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Breast Imaging |
1 From the Department of Radiology (W.A.B., C.L.A., E.T.) and Greenebaum Cancer Center (W.A.B.), University of Maryland, 419 W Redwood St, Suite 110, Baltimore, MD 21201; and the Technology Assessment Studies Assistance Program, American College of Radiology, Reston, Va (M.B.). Received December 14, 2000; revision requested January 19, 2001; final revision received May 31; accepted July 2. Supported in part by a grant from Ethicon Endo-Surgery, Cincinnati, Ohio. Address correspondence to W.A.B. (e-mail: waberg@umaryland.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: From July 1995 through February 2000, biopsy of all clustered amorphous calcifications not clearly stable for at least 5 years or in a diffuse scattered distribution was recommended. Logistic regression analysis was used to stratify the risk of malignancy by patient risk factors, calcification distribution, and stability.
RESULTS: Calcifications were retrieved from 150 biopsies; 30 (20%) proved malignant and included 27 ductal carcinomas in situ and three low-grade invasive and intraductal carcinomas (2–5 mm). Another 30 (20%) yielded high-risk lesions, including 21 atypical ductal hyperplasia, eight atypical lobular hyperplasia, and one lobular carcinoma in situ. In 150 lesions, stereotactic biopsy was performed on 113 and aborted in 10. Calcifications were retrieved from all 113 stereotactic biopsies. Of those with calcification retrieval, there were three histologic underestimates (accuracy, 97%). Stereotactic biopsy spared a surgical procedure in 57 (46%) of 123 patients. Needle localization was required for 23 (15%) of 150 patients due to poor conspicuity. Five (45%) of 11 biopsies performed in women with ipsilateral breast cancer showed malignancy (P = .025). When multiple lesions of amorphous calcifications were present in one breast, sampling of one reliably predicted the outcome of others.
CONCLUSION: We found a substantial rate of ductal carcinoma in situ and high-risk lesions associated with amorphous calcifications. Stereotactic biopsy can be successfully performed for the majority of subtle amorphous calcifications; however, only a minority were spared a surgical procedure.
Index terms: Breast, biopsy, 00.1261, 00.1267 • Breast, calcification, 00.81 • Breast neoplasms, diagnosis, 00.31, 00.32 • Stereotaxis, 00.1267
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mammographically amorphous or indistinct calcifications (Fig 1) have been considered indeterminate (2) or of intermediate concern, (3) with variable recommendations for follow-up or biopsy. They are described as "sufficiently small or hazy that a more specific morphologic classification cannot be made" (3). With the advent of improved film-screen combinations, they are being seen with greater frequency. Concurrently, methods for percutaneous sampling of calcifications have improved, with the development of directional vacuum-assisted breast biopsy (11–14). The purpose of our study was to assess the pathologic outcome of amorphous breast calcifications and the success of stereotactic biopsy for such lesions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In 1995 and 1996, mammography (CGR 500 T or GE 600 T unit; GE Medical Systems, Issy Les Moulineaux, France) was performed with film (UM-MA-HC; Fuji Medical Systems USA, Stamford, Conn) and cassettes (UM/fine or HR-fine; Fuji). Beginning in 1997, four of every five mammograms were obtained with a LoRad MIV unit (Hologic, Bedford, Mass). Comparison films were routinely requested, and the stability of calcifications for which biopsy was performed was recorded. Breast density was recorded according to the BI-RADS categories.
From July 1995 through December 1996, stereotactic biopsies were performed with a 14-gauge automated large-core biopsy gun and needle (Manan Medical Products, Northbrook, Ill) on a stereotactic table (LoRad DSM; Hologic), with a mean of six specimens (range, 4–12) per biopsy. From January 1997 through February 2000, an 11-gauge directional vacuum-assisted probe (Mammotome; Ethicon Endo-Surgery, Cincinnati, Ohio) was used. We acquired a mean of 12 specimens (range, 5–28) per biopsy, clockwise circumferentially, on the basis of the results by Jackman et al (15) that showed improved accuracy when more than 10 specimens per lesion were obtained.
