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Published online before print November 19, 2001, 10.1148/radiol.2221001471
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(Radiology 2002;222:165-170.)
© RSNA, 2001

Breast Imaging

Nonpalpable Breast Cancer: Mammographic Appearance as Predictor of Histologic Type1

Mercidyl Gelig Thurfjell, MD, PhD, Anders Lindgren, MD, PhD and Erik Thurfjell, MD, PhD

1 From the Department of Oncology, Radiology and Clinical Immunology, Section of Radiology, Uppsala University Hospital, SE-751 85 Uppsala, Sweden (M.G.T., E.T.); and Department of Pathology and Cytology, Central Hospital, Falun, Sweden (A.L.). Received August 30, 2000; revision requested October 18; final revision received May 8, 2001; accepted June 5. Address correspondence to E.T. (e-mail: erik.thurfjell@radiol.uu.se).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To investigate the association between mammographic appearance and histologic diagnosis of nonpalpable breast cancers.

MATERIALS AND METHODS: Mammographic characteristics of 317 consecutive clinically nonpalpable breast cancers in patients treated with breast-conserving surgery were reviewed. Malignant lesions were categorized as spiculated masses, other lesions, calcifications, and combined findings. Calcifications were characterized as amorphous, pleomorphic, or fine linear and branching. Logistic regression was used for the evaluation. Odds ratios (ORs) represent the magnitude of the association between a histologic diagnosis and a mammographic finding.

RESULTS: Spiculated mass without calcifications (n = 150) and calcifications alone (n = 79) accounted for three of four cancers. A spiculated mass without calcifications was strongly associated with invasive cancers (OR = 12). Calcifications alone were strongly associated with ductal carcinoma in situ (DCIS) (OR = 19). In a decreasing order, the following invasive cancers were each associated with spiculated lesions without calcifications: ductal carcinoma grade 1 (OR = 28), ductal carcinoma grade 2 (OR = 17), lobular carcinoma (OR = 11), and ductal carcinoma grade 3 (OR = 4.6). Fine linear and branching calcifications alone were associated with not only DCIS nuclear grades 3 (OR = 17) and 2 (OR = 9.7) but also with invasive ductal carcinoma grade 3 (OR = 13).

CONCLUSION: Mammographic appearance can be a predictor of histologic diagnosis in three of four nonpalpable breast cancers.

Index terms: Breast neoplasms, calcifications, 00.81, 00.813 • Breast neoplasms, diagnosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Screening mammography is used to detect breast cancer before it is clinically detectable. The radiologist who performs screening mammography, therefore, must be familiar with the wide range of mammographic findings of breast cancer in the preclinical phase. Because breast cancer often possesses intratumor heterogeneity (1), mammographic patterns of breast cancer have a wide range of variations. Correlation of mammographic and pathologic findings, however, has shown that certain histologic types of breast cancer have the propensity to manifest in characteristic mammographic patterns (1–6). The value of inferring on the histopathologic findings of a mammographically malignant lesion is in its potential influence on the therapeutic approach and management (7).

Logistic regression has been used sparingly in the analysis of mammographic characteristics in nonpalpable breast lesions. Ciatto et al (5) analyzed the mammographic characteristics of 1,182 nonpalpable breast lesions, and 548 of them were malignant. They found that stellate opacities and those with irregular contours have a significantly increased risk of being malignant compared with masses with smooth contours and that microcalcifications were likewise significantly associated with malignancies but to a lesser degree. Harkins et al (8) investigated the mammographic characteristics and demographic risk factors in a series of patients with 471 nonpalpable breast lesions that included 132 malignancies. In this latter series, masses with irregular contours were significantly associated with malignancy, and two-thirds of these were ductal carcinoma in situ (DCIS). They also found that when masses were malignant, those with a smooth contour were invasive in four of five cases.

