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Stereotactic 11-Gauge Vacuum-Assisted Breast Biopsy: A Validation Study

¹ Department of Radiology, University of Vienna Medical School, AKH Wien, Waehringer Guertel 18-20, A-1090 Vienna, Austria.
² Department of Gynecology, University of Vienna Medical School, AKH Wien, A-1090 Vienna, Austria.
³ Department of Surgery, University of Vienna Medical School, AKH Wien, A-1090 Vienna, Austria.
⁴ Department of Pathology, University of Vienna Medical School, AKH Wien, A-1090 Vienna, Austria.
⁵ Breast Imaging Section, Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.

Received March 11, 2002; accepted after revision May 17, 2002.

 
Address correspondence to G. Pfarl.

Abstract

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OBJECTIVE. The aim of our study was to determine the false-negative rate of stereotactic 11-gauge vacuum-assisted biopsy in a validation study of lesions that had subsequent surgical excision.

MATERIALS AND METHODS. Retrospective review was performed of 318 lesions that underwent stereotactic 11-gauge vacuum-assisted biopsy and subsequent surgical excision. A false-negative case was defined as a pathologically proven cancer in which stereotactic biopsy yielded benign results without atypia. Medical records, imaging studies, and histologic findings were reviewed.

RESULTS. False-negative findings were encountered at stereotactic 11-gauge vacuum-assisted biopsy in 3.3% (7/214) of pathologically proven cancers. False-negative findings occurred in 3.5% (4/115) of malignant calcification lesions versus 3.0% (3/99) of malignant masses (p = 1.0). The seven false-negative findings included five Breast Imaging Reporting and Data System (BI-RADS) category 5 lesions that yielded benign results at biopsy, one BI-RADS category 4 mass that benign breast tissue, and one BI-RADS category 4 cluster of calcifications in which no calcifications were retrieved. The false-negative rate was 10.0% (6/60) for radiologists who performed 15 or fewer previous stereotactic vacuum-assisted biopsy procedures versus 0.6% (1/154) for radiologists who performed more than 15 previous stereotactic vacuum-assisted biopsy procedures (p = 0.002).

CONCLUSION. Stereotactic 11-gauge vacuum-assisted biopsy had a false-negative rate of 3.3% that diminished to 0.6% with experience. All false-negative findings could be prospectively identified because of failure to sample calcifications or imaging-histologic discordance.

Introduction

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For the past decade, stereotactic biopsy has been increasingly used for the histologic diagnosis of breast lesions. In the 1990s, several investigators reported the results of validation studies in which consecutive lesions underwent stereotactic automated core biopsy and subsequent surgical excision [1,2,3,4,5,6,7,8]. These validation studies showed concordance between results of stereotactic 14-gauge automated core biopsy and surgical biopsy in 87-100% of cases and reported that stereotactic 14-gauge automated core biopsy had a false-negative rate of 3-8% [1, 2, 5,6,7,8].

Stereotactic 11-gauge vacuum-assisted biopsy technology is now available and has several advantages compared with automated core biopsy, including better calcification retrieval [9], fewer histologic underestimates [10,11,12], and a lower rebiopsy rate [13]. Although numerous clinical investigations of stereotactic 11-gauge vacuum-assisted biopsy have been conducted, there are no (to our knowledge) published validation studies of this method. We present the results of a large series of lesions that underwent stereotactic 11-gauge vacuum-assisted biopsy followed by subsequent surgical excision that can provide validation data for the biopsy technique.

Materials and Methods

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Biopsy Technique
Retrospective review was performed of medical records of the first 332 lesions that had stereotactic biopsy with an 11-gauge vacuum-assisted probe (Mammotome; Ethicon Endo-Surgery, Cincinnati, OH) at our institution, the University of Vienna Medical School, a referral center, from September 1997 to December 2001. These 332 lesions occurred in 325 patients having a median age of 56 years (range, 28-83 years). Stereotactic biopsy was offered for histologic diagnosis of lesions that were suspicious for or highly suggestive of malignancy provided that the patient was able to cooperate with the procedure and did not have a bleeding diathesis. Informed consent was obtained for all stereotactic biopsy procedures.

Stereotactic biopsy was introduced at our institution in 1994. From 1994 to 1997, all stereotactic biopsies were performed with automated core needles. The 14-gauge vacuum-assisted probe (Mammotome, Ethicon Endo-Surgery) was introduced in July 1997, and the 11-gauge vacuum-assisted biopsy probe was introduced in September 1997. During the study period, stereotactic 14-gauge vacuum-assisted biopsy was performed in 521 lesions; the choice of 14- or 11-gauge vacuum-assisted biopsy was made at the discretion of the radiologist performing the biopsy.

