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1 All authors: Department of Radiology, Breast Imaging Section, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
Received February 7, 2002;
accepted after revision March 6, 2002.
Address correspondence to L. Liberman.
Abstract
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MATERIALS AND METHODS. A retrospective review was performed of 788 consecutive solitary lesions in which the mammographic target was excised (n = 466) or sampled (n = 322) at stereotactic 11-gauge vacuum-assisted biopsy. Medical records and histologic findings were reviewed to determine the frequency of sparing surgery, discordance, histologic underestimation, rabiopsy, complete histologic removal of cancer, and complications. Statistical comparisons were made using the Fisher's exact test.
RESULTS. Complete excision rather than sampling of the mammographic target was associated with a significantly lower frequency of discordance (1/466, 0.2% vs 8/322, 2.5%; p = 0.004) and a trend toward fewer ductal carcinoma in situ underestimates (4/59, 6.8% vs 12/60, 20.0%; p = 0.07). Complete histologic removal of cancer was significantly more likely if the mammographic target was excised rather than sampled (19/91, 20.9% vs 7/106, 6.6%; p = 0.006); however, among 91 cancers in which the mammographic target was excised, surgery revealed residual cancer in 72 (79.1%). Complete excision rather than sampling of the mammographic target yielded no significant differences in the frequency of sparing surgery, atypical ductal hyperplasia underestimates, rebiopsy, or complications.
CONCLUSION. Complete excision rather than sampling of the mammographic target was associated with lower frequencies of discordance and ductal carcinoma in situ underestimation but had no other advantage or disadvantage. Among cancers in which the mammographic target was excised, surgery revealed residual cancer in almost 80%.
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Complete percutaneous excision of all imaging evidence of the lesion is a frequent occurrence at 11-gauge vacuum-assisted breast biopsy. Previous investigators have reported complete removal of the imaging target at 11-gauge vacuum-assisted biopsy in 46-89% of all lesions and in 64-97% of lesions measuring 1 cm or less [6, 15,16,17,18,19]. Potential advantages of complete excision of the mammographic target include improved lesion characterization and more complete removal of the disease process, whereas potential disadvantages include a higher complication rate. Whether complete excision is preferable to sampling the imaging target is not known.
This study was undertaken to determine whether complete excision rather than sampling of the mammographic target conveys any significant advantage or disadvantage at stereotactic 11-gauge vacuum-assisted breast biopsy in terms of frequency of sparing surgery, imaging histologic discordance, complete histologic removal of cancer, histologic underestimation, rebiopsy rate, or complications.
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These 800 lesions occurred in 797 women ranging in age from 28 to 88 years (median, 57 years). Seven hundred ninety-four women had solitary unilateral lesions that underwent stereotactic biopsy. In three women who had solitary unilateral lesions, stereotactic biopsy was performed during one procedure, followed by stereotactic biopsy during a separate procedure for subsequent metachronous lesions in the ipsilateral (n = 2) or contralateral (n = 1) breast.
Indications for Percutaneous Biopsy
Percutaneous biopsy was offered at our institution during this period as an
alternative to surgical biopsy for nonpalpable lesions that were suspicious
for or highly suggestive of malignancy unless the patient had a bleeding
diathesis, the patient was unable to cooperate with the procedure, or the
lesion could not be targeted. The choice of guidance modality for percutaneous
biopsy was based on several factors including lesion conspicuity and
radiologist and patient preference. The preferred percutaneous biopsy method
was generally sonographically guided 14-gauge automated core biopsy for masses
greater than 0.5 cm that could be seen with sonography and stereotactic
11-gauge directional vacuum-assisted biopsy for calcification lesions, masses
measuring 0.5 cm or less, or masses that were not sonographically evident.
Biopsy Technique
Stereotactic biopsy was performed on a dedicated table (StereoGuide; LoRad,
Danbury, CT) with digital spot mammography using an 11-gauge directional
vacuum-assisted biopsy probe (Mammotome; Biopsys/Ethicon Endo-Surgery). The
median number of specimens obtained per lesion was 15 (range, 4-47 lesions);
eight or more specimens were obtained in 790 (99%) of 800 lesions. Specimen
radiography was performed for all lesions evident as calcifications
[20].
The radiologist who performed stereotactic 11-gauge vacuum-assisted biopsy did not specifically attempt either to achieve or to avoid complete excision of the mammographic target but rather to obtain sufficient material for histologic diagnosis. If stereotactic images obtained after completion of tissue acquisition suggested that the mammographic target was completely or largely removed, a localizing clip (MicroMark; Biopsys/Ethicon Endo-Surgery) was placed at the biopsy site. A two-view mammogram was obtained after all stereotactic biopsy procedures.
