Complex Cystic Breast Masses

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APPLICATIONS OF CURRENT TECHNOLOGY
S53
Complex Cystic Breast
Masses: Diagnostic
Approach and ImagingPathologic Correlation1
CME FEATURE
See accompanying
test at http://
www.rsna.org
/education
/rg_cme.html
LEARNING
OBJECTIVES
FOR TEST 2
After reading this
article and taking
the test, the reader
will be able to:
䡲 Recognize the imaging features of
complex cystic breast
masses.
䡲 Describe current
biopsy techniques
used to diagnose
complex cystic breast
masses.
䡲 Identify the common pathologic diagnoses of complex
cysts in the breast.
Devang J. Doshi, MD ● David E. March, MD ● Giovanna M. Crisi,
MD, PhD ● Bret F. Coughlin, MD
Complex cystic breast masses demonstrate both anechoic (cystic) and
echogenic (solid) components at ultrasonography (US). US is used to
identify and characterize such masses and to guide percutaneous biopsy. Numerous pathologic entities may produce complex cystic breast
lesions or may be associated with them, and biopsy is usually indicated.
Common benign findings include fibrocystic changes, intraductal or
intracystic papilloma without atypia, and fibroadenoma. Common
atypical findings include atypical ductal hyperplasia, atypical papilloma, atypical lobular hyperplasia, and lobular carcinoma in situ.
Malignant findings include ductal carcinoma in situ, infiltrating ductal
carcinoma, and infiltrating lobular carcinoma. If the biopsy approach is
tailored to the individual patient and if the imaging features are closely
correlated with findings at pathologic analysis, US-guided percutaneous biopsy may be used effectively to diagnose and to guide management of complex cystic masses.
©
RSNA, 2007
TEACHING
POINTS
See last page
Abbreviations: DCIS ⫽ ductal carcinoma in situ, H-E ⫽ hematoxylin-eosin
RadioGraphics 2007; 27:S53–S64 ● Published online 10.1148/rg.27si075508 ● Content Codes:
1From
the Departments of Radiology (D.J.D., D.E.M., B.F.C.) and Pathology (G.M.C.), Baystate Medical Center–The Western Campus of Tufts
University School of Medicine, 759 Chestnut St, Springfield, MA 01199. Recipient of a Certificate of Merit award for an education exhibit at the 2006
RSNA Annual Meeting. Received February 21, 2007; revision requested April 2 and received April 23; accepted May 3. All authors have no financial
relationships to disclose. Address correspondence to D.J.D. (e-mail: djdoshi12@yahoo.com).
©
RSNA, 2007
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October 2007
Introduction
Teaching
Point
Cystic breast lesions are commonly observed at
ultrasonography (US) performed for the evaluation of palpable or mammographically detected
breast masses. Complex cysts contain cystic and
solid components and are associated with a variety of benign, atypical, and malignant pathologic
diagnoses. Complex cystic breast masses have a
substantial chance of being malignant; malignancy was reported in 23% (1) and 31% (2) of
cases in two series. For that reason, percutaneous or surgical biopsy is usually indicated. Techniques that may be used for sampling of complex
cystic breast masses include fine-needle aspiration, core-needle biopsy (with an automated
spring-loaded or vacuum-assisted device), and
surgical excision. This article reviews the imaging
evaluation of complex cystic breast masses, various approaches to percutaneous biopsy, and common pathologic diagnoses.
Imaging Evaluation
Mammography
Many patients with complex cystic masses have
undergone recent mammography, which may
help characterize the mass, depict associated microcalcifications (Fig 1), and show additional suspicious lesions (3). If a lesion appears fat-containing at mammography, it represents a benign entity such as an oil cyst or galactocele, and biopsy
can be avoided. For lesions that are proved malignant at biopsy, mammography may provide important information about the extent of disease
and thus may influence subsequent surgical management.
