ORIGINAL ARTICLE

Benign Papillomas Diagnosed on Large-gaugeVacuum-Assisted Core Needle Biopsy which Span<1.5 cm Do Not Need Surgical Excision

Andrew D. Mosier, DO,* Joren Keylock, MD,† and Donald V. Smith, MD‡

*Cleveland Clinic Foundation Imaging Institute, Cleveland, Ohio; †Department of Pathology,St. Claire Hospital, Lakewood, Washington; ‡Department of Radiology, Madigan Army MedicalCenter, Tacoma, Washington

n Abstract: The objective of our study is to determine if a carefully selected subset of benign breast papillomas (size≤1.5 cm) can be safely followed by imaging surveillance instead of immediate surgical excision. Over a 6½-year period, 86breast lesions were diagnosed as a benign papilloma (BP) utilizing an 11- or 8-gauge vacuum-assisted core needle biopsy(VACNB) device. In general, it was our intent to remove as much of the radiologically evident lesion as possible. These 86lesions underwent ≥2 years of imaging surveillance, without surgical excision following initial detection. With ≥2 years ofradiologic follow-up, none of the 86 BPs demonstrated imaging findings that necessitated repeat biopsy or surgical excision.Benign breast papillomas ≤1.5 cm that are biopsied using an 11- or 8-gauge VACNB device with intent to remove as muchof the radiologically evident lesion as possible are safe to undergo serial imaging surveillance rather than immediate surgi-cal excision. n

Key Words: benign papilloma, intraductal papilloma, papilloma excision

A papillary lesion of the breast is a general descrip-

tor for a continuum of benign to malignant

lesions, which include benign papillomas (BP), papillo-

matosis and sclerosing papillomas, atypical papillo-

mas, micropapillary ductal carcinoma in situ (DCIS),

and papillary breast carcinoma or invasive ductal car-

cinoma (IDC) (1,2). Papillary breast carcinoma itself

accounts for only about 2% of all breast cancers (3).

Despite this distinct terminological continuum of pap-

illary lesions, it can be difficult to differentiate border-

line lesions (i.e., atypical papilloma versus papillary

carcinoma) on the basis of histopathologic features. In

the past, this challenge has made certain difficult cases

arbitrarily subjective for the interpreting pathologist

(2,4).

The difficulties in management and disposition of

papillary breast lesions begin with the physician who

performs the biopsy. Sampling error leading to a false-

negative result is often cited as the foremost reason to

excise all papillary lesions diagnosed by fine-needle

aspiration (FNA) and smaller gauge core needle

biopsy (CNB). These sampling methods may miss

areas of atypia or small malignant foci (3,5–9). Patho-logic distinction may remain difficult even with biopsy

of the entire lesion, particularly when the lesion is not

reviewed by a pathologist subspecialized in breast dis-

orders (1,2,10).

More recently, studies have suggested that surgical

excision may not be necessary for accurate diagnosis

of benign papillary lesions sampled by larger (11- or

8-gauge) VACNB devices and confirmed as benign by

surgical excision (3,11), 2-year imaging follow-up, or

a combination of both (12,13).

In our study, the reliability of imaging surveillance

for BPs ≤1.5 cm initially sampled with an 11- or

8-gauge VACNB device was retrospectively assessed

over a 6½-year period at our institution. BPs greater

than 1.4 cm tend to be malignant more often than those

which were smaller (1); and no papillary lesion we

assessed (whether by mammography, ultrasound, or

Address correspondence and reprint requests to: Andrew D. Mosier,

The Cleveland Clinic Foundation Imaging Institute, 9500 Euclid Ave/A-10,

Cleveland, OH 44195, USA, or e-mails: mosier51@hotmail.com; andrew.d.

mosier4.mil@mail.mil

Disclaimer: The views expressed are those of the author(s) and do not

reflect the official policy of the Department of the Army, the Department of

Defense or the U.S. Government.