After all stereotactic biopsies were performed, specimen radiography was performed with the specimens placed on saline-moistened filter paper, with 22 kVp and 7 mAs, to confirm inclusion of representative calcifications. As described by Berg et al (16), specimens containing calcifications were colored with vital green dye (Bradley Products, Bloomington, Minn), then fixed with Bouin solution to facilitate identification of the calcifications by the pathologists. To facilitate identification of the biopsy site, and taking into consideration the subtlety of these lesions, a clip (MicroMark 1 or 2; Ethicon Endo-Surgery, Cincinnati, Ohio) was placed after all completed 11-gauge stereotactic biopsies. Even when residual calcifications are present, a new density can develop at the biopsy site due to scarring (17), and the presence of the clip facilitates proper interpretation of subsequent mammograms.
Direct excision was recommended for lesions on which stereotactic biopsy could not be performed, and the reasons were recorded. All lesions yielding malignancy or atypical ductal hyperplasia (ADH) at stereotactic biopsy were also recommended for excision. Needle localization was performed by using mammographic guidance and 20-gauge Hawkin type needles (Accura BLN; Medical Device Technologies, Gainesville, Fla) and a hook-wire combination. For all needle localizations, specimen radiography was performed on surgically excised tissue to evaluate for removal of the targeted calcifications and/or clip.
The histopathologic truth was considered the excisional result when excision showed malignancy. As part of our quality assurance program, all stereotactic biopsies were reviewed in consensus conference by one or two experienced breast pathologists and several general pathologists. The location of calcifications relative to other histopathologic findings was recorded. If the stereotactic biopsy showed malignancy or atypical hyperplasia and the excision was benign, the core biopsy result was considered truth, and the lesion was believed to have been excised at core biopsy. All malignancies were graded according to the Nottingham classification scheme (18). Mammographic follow-up was recommended at 6, 12, and 24 months, when excision was not performed, and the results of follow-up were documented. The rate of malignancy was compared with that in our experience with biopsy of all calcifications without associated mass or density from July 1995 to February 2000.
One of the study radiologists (W.A.B., C.L.A., or E.T.) recorded the stability of calcifications, compared with that on prior mammograms; distribution (clustered, multiple clusters, regional, linear, segmental); and patient risk factors (age, family history, prior or concurrent atypical hyperplasia or cancer). One radiologist (W.A.B.) assessed the rates of malignancy for each subgroup. The study statistician (M.B.) performed logistic regression analysis to estimate the effect of patient risk factors, the distribution of calcifications, and stability on the probability of malignancy and on the probability of a high-risk lesion (ADH, atypical lobular hyperplasia [ALH], or lobular carcinoma in situ [LCIS]).
