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1
Department of Radiology, Brigham and Women's Hospital, 75 Francis St., Boston,
MA 02115.
2
Department of Pathology, Brigham and Women's Hospital, Boston, MA 02115.
3
Department of Surgery, Brigham and Women's Hospital, Boston, MA 02115.
Received January 28, 2000;
accepted after revision May 2, 2000.
Address correspondence to M. L. Rosenfield Darling.
Abstract
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SUBJECTS AND METHODS. Evaluation of 428 large-core needle biopsies yielding atypical ductal hyperplasia (139 lesions) or ductal carcinoma in situ (289 lesions) was performed. The results of subsequent surgical excision were retrospectively compared with the needle biopsy results.
RESULTS. For lesions initially diagnosed as ductal carcinoma in situ, underestimation of invasive ductal carcinoma was significantly less frequent using the 11-gauge directional vacuum-assisted biopsy device when compared with the automated 14-gauge needle (10% versus 21%, p < 0.05) but was not significantly less frequent when compared with the 14-gauge directional vacuum-assisted device (10% versus 17%, p > 0.1). For lesions diagnosed initially as atypical ductal hyperplasia, underestimation of ductal carcinoma in situ and invasive ductal carcinoma was significantly less frequent using the 11-gauge directional vacuum-assisted biopsy device compared with the 14-gauge directional vacuum-assisted device (19% versus 39%, p = 0.025) and with the automated 14-gauge needle (19% versus 44%, p = 0.01).
CONCLUSION. The frequency of histologic underestimation of breast carcinoma in lesions initially diagnosed as atypical ductal hyperplasia or ductal carcinoma in situ using large-core needle biopsy is substantially lower with the 11-gauge directional vacuum-assisted device than with the automated 14-gauge needle and with the 14-gauge directional vacuum-assisted device.
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Despite improvements in technique, histologic underestimation of disease frequently occurs when lesions initially diagnosed using large-core needle biopsy as either atypical ductal hyperplasia or ductal carcinoma in situ are excised surgically. Previous reports have cited underestimation rates ranging from 11% to 75% for atypical ductal hyperplasia (subsequently diagnosed as ductal carcinoma in situ or invasive ductal carcinoma after surgical excision) and from 15% to 35% for ductal carcinoma in situ (subsequently diagnosed as invasive ductal carcinoma) using an automated 14-gauge needle [4, 8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23]. The few groups of researchers evaluating the directional vacuum-assisted device with a 14-gauge needle have shown improvement in underestimation rates ranging from 0% to 38% for atypical ductal hyperplasia and from 0% to 19% for ductal carcinoma in situ [14, 16, 17, 23]. Recent experiences with the 11-gauge directional vacuum-assisted device have been reported that suggest further slight improvement, citing underestimation rates of from 10% to 27% for atypical ductal hyperplasia and from 4% to 15% for ductal carcinoma in situ [20, 22,23,24,25,26].
This investigation was undertaken to evaluate the results of surgical excision of a large series of atypical ductal hyperplasia and ductal carcinoma in situ lesions diagnosed using large-core needle biopsy. The frequencies of histologic underestimation of lesions diagnosed using the automated 14-gauge needle, the 14-gauge directional vacuum-assisted device, and the 11-gauge directional vacuum-assisted device were compared.
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There were 292 cases of ductal carcinoma in situ (252 clusters of calcifications and 40 masses) and 148 cases of atypical ductal hyperplasia (122 clusters of calcifications and 26 masses) for a total of 440 lesions in 413 patients. Patients ranged in age from 24 to 89 years, with a mean age of 54 years and a median age of 52 years. Lesion size ranged from 2 to 80 mm (mean, 12.6 mm) for ductal carcinoma in situ lesions and from 2 to 41 mm (mean, 9.7 mm) for atypical ductal hyperplasia lesions. Surgical excision with preoperative wire localization of each of these 440 lesions was recommended and was performed in 428 (97.3%). The final histologic diagnosis was compared with the large-core needle biopsy diagnosis. Among the 12 patients who did not undergo surgery were two with ductal carcinoma in situ and three with atypical ductal hyperplasia who refused surgery and elected for mammographic follow-up at 6-month intervals. The remaining seven were patients with atypical ductal hyperplasia (n = 6) and ductal carcinoma in situ (n = 1) who delayed surgical excision.
