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1 Department of Diagnostic Radiology and Organ Imaging, Faculty of Medicine, The
Chinese University of Hong Kong, Prince of Wales Hospital, Ngan Shing St.,
Shatin, New Territories, Hong Kong.
2 Department of Anatomical and Cellular Pathology, The Chinese University of
Hong Kong, Prince of Wales Hospital, Hong Kong.
Received July 9, 2003;
accepted after revision October 9, 2003.
Address correspondence to W. W. M. Lam.
Abstract
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MATERIALS AND METHODS. Two radiologists analyzed the mammographic and sonographic features of 33 mucinous carcinomas. Mammographic features according to the Breast Imaging Reporting and Data System (BI-RADS) and sonographic features were recorded and analyzed. The imaging features of the mass were correlated with the nuclear grade and mucin content of these 33 mucinous carcinomas. The incidence of axillary lymph nodes metastasis in different histologic grades and their detection by imaging were also assessed.
RESULTS. As many as 21.2% (7/33) of mucinous carcinomas could not be detected mammographically. When they were detected mammographically, more than 92% of the tumors presented as a mass, either oval or lobular. Microlobulations were present in 38.5% of these lesions. The margin of the lesion as seen on mammography can be used to predict the histologic grade. A circumscribed margin was associated with a favorable histologic grade (p = 0.01), whereas an indistinct margin was more commonly associated with the mixed type of lesion (p = 0.05). Sonographically, mixed cystic and solid components, distal enhancement, and microlobulated margins were commonly found in mucinous carcinomas, with an incidence of 37.5%, 43.8%, and 56.3%, respectively. Homogeneity on sonography was associated with the pure type of mucinous carcinoma and hence a better prognosis. Sonography showed a sensitivity of 50%, specificity of 89%, positive predictive value of 60%, negative predictive value of 84%, and accuracy of 79.2% in the detection of axillary lymph node metastasis.
CONCLUSION. Both sonographic and mammographic assessments are important in the correct diagnosis of mucinous carcinoma, the prediction of histologic grade, and the prognosis of the tumors.
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Histologically, mucinous carcinoma can be divided into pure mucinous carcinoma and mixed mucinous carcinoma, depending on the mucinous content of the carcinoma. Pure and mixed mucinous carcinomas have different prognoses. Pure mucinous carcinoma is reported to be associated with a better prognosis [3] and a lower incidence of axillary lymph node metastasis [4].
Differentiation of mucinous carcinomas into pure and mixed types by their mammographic features has been described in the literature [1, 2, 4, 5]. However, there is little in the literature reporting the sonographic features in a large series of mucinous carcinomas. The role of sonographic features in correlation with pathologic findings has not been assessed [1].
Mucinous carcinomas can also be classified by their nuclear grade, which also has prognostic significance. Little exists in the literature on the correlation of mammographic and sonographic findings with nuclear grade.
In this study, we report the sonographic features of 33 pathologically proven mucinous carcinomas (diagnosed at 16-gauge needle biopsy, excisional biopsy, or mastectomy). We correlated both the mammographic and sonographic features with different histologic parameters.
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Mammographic Findings
We reviewed the images of all patients with mucinous carcinoma diagnosed at
fine-needle aspiration. Mammography in two standard imaging planes
(mediolateral oblique and craniocaudal) was performed using dedicated
film-screen mammographic equipment (Senographe DMR, General Electric Medical
Systems). Magnified and compression views were also available for analysis in
18 patients.
Mammographic films were reviewed independently by two radiologists. Any discrepancy was resolved by consensus. Both of these radiologists were fully qualified and had more than 7 years of experience in interpreting mammography. The radiologists were informed of the fine-needle aspiration result but not the histologic nodal status or the number, site, size, or histologic grade of the breast lesions. The mammographic findings were reported according to the Breast Imaging Reporting and Data System (BI-RADS) [6]: presence of a mass; the shape of the mass (round, oval, lobular, or irregular); calcification (benign, intermediate, or higher probability); and the margin characteristics (circumscribed, microlobulated, obscured margin, indistinct, or spiculated) were noted.
Sonographic Findings
All patients underwent breast sonography, which was performed using a
10-MHz linear array transducer with the VST Master's Series (Diasonics). The
examinations were performed by one of six attending radiologists who were all
fully qualified, with more than 2 years' experience in interpreting
mammography. The attending radiologist performed the sonographic examination
after mammography, and correlation with the mammographic results was possible
during the examination. The dimensions of all identified lesions were
measured. All lesions underwent color Doppler sonography and the images were
saved. All axillary lymph nodes, normal or abnormal, that had been identified
were imaged.
All the hard-copy films were reviewed and the sonographic features were recorded independently without reference to the mammographic findings. Again, any discrepancy in opinion was resolved by consensus. When a mass was present, the following features of the mass were evaluated: its maximum dimension, shape (oval, round, lobular, irregular), margin (microlobulated, indistinct, obscured, spiculated, circumscribed), echogenicity (hypoechoic, complex mass with solid and cystic components, heterogeneous, isoechoic), and acoustic features (shadowing, enhancement). The presence of vascularity was also retrospectively reviewed. The number of vessels present and the location (central or peripheral) of the vessels were recorded.
