DOI:10.2214/AJR.07.2056
AJR 2007; 189:1288-1293
© American Roentgen Ray Society
Imaging Differences in Metaplastic and Invasive Ductal Carcinomas of the Breast
Wei Tse Yang1,
Bryan Hennessy2,
Kristine Broglio3,
Chadwick Mills1,4,
Nour Sneige5,
W. Grant Davis5,6,
Vicente Valero7,
Kelly K. Hunt8 and
Michael Z. Gilcrease5
1 Department of Diagnostic Imaging, The University of Texas M. D. Anderson
Cancer Center, PO Box 301439, Unit 1350, Houston, TX 77230.
2 Department of Gynecology Medical Oncology, The University of Texas M. D.
Anderson Cancer Center, Houston, TX.
3 Quantitative Sciences Division, The University of Texas M. D. Anderson Cancer
Center, Houston, TX.
4 Present address: Department of Radiology, Baylor College of Medicine, Houston,
TX.
5 Department of Pathology, The University of Texas M. D. Anderson Cancer Center,
Houston, TX.
6 Present address: Physicians Reference Laboratory, Overland Park, KS.
7 Department of Breast Medical Oncology, The University of Texas M. D. Anderson
Cancer Center, Houston, TX.
8 Department of Surgical Oncology, The University of Texas M. D. Anderson Cancer
Center, Houston, TX.
Received February 16, 2007;
accepted after revision June 30, 2007.
Address correspondence to W. T. Yang
(wyang{at}di.mdacc.tmc.edu).
CME
This article is available for CME credit. See
www.arrs.org
for more information.
Abstract
OBJECTIVE. The purpose of this study was to compare the imaging
features of metaplastic breast carcinoma with those of invasive ductal
carcinoma.
MATERIALS AND METHODS. Women diagnosed on preoperative mammography
or sonography with metaplastic breast carcinoma and T-stage matched invasive
ductal carcinoma of the breast from a single pathology database were included
in the study. Clinical and pathologic information on all metaplastic cancers
was documented. Mammography and sonography variables were recorded using the
BI-RADS lexicon. Groups were compared using Fisher's exact test, the
chi-square test, or Wilcoxon's rank sum test, as appropriate.
RESULTS. Forty-three patients diagnosed with metaplastic carcinoma
were matched to 43 patients with ductal carcinoma by tumor T stage. Patients
with metaplastic carcinoma were younger (median, 46 vs 53 years, p =
0.048) than those with ductal carcinoma. Mammographically, metaplastic
carcinomas were less frequently irregular in shape (16% vs 74%, p
< 0.0001) and less frequently showed microlobulated or spiculated margins
(19% vs 56%, p = 0.0008) and calcifications (25% vs 51%, p =
0.02) when compared with ductal carcinomas. Sonographically, metaplastic
carcinomas were less frequently irregular in shape (27% vs 69%, p =
0.001) and less frequently showed angular margins (9% vs 49%) and posterior
acoustic shadowing (9% vs 49%, p < 0.0001).
CONCLUSION. Characteristic malignant imaging features, including
irregular shape, spiculated margins, segmentally distributed pleomorphic
calcifications, and posterior acoustic shadowing, are uncommon in metaplastic
carcinomas. These carcinomas tend to show more benign imaging features, such
as round or oval shape with circumscribed margins, when compared with ductal
carcinomas.
Keywords: breast neoplasm • invasive ductal carcinoma • mammography • metaplastic breast carcinoma • sonography
Introduction
Invasive breast carcinoma usually has an epithelial morphology with ductal
differentiation. Metaplastic carcinoma, on the other hand, is a heterogeneous
group of neoplasms with mixed epithelial and mesenchymal differentiation. This
mixed cell differentiation is seen both morphologically and
immunophenotypically, as evidenced by immunohistochemical expression of
markers of mesenchymal cells (vimentin), epithelial cells (pancytokeratin),
and myoepithelial cells (S-100, smooth-muscle actin, and p63). Metaplastic
breast carcinoma is uncommon, accounting for fewer than 5% of breast
carcinomas
[1–5].
Wargotz and Norris
[1–3]
and Wargotz et al. [4]
suggested five principal variants, including matrix-producing carcinoma,
spindle-cell carcinoma, squamous cell carcinoma, carcinosarcoma, and
metaplastic carcinoma with osteoclastic giant cells
[6]. Recently, low-grade
fibromatosis-like tumors have been described as a biologically distinct
subtype [7,
8].