Of the 428 biopsies yielding ductal carcinoma in situ or atypical ductal hyperplasia for which surgical follow-up was obtained, 403 were performed using stereotactic guidance on a dedicated stereotactic core biopsy unit (Mammotest [August 1991 through August 1994], Fischer Imaging, Denver, CO; and DSM [September 1994 through December 1999], Lorad, Danbury, CT), which was equipped with digital imaging beginning in 1993. Sixty-seven biopsies (40 calcifications and 27 masses) were performed with a 14-gauge automated biopsy device using the multiple-pass technique [4]; four to 11 core samples (mean, 7 samples) were obtained from each cluster of calcifications and three to eight core samples (mean, 5 samples) were obtained from each mass. From May 1996 through December 1999, all stereotactic biopsies were performed with a directional vacuum-assisted biopsy device (Mammotome; Ethicon Endo-Surgery, Cincinnati, OH) using a standardized technique that has been previously described [7]. These included 75 lesions (69 clusters of calcifications and 6 masses) biopsied with a 14-gauge needle (4-15 core samples; mean, 8 samples) and 261 lesions (255 clusters of calcifications and 6 masses) biopsied with an 11-gauge needle (5-22 core samples; mean, 9 samples). For calcification sampling, if a specimen radiograph did not show any particles of calcification, additional samples were removed [27]. Samples of targeted calcifications were obtained in all cases. For stereotactic biopsies using the 11-gauge directional vacuum-assisted biopsy device, if complete mammographic removal of the lesion occurred, a 2 x 2 mm radiopaque localizing clip (MicroMark; Ethicon Endo-Surgery) was inserted into the biopsy site to provide an accurate target for wire localization before excisional biopsy should it be necessary [23, 28, 29].
The remaining 25 lesions yielding ductal carcinoma in situ or atypical ductal hyperplasia on large-core needle biopsy were masses that were biopsied with an automated 14-gauge biopsy needle using sonographic guidance with a 7.5-MHz linear array transducer (AI Performa Plus; Acoustic Imaging, Denver, CO). From four to eight core samples (mean, 5 samples) were obtained from each mass. No calcification clusters were sampled using sonographic guidance.
Comparison was made between the histologic diagnosis based on large-core needle biopsy specimens and that based on surgically excised specimens for each lesion. A lesion was considered to be an underestimation if the surgical results yielded a discordant, higher grade lesion—that is, an underestimation was a lesion diagnosed using large-core needle biopsy results as atypical ductal hyperplasia but found at surgical excision to be ductal carcinoma in situ or invasive ductal carcinoma. Similarly, an underestimation was a lesion diagnosed initially as ductal carcinoma in situ but found at surgery to be invasive ductal carcinoma. If no residual atypical ductal hyperplasia or ductal carcinoma in situ was found in an accurately localized surgical specimen (needle biopsy tract identified), the lesion was considered to have been completely excised at the time of the large-core needle biopsy. The lesions for which the large-core needle biopsy diagnosis was the same as the surgical diagnosis were considered to be concordant.
Statistical analysis was performed using either the chi-square test or Fisher's exact test when appropriate. Statistical significance was assigned a p value of less than 0.05.
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Of the 139 lesions diagnosed as atypical ductal hyperplasia using large-core needle biopsy, 38 (27%) were found at surgical excision to be either ductal carcinoma in situ (27 lesions) or invasive ductal carcinoma (11 lesions) for the three devices combined. With the automated 14-gauge needle, 11 (44%) of 25 lesions (8 ductal carcinoma in situ and 3 invasive ductal carcinoma) were underestimated. With the 14-gauge directional vacuum-assisted biopsy device, 11 (39%) of 28 lesions (8 ductal carcinoma in situ and 3 invasive ductal carcinoma) were underestimated. With the 11-gauge directional vacuum-assisted biopsy device, 16 (19%) of 86 lesions (11 ductal carcinoma in situ and 5 invasive ductal carcinoma) were underestimated (Table 2). When these results are compared, the number of underestimations with the 11-gauge directional vacuum-assisted biopsy device is significantly lower than that with the automated 14-gauge needle (p = 0.01) and that with the 14-gauge directional vacuum-assisted biopsy device (p = 0.025). Differences between the 14-gauge directional vacuum-assisted device and the automated 14-gauge needle did not reach statistical significance (p > 0.5).
