Wo m e n s I m a g i n g O r i g i n a l R e s e a r c h

Chang et al.
Management of Benign Breast Papillomas

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Womens Imaging
Original Research

W O M E N S
IMAGING

Jung Min Chang1

Woo Kyung Moon1
Nariya Cho1
Wonshik Han2
Dong-Young Noh2
In-Ae Park 3
Eun-Jung Jung3
Chang JM, Moon WK, Cho N, et al.

Keywords: benign papilloma, malignancy, screening US,

ultrasound-guided biopsy, upgrade rate

Management of
Ultrasonographically Detected
Benign Papillomas of the Breast at
Core Needle Biopsy
OBJECTIVE. The purpose of this study is to retrospectively assess the upgrade rate determined by surgery for sonographically detected benign papillomas at core needle biopsy.
MATERIALS AND METHODS. Sixty-four benign papillomas, detected during screening ultrasound and diagnosed at ultrasound-guided core needle biopsy in 58 patients (mean
age, 44.6 years; range, 3067 years), were surgically excised. The upgrade rate to atypical lesion and malignancy was determined on a per-lesion basis. Statistical analysis was performed
to evaluate whether patients age and lesion variables (i.e., size, distance from the nipple, and
ultrasound findings) affected the upgrade rate.
RESULTS. Surgical excision revealed the presence of benign papillomas in 43 cases, no
residual lesion in 12 cases, atypical papillomas in seven cases, and papillary ductal carcinoma
in situ in two cases. The upgrade rates to atypical papilloma and to malignancy were 10.9%
(7/64; 95% CI, 4.5121.3%) and 3.1% (2/64; 95% CI, 0.3810.8%), respectively. Mean lesion
size was significantly larger for lesions that were upgraded to malignancies (1.4 cm vs 0.9 cm)
(p = 0.04). Age, distance from the nipple, and ultrasound findings were not significantly associated with underestimation of atypical lesions or malignancies after excision (p > 0.05).
CONCLUSION. Our results show that the upgrade rate to malignancy determined by
surgery for ultrasound-detected benign papillomas at core needle biopsy was 3.1% (2/64).
Accordingly, for the accurate diagnosis of ultrasound-detected benign papillomas at core needle biopsy, surgical excision is recommended.

DOI:10.2214/AJR.10.4615
Received March 15, 2010; accepted after revision
June 25, 2010.
This research was supported by the Basic Science
Research Program, through the National Research
Foundation funded by the Ministry of Education, Science,
and Technology (grant 20090080219), and by a grant from
the National R&D Program for Cancer Control, Ministry
of Health and Welfare, Republic of Korea (grant A01185).
1
Department of Radiology and Clinical Research
Institute, Seoul National University Hospital and the
Institute of Radiation Medicine, Seoul National
University Medical Research Center, 28, Yongon-dong,
Chongno-gu, Seoul 100-744, Republic of Korea. Address
correspondence to W. K. Moon (moonwk@radcom.snu.ac.kr).
2
Department of Surgery, Seoul National University
Hospital, Seoul, Republic of Korea.
3
Department of Pathology, Seoul National University
Hospital, Seoul, Republic of Korea.

AJR 2011; 196:723729

0361803X/11/1963723
American Roentgen Ray Society

apillary lesions of the breast

comprise a wide spectrum of lesions, ranging from benign papilloma to papilloma with foci of
atypia or papillary carcinoma [1], and differentiation of malignancy and benignity is difficult on the basis of imaging findings alone
[24]. Although imaging-guided core needle
biopsy is a highly reliable method for the diagnosis of breast lesions, the management of
benign papillomas diagnosed at core needle
biopsy remains controversial [525]. Surgical excision has been recommended in these
cases on the premise that a core needle biopsy may provide inadequate sampling of papillary lesions with subsequent false-negative
diagnoses or sampling error. Patients age,
size of the lesion, distance from the nipple,
imaging findings, and needle type may affect
the histologic upgrade rate. However, some
investigators have insisted that benign papillary lesions can be diagnosed accurately by
the use of core needle biopsy [5, 16, 18].