The purpose of this study was to investigate the mammographic characteristics of the different histologic types of preclinical breast cancer with logistic regression analysis and to determine the potential use of these characteristics in predicting the histologic diagnosis of nonpalpable breast cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The study included a consecutive series of 320 cases of clinically nonpalpable breast cancers in patients treated with breast-conserving surgery. The cases were from a database at the screening center of Uppsala University Hospital, Sweden, from February 1988 to August 1994. Cases were in women 33–87 years old, with a median age of 61 years. A total of 281 cases were detected at screening mammography, and 39 cases were diagnosed at clinical mammography. The screening program has been described in detail elsewhere (9). Sector resection and axillary dissection were routinely performed for invasive cancers. The axilla was not explored in women with carcinoma in situ or in women with poor physical condition. Preoperative hook-wire localization procedures were performed, and radiography of the excised specimens was performed before histologic examination.

A total of 310 cancers had been prospectively examined by the pathologist (A.L.). The grading system for the invasive adenocarcinomas proposed by Elston and Ellis (10) was used. The cancers were histopathologically categorized as follows (2): DCIS nuclear grade 1–3; invasive ductal carcinoma (including tubular carcinoma) grade 1–3; and lobular carcinoma and a miscellaneous group including colloid, medullary, and adenoid cystic cancers. Three women had metachronous bilateral breast cancers. Two cytologically proved but histologically unverified cancers and one invasive cancer not investigated by the pathologist author were excluded. Thus, the study material consisted of 317 clinically nonpalpable breast cancers. However, seven cases of DCIS were excluded in the analysis of the predictability of the different grades of DCIS, since the tumors had not been examined by the pathologist author, and nuclear grading information was lacking.

One of the authors (M.G.T.) retrospectively reviewed the screening and diagnostic mammograms, including the magnification views, and radiographs of the specimens in these 317 breast cancers. The mammographic criteria described by Tabar and Dean (11) were used for mammographic classification. These criteria are translatable to the Breast Imaging Reporting and Data System, or BI-RADS, mammographic classification system of the American College of Radiology (12).

The malignant lesions were categorized as follows: spiculated masses, other lesions with well- or ill-defined margins, calcifications, spiculated mass with calcifications, and other lesions with calcifications. Classification of masses as spiculated was performed in a strict manner, with adherence to the definition of a spiculated mass as a central nidus with marginal spicules. The presence of only one or two spicules was not enough of a basis on which to classify a lesion as spiculated; these lesions and all irregular masses, round masses, architectural distortions, asymmetric densities, and neodensities were classified as other lesions.

Calcifications were further characterized on the basis of whether they were amorphous (powdery), pleomorphic (granular), or fine linear and branching (casting) (12). In cases where there were combined calcification morphologic features, the predominant pattern was recorded. When at least one fine linear or branching calcification was present, the calcification was classified as fine linear and branching. Only the calcifications that were within, at least partially straddling, or in the immediate vicinity of an associated noncalcified lesion were accounted for in the categorization of cases where there were combined findings. The largest diameter of the lesion was measured. In cases of spiculated masses, only the central solid nidus was measured, and the marginal spicules were excluded. Likewise, the calcifications in the immediate vicinity of an associated noncalcified lesion in a combined finding were included in the measurement.

To determine the predictability pattern of the different mammographic findings for a specific histologic diagnosis, logistic regression analysis with statistical software (STATVIEW 5; SAS Institute, Cary, NC) was performed. In the estimation of the odds ratio (OR), we used the histologic diagnoses as the explanatory (independent) variables and the mammographic findings as the outcome (dependent) variables. For the outcome variables, we chose one of the mammographic findings as the reference group for the other findings to determine their maximum likelihood of being used to predict a specific histologic diagnosis. Thus, the ORs represent the magnitude of the association between a specific histologic diagnosis and a specific mammographic finding, compared with the other mammographic findings combined, given that the histologic diagnosis was a malignancy.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The frequency of mammographic findings categorized according to histopathologic diagnoses is graphically demonstrated in the Figure. The predominant findings were spiculated masses and calcifications alone, which accounted for 150 (47%) and 79 (25%), respectively, of 317 lesions. In spiculated masses without calcifications, invasive breast cancer accounted for 143 (95%) of 150 cases (Table 1). Invasive ductal carcinoma grades 1 and 2 was the predominant histologic diagnosis in this group, and this tumor accounted for 49 (33%) and 56 (37%), respectively, of 150 cases. DCIS accounted for 50 (63%) of 79 diagnoses in the group with calcifications as the sole finding but accounted for 15% or less in the other groups of mammographic findings (Table 1). There were no invasive lobular carcinomas manifesting as calcifications in this study. Cancers in the miscellaneous group did not manifest as calcifications, either alone or associated with a noncalcified lesion. Invasive lobular carcinoma manifested as spiculated masses with or without calcifications in 22 (81%) of 27 cases. Invasive ductal carcinoma grade 3 showed a complex distribution of findings. Axillary lymph node metastasis was found in 26 cases, which corresponded to 25 (8%) of 317 cancers or 26 (12%) of 219 invasive breast carcinomas examined with lymph node sampling (Table 1). The median diameter of all lesions was 13 mm, with a range of 3–125 mm (Table 2).



