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1
Department of Radiology, Breast Imaging Section, Memorial Sloan-Kettering
Cancer Center, 1275 York Ave., New York, NY 10021.
2
Department of Surgery, the Breast Service, Memorial Sloan-Kettering Cancer
Center, New York, NY 10021.
3
Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY
10021.
Received November 4, 1999;
accepted after revision January 12, 2000.
Supported by grant C015709 from the New York State Department of
Health.
Abstract
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MATERIALS AND METHODS. Of 1388 consecutive breast lesions that had percutaneous imaging-guided core biopsy, 155 (11%) were palpable. Palpable masses referred for percutaneous imaging-guided core biopsy included lesions that were small, deep, mobile, vaguely palpable, or multiple. Biopsy guidance was sonography in 140 lesions (90%) and stereotaxis in 15 (10%). Surgical correlation or minimum of 2 years follow-up is available in 115 palpable masses in 107 women. Medical records, imaging studies, and histologic findings were reviewed.
RESULTS. Of 115 palpable breast masses, 98 (85%) were referred by surgeons to the radiology department for percutaneous imaging-guided core biopsy and 88 (77%) had percutaneous imaging-guided core biopsy on the day of initial evaluation at our institution. Percutaneous imaging-guided core biopsy spared additional diagnostic tissue sampling in 79 (74%) of 107 women, including 57 women with carcinoma and 22 women with benign findings. Percutaneous imaging-guided core biopsy did not spare additional tissue sampling in 28 women (26%), including 15 women in whom surgical biopsy was recommended on the basis of percutaneous biopsy findings and 13 women with benign (n = 7) or malignant (n = 6) percutaneous biopsy findings who chose to undergo diagnostic surgical biopsy.
CONCLUSION. Percutaneous imaging-guided core biopsy is useful in the evaluation of palpable breast masses that are small, deep, mobile, vaguely palpable, or multiple. In this study, percutaneous imaging-guided core biopsy spared additional diagnostic tissue sampling in 74% women with palpable breast masses.
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Needle biopsy under the guidance of palpation is an alternative to surgical excision of palpable breast masses, but this approach has limitations. Palpation-guided fine-needle aspiration of palpable breast masses has a false-negative rate of 0-35%, a false-positive rate of 0-2%, and an insufficiency rate of 0-28% [2, 4,5,6,7,8]. Use of core needle biopsy as opposed to fine-needle aspiration can improve diagnostic yield and reduce or eliminate false-positive biopsies, but palpation-guided core needle biopsy has a false-negative rate of 0-36% and an insufficiency rate of 2-10% [6, 9,10,11]. The problems with palpation-guided needle biopsy may in part reflect difficulty positioning the needle within the lesion, and these problems have limited the widespread implementation of needle biopsy for palpable breast masses [12].
Percutaneous imaging-guided core biopsy is being increasingly used as an alternative to surgical biopsy for the diagnosis of nonpalpable breast lesions [13,14,15,16,17,18,19,20,21,22,23,24]. Validation studies of percutaneous imaging-guided 14-gauge automated core biopsy in which at least three specimens were obtained per lesion show false-negative rates of 0-5%, with 0% insufficient samples and 0% false-positive interpretations [14,15,16,17]. In the published literature, percutaneous imaging-guided 14-gauge automated core biopsy obviated surgical biopsy in 76-85% of nonpalpable lesions, decreasing the cost of diagnosis by 40-58% [18, 21,22,23,24].
Few data address the use of percutaneous imaging-guided core biopsy in the evaluation of breast masses that are palpable on physical examination [20, 25]. This study was undertaken to evaluate the utility of percutaneous imaging-guided core biopsy in the evaluation of palpable breast masses.
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Palpable lesions accounted for 155 (11%) of 1388 lesions that had percutaneous imaging-guided biopsy during this period, including 140 (33%) of 430 lesions that had sonographically guided biopsy and 15 (2%) of 958 lesions that had stereotactic biopsy. Palpable lesions were referred to the radiology department for imaging-guided percutaneous core biopsy at the discretion of the referring clinician. Women referred for imaging-guided percutaneous biopsy of palpable lesions primarily included those whose lesions were small, deep, mobile, or vaguely palpable; those in whom it was uncertain whether the palpable finding corresponded to the area of concern on the imaging study; and those who had multiple lesions warranting biopsy. In all women with palpable breast masses who underwent imaging-guided biopsy, a discrete mass was identified on sonography, mammography, or both methods.