Postbiopsy Management Protocol
After biopsy, histologic results were correlated with imaging findings, and
specific recommendations were made to the woman and her referring physician.
If stereotactic biopsy yielded benign findings concordant with the imaging
characteristics, the patient was referred for annual mammography. If
stereotactic biopsy yielded carcinoma, the patient was referred for definitive
surgery. Surgical biopsy was suggested if stereotactic biopsy revealed certain
histologic findings including atypical ductal hyperplasia, radial scar, or
possible phyllodes tumor; if there was discordance between histologic findings
and imaging characteristics; or if surgical excision was suggested by the
pathologist [21].
Definitions
Atypical ductal hyperplasia underestimates were defined as lesions yielding
atypical ductal hyperplasia at percutaneous biopsy and carcinoma at surgery
[22]. Ductal carcinoma in situ
underestimates were defined as lesions yielding ductal carcinoma in situ at
percutaneous biopsy and infiltrating carcinoma at surgery
[22]. Imaging—histologic
discordance was considered to have been present when the histologic findings
did not provide a sufficient explanation for the imaging features
[23].
A woman was considered to have been spared a surgical procedure if stereotactic biopsy yielded a benign diagnosis for which surgical excision was neither recommended nor performed. A woman was also considered to have been spared a surgical procedure if stereotactic biopsy yielded carcinoma treated with lumpectomy and axillary dissection, lumpectomy and sentinel lymph node biopsy, or mastectomy. Women with carcinomas measuring 1 cm or greater who were treated with wide excision only were also considered to have been spared a diagnostic surgical biopsy. A woman was not considered to have been spared a surgical procedure if surgical biopsy was recommended or performed after stereotactic breast biopsy or if she had a small (<1 cm) carcinoma diagnosed by stereotactic biopsy and treated by surgical excision without axillary surgery. A surgical procedure was not spared if the patient required two or more surgeries because of tumor at the margins or histologic underestimation [24].
Data Collection and Analysis
Patient, lesion, and procedural data were prospectively collected by the
radiologist performing the stereotactic biopsy using a standardized data
collection form. The radiologist who performed the biopsy also recorded his or
her impression of whether the mammographic target had been completely removed
on the basis of images obtained during stereotactic biopsy and the postbiopsy
two-view mammogram. Any apparent conflict between the stereotactic images and
the postbiopsy two-view mammogram was resolved by a composite judgment made by
the radiologist. Subsequent mammograms were not used in the assessment of
complete excision of the mammographic target.
Medical records and mammographic and histologic findings were reviewed. Clinical follow-up data were obtained to determine the frequency of sparing surgery, imaging—histologic discordance, atypical ductal hyperplasia underestimates, ductal carcinoma in situ underestimates, immediate rebiopsy, delayed rebiopsy, complete histologic removal of cancer, and complications.
Data were entered into a computerized spreadsheet (Excel; Microsoft, Redmond, WA). Statistical analysis was performed with the Fisher's exact test using statistical software (Epi-Info; Centers for Disease Control, Atlanta, GA). A p value of <0.05 was considered significant.
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Imaging—Histologic Discordance
Imaging—histologic discordance occurred in 18 (2.3%) of 800 lesions,
including nine lesions in which the mammographic target was missed, eight in
which the mammographic target was sampled, and one in which the mammographic
target was removed. The frequency of imaging—histologic discordance was
significantly lower among lesions that were excised at stereotactic 11-gauge
vacuum-assisted biopsy rather than sampled
(Table 2).
Among the eight lesions that were sampled with discordant results, surgical biopsy was performed in seven and yielded benign findings in six. In one lesion evident as architectural distortion for which stereotactic biopsy yielded sclerosing adenosis, surgery revealed ductal carcinoma in situ (DCIS) in a complex sclerosing lesion. No follow-up data are available for the eighth lesion that was sampled with discordant results—a lowsuspicion mass in an 80-year-old woman with multiple medical problems.
The one lesion in which the mammographic target was excised with discordant histology at stereotactic biopsy was a 0.5-cm irregular, spiculated mass. Stereotactic biopsy yielded fibroadipose tissue. Subsequent surgical excision showed a 0.3-cm infiltrating ductal carcinoma.
Complete Histologic Removal of Cancer
Among 198 stereotactically proven cancers in which subsequent surgical
pathologic results are available, surgery revealed residual cancer in 172
(86.9%), atypical ductal hyperplasia in three (1.5%), and benign findings
without atypia in 23 (11.6%). In the latter 26 lesions, a review of the
pathology confirmed the presence of cancer in the stereotactic biopsy
specimens and the presence of postbiopsy changes in the surgical
specimens.
