DOI:10.2214/AJR.07.3483
AJR 2008; 191:700-707
© American Roentgen Ray Society
Spectrum of Papillary Lesions of the Breast: Clinical, Imaging, and Pathologic Correlation
Malai Muttarak1,
Pailin Lerttumnongtum1,
Benjaporn Chaiwun2 and
Wilfred C. G. Peh3
1 Department of Radiology, Chiang Mai University, Chiang Mai, Thailand
50200.
2 Department of Pathology, Chiang Mai University, Chiang Mai, Thailand.
3 Department of Diagnostic Radiology, Alexandra Hospital, Singapore.
Received December 2, 2007;
accepted after revision March 28, 2008.
Address correspondence to M. Muttarak
(mmuttara{at}mail.med.cmu.ac.th).
Presented as a scientific exhibit and awarded a Certificate of Merit at the
2007 annual meeting of the American Roentgen Ray Society, Orlando, FL.
CME
This article is available for CME credit. See
www.arrs.org
for more information.
Abstract
OBJECTIVE. Papillary lesions of the breast are a heterogeneous group
of lesions that are difficult to diagnose as benign or malignant. The purpose
of this article is to review clinical presentation, imaging features, and
pathologic correlation of papillary lesions of the breast and to discuss the
prognosis and management of these lesions.
CONCLUSION. Recognition of the variety of benign and malignant
papillary lesions of the breast will facilitate diagnosis and proper
management.
Keywords: breast neoplasms • diagnosis • papillary lesions
Introduction
Papillary lesions of the breast are a heterogeneous group of breast lesions
that are difficult to diagnose as benign or malignant. These lesions have
varied morphologic features that carry differing prognostic implications for
affected patients. Accurate diagnosis is required to ensure that effective
treatment is achieved. Papillary lesions of the breast include benign
papillomas and malignant papillary lesions. The malignant papillary lesions
included in this article are micropapillary ductal carcinoma in situ (DCIS),
noninvasive papillary carcinoma, invasive papillary carcinoma, and invasive
micropapillary carcinoma. This article illustrates the spectrum of clinical
pres entations, management, imaging features of various techniques, and
pathologic cor relation of papillary lesions of the breast. Institutional
review board approval was granted, and informed consent was waived.
Papillomas
Papillomas of the breast can be divided into solitary papillomas, multiple
papillomas, and juvenile papillomatosis. Solitary or central papillomas arise
in the large subareolar ducts. Pathologically, a papilloma is a masslike
projection that consists of papillary fronds attached to the inner mammary
duct wall by a fibrovascular core that is covered with ductal epithelial and
myoepithelial cells. Ductal epithelial cells may undergo apocrine metaplasia,
hyper plasia, or atypia [1].
Clinically, solitary papillomas commonly occur in perimeno pausal women.
Patients commonly present with spontaneous nipple discharge that may be
bloody, serous, or clear. Women with solitary papillomas have a slightly
increased risk of developing breast carcinoma (1.5–2.0 times)
[2]. Central papillomas are
usually solitary, but multiple central papillomas have been reported
[3]. Central papillomas are
typically small and are often mammographically occult (Fig.
1A,
1B). Sonography or ducto graphy
is usually necessary for visualization of the lesion. A solitary papilloma
occasionally appears on mammo graphy as a circumscribed subareolar mass (Fig.
2A,
2B,
2C,
2D) or as a solitary dilated
retro areolar duct (Fig. 3A,
3B); these lesions are rarely
calcified. On sono graphy, a papilloma is seen as an intraductal mass in a
dilated duct, an intracystic mass, or a solid mass with a well-defined border
[2]. Ducto graphy may show an
intraluminal filling defect or ductal dilatation due to partial or complete
ductal obstruction. Recently, MRI has been reported to be a useful adjunct
technique to detect intraductal papilloma of the breast
[4].
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Fig. 1A —Papilloma in 41-year-old woman with left-sided bloody nipple
discharge. Left craniocaudal mammogram shows dense breast with no definite
abnormality. Mammography is indicated in any patient with pathologic nipple
discharge, but negative findings do not exclude breast lesions.
