly solid masses with eccentric cystic foci should be examined at biopsy; 18 of 79 of such complex cystic lesions proved malignant in this series. © Author contributions: Guarantor of integrity of entire study, W.A.B.; study concepts and design, W.A.B.; literature research, W.A.B., C.I.C.; clinical studies, W.A.B., C.I.C., O.B.I.; data acquisition and analysis/ interpretation, W.A.B., C.I.C., O.B.I.; manuscript preparation and definition of intellectual content, W.A.B.; manuscript editing, revision/review, and final version approval, W.A.B., C.I.C., O.B.I. © RSNA, 2003 RSNA, 2003 Breast sonography is appropriate in the initial evaluation of a woman younger than 30 years with a palpable lump and in the adjunctive evaluation of mammographic masses, persistent focal asymmetric densities, and palpable abnormalities not seen mammographically (1). Sonographically guided core-needle biopsy (CNB) is a readily performed, diagnostically accurate alternative to stereotactic or excisional biopsy (2,3). Sonographically guided aspiration of symptomatic cysts, complicated cysts, and possible abscesses is also readily performed. Sonographically guided fine-needle aspiration with multiple passes with a 20 –25-gauge needle is not favored for solid nonpalpable masses because of the substantial insufficient sample rate, averaging 10% in a multicenter trial (4). Sonographic feature analysis of solid masses continues to improve (5), though observer variability continues to be problematic in avoiding biopsy (6,7). An illustrated Breast Imaging Reporting and Data System (BI-RADS) ultrasonographic lexicon (8) may be helpful in improving observer performance. Confusion remains in the description and management of complicated cysts and com183 Radiology plex cystic lesions of the breast (8 –10). We sought to understand the pathologic basis of the sonographic features of cystic lesions of the breast and to determine appropriate assessment and management recommendations for these lesions based on sonographic appearance. MATERIALS AND METHODS Patients and Lesions From a database of 2,072 image-guided breast procedures performed from July 1995 through September 2001 at our institution, we sought to identify lesions with a prospectively recorded cystic component at sonography. In 133 patients, 150 pathologically proven cystic lesions were identified, representing 7.2% of all lesions. Of the 150 lesions, 92 (61%) were palpable. The mean age of patients was 48.4 years (age range, 14 –96 years). The mean lesion diameter was 22 mm (range, 4 –150 mm). Diagnosis was established with sonographically guided aspiration alone in 55 lesions from which fluid was withdrawn by using an 18- or 20-gauge needle and sent for cytologic examination and/or culture. For 81 lesions, sonographically guided CNB was performed by using a 14-gauge automated biopsy gun (Monopty; Bard, Covington, Ga). Initial aspiration was performed in 14 lesions, followed by CNB owing to persistence of a thick wall or a solid component. A mean of 4.1 (range, 1.0 – 8.0) passes were made per CNB. Our database is password protected, and our institutional review board did not require its approval or individual patient consent for review. Our database includes details of CNB and directional vacuum-assisted biopsies, aspirates when cytologic studies and/or cultures were performed, needle localizations, and ductograms. The database includes the mammographic and sonographic appearance of lesions as prospectively recorded. Of the 2,072 total procedures, 500 (24.1%) demonstrated a malignancy. Follow-up after Fine-Needle Aspiration or CNB Surgical excision was performed after any atypical (n ⫽ 2) or malignant (n ⫽ 18) result and was recommended for lesions with initial benign results, which recurred (n ⫽ 4) or increased (n ⫽ 7) at follow-up. The excised benign lesions were as follows: two recurrent cysts, two recurrent collections (one fat necrosis and/or seroma and one abscess), two papillomas that enlarged at follow-up, a 184 䡠 Radiology 䡠 April 2003 third benign papilloma in a patient with persistent nipple discharge, one infarcted fibroadenoma 13 cm in diameter and another palpable fibroadenoma, one scar tissue developing at an abscess site, and one enlarging lactating adenoma. If the lesion resolved after aspiration, and the cytologic specimen was benign, no further follow-up was recommended. Lesions proving to be benign cysts at CNB were not specifically followed up. If a proven abscess resolved clinically with antibiotics, no further follow-up was recommended. With a specific benign concordant result at CNB, such as fibroadenoma, lesions were followed up annually. For all other benign results, 6-, 12-, and 24-month follow-up was recommended. After a concordant benign result (other than cyst or abscess) at CNB or fine-needle aspiration, with no