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Papillary Lesions of the Breast at Percutaneous Core-Needle Biopsy¹

¹ From the Departments of Radiology (C.L.M., C.I.S.) and Pathology (J.C.), NYU Medical Center, 160 E 34th St, 3rd Floor, New York, NY 10016; and Departments of Pathology (D.H.) and Radiology (S.M.O.), New York Presbyterian Hospital-Columbia University, New York, NY. From the 2003 RSNA Annual Meeting. Received October 26, 2004; revision requested January 3, 2005; revision received February 24; accepted March 17; final version accepted May 17. Address correspondence to C.L.M. (e-mail: cecilia.mercado{at}med.nyu.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Purpose: To retrospectively review the imaging and histologic findings in patients in whom a benign papillary lesion was diagnosed at core-needle breast biopsy.

Materials and Methods: This retrospective study was approved by the institutional review board at each institution; patient consent was not required. The study was HIPAA compliant. The authors reviewed the findings from 42 patients (age range, 26–76 years; mean age, 54.3 years) with 43 benign papillary lesions diagnosed at core-needle biopsy. Thirty-six (84%) of the 43 lesions were surgically excised, and seven (16%) were followed up with long-term imaging. The authors assessed the radiographic findings, the histologic findings at core-needle biopsy, and the findings at subsequent surgical excision or imaging follow-up. Statistical analysis was performed on a per-patient basis and included the Blyth-Still-Casella procedure to construct exact 95% confidence intervals (CIs) and the Fisher exact test.

Results: At core-needle biopsy, lesions were diagnosed as papilloma (n = 29), sclerosing papilloma (n = 8), and benign papillary lesions not otherwise specified (n = 6). For the 36 lesions that were surgically excised, histologic follow-up showed no residual lesion in 10, intraductal papilloma in 14, intraductal papillomatosis in two, papilloma with adjacent foci of atypical ductal hyperplasia (ADH) in eight, and well-differentiated papillary ductal carcinoma in situ (DCIS) in two. Mammographic follow-up in the remaining seven lesions revealed stable calcifications in five (at 28–55 months) and no residual lesion in two (at 26–29 months). In nine of the 42 patients (21%), the diagnosis was upgraded to either ADH or DCIS (exact two-sided 95% CI = 11.4%, 36.4%).

Conclusion: The results strongly suggest that papillary lesions diagnosed as benign at core-needle biopsy should be surgically excised because a substantial number of lesions were upgraded to ADH and DCIS at excision.

© RSNA, 2006

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Papillary lesions of the breast comprise a wide spectrum of lesions ranging from benign papilloma, to papilloma with foci of atypia or carcinoma in situ, to intraductal adenocarcinoma with papillary growth pattern and papillary adenocarcinoma (1). The presence or absence of a myoepithelial cell layer in the papillary component of the lesion is the most important feature that helps differentiate a benign papilloma from a papillary carcinoma (1). Differentiation between these entities at histologic examination can be difficult (1,2). In previous studies, investigators evaluated the use of core-needle biopsy in the diagnosis of papillary lesions (3–12). Because these lesions are less frequently encountered, however, there are limited data upon which to base management recommendations. Thus, the purpose of our study was to retrospectively review the findings at imaging, histologic, and follow-up examinations in patients in whom a benign papillary lesion was diagnosed at core-needle breast biopsy.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patients
This retrospective review of images and data was approved by the institutional review board at each institution; patient consent was not required. The study was Health Insurance Portability and Accountability Act compliant for each institution. We (C.L.M., J.C.) searched the pathology databases from two institutions for women in whom a benign papillary lesion was diagnosed at core-needle breast biopsy and who subsequently underwent surgical excision or long-term imaging follow-up. Both institutions had similar patient populations. Forty-three lesions in 42 women were identified within a 6-year period (1997–2003). The mean patient age was 54.3 years (range, 26–76 years). Clinically, all lesions were nonpalpable. None of the patients presented with nipple discharge. All 43 lesions were peripheral in location (at least 2 cm from the nipple). Results from surgical excision were available for 36 patients, and results from long-term imaging follow-up were available for seven. The average length of radiographic follow-up was 39 months (range, 26–55 months). In this study, we included only those patients in whom subsequent surgical excision was performed or those who underwent imaging follow-up for at least 2 years.