Ultrasonography
At US, breast cysts are categorized as simple,
complicated, or complex (1,4,5). Appropriate
categorization is important because the management of each type differs. Simple cysts are defined
as anechoic, well-circumscribed, round or ovoid
masses with an imperceptible wall and increased
through-transmission of sound waves. When all
the criteria of simple breast cysts are present, they
are considered benign and do not require intervention. Painful cysts can be aspirated for symptom relief.
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Complicated cysts contain low-level internal
echoes or intracystic debris that may layer and
shift with changes in patient position. The homogeneous internal echoes within some complicated
cysts may produce an appearance identical to that
of a circumscribed solid mass. Complicated cysts
do not contain thick walls, thick septa, or other
discrete solid-appearing components. The risk of
malignancy among complicated breast cysts is less
than 2%; these cysts generally can be managed
with short-interval follow-up imaging or aspiration. However, if a complicated cyst is symptomatic, new, or enlarging, needle aspiration is indicated (1,5,6).
Complex breast cysts are defined as cysts with
thick walls, thick septa, intracystic masses, or
other discrete solid components (4). By using criteria adapted from Berg et al (1), we can categorize complex cystic breast masses into four classes
on the basis of their US features: Type 1 masses
have a thick outer wall, thick internal septa, or
both; type 2 masses contain one or more intracystic masses; type 3 masses contain mixed cystic
and solid components and are at least 50% cystic;
and type 4 masses are predominantly (at least
50%) solid with eccentric cystic foci.
Approach to Biopsy
Decision making about the best approach to use
for percutaneous biopsy of a complex cystic mass
involves balancing the need to obtain sufficient
material for an accurate diagnosis against the
need to minimize the invasiveness of the procedure. The percutaneous biopsy of complex cystic
masses may present a challenge, compared with
the biopsy of other types of breast lesions, because of the presence of a cystic component that
is typically disrupted during the biopsy procedure. In some cases, the decompression of the
cystic component may make it more difficult to
detect the remaining solid component at US and,
therefore, more difficult to target and sample it.
The techniques used for biopsy of complex cystic
breast masses include fine-needle aspiration,
core-needle biopsy, and surgical biopsy.
Avoiding Unnecessary Intervention
A thorough patient history and mammographic
evaluation may obviate intervention. For example, a hematoma with a complex cystic appearance might form soon after a needle biopsy, surgi-
Teaching
Point
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Figure 1. Infiltrating ductal carcinoma and ductal carcinoma in situ (DCIS) in a 44-year-old woman. (a) Mediolateral oblique mammogram shows a large mass with adjacent linear calcifications (arrow) in the upper part of the
right breast. (b) US image demonstrates a type 1 complex cystic mass with a thick wall and thick septum. The diagnosis was based on the results of a core-needle biopsy.
Figure 2. Oil cyst after reduction mammoplasty in a 23-year-old woman with a palpable
mass in the region of postoperative scarring in the left breast. (a) Doppler US image shows a
type 3 complex cystic mass without internal flow. (b) Tangential spot magnification mammogram, obtained after placement of an external marker, shows a well-circumscribed fatdensity mass (arrows) with a characteristically benign appearance. Biopsy was not indicated.
cal biopsy, or trauma. When a hematoma is suspected, a follow-up US examination (usually in
2–3 months) is recommended to reevaluate the
finding and verify regression. Areas of fat necrosis
due to surgery or trauma, as well as galactoceles,
also may appear as complex cystic masses (Fig 2).
Thus, biopsy may be averted in the appropriate
clinical setting or if the mass has a characteristically benign mammographic appearance.
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Figure 3. Complicated cyst in a 46-year-old woman. (a) US image shows dependent intracystic echoes.
(b) US image from a repeat examination with the patient in the left decubitus position shows mobility of the
intracystic material. The cyst resolved completely after fine-needle aspiration, which yielded nonbloody material, and core-needle biopsy was not indicated.
Figures 4, 5. (4) Papillary apocrine hyperplasia with atypical ductal hyperplasia. Doppler US image shows a
type 2 complex cystic mass with flow within the solid component (arrow). The mass was diagnosed at coreneedle biopsy, and the diagnosis was confirmed at surgical excision. (5) Papilloma in a 71-year-old woman.