atypia, we accepted as a defined standard those lesions that were excised, subjected to another biopsy or reaspirated with the same benign result, gone or decreasing in size at any follow-up, or stable at 23 full months of follow-up. Of the 95 lesions subjected to CNB, 73 (77%) had an acceptable standard. Of the 55 lesions subjected to only aspiration, 53 (96%) had an acceptable standard. Ninety-two proven benign lesions had at least one follow-up (range, 2– 60 months; mean, 24 months; median, 23 months). Forty-nine lesions had at least 24 months of follow-up after initial diagnostic aspiration or CNB. Twenty-seven lesions proven benign at CNB (n ⫽ 16), aspiration (n ⫽ 8), or both (n ⫽ 3) have not had documented follow-up. The status of the 19 lesions after CNB without further follow-up include six fibrocystic changes; three fibroadenomas; two focal fibrosis; two abscesses; two papillomas; and one each sclerosing adenosis, apocrine metaplasia, cyst, and fat necrosis. The eight lesions with initial diagnosis at aspiration and no further follow-up include five simple cysts, one abscess, and two apocrine metaplasia (one sonographically simple cyst and one clustered microcysts, both in the same patient). Imaging and Interpretation Sonography was performed in all 150 lesions by using a broad-bandwidth linear-array transducer with a center frequency of 10 MHz supplemented by a transducer with a center frequency of 7.5 MHz, as needed, to penetrate larger breasts (Performa, Acoustic Imaging, Tempe, Ariz; or Elegra, Siemens Medical Systems, Issaquah, Wash). Craniocaudal and medio- lateral oblique mammograms were obtained in 127 lesions by using a LoRad MIV unit (Hologic, Bedford, Mass) or DMR Plus unit (GE Medical Systems, Milwaukee, Wis). Spot compression views were obtained of all lesions manifested as asymmetric densities and of all palpable masses. Spot magnification views were obtained of all masses not clearly circumscribed on the original or spot compression views. Two radiologists (W.A.B. and C.I.C.) specializing in breast imaging reviewed the mammographic (n ⫽ 127) and sonographic (n ⫽ 150) images again and recorded features in consensus. All authors compared the imaging features with histopathologic and cytologic findings and/or culture diagnoses. Anechoic masses with an imperceptible circumscribed border and acoustic enhancement were classified as simple cysts. Complicated cysts were defined by Mendelson et al (8) as lesions with homogeneous low-level echoes that otherwise meet the criteria of a simple cyst. Circumscribed cystic lesions with imperceptible wall and fluid-debris level were included as complicated cystic lesions. Lesions composed entirely of clusters of tiny (2–5 mm) anechoic foci with no discrete solid component were termed clustered microcysts. Septations within a cyst were defined as thin (⬍0.5 mm, representing the combined thickness of two myoepithelial and epithelial cell layers) or thick (ⱖ0.5 mm). A thick wall was any perceptible wall. Intracystic masses had a discrete solid mural mass within a cyst. Grouped with these were mixed cystic and solid masses with at least 50% cystic component. Masses that were at least 50% solid with eccentric cystic foci were considered the final category. Sonographic and mammographic margins of the masses were recorded. For circumscribed lesions, the shape (round, oval, lobular, or tubular) was recorded. Lesions of mammographically focal increased density without convex borders were classified as focal asymmetries. RESULTS Of 150 cystic lesions, 16 were classified as simple cysts, 38 as complicated cysts, one as a cyst with thin septations, 16 as clustered microcysts, 23 as masses with thick wall and/or thick septations, 18 as intracystic or mixed cystic and solid masses, and 38 as mainly solid masses with eccentric cystic foci (Table 1). Of the 150 lesions, 18 (12%) proved to be maligBerg et al Radiology TABLE 1 Subclassification, Method of Sampling, and Rates of Malignancy of 150 Cystic Lesions Sonographic Feature Aspiration* CNB† Aspiration and CNB Malignancy Simple cyst (n ⫽ 16) Complicated cyst (n ⫽ 38) Cyst with thin septations (n ⫽ 1) ‡ Clustered microcysts (n ⫽ 16) Mass with thick wall and/or thick septations (n ⫽ 23) ‡ Intracystic mass, mixed cystic and solid (n ⫽ 18) § Solid mass with eccentric cystic foci (n ⫽ 38) 15 22 1 5 NA 13 NA 11 1 3 NA NA 0 (0) 0 (0) 0 (0) 0 (0) 9 10 4 7 (30) 2 1 13 34 3 3 4 (22) 7 (18) 55 81 14 18 (12) Total Note.