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Is Surgical Excision Warranted After Benign, Concordant Diagnosis of Papilloma at Percutaneous Breast Biopsy?

¹ Director of Breast Imaging Research Programs, Breast Imaging Section, Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
² Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY 10021.

Received January 29, 2005; accepted after revision March 2, 2005.

 
This work was supported by a grant from the Breast Cancer Research Foundation.

Address correspondence to L. Liberman (libermal{at}mskcc.org).

Abstract

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OBJECTIVE. The study objective was to determine the cancer frequency in lesions yielding a benign, concordant diagnosis of papilloma at percutaneous breast biopsy.

MATERIALS AND METHODS. Retrospective review was performed of 3,864 lesions that had percutaneous imaging-guided biopsy. In 50 lesions (1.3%), percutaneous biopsy yielded a benign, concordant diagnosis of papilloma. Surgical pathology (n = 25) or minimum 2 years' mammographic follow-up (n = 10) was available for 35 lesions that had biopsy with 11-gauge vacuum-assisted (n = 20) or 14-gauge automated (n = 15) needles. Medical records, imaging studies, and histologic results were reviewed.

RESULTS. Cancer was found in five (14%) of the 35 lesions yielding a benign, concordant diagnosis of papilloma at percutaneous biopsy. Cancer histology was ductal carcinoma in situ in four (80%) and node-negative invasive cancer in one. Four (80%) of five cancers were identified due to interval change at follow-up (median, 22 months; range, 7-25 months). In six (17%) of 35 lesions, surgery revealed high-risk lesions including atypical ductal hyperplasia (n = 3), radial scar (n = 2), and lobular carcinoma in situ (n = 1). There was a significantly (p = 0.02) higher frequency of cancer or high-risk lesion in women with multiple versus solitary papillomas and a trend (p = 0.09) toward a higher cancer rate in women with versus without a family history of breast cancer. Breast cancer history, menopausal status, mammographic pattern, biopsy method, and removal of imaging target had no significant impact on cancer rate.

CONCLUSION. In our study of percutaneously diagnosed papillomas, surgery revealed cancer in 14% and high-risk lesions in 17%. Lesions yielding a benign, concordant diagnosis of papilloma at percutaneous biopsy may warrant surgical excision.

Keywords: breast • breast cancer • biopsy • mammography • papilloma • sonography • women's imaging

Introduction

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An intraductal papilloma is a discrete, benign papillary tumor [1]. Most papillomas (75%) are located in the central part of the breast. Papillomas may be solitary, arising in one duct, or multiple, often arising in contiguous areas of a duct system. Solitary papillomas, most common in patients in the sixth decade, are usually central in location. Although they often present with symptoms such as nipple discharge or palpable subareolar mass, solitary papillomas may be mammographically detected, clinically silent lesions. Multiple papillomas, most often found in women in their 40s and 50s, are usually peripheral, asymptomatic lesions identified on mammography [2]. Most reports indicate a higher risk of subsequent breast cancer in women with multiple rather than solitary papillomas [1, 3].

The management of intraductal papillomas has long been controversial. In the early 20th century, some physicians treated intraductal papillomas with mastectomy [1]. In 1922, Dickinson [4] wrote the following: In the same year, Bloodgood [5] recommended surgical excision, rather than mastectomy, for papillomas. In a meta-analysis of published studies in the latter half of the 20th century, Rosen [1] reported that breast cancer occurred after excision of papilloma in 23 (4%) of 529 cases; of the 23 cancers, 12 occurred in the ipsilateral breast and 11 in the contralateral breast. These studies are limited by treatment with mastectomy in some women, unreliable distinction of benign papilloma from papillary carcinoma, and failure to separate solitary from multiple papillomas. Also, because the papillomas in these investigations were excised, these studies do not address the issue of the premalignant potential of papillomas that remain in the breast [1].

Every surgeon hesitates to mutilate a woman, and particularly this organ, but every surgeon with a conscience will attack that which is or may become cancer. Benign means "born good" but all tumors of the breast which have this title are apt to go bad and are not to be trusted.... Some surgeons resect in part; some do a complete plastic subcutaneous resection, and others a radical removal. Can we today say who does wisely?

In the 21st century, papillomas that are surgically excised require no further treatment. Controversy persists, however, regarding the need for excision of papillomas diagnosed at percutaneous breast biopsy. Theoretic reasons to excise percutaneously diagnosed papillomas include difficulties in pathologic interpretation (particularly in the distinction of benign papillomas from papillary carcinomas), possible sampling error in a papilloma that may contain areas of atypia or carcinoma, and the premalignant potential of these lesions [6]. Although some pathologists have recommended surgical excision for percutaneously diagnosed papillomas [6, 7], published data [8-22] have been limited by small numbers of cases; short follow-up; or inconsistent distinction of lesions yielding a benign, concordant diagnosis of papilloma from other papillary lesions, such as those referred for excision based on worrisome pathologic features, associated high-risk lesions, or imaging-histologic discordance. We undertook this study to determine the frequency of cancer in lesions yielding a benign, concordant diagnosis of papilloma at percutaneous breast biopsy.