For the core needle biopsy of breast mass lesions, ultrasound guidance is preferable to stereotactic guidance in terms of the patients comfort, procedure time, and relative cost [26].
Ultrasound-guided biopsy is performed in real
time, and direct needle visualization allows accurate tissue sampling. Several studies have focused on the management of benign papillomas
diagnosed at ultrasound-guided core needle biopsy [2225]. However, a majority of the lesions were in patients with nipple discharge or
palpable mass or associated mammographic
abnormalities. Recently, the increasing number
of screening breast ultrasound examinations
has led to the detection of more masses detected
only by this technique than ever before [27].
The upgrade rate of clinically and mammographically occult benign papillomas at ultrasound-guided core needle biopsy has not been
evaluated. Thus, the objective of this study
was to retrospectively assess the upgrade rate
determined by surgery for ultrasound-detected benign papillomas at core needle biopsy.

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Chang et al.

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Materials and Methods

Patients
This retrospective review of images and medical records was approved by the institutional review board of our institution. Between July 2007
and February 2009, ultrasound-guided core needle
biopsy was performed in 4,297 patients at our institution. Among these patients, benign intraductal papillomas were diagnosed after biopsy for 223
lesions in 198 patients (4.6%). From these lesions,
we retrospectively identified 91 screening ultrasound-detected (clinically and mammographically occult) consecutive lesions in 80 patients using an outcome audit of our biopsy database and
medical records. Mammogram findings of these
patients were negative even in retrospect. Among
the patients, five lesions in three patients who had
a history of atypical papilloma in the ipsilateral
breast and 22 lesions in 19 patients who refused
surgical excision were excluded. Finally, 64 lesions in 58 patients comprised our study population. The mean age of the patients was 44.6 years
(age range, 3067 years; median, 45 years). No
patient had a history of breast cancer. The prevalence of benign intraductal papillomas on screening ultrasound cannot be determined from this
series because the majority of the patients were
referred from outside institutions.
For the diagnosis of benign papilloma, proliferation of the ductal epithelium with fibrovascular core
formation, the presence of myoepithelial cells, and
the absence of cellular monotony were required.
Atypical papillomas were considered to show the
presence of focal cytologic or architectural atypia,
focal absence of myoepithelial cells, and monotonous epithelial proliferation [28]. In our institution,
surgical excision was recommended for the biopsy
result of benign papilloma in all cases.

Ultrasound and Core Needle Biopsy

For screening ultrasound, one of seven radiologists with 315 years of experience in breast imaging performed whole-breast ultrasound for women
with dense breasts (BI-RADS density category 3
and 4) [29] using 514 MHz linear transducers on
an ultrasound scanner (IU-22, Philips Healthcare;
or EUB-8500, Hitachi Medical). All masses detected during screening ultrasound were sampled under
ultrasound guidance by the use of the EUB-8500
scanner (Hitachi Medical). The biopsy procedures
were performed by one of five radiologists with
511 years of experience in breast imaging. Tissue
samples were obtained with an automated biopsy
gun with a 14-gauge needle (Pro-Mag 2.2, Manan
Medical Products) for 54 lesions and an 11-gauge
vacuum-assisted probe (Mammotome, EthiconEndosurgery) for 10 lesions. Each radiologist determined the type of biopsy to be performed, with

724

11-gauge vacuum-assisted biopsy being preferred

for intraductal lesions or complex masses. Nearly
complete excision was recommended in cases of
11-gauge vacuum-assisted biopsy. When 14-gauge
automated needle biopsy was selected, five core
samples were obtained in most cases. A mean of
six core samples (range, 210) was obtained per lesion with the 14-gauge needle, and seven core samples (range, 319) were obtained with the 11-gauge
vacuum-assisted probe. The biopsy procedure took
approximately 2030 minutes. No localizing clip
was used during this study.

Surgical Excision
The mean duration from core biopsy to surgical
excision was 52 days (range, 5145 days). For exact identification of biopsy-confirmed benign papillomas, ultrasound-guided preoperative needle localization was performed with a 21-gauge modified
Kopans spring-hook localization needle (Cook Medical) for all lesions. The excision specimens were examined to identify previous biopsy site changes to
ensure that the correct site was excised. Specimen
ultrasound was not performed in this study.
The surgical pathologic result was reviewed with
the ultrasound-guided core needle biopsy results,
and the lesions were classified into the following
categories: benign papilloma, no residual or other
benign lesions, atypical papilloma, ductal carcinoma in situ (DCIS), and invasive carcinoma. All
biopsy specimens were evaluated by a pathologist
with 20 years of experience in breast pathology.