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The initial lesion was completely excised at the time of core biopsy with no residual ductal carcinoma in situ or atypical ductal hyperplasia in the surgical specimen in 12 (13%) of 92 lesions with the automated 14-gauge needle, 10 (13%) of 75 lesions with the 14-gauge directional vacuum-assisted biopsy device, and 56 (30%) of 185 lesions with the 11-gauge directional vacuum-assisted biopsy device. The slight increase in the rate of complete excision with the 11-gauge directional vacuum-assisted biopsy device compared with the 14-gauge needles was not statistically significant (p > 0.1). For all needle types combined, atypical ductal hyperplasia lesions were significantly more frequently completely excised than were ductal carcinoma in situ lesions (42% versus 6%, p < 0.001). For each needle type evaluated separately, complete excision of atypical ductal hyperplasia lesions was significantly more frequent than of ductal carcinoma in situ lesions with the 11-gauge directional vacuum-assisted device (p < 0.001) and with the automated 14-gauge needle (p < 0.001). Differences in complete excision were not statistically significant when the two types of lesion were compared for the 14-gauge directional vacuum-assisted biopsy device (p = 0.08).
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The development of the directional vacuum-assisted biopsy device and the introduction of the 11-gauge needle has allowed improved accuracy in sampling clusters of calcifications and masses [7, 16, 17, 20, 22,23,24, 26]. Although the number of lesions in each of the prior series was relatively small, the collective data provided by these investigators indicate a decrease in the rate of histologic underestimation when comparing the 14-gauge automated needle with either the 14-gauge directional vacuum-assisted biopsy device or the 11-gauge directional vacuum-assisted biopsy device. The 11-gauge directional vacuum-assisted biopsy device removes a larger quantity of tissue per sample (96 mg) than the 14-gauge directional vacuum-assisted biopsy device (40 mg) and the automated 14-gauge needle (17 mg) [5, 6]. Calcification retrieval and complete mammographic lesion removal are more likely with the directional vacuum-assisted biopsy device instrument [7, 17, 25]. These improvements in tissue acquisition afforded by the newer device have diminished, but not eliminated, the problem of underestimation.
Regarding underestimations of invasive ductal carcinoma that yielded only ductal carcinoma in situ on large-core needle biopsy, our findings of a 21% underestimation rate for the automated 14-gauge needle, 17% for the 14-gauge directional vacuum-assisted biopsy device, and 10% for the 11-gauge directional vacuum-assisted biopsy device are consistent with the work of other investigators and depict this trend toward increased accuracy. Previously reported underestimations range from 15% to 67% for ductal carcinoma in situ diagnosed using the 14-gauge automated needle [4, 8, 10, 12, 17, 18, 20, 21]. This wide variability is likely caused by the small number of cases in some of these studies (range, 3-55 cases; mean, 26.5 cases). Burbank [17] found an underestimation rate of 0% of 32 ductal carcinoma in situ lesions biopsied with the 14-gauge directional vacuum-assisted biopsy device, although lesion size, biopsy technique, and patient age were comparable with our series; this difference may be caused by the larger average number of specimens per lesion (and therefore the lower chance of sampling error) obtained in his study (mean, 26 specimens) compared with our study (mean, 8 specimens). For the 11-gauge directional vacuum-assisted biopsy device, the previous series have shown underestimation rates of from 4% to 15% [20, 23, 24], similar to our findings. One additional series of 12 cases of ductal carcinoma in situ lesions reported by Liberman et al. [25] yielded zero underestimations. In this study, the mean number of specimens was greater than that in our series (15 versus 9 specimens), and this difference combined with the small number of cases may explain the lower underestimation rate compared with our data (Table 3).