DOI: 10.1111/tbj.12180

© 2013 Wiley Periodicals, Inc., 1075-122X/13The Breast Journal, Volume 19 Number 6, 2013 611–617

final pathology) was >1.5 cm. In general, it is our prac-

tice to remove as much of the radiologically evident

lesion as possible (whether calcifications and/or a mass

with stereotactic technique, or a mass with ultrasound-

guided biopsy technique). Of note, a predecessor study

at our institution by Sohn et al. (14) retrospectively

assessed the upgrade rate of papillary breast lesions

sampled by 14- or 11-gauge biopsies from January

1994 to December 2005. Sohn et al. found that only

two lesions initially designated as BP (1.1%) were

upgraded (to carcinoma) following surgical excision.

MATERIALS AND METHODS

Subjects

We reviewed all BPs at our institution from January

2003 to June 2009. January 2003 was designated as

our starting point because this is when we began more

routine use of our 8-gauge VACNB biopsy device. June

2009 was designated as the end point to give ≥2 years

for possible follow-up imaging surveillance (assuming

patients would return as scheduled). This end point

was additionally chosen because 2 years is the time

interval used to more closely follow a probably benign

finding until it can be reduced from a Breast Imaging-

Reporting and Data System (BI-RADS) 3 to BI-RADS

2. During this time, 4293 CNBs were performed.

For inclusion into the study, all papillary lesions

were confirmed as a BP following initial sampling by

an 11- or 8-gauge VACNB intended to remove as

much as possible of the sonographically visible lesion

or stereotactically visible calcifications. On average,

visible lesional removal required four samples with an

8-g VACNB device, and six to seven with and 11-g

VACNB device. These BP then demonstrated benign

radiographic findings for at least 2 years on follow-up

mammograms, without change necessitating repeat

biopsy or surgical excision. In most cases, follow-up

consisted of mammograms every 6 months for

2 years, and then annually thereafter.

One hundred and fifty-two papillary lesions were

identified by an 11- or 8-gauge VACNB. Of these, 11

papillary lesions (7.1%) were associated with atypia

(PA) and 12 (7.7%) with malignancy (PM). These 23

PAs and PMs were excluded because it is standard of

care to recommend surgical removal for all PAs and

PMs. Ten BPs were surgically excised after VACNB

due to patient preference, and were therefore excluded

from the study (even though these 10 were confirmed

as BPs following surgery). Finally, one papilloma was

excluded because it was initially designated a BI-

RADS five lesion, requiring surgical excision. The

surgical specimen revealed a final diagnosis of a BP.

Fifteen BPs have not yet completed 2 years of imaging

follow-up (either due to patient noncompliance; or

because the patient has not yet completed a follow-up

mammogram at least 2 years from the excision date).

These 15 have therefore been excluded. In addition,

17 have been lost to follow-up prior to 2 years of

imaging follow-up, mostly due to patient relocation.

Thus, these 17 have also been excluded.

Eighty-six BPs (in 84 women; two women had mul-

tiple BPs) remained following the aforementioned

exclusions. The average age of the patient at the time

of biopsy was 54 years 6 months (range of 32.9–

83.1). The average length of radiographic follow-up

(from initial biopsy to the most recent examination

reconfirming a benign appearance) is 4 years

10 months (range of 2–8.83 years), with 41/86 lesions

above this average length of follow-up time.

Overall, only 45 of 86 BPs were initially radiologi-

cally evident by mammography as a mass/focal

asymmetry with (8) or without (37) suspicious micro-

calcifications. The remaining 41 BPs were incidentally

discovered in the management of suspicious microcal-

cifications (29), bloody nipple discharge (5), a palpa-

ble abnormality (5), or on the preoperative MRI of a

contralateral breast cancer (2).