Imaging Techniques
Bilateral mammography was performed with a dedicated mammography unit (Senographe 800T, GE Medical Systems, Milwaukee, Wis; or Lo-Rad MIV, Hologic, Bedford, Mass). Routine craniocaudal and mediolateral oblique views of the breast(s) and spot- or open-magnification views over the area of the lesion were obtained. Ultrasonography (US) was performed by using a 5–9- or 13-MHz linear-array transducer (Elegra; Siemens, Issaquah, Wash).

Biopsy
Core-needle biopsy was performed with US guidance in 20 of the 43 lesions and with stereotactic guidance in 23. For US, all masses were sampled by using a 5–9- or 13-MHz linear-array transducer (Elegra). Tissue samples were obtained with an automated biopsy gun with a 14-gauge needle (Bard Magnum; C.R. Bard, Covington, Ga) in 17 lesions and with an 11-gauge handheld biopsy device (Mammotome; Biopsys/Ethicon Endo-Surgery, Cincinnati, Ohio) in three. The type of biopsy performed was determined by the radiologist at the time of the procedure. The biopsy procedures were performed by radiologists (S.M.O., C.L.M., C.I.S.) with 5–11 years experience in breast imaging.

All patients with radiographically detected calcifications and lesions not identified at US underwent stereotactic biopsy with a dedicated prone table (Universal Table, U.S. Surgical, Norwalk, Conn; or Stereoguide, Lorad Medical Systems, Danbury, Conn). An 11-gauge directional vacuum biopsy device (Mammotome) was used in 22 lesions, and an automated biopsy gun (Bard Magnum) with a 14-gauge, 10-cm-long needle (Bard Magnum) was used in one lesion.

A mean of nine core samples (range, 3–18) were obtained per lesion when core-needle biopsy was performed with stereotactic guidance, and a mean of four core samples (range, 3–5) were obtained per lesion when biopsy was performed with US guidance. Radiography of the specimen was performed in all lesions that contained microcalcifications (n = 16). A localizing clip (Micromark; Byopsys/Ethicon Endo-Surgery) was placed at the biopsy site in all 23 patients who underwent stereotactic core-needle biopsy and in the three patients who underwent US-guided core-needle biopsy with the handheld biopsy device.

Image Evaluation
All lesions were evaluated for size. The mammographic and US appearances of the lesions were characterized according to the Breast Imaging Reporting and Data System (BI-RADS) lexicon and assessment categories (13). The imaging (mammography and US) findings for all lesions were reviewed retrospectively by a radiologist (C.L.M.) who was fellowship trained in breast imaging and had 9 years of experience. A pathologist (J.C., D.H., with 9 and 10 years experience in breast disease, respectively) at each institution independently reviewed the histologic findings from the core-needle biopsies and the surgical excisions.

Glass slides were evaluated for the presence of fibrovascular cores. The epithelial lining of the papillary processes was evaluated for the presence of atypia. Architectural and nuclear criteria for ductal carcinoma in situ (DCIS) were also evaluated.

Concordance and Management
The radiologist who performed the core-needle biopsy determined the concordance between the imaging and histologic findings of each case and the management of the benign papillary lesions. The findings were discordant when a BI-RADS score of 5 (highly suspicious for malignancy) was given to the lesion at imaging and the corresponding histologic finding was benign. In addition, the findings were discordant when a lesion manifested as a new finding in a postmenopausal woman (considered moderately suspicious with a BI-RADS score of 4) and had a benign histologic diagnosis at core-needle biopsy. Although most patients were referred for surgical excision, the management of papillomas classified as benign at core-needle biopsy is not uniform and, in some cases, a recommendation of short-term imaging follow-up was given.

Statistical Analysis
All statistical computations were performed by using software (SAS system for Windows, version 9.0; SAS Institute, Cary, NC), and results were declared statistically significant at the two-sided 5% significance level.

Upgrade rate.—An upgrade in diagnosis was determined when a patient had at least one lesion that was classified as atypical ductal hyperplasia (ADH) or DCIS at surgical excision or follow-up. Upgrade rates are given in terms of patients with lesions classified as ADH, DCIS, or either ADH or DCIS. Patients were classified into groups on the basis of properties associated with their lesions. The groups consisted of (a) all patients, (b) patients with lesions that were excised, (c) patients with sclerosing lesions, and (d) patients with nonsclerosing lesions. Because both lesions within the lone patient with multiple lesions were excised nonsclerosing papillomas seen as ADH at excision, there was no ambiguity for this patient in terms of upgrade type or patient group classification.