Power Doppler US image shows a type 2 complex cystic mass with flow within the solid components. The
mass was diagnosed at core-needle biopsy.
Palpable Lesions
When a complex cystic mass is palpable, percutaneous biopsy with US guidance is preferable to
guidance with palpation only. The potential pit-
falls of aspiration or core biopsy performed only
with palpation for guidance include (a) difficulty
in accurately targeting the solid component,
(b) fluid aspiration or extraluminal leakage rendering a mass impalpable during biopsy and making subsequent biopsy passes less accurate, and
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Figure 6. Fibrocystic changes in a 59-year-old woman with a palpable breast mass. (a) Initial US image
shows a cyst with a slightly thick wall (type 1). Fine-needle aspiration yielded nonbloody fluid. (b) Follow-up
US image shows a residual ill-defined hypoechoic mass demarcated by electronic calipers. Histologic analysis
of a core-needle biopsy specimen obtained with a 14-gauge automated device indicated cystic apocrine metaplasia and dense fibrous stroma with reactive stromal changes, findings consistent with cyst wall.
(c) resolution of palpability in conjunction with
benign findings at cytologic and histologic analysis, which may be falsely reassuring and delay the
diagnosis of a potential malignant lesion.
Fine-Needle Aspiration
Teaching
Point
Teaching
Point
Fine-needle aspiration may be performed initially
if the presence of a true solid component within a
complex cystic mass is in question on the basis of
US findings; it may be unclear whether the intracystic echogenicity represents debris, pus, or a
clot within a complicated cyst, or a mass within a
complex cyst. The evaluation of mobility and flow
is a useful strategy for distinguishing between a
complex cyst and a complicated cyst. If the echogenic component is mobile with a position
change, it represents debris, pus, or a clot (Fig 3).
If the echogenic component is immobile, it may
represent either a true intracystic mass or debris
adherent to the cyst wall. The demonstration of
flow within a solid-appearing region at Doppler
imaging is indicative of a true intracystic mass
(Figs 4, 5). If no flow is seen, it is impossible to
differentiate a debris-containing mass from a hypovascular mass.
When a complex cystic mass is aspirated and
the aspirate appears purulent, it is submitted for
microbiologic analysis and antibiotic sensitivity
testing. A bloody aspirate is submitted for cytologic examination. A clip is placed internally at
the aspiration site if the aspirate is submitted for
cytologic examination and there is no residual
mass or other adjacent imaging landmark (7). If a
mass resolves after aspiration that yields nonbloody and nonpurulent fluid, the aspirate is discarded (8).
If a complex cyst contains a true solid component, biopsy is indicated for histologic diagnosis.
When fine-needle aspiration is performed and a
solid mass remains visible at US, core-needle biopsy of the residual solid lesion may be performed
immediately after the aspiration procedure (Figs
6, 7). Reliance solely on benign cytologic findings
in the fine-needle aspirate is not advisable, because the residual mass may represent a malignancy even if the aspirated material does not contain malignant cells (9,10).
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Figure 7. Infiltrating ductal carcinoma in a 33-year-old woman with a palpable breast mass. (a) US image demonstrates a thick-walled complex cystic mass (arrows). (b) US image shows the mass during fine-needle aspiration,
which yielded bloody fluid. The mass did not resolve completely. (c, d) US images obtained during core-needle biopsy, before (c) and after (d) firing of a 14-gauge automated device, show sampling of the small residual solid component. (e, f) Photomicrographs (original magnification, ⫻100 in e, ⫻400 in f; hematoxylin-eosin [H-E] stain) of a
specimen obtained at core-needle biopsy reveal grade 3 infiltrating ductal carcinoma.
US-guided Core-Needle Biopsy
Teaching
Point
Core-needle biopsy of a complex cyst may be performed without prior fine-needle aspiration if the
lesion (a) contains a definite solid component
observed at US or flow observed at color Doppler
imaging, (b) demonstrates associated suspicious
mammographic findings (clustered calcifications,
suspicious shape or margins, or architectural distortion), or (c) contains a small solid-appearing
component that would be difficult or impossible
to target with a large-gauge needle after fluid aspiration.
