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Centennial Dissertation |
1 Department of Radiology, Breast Imaging Section, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
Received December 7, 1999;
accepted after revision January 4, 2000.
Honoring George C. Johnson, MD and George E. Pfahler, MD
Introduction
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Stereotactic core biopsy can be performed with the patient prone or upright. The prone tables are more expensive but have several advantages including more working room, decreased likelihood of patient motion and vasovagal reaction, and the added benefit of the table acting as a psychologic barrier between the patient and the procedure. Use of decubitus positioning on the upright unit has been reported and may improve results [12]. Digital imaging, available with prone and upright units, decreases the time necessary to do the procedure, which may increase the likelihood of success [7].
Sonography
Sonographically guided 14-gauge automated core biopsy was first described
by Parker et al. [16] in 1993,
who used a 14-gauge automated needle and long-excursion gun to sample 181
lesions. These researchers reported 100% concordance between results of
sonographically guided 14-gauge automated core biopsy and surgery in the 49
lesions with surgical correlation, and no carcinomas were identified at the
12- to 36-month follow-up in the 132 lesions yielding benign results.
Sonography has many advantages as a guidance technique for percutaneous breast biopsy, including lack of ionizing radiation, use of readily available nondedicated equipment, accessibility of all areas of the breast and axilla, real-time visualization of the needle, multidirectional sampling, and low cost [14, 16, 17]. The main disadvantage of sonographic guidance is that the lesion must be sonographically evident to undergo sonographically guided biopsy. Thus, sonographically guided core biopsy may not be feasible for calcifications or for the small subset of solid masses that are sonographically inapparent. For lesions amenable to either stereotactic or sonographically guided biopsy, if appropriate equipment and expertise are available, sonographically guided biopsy may be preferable in terms of patient comfort and radiation exposure, procedure time, and cost [17].
MR Imaging
MR imaging can reveal breast cancer that is not detected on mammography,
sonography, or physical examination
[19]. Although MR imaging has
a high sensitivity in detecting breast cancer, approaching 100% in some
series, the reported specificity has ranged from 37% to 97%
[19]. Further work is
necessary to refine the indications for the use of breast MR imaging in cancer
detection and to develop techniques for performing MR imaging—guided
breast biopsy. To date, most studies of MR imaging—guided biopsy used
prototype equipment and either needle localization or fine-needle aspiration
biopsy; published experience with core biopsy is limited
[18,19,20,21,22,23,24,25,26,27].
The largest series to date is that of Heywang-Koebrunner et al.
[27], who reported successful
MR imaging—guided directional vaccum-assisted biopsy in 99 (99%) of 100
MR imaging—detected lesions, of which 25 were found to be carcinoma.
MR imaging—guided percutaneous breast biopsy poses several challenges [20]. Except in open magnets, the patient must be removed from the magnet to gain access to the breast for performing the biopsy. Because MR imaging is generally performed with the patient prone, the lateral portion of the breast is accessible, but access to the medial breast may be more difficult. One has limited time after contrast injection before lesion visibility diminishes because of the transient nature of contrast enhancement. For MR imaging—guided surgical biopsy, confirmation of lesion retrieval is difficult because the lesion does not enhance ex vivo; Liberman et al. [31] suggest that placement of an MR-compatible localizing clip may be useful in this regard. Finally, dedicated MR imaging—guided biopsy equipment must be developed, including coils, breast immobilization and compression devices, needle guides, and nonferromagnetic needles with minimal artifacts. MR imaging—guided biopsy is still investigational and is in great need of more research, both with respect to technical development and to defining the clinical context in which this technology may be most valuable.
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Fewer Surgeries
For many women with benign breast disease, percutaneous biopsy can obviate
surgery. The goal of percutaneous breast biopsy is to obtain a histologic
diagnosis of a lesion that is of sufficient concern to warrant biopsy.
Approximately 70-80% of nonpalpable breast lesions referred for biopsy are
benign [43]. If percutaneous
imaging-guided biopsy yields a benign diagnosis concordant with the imaging
characteristics (as occurs in most women who have percutaneous breast biopsy),
surgery can usually be avoided
[39].
Percutaneous biopsy can also decrease the number of surgical procedures performed in women with breast cancer (Fig. 2A,2B,2C,2D). Smith et al. [37] found that the average number of surgeries performed was 1.25 in women with percutaneously diagnosed cancer versus 2.01 in women with surgically diagnosed cancer. In two other studies, a single surgical procedure was performed in 84-90% of women with percutaneously diagnosed cancer versus 24-29% in women with surgically diagnosed cancer [34, 36]. Liberman et al. [35] found that among women who had breast-conserving surgery, the likelihood of obtaining clear histologic margins of resection at the first operation was 92% for women with percutaneously diagnosed cancer versus 64% for women with surgically diagnosed cancer. Some women with percutaneously diagnosed infiltrating breast cancer may undergo breast-conserving surgery with sentinel lymph node biopsy, allowing a minimally invasive approach to diagnosis and treatment [44]. Percutaneous biopsy may also allow the determination that carcinoma is multifocal (multiple sites in the same quadrant) or multicentric (multiple sites in different quadrants), altering treatment recommendations [45, 46].
