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Multiple Bilateral Masses Detected on Screening Mammography

Assessment of Need for Recall Imaging

¹ Department of Radiology, University of California San Francisco Medical Center, Box 1667, San Francisco, CA 94143-1667.
² Present address: Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, 75 Francis St., Boston, MA 02115.

Received August 30, 1999; accepted after revision December 15, 1999.

 
Presented at the annual meeting of the American Roentgen Ray Society, New Orleans, May 1999.

Address correspondence to J. W. T. Leung.

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. When multiple bilateral partially circumscribed masses having a similar appearance are detected on screening mammography, some radiologists recommend recall examination to identify imaging features suggestive of malignancy that are not evident on standard screening views. This study assesses the need for such recall imaging.

SUBJECTS AND METHODS. Cases of multiple masses were identified by reviewing the mammographic reports of 84,615 consecutive screening examinations. Each case of multiple masses was prospectively interpreted as benign, with recommendations for follow-up mammography in 1 year and for aspiration of any palpable masses if clinically indicated. Subsequently diagnosed cancers were identified through data linkage with our regional tumor registry and through our institution's computer-based outcomes tracking system.

RESULTS. Among 84,615 consecutive screening examinations, we identified 1440 (1.7%) cases of multiple masses. Among the multiple-masses cohort, two interval cancers were found. Both were early-stage (T1bN0M0; T1cN0M0) and low-grade (histologic grade 1) cancers. The interval cancer rate among the multiple-masses cohort was 0.14%, which is somewhat lower than the age-matched United States incident cancer rate of 0.24%.

CONCLUSION. The frequency of cancer development and the stage at cancer diagnosis among nonrecalled cases of multiple masses are similar to those observed in the general screening mammography population. Therefore, recall imaging for women with multiple masses does not appear to be justified.

Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Multiple bilateral masses detected on screening mammography pose a distinct interpretative challenge. By multiple bilateral masses, we mean at least three masses, with at least one mass in each breast. To be considered partially circumscribed, at least 75% of the margins of a mass should be circumscribed, with the remaining margins obscured by adjacent fibroglandular tissue. No part of the margins may be indistinct or spiculated. The multiple masses must have a similar appearance in that not one of them can be substantially different from the others in terms of size, margin characteristics, or density.

It is unusual to encounter multiple bilateral partially circumscribed similar-appearing masses that represent malignancy (multifocal or multicentric breast cancer, metastases from extramammary sites, lymphoma) [1,2,3,4]. Rather, the multiple masses encountered in everyday practice mostly represent cysts or (less frequently) fibroadenomas [5, 6], both of which are benign. Furthermore, the few cases of multifocal or multicentric breast cancer usually are limited to one breast and also commonly display suspicious mammographic features, such as masses with poorly defined or spiculated margins (Fig. 1A,1B,1C,1D), widespread malignant-appearing microcalcifications, or both. Thus, many radiologists consider the finding of multiple masses to be benign, similar to the finding of numerous bilateral scattered similar-appearing microcalcifications.

View larger version (75K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —49-year-old woman with multicentric cancer in right breast. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple ill-defined and spiculated masses are seen in right breast (B and D), representing multiple foci of breast cancer. Note that masses are unilateral and each mass displays mammographic features suggestive of malignancy. Therefore, patient was recalled from screening and was not considered as multiple-masses case.

View larger version (86K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —49-year-old woman with multicentric cancer in right breast. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple ill-defined and spiculated masses are seen in right breast (B and D), representing multiple foci of breast cancer. Note that masses are unilateral and each mass displays mammographic features suggestive of malignancy. Therefore, patient was recalled from screening and was not considered as multiple-masses case.

View larger version (75K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —49-year-old woman with multicentric cancer in right breast. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple ill-defined and spiculated masses are seen in right breast (B and D), representing multiple foci of breast cancer. Note that masses are unilateral and each mass displays mammographic features suggestive of malignancy. Therefore, patient was recalled from screening and was not considered as multiple-masses case.

View larger version (68K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —49-year-old woman with multicentric cancer in right breast. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple ill-defined and spiculated masses are seen in right breast (B and D), representing multiple foci of breast cancer. Note that masses are unilateral and each mass displays mammographic features suggestive of malignancy. Therefore, patient was recalled from screening and was not considered as multiple-masses case.