Any axillary lymph nodes recorded on hard-copy films were analyzed. Axillary lymph node metastasis was diagnosed when the lymph nodes appeared round rather than oval (with a long axis–to–short axis ratio of < 1.5), when there was loss of the echogenic hilum, or when central necrosis was present.
Histologic Findings and Analysis
All the histologic and cytologic slides of these patients were retrieved
and reviewed independently by two pathologists. For histology, all the
materials were fixed in formalin and routinely processed, and the 4-µm
sections were stained with H and E.
The percentage by volume of extracellular mucin was calculated in each
tumor mass. The mucin-containing carcinomas were then separated into two
categories: pure mucinous (
90% mucin) and mixed mucinous (< 90%
mucin). Nuclear grade of tumors cells was also assessed and classified as
grade 1, 2, or 3, with grade 1 nuclei showing low-grade features and grade 3
nuclei showing a high degree of pleomorphism
[7]. In cases treated with
mastectomy and axillary sampling and dissection, the total number of lymph
nodes sampled and the number of nodes having positive findings were recorded.
The presence or absence of associated ductal carcinoma in situ was also
assessed.
Statistical Analysis
All results were analyzed with the SPSS version 10.0 (Statistical Package
for the Social Sciences) for Windows (Microsoft). Statistical significance of
age distribution and tumor size in different histologic groups was calculated
using the Student's t test. Statistical significance for the number
of axillary lymph nodes with metastasis in different histologic groups was
calculated using the chi-square test with a two-by-two contingency table.
Statistical significance for the number of patients with nodal metastases and
the presence of each mammographic and sonographic feature in different
histologic groups was calculated using Fisher's exact test. Two-tailed
probability values of less than 0.05 were considered significant.
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Because the lesions were chosen from pathologic review and not from imaging findings, as many as 21.2% (7/33) of the mucinous carcinomas could not be detected on mammography, and five of these tumors were clinically nonpalpable. On sonography, six of these lesions (maximum dimension, 0.9–2 cm) were detected. When the lesion was mammographically detectable, mucinous carcinomas commonly presented as a mass, either oval or lobular (24/26, 92.3%), with a circumscribed or a microlobulated margin (18/26, 69.2%) (Figs. 1A, 1B and 2A, 2B). Circumscribed margins were found only in pure mucinous carcinoma (8/16, 50%), whereas indistinct margins were more commonly found in the mixed type (n = 4) than in the pure type (n = 1) (Fisher's exact test, p = 0.05).
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When the mucinous carcinomas were classified according to nuclear grade, none of the mammographic features showed any association with nuclear grade. Microcalcifications were present in only four tumors, including the tumor with associated ductal carcinoma in situ. The microcalcifications in the other three tumors were incidental benign findings and did not contribute to the characterization of the tumor type.
Sonographic Findings
Ninety-seven percent of the mucinous carcinomas (32/33) presented as a mass
on sonography. Microlobulation was more commonly shown on sonography than
mammography and was detected in 56.3% (18/32) of the tumors.
Mucinous carcinomas presented as a homogeneous mass in 18.8% (6/32) of cases, either isoechoic or hypoechoic to the subcutaneous fat. Up to 37.5% (12/32) of all sonographically detected lesions presented as a complex mass with solid and cystic components. Distal acoustic enhancement was identified in 14 (43.8%) of 32 lesions. None of the tumors with less than 40% mucin content (n = 3) showed any distal enhancement. For tumors with 50% or more mucin content, up to 46.7% (14/30) showed distal acoustic enhancement. Vascularity (4.2 ± 2.6 vessels) was noted in 11 tumors in both the periphery and the center of the lesion.
With regard to predicting histologic grade using sonographic features, homogeneity was found only in pure mucinous carcinoma (Fisher's exact test, p < 0.01). An irregularly shaped mass was more commonly found in grade 2 tumor (Fisher's exact test, p = 0.04).
Sonography revealed abnormal axillary lymph nodes in five patients. Sonography showed a sensitivity of 50%, specificity of 89%, positive predictive value of 60%, negative predictive value of 84%, and accuracy of 79.2% in the detection of axillary lymph node metastasis. The sonographic results are given in Tables 3 and 4.
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Histologic Findings
On the basis of the mucinous content, 20 (60.6%) of 33 lesions were
classified as pure mucinous carcinoma; the remaining 13 (39.4%) of 33 tumors
were classified as mixed mucinous carcinoma.
On the basis of the nuclear grade, 24 (72.7%) of 33 tumors were classified as grade 1, nine (27.3%) of 33 were classified as grade 2, and none of these tumors was grade 3. Patients with grade 2 tumors were statistically younger than patients with grade 1 tumors (Student's t test, p = 0.02). No significant difference was seen in the age distribution of patients between the pure and mixed types of mucinous carcinoma (Student's t test, p = 0.85).