Data Collection and Statistical Analysis

The radiologists who performed the procedures
recorded the lesion size (maximal diameter as
measured on ultrasound), lesion distance from the
nipple, and final assessment category according to
the American College of Radiologys BI-RADS
[30]. Category 4 was subclassified into 4A (low
suspicion), 4B (intermediate suspicion), and 4C
(moderate suspicion); category 4A included estimated malignancy rates from greater than 2% to
less than 10%, category 4B estimated malignancy rates from greater than 10% to less than 50%,
and category 4C estimated malignancy rates from
greater than 50% to less than 95%. A solid mass
with circumscribed margins, oval shape, and horizontal orientation was included into category 3.
Intraductal masses were regarded as special cases according to BI-RADS and were assessed as
category 4A. Irregularly shaped complex masses
were assessed as category 4B or higher. However,
what lesions and imaging characteristics should
be placed in BI-RADS 4 subcategories were not
specifically defined.
Pathologic analysis results of benign papilloma
were compared with ultrasound findings to deter-

mine concordances and discordances of biopsy results. Benign pathologic results were considered
concordant if no imaging features that were BIRADS category 4B, 4C, or 5 (highly suggestive of
malignancy) were present [15]. The findings were
considered discordant when a BI-RADS category
of 4B, 4C, or 5 was assigned to a lesion at the time
of imaging and the corresponding histologic finding was benign papilloma.
An upgrade in diagnosis was determined when
a patient had at least one lesion that was classified as atypia, DCIS, or an invasive cancer after
surgical excision. On a per-lesion basis, the Fishers exact test was used for the differences in the
ultrasound findings between benign, atypical, and
malignant papillary lesions. The chi-square test,
Fishers exact test, and Student t test were performed to evaluate whether patient age, lesion
variables (size, distance from the nipple, ultrasound findings, and final assessment category), biopsy procedures (needle type and core number),
and imaging-histologic concordance affected differences in the upgrade rate. A p value less than
0.05 indicated statistical significance. All statistical analyses were performed with the use of SPSS
software (version 12.0, SPSS).

Results
The histopathologic findings of the 64
surgically excised lesions revealed the presence of benign papillomas in 43 cases, atypical papillomas in seven cases, and DCIS in
two cases. In 12 cases, residual lesions could
not be identified in the previous biopsy site
and were presumed to have been entirely excised at core biopsy. The upgrade rate to a
malignancy was 3.1% (95% CI, 0.3810.8%)
and that to an atypical papilloma was 10.9%
(95% CI, 4.5121.3%).
Ultrasound findings of 64 papillary lesions and lesion variables affecting histologic upgrades are shown in Tables 1 and 2.
The ultrasound findings showed no significant difference between the benign, atypical,
and malignant lesion groups. However, the
mean lesion size as measured on ultrasound
for the malignancies was 1.4 0.4 cm (median, 1.4 cm) and was larger than benign (0.9
0.4 cm; median, 0.8 cm) or atypical lesions
(0.7 0.2 cm; median, 0.7 cm); a statistically
significant relationship between lesion size
and the presence of a malignancy after surgical excision was noted (p = 0.04). Statistical significance was not noted for patient age
(p= 0.46), lesion distance from the nipple
(p = 0.57), BI-RADS assessment (p = 0.93)
on ultrasound, core number (p = 0.92), imaging-histologic concordance or discordance

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Management of Benign Breast Papillomas

