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Breast Imaging |
1 From the Department of Radiology, Palo Alto Medical Clinic, 795 El Camino Real, Palo Alto, CA 94301 (R.J.J.); and the Department of Radiology, Stanford University Medical Center, Stanford, Calif (R.L.B., D.M.I.). From the 2001 RSNA scientific assembly. Received September 14, 2001; revision requested November 15; revision received January 9, 2002; accepted March 12. Supported in part by an educational grant from Biopsys Medical to the Palo Alto Medical Foundation. Address correspondence to R.J.J. (e-mail: jackmanr@pamf.org).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Clinical, mammographic, and stereotactic biopsy features in 104 consecutive nonpalpable ADH lesions were correlated with the presence of carcinoma at lumpectomy. The results were analyzed with 
2 statistic, with P < .05 indicative of significant difference.
RESULTS: Surgical excision revealed carcinoma in 22 (21%) of 104 ADH lesions. The lowest incidences of carcinoma (each P < .02) were 16% (15 of 92) in patients with no personal history of breast carcinoma, 13% (nine of 67) when maximum lesion diameter was less than 10 mm, and 8% (three of 36) when 100% of the mammographic lesion was removed at stereotactic biopsy.
CONCLUSION: No clinical, mammographic, or biopsy features alone or in combination could be used to define a substantial subset of probably benign lesions with a less than 2% chance of carcinoma at lumpectomy.
© RSNA, 2002
Index terms: Biopsies, technology • Breast, biopsy, 00.1261, 00.1267 • Breast, ducts, 00.711 • Breast neoplasms, diagnosis, 00.32, 00.81
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Mammographically visible lesions are categorized by using the Breast Imaging Reporting and Data System (BI-RADS) lexicon of the American College of Radiology (27). Lesions in category 3 are "probably benign—short interval follow-up suggested." The frequency of cancer in this group is less than 2% (28). Mammographic follow-up, rather than biopsy, is usually advised for such lesions.
The purpose of our study was to determine if a subset of lesions diagnosed as ADH at 11-gauge vacuum-assisted stereotactic biopsy in prone patients fit the "probably benign" definition of a less than 2% chance of carcinoma at subsequent surgery, allowing a recommendation of imaging follow-up rather than surgical excision.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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ADH, without associated malignancy, was diagnosed in 131 (7%) of the 1,964 lesions. None of the ADH lesions were previously reported in published studies. ADH was diagnosed in 104 (9%) of 1,190 microcalcification lesions, 22 (4%) of 619 mass lesions without calcifications, and five (3%) of 155 mass lesions with calcifications. A subsequent surgical lumpectomy was performed in 104 (79%) of the 131 ADH lesions (including 81 [78%] of 104 microcalcification lesions, 18 [82%] of 22 noncalcified masses, and five [100%] of five calcified masses), and these 104 lesions constitute our study group. All study lesions were nonpalpable. Twenty-seven of 131 ADH lesions were excluded if subsequent surgical excision was accomplished with mastectomy (n = 9, excluded because of difficulty in correlating surgical histologic findings with percutaneous histologic findings), if the lesion was not subjected to surgical excision (n = 17, excluded because histologic correlation was not possible), or if the patient was lost to follow-up (n = 1).
Mastectomy was performed in nine lesions because of synchronous carcinoma (n = 7), metachronous carcinoma (n = 1, with contralateral mastectomy 6 years earlier), or bilateral high-risk lesions (n = 1, with lobular carcinoma in situ in the contralateral breast). Surgery was not performed for 17 lesions because the referring physician did not recommend surgery to the patient (n = 7, because of either lack of physician concern about the lesion [n = 5] or physician decision that nonbreast illness made surgery unwise [n = 2]), or the patient declined the recommended surgery (n = 10). Mammographic follow-up in 14 of the 17 available nonsurgical cases was accomplished for 5–35 months (median, 21 months) with the lesion gone (n = 9), decreased (n = 2), unchanged (n = 2), or increased (n = 1) at the time of follow-up. The 104 biopsies in the study group were in 99 breasts in 99 patients (age range, 37–85 years; median, 55 years). Five patients had two ADH lesions in the same breast, with biopsies performed on the same day. Medical records were reviewed by one of the authors (R.J.J.) to determine whether the patient had a personal history of breast carcinoma (either synchronous or metachronous) and/or a family history of breast carcinoma in a first-degree relative (mother, sister, or daughter).