All palpable lesions had biopsy with a 14-gauge automated needle (Automatic Cutting Needle, Manan Medical Products, Northbrook, IL; Biopty-Cut Needle, Bard Urological, Covington, GA; or Ultra-Core Biopsy Needle, Medical Device Technologies, Gainesville, FL) and a spring-loaded automated gun, with long excursion (Pro-Mag 2.2, Manan Medical Products; or Biopty, Bard Urological) in 154 lesions and with short excursion (Pro-Mag 1.2, Manan Medical Products) in one lesion. The median number of specimens obtained per lesion was four (range, 1-7); at least three specimens were obtained from 138 (89%) of the 155 lesions.
Treatment recommendations after percutaneous imaging-guided core biopsy were made in accordance with a previously described protocol [18, 21]. If percutaneous biopsy yielded carcinoma, the patient was referred for definitive treatment. If percutaneous biopsy yielded benign findings concordant with the imaging characteristics and physical examination, the patient was referred for imaging follow-up (usually at 1 year) and for follow-up physical examination as directed by her clinical physician. Surgical excision was recommended for specific histologic findings including atypical ductal hyperplasia, radial scar, and possible phyllodes tumors. Surgical excision was also recommended if suggested by the pathologist or if there was discordance between histologic findings and imaging features or physical findings [18, 21].
The patient was considered to have been spared additional diagnostic tissue sampling if percutaneous imaging-guided core biopsy yielded a benign finding for which surgery was neither recommended nor performed or if percutaneous biopsy yielded carcinoma for which the patient underwent treatment (either therapeutic surgery or chemotherapy) without additional biopsy procedures. Percutaneous imaging-guided core biopsy was not considered to have spared additional diagnostic tissue sampling if surgical biopsy was recommended, performed, or both.
Surgical correlation or minimum of 2 years follow-up are available in 115 palpable masses; these 115 masses constitute the basis of this article. Lesions were classified according to the Breast Imaging Reporting and Data System (BI-RADS) [26]. Medical records, imaging studies, and histologic findings were reviewed. The rate of and indications for rebiopsy and the frequency of sparing additional diagnostic tissue sampling were determined. Data were entered into a computerized spreadsheet program (Excel; Microsoft, Redmond, WA). Tests for statistical significance were performed with the chi-square test using a computerized statistics program (Epi-Info, Atlanta, GA). Exact confidence limits were calculated using the Geigy scientific tables [27].
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Referral, Timing, and Guidance for Biopsy
Of the 115 palpable masses, 98 (85%) were referred by surgeons to the
radiology department for imaging-guided biopsy. In 88 (77%) of the 115
palpable masses, percutaneous biopsy was performed on the day of initial
evaluation at our institution. Guidance for percutaneous biopsy was sonography
in 100 (87%) of 115 lesions and stereotaxis in 15 (13%). Reasons for choosing
stereotactic rather than sonographic guidance in 15 lesions were radiologist
preference in six, associated calcifications in four, lesion not seen on
sonography in three, and separate nonpalpable lesion undergoing stereotactic
biopsy in two. Percutaneous biopsy findings and outcome in these 115 palpable
masses are shown in Table
1.
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In six palpable masses in six women, the surgeon had performed fine-needle aspiration biopsy under the guidance of palpation before referring the patient for percutaneous imaging-guided core breast biopsy. In two of these women, palpation-guided fine-needle aspiration biopsy yielded benign results discordant with the imaging and physical findings (Fig. 1A,1B,1C,1D). In two women, palpation-guided fine-needle aspiration biopsy yielded atypical cells. In one woman who had prior ipsilateral breast-conserving surgery for carcinoma and in one woman who had stage IV breast cancer, palpation-guided fine-needle aspiration biopsy yielded malignant cells (adenocarcinoma), but the surgeon requested percutaneous imaging-guided core biopsy to obtain more detailed histologic results before definitive treatment. In all six of these women, percutaneous imaging-guided core biopsy yielded infiltrating ductal carcinoma.
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Malignant Lesions
In 69 (60%) of 115 lesions, percutaneous biopsy findings were malignant
(Figs.
1A,1B,1C,1D
and
2A,2B).