(p = 0.66), and needle type (p = 0.73). None
of the cases upgraded to atypia or malignancy, however, were biopsied with the 11-gauge
vacuum-assisted probe.
Individual characteristics of cases that
were upgraded to atypia or malignancy are
listed in Table 3. On ultrasound, one cancer
was depicted as a 1.7-cm intraductal mass,
and the other cancer was depicted as a 1.1cm indistinct hypoechoic mass (Fig. 1). The
BI-RADS final assessment category of both
cancers was category 4A and was considered
to show imaging findings concordant with
the biopsy results. Low-nuclear-grade DCIS
was found apart from intraductal papillomas
in both cases. In the cases of seven atypical papillomas, the lesion size on ultrasound
ranged from 0.4 cm to 1.2 cm. The BI-RADS
final assessment categories were category 4A
for six lesions and category 4B for one lesion.
One lesion was considered to show discordant findings, because the case showed an irregularly shaped complex mass assessed as
category 4B. The rest of the lesions were
considered to show ultrasound findings concordant with the biopsy results. Atypia was
found within papilloma in four cases and in
the surrounding tissue in three cases.
Discussion
In the current study, we retrospectively assessed the upgrade rate of benign papillomas
detected during screening ultrasound and
diagnosed at core needle biopsy. After surgical excision, benign papillomas were upgraded to DCIS in 3.1% (2/64) of cases. Although the rate of upgrade to malignancy in
our study was not high compared with the
rates in previous studies (Table 4), it was still
greater than the accepted 2% or lower probability of malignancy in BI-RADS category
3 probably benign lesions, for which conservative management with close imaging follow-up is recommended [2931]. In addition, 10.9% (7/64) of benign papillomas in
our study were upgraded to atypical papillomas after surgical excision. Identification
of patients with atypical papilloma is important because in many institutions, these patients may be candidates for risk reduction
management strategies and may be offered
chemoprevention [32, 33].
The results of our study revealed a considerable upgrade rate (14%) for benign papilloma to atypical lesions or DCIS. Malignancies were either focal within a papillary
lesion or just adjacent to the papilloma. Because pathologic diagnosis of papillomas and

classification of atypical features by core biopsy is challenging, relatively minor differences in core biopsy classification could potentially translate into different outcomes at
surgical excision [1]. In addition, the distinction of benign from atypical papillary lesions
is often problematic for pathologists even
when the entire lesion is removed, and this
is more of an issue when the pathologists are
not subspecialized in breast pathology. Pap-

illoma can degenerate into malignancy over

time, and this risk may be greater with added
atypical hyperplasia outside the papilloma.
Most of the subsequent invasive carcinomas
develop in the same breast, probably near the
site of the original papilloma [32].
The recommendation of physicians who
do not call for the excision of all papillary lesions is that benign papillomas diagnosed at
core needle biopsy do not have to be excised

TABLE 1: Ultrasound Findings of Benign, Atypical, and Malignant Papillary

Lesions at Surgery
Surgical Results
Ultrasound Findings

Benign (n = 55)

Atypical (n = 7)

Malignant (n = 2)

28

Parallel

27

Not parallel

12

Circumscribed

12

Not circumscribed

27

Indistinct

26

Angular

Microlobulated

Spiculated

Abrupt interface

39

Echogenic halo

Shape
Round
Oval
Irregular

0.12

Orientation

0.33

Margin

0.78

Lesion boundary

Not applicable

Echo pattern

0.98

Anechoic

Hyperechoic

Hypoechoic

33

Complex

Isoechoic

Posterior feature

0.82

Normal

27

Enhancement

10

No

21

Duct dilatation

18

16

Shadowing
Surrounding tissue change

Architectural distortion
Intraductal mass

1.000

0.487

NoteIntraductal masses were regarded as special cases according to BI-RADS and are not described as
masses with margins, shape, and so forth.