Mammographic and Biopsy Evaluation
Each prebiopsy mammogram was retrospectively and independently reviewed by two of the authors (R.J.J., R.L.B.) to categorize lesions according to mammographic lesion type (mass with or without associated microcalcifications or microcalcifications alone) and BI-RADS category (categories 3–5) and by one of the authors (R.J.J.) to measure maximum mammographic lesion diameter. The radiologist (including R.J.J.) performing the biopsy recorded the number of tissue samples obtained during biopsy of each lesion (median, 18; range, 9–110) and the presence or absence of calcifications on specimen radiographs of each calcified lesion.
Histologic slides of percutaneous biopsy specimens were interpreted either at the Palo Alto Medical Clinic (where all the biopsies were performed) or at Stanford University Medical Center (Calif) (one of the referring institutions). Pathologists recorded the histologic diagnosis based on percutaneous biopsy specimens for each lesion as malignant, high-risk, or benign. Malignant lesions (ie, invasive carcinoma, ductal carcinoma in situ [DCIS], lymphoma, and sarcoma) were excluded. In addition to ADH, we consider atypical lobular hyperplasia, lobular carcinoma in situ, and radial scar to be high-risk lesions because the associated presence of carcinoma can be underestimated at percutaneous biopsy and surgical excision is usually advised. High-risk lesions in 17 such cases associated with ADH were atypical lobular hyperplasia (n = 11), lobular carcinoma in situ (n = 3), or radial scar (n = 3). These other high-risk lesions were excluded when present without associated ADH. Lesions not histologically categorized as malignant or high-risk were classified as benign and were excluded.
Two of the authors (R.J.J., R.L.B.) each retrospectively and independently reviewed a combination of mammographic images obtained before biopsy, immediately after stereotactic biopsy, and, if available, immediately before lumpectomy to estimate the percentage of the lesion that had been removed during the stereotactic biopsy. Estimated percentage removal was scored as 0%, 1%–49%, 50%–89%, 90%–99%, or 100%. The two lesions without postbiopsy images available for review were excluded from scoring for estimated percentage of lesion removal. Five lesions were scored as 0% removal. Two, with no apparent lesion change between pre- and postbiopsy images, were a mass (n = 1) and a calcification lesion (n = 1). In addition, for the calcification lesion the specimen radiograph was negative. Three masses that were larger after biopsy than before biopsy, presumably because of a hematoma along with a residual mass after biopsy, were also scored as 0% removal. The same two authors used the same images, plus the lumpectomy specimen radiographs, to estimate the accuracy of the lumpectomy (accurate or inaccurate). Prelumpectomy localizations were performed with a variety of needles (n = 103, with or without associated wires and dyes) or with a mammographic map (n = 1). The four lesions treated at lumpectomy but with no specimen radiograph available for review were excluded from scoring for accuracy of the lumpectomy.
A combined consensus review was used to resolve disagreements about any of the independent retrospective scores. All retrospective reviews were performed with knowledge that ADH was found at stereotactic biopsy but without knowledge of the lumpectomy histologic results.
Pathologists from six medical institutions recorded the lumpectomy histologic diagnosis for each lesion as malignant, high-risk, or benign. DCIS lesions were recorded as low, intermediate, or high grade. The pathologists were aware of the percutaneous biopsy diagnosis of ADH and were variably aware of clinical, mammographic, and stereotactic biopsy data about each lesion. The recorded histologic diagnoses from both the percutaneous biopsies and the surgical procedures were accepted for this study, and the histologic slides were not reviewed. Percutaneous biopsy material was routinely processed to create slides from three different depths. More slides were processed at the discretion of the pathologists at the two institutions. Lumpectomy biopsy material was processed at the discretion of the pathologists at six institutions.