These 69 malignant lesions occurred in 63 women, all of whom were referred for
definitive treatment. Percutaneous biopsy revealed malignant lesions in six
(20%) of 30 women less than 40 years old, in 38 (68%) of 56 women between 40
and 59 years, and in 19 (90%) of 21 women 60 years old or older (p
< 0.0001). Of the 63 women with malignant findings at percutaneous biopsy,
three women had no subsequent surgery, two were treated with chemotherapy (for
stage IV breast cancer and metastatic endometrial cancer), and one declined
surgery. Surgery was performed after a malignant percutaneous diagnosis in 60
women. In six (10%) of these 60 women, the initial surgical procedure was an
excisional biopsy, which was performed because of patient or physician
preference.
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In 54 (90%) of 60 women who had surgery after a malignant diagnosis at percutaneous biopsy, the initial surgical procedure was a therapeutic operation, which was lumpectomy in 25 women and mastectomy in 29 women. The 29 women who had mastectomy as the first operation included 11 with two or more sites of carcinoma diagnosed percutaneously (Fig. 2A,2B) and six with percutaneous diagnosis of recurrent carcinoma after breast-conserving surgery. In 44 of 54 women who had therapeutic surgery after percutaneous diagnosis of carcinoma, axillary dissection (n = 42) or sentinel lymph node biopsy (n = 2) was performed during the initial surgery. Reasons for not performing axillary surgery during the initial operation in 10 women included prior axillary dissection (n = 6), age and comorbid conditions (n = 3), and percutaneous diagnosis of ductal carcinoma in situ (DCIS) (n = 1). A single therapeutic operation was performed in 47 (87%) of these 54 women, including 28 (97%) of 29 women treated with mastectomy and 19 (76%) of 25 women who had breast conservation.
Surgery confirmed the percutaneous biopsy diagnosis in 58 (97%) of 60 women with percutaneously diagnosed malignant lesions, including 57 women with infiltrating carcinoma and one woman with lymphoma. In the remaining two women, percutaneous biopsy yielded DCIS, but surgery revealed DCIS and infiltrating ductal carcinoma. In one of these two women, percutaneous biopsy of two lesions yielded DCIS with findings suspicious for microinvasion; mastectomy and level I axillary lymph node dissection were performed as the initial surgery. The other woman with a percutaneous diagnosis of DCIS had infiltrating carcinoma at mastectomy and returned for axillary dissection as a separate procedure. The median size of infiltrating carcinoma at surgery in 59 women was 2.2 cm (range, 0.2-9.0 cm); axillary surgery, performed in 48 women, revealed metastases in 18 (38%).
Benign Lesions
In 31 (27%) of 115 lesions, percutaneous biopsy yielded benign results
concordant with imaging and physical findings (Fig.
3A,3B,3C,3D).
These 31 benign palpable masses occurred in 29 women. Seven (23%) of these 31
benign palpable masses were subsequently excised because of patient or
physician preference at a median of 1.0 months (range, 0.4-3.0 months) after
percutaneous biopsy; all were benign at surgery. The remaining 24 benign
palpable masses were stable on follow-up (range, 24-69 months; median, 53
months). Stability was revealed on imaging follow-up (range, 24-69 months;
median, 54 months) in 18 lesions and at clinical follow-up (range, 27-65
months; median, 29 months) in six lesions. The six benign palpable masses with
clinical but no imaging follow-up occurred in four women, including three
women younger than 30 years old and one woman with a palpable mass (fat
necrosis) in a transverse rectus abdominis myocutaneous flap after
mastectomy.
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Surgical Biopsy
In 15 (13%) of 115 lesions, surgical biopsy was performed on the basis of
nonmalignant percutaneous biopsy findings. Correlation of percutaneous biopsy
and surgical histologic findings in these 15 lesions is shown in
Table 2. Of the 15 lesions for
which surgical biopsy was suggested, surgery revealed carcinoma in four (27%)
(Fig.
4A,4B,4C,4D).
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Multiple Lesions
In 17 women, percutaneous imaging-guided core biopsy was performed of two
or more lesions in the ipsilateral breast. In 13 of these 17 women, two or
more sites of carcinoma were found by percutaneous biopsy (Fig.
2A,2B).
Mastectomy was performed in 11 (85%) of these 13 women; breast conservation
was performed in two women, each of whom had two foci of carcinoma in close
proximity in the same quadrant. In two women, percutaneous biopsy revealed one
carcinoma and one benign lesion; both women had breast-conserving surgery. In
two women, percutaneous biopsy yielded two benign lesions and surgery was
avoided.