Among the 332 lesions that underwent stereotactic 11-gauge vacuum-assisted biopsy, 251 had biopsy performed by one of seven attending radiologists specializing in breast imaging, who had performed an average of 2.6 (range, 0-18) stereotactic 14-gauge vacuum-assisted biopsy procedures before the beginning of this study. The remaining 81 lesions underwent biopsy by a resident in training who had not performed stereotactic biopsy before the study period, under the supervision of an attending radiologist.

Biopsies were performed with patients prone on a dedicated table (Mammotest; Fischer Imaging, Denver, CO). An average of 15-20 specimens were obtained per lesion. Among the 332 lesions that had stereotactic 11-gauge biopsy during this period, 318 had subsequent surgical excision and constitute the basis of this article. Mammographic findings in these 318 lesions were calcifications without mass in 166 (52.2%), mass without calcifications in 84 (26.4%), mass with calcifications in 44 (13.8%), asymmetric densities in 19 (6.0%), and architectural distortions in five (1.6%). Median mammographic lesion size was 14.9 mm (range, 3-51 mm).

Management Protocol
In our institution, our surgeons preferred to use stereotactic biopsy as a preoperative investigation that was performed in addition to (not in lieu of) surgery. If cancer was found at stereotactic biopsy, the surgeon performed a therapeutic operation, including axillary surgery if indicated. If stereotactic biopsy yielded atypia or other specific lesions such as a radial scar or possible phyllodes tumor, the surgeon performed a wide excision. If stereotactic biopsy yielded benign findings concordant with imaging features, the surgeon usually performed a surgical excision but would take less tissue than in an excision performed after stereotactic diagnosis of cancer or atypia. For women with benign lesions, the use of stereotactic biopsy in addition to, rather than in lieu of, surgical biopsy resulted in more procedures and higher cost, but that was the preference of our referring clinicians and was a practice of which patients were aware before undergoing the stereotactic biopsy procedure.

Data Collection and Analysis
Medical records were reviewed by a radiologist specializing in breast imaging to determine the pre-biopsy classification of lesion type, size, and level of suspicion according to the Breast Imaging Reporting and Data System (BI-RADS) [14] as probably benign (BI-RADS category 3), suspicious (category 4), or highly suggestive of malignancy (category 5). Medical records and histologic findings were reviewed to determine surgical outcomes.

Stereotactic biopsy results were considered discordant if the histologic findings did not provide a sufficient explanation for the imaging features [15]. A pathologically proven cancer was a lesion that yielded cancer at either stereotactic biopsy, surgery, or both, confirmed at subsequent pathology review. A false-negative finding was defined as a pathologically proven cancer in which stereotactic biopsy yielded benign findings with no atypia [16].

Data were entered into a computerized spread-sheet (Excel; Microsoft, Redmond, WA) for analysis. Statistical analyses were performed with statistical software (Epi-Info; Centers for Disease Control, Atlanta, GA) using the chi-square and Fisher's exact tests.

Results

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Stereotactic and Surgical Histology
In these 318 lesions, stereotactic biopsy yielded benign findings in 100 (31.4%), atypical ductal hyperplasia in 17 (5.3%), ductal carcinoma in situ (DCIS) in 91 (28.6%), and infiltrating cancer in 110 (34.6%) (Table 1). Of 201 stereotactically proven cancers, surgery revealed cancer in 199; in two stereotactically proven cancers, stereotactic biopsy yielded DCIS but surgery showed atypical ductal hyperplasia and biopsy site change. Histologic review of these two cases confirmed the presence of DCIS in the stereotactic biopsy material, suggesting that the DCIS was completely removed at stereotactic biopsy. No false-positive findings were encountered.

Among 17 lesions yielding atypical ductal hyperplasia at stereotactic 11-gauge vacuum-assisted biopsy, surgery revealed carcinoma in six (35.3%). Among 91 lesions yielding DCIS at stereotactic 11-gauge vacuum-assisted biopsy, surgery revealed invasive carcinoma in 11 (12.1%). Among two lesions yielding papilloma, two lesions yielding phyllodes tumor, and one lesion yielding a radial scar at stereotactic biopsy, all were confirmed at surgery to be benign. Among 13 lesions yielding discordant results, surgery revealed carcinoma in seven (53.8%).

