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(Radiology. 2000;216:831-837.)
© RSNA, 2000


Breast Imaging

Uncommon High-Risk Lesions of the Breast Diagnosed at Stereotactic Core-Needle Biopsy: Clinical Importance1

Liane E. Philpotts, MD, Nancy A. Shaheen, MD 2, Kiren S. Jain, MD, Darryl Carter, MD and Carol H. Lee, MD

1 From the Departments of Diagnostic Radiology (L.E.P., N.A.S., K.S.J., C.H.L.) and Pathology (D.C.), Yale University School of Medicine, 333 Cedar St, PO Box 208042, New Haven, CT 06520. From the 1998 RSNA scientific assembly. Received October 28, 1999; revision requested December 15; revision received February 14, 2000; accepted February 22. Address correspondence to L.E.P. (e-mail: philpotts@biomed.med.yale.edu).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To assess the outcome of papillary lesions, radial scars, or lobular carcinoma in situ (LCIS) diagnosed at stereotactic core-needle biopsy (SCNB).

MATERIALS AND METHODS: Retrospective review of 1,236 lesions sampled with SCNB yielded 22 papillary lesions, nine radial scars, and five LCIS lesions. Diffuse lesions such as papillomatosis, papillary ductal hyperplasia, papillary ductal carcinoma in situ (DCIS), and atypical lobular hyperplasia were not included. The mammographic findings, associated histologic features, and outcome were assessed for each case.

RESULTS: Sixteen papillary lesions were diagnosed as benign at SCNB. Of these, five were benign at excision, and 10 were unremarkable at mammographic follow-up. At excision of an unusual lesion containing a microscopic papillary lesion, DCIS was found. Three of four papillary lesions suspicious at SCNB proved to be papillary carcinomas; the fourth had no residual carcinoma at excision. Eight of nine radial scars were excised, which revealed atypical hyperplasia in four scars but no malignancies. One LCIS lesion was found at excision to contain DCIS.

CONCLUSION: Benign or malignant papillary lesions were accurately diagnosed with SCNB in the majority of cases. Cases diagnosed as suspicious for malignancy or with atypia or unusual associated histologic findings should be excised. No malignancies were found at excision of radial scars diagnosed at SCNB. Surgical removal of these lesions following SCNB may not be routinely necessary. DCIS was found in one lesion diagnosed as LCIS at SCNB, which suggests that removal of these lesions may be prudent.

Index terms: Breast, biopsy, 00.1267 • Breast, diseases, 00.31, 00.32, 00.321 • Breast, radial scar, 00.31 • Breast neoplasms, diagnosis, 00.31, 00.32, 00.321


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Papillary lesions, radial scars, and lobular carcinoma in situ (LCIS) are infrequent histologic entities found at stereotactic core-needle biopsy (SCNB) (15). The management of these lesions after a SCNB diagnosis has not been well established (4,5). Differentiation of benign papillomas from papillary carcinomas (68) and of LCIS from ductal carcinoma in situ (DCIS) (9,10), particularly with the limited material from core-needle samples, can be difficult. Radial scars may have some morphologic similarity to tubular carcinoma, as well as a reported association with carcinoma (1114). Radial scars and LCIS are also markers for an increased risk of invasive carcinoma (1518). Removal of papillary lesions, radial scars, and certain LCIS lesions has been advocated after a SCNB diagnosis (2,5,1921). The purpose of this study was to determine the outcome of lesions diagnosed at SCNB as papillary lesions, radial scars, or LCIS in terms of surgical correlation or mammographic follow-up findings.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
From July 1992 to July 1998, 1,236 lesions in 1,129 patients were sampled by using SCNB. At our institution, SCNB is offered to all patients requiring a biopsy of a mammographic abnormality in whom it is considered technically feasible. Lesions appearing mammographically as masses, including architectural distortion, and calcifications are all considered, regardless of size.

From July 1992 until October 1996, 655 SCNBs were performed by using a 14-gauge needle (Biopty-Cut; Bard Radiologic, Covington, Ga) and an automated gun (Biopty Gun; Bard Radiologic). The technique of performing biopsy with this method has been described (22). The mean number of cores obtained in this group of cases was 6.0 (range, two to 18).

From October 1996 to July 1998, 581 cases (patient age range, 28–88 years; mean patient age, 54 years) were sampled with a vacuum suction device. Thirty procedures were performed by using a 14-gauge probe, and 551 procedures were performed by using an 11-gauge probe (Mammotome; Biopsy/Ethicon Endo-Surgery, Cincinnati, Ohio). The technique of performing these biopsies has also been described (23). The mean number of cores obtained was 8.4 (range, five to 20) in the 14-gauge vacuum suction probe group and was 11.4 (range, one to 30) in the 11-gauge vacuum suction probe group.