The Blyth-Still-Casella procedure was used to construct exact 95% confidence intervals (CIs) for the upgrade rate defined in terms of each lesion type within each patient group. The Fisher exact test was used to compare patients who had sclerosing lesions with those who had nonsclerosing lesions in terms of the rate of upgrade to each lesion type.

Negative predictive value.—The negative predictive value was estimated for malignancies defined as DCIS. The Blyth-Still-Casella procedure was used to construct exact 95% CIs for the negative predictive value for malignancy.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Histologic and Imaging Findings
A summary of the histologic and imaging findings in the 36 surgically excised lesions is given in Table 1. At core-needle biopsy, the histologic diagnoses of the 43 lesions were as follows: 29 papillomas, eight sclerosing papillomas, and six benign papillary lesions not otherwise specified. At mammography, these lesions manifested as masses in 23, calcifications in 14, a mass with calcifications in two, and an asymmetric density in three. One lesion was mammographically occult, and US demonstrated an intracystic echogenic lesion in the periphery of the breast. Twenty-four lesions were evaluated with US. US scans were available for 20 lesions; four lesions were not visualized with US. The US appearance of the 20 lesions included hypoechoic solid masses in 15 lesions, complex masses with solid and cystic components in two lesions, intracystic masses in two lesions, and a mass within a dilated duct in one lesion. Eight lesions were round and seven were oval. Five lesions had an irregular shape. Margins were circumscribed in 17 lesions and noncircumscribed in two. The mean lesion size was 0.9 cm (range, 0.3–3.0 cm) for all lesions, 0.9 cm (range, 0.3–3.0 cm) for masses, 0.8 cm (0.3–1.5 cm) for calcifications, 0.4 cm (0.3 and 0.6 cm) for masses with calcifications, and 0.8 cm (0.6–1.0 cm) for asymmetric densities. The intracystic echogenic lesion was 0.4 cm in diameter. Thirty-nine lesions were characterized as BI-RADS category 4 (suspicious) and four as BI-RADS category 5 (highly suggestive of malignancy).

Papillary Lesions Classified as Benign at Surgical Excision or Imaging Follow-up
Twenty-six of the 36 lesions (72%) diagnosed as benign at core-needle biopsy were benign at surgical excision: 14 were papillomas, and two were papillomatoses. In 10 cases, no residual lesion was identified (Table 2).

One of the 35 patients who underwent surgical excision was originally followed up radiographically for 25 months without a change in residual calcifications. Continued mammographic follow-up for 37 months revealed an interval increase in the size of the residual calcifications at the biopsy site. At this time, the patient underwent surgical excision. Results of histologic examination revealed papillomas with focal atypia and an adjacent focus of ADH (Fig 1). At retrospective review of the images, there was a slight interval increase in the residual calcifications 6 months after stereotactic biopsy that was not detected initially.

View larger version (141K): [in this window] [in a new window] [Download PPT slide]   Figure 1a: Atypical papilloma with adjacent ADH. (a) Mediolateral oblique view of right breast in 50-year-old woman shows 1-cm cluster of heterogeneous microcalcifications. Histologic examination of specimens from core-needle biopsy (not shown) revealed intraductal papilloma with branching fronds. No atypia was identified. (b) Mediolateral oblique view of right breast of same woman obtained 37 months after core-needle biopsy shows interval increase in microcalcifications at biopsy site. Histologic examination of specimens from excisional biopsy (not shown) revealed atypical intraductal papilloma with solid areas of epithelial cells and adjacent ducts that displayed ADH.

View larger version (140K): [in this window] [in a new window] [Download PPT slide]   Figure 1b: Atypical papilloma with adjacent ADH. (a) Mediolateral oblique view of right breast in 50-year-old woman shows 1-cm cluster of heterogeneous microcalcifications. Histologic examination of specimens from core-needle biopsy (not shown) revealed intraductal papilloma with branching fronds. No atypia was identified. (b) Mediolateral oblique view of right breast of same woman obtained 37 months after core-needle biopsy shows interval increase in microcalcifications at biopsy site. Histologic examination of specimens from excisional biopsy (not shown) revealed atypical intraductal papilloma with solid areas of epithelial cells and adjacent ducts that displayed ADH.