Materials and Methods

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Patients and Lesions
Retrospective review was performed of 3,864 lesions that had percutaneous imaging-guided biopsy under stereotactic (n = 2,078) or sonographic (n = 1,786) guidance during a 7-year period from July 1, 1997 to July 1, 2004. Biopsies were performed by one of 11 attending radiologists specializing in breast imaging. For each lesion, the attending radiologist correlated the imaging findings with percutaneous biopsy histology to assess whether histology was concordant (i.e., provided a sufficient explanation for imaging findings) [23]; the results of this assessment were included in the radiology report. In 50 (1.3%) of 3,864 lesions, percutaneous biopsy yielded a benign, concordant diagnosis of papilloma. Subsequent surgical pathology (n = 25) or a minimum of 2 years of mammographic follow-up data (n = 10) were available in 35 lesions; these 35 lesions constitute the basis of this study.

The 35 lesions occurred in 32 women of a median age of 57 years (range, 44-81 years). Twenty-five women (78%) were postmenopausal and seven (22%) were premenopausal. Twenty-five (71%) of the 35 lesions were solitary papillomas and 10 lesions (29%) were diagnosed in women with previous or concurrent multiple papillomas. The median size of these 35 lesions was 0.8 cm (range, 0.3-1.5 cm). Mammographic findings were mass in 18 (51%), calcifications in 14 (40%), and both in three (9%); all lesions had been categorized before biopsy as BI-RADS category 4 (suspicious) [24]. One lesion presented with nipple discharge and a mammographic mass, and the other 34 lesions were asymptomatic lesions identified at screening mammography.

Biopsy Method
In 20 (57%) of the 35 lesions (including 17 calcific lesions, two masses that were not seen on sonography, and one mass seen on mammography and sonography in a patient with nipple discharge), biopsy was performed under stereotactic guidance (StereoGuide with Digital Spot Mammography, Lo-Rad) with an 11-gauge vacuum-assisted biopsy probe (Mammotome, Biopsys/Ethicon Endo-Surgery) using a localizing clip (MicroMark, Biopsys/Ethicon Endo-Surgery) after biopsy at the discretion of the radiologist performing the procedure. The median number of specimens obtained at stereotactic biopsy was 14 (range, 8-35). A two-view mammogram was obtained after all stereotactic biopsies.

In 15 (43%) of the 35 lesions (masses that could be identified on sonography), biopsy was performed under sonographic guidance (128XP, Acuson; or Ultramark 4 Plus, Advanced Technology Laboratories) with a 14-gauge automated needle (Manan, Manan Medical Products; Biopty-Cut, Bard Urological; or Ultra-Core, Medical Device Technologies). The median number of specimens obtained at sonographically guided biopsy was four (range, 1-6), with three or more specimens obtained in 14 (93%) of 15 cases; one lesion disappeared after a single core had been obtained, and no additional specimens were obtained. No clips were placed after sonographically guided biopsies.

The radiologist who performed the biopsy assessed whether the imaging target was completely removed or was sampled. This assessment was made and recorded after biopsy had been performed for sonographically guided biopsies and after the postbiopsy two-view mammogram was obtained for stereotactic biopsies. Complete excision of the imaging target occurred in 17 (49%) of the 35 lesions, including 16 (80%) of the 20 stereotactic biopsies versus one (7%) of the 15 sonographically guided biopsies (p < 0.0001). The imaging target was completely removed in 13 (76%) of 17 calcific lesions versus four (22%) of 18 uncalcified masses (p < 0.01).

Follow-Up
Among 25 lesions with surgical follow-up, surgery was performed promptly (median, 5 weeks; range, 1-15 weeks) in 20, due to the preference of the patient or referring clinician. The imaging features were concordant with the diagnosis of benign papilloma that had been obtained at histologic analysis of the needle biopsy specimens. Surgical excision was performed later (median, 25 months; range, 7-38 months) in the remaining five lesions because of interval growth at mammography in three, new palpable and mammographic mass at the biopsy site in one, and new bloody nipple discharge in one. Among the 10 lesions with a minimum of 2 years of mammographic follow-up, the median follow-up was 39 months (range, 25-57 months).