Of the 132 patients who underwent 150 biopsies, 13 patients had more than one lesion and five of the 13 patients had three. For the 13 patients, all observations but one were randomly excluded. After this random exclusion, we estimated the probability of malignancy by using binomial logistic regression analysis of the remaining 22 malignancies in relation to the 110 remaining nonmalignant lesions. Further, we estimated the probability of occurrence of one of the three outcomes (benign, high-risk, or malignant) by using multinomial logistic regression analysis of the 22 malignancies, 28 high-risk lesions, and 82 benign lesions. Odds ratios were calculated as the ratio of odds of malignancy with an independent variable dummy of 1, positive, as compared with an independent variable dummy of 0, negative; and 95% CIs were calculated. Odds ratios were reported where the lower confidence bound was greater than 1.0 or the upper confidence bound was less than 1.0.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Numerous calcifications were retrieved in all (100%) of the 113 lesions manifesting as amorphous calcifications for which stereotactic biopsy was performed with tissue acquisition. There were three histologic underestimates: Stereotactic biopsy was accurate for 110 (97%) of 113 lesions. Of the 15 foci of ADH sampled with 11-gauge biopsy, one (7%) yielded a 2-mm focus of DCIS at excision. The one lesion that yielded ADH at 14-gauge biopsy also proved to include DCIS at excision and was therefore histologically underestimated at core biopsy. Of the six lesions yielding ALH at 11-gauge biopsy that were excised, one proved to have calcifications both in fibrocystic changes (initially sampled on core biopsy) and adjacent DCIS at excision (19). Of the 16 foci of DCIS at stereotactic biopsy that were excised, there were no true underestimates. One patient had a mammographically occult 1.4-cm invasive ductal carcinoma at excision surrounded by and at least 1.5 cm away from three clusters of calcifications (two amorphous and one pleomorphic, all due to DCIS). Three 11-gauge biopsies yielded DCIS with invasive ductal carcinoma, with all of the invasive components 5 mm or smaller. Stereotactic biopsy spared a surgical procedure in 57 (46%) of 123 patients, as the calcifications were gone (n = 35) or well sampled (n = 22), with a benign concordant result in all cases. Ten (43%) of 23 high-risk lesions and five (26%) of 19 malignancies excised after 11-gauge stereotactic biopsy showed no residual lesion histopathologically at excision.
Excisional results were available for all but two atypical lesions and for all but one malignancy. The first two were ALH and were believed to have no residual lesion mammographically and remained so at 24-month follow-up. The one malignancy at stereotactic biopsy that was not excised was DCIS in a patient undergoing simultaneous chemotherapy for small cell lung cancer. The one papilloma was excised at the patient’s request. At least 24 months mammographic follow-up was performed for 37 (51%) of 72 remaining lesions with benign stereotactic biopsy results. Of the 37 lesions, 11 (30%) showed no residual lesion, four (11%) showed a decrease in the number of calcifications consistent with sampling, and 22 (59%) were stable. Another 22 lesions had mammographic follow-up at 12–23 months, including 11 (50%) with no residual lesion and four with fewer than five residual calcifications each. The other seven were stable. The 13 lesions with 6 months (n = 5) or no follow-up (n = 8) were believed to have been completely removed on the basis of mammograms obtained immediately after stereotactic biopsy.
Overall, 30 (20%) of 150 lesions proved malignant, including 27 DCIS tumors and three (one microinvasive, one 2-mm, and one 5-mm) low-grade invasive and intraductal carcinomas (Table 2). Two of the DCIS lesions could not be graded due to treatment effects (one in a patient prior chemotherapy at age 25 for concurrent ipsilateral invasive breast cancer with no initial mammogram, and one following radiation, consistent with residual tumor). Of the 25 graded DCIS lesions, 15 (60%) were of low nuclear grade; seven (28%), of intermediate grade; and three (12%), of high grade. Calcifications were within the DCIS in 28 (93%) of 30 malignancies and in adjacent benign ducts in two lesions with malignancy (Fig 2).
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From July 1995 through February 2000, we performed 1,126 breast biopsies at the University of Maryland, Baltimore. Of these, 442 (39%) were for calcifications without associated mass. Of the lesions manifesting as calcifications, 91 (21%) proved to be malignant; 25 (5.7%) revealed ADH; nine (2%) revealed ALH; and nine (2%) revealed LCIS. Lesions that manifested as amorphous calcifications represented 150 (34%) of 442 biopsies for calcifications, and 30 (33%) of 91 malignancies manifested as calcifications. Overall, 21 (84%) of 25 ADH foci and nine (50%) of 18 ALH or LCIS foci were found with lesions manifesting as amorphous calcifications without associated mass.
Despite their subtlety, amorphous calcifications were most often identified in breasts with heterogeneously dense (93 of 150 foci, 20 malignant) or extremely dense (17 of 150, one malignant) parenchyma. Malignancy rates did not vary with breast density, and the distribution of breast densities in patients in this study was not significantly different from that in our biopsy population as a whole.