Statistical Analysis
Data were analyzed with statistical software (StatView; Abacus Concepts, Berkeley, Calif). P values of less than .05, determined with the 2, test were considered indicative of a significant difference. Age, personal history of breast carcinoma, and family history of breast carcinoma were variables per patient. All other variables were per lesion, and the lesion was therefore used as the unit of analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Table 1 shows the comparison among underestimation rates for associated carcinoma at surgical excision according to patient, mammographic, and stereotactic biopsy variables. Statistically significant decreased underestimation rates (P < .02 for each) were found if the patient did not have a personal history of breast cancer, if maximum lesion diameter was less than 10 mm, or if 100% of the lesion was removed at the stereotactic biopsy.
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Nonsignificant decreased underestimation rates occurred with decreased patient age at the time of biopsy, negative family history of breast carcinoma, presence of calcification lesions, lower BI-RADS category, decreased number of tissue specimens, and absence of a second high-risk lesion at percutaneous biopsy.
At least 12 specimens were obtained from all lesions but one, a 9-mm microcalcification cluster in which nine specimens were obtained. The specimen radiograph for this lesion was positive; the lesion was scored as 50%–89% removal; and it was benign at excision. Specimen radiographs of stereotactic biopsy specimens showed calcifications in all five calcified masses and in all but two (2%) of 80 microcalcification lesions. The latter two lesions each showed histologic calcifications; one was a 7-mm microcalcification cluster (sampled with 110 specimens; scored as 0% removal; benign tissue at excision), and the other was a 20-mm microcalcification cluster (sampled with 43 specimens; scored as 1%–49% removal; DCIS at excision). In the latter case, fewer calcifications were mammographically evident after biopsy than before biopsy, despite radiographs of all 43 specimens that failed to reveal calcifications. The only other lesion sampled with more than 40 specimens was a 5-mm microcalcification cluster (sampled with 47 specimens; positive specimen radiograph; scored as 90%–99% removal; DCIS at excision).
The lumpectomy was scored as accurate in all 100 lesions for which specimen radiographs were available for review.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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For this study, we used patient, mammographic, and stereotactic features to attempt to define a subset of ADH lesions diagnosed at 11-gauge vacuum-assisted prone stereotactic biopsy as probably benign, with a less than 2% chance of being carcinoma at subsequent excision. In total, 21% (22 of 104) of the ADH lesions for which surgical lumpectomy was subsequently performed were found to be carcinoma.
Most of the factors that we evaluated were relatively easy to score; estimating the percentage of lesion removed at vacuum-assisted biopsy was difficult. In general, the estimates were more difficult when using digital images obtained immediately after prone stereotactic biopsy; estimates were easier when using conventional filmed mammograms obtained in upright patients immediately before lumpectomy. In addition, evaluation of microcalcification clusters was easier than evaluation of masses for two reasons. First, examination of individual calcifications on pre- and postbiopsy images allowed us to more readily estimate which calcifications had been removed. Second, a postbiopsy hematoma was much more likely to obscure a mass than to obscure calcifications. Lumpectomy specimen radiographs are not available at the time a decision is made whether to surgically excise or mammographically follow an ADH lesion found at percutaneous biopsy, and we think those images should not be used to estimate percentage of lesion removal.
As shown in Table 1, even the three statistically significant variables were not sufficient to help define a subset of probably benign lesions. Underestimation rates of 16% for lesions in patients with no personal history of breast cancer, 13% for lesions smaller than 10 mm in maximum diameter, and 8% for lesions with 100% removal at stereotactic biopsy were all too high to recommend follow-up rather than surgery. Carcinoma was found in 9% (three of 32) of lesions with all three favorable variables. None of the six lesions classified as BI-RADS category 3 was an underestimate, but six lesions are too small a subset to be meaningful.