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Chang et al.
as long as there is radiologic and clinical concordance [16, 20]. Ultrasound findings common to benign papilloma are oval or round
hypoechoic mass with indistinct or circumscribed margin or intraductal mass. However,
these findings are also seen in malignant papillary lesions [2, 3]. In our study, both DCIS
lesions and six of seven atypical lesions would
have been missed if follow-up was chosen according to the decision of concordance between the ultrasound and histologic findings.
This finding is consistent with data reported
by Liberman et al. [12], in which surgery revealed either cancer (14% [5/35]) or high-risk
lesions (17% [6/35]) in almost one-third (31%)
of lesions yielding a benign concordant diagnosis of papilloma at percutaneous biopsy. In
their study, four of five cancers, including one
invasive ductal carcinoma, were identified as
a result of interval change at follow-up (median, 22 months; range, 725 months).
In previous reports on the upgrade rate of
benign papillomas diagnosed at core needle biopsy, an age of more than 50 years,
the presence of nipple discharge or palpable
mass, peripheral location, and microcalcifications were found to be significantly related
to the risk of malignancy after surgical excisions [17, 23]. In our study, which studied
ultrasound-detected papillomas at core needle biopsy, however, lesion size was the only
significant factor associated with upgrade to
malignancy. Clearly, a 2-cm papillary lesion
may be more heterogeneous than a 0.5-cm
one, and obtaining enough tissue from the
larger lesion is important to avoid the sampling error [34].

TABLE 2: Variables Affecting Histologic Upgrade at Surgical Excision in

64 Benign Papillomas at Ultrasound-Guided Core Needle Biopsy
Surgical Results
Variables

Benign (n = 55) Atypical (n = 7) Malignant (n = 2)

Age (y)

p
0.46

Mean SD

44.7 7.4

43.4 12.4

40.5 0.7

Median (range)

46 (3065)

44 (3067)

40.5 (4041)
0.040a

Maximum lesion diameter (cm)

Mean SD
Median (range)

0.9 0.4

0.7 0.2

1.4 0.4

0.8 (0.42)

0.7(0.41.2)

1.4 (1.11.7)

Lesion distance from the nipple (cm)

Mean SD

0.57
1.83 1.65

2.0 1.26

2.5 0.7

1.7 (07)

2.0 (03.5)

2.5 (23)

Category 4A

50

Category 4B

Category 4C or 5

14-gauge automated

45

11-gauge vacuum-assisted

10

Mean SD

5.7 1.1

5.6 1.8

60

Median (range)

6 (219)

6 (28)

Median distance (range)

BI-RADS assessment

0.93

Category 3

Biopsy needle type

0.73

No. of core specimens obtained

0.92

Imaging-histologic concordance

0.66

Concordant

48

Discordant

ap < 0.05 indicates the difference between two groups; benign or atypical lesions versus malignancy using the

Student t test.

TABLE 3: Summary of Cases Upgraded to Atypical Papilloma or Malignancy after Surgical Excision
Distance
Case Patient Lesion
from the
No. Age (y) Size (mm) Nipple (mm)

Ultrasound Finding

Biopsy
BI-RADS Needle No. of
Category Gauge Cores

ImagingHistologic
Concordance

Surgical Pathology

40

17

30

Intraductal mass

4A

14

Concordant

Focal DCIS and intraductal papillomas

41

11

20

Indistinct hypoechoic mass

4A

14

Concordant

1.3-cm DCIS and intraductal papillomas

30

Intraductal mass

4A

14

Concordant

Atypical papillomas

44

12

20

Irregular complex mass

4B

14

Discordant

Atypical papillomas

44

20

Indistinct hypoechoic mass

4A

14

Concordant

Atypical papillomas

67

35

Indistinct hypoechoic mass

4A

14

Concordant

Atypical papilloma and intraductal

papilloma

46

20

Indistinct hypoechoic mass

4A

14

Concordant

Atypical papillomas

43

40

Circumscribed hypoechoic mass

4A

14

Concordant

Atypical papilloma and intraductal

papillomas

30

35

Circumscribed hypoechoic mass

4A

14

Concordant

Atypical papilloma and intraductal

papillomas

NoteDCIS = ductal carcinoma in situ.