Overall Outcome
Of the 107 women who had percutaneous imaging-guided core biopsy of
palpable breast masses, 79 women (74%; 95% confidence interval [CI], 64-82%)
were spared additional diagnostic tissue sampling. These 79 women included 57
women with a percutaneous diagnosis of carcinoma and 22 women with benign
lesions who had imaging follow-up (Table
1). In 28 women (26%; 95% CI, 18-36%), a surgical excisional
biopsy was performed after percutaneous imaging-guided core biopsy. The 28
women included 15 women who had surgical excisional biopsy because of
percutaneous biopsy findings, seven women with benign lesions for which they
desired surgical excision, and six women with malignant lesions who had
surgical excisional biopsy because of patient or physician preference
(Table 1). No complications of
percutaneous imaging-guided core biopsy were encountered.
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Why use imaging guidance for percutaneous biopsy of a breast mass that is palpable? The question is not merely academic. National Medicare average allowed charges are $141 for core biopsy under palpation, $373 for sonographically guided core biopsy, $624 for stereotactic core biopsy, and $962 for surgical excision of a palpable breast mass (Dutton B, written communication) (Table 3). The procedural cost for percutaneous core biopsy is higher when it is performed under imaging guidance rather than under the guidance of palpation. However, if imaging guidance increases the likelihood of sparing surgery, imaging-guided percutaneous core biopsy could decrease the cost of diagnosis compared with that of palpation-guided needle core biopsy.
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The literature supports the utility of percutaneous imaging-guided biopsy in the assessment of palpable breast masses, but published experience is limited. Hatada et al. [28] found a significantly higher sensitivity and accuracy for fine-needle aspiration biopsy under the guidance of sonography (n = 64) rather than palpation (n = 69) in palpable breast masses measuring 2.0 cm or less. Pijnappel et al. [25] reported 27 palpable breast masses that had percutaneous 14-gauge automated core biopsy under sonographic (n = 16) or stereotactic (n = 11) guidance. In these 27 cases, prior palpation-guided fine-needle aspiration biopsy performed by the surgeon yielded nondiagnostic results. Percutaneous imaging-guided core biopsy yielded material sufficient for diagnosis in all 27 cases, including 22 infiltrating carcinomas and five benign lesions. In all 27 cases, subsequent surgical excision confirmed the percutaneous imaging-guided core biopsy findings.
Our findings suggest that imaging-guided percutaneous biopsy is useful when it is difficult to reliably place the needle in the lesion under the guidance of palpation—that is, in lesions that are small, deep, mobile, or vaguely palpable. Imaging-guided percutaneous core biopsy may also be helpful for women with multiple lesions, particularly if a lesion is highly suspicious or nonpalpable; the preoperative determination of whether a woman has one or two cancers in the ipsilateral breast may alter the treatment planning from breast conservation to mastectomy [29, 30]. Clinicians intimately involved in the evaluation of palpable breast masses found percutaneous imaging-guided core biopsy useful: in this study, 85% of the cases were referred by surgeons. It is important that the referring clinician, ideally the surgeon, has the opportunity to examine the palpable mass before percutaneous biopsy because the biopsy procedure may alter the physical examination.
For 87% (100/115) of the palpable breast masses in this study, biopsy was performed under sonographic rather than stereotactic guidance. Sonographically guided biopsy is fast: its use contributed to our ability to perform biopsy in 77% (88/115) of the lesions on the day of initial evaluation at our facility. Sonography has other advantages, including lack of ionizing radiation, real-time visualization of the needle, and lower cost [16, 18, 31]. In spite of the advantages of sonography, stereotactic guidance may be helpful for some palpable breast masses, such as those that have associated calcifications, those that are particularly mobile, or those that are not seen on sonographic examination. The choice of guidance technique is also influenced by equipment availability, expertise, and patient considerations.
Percutaneous imaging-guided core biopsy revealed a malignant lesion in 59% (63/107) of the patients in this study, all of whom were referred for definitive treatment. Preoperative diagnosis of carcinoma allows a woman and her surgeon to plan the appropriate one-stage surgical procedure, with axillary lymph node dissection or sentinel lymph node biopsy if core biopsy shows invasive carcinoma [32]. Core biopsy is often preferable to fine-needle aspiration for preoperative diagnosis of carcinoma because of the more detailed histologic information, the higher likelihood of providing a definitive diagnosis of invasive cancer, and the ability to send tissue for ancillary studies [9]. In appropriate settings, a core biopsy diagnosis of cancer may facilitate the treatment of women who require preoperative chemotherapy [33].