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Fig. 1B —Papilloma in 41-year-old woman with left-sided bloody nipple
discharge. Sonogram shows dilated duct and intraductal mass (arrow).
Excisional biopsy revealed papilloma. Advanced sonographic technology can
depict cause of nipple discharge and also guide biopsy (fine-needle
aspiration, core needle, and vacuum-assisted biopsy; preoperative localization
for excisional biopsy; and percutaneous ductography). However, sonography is
inferior to ductography for detecting peripheral lesions without ductal
dilatation.
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Fig. 2A —Papilloma in 70-year-old woman with palpable mass in right
breast. Right craniocaudal mammogram shows fatty breast with large oval
circumscribed mass in subareolar region and groups of calcifications medially
that subsequently proved to be benign.
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Fig. 2B —Papilloma in 70-year-old woman with palpable mass in right
breast. Sonogram of left breast shows oval parallel circumscribed complex
cystic mass containing intracystic mass (M) with posterior acoustic
enhancement. Simple mastectomy was performed.
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Fig. 2C —Papilloma in 70-year-old woman with palpable mass in right
breast. Gross specimen shows cystic mass (arrowheads) and intracystic
nodular solid mass (arrow) corresponding to sonographic findings.
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Fig. 2D —Papilloma in 70-year-old woman with palpable mass in right
breast. Photomicrograph shows branching papillary structures lined by benign
columnar cells and fibrovascular core (arrow). (H and E,
x100)
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Fig. 3A —Papilloma in 52-year-old woman with left-sided
serosanguineous nipple discharge. Left craniocaudal mammogram shows fatty
breast with dilated duct (arrowheads) connecting to circumscribed
mass (arrow).
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Fig. 3B —Papilloma in 52-year-old woman with left-sided
serosanguineous nipple discharge. Color Doppler sonogram of left breast shows
dilated duct connecting to oval parallel circumscribed isoechoic mass having
vascular flow. Lesion was entirely removed by vacuum-assisted core biopsy and
revealed papilloma.
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Multiple or peripheral papillomas arise in the terminal ductal lobular
units. The basic histopathologic features are similar to those of central
papillomas, but ductal epithelial cells are more frequently associated with
hyperplasia, atypia, DCIS, or invasive carcinoma, as well as with sclerosing
ade nosis or a radial scar [1].
There is an increased risk of carcinoma in these patients that is related to
the presence of proliferative epithelial change
[1,
3]. Clinically, patients
commonly present with palpable masses. Multiple papillomas are usually found
bi laterally, and recurrence after surgical treatment is more common
[3]. Mammo graphic findings of
multiple papillomas are variable and include round, oval, or slightly
lobulated well-circumscribed or spiculated masses (Figs.
4A,
4B,
5A,
5B,
5C,
6A,
6B) with or without calci
fications, foci of micro calcifications, clusters of nodules, and asymmetric
density [3]. On sonography,
multiple papillomas are seen as round, oval, or lobulated circumscribed solid
masses or complex masses.
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Fig. 4A —Multiple papillomas in 53-year-old woman with palpable mass
laterally in left breast. Left craniocaudal mammogram shows heterogeneously
dense breast, partially circumscribed lobulated mass (M) laterally, and
circumscribed lobulated mass medially (arrow).
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Fig. 4B —Multiple papillomas in 53-year-old woman with palpable mass
laterally in left breast. Composite sonograms of left breast show irregular
parallel angular hypoechoic mass in inner quadrant (arrow) and oval
parallel circumscribed slightly hyperechoic mass with cystic component (C) in
outer quadrant. Excisional biopsy of both masses was performed and revealed
multiple papillomas.
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Fig. 5B —Multiple papillomas in 50-year-old woman with right-sided
bloody nipple discharge. Sonogram of right breast shows oval parallel
circumscribed isoechoic mass (arrow) connected to dilated duct and
multiple intraductal masses (arrowheads).
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Fig. 5C —Multiple papillomas in 50-year-old woman with right-sided
bloody nipple discharge. Right craniocaudal ductogram shows cystic dilatation
with filling defects (arrows) connected to mildly dilated duct.