However, sonography is advocated by other radiologists as the next step in the evaluation of multiple masses [7], primarily to identify the one mass that may be malignant among the multiple findings. Although sonography is highly accurate for making the benign diagnosis of simple cyst [8, 9], its reliability for characterizing solid breast masses remains controversial [10,11,12,13,14,15,16,17,18,19,20]. Some breast cancers have benign-appearing morphologic features, and other (especially small) malignancies are isoechoic to surrounding tissues and are thus sonographically occult. In addition, many sonographically indeterminate lesions are found to be benign at tissue diagnosis. Because of the high false-positive rate (and its associated cost and morbidity) as well as a moderate false-negative rate, the practice of bilateral whole-breast sonography is not the standard of patient care in the United States [21, 22].

The sonographic evaluation of multiple masses is further complicated by the inherent difficulty of correlating sonographic findings with the masses already identified on mammography. It is important to ensure that a given sonographic finding indeed represents a particular mammographic mass. In the clinical setting of multiple masses, this task is very challenging (often it is impossible) because of the multiplicity of masses, many of which are similar in size. Additional interventions, such as inserting needles into the breasts under sonographic guidance and then obtaining mammographic confirmation that the mammographic and sonographic lesions correlate with one another, are not only costly but also result in considerable added morbidity.

The use of fine-detail mammography with spot compression, magnification, or both techniques is also time-consuming as a supplement to mammographic screening unless this additional imaging is targeted at one mass that appears to have mammographic features different from those of all the others.

Radiologists have different opinions about the appropriate management of multiple masses. An evidence-based consensus regarding the need to recall women with multiple masses is desirable to establish a uniform standard of patient care. This issue also has important implications concerning the cost-effectiveness of screening mammography.

For many years we have interpreted the finding of multiple masses as benign, with recommendations limited to follow-up mammography in 1 year and aspiration of any palpable masses if clinically indicated. In this study, on the basis of our large-scale clinical experience, we assess the efficacy of this approach by determining the frequency, size, nodal status, and stage of cancers that develop among cases of multiple masses in a screening population.

Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
From April 1985 through December 1996, 84,615 mammographic screening examinations were performed on nominally asymptomatic women in our breast imaging practice. Among these consecutive screening examinations, those with multiple masses were identified by reviewing the mammography reports produced by the interpreting radiologists. Each case of multiple masses was prospectively interpreted as benign, regardless of whether previous examinations were available for comparison, with recommendations for repeat mammography in 1 year and aspiration of any palpable masses if clinically indicated. In the course of the study period, there were many interpreting radiologists, all of whom followed the same criteria when rendering the interpretation of "multiple bilateral partially circumscribed similar-appearing masses."

Because we perform screening mammography in a rapid throughput, batch-interpreted fashion, the mammograms are interpreted when the patient is no longer on-site, and we do not have access to our screening patients to perform physical examinations. Our screening population was nominally asymptomatic, meaning that neither the patient nor the referring clinician had indicated any symptoms or signs indicative of breast cancer. The decision to aspirate any palpable masses was made by the referring clinician, who was directed by our report to examine the patient again and base the decision on clinical criteria (both historical information and findings on physical examination), insofar as the radiologic features were benign.

In studies for which there were comparison examinations, interpretation was further classified into one of four categories: no interval change; one or more masses increased while one or more other masses decreased; more than one mass increased; and one or more masses decreased. Cases in which only one mass increased while all other masses remained stable were interpreted as requiring recall examination; these cases were not included in this study. Also not included in this study were cases of multiple bilateral masses in which one mass appeared different from the other masses (Fig. 2A,2B). These were cases in which one mass was disproportionately larger or denser, or its margins were significantly less-defined. Such cases were also interpreted as requiring recall examination. Finally, correlation with any palpable findings were recorded for all cases of multiple masses.

View larger version (107K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —49-year-old asymptomatic woman with several masses revealed on screening mammography. Mammogram of left breast in mediolateral oblique projection reveals several masses in upper aspect of breast.