Management and Follow-up

Thirty-seven BPs were initially discovered on mam-

mography as a mass or focal asymmetry without asso-

ciated calcifications. All 37 of the BPs were next

imaged with ultrasound, which redemonstrated the

mammographically evident mass in 35 of 37. These

35 BPs were biopsied with ultrasound guidance. The

other two BPs not visualized by ultrasound underwent

biopsy with stereotactic guidance.

Eight BPs were initially discovered on mammogra-

phy as a mass/focal asymmetry with associated micro-

calcfications. All eight were next imaged with

ultrasound, which redemonstrated the mass in seven

of the eight. Five of the eight underwent stereotactic

biopsy (including the one BP, which did not show an

associated mass on ultrasound). The other three BPs

were biopsied with ultrasound guidance because the

sonographic mass was more obvious than the mam-

mographic calcifications.

612 • mosier ET AL.

Twenty-nine BPs were initially discovered on mam-

mography as microcalcifications without an associated

mass or asymmetry. Because there was no associated

mass or asymmetry, and because 0 of the 29 patients

reported a palpable lesion, ultrasound was not per-

formed. All 29 underwent stereotactic 11- or 8-g

VACNB.

Five BPs were initially discovered on ultrasound as

part of the management for a clinically palpable mass.

Five other BPs were first discovered on US (2) or MRI

(3) as part of the management for bloody nipple dis-

charge. All 10 of these BPs underwent ultrasound-

guided VACNB. We generally evaluate bloody nipple

discharge with MRI and mammography—often with

additional MR-directed (or 2nd-look) ultrasound

when appropriate. The three BPs associated with

bloody nipple discharge [initially discovered on MRI]

were subsequently confirmed on a MR-directed ultra-

sound exam prior to ultrasound-guided VACNB.

Two BPs were initially discovered as small masses

on preoperative MRI in the management of a contra-

lateral breast cancer. They were subsequently con-

firmed on MR-directed ultrasound. Next, they

underwent ultrasound-guided VACNB and were con-

firmed as BPs. To date, both remain unchanged in

their mammographic appearance.

When the BPs of this study were biopsied with

ultrasound guidance (and the percentage removed was

included in the postprocedure report by the radiolo-

gist), no less than 75% and no more than 90% of

the radiographically evident lesion was reportedly

removed. Often because of location (retroareolar,

within a dilated duct) and/or clinical history (bloody

nipple discharge), we had a high degree of suspicion

before the biopsy that the mass may be a BP.

However, when the BPs of this study were biopsied

with stereotactic guidance for a cluster of suspicions

microcalcification, we often did not suspect that the

suspicious microcalcifications were possibly caused by

a BP prior to biopsy. Therefore, when stereotactic

biopsy of suspicious grouped or clustered calcifications

is performed, it is our practice to remove most (>75%)

to all of the radiographically evident calcifications.

However, we do not routinely report a percentage or

estimation of calcifications removed. Nor do we repo-

sition the stereotactic biopsy needle unless absolutely

necessary (for reasons beyond the scope of this paper)

if calcifications are adequately obtained within the

biopsy specimen on specimen mammography.

After each biopsy (ultrasound-guided or stereotac-

tic), a clip is placed, and a postprocedure mammo-

gram is obtained. We do not routinely review biopsy

margins with pathology. Instead, follow-up mammo-

grams are obtained every 6 months for 2 years, and

annually thereafter.

Mammographic images of a BP, and its typical

appearance on multiple follow-up images, have

been included below (Fig. 1). There is no growth/

development of a new mass or suspicious calcifications

at or adjacent to the clip (biopsy site) over the course

of the follow-up images. In addition, ultrasound

(Fig. 2), MRI/US (Fig. 3), and implant/implant-

displaced mammograms (Fig. 4) of BPs are presented

for review.

Figure 1. Initial (left), 6-month follow-up

(middle), and 3-year follow-up (right) cranio-

caudal views of the left breast demonstrate a

nonspecific mass (white circle) in the upper-

outer quadrant of the left breast (bracketed

by the black oil pencil). The mass on the

initial mammogram was excised and a clip

was placed. The mammographic appearance

remained benign without development of

suspicious calcifications or a mass at or

adjacent to the biopsy site.