—Data are the number of lesions. Data in parentheses are percentages. NA ⫽ not applicable. * Aspirations were performed with sonographic guidance by using an 18 –20-gauge needle and single pass. † Performed with 14-gauge automated biopsy gun with sonographic guidance. ‡ Thin septations are defined as ⬍0.5 mm, thick septations are defined as ⱖ0.5 mm. § Fourteen intracystic masses and four masses that were mixed cystic and solid and at least 50% cystic. nant, and 15 (83%) of 18 malignant lesions were palpable. Simple Cysts Sixteen sonographically simple cysts were aspirated because they were tender and palpable. One lesion required CNB owing to questionable persistence of the wall after aspiration (Table 1) and proved to be due to apocrine metaplasia. One abscess had the appearance of a simple cyst (Table 2). Follow-up was available for all but three simple cysts. Of 13 cysts with follow-up, five (39%) recurred and one of those was excised owing to a thick wall at recurrence (yielding a benign cyst) (Table 3). Complicated Cysts Of the 38 sonographically complicated cysts, 19 yielded benign cyst fluid (Fig 1); six, abscesses; five, fibrocystic changes; four, apocrine metaplasia; two, fat necrosis; and one each, papilloma and galactocele (Table 2). At times, echogenic foci could be seen to be moving within the cyst fluid (Fig 2). Seventeen cysts were palpable and none proved to be malignant. Of 34 complicated cysts with an acceptable standard, one galactocele recurred and was reaspirated (Table 3). Three apparent complicated cysts were excised: one recurrent cyst, one papilloma that enlarged due to infarction, and one fat necrosis and/or seroma at a site of prior benign surgical biopsy that was subjected to three aspirations with recurrence. Volume 227 䡠 Number 1 Cyst with Thin Septations One palpable 4-cm cyst containing thin (⬍0.5 mm) septations (Fig 3) was aspirated to resolution with benign cytologic results and has recurred at 12 months. Clustered Microcysts Of 16 masses characterized as clusters of microcysts (Fig 4), seven (44%) were due to apocrine metaplasia; six (38%), fibrocystic changes; two (13%), cysts; and one (6%), fibroadenoma, with no malignancies (Table 2). Twelve (75%) of 16 masses had an acceptable standard. One cluster of microcysts had slightly enlarged at initial 6-month follow-up and was subjected to another CNB with the same result of fibrosis with cysts; this mass has been stable at 53-month followup. Masses with Thick Wall and/or Thick Septations Another 23 cystic lesions had thick (ⱖ0.5 mm) walls and/or thick (ⱖ0.5 mm) septations, of which seven (30%) were malignant (Figs 5–7). Of the seven malignancies, six (86%) were invasive ductal carcinomas (IDCs) grade 3, one of which had an associated intraductal component, and one was IDC grade 2 (Table 2). Of 18 abscesses, eight (44%) manifested as thick-walled cystic masses (Fig 8). Two abscesses with this appearance recurred: one was reaspirated and one was surgically incised and drained (Table 3). An- other patient developed an irregular mass at the site of the initial abscess drainage; the mass was excised, showing scar tissue. Other benign causes of thick-walled cysts included simple cysts (including one with rupture and chronic inflammation), fibrocystic changes, and fat necrosis (Table 2). One fibrocystic change with atypia at cytologic examination recurred and was excised with benign results. Intracystic or Mixed Cystic and Solid Masses Of 18 total intracystic (n ⫽ 14) or mixed cystic and solid (n ⫽ 4, at least 50% cystic) masses, four (22%) proved to be malignant, including two intracystic papillary carcinomas (ductal carcinoma in situ [DCIS]) (Fig 9), one infiltrating and intraductal carcinoma (Fig 10), and one IDC grade 3. Five (28%) were due to benign papillomas (Table 2). One large galactocele appeared to be a complex cystic and solid mass due to intervening normal tissue (Fig 11) and was aspirated twice. One intracystic mass revealed fibrocystic changes and a single adjacent duct profile with atypical ductal hyperplasia; this mass was excised, showing only fibrocystic changes. One papilloma showed moderate enlargement (16 mm, compared with 10 mm) at 5 years of follow-up, and findings at excision confirmed benign papilloma. Another papilloma was excised due to persistent nipple discharge. Solid Masses with Eccentric Cystic Foci Of 38 predominantly solid masses with eccentric cystic foci, seven (18%) proved malignant (Table 1), including two IDCs (Fig 12), two invasive and intraductal carcinomas, one invasive lobular carcinoma, one mixed invasive lobular and ductal carcinoma with associated DCIS, and one intracystic papillary DCIS (Table 2). Other lesions with this appearance included fibrocystic changes (n ⫽ 14), fibroadenoma (n ⫽ 11), fat necrosis (n ⫽ 1), abscess (n ⫽ 1), and lactating adenoma (n ⫽ 1) (Table 2). Margin Characteristics Of 18 malignancies, three (17% [one intracystic papillary DCIS and two IDCs grade 3]) were circumscribed round or oval masses at mammography (Table 4). Another three (17% [one intracystic papillary DCIS, one medullary carcinoma, and one IDC grade 3]) were partially obscured. Similarly, five (6%) of 83 sono- Cystic