The differential diagnosis between invasive ductal carcinoma and
metaplastic carcinoma is important for treatment planning and prognosis. A
recent study described significantly worse overall survivalfor the metaplastic
subtype compared with a control group
[9]. We undertook a study to
compare imaging features of invasive ductal carcinomas and metaplastic
carcinomas to determine whether significant differences are shown on
conventional imaging methods, including mammography and sonography.
Materials and Methods
Clinical Data and Pathology
Forty-three patients from the surgical pathology database of a single
institution who had a diagnosis of metaplastic breast carcinoma from January
1995 to June 2005 and who had undergone preoperative imaging with mammography
or sonography were included in this study. A second study group comprised 43
patients with invasive ductal carcinoma from the same surgical pathology
database diagnosed during the same time period who were matched to the
patients with metaplastic carcinoma by tumor T stage (size) and who also had
breast imaging available for review. Tumors in seven patients were classified
as stage T1 (< 2 cm), in 34 patients as stage T2 (> 2 cm and < 5 cm),
and in two patients as stage T3 (> 5 cm) in each group. A total of 21,037
patients were diagnosed with invasive ductal carcinoma during this period.
Information about histopathologic features was obtained from pathology
reports or, for selected cases requiring clarification of the pathology
findings, through review of H and E–stained slides by one of two
dedicated breast pathologists and one breast pathology fellow. The clinical
charts were reviewed by a senior medical oncology fellow to collect
information on tumor stage, estrogen and progesterone receptor status,
HER2/neu status, and clinical follow-up. The clinical and pathologic
tumor stages were determined using the sixth edition of the cancer staging
manual of the American Joint Committee on Cancer
[10].
Imaging
Mammography—Mammography was performed using a Lorad M3
(Hologic) or a DMR series mammography unit (GE Healthcare). Standard two-view
diagnostic mammography was performed, with additional views as deemed
necessary. Two mammographers with 3 and 10 years' experience in breast imaging
reviewed all available mammograms and sonograms. These reviews were done
independently and without knowledge of the clinical and pathologic findings.
Agreement as to the presence or absence of findings was by consensus. Breast
parenchymal density was classified according to the American College of
Radiology BI-RADS classifications
[11]. Mammograms were reviewed
for focal masses, calcifications, asymmetric density, architectural
distortion, and associated features such as skin thickening and retraction,
nipple retraction, and axillary lymphadenopathy.
Sonography—Real-time gray-scale sonography and color Doppler
sonography were performed using an Elegra unit (Siemens Medical Solutions) by
an attending radiologist who was one of a group of 10 radiologists (including
two of the authors) assigned to breast sonography. Sonograms were assessed for
masses (solid or cystic) and their shapes, margins, echo patterns, posterior
acoustic features, calcifications, vascularity determined by color Doppler
imaging, and effects on surrounding tissue, according to the BI-RADS
sonography lexicon [12,
13] as determined by the two
mammographers. Disease was also assessed as unifocal, multifocal, or
multicentric in all patients who underwent sonography. Sonographic assessment
of the regional lymph node basins, including the axillary, infraclavicular,
internal mammary, and supraclavicular regions, was documented according to
previously published criteria
[14,
15]. Whole-breast and nodal
basin sonography are routinely performed at our institution because most
patients present for staging of a known malignancy.
Statistical Methods
Mammography variables, including size, shape, margin, and density of masses
as well as morphology and distribution of calcifications, were recorded
according to BI-RADS criteria. Sonography variables recorded included mass
size, shape, margin, posterior acoustic phenomena, vascularity, and axillary
lymph node status according to BI-RADS criteria. Imaging features were
tabulated and compared between groups using Fisher's exact test, the chisquare
test, or Wilcoxon's rank sum test, as appropriate. Values for p are
not presented when there were fewer than five patients in a category;
p values of less than 0.05 were considered statistically
significant.
Results
Patients with metaplastic breast carcinoma were slightly younger than
patients with ductal carcinoma (p = 0.048). The median age for the
patients with metaplastic carcinoma was 46 years (range, 33–61 years)
compared with 53 years (range, 33–84 years) for those with ductal
carcinoma. The median size of metaplastic carcinomas was 3 cm (range,
1–10 cm) compared with 2.4 cm (range, 1–5 cm) for ductal
carcinomas. Thirty-seven (86%) of 43 patients with metaplastic carcinoma
presented with a palpable mass, compared with 34 (79%) of 43 with ductal
carcinoma.