All procedures were performed with a dedicated prone table; from July 1992 through June 1997, the table was a Stereoguide table (LoRad, Danbury, Conn). From July 1997 through July 1998, the table was a Universal table (U.S. Surgical Corporation, Norwalk, Conn).

A retrospective review of the records of the breast imaging department was performed to identify cases in which the histologic SCNB findings included papillary lesions, radial scars, or LCIS, with or without other benign histologic findings. Only solid papillary tumors were assessed. Papillomatosis, papillary ductal hyperplasia, or papillary DCIS, which are diffuse lesions that do not form a localized tumor mass but extend throughout a ductal system, were not included. Lesions reported as only LCIS were considered. Those diagnosed as atypical lobular hyperplasia (ALH) alone were not included.

Of 1,236 SCNB cases, 38 (3.1%) were included: 23 papillary lesions (1.9%), 10 radial scars (0.8%), and five LCIS lesions (0.4%). From biopsy data recorded prospectively at the time of biopsy by the performing radiologist (all were experienced breast radiologists; includes L.E.P., C.H.L., N.A.S., and K.S.J.), the initial mammographic features of mass, architectural distortion, or calcifications; the size as measured from the largest mammographic diameter; the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS) assessment category (24); and the number of cores obtained at biopsy were assessed for each case. Calcified lesions were classified as "calcifications" if that was the dominant feature prompting biopsy. Mass lesions containing calcifications were included with masses. The associated histologic SCNB findings were recorded. The outcome of these lesions in terms of surgical histologic or mammographic follow-up findings after SCNB was assessed by one of two authors (L.E.P. or N.A.S.).

During the time of the study, we did not have a routine policy regarding the management of papillary lesions diagnosed at SCNB. The recommendation for repeat biopsy was at the discretion of the individual radiologist responsible for the procedure. Among 23 papillary lesions, subsequent surgery was performed in 12 (52%) and follow-up mammography was performed in 10 (43%). One had neither surgical nor mammographic follow-up information available and was excluded, which left 22 papillary lesions in the group.

During the study, it was our standard policy to recommend subsequent surgical removal of all radial scars and LCIS lesions found at SCNB. Excision was performed in eight of 10 (80%) radial scars, and mammographic follow-up information was available in another one (10%). One radial scar in a patient was excluded because mastectomy was performed for carcinoma elsewhere in the breast, and surgical correlation was not available. Thus, there were nine radial scars in the study group. All five (100%) LCIS lesions were surgically excised.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Twelve of the 22 papillary lesions (55%) manifested as masses, and 10 (45%) manifested as calcifications. Sixteen were diagnosed as benign or probably benign at SCNB (12 papillomas, two papillary lesions of unknown importance, and two probably benign papillary tumors), two were associated with atypical hyperplasia (one benign papillary tumor with atypical ductal hyperplasia [ADH] and one intracystic papillary tumor with atypia), and four were reported as suspicious for malignancy. Surgical excision was performed in all the atypia (n = 2) and suspicious (n = 4) cases. Six of the benign or probably benign cases were excised for reasons of uncertainty of findings (n = 3), small amount of tissue obtained (n = 1), mammographic-histologic discordance (n = 1), and associated unusual lesion (n = 1).

The initial mammographic findings and the SCNB and surgical histologic outcomes of the 12 papillary lesions that were excised are found in Table 1A. Five of the six benign or probably benign lesions were proved to be benign at excision. One case was diagnosed as borderline DCIS. This case had been diagnosed at SCNB as microscopic papilloma, fibrocystic changes, and a localized lesion with elastosis of the stroma and a profusion of small ducts with extensive apocrine metaplasia. The unusual histologic findings in this case (including suspicion for radial scar) prompted the recommendation for rebiopsy. The finding of microscopic papilloma at SCNB was considered incidental. Also, no radial scar was found at excision. Of the two cases that showed atypical hyperplasia at SCNB, both were benign at excision; one was a radial scar with benign nonspecific findings, and the other showed fibrocystic changes with atypia.


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TABLE 1. Papillary Lesions Diagnosed at SCNB
 
Three of the four papillary lesions diagnosed as suspicious for carcinoma at SCNB proved to be malignant at excision. Two were papillary carcinomas alone (one was intracystic), and one was intracystic papillary carcinoma associated with DCIS. The fourth case revealed only ADH at excision. The entire tumor was presumed to have been removed at 11-gauge vacuum-assisted biopsy, as the scar from the SCNB was identified in the surgical specimen.