Lesions of the Breast: Sonographic-Pathologic Correlation 䡠 185 Radiology TABLE 2 Correlation of Histopathologic Outcome and Sonographic Features for 150 Cystic Lesions Finding Simple Cyst Complicated Cyst 8 0 7 1 0 0 0 0 0 0 19 ⫹ 1* 5 4 6 0 1 2 1 0 0 Benign Cyst FCC AM Abscess Fibroadenoma Papilloma Fat necrosis Galactocele Periductal mastitis/cyst rupture Lactating adenoma Malignant IDC IDC and DCIS DCIS ILC IDC, DCIS, and ILC Total 0 0 0 0 0 Mass with Thick Wall and/or Thick Septations Intracystic Mass, Mixed Cystic and Solid Solid Mass with Eccentric Cystic Foci Total 2 6 7 0 1 0 0 0 0 0 3 1 1 8 0 0 2 0 1 0 1 3 1 2 0 5 0 1 1 0 1 14 2 1 11 0 1 0 0 1 35 (23) 29 (19) 22 (15) 18 (12) 12 (8) 6 (4) 5 (3.3) 2 (1.3) 2 (1.3) 1 (0.7) 0 0 0 0 0 6 1 0 0 0 1 1 2 0 0 2 2 1 1 1 9 (6) 4 (2.7) 3 (2) 1 (0.7) 1 (0.7) 16 23 18 38 150 Clustered Microcysts 0 0 0 0 0 38 ⫹ 1* 16 Note.—Data are the number of lesions. Data in parentheses are percentages. AM ⫽ apocrine metaplasia without other fibrocystic changes; FCC ⫽ fibrocystic changes, including fibrosis, sclerosing adenosis, and apocrine metaplasia; ILC ⫽ invasive lobular carcinoma. * One cyst manifested multiple thin (⬍0.5 mm) septations. TABLE 3 Results of Follow-up of 150 Cystic Lesions after Initial Aspiration (n ⴝ 55), CNB (n ⴝ 81), or Both (n ⴝ 14) Follow-up Sonographic Appearance None ⱕ6 Month Simple cyst (n ⫽ 16) 3 cysts 1 (gone) Complicated cyst (n ⫽ 38) 3 cysts, 2 abscesses, 3 other Cyst with thin septations (n ⫽ 1) Clustered microcysts (n ⫽ 16) NA 5 (1 recurrent galactocele, reaspirated; 4 gone) NA 2 Mass with thick wall and/or thick septations (n ⫽ 23) 1 abscess Intracystic mass or mixed cystic and solid (n ⫽ 18) Mass with eccentric cystic foci (n ⫽ 38) 2 All lesions (n ⫽ 150) 12 Month* ⱖ24 Month† Surgery Defined Standard‡ 5 (3 recurred, 2 gone) 8 gone 6 (1 recurred, 5 gone) 14 gone 1 recurred NA NA 0 2 (1 gone, 1 stable) 4 (1 gone, 2 decreasing in size, 1 stable) NA 12 (75) 1 gone 10 (1 fibrocystic change with atypical cells, benign; 1 scar after abscess; 1 recurrent abscess; 7 malignancies) 23 (100) 1 gone 4 gone 1 cyst, 10 other 4 (1 recurrent abscess, reaspirated; 3 gone) 4 (1 gone, 3 decreasing in size) 2 (1 gone, 1 stable) 8 (7 gone, 1 fibrocystic change subjected to another biopsy) 7 gone 27 18 26 5 (1 gone, 3 stable, 1 fibroadenoma increasing in size) 1 cyst recurred as thick-walled cyst 16 (100) 3 (1 recurrent cyst, 1 recurrent fat necrosis, 1 papilloma enlarging due to infarction) 35 (92) 7 (2 papillomas; 1 atypical ductal hyperplasia at CNB, benign; 4 malignancies) 10 (6 gone, 3 10 (2 large palpable fibroadenomas, 7 malignancies, 1 enlarging lactating decreasing adenoma) in size, 1 stable) 48 31 16 (89) 24 (63) 126 (84) Note.—Unless otherwise specified, data are the number of lesions. NA ⫽ not applicable. * Follow-up imaging at least 11 full months after initial diagnosis is considered 12-month follow-up (range, 11–18 months; median, 14 months). † Follow-up imaging of at least 23 full months after initial diagnosis is considered 24-month follow-up (range, 23– 60 months; median, 32 months). ‡ Pathologic cysts and abscesses with clinical resolution were accepted as were all lesions excised, subjected to another biopsy, or reaspirated with the same benign result, benign (without atypia) that were gone or decreasing at any follow-up, or stable after 23 full months of follow-up. Data in parentheses are percentages. 186 䡠 Radiology 䡠 April 2003 Berg et al Radiology Figure 1. Complicated cyst with inflammatory changes. Transverse sonogram (10 MHz) of palpable mass obtained in a 53-year-old woman demonstrates a well-defined mass with homogeneous mobile low-level internal echoes and posterior acoustic enhancement (arrows). Aspiration yielded benign cyst with inflammatory changes. graphically circumscribed oval or round masses were malignant, and all five were palpable. Another seven (22%) of 32 sonographically circumscribed lobular masses were malignant. DISCUSSION A sonographically simple cyst (anechoic with a well-defined imperceptible wall and posterior acoustic enhancement) can be dismissed as benign (11), BI-RADS category 2 (12). If the patient is symptomatic with pain or a very large cyst, aspiration can be performed electively. When the fluid is typical of that of a benign cyst, such as cloudy yellow or greenish black fluid, it can be discarded as is generally our practice. We send such fluid for cytologic examination only at patient request or for patients with a personal history of cancer or an atypical lesion. Ciatto et al (13) in their series of 6,782 consecutive cysts that were aspirated found five papillomas, all of which had bloody fluid. Smith et al (14), in their analysis of 660 aspirates, and Hindle et al (15), in an analysis of 689 medical records, similarly suggest discarding the fluid unless it is