Without a preoperative diagnosis, women with palpable breast cancer may have a two-stage surgical procedure (diagnostic biopsy followed by definitive therapy) or a one-stage procedure based on frozen-section analysis. The latter approach has two limitations. First, it deprives women of the opportunity to consider treatment options and seek opinions armed with a tissue diagnosis. Second, frozen-section analysis is not always accurate or definitive. In a study of frozen-section analysis, the diagnosis was deferred to paraffin section in 30 (5%) of 556 lesions (including 11 cancers), and the frozen-section findings were falsely negative in eight (5%) of 164 cancers [34]. False-positive diagnoses may occur at frozen-section: in a study of frozen-section analysis of 672 lesions, the diagnosis was modified on the basis of permanent sections in 27 cases (4%), with 27 false-negatives and three false-positives [35].
In 14% (15/107) of women, surgical biopsy was suggested after percutaneous imaging-guided core biopsy. Among the palpable masses, we encountered some of the same scenarios that have been shown to warrant excision after percutaneous imaging-guided core biopsy of nonpalpable lesions, including certain histologies (e.g., atypical ductal hyperplasia, possible phyllodes tumors, radial scar), imaging-histologic discordance, or inadequate tissue [36]. The 14% frequency of recommending repeated biopsy in our study of palpable lesions was within the 9-18% frequency of repeated biopsy reported in studies that involved primarily or exclusively nonpalpable lesions [18, 21, 36,37,38]. It is possible that the use of newer technologies such as directional vacuum-assisted biopsy device may lower the rebiopsy rate for palpable masses, as has been shown for nonpalpable lesions [38].
We found two limitations of percutaneous imaging-guided core biopsy for women with benign palpable breast masses. First, the likelihood that a benign diagnosis concordant with the imaging characteristics will spare a surgical procedure is less for women with palpable than for those with nonpalpable breast masses. The frequency of subsequent excision after a benign percutaneous diagnosis was 23% (7/31) in this study, versus 4-9% in previous studies of nonpalpable breast lesions [18, 39,40,41]. Even after a benign tissue diagnosis, a palpable lump that remains in the breast may be bothersome to the woman, her doctor, or both.
Therefore, when discussing the biopsy options for palpable breast masses, particularly those that are less likely to be malignant (BI-RADS category 4), it should be determined whether the woman and her physician would be comfortable with the palpable lump remaining if the diagnosis is benign. If removal of the palpable lump is desired, excision may be preferable. Currently, percutaneous biopsy is only approved for diagnosis, not for treatment. In the future, large tissue-acquisition devices such as the 11-gauge directional vacuum-assisted biopsy probe may be useful for percutaneous excision of a benign palpable breast lump, particularly if it is small [41].
A second limitation of percutaneous imaging-guided biopsy of benign palpable breast masses relates to the need for follow-up. Goodman et al. [42] have shown the problems in obtaining follow-up after percutaneous core breast biopsy. Follow-up is especially challenging in women with palpable breast masses who are younger than 40 years old, the age at which mammographic screening generally commences. For some young women, excision may be preferable because removal of a benign lump may diminish or eliminate the need for its surveillance. The need for follow-up should be considered in the discussion of biopsy options and should be emphasized when communicating benign results.
Percutaneous imaging-guided core biopsy obviated additional diagnostic tissue sampling in 74% of the women in our study. In certain scenarios, percutaneous imaging-guided core biopsy of a palpable breast mass may strike an appropriate balance between the simpler approach of needle biopsy under palpation and the more invasive and expensive approach of surgical excision. Percutaneous imaging-guided core biopsy expedites management of palpable breast masses that are suspicious for carcinoma, particularly in women whose lesions are small, deep, mobile, vaguely palpable, or multiple. Further investigation is necessary to develop evidence-based algorithms to assist in the choice of diagnostic biopsy procedure for specific sub-groups of women with palpable breast masses and to compare the accuracy and cost-effectiveness of these techniques.
Acknowledgments
We thank Benson Dutton of the Health Care Financing Administration for
insightful interpretation of Medicare data and David C. Perlman for invaluable
assistance. We gratefully acknowledge the irreplaceable contribution of
William J. Sobaski of the Health Care Financing Administration to our analyses
of cost-effectiveness, and we dedicate this manuscript to his memory.
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