The final histologic diagnosis, based on review of stereotactic and subsequent surgical pathology, was cancer in 214 lesions, including 201 lesions that yielded cancer at stereotactic biopsy, six lesions that yielded atypical ductal hyperplasia at stereotactic biopsy, and seven lesions in which stereotactic biopsy yielded benign findings without atypia (Table 1).

False-Negative Findings
False-negative findings were encountered in seven lesions (Table 2). The median mammographic size of these seven lesions was 0.9 cm (range, 0.5-2.0 cm). Mammographic findings in these seven cases were calcifications in four, mass in two, and both in one. Five (71%) of the seven missed cancers were prospectively classified as BI-RADS category 5 and two (29%), as BI-RADS category 4. The median number of specimens obtained in these seven lesions was 16 (range, 15-20).

Stereotactic biopsy histology in these seven false-negative cases was benign breast tissue in four and fibrocystic mastopathy in three (including two with duct hyperplasia). Surgical histology in these missed cancers was infiltrating ductal carcinoma in four, infiltrating lobular carcinoma in one, and DCIS in two. The median histologic size of infiltrating carcinoma was 1.1 cm (range, 0.6-1.7 cm). In all patients with infiltrating carcinoma, the lymph nodes were negative for cancer.

In two missed cancers that were evident as clusters of pleomorphic calcifications (BI-RADS category 5), calcifications were present on specimen radiographs but were not seen histologically. Stereotactic biopsy revealed benign breast tissue without calcifications in both cases; surgical excision yielded DCIS in one and infiltrating ductal carcinoma in the other. In one missed cancer that was evident as a cluster of amorphous calcifications (BI-RADS category 4), specimen radiography was not performed (a deviation from our protocol); no calcifications were seen at histologic analysis. Stereotactic biopsy revealed fibrocystic mastopathy; surgical excision showed infiltrating ductal carcinoma.

In one missed cancer that was evident as a cluster of pleomorphic calcifications (BI-RADS category 5), calcifications were identified at specimen radiography and at histologic analysis; stereotactic biopsy yielded benign breast tissue with calcifications, and surgery revealed DCIS. Review of stereotactic images in that case suggested that the calcifications that were targeted did not correspond to the most suspicious calcifications in that region.

In one missed cancer evident as a spiculated mass with calcifications (BI-RADS category 5), calcifications were not identified at either specimen radiography or histologic analysis; stereotactic biopsy yielded fibrocystic change without calcifications, and surgical excision yielded infiltrating ductal carcinoma. In one missed cancer evident as a spiculated mass (BI-RADS category 5), stereotactic biopsy revealed benign breast tissue, and surgery showed infiltrating ductal carcinoma. Review of the stereotactic images suggests that needle placement may have been suboptimal. In one missed cancer evident as an indistinct mass (BI-RADS category 4), the lesion was subtle and difficult to target; on the postbiopsy mammogram, the area sampled appeared to be slightly caudad to the lesion. Stereotactic biopsy revealed benign breast tissue; surgery revealed infiltrating lobular carcinoma.

False-negative findings were encountered in seven of 214 histologically proven cancers in this study, for a false-negative rate of 3.3%. False-negative findings were encountered in 3.5% (4/115) of malignant calcification lesions versus 3.0% (3/99) of malignant masses (p = 1.0). In six (85.7%) of the seven false-negative cases, the biopsy was performed by an operator who had previously performed 15 or fewer stereotactic vacuum-assisted biopsy procedures (Table 2). The false-negative rate was 10.0% (6/60) for radiologists who performed 15 or fewer previous stereotactic vacuum-assisted biopsy procedures versus 0.6% (1/154) for radiologists who performed more than 15 previous stereotactic vacuum-assisted biopsy procedures (p = 0.002).

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
In pioneering studies in the 1990s, Parker et al. [1, 2] and others [3,4,5,6,7,8] reported the results of lesions that underwent stereotactic automated core biopsy and subsequent surgical excision (Table 3). These validation studies included 1043 lesions, of which 387 were malignant [1,2,3,4,5,6,7,8]. Among the studies that used only 14-gauge automated needles [2, 5, 6], false-negative rates ranged from 3% to 8% (mean, 6%) (Table 3). When stereotactic vacuum-assisted biopsy was introduced [17], stereotactic automated core biopsy was in widespread clinical use. Numerous clinical investigations of stereotactic vacuum-assisted biopsy were performed, but no validation study in consecutive lesions with surgical correlation has yet (to our knowledge) been reported.