Table 3 presents findings of the influence of patient risk factors on the rate of malignancy and high-risk lesions. A prior history of ADH or LCIS or personal history of breast cancer indicated a trend toward increased risk of malignancy (Fig 2), but the trend was not statistically significant. Eleven patients had ipsilateral carcinoma: nine synchronous invasive cancer and two metachronous DCIS. In the 11 patients, five (45%) biopsies for amorphous calcifications yielded malignancy (vs 20% overall rate, P = .025 at 
2 analysis). Of 24 biopsies performed in women with contralateral metachronous (n = 20) or synchronous (n = 4) cancer, six (25%) yielded malignancy, results similar to those of the overall group. Those in the youngest age group, 28–39 years, showed higher risk of malignant outcome (Table 4), with an odds ratio of 7.0 (95% CI: 1.3, 38), although there were a small number of such lesions and patients. Two of the malignancies were in women with concurrent cancer, and the third was in a woman with a strong family history of cancer.
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Prior mammograms were available for 112 (75%) of 150 lesions (Table 6). In 45 foci, the calcifications were too numerous to count to allow adequate comparison but showed no definite change. In the remaining 67, retrospectively, but not prospectively, the amorphous calcifications referred for biopsy were identified on 52 (78%) of prior mammograms. Thirty-nine were believed to be probably increasing in number, of which seven (18%) proved malignant and seven (17%) yielded high-risk lesions (five ADH and two ALH). Of the 11 considered stable, one (9%) proved malignant (multifocal DCIS) and one (9%) yielded ADH.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Distribution of calcifications influences the likelihood of malignancy. In the study by Liberman et al (5), 74% of all segmentally distributed calcifications proved malignant, as did 68% of those in a linear distribution, compared with 36% of clustered calcifications. We found a higher rate of malignancy when amorphous calcifications were in a segmental (43%) or linear (40%) distribution, compared with a 17% rate for clustered calcifications, although the differences in malignancy rates did not achieve statistical significance. The presence of multiple clusters of a similar morphology has been considered a reassurance of benignity by some and stated as an infrequent presentation of malignancy (2). In this series, six (19%) of 31 amorphous calcifications presenting as multiple clusters within a 2-cm2 area proved malignant; these results are similar to the 20% overall rate of malignancy. Bilaterality did not decrease the risk of malignancy. The presence of more than one lesion in this study in the same patient significantly increased the risk of malignancy. Reassuringly, when multiple similar lesions were present in the same breast, sampling one lesion reliably predicted the outcome of the others.
Stability of calcifications is not a reliable criterion for a benign etiology. In the study by Lev-Toaff et al (22), 25 (24%) of 105 clusters of malignant calcifications were stable for 8–63 months (mean, 25.4 months), including three (12%) with an invasive component. Of those with increasing or new calcifications, 37% were invasive (22). In this series, one (9%) of the 11 lesions manifesting as stable amorphous calcifications (for 26 months) proved to be multifocal high-grade DCIS.
Patient risk factors also affect the likelihood of malignancy. Roubidoux et al (23) observed that in women with cancer, contralateral breast biopsies were nearly twice as likely to be malignant or show atypical hyperplasia. Although our results failed to reach statistical significance, we observed a similar trend toward increased likelihood of malignancy with a prior or concurrent history of high-risk lesion or cancer. Biopsies of amorphous calcifications in the same breast as past or current cancer were more likely to be malignant (P = .025).
From 48% to 63% of breast cancers have been shown to contain calcifications (24,25). When seen with a mass, the histopathologic finding is typically invasive ductal carcinoma. Invasive ductal carcinoma rarely manifests as isolated clustered calcifications. In the three cases with invasive carcinoma in our series, all of the invasive components were 5 mm or smaller. DCIS more often manifests as calcifications without a mass: It had this appearance in 37 (68%) of 54 DCIS lesions in one series (26) and in 72 (72%) of 100 in another (27).