bloody. The differentiation of a simple cyst from one with internal echoes or even solid lesions can be problematic at times, particularly if the lesion is deep or very small. With current transducers, most simple cysts 5 mm or larger can be reliably characterized with standard linearVolume 227 䡠 Number 1 Figure 2. Complicated cyst, apocrine metaplasia. Radial sonogram (7.5 MHz) obtained in a 43-year-old woman shows mobile debris with a fluid-debris level (arrow) in a symptomatic cyst that otherwise met the criteria of simple cyst. Aspiration yielded apocrine metaplasia. array high-frequency transducers (center frequency of at least 10 MHz). Use of lower-frequency transducers, such as 7.5 MHz or lower, may be necessary for characterization of deeper cysts. Decrease in dynamic range can improve the ability to differentiate cystic and solid lesions. The use of tissue harmonic imaging may improve operator confidence in characterizing a lesion as a cyst, as has been shown in abdominal sonography (16), and is especially helpful in reducing artifactual internal echoes (17). Of 25 lesions in this series suspected to be complicated cysts that were initially aspirated, 22 (88%) resolved at aspiration and three (two abscesses and one fibrocystic change with apocrine metaplasia) had remaining thick walls. Another 13 (34%) of 38 lesions with the appearance of a complicated cyst in retrospect were subjected to initial diagnosis at CNB because they were believed to be solid at real-time evaluation. Spatial compounding, in which the sonographic image is derived from the input of multiple off-perpendicular beams, may also facilitate evaluation of complicated cysts and masses that might be cysts or solid masses. In an evaluation of 166 cysts and/or complex cysts, spatial compounding increased diagnostic certainty in 77% of lesions (Stavros AT, personal communication, 2002). In 13 masses indeterminate for a cyst or a solid mass, diagnostic certainty was improved with spatial compounding in 85% of cases (Stavros AT, per- Figure 3. Cyst with thin septations. Transverse sonogram (7.5 MHz) obtained in a 48year-old woman shows a large cyst with thin (⬍0.5 mm) septations (arrowheads) that otherwise met the criteria for a simple cyst. This finding may represent the continuum of the spectrum from apocrine metaplasia as the acini fuse. Because it was large and tender, the cyst was aspirated to complete resolution, and results of cytologic examination yielded benign cyst contents. This recurred at 1-year follow-up. sonal communication, 2002). Margin definition is similarly improved with spatial compounding (18). Spatial compounding is particularly helpful in decreasing speckle and other sources of noise; as a result, there is better definition of internal structure within masses (18). The improved signalto-noise ratio also facilitates recognition of small cysts, though posterior enhancement is less apparent with spatial compounding (18). Merritt et al (18) found that the benefits of real-time spatial compounding decreased with increasing lesion depth. In the series of Venta et al (10), only one (0.3%) of 308 complicated cysts proved malignant, which was a 3-mm focus of DCIS diagnosed at CNB. Buchberger et al (19) found none of 133 such lesions malignant, and Kolb et al (20) found none of 126 such lesions malignant in their series of screening sonography. In our series, none of 38 complicated cysts proved to be malignant. Thus, cumulatively, only one (0.2%) of 605 complicated cysts has proved to be malignant. If a complicated cyst remains difficult to distinguish from a solid mass based on imaging characteristics alone, then we must consider the implications of following the mass if indeed it is solid. Of 2,072 breast imaging procedures in our database, three (0.1%) were believed to be complicated cysts, with aspiration initially attempted, but which proved entirely solid, yielding two fibroadenomas and one fibrocystic change at CNB. Each Cystic Lesions of the Breast: Sonographic-Pathologic Correlation 䡠 187 Radiology Figure 4. Clustered microcysts, apocrine metaplasia. Radial sonogram (10 MHz) obtained in a 50-year-old woman shows an incidental aggregate of tiny cystic foci (arrowheads) without a discrete solid component. In our experience, these sonographic features have been shown to correspond to benign breast disease, such as apocrine metaplasia, or fibrocystic changes without apocrine metaplasia. At histopathologic examination of the 14gauge CNB specimen, dilated acini were demonstrated, lined by apocrine metaplastic epithelium. We now classify such nonpalpable lesions as probably benign with a 6-month follow-up. of these three solid masses were deep at the chest wall. Stavros et al (5) showed that nonpalpable, oval or gently lobulated, circumscribed, homogeneously hypoechoic masses with