Multiple filling defects (arrowheads) are seen in central and
peripheral ducts. Note that ductogram shows extent of masses in peripheral
ducts better than sonogram does. Excisional biopsy revealed multiple
papillomas.
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Fig. 6A —53-year-old woman with multiple papillomas found on screening
mammography. Left mediolateral oblique mammogram shows spiculated mass
(arrow) in subareolar region. Sonogram of left breast (not shown)
showed irregular hypoechoic mass. Fine-needle aspiration biopsy (not shown)
revealed benign epithelial cells. Because imaging findings were suggestive of
malignant lesion, excisional biopsy was performed.
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Fig. 6B —53-year-old woman with multiple papillomas found on screening
mammography. Photomicrograph of excised specimen shows a few dilated ducts
(arrows) among fibrous stroma (asterisk). These ducts
contain papillary proliferation of benign ductal epithelial cells and
fibrovascular cores. (H and E, x100)
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Juvenile papillomatosis occurs in young women. Pathologic findings consist
of papillomatosis and extensive cyst formation
[5]. Clinically, patients
present with a palpable mass and are frequently mistakenly believed to have a
fibroadenoma. Patients with juvenile papillomatosis often have a family
history of breast carcinoma, and the patients themselves have an increased
risk for developing breast carcinoma. An article by Rosen et al.
[5] showed that 28% of patients
with juvenile papillomatosis had one or more relatives with breast cancer.
Careful clinical surveillance is recommended for women with juvenile papillo
matosis and their female relatives (including first- and second-degree
relatives). Because the lesions usually occur in young women, patients are
usually first evaluated with sonography (Fig.
7A,
7B). Juvenile papillomatosis
is seen on sonography as an ill-defined heterogeneous mass with multiple
peripheral small cystic spaces. Mammography usually shows dense breast tissue
with no detectable lesion or asymmetric density
[6].
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Fig. 7A —Juvenile papillomatosis in 26-year-old woman with palpable
right breast mass. Sonography is imaging technique of choice in young patient
with breast mass because breast is dense and incidence of breast carcinoma is
low. Sonogram of right breast shows irregular parallel spiculated
heterogeneously echoic mass. Because sonographic findings were suggestive of
malignancy, mammography was performed (not shown) and showed extremely dense
breast with spiculated mass. No malignant cells were detected at fine-needle
aspiration biopsy of mass, but imaging findings were suggestive of malignancy,
and excisional biopsy was performed.
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Fig. 7B —Juvenile papillomatosis in 26-year-old woman with palpable
right breast mass. Sonography is imaging technique of choice in young patient
with breast mass because breast is dense and incidence of breast carcinoma is
low. Photomicrograph shows a few dilated ducts (arrows) containing
papillary proliferation of benign ductal epithelial cells, fibrovascular
cores, and multiple cysts (C) interspersed with dense stroma. (H and E,
x40)
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Malignant Papillary Lesions
Micropapillary DCIS is a variant of DCIS. The neoplastic cells grow around
the internal lining of a duct space with papillary projections, but most do
not have a fibrovascular core
[7]. These neoplastic cells may
break off or undergo focal necrosis and may be associated with calcifications
(Fig. 8A,
8B). Micropapillary DCIS
without calcification is difficult to recognize on mammography. It may also be
seen on mammograms as an area of architectural distortion. Micro pap illary
DCIS is more likely to ramify ex tensively in the ductal system, so it may be
difficult to obtain clear margins on local excision of this lesion. The actual
extent of micropapillary DCIS may be beyond the zone of suspicious
microcalcifications. Although recently MRI has been used to detect tumor
extension in non–comedo carcinoma
[8], the accuracy of MRI in the
detection of DCIS with a micropapillary pattern is unknown.
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Fig. 8A —55-year-old woman with micropapillary ductal carcinoma in
situ (DCIS) found on screening mammography. Magnified craniocaudal mammogram
shows clustered amorphous microcalcifications (arrow). Excisional
biopsy was performed by preoperative needle localization.