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  		Figure 1. Diagram shows mammographic findings according to histologic diagnosis. Spiculated masses, other lesions, calcifications only, and combined findings are stratified according to histologic diagnosis. CALC = calcifications, IDC = invasive ductal carcinoma (1, 2, and 3 = grades 1, 2, and 3, respectively), LOB = invasive lobular carcinoma, MISC = miscellaneous cancer group, ROUND = rounded, SPIC = spiculated.

 

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  		TABLE 1. DCIS and Axillary Lymph Node Status in Invasive Breast Cancer according to Finding

 

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  		TABLE 2. Median Size and Size Range for Different Findings Measured on Mammograms

 
Just as invasive carcinoma was strongly associated with spiculated masses, so too was DCIS associated with calcifications alone when histologic diagnosis was used as a dichotomized variable (Table 3). An invasive breast cancer had a 12 times greater chance to manifest as a spiculated mass without calcifications than it had of manifesting as other findings combined. Likewise, DCIS showed a 19 times greater chance to manifest as calcifications alone than it had of manifesting as the other findings. When the group of calcifications alone was subcategorized into amorphous, pleomorphic, or fine linear and branching, the association with DCIS was greatest for the amorphous calcifications (OR = 31) and smallest for the fine linear and branching type (OR = 3.6).


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  		TABLE 3. Association between Mammographic Findings and Breast Cancer

 
We found several significant observations after subcategorizing the histologic diagnoses of the invasive breast cancers (Table 4). In a decreasing order, invasive ductal carcinoma grade 1 (OR = 28), invasive ductal carcinoma grade 2 (OR = 17), invasive lobular carcinoma (OR = 11), and invasive ductal carcinoma grade 3 (OR = 4.6) each were significantly associated with spiculated masses without calcifications. The miscellaneous group (OR = 25) was strongly associated with the findings of other lesions without calcifications. Invasive lobular carcinoma (OR = 4.6) was the only histologic type that was significantly associated with a spiculated mass with calcifications. As expected, DCIS was strongly associated with calcifications as the sole finding (OR = 38) when invasive ductal carcinoma grade 1 was used as the reference. Also, invasive ductal carcinoma grade 3 (OR = 5.7) was significantly associated with calcifications alone.


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  		TABLE 4. Association between Mammographic Findings and Malignant Histologic Diagnoses

 
Subcategorization of calcifications gave important information. We found that DCIS of nuclear grade 1 (OR = 69) was more strongly associated with amorphous calcifications compared with DCIS of nuclear grades 2 (OR = 31) and 3 (OR = 19) (Table 5). There were no differences in the strength of association for the different nuclear grades of DCIS with the pleomorphic type of calcifications. DCIS of nuclear grades 3 (OR = 17) and 2 (OR = 9.7) was significantly associated with fine linear and branching calcifications but so was invasive ductal carcinoma grade 3 (OR = 13). There were no cases of low-nuclear-grade DCIS that manifested with the fine linear and branching pattern of calcifications in this study. Subcategorization of the calcifications in the groups with combined findings provided no significant associations.