Stomper and Connolly (28) correlated the subtypes of DCIS with mammographic calcification appearance. Of the 23 with predominantly linear calcifications, 18 (78%) were high-grade (comedo subtype) DCIS, whereas 23 (53%) of 43 of those with predominantly granular calcifications were of noncomedo subtypes (cribriform, solid, or papillary) (28). Similar results were found in the series by Evans et al (29). Calcifications in low-grade DCIS were predominantly punctate in 36% of cases, compared with only 13% with high-grade DCIS (29). In our series of amorphous calcifications, 27 (90%) of 30 malignancies were DCIS and 15 (60%) of 25 evaluable DCIS lesions were of low nuclear grade.
One could question why the substantial malignancy rate and the variability in management of amorphous calcifications have not previously come to attention. As noted, these lesions are often low-grade DCIS. Thus, the answer may in part reflect the relative stability and at times innocuous behavior of low-grade DCIS. Tabar et al (30) examined the sojourn times (duration of preclinical screen-detectable phase) for breast cancer by grade, histologic type, and patient age. For women 40–49 years of age, the sojourn time was estimated at 2 years, regardless of histopathologic findings (30). For women 50–69 years of age, low-grade DCIS was estimated to have a sojourn time of 7.7 years, compared with 2 years for invasive lobular carcinoma and 1.2 years for medullary carcinoma (30).
Should biopsy be performed on lesions likely to be a low-grade DCIS? Importantly, there is overlap in mammographic features between low-grade and high-grade DCIS. Of 25 graded DCIS in this series, three (12%) were high grade. Further, three (10%) of 30 malignancies were invasive cancers. Further, there is the possibility of impure lesions, with low-grade DCIS mixed with cells of higher malignant potential. In the same analysis by Tabar et al (30), the potential for a tumor to dedifferentiate to its worst component was estimated as highly likely in women 40–49 years of age (91% of ductal tumors), compared with only 38% of such tumors in women 55–69 years of age. This would suggest that biopsy of low-grade or even precancerous lesions may be of greatest importance in women younger than 50 years, although further study is needed. Of the 30 malignancies diagnosed in our series, three (10%) were in women younger than 40 years and eight (27%) were in women 40–49 years of age.
ADH is most often found in association with amorphous calcifications, although it can also be adjacent to them (31). Indeed, in our collective biopsy experience, 21 (84%) of 25 foci of ADH that manifested as calcifications were considered amorphous; the remaining four (16%) of 25 were pleomorphic. ADH is considered a marker for an increased risk of breast cancer, from four- to fivefold, with 10 (56%) of 18 subsequent breast cancers occurring in the same breast in one long-term study of more than 10,000 benign biopsies (32). When ADH is found at core biopsy, excision is appropriate. Distinction of ADH from DCIS can be problematic when only a few duct profiles are involved and the two entities can be interspersed. With 14-gauge automated core biopsy systems, 52%–56% of such lesions prove malignant at excision (33,34). Even with 11-gauge and larger vacuum-assisted devices, 13%–27% will prove malignant (13,35,36). Vicini et al (37) suggested that both ADH and cancerization of the lobules, when associated with DCIS, may need to be considered as part of the DCIS lesion to be excised. Thus, the finding of mammographic calcifications with a high likelihood of yielding ADH may in and of itself be an appropriate indication for excisional biopsy.
In this series, amorphous calcifications were frequently overlooked on prior mammograms, with 52 (78%) of 67 seen retrospectively but not prospectively. Such calcifications are frequently at the threshold of visibility on routine mammographic images and require spot magnification views for adequate characterization. This may have implications for digital mammography. In the current GE digital mammographic system, 100-µm pixel size may preclude detection of some lesions that manifest as amorphous calcifications. Further study of this issue is needed.