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —49-year-old asymptomatic woman with several masses revealed on screening mammography. Photographic enlargement of upper aspect of left breast shows most masses to be partially or well-circumscribed. However, uppermost mass (arrow) stands apart from others in that its margins are spiculated. Patient was recalled for diagnostic imaging and subsequent imaging-guided biopsy. Invasive ductal carcinoma was diagnosed for uppermost mass.

We defined interval cancer in the multiple-masses cohort as any invasive carcinoma or ductal carcinoma in situ that was diagnosed within 1 year of the interpretation of multiple masses (we recommend repeat mammography in 1 year in all such cases), excluding cancers diagnosed as a result of our recommendation for aspiration (if clinically indicated) of masses palpable at the time of mammographic interpretation.

Subsequently diagnosed (interval) cancers were identified primarily by computer linkage with our regional Surveillance, Epidemiology and End Results (SEER) tumor registry, with linkage performed a minimum of 2 years after screening mammography. This delay between screening and linkage allows for the 1-year interval that we recommend between screening mammography in cases of multiple masses and for another year so that outcomes data from newly diagnosed cancers can be entered into the database of the tumor registry. In the past, such linkage and use of the computer-based outcomes tracking system at our own institution (also used in this study) have identified more than 95% of breast cancer cases in our catchment area [23].

Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
From our overall experience with 84,615 consecutive mammographic screening examinations performed on 40,419 women, we identified 1440 (1.7%) examinations with multiple masses among 907 (2.2%) women (Figs.3A,3B,3C,3D and 4A,4B,4C,4D). Table 1 indicates the distribution of multiple-masses examinations as a function of whether the masses showed stability or interval change when compared with a previous examination. Palpable findings that definitely correlated with a mammographic mass were found in 36 cases of multiple masses, and palpable findings that possibly correlated with a mammographic mass were identified in 21 cases. There were no palpable findings in the remaining 1383 cases.

View larger version (53K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —66-year-old asymptomatic woman with multiple masses revealed on screening mammography. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple partially or well-circumscribed masses are identified in all areas of both breasts. Masses appear similar to one another, and none display any mammographic features of malignancy. Findings strongly suggest that masses are benign.

View larger version (62K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —66-year-old asymptomatic woman with multiple masses revealed on screening mammography. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple partially or well-circumscribed masses are identified in all areas of both breasts. Masses appear similar to one another, and none display any mammographic features of malignancy. Findings strongly suggest that masses are benign.

View larger version (75K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —66-year-old asymptomatic woman with multiple masses revealed on screening mammography. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple partially or well-circumscribed masses are identified in all areas of both breasts. Masses appear similar to one another, and none display any mammographic features of malignancy. Findings strongly suggest that masses are benign.

View larger version (76K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3D. —66-year-old asymptomatic woman with multiple masses revealed on screening mammography. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple partially or well-circumscribed masses are identified in all areas of both breasts. Masses appear similar to one another, and none display any mammographic features of malignancy. Findings strongly suggest that masses are benign.

View larger version (93K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —59-year-old asymptomatic woman with multiple masses revealed on screening mammography. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple masses in this patient are smaller in size and fewer in number than those of patient depicted in Figure 3A,3B,3C,3D. Though imaging findings are less dramatic, multiple masses seen in this case are also partially or well-circumscribed, bilateral, and similar-appearing to one another. Thus, these masses are also likely benign.

View larger version (93K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —59-year-old asymptomatic woman with multiple masses revealed on screening mammography. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple masses in this patient are smaller in size and fewer in number than those of patient depicted in Figure 3A,3B,3C,3D. Though imaging findings are less dramatic, multiple masses seen in this case are also partially or well-circumscribed, bilateral, and similar-appearing to one another. Thus, these masses are also likely benign.

View larger version (84K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —59-year-old asymptomatic woman with multiple masses revealed on screening mammography. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple masses in this patient are smaller in size and fewer in number than those of patient depicted in Figure 3A,3B,3C,3D. Though imaging findings are less dramatic, multiple masses seen in this case are also partially or well-circumscribed, bilateral, and similar-appearing to one another. Thus, these masses are also likely benign.