Alternate Management of Benign Papillomas • 613

Procedure

An 8- or 11-gauge VACNB device (Mammotome;

Ethicon Endo-Surgery, Cincinnati, OH) was used for

both ultrasound-guided and stereotactic biopsies. Pref-

erence was given to the 8-gauge biopsy device with

intent to remove as much of the lesional calcifications

(stereotactic approach) or mass (ultrasound or stereo-

tactic approach) as possible. An 8-gauge needle was

also preferred when possible to retrieve a larger histo-

logic sample per core, and for more complete sam-

pling of the lesion. Exceptions to our preference for

the 8-gauge system were made in the following

instances: 1—the lesion was too close to the skin sur-

face; 2—compression was not adequate for stereotactic

technique leading to a negative stroke margin; or

3—color Doppler demonstrated abundant vascularity

or a large vessel adjacent to the lesion (to mitigate the

risk of a hematoma).

RESULTS

To date, 0 of the 86 BPs that have undergone at

least 2 years of benign mammographic follow-up have

demonstrated change on imaging that would necessi-

tate repeat biopsy or surgical excision. We did

encounter one case of interest where the patient

underwent a mastectomy for DCIS in a different

quadrant from a BP identified 4 years earlier in the

same breast. The clip of that BP was 5.0 cm from the

Figure 2. Grayscale (left) and color Doppler (right) ultrasound images of the left breast demonstrate a hypoechoic, retroareolar 8–9 mm

mass in a dilated duct with a mild amount of blood flow. The mass has the usual location and appearance of a benign papilloma (BP). This

mass underwent an 8-g vacuum-assisted core needle biopsy and was confirmed as a BP.

Figure 3. Longitudinal ultrasound (top left)

of the left breast demonstrates an isoechoic

mass (white arrowhead) attached to a slen-

der pedunculated stalk (white circle) within a

dilated duct. MR (Siemens 3.0 T, prone) T1

postcontrast with fat saturation (top right;

sagittal, 20 cc IV Magnevist, TR 4, TE 1.4,

ST 1), T1 (bottom left; axial, TR 6.7, TE

2.63, ST 1.5), STIR (bottom right; axial, TR

6040, TE 63, ST 3) demonstrates an

enhancing mass (white circle) attached to the

slender pedunculated stalk (white circles on

T1 and STIR) within a dilated duct. Following

8-g vacuum-assisted core needle biopsy, the

imaging findings were confirmed as a pedun-

culated, intraductal papilloma.

614 • mosier ET AL.

closest margin of the intermediate-grade DCIS on final

pathology, and no atypia or malignancy was identified

at or adjacent to the clip.

The average size of the 86 BPs (when reported) was

7.5 mm (n = 49; range of 3–15 mm). The average

number of cores was 6.6 (range: 2–18) for 11-gauge

biopsies, and 4.33 (range: 1–8) for 8-gauge biopsies.

Forty-four biopsies (51.2%) were performed with an

11 gauge device; 27 by US-guidance and 17 by stereo-

tactic technique. Forty-two (48.8%) biopsies were per-

formed with an 8 gauge device; 26 by US-guidance

and 16 by stereotactic technique. Fifty-six papillomas

were located in the left breast and 30 in the right

breast.

DISCUSSION

Because many papillary lesions are undetected [as a

discrete mass] on mammography, differentiation by

imaging alone has previously proven unreliable (15);

however, a newer study notes that certain sonographic

features suggest benignity. Benign papillary lesions

tend to demonstrate homogeneous echotexture, in

contrast to malignant or high-risk lesions, which often

demonstrate mixed or complex cystic echogenicity. In

addition, benign papillary lesions were more often

well-circumscribed when compared with malignant

equivalents. Finally, no benign papillary lesion demon-

strated angular margins or spiculation (3).