Pathologic Evaluation
All core biopsy specimens were processed entirely. From each paraffin block, sections were obtained at three different levels. All sections were stained with H and E. The diagnosis of papilloma was rendered when the lesion had a "papillary arborescent growth pattern supported by a fibrovascular stalk" [25]. Intraductal epithelial proliferations not supported by a fibrovascular stalk, such as papillomatosis and intraductal hyperplasia, were excluded. Myoepithelial cells, usually uniformly distributed in benign papillomas and largely over-grown in papillary cancers, were useful in distinguishing benign from malignant papillary lesions [1]. In surgical specimens, the features recorded included histologic findings; the presence of residual papilloma; and the relationship of any carcinoma, if present, to residual papilloma, if present.

Data Collection and Analysis
Medical records, pathology findings, and imaging studies obtained before, during, and after biopsy were reviewed. Data were entered into a computerized spreadsheet (Excel, Microsoft). Statistical analysis was performed using statistical software (Epi-Info, Centers for Disease Control and Prevention). A p value of less than 0.05 was considered statistically significant. The 95% confidence intervals (CI) were calculated using the Geigy Scientific Tables [26]. Permission to conduct this study was obtained from our institutional review board.

Results

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Outcomes in 35 lesions yielding a benign, concordant diagnosis of papilloma at percutaneous biopsy that had either surgical pathology (n = 25) or a minimum of 2 years of mammographic follow-up (n = 10) are shown in Table 1. Four (80%) of the five cancers were ductal carcinoma in situ (DCIS) and one was a node-negative 1.8-cm invasive ductal cancer and DCIS (Table 2). One of the five cancers was diagnosed promptly, 3 weeks after percutaneous biopsy, in surgical excision performed due to physician and patient preference. Four (80%) of the five cancers were diagnosed subsequently at a median of 22 months (range, 7-25 months) after biopsy, due to interval growth at mammography (n = 2), new bloody nipple discharge (n = 1), and new palpable and mammographic mass at the biopsy site (n = 1).

Surgery revealed high-risk histology results in six (17%) of 35 percutaneously diagnosed papillomas, including atypical ductal hyperplasia (ADH) in three, radial scar in two, and lobular carcinoma in situ (LCIS) in one. Percutaneously diagnosed papillomas were significantly (p = 0.02) more likely to have either cancer or a high-risk lesion at surgery in women with multiple rather than solitary papillomas (Table 3). There was a trend (p =0.09) toward a higher frequency of cancer in lesions that occurred in women with versus without a family history of breast cancer (Table 4). The frequency of cancer did not differ significantly as a function of history of previous breast cancer, tissue acquisition device or guidance technique, presence of a mammographic mass, or menopausal status (Table 4).

Complete percutaneous removal of the imaging target occurred in 17 (49%) of the 35 percutaneously diagnosed papillomas in this study and in 10 (40%) of the 25 surgically excised lesions. Complete percutaneous histologic excision of the papilloma occurred in four (16%) of the 25 surgically excised lesions, including three (30%) of 10 lesions in which the imaging target was percutaneously removed versus one (7%) of 15 lesions in which the imaging target was not percutaneously removed (p =0.3). The frequency of cancer did not differ significantly as a function of complete removal of the imaging target or complete histologic excision of the papilloma (Table 4).

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
A benign, concordant diagnosis of papilloma was obtained in 1.3% of percutaneous breast biopsies performed at our institution during a 7-year period. Cancer was found at surgical excision in 14% of lesions yielding a benign, concordant diagnosis of papilloma at percutaneous biopsy; among these cancers, most (80%) were DCIS. The frequency of cancer is higher than the < 2% frequency of cancer in lesions interpreted as probably benign (BI-RADS category 3) [24] and referred for 6-month follow-up imaging [27, 28]. The 14% frequency of cancer is slightly lower than the 20-40% frequency of cancer reported for lesions interpreted as suspicious (BI-RADS category 4) [24] and referred for biopsy [29-32].

Our findings should be interpreted in the context of the literature (Table 5). In prior reports, a benign, concordant diagnosis of papilloma was obtained in 0.5-4% of percutaneous breast biopsies. Among 325 lesions yielding a benign, concordant diagnosis of papilloma at percutaneous core or vacuum-assisted biopsy with subsequent surgical (n = 184) or imaging (n = 141) follow-up in the literature, cancer was found in 11 (3%; range, 0-17%). The 14% cancer rate among percutaneously diagnosed papillomas in our study is at the high end of the range previously reported. The high cancer rate in our study may reflect a variety of factors such as the relatively large number of patients; long median duration of imaging follow-up; and specific features of our patient population, including risk factors (such as family history of breast cancer) and specific histology results (such as multiple papillomas).