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Figure 8. Intracystic papilloma. (a) US image shows a type 2 complex cystic mass. (b) US image obtained during a vacuum-assisted biopsy shows an 11-gauge needle probe (arrows) positioned deep to the
mass. The diagnosis was established at vacuum-assisted biopsy.
Figure 9. Intracystic papilloma in a 45-year-old woman. US
image shows a type 2 complex cystic mass that contains a small
intracystic papilloma suspended on a stalk. The mass was surgically excised. If a percutaneous biopsy had been performed, the
solid part of the mass may have been difficult or impossible to
target for biopsy after the fluid-filled portion was drained.
In our practice, a core-needle biopsy is performed when a solid component is present. Either
a 14-gauge spring-loaded device or an 11-gauge
vacuum-assisted device is used. We found this
approach accurate in a series of 31 patients with
32 complex cystic masses and with 1-year follow-up of benign lesions (2). A US-guided coreneedle biopsy performed with a 14-gauge springloaded device is a low-cost, well-tolerated approach for the biopsy of lesions with a solid
component that is expected to remain clearly visible throughout the procedure. For biopsy of
masses that are primarily cystic and have only a
small solid component, we prefer to use an 11gauge hand-held vacuum-assisted device (Fig 8).
After the biopsy, if there is a concern that the residual mass might be difficult to localize for subsequent surgical excision on the basis of pathologic findings, a clip is deployed at the biopsy site.
Clip deployment devices for use with springloaded and vacuum-assisted needle biopsy devices are widely available. Furthermore, several
types of clips are visible both at US and at mammography, and their visibility may facilitate wire
localization when either modality is used for guidance. Specimen radiography is performed if the
lesion is associated with calcifications. Surgical
excision of a complex cystic mass is recommended instead of core-needle biopsy if adequate
sampling with core-needle biopsy would be technically difficult because of the size or location of
the solid components (Fig 9).
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Figure 10. Fibrocystic changes in a 45year-old woman with a nonpalpable mass
poorly depicted at mammography. (a) US
image shows a type 1 complex cystic mass
with thick septa. (b, c) Photomicrographs
(original magnification, ⫻40; H-E stain) of
specimens from core-needle biopsy show apocrine metaplasia (b) and apocrine metaplasia
with cyst formation (c).
Figure 11. Papilloma without atypia
in a 62-year-old
woman. (a) Craniocaudal mammogram
shows a well-circumscribed mass (arrow)
in the medial part of
the breast. (b) Doppler US image demonstrates a type 3
complex cystic mass.
(c) Photomicrograph
(original magnification, ⫻100; H-E stain)
of a specimen from a
core-needle biopsy
shows intraductal
papilloma without
atypia, with apocrine
metaplasia and
microcalcifications.
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Figure 12. Lobular carcinoma in situ associated with multiple papillomas in a 45-year-old
woman with mammographic findings of a mass and calcifications. (a) US image shows a type 2
complex cystic mass. (b) Radiograph of a specimen obtained at core-needle biopsy with an 11gauge vacuum-assisted device shows calcifications. (c) Photomicrograph (original magnification,
⫻100; H-E stain) of a core-needle biopsy specimen demonstrates an infarcted papilloma with calcifications. (d) Photomicrograph (original magnification, ⫻40 [background], ⫻400 [inset]; H-E
stain) of the subsequent excisional biopsy specimen shows incidental lobular carcinoma in situ.
Pathologic Findings
Complex cystic breast masses may be due to a
wide range of pathologic entities, including benign, atypical (high-risk), and malignant lesions.
Benign Lesions
Common benign diagnoses of complex cystic
breast masses include fibrocystic changes, intraductal or intracystic papilloma without atypia,
and fibroadenoma (1).
Fibrocystic changes include adenosis, sclerosing adenosis, apocrine metaplasia, cyst formation
with or without rupture, and ductal ectasia. Fibrocystic changes are nonproliferative changes
with three predominant morphologic features:
cyst formation, fibrosis, and adenosis (Fig 10)
(11,12). These findings are not associated with an
increased risk for breast cancer (13–15).