Multiple additional confounding variables must be

considered. It has been postulated that papillomas

may be a precursor of papillary carcinoma; or that

they may degenerate into a malignant lesion over

time (1,10,14,16). Also, a carcinoma in situ [PM]

diagnosed by CNB may be upgraded to invasive can-

cer when the entire lesion is examined (17–20).These observations, however, were based on results

from smaller gauge core biopsy without vacuum

assistance; and without [expressed] intent to remove

as much of the radiographically evident lesion as

possible. It is indeed known that CNB without vac-

uum assistance has been associated with significantly

higher false-negative rates and histologic upgrade

than biopsies performed with vacuum assistance. The

aforementioned studies are also reporting the upgrade

rate of PA and PM, which we always recommend

for surgical excision and have therefore excluded

from our study. Moreover, more recent studies sug-

gest that histologic upgrade from lesional undersam-

pling is not as prevalent with VACNB as previously

suggested (13).

A recent study by Chang et al. correlates the size of

a benign papillary lesion with its potential for histo-

logic upgrade to carcinoma. As may be expected,

malignancies tended to be larger (average of 1.4) than

benign lesions (average of 0.9 cm) (1). However, we

did not have a benign papillary lesion greater than

1.5 cm in our sample group, and the average size of

papillary lesions in our study was around 7.5 mm.

As recently as 2008, the surgical literature reported

that all papillomas require surgical excision regardless

of radiologic–pathologic correlation when utilizing a

14-gauge CNB technique (21). In that same year, a

similar conclusion was suggested by Shin et al.

Figure 4. Implant (left) nondisplaced, cranio-

caudal mammographic views of the right

breast obscure a subtle mass. The triangular

marker represents a palpable abnormality.

Implant-displaced, craniocaudal views (mid-

dle) confirm a mass at the site of the palpa-

ble abnormality. This mass was biopsied and

confirmed as a benign papilloma. Nine

months later, the patient returned for follow-

up imaging (right, CC view of the right

breast) and no residual mass is visualized at

the site of the biopsy (clip).

Alternate Management of Benign Papillomas • 615

Regardless of the somewhat inconsistent nature of rec-

ommended follow-up for benign papillary lesions, it is

the accepted standard of care to excise all papillomas

with any degree of atypia or malignancy (14,22,23).

Chang et al. affirmed that surgical excision is required

for accurate diagnosis of papillary lesions sampled by

CNB (1); however, a more recent paper by the same

author suggests that surgical excision may not be nec-

essary when these lesions are sampled by an 11-gauge

US-guided VACNB device (11). A recent article by

Kim et al. also challenges the recommendation for

surgical excision, as this study demonstrated a 0%

upgrade rate to carcinoma in 54 BPs initially biopsied

by an 11- or 8-gauge VACNB technique. Kim et al.

has also followed a large number of initially BPs that

were not immediately excised and remained radio-

graphically benign without changes necessitating surgi-

cal excision (13).

Some studies have reported that BPs demonstrating

radiologic–pathologic concordance can be safely

observed with mammographic follow-up (22,24,25).

In 2008, Kim et al. reported that surgical excision is

not necessary for accurate diagnosis in a series of 39

papillary lesions removed by 11- or 8-gauge

US-guided vacuum-assisted technique (12).

What is becoming clear is that sampling error is

significantly reduced with increased core needle gauge

size (11–13), vacuum assistance (3), and intent to per-

cutaneously remove most or all of the visualized lesion

(12). Furthermore, the use of an 8-gauge VACNB to

achieve lesion removal appears to circumvent the need

for subsequent excision (12), particularly when the

lesion demonstrates benign findings on follow-up for

≥2 years (22) (Table 1).

A few limitations of our study merit consideration.