Among 35 percutaneously diagnosed papillomas in our study, surgery revealed high-risk lesions (ADH, LCIS, or radial scar) in six (17%). In prior studies of lesions, surgery revealed ADH in up to 15-19% of percutaneously diagnosed benign papillomas [11, 15, 22]. ADH may be heterogeneously distributed within or adjacent to a papilloma; hence, it is possible to perform percutaneous biopsy of a papilloma without sampling the ADH [6]. Finding a high-risk lesion such as ADH or LCIS at surgery may alter patient management, leading to more intensive surveillance and consideration of risk-reducing measures, such as tamoxifen therapy [33]. One can also hypothesize that if ADH in or around a papilloma is premalignant, removing the papilloma may decrease the likelihood of subsequent breast cancer. This hypothesis suggests that even if prompt surgical excision of percutaneously diagnosed papillomas has a low cancer yield, failure to excise the papilloma may enable evolution of premalignant change to cancer. That 80% of our cancers were identified due to interval change at follow-up and that 80% of those cancers were DCIS supports but does not prove this hypothesis.

In almost one third (31%) of lesions yielding a benign, concordant diagnosis of papilloma at percutaneous biopsy, surgery revealed either cancer or a high-risk lesion. The likelihood of finding either cancer or a high-risk lesion at surgery was significantly (p = 0.02) higher in women with multiple as compared with solitary papillomas. This finding is consistent with prior reports that women with multiple rather than solitary papillomas have a higher frequency of subsequent breast cancer [1, 3]. It is also consistent with data from Ohuchi et al. [34]. In their 3D reconstruction study of surgically excised papillomas, Ohuchi et al. found cancer in six (24%), of which five were DCIS and one was a 0.8-cm invasive ductal carcinoma and DCIS; of the six cancers found, five (33%) of 15 were cases of multiple papillomas versus one (10%) of 10 cases of solitary papillomas [34]. Although both solitary and multiple papillomas have been described as markers of increased breast cancer risk [35], we found that multiple papillomas were more likely than solitary papillomas to be associated with ADH or early malignant change.

Some researchers have suggested that wider sampling of certain high-risk lesions (such as radial scars) with an 11-gauge vacuum-assisted biopsy probe rather than a 14-gauge automated needle may provide more accurate diagnosis, perhaps sparing the need for surgical excision in selected cases [36]. Vacuum-assisted 11-gauge biopsy may cure nipple discharge in women with symptomatic papillomas [37], but the utility of 11-gauge vacuum-assisted biopsy in sparing surgical excision of papillomas remains unproven. We found no statistically significant difference in the likelihood of cancer as a function of percutaneous biopsy method. Most lesions had residual papilloma at surgery, regardless of whether the imaging target was excised (Figs. 1A, 1B, 1C, 1D, 1E, and 1F). The cancer rate did not differ significantly as a function of complete percutaneous removal of the imaging target or complete histologic excision of the papilloma. Like Jackman et al. [38] in their study of lesions in which percutaneous biopsy yielded ADH, we found no reliable predictors of benignity in lesions yielding a benign, concordant diagnosis of papilloma at percutaneous biopsy.

View larger version (131K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A —56-year-old woman with left breast bloody nipple discharge. Mediolateral oblique mammogram of left breast shows 0.8-cm lobulated, predominantly circumscribed mass in left breast, upper outer quadrant.

View larger version (120K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B —56-year-old woman with left breast bloody nipple discharge. Mediolateral oblique mammogram obtained during left breast ductography shows opacification of retroareolar duct leading to mass and filling defect in mass.

View larger version (118K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C —56-year-old woman with left breast bloody nipple discharge. Mediolateral oblique left mammogram obtained after stereotactic 11-gauge vacuum-assisted biopsy shows complete removal of imaging target. Air and localizing clip are present at biopsy site.

View larger version (155K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D —56-year-old woman with left breast bloody nipple discharge. Histologic analysis of stereotactic biopsy material shows benign papilloma. (H and E)

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1E —56-year-old woman with left breast bloody nipple discharge. Mediolateral oblique left mammogram obtained 22 months after biopsy shows interval development of new mammographic mass at biopsy site, corresponding to palpable lump denoted by radiopaque skin marker.

View larger version (179K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1F —56-year-old woman with left breast bloody nipple discharge. Histology slide from surgical excision shows benign papilloma centrally and infiltrating ductal carcinoma at periphery. Review of all slides from surgical excision yielded revealed infiltrating ductal carcinoma, poorly differentiated, measuring 1.8 cm, and ductal carcinoma in situ, admixed with papilloma. Patient had lumpectomy and sentinel node biopsy, with negative sentinel lymph nodes. (H and E)

Acknowledgments
 
We thank David C. Perlman for his invaluable assistance.

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