Intraductal or intracystic papilloma without
atypia is composed of multiple branching fibrovascular cores lined by two layers of epithelial and
myoepithelial cells (Figs 11, 12) (11,12). This
diagnosis is associated with a slightly increased
(by one and a half to two times) risk for breast
cancer (13–15) when multiple lesions are present.
Fibroadenoma, a fibroepithelial tumor, is composed of glandular and stromal tissue. The
stroma encloses glandular spaces lined by myoepithelial and epithelial cells. The stroma may be
fibrous, hyalinized, or myxoid (Fig 13) (11,12).
The diagnosis of fibroadenoma is not associated
with an increased risk for breast cancer (13–15).
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Figure 13. Fibroadenoma in a 48-year-old
woman. (a) Craniocaudal mammogram shows
an oval mass (arrow) in the lateral part of the
breast. (b) US image demonstrates a type 1 complex cystic mass. (c) Photomicrograph (original
magnification, ⫻40; H-E stain) of a specimen
from core-needle biopsy reveals fibroadenoma.
Atypical and High-Risk Lesions
Common atypical pathologic findings in complex
cystic breast masses include atypical ductal hyperplasia and atypical papilloma. Lobular neoplasia
(atypical lobular hyperplasia or lobular carcinoma
in situ) also may be associated with complex cystic breast masses.
Atypical ductal hyperplasia bears a histologic
resemblance to low-grade DCIS but is more limited in its extent. The lesion is characterized by a
partially monomorphic cell population, regular
cell placement, and microlumen formation
(11,12). It is associated with a moderately increased (four- to fivefold) risk for breast cancer
(13–15).
Atypical papilloma demonstrates areas of
atypical ductal hyperplasia within an intraductal
or intracystic papilloma or papillary lesion (11,
12). This lesion also is associated with a moderately increased (four- to fivefold) risk for breast
cancer (13–16).
Lobular neoplasia is usually found incidentally
at biopsy and produces no characteristic mammographic features (17). Atypical lobular hyperplasia
is characterized by a proliferation of monomorphic lobular-type cells similar to those in lobular
carcinoma in situ, except that they do not fill or
distend more than 50% of acini within the lobule
(11,12). Atypical lobular hyperplasia is associated
with a moderately increased (four- to fivefold)
risk for breast cancer (13–15,18). Lobular carcinoma in situ, which usually is also an incidental
pathologic finding, consists of a loosely cohesive
population of neoplastic cells with scant cytoplasm and small round to larger nuclei; the neoplastic cells fill and expand the lobules and terminal ducts (11,19). Lobular carcinoma in situ is
associated with a markedly increased (eight- to
10-fold) risk for breast cancer (13,14,18).
Malignant Lesions
The most common malignancies among complex
cystic masses include DCIS and infiltrating ductal
carcinoma. Infiltrating lobular carcinoma also
may have a complex cystic appearance. Berg et al
(1) reported two findings of infiltrating lobular
carcinoma (one a mixed lesion with infiltrating
ductal carcinoma and DCIS) among 18 carcinomas (11%) in their patient series; both were type
4 complex cystic lesions.
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Figure 14. DCIS in a 64-year-old
woman. (a) Mammogram shows an
oval mass that corresponds to a palpable abnormality. (b) US image depicts a type 3 complex cystic mass.
(c) Photomicrograph (original magnification, ⫻100; H-E stain) of a specimen
from core-needle biopsy reveals lowgrade cribriform DCIS.
DCIS consists of a proliferation of monomorphic neoplastic epithelial cells that fill the ductal
lumina. Different types of DCIS are recognized
on the basis of their architectural pattern and
nuclear characteristics. The myoepithelial cell
layer remains intact (Fig 14) (11,20). DCIS is
associated with a markedly increased (eight- to
10-fold) risk for infiltrating ductal carcinoma
(13,14).