The initial mammographic findings, SCNB findings, and mammographic follow-up findings of the 10 papillary lesions that were not excised are found in Table 1B. All were reported as papillomas or probable papillomas at SCNB. Mammographic follow-up (at a mean of 22 months after SCNB) showed five lesions to be gone (at 13, 19, 26, 33, and 34 months), three lesions to be decreased in size (at 6, 16, and 30 months), and two lesions to be unchanged in size (at 11 and 28 months).

The mammographic and histologic findings in the nine radial scars are found in Table 2. Only three cases manifested mammographically as architectural distortion. Four cases were calcifications, and two cases were masses. Seven radial scars were reported to be associated with benign findings, and two were reported to be associated with ADH at SCNB. Both cases with associated ADH and two cases with associated benign findings at SCNB were found at excision to have ADH. However, no malignancies were found. One case of radial scar with associated benign findings was not excised because of patient refusal. Mammographic follow-up in this case showed stable findings at 15 months.


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TABLE 2. Radial Scars Diagnosed at SCNB
 
The initial mammographic and histologic findings from the five cases of LCIS found at SCNB are shown in Table 3. Two manifested mammographically as masses, and three manifested mammographically as calcifications. Four cases were diagnosed with associated atypia at SCNB: three with ALH and one with ADH. None of these were found to be malignant at excision. The one case of LCIS without atypia, however, revealed LCIS with DCIS at excision.


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TABLE 3. LCIS Diagnosed at SCNB
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Papillary lesions, radial scars, and LCIS are lesions that are diagnosed infrequently at SCNB. In our series, these lesions were found in only 3.1% of all SCNB cases: papillary lesions, 1.9%; radial scars, 0.8%; and LCIS, 0.4%. Liberman et al (4) reported papillary lesions in 34 of 1,077 cases (3%), and Rubin et al (2) reported papillary lesions in eight of 200 core-needle biopsies (4%). Jackman et al (3) reported radial scars in five of 483 SCNBs (1%). Liberman et al (5) found LCIS in 16 of 1,315 core-needle biopsies (1.2%).

Papillary lesions may be either benign or malignant. Benign papillomas can occur either as solitary central papillomas or as multiple peripheral lesions. Malignant papillary tumors include intracystic papillary carcinoma and invasive papillary carcinoma. At mammography, benign papillomas can be occult or manifest as masses or calcifications (11,25,26). Papillary carcinomas, likewise, may be identified as masses or calcifications, which makes mammographic differentiation of benign and malignant forms impossible (2729). At histologic analysis, a benign papilloma is identified as a fibrovascular stalk covered with normal ductal epithelium consisting of layers of epithelial and myoepithelial cells (Fig 1). A papillary carcinoma, on the other hand, has only a single cell layer surrounding the central stalk, lacking the myoepithelial layer seen in the benign lesion (Fig 2).



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Figure 1a. Papilloma. (a) Craniocaudal mammogram of the left breast in a 58-year-old woman shows a new, 9-mm, lobulated, circumscribed mass (arrow). (b) Photomicrograph of the SCNB specimen demonstrates an intracystic papillary lesion in which the predominant feature is the fibrovascular core (arrow), with minimal proliferation of both epithelium and myoepithelium on its surface. (Hematoxylin-eosin stain; original magnification, x25.)

 


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Figure 1b. Papilloma. (a) Craniocaudal mammogram of the left breast in a 58-year-old woman shows a new, 9-mm, lobulated, circumscribed mass (arrow). (b) Photomicrograph of the SCNB specimen demonstrates an intracystic papillary lesion in which the predominant feature is the fibrovascular core (arrow), with minimal proliferation of both epithelium and myoepithelium on its surface. (Hematoxylin-eosin stain; original magnification, x25.)

 


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Figure 2a. Papillary carcinoma. (a) Magnification view of a mammogram of the right breast in a 74-year-old woman shows two clusters of increasing pleomorphic calcifications; the anterior cluster is the lesion of interest (arrow). (b) Photomicrograph demonstrates this intracystic papillary carcinoma (arrow) to be markedly cellular and predominantly epithelial in this SCNB specimen. The posterior cluster of calcifications proved to be cribriform DCIS. (Hematoxylin-eosin stain; original magnification, x50.)

 


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Figure 2b. Papillary carcinoma. (a) Magnification view of a mammogram of the right breast in a 74-year-old woman shows two clusters of increasing pleomorphic calcifications; the anterior cluster is the lesion of interest (arrow). (b) Photomicrograph demonstrates this intracystic papillary carcinoma (arrow) to be markedly cellular and predominantly epithelial in this SCNB specimen. The posterior cluster of calcifications proved to be cribriform DCIS. (Hematoxylin-eosin stain; original magnification, x50.)