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A surgeon's approach is different when performing a diagnostic surgical biopsy than when performing a therapeutic operation after a percutaneous diagnosis of breast cancer. The goal of a surgical biopsy is to obtain a tissue diagnosis. Most surgeons prefer to resect the minimal amount of tissue necessary for that purpose, to minimize potential cosmetic deformity for a lesion that may be benign. The goal of a therapeutic operation is to remove all the cancer with clear histologic margins. Surgeons generally remove a larger volume of tissue in this scenario to accomplish the necessary excision. A percutaneous diagnosis of cancer facilitates operative planning, usually allowing the surgeon to achieve a therapeutic result in a single procedure [34,35,36,37].
Lower Cost
Percutaneous biopsy can decrease the cost of diagnosis of indeterminate or
suspicious nonpalpable breast lesions. Lindfors and Rosenquist
[38] found that use of
stereotactic 14-gauge automated biopsy rather than surgical biopsy reduced the
marginal cost per year of life saved by 23%. Others reported that stereotactic
14-gauge automated core biopsy obviated a surgical procedure in 76-81% of
lesions, resulting in a 40-58% decrease in the cost of diagnosis
[39,40,41,42].
Liberman et al. [17] found
that sonographically guided 14-gauge automated core biopsy obviated a surgical
procedure in 128 (85%) of 151 lesions and yielded a 56% decrease in the cost
of diagnosis. For masses amenable to either stereotactic or sonographically
guided biopsy, cost savings are likely to be greater if the biopsy is
performed under sonographic guidance
[17].
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Directional vacuum-assisted biopsy instruments are now available for performing percutaneous biopsy and are particularly helpful in the assessment of calcific lesions (Fig. 3A,3B,3C,3D). Compared with the 14-gauge automated needle, the vacuum-assisted devices obtain larger tissue specimens, with median specimen weights of approximately 17 mg for the 14-gauge automated needle, 35 mg for the 14-gauge directional vacuum-assisted biopsy probe, and 100 mg for the 11-gauge directional vacuum-assisted biopsy probe [50,51,52]. The vacuum device allows multiple specimens to be obtained with a single insertion, enables the operator to suction blood from the biopsy cavity, and facilitates contiguous sampling [49]. Several investigators have reported calcification retrieval rates of 99-100% for 14- or 11-gauge directional vacuum-assisted breast biopsy, significantly higher than the 86-94% calcification retrieval rate observed with 14-gauge automated large-core biopsy [53,54,55].
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Histologic Underestimates
In some instances, percutaneous biopsy identifies the presence of a
high-risk or malignant lesion but incompletely characterizes the pathology,
which has been termed a "histologic underestimate"
[56]. Examples include lesions
yielding a stereotactic biopsy diagnosis of atypical ductal hyperplasia (ADH)
for which subsequent surgery yields carcinoma ("ADH
underestimate") and lesions yielding a stereotactic biopsy diagnosis of
ductal carcinoma in situ (DCIS) for which subsequent surgery yields
infiltrating carcinoma ("DCIS underestimate")
[56]. Because most lesions
containing ADH or DCIS contain calcifications, histologic underestimates at
percutaneous biopsy are most often encountered in calcific lesions
[57,
58].
ADH has been defined as a lesion that has some but not all the features of DCIS, a lesion that has all the features of DCIS but involves only one duct, or a lesion that has all the features of DCIS but measures less than 2 mm [58]. Therefore, the potential exists that a small sample of a DCIS lesion may be interpreted by the pathologist as representing ADH. Furthermore, some lesions may contain both ADH and DCIS, or DCIS and infiltrating carcinoma; histologic underestimation in such cases may simply result from sampling error. Both ADH and DCIS underestimates decrease the frequency with which percutaneous biopsy spares a surgical procedure: an ADH underestimation leads to a recommendation for surgical biopsy, and a DCIS underestimation may require that the patient have a second operation to assess the axilla.
Directional vacuum-assisted biopsy diminishes but does not eliminate the problem of histologic underestimates. Of lesions yielding ADH at 14-gauge automated core biopsy, approximately 20-56% have carcinoma at surgery [6, 57,58,59,60,61,62]; of lesions yielding ADH at directional vacuum-assisted biopsy, approximately 0-38% have carcinoma at surgery [59,60,61,62,63]. Among lesions yielding DCIS with the 14-gauge automated needle, 16-35% contain infiltrating carcinoma at surgery [6, 15, 59, 64,65,66]; of lesions yielding DCIS with the directional vacuum-assisted biopsy device, approximately 0-19% have infiltrating carcinoma at surgery [15, 59, 65,66,67]. ADH and DCIS underestimations have also been reported after biopsy with the Advanced Breast Biopsy Instrumentation (ABBI) system (U. S. Surgical, Norwalk, CT) [68, 69].