View larger version (127K): [in this window] [in a new window] [Download PPT slide]   Figure 2a: Atypical papilloma with adjacent DCIS. (a) Magnification view of mammogram of right breast in 54-year-old woman demonstrates cluster of pleomorphic microcalcifications arranged in linear distribution. Histologic examination of specimens from core-needle biopsy (not shown) revealed intraductal papilloma partially with sclerotic fronds lined with two cell layers. (b) Photomicrograph of excisional biopsy specimen demonstrates papillary neoplasm with two cell layers and atypical micropapillary tufts (thick arrow) and an adjacent duct that contains DCIS (thin arrow). (Hematoxylin-eosin stain; original magnification, x40.)

View larger version (162K): [in this window] [in a new window] [Download PPT slide]   Figure 2b: Atypical papilloma with adjacent DCIS. (a) Magnification view of mammogram of right breast in 54-year-old woman demonstrates cluster of pleomorphic microcalcifications arranged in linear distribution. Histologic examination of specimens from core-needle biopsy (not shown) revealed intraductal papilloma partially with sclerotic fronds lined with two cell layers. (b) Photomicrograph of excisional biopsy specimen demonstrates papillary neoplasm with two cell layers and atypical micropapillary tufts (thick arrow) and an adjacent duct that contains DCIS (thin arrow). (Hematoxylin-eosin stain; original magnification, x40.)

View larger version (122K): [in this window] [in a new window] [Download PPT slide]   Figure 3a: Papillary DCIS. (a) Magnification view of mammogram of right breast in 75-year-old woman demonstrates cluster of heterogeneous microcalcifications. (b) Photomicrograph of core-needle biopsy specimen shows intraductal papilloma with fibrovascular cores and mild ductal epithelial hyperplasia. (Hematoxylin-eosin stain; original magnification, x400.) (c) Photomicrograph of excisional biopsy specimen shows atypical epithelial proliferation in micropapillary arrangements (arrow), which is consistent with intraductal papillary carcinoma. (Hematoxylin-eosin stain; original magnification, x400.)

View larger version (139K): [in this window] [in a new window] [Download PPT slide]   Figure 3b: Papillary DCIS. (a) Magnification view of mammogram of right breast in 75-year-old woman demonstrates cluster of heterogeneous microcalcifications. (b) Photomicrograph of core-needle biopsy specimen shows intraductal papilloma with fibrovascular cores and mild ductal epithelial hyperplasia. (Hematoxylin-eosin stain; original magnification, x400.) (c) Photomicrograph of excisional biopsy specimen shows atypical epithelial proliferation in micropapillary arrangements (arrow), which is consistent with intraductal papillary carcinoma. (Hematoxylin-eosin stain; original magnification, x400.)

View larger version (157K): [in this window] [in a new window] [Download PPT slide]   Figure 3c: Papillary DCIS. (a) Magnification view of mammogram of right breast in 75-year-old woman demonstrates cluster of heterogeneous microcalcifications. (b) Photomicrograph of core-needle biopsy specimen shows intraductal papilloma with fibrovascular cores and mild ductal epithelial hyperplasia. (Hematoxylin-eosin stain; original magnification, x400.) (c) Photomicrograph of excisional biopsy specimen shows atypical epithelial proliferation in micropapillary arrangements (arrow), which is consistent with intraductal papillary carcinoma. (Hematoxylin-eosin stain; original magnification, x400.)

Negative Predictive Value
The negative predictive value of core-needle biopsy for excluding malignancy (ie, DCIS) among benign papillary lesions of the breast was 94% (34 of 36 lesions). The exact two-sided 95% CI for the negative predictive value for malignancy was 81.4%–99.0%.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
With the widespread use of core-needle biopsy in the initial diagnosis of mammographic lesions, papillary lesions of the breast are occasionally encountered. These lesions include a wide spectrum of entities that range from benign papillomas to invasive papillary adenocarcinomas (1,14). Among the published studies (Table 5), there continues to be a lack of agreement about the management of benign papillomas diagnosed with core-needle biopsy, with some lesions followed up with imaging and others surgically excised (3–12).

Foci of DCIS or ADH can be seen in benign papillary lesions and are more common in patients with multiple peripheral papillomas than in those with solitary central papillomas (16,17). The relative and/or absolute risk for the development of invasive breast carcinoma in patients with a history of ADH or DCIS at breast biopsy has been well documented (18,19). The risk of these lesions within a papillary lesion, however, has not been fully established (17). Results of one study (19) showed that the presence of atypia in a papilloma is associated with a significantly increased risk of the development of breast cancer—7.5 times higher than in benign papillomas. Another study (17) showed that papillomas with an atypical epithelial proliferation have an increased risk of subsequently developing invasive carcinoma when compared with papillomas in general and therefore should be surgically excised. The certainty that a papilloma determined to be benign at core-needle biopsy will not have another lesion at excision is questionable. ADH or DCIS in papillomas may be present only focally, and a sample of a papilloma obtained with core-needle biopsy may not be representative of the entire lesion.