 
SCNB appears to yield an accurate diagnosis in the majority of cases of solid papillary lesions. In our study, most lesions that were reported as papillomas or benign papillary tumors at SCNB were truly benign at excision or were stable at follow-up. Our findings are similar to those reported by Liberman et al (4), where seven benign papillomas were confirmed with surgery or mammographic follow-up. In that series, diagnosis of benign papillary lesions at SCNB was found to be accurate when the imaging findings were concordant with the histologic findings.

Only two cases (9%) of papillary lesions were associated with atypical hyperplasia in our series, neither of which proved to be malignant at excision. Liberman et al (4) found a much higher rate of atypia in 10 of 26 cases (39%), with three (30%) ultimately proving to be malignant. The finding of atypical hyperplasia in a papilloma has been shown to increase the risk of the development of invasive carcinoma (30). Furthermore, the need for rebiopsy of all atypical hyperplasia lesions at SCNB has been well established (3134).

For malignant papillary lesions, the SCNB diagnosis also appears to have been accurate. Three cases that were reported as suspicious for carcinoma after SCNB were indeed malignant, and a fourth was completely excised during SCNB. We did not have any cases of invasive papillary carcinoma in our series; thus, the ability to differentiate the in situ from the invasive forms with SCNB cannot be determined from our data.

A great deal of controversy has surrounded radial scars of the breast. Histologically, these lesions have a central, fibroelastic core with entrapped glandular elements and a radiating system of ducts (Fig 3). The entrapped glands in the central aspect of these lesions superficially resemble tubular carcinomas, which leads some to believe there is an association between these two entities (12,14). Radial scars contain entrapped ducts lined with two layers of cells, epithelial and myoepithelial, with no substantial nuclear atypia, surrounded by a basement membrane, whereas tubular carcinomas have glandular structures lined with a single layer of cells, with nuclear atypia and no basement membrane (11). Some investigators have reported radial scars in association with carcinoma (1214).



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Figure 3a. Radial scar. (a) Spot compression mammogram in the craniocaudal projection in a 62-year-old woman shows an area of architectural distortion (arrows). (b) Photomicrograph of the SCNB specimen demonstrates a radial configuration of the proliferating ducts around the elastotic center (arrow). Each of the individual ducts has hyperplasia but not malignancy within its basement membrane. (Hematoxylin-eosin stain; original magnification, x50.)

 


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Figure 3b. Radial scar. (a) Spot compression mammogram in the craniocaudal projection in a 62-year-old woman shows an area of architectural distortion (arrows). (b) Photomicrograph of the SCNB specimen demonstrates a radial configuration of the proliferating ducts around the elastotic center (arrow). Each of the individual ducts has hyperplasia but not malignancy within its basement membrane. (Hematoxylin-eosin stain; original magnification, x50.)

 
Classically, radial scars manifest mammographically as a spiculated mass or architectural distortion with a central radiolucent area. However, many have an opaque center and calcifications that simulate invasive carcinoma; thus, mammography cannot reliably be used to distinguish between the two (3538). Many agree that for a mammographically detected lesion suggestive of a radial scar, surgical excision rather than SCNB should directly be performed (12,21,35). However, many radial scars are found at SCNB of nonspiculated masses or calcifications. Furthermore, at histologic analysis, many radial scars occur as multiple, microscopic lesions.

We found no carcinomas at the excision of SCNB-detected radial scars in our series, although there was a high rate of atypia at excision (50%). This perhaps reflects the proliferative nature of these lesions. While our numbers are small, the routine recommendation for excision of all radial scars found at SCNB may not be supported. Jackman et al (3) found carcinoma in two of five (40%) radial scars diagnosed at SCNB. Four (80%) were spiculated masses. The difference in our results may reflect the incidental nature of the radial scars in our cases. Many were found after SCNB of calcifications (44%) rather than of architectural distortion (33%) or masses (22%). Larger series are needed to determine the true risk of associated carcinoma with these incidental lesions.

LCIS has no specific mammographic features but rather is an incidental finding at biopsy (1618). It is often a diffuse, bilateral process. LCIS used to be considered a premalignant lesion and was treated with mastectomy but now is recognized only as a marker for increased risk of invasive carcinoma. At histologic analysis, expanded lobules with atypical epithelial cells containing small uniform nuclei are found. ALH has similar characteristics as LCIS, but the involvement of the terminal ducts and lobules is not as pronounced. When the abnormal cells of LCIS spill out of the lobule and terminal ducts, similarity with DCIS occurs. While histologic differentiation of LCIS and DCIS is usually not difficult, areas of overlap exist (10).