Successful stereotactic biopsy requires sufficient lesion conspicuity to permit accurate targeting. Amorphous calcifications tend to be barely visible with current stereotactic equipment. As a guide, we have found that a lesion should be visible without a magnifying lens on routine mammograms to have adequate conspicuity for stereotactic guidance. Even so, we are frequently asked to attempt a stereotactic biopsy in lieu of needle localization and excision because of a shortage of operating room time and personnel. In our series, six (4.8%) of 123 attempted stereotactic biopsies for amorphous calcifications were aborted due to inadequate conspicuity, and another 17 lesions were recommended for direct needle localization due to poor conspicuity. Overall, biopsy could not be performed stereotactically on 23 (15%) of 150 lesions due to poor conspicuity. For many others, the lesion was at the threshold of visibility, and operator confidence in targeting was low, although calcifications were retrieved at all 113 stereotactic biopsies in which tissue was acquired. In the series by Liberman et al (12), amorphous morphology portended higher failure rates for stereotactic vacuum-assisted biopsy, with a three (21%) of 14 failure rate, compared with three (3%) of 98 failure rate for all other types of calcifications.
In general, stereotactic biopsy is less cost-effective for initial diagnosis of suspicious calcifications than of masses. Liberman et al (38) reported that only 42% of suspicious calcifications were spared a surgical procedure at initial 14-gauge core biopsy. Improved results were seen with 11-gauge vacuum-assisted biopsy, at which 73% of calcific lesions were spared a surgical procedure (39), and indeed, the 11-gauge system expands the range of lesions amenable to stereotactic biopsy. While stereotactic biopsy of amorphous calcifications was largely feasible in our experience, only 46% of lesions were spared an open biopsy. Indeed, in the surgical literature, Johnson et al (40) report cost and time savings when initial needle localization and open biopsy are performed for malignant-appearing microcalcifications. With clip placement and improved reimbursement for stereotactic vacuum-assisted biopsy, the cost savings are minimal compared with those of surgical biopsy.
Calcifications can be both within and adjacent to cancer and atypical hyperplasias or only adjacent to such processes. In several series (8,41–45), calcifications were both within and outside of neoplastic areas in about 35% of cases and near to but at a finite distance from malignancy in 16% of cases. In our series, two (6.7%) of 30 malignancies, one (4.8%) of 21 ADH lesions, six (75%) of eight ALH lesions, and one LCIS lesion were only adjacent to targeted calcifications. All such lesions adjacent to calcifications were sampled with 11-gauge vacuum-assisted biopsy.
In summary, with a 20% rate of malignancy and 20% rate of high-risk disease, amorphous calcifications should be considered suspicious and referred for biopsy. The rate of malignancy paralleled that of all calcifications for which biopsy was performed at our institution. Ninety percent of malignancies were DCIS, and the remainder had small coexistent invasive components. ADH was far more likely to have amorphous calcifications than other morphologies. Stereotactic biopsy was successfully performed for the majority of subtle amorphous calcifications, although only a minority of lesions were spared a surgical procedure. Direct needle localization and excision should be considered for such lesions. While long-term follow-up (>2 years) is not available for all lesions with benign results at stereotactic biopsy, we achieved 91% accuracy with 14-gauge core biopsy and 98% accuracy with 11-gauge vacuum-assisted biopsy for amorphous calcifications. Biopsy of such calcifications facilitates diagnosis of breast cancer at its earliest, most curable stage.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, W.A.B.; study concepts and design, W.A.B.; literature research, W.A.B.; clinical studies, W.A.B., E.T.; data acquisition, W.A.B., C.L.A., E.T.; data analysis/interpretation, W.A.B., C.L.A.; statistical analysis, M.B., W.A.B.; manuscript preparation, definition of intellectual content, and editing, W.A.B.; manuscript revision/review, W.A.B., M.B.; manuscript final version approval, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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