Table 2 shows a summary of articles (including this study) where at least 10 ADH lesions (with or without another high-risk lesion) were diagnosed at prone stereotactic biopsy performed with either a 14-gauge large-core technique or a 14- or 11-gauge vacuum technique. To be included, articles had to include both the total number of lesions subjected to biopsy and the number of cancers found in those ADH lesions that were subjected to subsequent surgery. Similar to Reynolds (37), we attempted to avoid duplication of data in compiling the total numbers in Table 2.
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By using mammographic and stereotactic biopsy features, data regarding a lower ADH underestimation rate for vacuum-assisted biopsy as compared with that for large-core biopsy (10) were reinterpreted (40). The underestimation rate was higher with masses (44% [11 of 25]) than with microcalcifications (27% [28 of 103]) (P > .1), with a large-core biopsy technique (48% [26 of 54]) than with a vacuum-assisted technique (18% [13 of 74]) (P < .001), and with 10 or fewer specimens per lesion (48% [27 of 56]) than with more than 10 specimens per lesion (17% [12 of 72]) (P < .001). Interestingly, those same three factors were associated with higher DCIS underestimation rates, with invasive carcinoma found at surgical excision (40).
Despite obtaining an unusually large number of specimens, we found that the only three lesions sampled with more than 40 specimens included two histologic underestimates and the only two negative specimen radiographs. These data suggest that the observed results are unlikely to be reversed by obtaining even more specimens per lesion.
For unknown reasons, ADH has different implications in the literature, depending on whether it is diagnosed at surgical biopsy or percutaneous biopsy. Women with ADH diagnosed at surgical biopsy carry a moderately increased risk for developing invasive carcinoma at any site in either breast, but there is not thought to be a markedly increased risk of carcinoma at the biopsy site itself (31–36). Re-excision is not usually recommended. In contradistinction, surgical resection of the site when ADH is diagnosed at percutaneous core biopsy has been routinely recommended since Jackman et al (1) and Liberman et al (2) reported that 14-gauge large-core biopsy resulted in underestimation of the associated presence of carcinoma in more than 50% of lesions.
We postulate that if ADH lesions initially diagnosed at surgical biopsy were to be surgically re-excised, some percentage of the lesions would reveal carcinoma at the second surgery. We do know that needle-localized breast biopsy as the initial histologic procedure has a false-negative rate (ie, initial biopsy results are benign, with no malignant or high-risk lesions, and repeat biopsy reveals carcinoma) of 2.0% (range, 0%–8%) (38) and a DCIS underestimation rate (ie, initial biopsy shows DCIS and subsequent re-excision reveals invasive carcinoma) of 11% (six of 56) (39).
Adrales et al (23) made another attempt to define which lesions diagnosed as ADH at percutaneous biopsy are most likely to be histologic underestimates by evaluating 62 ADH lesions diagnosed at 11-gauge vacuum-assisted biopsy. The nine (15%) lesions determined to be carcinoma at surgical excision were significantly more likely to be found in patients with a previous contralateral breast cancer (P = .02) and with incomplete removal of calcifications at stereotactic biopsy (P = .02). No individual factor was found to be associated with a less than 2% chance of malignancy at excision. However, none of the 40 of 62 patients with no personal or family history of breast cancer and no markedly atypical hyperplasia at stereotactic biopsy had carcinoma found at surgical excision.
In three reports (19,22,23), all ADH cases in which the lesion depicted on the mammogram was completely removed at 11-gauge vacuum-assisted stereotactic biopsy were free of carcinoma at surgical excision. The number of ADH lesions with complete removal and the total number of ADH lesions were five of 10 (19), six of 26 (22), and 23 of 62 (23).