Complete histologic removal of cancer was significantly more likely if the mammographic target was excised rather than sampled (Table 2). However, among 91 women in whom the mammographic target was removed, surgery revealed residual cancer in 72 (79.1%) (Table 2).
Ductal Carcinoma In Situ Underestimates
Among 120 lesions yielding DCIS at stereotactic 11-gauge vacuum-assisted
biopsy in which surgical pathologic results were available, surgery revealed
infiltrating carcinoma in 17 (14.2%). There was a trend toward lower frequency
of DCIS underestimates for lesions in which the mammographic target was
excised at stereotactic 11-gauge vacuum-assisted biopsy rather than sampled
(Table 2).
Atypical Ductal Hyperplasia Underestimates
Among 49 lesions yielding atypical ductal hyperplasia at stereotactic
11-gauge vacuum-assisted biopsy that had subsequent surgical excision,
carcinoma was found in 12 (24.5%) including DCIS in nine, infiltrating ductal
carcinoma and DCIS in two, and infiltrating ductal carcinoma in one. The
frequency of atypical ductal hyperplasia underestimates did not differ
significantly between lesions in which the mammographic target was excised
rather than sampled (Table
2).
Sparing Surgery
Surgery was spared in 645 (80.6%) of 800 lesions. Reasons for not sparing
surgery in 155 lesions included recommendation for immediate rebiopsy in 96,
subcentimeter carcinoma treated by excision alone in 30, tumor at or close to
the margins in 24 (including three with DCIS underestimation), and DCIS
underestimation in five (requiring axillary surgery at a later date). The
frequency of sparing surgery did not differ significantly for lesions that
were excised at stereotactic 11-gauge vacuum-assisted biopsy rather than
sampled (Table 2).
Immediate Rebiopsy
Prompt surgical biopsy was recommended in 96 (12.0%) of 800 lesions as a
result of atypical ductal hyperplasia in 57, benign histologies for which
excision was suggested in 21, and imaging-histologic discordance in 18. The
rate of recommending prompt surgical biopsy did not differ significantly
between lesions in which the mammographic target was excised at stereotactic
11-gauge vacuum-assisted biopsy rather than sampled
(Table 2).
Delayed Rebiopsy
Imaging follow-up data are available in 317 lesions that yielded benign
findings concordant with imaging features, with a median follow-up of 23
months (range, 6-61 months). Interval change at the biopsy site on subsequent
mammography prompted rebiopsy at a later date in six (1.9%) of these 317
lesions, based on mammograms performed at a median of 21 months (range, 13-35
months) after stereotactic biopsy. The frequency of delayed rebiopsy did not
differ significantly between lesions in which the mammographic target was
excised rather than sampled (Table
2).
Three of the six lesions that had delayed rebiopsy were calcific lesions that were sampled at stereotactic biopsy; interval development of new calcifications at the biopsy site prompted surgical excision, yielding benign findings in two lesions and carcinoma in one lesion. In the latter case, initial stereotactic biopsy of amorphous and pleomorphic calcifications yielded benign breast tissue with fibrosis and calcification; new calcifications developed at the biopsy site 27 months later, for which surgical excision yielded DCIS, with calcifications in DCIS and in nonneoplastic breast tissue.
In the remaining three lesions that had delayed rebiopsy (two masses and one calcific lesion), stereotactic biopsy resulted in complete removal of the mammographic targets, but new masses were detected at the biopsy site on follow-up. Rebiopsy yielded benign results in two lesions and carcinoma in one lesion. In the latter case, stereotactic biopsy of a circumscribed mass yielded papilloma, with complete removal of the mammographic mass; the patient developed a palpable spiculated mass at the biopsy site 22 months later, for which surgical excision showed poorly differentiated, infiltrating ductal carcinoma.
Complications
Complications were encountered in 17 (2.1%) of 800 lesions. In these 17
lesions, the mammographic target was excised in five, sampled in five, and
missed in seven lesions. Complications included bleeding that required
compression for 1-2 hr to achieve hemostasis (n = 12), delayed
hematomas leading to return after discharge for compression and observation
(n = 2), vasovagal reaction (n = 2), and pain that led to
aborting the procedure (n = 1). The complication rate did not differ
significantly between lesions in which the mammographic target was excised at
stereotactic 11-gauge vacuum-assisted biopsy rather than sampled
(Table 2).