View larger version (87K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4D. —59-year-old asymptomatic woman with multiple masses revealed on screening mammography. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection. Multiple masses in this patient are smaller in size and fewer in number than those of patient depicted in Figure 3A,3B,3C,3D. Though imaging findings are less dramatic, multiple masses seen in this case are also partially or well-circumscribed, bilateral, and similar-appearing to one another. Thus, these masses are also likely benign.

Among the 1440 cases of multiple masses, breast cancer was diagnosed in four women within 1 year of screening mammography (Fig. 5A,5B,5C,5D). Two of these women had palpable masses at the time of screening, with cancer diagnosis resulting from the radiologist's recommendation for aspiration of any palpable masses if clinically indicated. The other two women had true interval cancers; one developed a palpable mass prompting cancer diagnosis 8 months 12 days after screening, the other presented with nipple discharge leading to cancer diagnosis via ductography and wire localization 10 months 12 days after screening. Therefore, the interval cancer rate among the multiple-masses cohort was 0.14% (2/1440).

View larger version (73K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A. —56-year-old woman with multiple masses revealed on screening mammography, who was diagnosed with breast cancer 8 months 12 days later by fine-needle aspiration of a then-palpable upper outer right breast mass. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection.

View larger version (75K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B. —56-year-old woman with multiple masses revealed on screening mammography, who was diagnosed with breast cancer 8 months 12 days later by fine-needle aspiration of a then-palpable upper outer right breast mass. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection.

View larger version (73K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5C. —56-year-old woman with multiple masses revealed on screening mammography, who was diagnosed with breast cancer 8 months 12 days later by fine-needle aspiration of a then-palpable upper outer right breast mass. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection.

View larger version (73K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5D. —56-year-old woman with multiple masses revealed on screening mammography, who was diagnosed with breast cancer 8 months 12 days later by fine-needle aspiration of a then-palpable upper outer right breast mass. Mammograms of left (A) and right (B) breasts in mediolateral oblique projection and of left (C) and right (D) breasts in craniocaudal projection.

Table 2 describes the imaging, histologic, and staging features of the four cancers in the multiple-masses cohort. The two interval cancers were, on average, slightly smaller and slightly earlier in stage than the two cancers already palpable at the time of screening. Furthermore, both interval cancers were low-grade (grade 1) tumors, whereas the initially palpable cancers were grade 2 and grade 3, respectively.

From our overall screening experience of 84,615 examinations, 462 cancers were detected on mammography. Of these cancers, 126 (27.3%) were classified as stage 0, 239 (51.7%) as stage I, and 67 (14.5%) as stage IIa. The mean tumor diameter for invasive cancer was 15 mm. The interval cancers in our multiple-masses cohort appear to be in the middle range of this overall screening experience; both were stage I cancers with a mean tumor diameter of 13.5 mm.

The four women with multiple masses who were subsequently diagnosed with breast cancer were contacted by telephone in April 1999. They were all alive, well, and reported being cancer-free for intervals ranging from 4 to 9 years since the diagnosis of breast cancer.

Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
This study, involving almost 85,000 consecutive prospectively interpreted screening examinations, shows that multiple masses detected on mammography are almost invariably benign. Indeed, the presence of multiplicity and bilaterality strongly suggests benignity for a variety of mammographic lesions, not just partially circumscribed masses [24,25,26]. However, this observation likely is valid only if the lesions do not display mammographic features suggestive of malignancy, such as spiculated margins or pleomorphic microcalcifications (Fig. 1A,1B,1C,1D). Radiologists also must be vigilant in searching for one mass that appears different from all other masses in what otherwise might be interpreted as a multiple-masses case, so that a coexisting breast cancer will be identified despite the visual distraction produced by the presence of multiple masses (Fig. 2A,2B). Furthermore, the interval growth involving several of the multiple masses does not appear to increase the likelihood of malignancy. None of the cancers identified in our multiple-masses cohort was found among such cases, of which there were 26 (Table 1). In contrast, when a single mass enlarged disproportionately to the other masses or when changes suggestive of malignancy occurred in a single mass (such as disproportionate increase in density or developing indistinctness of margins), the involved cases were considered ineligible for study and subject to recall examination.

Cases of multiple masses are encountered on a regular basis on screening mammography. Kopans [5] reports a frequency of 120 cases (0.5%) of multiple masses on initial screening in a population of approximately 23,000 women. In our series of 84,615 examinations, we report a frequency of 1.7% for cases of multiple masses. In other words, in a busy mammography practice, performing 50 screening examinations a day, one can expect to encounter approximately one multiple-masses case each day.