Because one patient had two lesions in our study, the upgrade rates are expressed on a per-patient basis. A benign papillary lesion was upgraded to a papillary lesion with adjacent ADH in seven of the 42 patients (17%) and to DCIS in two (5%). Lesions were upgraded to either ADH or DCIS in nine of the 42 patients (21%). Lesions were upgraded in nine of 35 patients with surgically excised lesions (26%).

Of the nine patients with 10 lesions that were underdiagnosed at core-needle biopsy, five patients presented with masses (one patient had two masses); three patients, with calcification; and one patient, with a mass with calcification. The masses were sampled at core-needle biopsy with either stereotactic or US guidance. It is difficult to be certain of complete sampling with removal of the lesion when dealing with mass lesions, because residual tissue can be obscured by overlapping densities caused by lidocaine infiltration or bleeding when using stereotactic guidance or by air artifact when using US guidance. The three calcification cases were all sampled with an 11-gauge stereotactic vacuum device, and the one case of a mass with calcifications was sampled with stereotactic guidance and an automated gun with a 14-gauge core needle. In these cases, calcifications were identified in only one or two of the core specimens obtained; these results indicate that the lesion may have been undersampled.

The results of our study revealed a considerable upgrade rate for benign papillary lesions of the breast to either ADH or DCIS at core-needle biopsy. This may be secondary to undersampling of the lesion proper or the surrounding tissue, which may contain foci of ADH, as some studies have suggested (19). Page et al (19) showed that in papillomas with foci of ADH, the area of ADH comprises less than 25% of the entire papilloma and at excision the surrounding breast tissue shows ADH in 63% of cases, concluding that samples of papillomas obtained with core-needle biopsy may not be representative of the entire lesion.

In our study, both cases that ultimately had carcinoma at excision would have been removed owing to the discordance of the radiologic and histologic findings; one lesion was a cluster of calcifications classified as BI-RADS category 5 (13), and the other was a new area of calcifications in an elderly woman. However, cases with ADH would have been missed. This is important because data have suggested that papillomas with atypia appear to represent true precursor lesions (15,19). Moreover, identification of patients with ADH is important because in many institutions, these patients may be candidates for risk reduction management strategies and offered chemoprevention. Although the rate of upgrade to DCIS in our study was low (5%; 95% CI: 0.8%, 15.7%), it was still greater than the reported 2% or lower probability of malignancy in BI-RADS category 3 probably benign lesions (13), for which conservative management with close imaging follow-up is recommended. Even though the low end of the 95% CI (0.8%) is less than the reported 2% probability of malignancy for which lesions would be sampled at surgical biopsy, excision is recommended in patients in whom benign papillary lesions are diagnosed at core-needle biopsy because the histologic findings from surgical excision may alter the treatment of some patients.

This study was limited because symptomatic patients with nipple discharge or palpable masses were not included. Therefore, the risk of an upgraded diagnosis may have been underestimated. A second limitation of the study was the small sample size owing to the rarity of papillary lesions of the breast.

Given the considerable rate of upgrade to either ADH or DCIS (26%) found for all patients with excised benign papillary lesions in our study, we recommend excision of all benign papillary lesions of the breast diagnosed with core-needle biopsy. Additional long-term studies are needed to assess whether radiologic follow-up can be an acceptable alternative to excision. At this time, however, we conclude that benign papillary lesions of the breast are best managed with surgical excision.

	ACKNOWLEDGMENTS

 
The authors thank James S. Babb, PhD, for his invaluable assistance with statistical analysis.

	FOOTNOTES

 

Abbreviations: ADH = atypical ductal hyperplasia • BI-RADS = Breast Imaging Reporting and Data System • CI = confidence interval • DCIS = ductal carcinoma in situ

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, C.L.M.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, C.L.M., J.C.; clinical studies, C.L.M., D.H., J.C.; and manuscript editing, C.L.M.

	References

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2382041839v1 238/3/801    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Mercado, C. L. Articles by Cangiarella, J. Search for Related Content PubMed PubMed Citation Articles by Mercado, C. L. Articles by Cangiarella, J.