726

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Management of Benign Breast Papillomas

Fig. 141-year-old woman with benign papilloma with adjacent ductal carcinoma in situ (DCIS).
A and B, Transverse (A) and longitudinal (B) ultrasound images show 11-mm hypoechoic oval mass (arrow, A and B) with indistinct margins, horizontal orientation, and no
posterior acoustic features in left upper breast. Final assessment was BI-RADS category 4A.
C, Photomicrograph of core needle biopsy specimen shows intraductal papilloma with fibrovascular cores and mild ductal epithelial hyperplasia. (H and E, 400)
D, Photomicrograph of excisional biopsy specimen shows papillary DCIS (arrow) adjacent to intraductal papilloma (arrowhead). (H and E staining, 40)

Some researchers have suggested that

wider sampling of papillary lesions with an
811-gauge vacuum-assisted probe rather
than a 14-gauge automated needle may provide more accurate diagnosis, perhaps sparing the need for surgical excision [16, 18,
24]. However, Liberman et al. [12] have reviewed this issue and found no statistical
difference between the use of 11-gauge and

14-gauge core biopsies. In our study, none of

the cases upgraded to atypia or malignancy
were biopsied with the 11-gauge vacuum-assisted probe, although the difference failed
to achieve statistical significance. Lesions
that were biopsied with an 11-gauge vacuumassisted probe represented a relatively small
percentage of lesions in our study. Therefore,
further study is necessary to confirm the role

of ultrasound-guided vacuum-assisted biopsy in the diagnosis of papillary lesions.

There are several limitations to our study.
One limitation is that our study population
was small and the findings were from a single
metropolitan-based cancer center. In addition,
of the benign papillomas detected during
screening ultrasound, we included only cases
with surgical excision, which could have led

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Chang et al.
TABLE 4: Upgrade Rate after Surgical Excision of Benign Papillomas Initially Diagnosed at Core Needle Biopsy:
Summary of Literature

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Study

Year

Type of Guidance

Needle Gauge

No. of Excised Lesions

Upgrade to Atypia

Upgrade to Cancer

Puglisi et al. [7]

2003

Ultrasound, stereotactic

14

31

Not specified

2/31 (6.5%)

Renshaw et al. [8]

2004

Not specified

11 and 14

18

Not specified

0/18 (0%)
0/11 (0%)

Agoff et al. [9]

2004

Not specified

9, 11,and 14

11

0/11 (0%)

Ivan et al. [10]

2004

Ultrasound, stereotactic

1120

0/6 (0%)

0/6 (0%)

Liberman et al. [12]

2006

Ultrasound, stereotactic

11 and 14

25

6/25 (24%)a

5/25 (20%)

Mercado et al. [13]

2006

Ultrasound, stereotactic

11 and 14

36

8/36 (22.2%)

2/36 (5.6%)

Sydnor et al. [16]

2007

Ultrasound, stereotactic

11 and 14

23

Not specified

4/23 (17.4%)b

Rizzo et al. [11]

2008

Stereotactic

11

86

12/86 (14%)

9/86 (10.5%)

Shin et al. [24]

2008

Ultrasound

8,11,and 14

86

6/86 (6.9%)a

12/86 (14%)

Kil et al. [22]

2008

Ultrasound, stereotactic

11 and 14

68

Not specified

6/68 (8.8%)

Bernik et al. [19]

2009

Ultrasound, stereotactic

916

47

13/47 (27.7%)

4/47 (8.5%)

Ahmadiyeh et al. [20]

2009

Ultrasound, stereotactic

8, 11, and 14

29

Not specified

1/29 (3.4%)

Jaffer et al. [21]

2009

Ultrasound, stereotactic

1420

104

8/104 (7.7%)

9/104 (8.7%)

570

53/401 (13.2%)

54/570 (9.5%)

Total

aHigh-risk lesions such as radial scar, lobular carcinoma in situ, atypical lobular hyperplasia were included.
bAuthor treated lobular carcinoma in situ as malignant.

to overestimation of the upgrade rate. The absence of excision for a total of 27 lesions in 22
patients is a limitation. In our study, a localizing clip or specimen ultrasound was not used,
and this may be a limitation. At needle localization of ultrasound-detected breast lesions,
marker placement under ultrasound guidance
can be beneficial because it enables immediate confirmation of accurate surgical removal
of the localized lesion at surgical excision
[35].
In conclusion, because 3.1% of benign papillomas diagnosed at core needle biopsy were
associated with malignancy at surgical excision, we recommend surgical excision for the
accurate diagnosis of ultrasound-detected benign papillomas of the breast diagnosed at
14-gauge core needle biopsy. However, further study is still needed to confirm the role of
ultrasound-guided vacuum-assisted biopsy in
the diagnosis of papillary lesions.
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