A powerful indicator of the extremely low likelihood of malignancy among cases of multiple masses is the fact that the interval cancer rate for our cohort (0.14%) was similar to that reported for the general population undergoing routine mammography in various screening studies, including the Screening Mammography Program of British Columbia (0.10%), the Health Insurance Plan of New York (0.14%), the Breast Cancer Detection Demonstration Project (0.19%), and the Canadian National Breast Screening Study (0.24%) [27,28,29,30,31].

The interval cancer rate among our multiple-masses cohort (0.14%) is also somewhat lower than the age-matched United States incident cancer rate of 0.24% [32, 33]. This suggests that cancer development in the multiple-masses cohort may be even less frequent than that which occurs in the general population. The small difference may not be statistically significant. However, insofar as patients with multiple masses do not appear to be at substantially increased risk for development of breast cancer, one can expect a low yield of finding nonpalpable cancer on sonography or on additional diagnostic mammography. Indeed, a major reason why neither sonography nor additional mammography is used for routine screening is the extremely low probability of malignancy once most nonpalpable cancers have been detected on standard screening views.

Another reason why sonography is not used as a screening modality is the cost and morbidity associated with false-positive sonographic findings. When establishing practice standards for patients with multiple masses, we must consider the downstream effects of recalling these patients for additional imaging. Sonography is the most likely imaging procedure to be performed when patients with multiple masses are recalled after screening. Even if the two interval cancers in our study were both detectable on sonography, the yield of two cancers among 1440 cases of multiple masses would be extremely low. Furthermore, a certain percentage of these sonographic examinations would result in the identification of breast masses that do not satisfy the sonographic criteria for simple cyst and that would require further intervention, including aspiration, biopsy, or short-term imaging surveillance. Thus, in addition to the cost of initial sonography for all multiple-masses cases, we must also account for the cost and morbidity of aspiration, biopsy, or short-term surveillance for positive sonographic findings among some of the cases. Most radiologists would find it difficult to justify these costs to identify only two cancers that would still be diagnosed as early-stage tumors without any recall imaging.

Some radiologists may choose to interpret examinations showing multiple masses as Breast Imaging Reporting and Data System (BI-RADS) [34] assessment category 3 (probably benign, recommend short-term interval follow-up), simply on the basis of standard mammographic screening views. Indeed, this approach may appear to be attractive because it represents an intermediate recommendation between our practice of providing a BI-RADS category 2 assessment (benign, 1 year follow-up) and those who choose to render a BI-RADS category 0 assessment (recall imaging). However, we discourage the intermediate approach on several grounds. First, there are many cogent reasons why probably benign assessments should be made only after full diagnostic imaging has been undertaken [26, 35]. More important, the interval cancer rate associated with multiple masses (0.14%) is much lower than the approximately 1% incident cancer rate reported for solitary probably benign lesions, suggesting that even short-term interval follow-up represents overaggressive management. Finally, the limited experience with interval cancers among cases of multiple masses indicates that omission of recall and follow-up imaging does not appear to adversely affect prognosis (our two cases of cancer were early-stage and low-grade tumors).

We conducted this study to provide evidence-based data to address the current controversy regarding the appropriate management recommendations for cases of multiple masses. Our data indicate that there appears to be no increased risk of cancer development for women with multiple masses and that very few such women will develop interval cancers if management is limited to recommendations for repeat mammography in 1 year and aspiration of any palpable masses if clinically indicated. Furthermore, our data show that the rare interval cancer that does arise using this management approach is diagnosed at an early stage with a favorable prognosis.

Recall imaging and any downstream interventional procedures or follow-up imaging not only require considerable monetary costs, but also are associated with anxiety and more tangible forms of morbidity. Our study, though evidence-based, does not directly address the issues of associated costs and morbidity because our practice does not recall patients with multiple masses detected on screening mammography. Proponents of recall imaging for this population are ideally suited to produce the necessary data. However, in the absence of such data, our results suggest that asymptomatic patients with multiple masses can be managed effectively without additional recall imaging.

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