Table 1 describes the
clinical and tumor characteristics of the 43 patients with metaplastic breast
carcinomas. Most metaplastic breast carcinomas were hormone
receptor–negative (estrogen receptor and progesterone receptor) (39/40,
97.5% and 33/38, 86.8%, respectively) and HER2/neu-negative (22/23,
95.7%; unknown in 20/43, 46.5%) compared with estrogen receptor and
progesterone receptor negativity rates of 25% (10/40) and 47.5% (19/40),
respectively, for ductal carcinoma, and HER2/neu negativity of 73.7%
(28/38; unknown in 11.6% [5/43]). Axillary lymph node disease was noted in
23.7% (9/38) of patients with metaplastic carcinoma compared with 47.5%
(19/40) of patients with ductal carcinoma, and axillary nodal status was
unknown in 11.6% (5/43) of patients with metaplastic carcinoma compared with
7.0% (3/43) of patients with ductal carcinoma.
The median follow-up was 47 months (range, 4–137 months). Four (9%)
of 43 patients were lost to follow-up, 27 (62.7%) are currently alive with no
evidence of disease, and 12 (27.9%) died. The cause of death was breast
carcinoma in 11 patients and concurrent lymphoma in one. A total of 17
recurrences were seen in 17 patients. Four of the recurrences were local, 12
were distant, and one was combined local and distant. The most common site of
metastatic disease was the lung (n = 10), followed by liver and bone.
The median time to recurrence was 12.5 months.
Table 2 shows the
mammography characteristics of metaplastic carcinomas. Mammography was not
performed in three patients with metaplastic carcinoma. Mammographically,
metaplastic carcinomas were more frequently round, oval, or lobular (Figs.
1,
2A,
2B,
3A,
3B,
4A,
4B,
5A,
5B) (84% vs 26%, p
< 0.0001) and more frequently showed circumscribed margins (Figs.
1 and
3A,
3B) (15% vs 1%, p =
0.001) than ductal carcinomas. Calcifications were more frequently noted in
ductal (51% vs 25%, p = 0.02) than in metaplastic carcinomas
(Fig. 1) and were more
frequently linear, pleomorphic, or heterogeneous in morphology (40% vs 77%,
p = 0.06) in ductal than in metaplastic carcinomas. Consistent with
the size distribution of tumors, overlying skin thickening (13%) was
relatively infrequent in this study because only three tumors were larger than
5 cm.
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Fig. 1 —Right mediolateral oblique mammogram shows lobular mass with
internal coarse calcifications (arrows) in 66-year-old woman who
presented with palpable mass. Final pathology showed invasive metaplastic
carcinoma with malignant chondroosseous neoplasm.
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Fig. 2A —54-year-old woman with palpable mass. Craniocaudad right
mammogram shows high-density round mass with partially indistinct margins
(long arrows) and partially circumscribed margins (short
arrows).
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Fig. 2B —54-year-old woman with palpable mass. Transverse sonogram
shows oval mixed solid and cystic mass (long arrow) with partially
indistinct margins showing posterior acoustic enhancement (short
arrows). Final pathology revealed spindle cell carcinoma most consistent
with sarcomatoid metaplastic carcinoma.
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Fig. 3B —55-year-old woman with palpable mass. Transverse sonogram of
same breast shows solid oval mass with microlobulated margins (long
arrow) and posterior acoustic enhancement (short arrows). Final
pathology showed high-grade invasive sarcomatoid carcinoma.
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Fig. 4A —52-year-old woman with palpable mass in left breast. Left
mediolateral oblique mammogram shows high-density lobular mass (long
arrows) with associated left axillary adenopathy (short
arrows).
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Fig. 4B —52-year-old woman with palpable mass in left breast. Color
Doppler transverse sonogram shows lobular circumscribed solid hypoechoic and
hypervascular mass (arrows). Final pathology revealed high-grade
invasive squamous cell carcinoma.
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Fig. 5A —63-year-old woman with palpable mass in left breast. Left
craniocaudad mammogram shows high-density round mass with partially spiculated
margins (arrows). Overlying marker denotes palpable mass.
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Fig. 5B —63-year-old woman with palpable mass in left breast.
Transverse sonogram shows irregular mixed solid and cystic mass (long
arrow) with mild posterior acoustic enhancement (short arrows).
Final pathology revealed sarcomatoid carcinoma with osseous metaplasia.