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Fig. 8B —55-year-old woman with micropapillary ductal carcinoma in
situ (DCIS) found on screening mammography. Photomicrograph shows dilated
ducts containing proliferation of neoplastic ductal epithelial cells arranged
in micropapillary pattern (arrows). Note absence of fibrovascular
core in DCIS. (H and E, x200)
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Papillary carcinoma is rare, constituting 1–2% of breast cancers
[9]; it can be noninvasive or
invasive. The noninvasive form may extend throughout a ductal system
(intraductal) or may be confined within a cystic structure (intracystic). The
neoplastic epithelial cells are usually characteristic of low-grade DCIS.
These cells are arranged in either solid, cribriform, micropapillary, or
stratified spindle cell patterns
[1]. Invasive carcinoma, when
present, is usually detected at the periphery of the lesion. Invasive
papillary carcinoma may have various growth patterns, either remaining a
papillary pattern or, more commonly, having a nonspecific pattern.
Underestimation of the degree of disease may occur by sampling error at
percutaneous biopsy because the center of the lesion is often targeted,
thereby missing the more aggressive elements that tend to be more peripherally
located in these lesions.
This tumor usually occurs in older women and most commonly presents with a
palpable mass. Bloody nipple discharge occurs in approximately 22–34% of
patients [9]. Generally,
patients with papillary carcinoma have a better prognosis, with less axillary
nodal involvement than those with other forms of ductal carcinomas
[1,
7].
On mammography, papillary carcinoma is seen as a solitary round, oval, or
lobulated circumscribed mass (Fig.
9A,
9B,
9C) or as clusters of
well-defined masses [9]. Masses
may have associated micro calcifications (Fig.
10A,
10B,
10C,
10D). Sonography reveals
single or multiple circumscribed solid or complex mixed cystic and solid
masses. These tumors tend to bleed centrally. Color Doppler sonography can
show blood flow in the tumors and help differentiate them from blood clots.
Papillary carcinoma is difficult to differentiate from benign papillomas using
imaging features alone.
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Fig. 9A —Invasive papillary carcinoma in 69-year-old woman with mass
in left breast. Note that mammography and sonography of this patient are
difficult to differentiate from those of papilloma in Figure
2A,
2B,
2C,
2D. However, presence of
complex solid–cystic mass with spontaneous intracystic bleeding in older
age woman is suggestive of papillary carcinoma rather than papillomas. Left
craniocaudal mammogram shows fatty breast with large lobulated circumscribed
mass (arrow) laterally.
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Fig. 9B —Invasive papillary carcinoma in 69-year-old woman with mass
in left breast. Note that mammography and sonography of this patient are
difficult to differentiate from those of papilloma in Figure
2A,
2B,
2C,
2D. However, presence of
complex solid–cystic mass with spontaneous intracystic bleeding in older
age woman is suggestive of papillary carcinoma rather than papillomas.
Sonogram shows oval parallel circumscribed complex cystic mass containing
solid nodular projection (M) and highly echogenic fluid–fluid level
(arrow) of blood. Excisional biopsy was performed and revealed
papillary carcinoma. Modified radical mastectomy was subsequently
performed.
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Fig. 9C —Invasive papillary carcinoma in 69-year-old woman with mass
in left breast. Note that mammography and sonography of this patient are
difficult to differentiate from those of papilloma in Figure
2A,
2B,
2C,
2D. However, presence of
complex solid–cystic mass with spontaneous intracystic bleeding in older
age woman is suggestive of papillary carcinoma rather than papillomas.
Photomicrograph shows dilated duct with papillary fronds and lined by
malignant columnar cells (short arrows). Note invasive focus
(long arrow). (H and E, x200)
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Fig. 10A —Noninvasive papillary carcinoma, solid type, in 44-year-old
woman with left-sided bloody nipple discharge. Magnified mediolateral oblique
mammogram shows extremely dense breast with group of pleomorphic
calcifications.
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Fig. 10B —Noninvasive papillary carcinoma, solid type, in 44-year-old
woman with left-sided bloody nipple discharge. Sonogram shows dilated duct
(arrowhead) filled with echogenic contents and multiple
calcifications (arrow). Fine-needle aspiration biopsy was performed
under sonographic guidance.