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Evaluation of our data for the automated 14-gauge needle reveals that the overall underestimation rate of ductal carcinoma in situ and invasive ductal carcinoma for lesions yielding only atypical ductal hyperplasia on large-core needle biopsy is 44%. Results of underestimation rates from prior studies [4, 8, 9, 11,12,13,14,15,16,17,18,19, 21,22,23] have ranged from 11% to 75%, with sample sizes of from two to 54 cases (mean, 22.4 cases), which is comparable with our series. The largest series was reported by Jackman et al. [16] in which 54 lesions yielding atypical ductal hyperplasia on large-core needle biopsy were surgically excised; 18 ductal carcinoma in situ lesions and eight invasive ductal carcinoma lesions were found for an overall underestimation rate of 48%. The lowest reported rate of underestimation for the automated 14-gauge needle is 11% by Lin et al. [19]. In this series, 18 lesions were diagnosed as atypical ductal hyperplasia on large-core needle biopsy; one lesion proved to be ductal carcinoma in situ after immediate excision, and one proved to be ductal carcinoma in situ after excision when the calcifications recurred at an unspecified follow-up interval. These investigators did not specify the mean number of core specimens obtained but state that it was "rarely more than six" (Table 4).
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Evaluation of the 14-gauge directional vacuum-assisted biopsy device in our experience shows an underestimation rate of 39% for core biopsies yielding atypical ductal hyperplasia. This finding compares favorably with that of a series [23] that reported a 38% underestimation rate for this device, with 24 atypical ductal hyperplasia lesions yielding seven ductal carcinoma in situ and two invasive ductal carcinoma lesions at excision. Both of these rates are higher than the two rates reported in the other large series for this device: Burbank [17] had a 0% underestimation rate for eight lesions, and Jackman et al. [16] showed an overall underestimation of 18% for 74 atypical ductal hyperplasia lesions yielding 10 ductal carcinoma in situ and three invasive ductal carcinoma lesions at surgery. In these latter two reports, the mean number of tissue specimens was greater than that in our series, 27 and 15.8 core specimens, respectively, compared with a mean of eight core specimens. Other factors such as lesion size, biopsy technique, and patient age are comparable; therefore, the lower average number of specimens obtained may again account for the higher rate of underestimation that we report in this group (Table 4).
For the 86 biopsies performed with the 11-gauge directional vacuum-assisted biopsy device yielding atypical ductal hyperplasia, the underestimation rate for ductal carcinoma in situ and invasive carcinoma was 19%. Brem et al. [26] and Philpotts et al. [22] have recently reported similar results in their series with underestimation rates of 25% (4 of 16 lesions) and 26.7% (4 of 15 lesions), respectively. In an evaluation of calcium retrieval, Liberman et al. [24] reported a slightly lower underestimation rate, with one (10%) of 10 atypical ductal hyperplasia lesions revealing ductal carcinoma in situ at excision. Compared with the findings of Liberman et al., our mean number of core specimens was lower, with nine specimens versus 14 specimens. Because other factors were comparable, a smaller number of specimens combined with a larger number of cases may also account for the difference in this group (Table 4).
We have shown that in our series of large-core biopsies, use of the 11-gauge directional vacuum-assisted biopsy device results in the lowest rate of underestimation of disease for lesions initially diagnosed as atypical ductal hyperplasia or ductal carcinoma in situ when compared with other widely used needle types. On the basis of our experience, our current practice is to sample all suspicious calcifications judged to be amenable to stereotactic biopsy using the 11-gauge directional vacuum-assisted biopsy device. If atypical ductal hyperplasia or ductal carcinoma in situ is diagnosed on the basis of the large-core needle biopsy, surgical excision is recommended. Although our average number of core specimens obtained with the 11-gauge needle was less than that of those few studies showing lower underestimation rates, the sample sizes of the other studies were small. Evaluation of a larger number of cases would be needed to determine the optimal number of core specimens required to significantly lower the underestimation rate while at the same time to minimize the risk of complications such as bleeding or infection. At this point, our practice is to obtain an average of nine core specimens and to confirm radiographically that the targeted calcifications are in the specimens. The 14-gauge directional vacuum-assisted device and the automated 14-gauge needle are not currently used for stereotactic biopsy of calcifications at our institution.