no distinctive posterior features and no suspicious features had less than 2% risk of malignancy, though this has not yet been reproduced at multiple centers. Possibly solid masses with posterior enhancement (as would be seen with complicated cysts) have not been so characterized. Complex cystic masses with discrete solid components clearly require biopsy based on the results of this series. It is hoped, however, that through the use of spatial compounding, tissue harmonic imaging, decrease in the dynamic range, and increase in operator experience, lesions suspected to be complicated cysts will be followed up. Multicenter validation of this approach is planned. With further experience, we may find that when mobile internal echoes are depicted in such a lesion, classification as benign may be appropriate. Anecdotally, we have noted that complicated cysts are seen in patients with other simple cysts; an isolated complicated cyst versus a solid mass may not have the same risk of malignancy, though this concept also requires validation. A new or enlarging complicated cyst versus solid mass likely 188 䡠 Radiology 䡠 April 2003 Figure 5. Thick-walled cystic mass, IDC grade 3. Radial sonogram (10 MHz) of a palpable mass obtained in a 43-year-old woman demonstrates an indistinctly marginated centrally cystic mass with a thick wall (arrows). Cytologic finding of the sonographically guided bloody aspirate of the cystic component was suggestive of malignancy, and CNB of the residual solid component yielded IDC, grade 3. The lesion resolved after neoadjuvant chemotherapy, and the site was difficult to identify for excision. Clip placement is advocated if the lesion is subtle or neoadjuvant chemotherapy is planned. merits aspiration as the risk of malignancy may be greater in this context. Symptomatic complicated cysts generally warrant aspiration. This would include tender or palpable complicated cysts. Again, as with simple cysts, we examine cytologic specimens only of bloody fluid. An abscess can appear as a well-defined cystic lesion with low-level internal echoes, and abscesses accounted for six (16%) of 38 complicated cysts in our series. When an abscess is suspected clinically at imaging or at inspection of the fluid, we send the fluid for culture and Gram staining and initiate a course of antibiotics that is appropriate for skin organisms. In the appropriate clinical setting, hematomas, fat necrosis, and galactoceles can appear as complicated cysts. Management should be predicated on the basis of patient symptoms. Of 35 lesions proving to be cysts, seven (20%) recurred after initial aspiration. Cysts with a proliferative apocrine lining have been suggested to be at higher risk of recurrence than those with flat epithelium (21) and to carry an increased risk of malignancy (22) that is on the order of two-fold relative risk (23,24). Indeed, Bodian et al (24) suggested that the risk of malignancy was proportional to the number of cyst aspirations (which in turn may be related to proliferative Figure 6. IDC (medullary type) with thick wall and thick septations. (a) Radial sonogram (7.5 MHz) of a palpable mass obtained in a 46-year-old woman demonstrates a thickwalled (arrows) cystic mass with thick septations (arrowheads). Posterior acoustic enhancement is present. The margins appear indistinct. (b) Mammographically, this was a new, partially circumscribed, and partially indistinctly marginated mass (arrow) in a patient with multiple bilateral circumscribed masses due to fibroadenomas and a cyst. Sonographically guided CNB with a 14-gauge needle and subsequent excision confirmed IDC grade 2, medullary type. changes in the cysts), with women who had undergone more than 10 cyst aspirations at up to a six-fold increased risk of breast cancer. None of the recurrent cysts in our series had apocrine lining, and the two recurrent cysts that were excised proved to be benign. With the detail apBerg et al Radiology Figure 7. Thick-walled cystic mass with thick septations, IDC grade 3. Transverse sonogram (10 MHz) obtained in a 35-year-old woman shows a cystic mass with posterior acoustic enhancement, thick wall, and thick septations (arrowheads). Aspiration yielded bloody fluid, and CNB findings of the residual solid component yielded IDC grade 3. Figure 8. Thick-walled complicated cyst, abscess. Radial sonogram (10 MHz) obtained in a 48-year-old woman shows a cystic mass with thick wall (arrows), posterior acoustic enhancement, and internal echoes that were mobile, with fluid-debris level (arrowhead) near the nipple. The surrounding tissue shows increased echogenicity compatible with edema. The mass was tender and palpable and was therefore aspirated to resolution, yielding pus. parent with use of current sonographic transducers, it is doubtful that excision is necessary for a