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  		TABLE 5. Association between Different Types of Calcifications and Malignant Histologic Diagnoses

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The findings in our study should be interpreted in the context of whether the radiologist can offer certain prebiopsy histologic predictions when he or she encounters nonpalpable mammographic malignancies. Three of four nonpalpable breast cancers in our series manifested as either spiculated masses or calcifications as the mammographic finding. A spiculated mass without calcifications was strongly associated with an invasive cancer and was likely to be invasive ductal carcinoma grade 1 or 2. The finding of calcifications alone was strongly associated with DCIS, but invasive ductal carcinoma grade 3 was an important differential diagnosis when calcifications were fine linear and branching. We recommend caution in predicting the histologic diagnosis for the other types of findings that represent the remaining one-fourth of the cancers. The histologic predictions would be accurate in seven of eight cases in our study (Table 6). Predictions in the subgroup manifesting as pleomorphic calcifications would be the weak spot, because 16 (59%) of 27 of the incorrect predictions were made in this subgroup.


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  		TABLE 6. Prediction of Histologic Diagnosis in Nonpalpable Breast Cancers on the Basis of Mammographic Findings

 
Our study has certain limitations. Since the study was confined to only patients who underwent breast-conserving surgery and who had histologically proved cancers, the predictive value for breast cancer with different characteristics was not evaluated. The characteristics of the cancers, such as multifocal cancer and extensive DCIS, in patients who underwent mastectomy have not been accounted for. From other studies, we know that the positive predictive value for malignancy of nonpalpable lesions varies from 19% to 53% (5,8,13–17). High positive predictive values for breast cancer have been reported (17) for spiculated masses (94%) and fine linear and branching calcifications (83%). On the other hand, it is well-known that amorphous (powdery) calcifications have a decreased positive predictive value, and these findings are considered to be of intermediate concern by the American College of Radiology (12). Likewise, noncalcified lesions with circumscribed margins are much less likely to be malignant than those with ill-defined margins. We chose, however, not to subcategorize the group of other lesions because of the relatively small number of cases in this group. We included three cases of pure architectural distortion in the group of other lesions. Fourteen cancers were isodense to surrounding benign fibroglandular tissue, while 22 cancers were of relatively increased density. Five of the 14 isodense cases were neodensities.

It is possible that in some of our categorized cases with combined findings, one of the findings might have represented a benign tumor adjacent to a malignancy. For example, a spiculated mass could have represented a radial scar (18) in proximity to malignant calcifications. Likewise, calcifications representing a DCIS or a benign tumor could be adjacent to an invasive cancer manifesting as a noncalcified lesion or in some instances could have been a mammographically occult lesion.

Spiculated masses accounted for almost half of the nonpalpable malignant lesions in our study, which included a larger number of these masses than were included in other series. Approximately one of three cancers (29%–36%) was a spiculated mass in three studies (13,16,17), and spiculated masses accounted for only 21% of cancers in a larger series (5). Among the invasive cancers in our series, both the invasive ductal and lobular carcinomas manifested as pure spiculated masses. Ciatto et al (5) likewise observed that tubular cancers were more significantly associated with stellate opacities than the average in their study. Our findings and those of Ciatto et al that nonpalpable spiculated masses were predominantly invasive cancers are contrary to the observations made by Harkins et al (8), who suggested that masses with irregular contour were predominantly DCIS.

In our series, we found that 25% of our cases manifested as calcifications, which is in concordance with findings of Rissanen et al (16) but lower than the 35%–58% reported in other series (5,8,13–15, 17,19). These differences are, most likely, largely due to the limitation of our cases to cancers treated with breast-conserving surgery, thus excluding cases with widespread DCIS. Another explanation may be that we found more spiculated cancers before they became palpable or that we missed some malignant calcifications.