Maximum dimension of the tumors ranged from 0.3 to 10 cm. No significant difference was seen in the size of the tumors in relation to mucinous content (Student's t test, p = 0.12) or nuclear grade of the tumors (Student's t test, p = 0.16). Twenty-four patients underwent mastectomy, with 424 axillary lymph nodes sampled. Six patients (37 nodes) had axillary nodal metastases. Whether a mucinous carcinoma was of the mixed or the pure type was not predictive of the incidence of axillary lymph node metastasis (Fisher's exact test, p = 0.36). However, a significant difference was seen in the number of lymph nodes having nuclear grade 1 (n = 6) and those having nuclear grade 2 (n = 31) (chi-square test, p < 0.01). Only one patient in our series was found to have associated ductal carcinoma in situ.
Details of age distribution, tumor size, and the axillary lymph node status are shown in Table 5.
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Sonographic Findings
Few data are available for the sonographic appearance of mucinous
carcinoma. We have adopted a sonographic classification of the mass similar to
the BI-RADS classification used in mammography. We assessed the sonographic
features that might suggest the correct diagnosis and correlated them with
histologic grade. In the series of Markopoulos et al.
[9], of 1,510 new breast
cancers, only 18 cystic carcinomas were diagnosed. Ten of these carcinomas
were intracystic papillary carcinoma, one was a mucinous carcinoma, and seven
were cystic degeneration of ductal carcinoma. In our series, 36.4% of lesions
(12/33) presented as a complex mass with cystic and solid components, which is
an unusual feature in invasive ductal carcinoma. The presence of cystic
components in a mass in an older patient should therefore raise the suspicion
of mucinous carcinoma.
Previous articles have reported the sonographic appearance of mucinous carcinoma in small groups of patients. Most lesions were hypoechoic [1, 10]. Of these lesions, 37.5–71% showed distal enhancement [1, 10]. Memis et al. [11] showed that echogenicity might be used to predict the histologic type because isoechoic masses were found in pure mucinous carcinoma, whereas hypoechoic masses were found in mixed mucinous carcinoma.
To our knowledge, we have presented the largest series of mucinous carcinomas with sonographic findings. More than one third of the mucinous carcinomas presented as complex masses with cystic and solid components. Distal enhancement was another common sonographic feature of mucinous carcinoma. This feature was probably the result of the high water content and transmission of the ultrasound beam through the mucin and was therefore more commonly found in tumors with a high mucin content. These anechoic areas are not truly cystic but represent mucin with floating malignant cells. Vascularity was also found in about a third of the tumors, although the pattern and number did not show any association with the histologic type. We therefore suggest that sonographic depiction of a complex mass with cystic and solid components, vascularity, and distal enhancement in older women should raise a strong suspicion of mucinous carcinoma. We also showed that the sonographic appearance might provide a clue to the histologic classification and thus to the prognosis. Pure mucinous carcinoma may present as a homogeneous lesion, either hypoechoic or isoechoic relative to the subcutaneous fat layer. However, none of the mixed mucinous carcinomas presented as a homogeneous mass.
Cardenosa et al. [2] reported that associated ductal carcinoma in situ was found in as many as one third of patients; however, the incidence was much lower (3.3%) in our series. No specific reason accounts for the observation. Racial difference might be a contributing factor because all of the patients in our group were Chinese.
The diagnosis of mucinous carcinoma in most patients who present with a palpable breast mass could be made by fine-needle aspiration [12]. It might occasionally be difficult to differentiate fibrocystic changes and mucous-containing tumors from mucinous carcinoma at fine-needle aspiration. Imaging-guided core needle biopsy allows accurate histologic assessment [13, 14].
Age Distribution, Tumor Size, and Axillary Lymph Node Metastasis
Mucinous carcinoma predominantly affects older women. The mean age of our
patients was 64.3 years, which is comparable to the mean age in previous
reports [4,
15–17].
Patients with grade 2 tumors were statistically younger than patients with
grade 1 tumors. Age at presentation might therefore be an important prognostic
factor.
The mixed type of mucinous carcinoma might present as a large tumor [4, 18, 19]. However, our study and that of Paramo et al. [20] did not find a statistically significant difference in tumor size between the mixed and pure types.
The literature has shown that pure mucinous carcinomas are associated with a low incidence of axillary lymph node metastasis (0–12%) [4, 8, 20]. In our series, the incidence of axillary lymph node metastasis was much greater (36%) in the mixed group, although it was not statistically significant. The nuclear grade correlated with axillary lymph node status and might therefore be an important histologic classification for prognosis.
In our study, sonography showed a sensitivity of only 50% and an accuracy of 79.2% for the detection of axillary lymph node metastasis.
Conclusion
As many as 21.2% of mucinous carcinomas might not be detected
mammographically. Mucinous carcinoma commonly presents as a mass with
microlobulation on mammography and sonography. The presence of both cystic and
solid components and the presence of distal enhancement are important
sonographic features that might suggest the diagnosis. Imaging features, such
as an indistinct margin on mammography and an irregular shape on sonography,
are associated with tumors having a less favorable histologic grade. On the
other hand, a circumscribed margin on mammography and homogeneity on
sonography favor the pure type and a better prognosis.
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