If a suspicious mass is visible sonographically, large-core needle biopsy is performed at our institution with an automated 14-gauge needle; direct sonographic visualization of the needle within the mass at the time of the biopsy is used to confirm targeting accuracy. For masses that are also visible mammographically, an 11-gauge stereotactic biopsy is performed only if the operator deems the mass too small or indistinct to target accurately under sonographic guidance. Although the data presented in this study show that the 11-gauge directional vacuum-assisted device has a lower underestimation rate than the automated 14-gauge needle for all lesions combined, the number of masses was small and therefore no statistically meaningful information can be obtained regarding masses alone. Our current practice regarding biopsy of masses has not changed on the basis of the results of this study.
When no residual atypical ductal hyperplasia or ductal carcinoma in situ was identified histologically after a large-core needle biopsy in an adequately localized surgical specimen, the lesion was considered to have been completely excised at the time of core biopsy. Complete excision occurred in 13% of our cases when the automated 14-gauge needle was used, in 13% of cases when the 14-gauge directional vacuum-assisted biopsy device was used, and in 20% of cases when the 11-gauge directional vacuum-assisted biopsy device was used. The larger volume of tissue per specimen obtained by the 11-gauge needle likely accounts for the higher incidence of complete lesion removal in this group, although the difference was not statistically significant (p > 0.1) [6]. For all needles combined, atypical ductal hyperplasia lesions (42%) were statistically more likely to have been completely removed than were ductal carcinoma in situ lesions (6%) (p < 0.001). The smaller size of atypical ductal hyperplasia lesions in this series (range, 2-41 mm; mean, 9.7 mm) compared with that of the ductal carcinoma in situ lesions (range, 2-80 mm; mean, 12.6 mm) may account for this difference.
Complete histologic removal at diagnostic stereotactic biopsy has been described previously. For atypical ductal hyperplasia and ductal carcinoma in situ lesions, Burbank [17] found higher rates of complete histologic removal using the 14-gauge directional vacuum-assisted biopsy device (18%) than using the automated 14-gauge needle (4%). Another study reported that in five (18%) of 28 lesions diagnosed as ductal carcinoma in situ using the 11-gauge directional vacuum-assisted biopsy device, no residual ductal carcinoma in situ was found at surgical excision [23]. Liberman et al. [25] examined 12 lesions diagnosed as ductal carcinoma in situ using 11-gauge directional vacuum-assisted needle biopsy in which the mammographic lesion was completely removed at the time of the biopsy—that is, no residual abnormality was visible. Histologically, only 25% of these lesions had no residual ductal carcinoma in situ at the site at surgical excision. Of three invasive cancers in this series that were also mammographically completely removed at the time of biopsy, all had residual invasive carcinoma at surgery. Importantly, Liberman et al. caution that on the basis of their data, complete mammographic removal of a lesion at the time of percutaneous large-core needle biopsy does not ensure complete histologic removal and cannot be used as a measure of the adequacy of lesion removal. Although our study and the work of others have shown that complete histo-logic removal of atypical ductal hyperplasia and ductal carcinoma in situ lesions can occur using the currently available large-core needle biopsy techniques, further investigation is warranted before attempting to use the percutaneous vacuum-assisted technique as a therapeutic tool. In our current practice, no attempt is made to completely mammographically remove a lesion at the time of large-core needle biopsy.
In summary, the data presented here confirm that histologic underestimation of disease may occur with imaging-guided large-core needle biopsy when the core specimens yield atypical ductal hyperplasia or ductal carcinoma in situ. The introduction of the directional vacuum-assisted biopsy instrument and the use of the 11-gauge needle have substantially diminished the likelihood of under-estimation. It is imperative that breast lesions diagnosed as yielding either atypical ductal hyperplasia or ductal carcinoma in situ using large-core needle biopsy results still undergo surgical excision to exclude the presence of a higher grade lesion that may have been missed because of sampling error.
Acknowledgments
We thank Lisa Loftus-Smith for her help in preparation of this
manuscript.
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