The spiculated masses had a smaller median size compared with all other types of findings and a smaller ratio of lymph node metastasis than all other findings with the exception of the calcification group (Tables 1, 2). Therefore, we do not believe that the increased ratio of spiculated masses in our series can be attributed to initially missing small nonspiculated lesions and to detecting them subsequently when they acquired spicules. In earlier studies, such as that by Sickles (19) in which mammograms obtained in 1976–1984 were used, the ratio of spiculated masses was lower compared with that in our study. This difference probably can be explained in part by the progress in mammographic technique (20), since in our study, the mammograms were performed in 1988–1994 and were developed through the extended processing cycle. Our ratios of different mammographic findings agree with those in studies of breast cancer cohorts that were based on population-based screening, which included palpable and nonpalpable cancers (1,21).

We found that fine linear and branching calcifications were significantly associated with invasive ductal carcinoma grade 3 and DCIS. Likewise, Ciatto et al (5) reported that DCIS per se and invasive comedo cancers with an extensive intraductal component were associated with calcifications. Evans et al (22) attributed the presence of fine linear and branching calcifications representing DCIS to the detection of small grade 3 invasive cancers. The prognosis for patients with this group of invasive cancers is worse than for those with other types of invasive cancers smaller than 15 mm (23).

Amorphous (powdery) calcifications were primarily seen among the low-nuclear-grade DCIS in our study. Holland et al (2) described the amorphous calcifications among the solid type of well-differentiated DCIS. The pleomorphic (granular) pattern of calcifications did not demonstrate a significant predictable mammographic distribution among the cases of DCIS. Although pleomorphic calcifications were found in well-differentiated DCIS (3), they occurred more frequently among the intermediate- and high-nuclear-grade carcinomas (4). Stomper and Connolly (24) observed an overlap in the association of pleomorphic calcifications between the comedo and the noncomedo subtypes of DCIS, with an almost equal occurrence of 47% and 53%, respectively.

When logistic regression analysis is used, the choice of the reference group is an important factor in the analysis, and it must be determined with care. The reference group should be chosen so that the risk ORs make sense when the results are interpreted. We derived the dichotomized analysis of DCIS versus invasive cancer naturally. When we subcategorized the histologic diagnoses, we used several alternative reference groups but concluded that the reference groups noted in Tables 4 and 5 were the most reasonable to choose. However, we used different reference groups to show the association between different types of calcifications and malignant histologic diagnoses (Table 5), because of the limited number of invasive cancers in amorphous calcifications and the limited number of cases of invasive ductal carcinoma grade 1 associated with fine linear and branching calcifications.

To summarize, we established that the mammographic appearance was a predictor of histologic diagnosis in three of four nonpalpable breast cancers in this study. A spiculated mass without calcifications was very likely an invasive breast cancer, whereas calcifications were strongly associated with DCIS; invasive ductal carcinoma grade 3 was an important differential diagnosis when the calcifications were fine linear and branching. In Sweden, patients with a cytologically proved nonpalpable breast cancer that does not manifest as calcifications alone often undergo breast-conserving surgery with simultaneous axillary dissection after they provide informed consent. Our results indicate that this practice should be limited to spiculated masses without calcifications to reduce the number of unnecessary axillary dissections that are performed.

Although certain mammographic features of nonpalpable breast cancer are strongly predictive of specific histologic diagnoses, these features may not be sufficiently predictive to guide subsequent treatment decisions. The radiologist should continue to recommend tissue diagnosis as the standard whenever cancer treatment decisions must be made. Therefore, it is self-evident that histologic diagnosis (on the basis of percutaneous or surgical biopsy findings) usually is required to make proper decisions concerning cancer treatment.


   FOOTNOTES
 
Abbreviations: DCIS = ductal carcinoma in situ, OR = odds ratio

Author contributions: Guarantors of integrity of entire study, M.G.T., E.T.; study concepts, E.T.; study design, M.G.T., E.T.; literature research, M.G.T., E.T.; clinical studies, M.G.T., E.T.; data acquisition and analysis/interpretation, M.G.T., A.L., E.T.; statistical analysis, E.T.; manuscript preparation and definition of intellectual content, M.G.T., E.T.; manuscript editing, M.G.T.; manuscript revision/review and final version approval, M.G.T., A.L., E.T.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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