Infiltrating ductal carcinoma is characterized
by glandular or solid clusters of malignant tumor
cells with infiltrating margins. The appearance of
the lesion is highly variable and depends on the
degree of cellularity, stromal reaction, necrosis,
and inflammatory cell infiltration (Fig 7) (11,21).
Infiltrating lobular carcinoma is characterized
by loosely cohesive tumor cells that infiltrate the
fibrous stroma as single cells, form threadlike
strands, or do both. The tumors are classified as
classic or pleomorphic on the basis of the nuclear
characteristics of the neoplastic cells (22).
Imaging-Pathologic Correlation
As with percutaneous biopsies of all breast lesions, the pathologic findings from biopsies of
complex cystic masses should be correlated with
the imaging features to determine whether they
are concordant. An understanding of the common histologic findings that produce a complex
cystic appearance at US is important in this process. To establish concordance, the specific imaging features of concern (such as a thick-walled
cyst or an intracystic mass) should be explainable
on the basis of the pathologic findings. The pathologist should be provided with a detailed description of the imaging findings, including differential diagnoses, to enable an optimal comparison
of the pathologic findings with the imaging features of the lesion.
Pathologic findings that appear to be discordant with imaging findings should be discussed
with the pathologist. Pathologic, imaging, and
clinical correlation is essential to ensure that the
targeted lesion was adequately sampled; in cases
of discordance, a repeat core-needle biopsy or
surgical biopsy should be considered. Among the
common pathologic findings of complex cystic
masses, it is widely agreed that atypical ductal
hyperplasia and atypical papilloma are indications
for surgical excision. The management of lobular
neoplasia and of papillary lesions without atypia is
more controversial and has been discussed elsewhere (7,23,24). Six-month follow-up imaging of
patients with benign concordant pathologic findings is recommended to reevaluate the lesion and
minimize the potential consequences of a falsenegative biopsy result (25).
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Conclusions
Complex cystic breast masses are suspicious US
findings that usually warrant biopsy. US is the
modality of choice for characterizing and guiding
biopsy of these lesions. Common benign causes
of complex cystic masses include fibrocystic
changes, intraductal or intracystic papilloma
without atypia, and fibroadenoma. Atypical findings include atypical ductal hyperplasia, lobular
neoplasia, and atypical papilloma. Malignant
findings include DCIS, infiltrating ductal carcinoma, and infiltrating lobular carcinoma. USguided percutaneous biopsy is an effective
method for diagnosing and guiding the management of complex cystic masses.
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This article meets the criteria for 1.0 credit hour in category 1 of the AMA Physician’s Recognition Award. To obtain
credit, see accompanying test at http://www.rsna.org/education/rg_cme.html.
RG
Volume 27 • Special Issue • October 2007
Doshi et al
Complex Cystic Breast Masses: Diagnostic Approach and
Imaging-Pathologic Correlation
Devang J. Doshi, MD, et al
RadioGraphics 2007; 27:S53–S64 ● Published online 10.1148/rg.27si075508 ● Content Codes:
Page S54
Complex cystic breast masses have a substantial chance of being malignant; malignancy was reported
in 23% and 31% of cases in two series. For that reason, percutaneous or surgical biopsy is usually
indicated.
Page S54
Complex breast cysts are defined as cysts with thick walls, thick septa, intracystic masses, or other
discrete solid components.
Page S57
Fine-needle aspiration may be performed initially if the presence of a true solid component within a
complex cystic mass is in question on the basis of US findings; it may be unclear whether the
intracystic echogenicity represents debris, pus, or a clot within a complicated cyst, or a mass within a
complex cyst.
Page S57
The evaluation of mobility and flow is a useful strategy for distinguishing between a complex cyst and
a complicated cyst.
Page S58
Core-needle biopsy of a complex cyst may be performed without prior fine-needle aspiration if the
lesion (a) contains a definite solid component observed at US or flow observed at color Doppler
imaging, (b) demonstrates associated suspicious mammographic findings (clustered calcifications,
suspicious shape or margins, or architectural distortion), or (c) contains a small solid-appearing
component that would be difficult or impossible to target with a large-gauge needle after fluid
aspiration.