Missed Lesions
The 12 lesions missed at stereotactic biopsy were all calcified lesions in
which no calcifications were identified on specimen radiographs. In seven of
these 12 lesions, complications occurred during the stereotactic biopsy
procedure.
Among the 12 missed lesions, one lesion was shown to represent skin calcifications, and routine follow-up was suggested. One lesion for which stereotactic biopsy revealed DCIS underwent wide excision, yielding DCIS with microinvasion. One lesion yielded atypical ductal hyperplasia at stereotactic biopsy; surgery showed infiltrating ductal carcinoma. In the remaining nine lesions, rebiopsy was suggested because of discordance; surgical biopsy, performed in seven, yielded benign results. One woman who did not have surgery had a stable mammogram at 15 months; one woman left the country and was lost to follow-up.
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In our study, complete removal rather than sampling of the mammographic target was associated with a significantly lower frequency of imaging-histologic discordance. Liberman et al. [23] reported discordance in 3% of lesions that underwent percutaneous imaging-guided breast biopsy; among discordant lesions, subsequent surgery revealed carcinoma in 24%. Other investigators [23] have reported a 1-6% frequency of discordance at percutaneous biopsy, with cancer at subsequent surgery in 0-64% of discordant lesions. The frequency of discordance is lower among lesions in which the mammographic target was excised: if the lesion identified at imaging is removed, then the histologic findings should reflect the lesion that underwent biopsy. However, because discordance is uncommon at stereotactic 11-gauge vacuum-assisted biopsy, lowering the frequency of discordance benefits few women.
There was a trend toward lower frequency of DCIS underestimation among lesions in which the mammographic target was excised rather than sampled. In prior reports of lesions yielding DCIS at stereotactic 11-gauge vacuum-assisted biopsy, surgery revealed invasive carcinoma in 4-18% [6, 9,10,11,12, 25, 26]. Obtaining a needle biopsy diagnosis of DCIS in a lesion that contains DCIS and infiltrating carcinoma reflects sampling error. Removal of the mammographic target lowers the likelihood of sampling error but does not eradicate it, because the mammogram itself may underestimate the extent of the lesion, particularly in lesions containing DCIS [27].
Fewer atypical ductal hyperplasia underestimates occurred among lesions in which the mammographic target was excised rather than sampled, but the difference did not achieve statistical significance. In prior reports of lesions yielding atypical ductal hyperplasia at stereotactic 11-gauge vacuum-assisted biopsy, surgery revealed carcinoma in 10-27% [6, 8,9,10, 13, 28]. Our data, like those of Jackman et al. [29], indicate that atypical ductal underestimation can occur regardless of whether the imaging target was sampled or completely excised. Surgical excision is warranted for lesions yielding atypical ductal hyperplasia at stereotactic biopsy, whether or not residual lesion is present on imaging studies [29].
The immediate rebiopsy rate did not differ significantly for lesions in which the mammographic target was excised rather than sampled. One can hypothesize that there are specific scenarios in which percutaneous excision rather than sampling of the mammographic target is preferable [30, 31], but further study with a larger series of cases would be necessary to test this hypothesis. Delayed rebiopsy rates also did not significantly differ for lesions in which the mammographic target was excised rather than sampled, but our data are limited by incomplete follow-up. Two women developed cancer on follow-up at the site of prior benign stereotactic biopsy; the original mammographic target had been sampled in one woman and excised in the other.
One potential advantage of complete excision that we did not address in our study was the psychologic benefit of telling the patient that the imaging finding was completely removed ("Mrs. Jones, we got it all out"). In our opinion, such information provides false reassurance. Previous investigators have shown that among cancers in which all imaging evidence of the lesion was removed at 11-gauge vacuum-assisted biopsy, surgery revealed residual cancer in 50-73% [18, 32]. In our study, we found residual cancer present in almost 80% of stereotactically proven cancers in which the mammographic target was excised at stereotactic biopsy. Complete removal of the imaging finding, therefore, does not ensure complete excision of the disease process.
The recent explosion in percutaneous biopsy technology confronts us with the Goldilocks [33] question: how much tissue is not enough, how much is too much, and how much is just right? In our study, complete excision of the mammographic target was associated with a significantly lower frequency of discordance and a trend toward lower frequency of DCIS underestimation but had no other significant advantage or disadvantage. Further work, including long-term follow-up of the lesions excised and sampled at stereotactic 11-gauge vacuum-assisted biopsy, will be necessary before we can determine how much tissue removal at percutaneous breast biopsy is "just right."
Acknowledgments
We thank David C. Perlman for invaluable assistance.
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