In our study, we found false-negative cases in seven (3.3%) of 214 pathologically proven cancers that underwent stereotactic 11-gauge vacuum-assisted breast biopsy. Among radiologists who had performed more than 15 previous stereotactic biopsies, the false-negative rate was 0.6%. These false-negative rates, which include our learning experience for the 11-gauge method, compare favorably with the 3-8% range reported in the validation studies of stereotactic 14-gauge automated core biopsy [2, 5, 6], as well as the 0-8% (mean, 2%) range of false-negative rates reported in studies of needle localization and surgical biopsy [18]. All missed cancers could be recognized prospectively because of failure to identify calcium on specimen radiographs, failure to identify calcium at histologic analysis, imaging—histologic discordance, or a combination of these features.

Imaging—histologic discordance occurred in all seven missed cancers at stereotactic 11-gauge vacuum-assisted biopsy. These seven lesions included five BI-RADS category 5 lesions that yielded benign results, one BI-RADS category 4 mass that yielded benign breast tissue, and one BI-RADS category 4 cluster of calcifications in which no calcifications were retrieved. Imaging—histologic discordance has been reported in 0-6% (mean, 4%) of lesions that had percutaneous imaging-guided biopsy in previous studies; among discordant lesions, cancer has been found in 0-64% (mean, 18%) [13, 15, 16, 19,20,21]. Imaging—histologic discordance is an indication for repeating biopsy because of the high prevalence of carcinoma in these discordant lesions [15].

Failure to identify calcifications on specimen radiographs, which occurred in one of our false-negative cases, has been previously shown to correlate with nondiagnostic results at stereotactic biopsy. Liberman et al. [22] found that the likelihood of obtaining diagnostic material at stereotactic biopsy was significantly greater if calcifications were present on specimen radiographs than if they were absent (81% vs 38%, p < 0.001). If the stereotactic biopsy is performed for calcifications and yields benign findings with no calcifications on specimen radiography, a repeated biopsy is generally warranted. Identification of calcifications at histologic analysis in the absence of calcifications on the specimen radiographs is usually not adequate, because calcifications may be seen microscopically in lesions that lack calcifications on the mammogram [23, 24].

Failure to identify calcifications at histologic analysis occurred in four calcific lesions that yielded false-negative results. In two of these four cases, calcifications were identified at specimen radiography but not at histologic analysis. In this scenario, which can also occur at surgical biopsy, the pathologist should obtain deeper levels from the biopsy material and should look at the tissue with polarized light to search for calcium oxalate (weddellite) crystals [22, 25]. If these maneuvers fail to yield calcifications, the need for rebiopsy is determined on the basis of the specific imaging findings before and after biopsy and the histologic diagnosis. If review of the pre- and postbiopsy mammograms and specimen radiographs indicates that the calcifications were well sampled and the diagnosis is otherwise concordant, rebiopsy may not be necessary; however, if the sampling was poor or the diagnosis is discordant, rebiopsy is indicated.

False-negative cases were significantly more frequent among radiologists who had performed 15 or fewer previous stereotactic biopsy procedures than among radiologists who had performed more than 15 procedures (10.0% vs 0.6%, p = 0.002). Liberman et al. [26] described a learning curve for stereotactic 11-gauge vacuum-assisted breast biopsy, with a greater false-negative rate for the first 15 cases than for subsequent cases (7.4% vs 0%, p < 0.06). In that study, the learning curve existed for stereotactic 11-gauge vacuum-assisted biopsy among radiologists who had a prior collective experience of more than 500 cases with stereotactic 14-gauge automated core or 14-gauge vacuum-assisted biopsy [26]. Our findings lend further support to the importance of operator experience in achieving optimal results for stereotactic biopsy and reinforce the need for training and supervision early in one's experience performing the procedure.

In conclusion, we found that stereotactic 11-gauge vacuum-assisted breast biopsy had a false-negative rate of 3.3%, which decreased to 0.6% with experience. All false-negative findings could be prospectively identified because of failure to sample calcifications or imaging—histologic discordance. These findings, which show accuracy comparable to that of surgical biopsy, validate the use of stereotactic 11-gauge biopsy as an alternative to needle localization and surgical excision, as currently practiced in many centers throughout the world. Our data indicate the importance of experience in optimizing the outcome of stereotactic 11-gauge vacuum-assisted biopsy. Careful attention to identification of calcifications at specimen radiography and at histologic analysis for calcific lesions and imaging—histologic correlation for all lesions can enable prospective identification of missed cancers and avoid a delay in diagnosis.

References

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