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Fig. 10C —Noninvasive papillary carcinoma, solid type, in 44-year-old
woman with left-sided bloody nipple discharge. Fine-needle aspiration smear
shows fragments of atypical columnar cells suggestive of papillary tumor with
necrotic material in background. Microcalcification (arrow) is noted
among tumor fragments. (Papanicolaou stain, x200)
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Fig. 10D —Noninvasive papillary carcinoma, solid type, in 44-year-old
woman with left-sided bloody nipple discharge. Because at cytology
differentiating benign from malignant papillary tumors is difficult,
excisional biopsy was performed with aid of marker on skin. Photomicrograph of
excised specimen shows distended duct (arrowheads) occupied by
spindle-shaped cells with necrosis and calcifications in center
(arrow). (H and E, x100)
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Pure invasive micropapillary carcinoma is rare, accounting for less than 2%
of breast cancers, but a focal form of micropapillary growth has been reported
in 3–6% of common types of invasive carcinomas. This lesion has
distinctive histologic features characterized by the invasive micropapillary
growth of tumor cells without a fibrovascular core. These tumor cells are
polygonal to elongated with an eosinophilic to amphophilic cyto plasm
surrounded by a clear space. This lesion occurs in the same age range as in
vasive ductal carcinoma of no particular type
[10], with an extremely high
incidence of regional lymph node involvement and a poor prognosis. Patients
with this tumor may not benefit from a sentinel lymph node procedure
[7]. Mammographic findings of
invasive micropapillary carcinoma include a round, oval, or irregular mass
with indistinct, microlobulated, or spiculated margins (Fig.
11A,
11B). Associated
microcalcifications, either isolated or associated with a mass, have been
reported in 44% of the cases. On sonography, invasive micropapillary carcinoma
appears as a homogeneously hypo echoic irregular or microlobulated mass with
posterior acoustic shadowing or normal sound transmission. These imaging
features cannot be differentiated from those of other types of breast
carcinoma [11].
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Fig. 11A —Invasive micropapillary carcinoma in 38-year-old woman with
palpable mass in right breast. Right mediolateral oblique mammogram shows
dense breast with ill-defined mass (short arrow), multiple
pleomorphic calcifications superiorly, and enlarged increased density right
axillary nodes (long arrow). Fine-needle aspiration biopsy (not
shown) revealed ductal carcinoma. Modified right mastectomy was performed and
revealed invasive micropapillary carcinoma with axillary node metastases in
three of 19 nodes.
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Fig. 11B —Invasive micropapillary carcinoma in 38-year-old woman with
palpable mass in right breast. Photomicrograph shows clusters of tumor cells
with intervening clear spaces that are characteristic of invasive
micropapillary carcinoma. (H and E, x100)
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Management of Papillary Lesions of the Breast
Debate continues as to whether a core biopsy is reliable to differentiate
benign from malignant papillary lesions. Although some authors have suggested
that a core biopsy [12] or
stereotactic directional vacuum-assisted biopsy
[13] may be reliable for
differentiating between benign and malignant papillary lesions, especially
when the results correlate with imaging findings (thereby obviating excision),
other authors strongly disagree. Lam et al.
[14] suggested that a core
biopsy is unreliable and excisional biopsy for definitive diagnosis should be
performed. Liberman et al.
[15] found that for
percutaneously diagnosed papillomas, surgery revealed cancer in 14% of cases
and high-risk lesions in 17%. This means that even for lesions yielding a
benign concordant diagnosis of papilloma at percutaneous biopsy, surgical
excision may be warranted. Frequent association of epithelial displacement
with the biopsy of papillary lesions has been reported
[16], which may be explained
by the friable nature of the lesions. Although the biologic significance of
epithelial displacement is currently unknown, it is important to recognize
this iatrogenic artifact so that this finding is not misinterpreted as stromal
or lymphatic invasion.
Conclusion
The appearances of papillary lesions of the breast vary clinically,
radiologically, and pathologically. Familiarity with the features of these
benign and malignant papillary lesions may be helpful in achieving diagnosis
and proper management.
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Abstract
Introduction