The sample size was affected by 17 patients who were

lost to follow-up (usually due to patient relocation). A

second limitation is lack of definitive radiologic–path-ologic correlation, as none of the 86 BPs included in

the study has undergone surgical excision for histo-

logic confirmation. Indeed, BPs subjected to surgical

excision could have represented a control group for

the study, allowing for true statistical analysis of BPs

diagnosed by VACNB at our institution. However,

because 24 months of serial imaging is required to

reassign a BI-RADS 3 (probably benign) lesion to

BI-RADS 2 (benign), it is unlikely that a surgically

excised control group would change the management

or categorization of these lesions as the average fol-

low-up time of the BPs we reviewed is 58 months.

Finally, even though the 86 BPs in this study are the

largest current [reported] group of BPs followed exclu-

sively by imaging, an even greater number of BPs

would have allowed for greater levels of assurance.

Our data suggest that at 2 years post biopsy, there

is no difference in the outcome of BPs initially biop-

sied by a large-gauge VACNB and closely followed by

imaging surveillance, versus those which are immedi-

ately surgically excised. Therefore, BPs less than

1.5 cm, biopsied by 11- or 8-g CNB, using vacuum

assistance, with intent to remove as much of the

radiographically-evident lesion as possible, do not

require immediate surgical excision if instead followed

by short-interval imaging surveillance. The radio-

graphic follow-up of BPs should, therefore, be a focus

of future interest as the cost, risk, and morbidity of

surgical excision can potentially be avoided.

LEARNING POINTS

1 All papillary lesions with atypia and malignancy

should undergo surgical excision.

Table 1. Summary of Recent Studies on Management of Papillary Breast Lesions

Study

Number of papillary lesions

upgraded after surgical excision Conclusion

Kim et al. (13) 14 g – 12 of 157 (7.6%)

11 and 8 g – 0 of 54 (0%)

Surgical excision may not be mandatory for benign papillary lesions removed by US-guided

VACNB

Chang et al. (1) 14 g – 8 of 54 (14.8%)

11 g – 0 of 10

Surgical excision is required for accurate diagnosis of benign papillomas removed by CNB

Chang et al. (11) 11 and 8 g – 3 of 49 to

atypical (6.1%), 0 to malignancy

Surgical excision may not be required for benign papillomas removed by 11-gauge

US-guided VACNB

Shin et al. (3) 11 and 8 g – 2 of 15 (13.3%)

to atypical, and 2 to malignancy

Surgical excision should be performed for accurate diagnosis of papillary lesions

Kim et al. (12) 11 g – 0 of 29 (0%)

8 g – 0 of 10 (0%)

Surgical excision may not be required for benign papillary lesions excised by US-guided

directional vacuum-assisted removal

Sydnor (22) 14 and 11 g – 1 of 38 (2.6%) Mammographic follow-up is reasonable for a benign papilloma diagnosed at core biopsy

based on an infrequent (3%) association of this lesion with cancer

616 • mosier ET AL.

2 Papillary lesions eligible for mammographic fol-

low-up (instead of surgical excision) include those

which meet all of the following criteria:

• a papillary lesion less than 1.5 cm on initial

radiographic imaging (measured if visualized as

a mass on mammogram or ultrasound);

• biopsied by a large-gauge (11 or 8 g), vacuum-

assisted, core needle biopsy device; and

• confirmed as a BP by pathology.

3 Typically, follow-up should include a mammogram

every 6 months for the first 2 years, and annually

thereafter.

4 Any concerning mammographic change (increasing

calcifications or new/recurrent mass at the site of the

biopsy clip) should prompt a full re-assessment and

discussion of surgical excision even if a repeat biopsy

is benign.

5 When following over 86 BPs with the criteria from

learning points 1–3, 0 of the 86 BPs have demon-

strated any change necessitating repeat biopsy or sur-

gical excision with an average of 58 months of benign

imaging follow-up.

CONFLICTS OF INTEREST

None.

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Alternate Management of Benign Papillomas • 617