LCIS was found in association with atypical hyperplasia at SCNB in the majority (80%) of our LCIS cases. The single case of malignancy at excision, however, was in a case of LCIS without associated atypical hyperplasia at SCNB. This case manifested mammographically as a mass. Given that LCIS is an incidental finding, this was considered a mammographic-histologic discrepancy. Whether the failure to diagnose DCIS represented a sampling error or misdiagnosis at SCNB is not known. While LCIS is not a premalignant lesion itself, it has some cytologic similarities to ALH, DCIS, and invasive lobular carcinoma (10,1618). Thus, from findings in our small sample, it appears prudent to recommend the excision of LCIS lesions diagnosed at SCNB. Liberman et al (5) found cancer in four of 14 (29%) LCIS cases diagnosed at core biopsy. In those cases, LCIS was found in association with other high-risk lesions or had features overlapping with DCIS. Similarly, Lechner et al (39), in a multiinstitutional study of 32,424 lesions in which percutaneous core biopsy was performed, found 20 of 58 (34%) LCIS lesions diagnosed at SCNB to be malignant at excision.

As with histologic interpretation of all SCNB specimens, careful examination of the specimens is necessary to confidently exclude atypical or malignant findings. Differentiating benign from malignant papillary lesions, radial scars from tubular carcinomas, and LCIS from DCIS should be possible with careful review, although fragmentation of the lesions increases the challenge to diagnose these lesions correctly. Pathologist experience and expertise in the interpretation of breast tissue, especially core biopsy specimens, likely plays a role in the accurate diagnosis of these lesions. If there is any doubt as to the benign nature of a lesion, then surgical excision should be recommended.

The amount of tissue submitted, furthermore, likely relates to a more accurate diagnosis. Specimens obtained with an 11-gauge vacuum probe are significantly larger than those obtained with a 14-gauge needle and automatic gun (40). Use of the vacuum suction device has reduced the frequency of underestimation of carcinoma, particularly in cases of atypical hyperplasia and DCIS (33,41). Because of the small number of cases, comparison of the differences in the accuracy of the 14-gauge needle and automated gun versus the vacuum suction probe was not possible. In the two cases of SCNB underestimation (one papillary and one LCIS lesion), SCNB was performed with the 14-gauge needle and automatic gun, with only five cores obtained in each case. Whether the vacuum suction device will prove to be even more accurate in diagnosing these lesions is yet to be determined.

Because papillary lesions, radial scars, and LCIS are not common diagnoses at SCNB, our study is limited by the small number of cases of each. Larger studies will be necessary to corroborate our findings with the outcome and management of these lesions after SCNB.

Also, a large number of the papillary lesions were not excised. The choice to follow up such lesions rather than excise them may have been biased by the increased level of confidence of a benign diagnosis obtained after using the 11-gauge vacuum suction probe compared with the confidence after using the 14-gauge needle and automated gun. Most (eight of 10) of the cases followed up mammographically were completely or almost completely removed at biopsy and were noted to be either gone or decreased in size at follow-up.

Another potential limitation is the mean follow-up time of only 22 months. A follow-up time of 2–3 years following SCNB has been advocated for lesions sampled with the automatic gun (42). The appropriate follow-up period for lesions sampled with vacuum suction biopsy, however, has not been determined.

The results of this study show that most benign papillary lesions and some radial scars diagnosed at SCNB may not require surgical excision, but lesions diagnosed as LCIS, atypical, or suspicious for malignancy and those with unusual associated histologic findings, pathologist’s uncertainty, or mammographic-histologic discordance should be excised. The data presented in this study should aid physicians performing core-needle biopsies in the management of these lesions.


    FOOTNOTES
 
2 Current address: Utica, NY. Back

Abbreviations: ADH = atypical ductal hyperplasia, ALH = atypical lobular hyperplasia, BI-RADS = Breast Imaging Reporting and Data System, DCIS = ductal carcinoma in situ, LCIS = lobular carcinoma in situ, SCNB = stereotactic core-needle biopsy

Author contributions: Guarantor of integrity of entire study, L.E.P.; study concepts and design, L.E.P.; definition of intellectual content, L.E.P., D.C.; literature research, L.E.P.; clinical studies, L.E.P., N.A.S., K.S.J., C.H.L.; data acquisition, L.E.P., N.A.S., K.S.J.; data analysis, L.E.P.; manuscript preparation, L.E.P., D.C.; manuscript editing, L.E.P., D.C., C.H.L.; manuscript review, all authors.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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