Recent attempts (17,41–43) have been made to use histologic features to identify a subset of lesions diagnosed as ADH at percutaneous biopsy with lower risk. The goal (as in our study, in which we used clinical, mammographic, and biopsy features but not histologic features) was to determine those lesions with a sufficiently low underestimation rate that they can be safely followed rather than surgically excised. Encouraging results have been found in reports (17,41) with a relatively small number of lesions.
Ely et al (41) retrospectively reviewed histologic slides of 47 ADH lesions diagnosed at 14- or 11-gauge percutaneous biopsy (with other biopsy details not provided) that were later surgically resected. The extent of ADH at percutaneous biopsy was graded according to the number of large ducts and/or terminal duct-lobular units affected. Carcinoma was found at surgery in 0% (zero of 24) of lesions with two or fewer foci involved, 50% (four of eight) of lesions with three foci involved, and 87% (13 of 15) of lesions with four or more foci involved (P < .001). The 17 breast carcinomas were 15 cases of DCIS and two of invasive carcinoma. Two factors suggest that the 47 lesions in this study may not be representative of the usual medical practice. First, the 47 study lesions were only 31% of the 152 ADH lesions designated at "core, needle, or stereotactic" biopsy at Vanderbilt University Medical Center (Nashville, Tenn). Second, 77% (36 of 47) of the study lesions were cases sent for consultation.
O’Hea and Tornos (17) retrospectively reviewed 19 ADH lesions diagnosed at 14-gauge large-core biopsy that were later surgically excised. They assigned the lesions to three groups on the basis of the severity of atypia at large-core biopsy. Carcinoma was found at surgical excision of lesions in 0% (zero of eight) in group 1 (mild atypia, not meeting criteria for ADH), 33% (two of six) in group 2 (true ADH), and 80% (four of five) in group 3 (severe ADH, borderline DCIS) (P < .01).
From 3,026 biopsied lesions, Renshaw et al (42) and Renshaw (43) retrospectively reviewed the 216 (7%) lesions diagnosed at 14- or 11-gauge percutaneous biopsy as ADH or atypia not otherwise specified. Biopsy was usually performed with stereotactic or US guidance, with other biopsy details not available. Material from subsequent surgical excision was available for 105 (49%) of 216 lesions. After review, 95 lesions qualified as ADH; and two lesions, as atypical small acinar proliferation. DCIS was found at surgical excision in 14% (13 of 95) of qualifying ADH lesions. No subset of lesions was found with a less than 2% chance of carcinoma at surgical excision.
One potential weakness of our study was the acceptance of the original histologic interpretation. We are performing a retrospective histologic review of our ADH lesions diagnosed at 11-gauge vacuum-assisted biopsy to determine if that approach will allow us to define a subset of ADH lesions not requiring surgical excision. A second potential weakness concerns the difficult task of estimating the percentage of lesion removal; we did not test our interobserver or intraobserver accuracy and do not know if subsequent correlation studies would reveal similar results.
In conclusion, ADH was more reliably diagnosed when the patient did not have a personal history of breast carcinoma, the lesion measured less than 10 mm, and/or 100% of the lesion was removed at stereotactic biopsy, but we could find no clinical, mammographic, and/or biopsy features that could be used to define a substantial subset of lesions with a less than 2% chance of carcinoma at subsequent surgical excision.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Abbreviations: ADH = atypical ductal hyperplasia, BI-RADS = Breast Imaging Reporting and Data System, DCIS = ductal carcinoma in situ
Author contributions: Guarantor of integrity of entire study, R.J.J.; study concepts and design, R.J.J., R.L.B., D.M.I.; literature research, R.J.J.; clinical studies, R.J.J.; data acquisition, R.J.J., R.L.B.; data analysis/interpretation, R.J.J., R.L.B., D.M.I.; manuscript preparation, definition of intellectual content, editing, revision/review, and final version approval, R.J.J., R.L.B., D.M.I.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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