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Table 3 shows the
sonographic characteristics of ductal and metaplastic carcinomas. Sonography
was performed in 39 and 33 patients with invasive ductal and metaplastic
carcinoma, respectively. A typical malignant irregular shape was noted in 69%
of ductal versus 27% of metaplastic carcinomas (p = 0.001). Angular
margins were present in 49% of ductal versus 9% of metaplastic carcinomas.
Circumscribed and indistinct margins were more frequent in metaplastic than in
ductal carcinomas (55% vs 18%) (Fig.
4A,
4B). Posterior acoustic
shadowing was noted in 49% of ductal versus 9% of metaplastic carcinomas, and
posterior acoustic enhancement (Figs.
2A,
2B,
3A,
3B, and
5A,
5B) was noted in 18% of ductal
versus 67% of metaplastic carcinomas (p < 0.0001).
Discussion
Metaplastic carcinomas displayed more benign mammographic features in our
series and typically showed a round or oval mass with circumscribed margins
compared with invasive ductal carcinomas, which typically showed an irregular
shape and spiculated margins. A significantly lower frequency of
malignant-type pleomorphic, linear microcalcifications was observed in
metaplastic than in ductal carcinomas. These findings concur with previous
publications involving fewer patients
[16–20].
Sonographically, metaplastic carcinomas showed more benign features
characterized by an oval, round, or lobular solid hypoechoic mass with
circumscribed or indistinct margins in our series when compared with ductal
carcinomas. Metaplastic carcinomas frequently showed posterior acoustic
enhancement, whereas posterior acoustic shadowing was more frequently
associated with invasive ductal carcinomas. These combined mammographic and
sonographic features may lead to misinterpretation of metaplastic carcinoma as
a probably benign or a BI-RADS category 3 lesion
[11,
12], which could potentially
result in delayed diagnosis of carcinoma even if appropriately categorized and
evaluated. The differential diagnosis of an oval, round, or lobular solid mass
with circumscribed margins includes the triad of circumscribed carcinomas:
medullary, mucinous, and papillary carcinomas
[21–25].
Recent publications have described significantly more circumscribed malignant
noncalcified mammographic masses representing high-grade invasive carcinomas
in patients who have gene mutations than in the control group
[26,
27].
Metaplastic breast carcinomas presented at a younger age than ductal
carcinomas. However, this comparison of age between the two groups
(metaplastic and ductal carcinoma) is limited by selection bias because the 43
matched invasive ductal carcinomas represent a small fraction (
0.2%) of
the total number of ductal carcinomas ( 21,037) diagnosed during this
period. Some studies have found tumor size to be the most important
determinant of patient outcome, and tumors greater than 5 cm have the poorest
prognosis [2,
28]. The presenting symptom is
usually a palpable mass, as was the case in our series, in which 86% of
patients presented with a palpable breast mass.
Metaplastic breast carcinoma displays a biologic behavior different from
that of typical invasive ductal carcinoma. Metaplastic tumors tend to be large
at presentation, to be hormone receptor–and HER2/neu-negative,
and to have a low incidence of regional lymph node involvement
[5,
29]. The number of patients
with documented axillary nodal metastasis at the time of axillary nodal
dissection was 23.7% in our series. This figure is within the reported range
for metaplastic breast carcinoma
[30,
31] but is still lower than
the expected yield for invasive ductal carcinoma
[32] and the percentage of
axillary nodal involvement of 48.8% in the control group of ductal carcinomas
in this study. Metaplastic carcinomas have a greater tendency for early
hematogenous dissemination. These tumors have uncertain prognostic
significance. It has been suggested that metaplastic carcinomas have a worse
prognosis than typical ductal carcinomas
[9,
33], and that duration of
symptoms, TNM stage, tumor size, and axillary nodal status are significant
prognostic factors of survival
[34]. We postulate that the
poorer outlook associated with metaplastic carcinomas is the result of a
difference in biology that reflects morethe sarcomatoid than the epithelial
spectrum of tumor behavior; the sarcomatoid spectrum is associated with higher
hematogenous and lower lymphatic spread and higher hormone and
HER2/neu receptor negativity.
It is therefore incumbent on the breast imager to be aware of
more-benign-appearing mammographic and sonographic lesions that can represent
aggressive malignancies with poorer prognosis and overall survival
[9,
33,
34]. Awareness of this overlap
in the imaging findings between metaplastic carcinomas, invasive carcinomas in
patients who have oncologic genes, and probably benign lesions should prompt
timely biopsy and ancillary testing of the histologic specimens.
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Abstract
Introduction