recurrent simple cyst unless it is desired by the patient. The instillation of air at the time of aspiration appears to decrease the risk of recurrence (25), but it did not prevent recurrence of a 7-cm postoperative seroma with fat necrosis in our series. In an overlapping series, we previously suggested that pure clusters of microcysts Volume 227 䡠 Number 1 Figure 9. Intracystic mass, intracystic papillary DCIS. Radial sonogram (10 MHz) of a palpable mass obtained in a 36-year-old woman revealed a well-defined mass with a discrete solid component (arrow). Sonographically guided CNB yielded atypical ductal hyperplasia with papillary features. Excisional histopathologic examination revealed intracystic papillary DCIS. Atypical papillary lesions observed at CNB should be excised due to a 30% risk of malignancy at excision (39 – 41). without discrete solid components can be considered probably benign (26) and be followed up. Such lesions are often due to apocrine metaplasia, though fibrocystic changes without apocrine metaplasia can have a similar appearance. It is possible that larger cysts with thin septations represent the continuum of the spectrum from apocrine metaplasia to cysts as acini fuse (26). In our collective experience (27), we have biopsy proof (n ⫽ 18) or 2-year follow-up results (n ⫽ 48) of 66 lesions prospectively characterized as clustered microcysts with no malignancies, and we now follow such lesions at 6, 12 and 24 months. Multicenter validation of this approach is required and planned. A thick wall or thick septations (ⱖ0.5 mm) in an otherwise cystic lesion without antecedent trauma or evidence of infection should suggest possible malignancy and prompt biopsy. We found that seven (35%) of 20 lesions without such relevant history were malignant, with six (86%) of seven due to high-grade IDCs. With current transducers, the sonographic borders of thick-walled cystic lesions are more typically indistinct, though the mammographic appearance may be circumscribed. While low-grade IDC is more often spiculated, circumscribed borders can occur with highgrade malignancies, which were seen in 16% of such lesions in the series of Lamb et al (28). Of eight high-grade IDCs in our Figure 10. Intracystic mass with thick septations, infiltrating and intraductal cribriform carcinoma. Transverse sonogram (7.5 MHz) of a palpable mass obtained in a 77-year-old woman shows a complex mixed cystic (C) and solid (S) mass. Excision showed infiltrating and intraductal cribriform carcinoma. series, three (33%) were circumscribed at sonography. One of these high-grade cancers had medullary features, and the others were IDC not otherwise specified. While aspirates can demonstrate malignant cells, the cystic component of thick-walled cysts can be necrotic or acellular (and thereby nondiagnostic), and CNB of the wall or septations is preferred to provide a specific diagnosis and facilitate definitive treatment. Indeed, the cystic component of high-grade malignancies in this series represented areas of necrosis. Placement of a clip or an embolization coil marker at the time of sonographic biopsy (29 –31) will facilitate subsequent identification of the lesion if excision is required. This is particularly important for lesions that are small (ⱕ7 mm in our experience) or appear to resolve after aspiration or CNB or if neoadjuvant chemotherapy is planned (32). Abscesses, apocrine metaplasia, and inflamed or ruptured cysts or ducts can also present as thick-walled cysts. Hematomas can also have thick walls or thick septations. Fat necrosis can manifest as a thick-walled cystic lesion or a mixed complex cystic and solid mass, accounting for seven (23%) of 31 lesions with fat necrosis in one series (33) and nine (8%) of 112 in another (34). Short follow-up (2–3 months until resolution) of a thickwalled cystic lesion may be appropriate in the proper clinical setting of trauma or signs of infection. Any enlargement of such a lesion should prompt biopsy, as an underlying malignancy can either bleed due to trauma or cause obstruction Cystic Lesions of the Breast: Sonographic-Pathologic Correlation 䡠 189 Radiology TABLE 4 Mammographic and Sonographic Margins of 150 Cystic Lesions and Rates of Malignancy Margins No. of Lesions No. of Malignant Lesions Mammographic Circumscribed round or oval Circumscribed lobular Circumscribed tubular Obscured Microlobulated Indistinct Spiculated Asymmetric density Not seen Total with mammographic evaluation 37 19 1 25 4 14 2 7 18 127* 3 (8) 0 (0) 0 (0) 3 (12) 0 (0) 5 (36) 2 (100) 1 (14) 2 (11) 16 (13)* Sonographic Circumscribed round or oval Circumscribed lobular Circumscribed tubular Microlobulated Indistinct Irregular Total with sonographic evaluation 83 32 2 17 13 3 150 5 (6) 7 (22) 0 (0) 2 (12) 3 (23) 1 (33) 18 (12) Note.—Data in parentheses are percentages. * No mammograms were obtained for 23 lesions, including two malignancies. of ducts and predispose the patient to infection. Both benign and malignant papillary lesions often manifest as intraductal or intracystic masses (35–37), and three (75%) of four malignant intracystic masses were papillary in this series. Intracystic papillary carcinoma remains uncommon, accounting for only 0.6% of breast cancer in one series (38) and for 0.8% (four of 500) of breast cancers in our biopsy population. Caution is appropriate in accepting benign papilloma as a diagnosis at CNB, because malignancy and atypia can be focal in a large papilloma. Mammographic- and sonographichistopathologic concordance, including size concordance, are critical with papillary lesions, as benign papillomas can also be an incidental finding adjacent to cancers, with such malignancies reported in two (17%) of 12 lesions excised after a CNB diagnosis of benign papilloma in two series (39,40). Any irregular or indistinctly marginated masses yielding benign papilloma at CNB should be considered discordant and prompt excision (40). Clearly, atypical papillary lesions should be excised, with six (30%) of 20 proving malignant in several small series (39 – 41). In the review of Reynolds (42), one (50%) of two sclerosed papillomas proved to be malignant. Eccentric cystic foci can be due to dilated ducts, acini, or necrosis. Fibroadenomas rarely can have eccentric cystic foci, as was first described by Jackson et al 190 䡠 Radiology 䡠 April 2003 (43). Only 12 (2.9%) of 407 fibroadenomas in our database had cystic foci. The presence of cystic foci in a mass that is otherwise consistent with a fibroadenoma may suggest a possible phyllodes tumor, though such tumors are rare. Cystic foci were seen in seven (23%) of 30 phyllodes tumors in the series of Liberman et al (44) and were more common in malignant phyllodes tumors. Apocrine metaplasia can coexist with a variety of benign lesions, including fibroadenoma, and be evident as eccentric cystic foci (26). Malignancies with eccentric cystic foci had no particular distinguishing features in our series, with low- and highgrade IDC, invasive lobular carcinoma, and intraductal carcinoma rarely having this appearance. The margin characteristics of cystic lesions also merit discussion. For nonpalpable mammographically circumscribed masses, Sickles (45,46) and Varas et al (47) have shown that the risk of malignancy is less than 2% and that such lesions can be followed up. Indeed, none of the 29 nonpalpable sonographically circumscribed round or oval lesions were malignant in our series. Of the 54 palpable circumscribed round or oval lesions, five (9%) proved to be malignant. Those five malignancies were seen as intracystic masses (n ⫽ 2), thick-walled cystic masses (n ⫽ 2), and a predominantly solid mass with eccentric cystic foci (n ⫽ 1). All sonographically circumscribed lobulated masses that were malignant in this series Figure 11. Complex mass, galactocele. Transverse sonogram (7.5 MHz) of palpable mass occupying most of the breast obtained in a 18-year-old woman shows a complex cystic (C) and solid (S) mass. Aspiration was performed for symptomatic relief, yielding 250 mL of breast milk. The solid components were due to intervening normal breast tissue with extensive galactocele. Figure 12. Predominantly solid mass with eccentric cystic spaces, IDC grade 3. Transverse sonogram (10 MHz) of a palpable mass obtained in a 36-year-old woman with prior contralateral cancer 2 years earlier shows lobulated hypoechoic mass with eccentric cystic spaces (arrowheads). Findings of fine-needle aspiration (at an outside institution) showed atypical cells but were nondiagnostic. Gadolinium-enhanced breast magnetic resonance (MR) imaging demonstrated a rim-enhancing mass that was highly suggestive of malignancy. On the basis of MR imaging findings, the patient was referred for excision and sentinel node biopsy, which revealed IDC grade 3. were complex cystic and solid masses. As has previously been suggested (48), sonography may be helpful in identifying those circumscribed masses that merit biopsy. In conclusion, sonographically simple cysts can be dismissed as benign. On the Berg et al Radiology basis of the collective experience of this series and of the literature, the majority of incidental nonpalpable complicated cysts containing low-level echoes or fluid-debris levels may be be classified as probably benign, though further study is warranted and planned. Symptomatic complicated cysts should be managed on clinical grounds and generally warrant aspiration, with abscess, hematoma, fat necrosis, and galactocele in the differential diagnosis. In this series, all clustered microcysts were benign, though further study is required. 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