It is prudent to suggest that a diagnosis of ADH with any existing percutaneous biopsy technology is an indication for surgical excision because of the high prevalence of carcinoma in these lesions. Lesions yielding DCIS at percutaneous biopsy may contain areas of invasive carcinoma at surgery, regardless of whether the biopsy was performed with a 14-gauge automated needle, a directional vacuum-assisted biopsy probe, or a larger biopsy device.
False-Negative Diagnoses
In clinical follow-up studies after stereotactic 14-gauge automated core
biopsy, the frequency of missed carcinoma averaged 2.8% (range, 0.3-8.2%),
with approximately 70% of missed cancer identified shortly after biopsy
(immediate false-negatives) and 30% identified subsequently (delayed
false-negatives) [70,
71]. Although this frequency
is comparable to the frequency of missed cancer at needle localization and
surgical biopsy, which has an average cancer miss rate of 2.0% (range, 0-8%)
[72], it indicates the
possibility of a delay in the diagnosis of breast cancer.
The radiologist can take several steps to diminish the likelihood and potential impact of a false-negative diagnosis. Optimizing technique, particularly with respect to lesion targeting, can maximize the chance that the needle will sample the lesion [58]. For lesions evident as calcifications, calcifications should be identified on specimen radiographs; if calcifications are not observed on specimen radiographs and the diagnosis is benign, additional tissue sampling may be warranted even if calcifications are identified histologically. Careful correlation of the imaging and histologic findings will allow the radiologist to identify discordant lesions prospectively and recommend prompt rebiopsy, avoiding delay in diagnosis. And finally, the radiologist should emphasize to the patient the importance of follow-up mammography after benign percutaneous biopsy, so that any interval change can be identified and evaluated.
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Controversy exists regarding the use of percutaneous core biopsy in the evaluation of lesions that are highly suggestive of malignancy (BI-RADS category 5), approximately 75-90% of which represent carcinoma. The usefulness of percutaneous core biopsy for category 5 lesions depends on the surgical treatment protocol that would otherwise have been used [74]. If the protocol in the absence of percutaneous biopsy would be to perform a diagnostic surgical biopsy followed by a second (therapeutic) surgery if carcinoma was found, performing a percutaneous biopsy could spare a surgical procedure. If the protocol in the absence of percutaneous biopsy would be to confirm the diagnosis of carcinoma with a frozen section and then to perform a one-stage therapeutic operation, percutaneous biopsy would not spare the patient a surgical procedure. In prior studies of stereotactic 14-gauge automated core biopsy, the frequency of sparing surgery was higher for BI-RADS category 5 masses (76-77%), which usually represent invasive carcinoma, than for BI-RADS category 5 calcifications (42-55%), which usually represent DCIS [40, 74, 75].
Controversy also exists regarding the role of percutaneous core biopsy in the evaluation of "probably benign" (BI-RADS category 3) lesions, which have a 0.5-2% frequency of carcinoma [76,77,78,79,80,81,82,83]. The traditional management of BI-RADS category 3 lesions is short-term follow-up mammography, which is less invasive and less expensive (by a factor of 8) than percutaneous core biopsy [83]. Biopsy could be considered in a small subset of category 3 lesions—for example, if follow-up is unavailable or compromised (because of geographic considerations, an impending pregnancy, or impending breast augmentation or reduction surgery), if a synchronous carcinoma is present (especially in the ipsilateral breast and breast-conserving surgery is planned), if the patient is at high risk for developing breast cancer, or if the patient's anxiety precludes short-term follow-up.
Complete Lesion Removal
The goal of percutaneous biopsy is diagnosis, not treatment. However,
percutaneous biopsy may result in complete removal of the mammographic lesion,
particularly if a large volume of tissue is obtained
[84,
85]. Studies of stereotactic
14-gauge directional vacuum-assisted biopsy reported complete removal of the
mammographic lesion in 13-48% of all lesions and in 58-93% of lesions
measuring 5 mm or less [85].
Complete removal of the mammographic target does not ensure complete excision
of the abnormality. In one study of 15 carcinomas in which the mammographic
lesion was removed at stereotactic 11-gauge directional vacuum-assisted
biopsy, surgery revealed residual carcinoma in 11 (73%)
[85]. Therefore, it is
desirable to place a localizing clip at the biopsy site when the mammographic
lesion is removed (Fig.
3A,3B,3C,3D)
to facilitate subsequent localization if necessary
[31,
86].
Are there scenarios in which complete removal of the mammographic target is desirable? Although complete lesion removal is generally not the goal of percutaneous biopsy, theoretically reasons exist why it may be advantageous in some cases. Complete lesion removal may reduce or eliminate sampling error, perhaps decreasing the likelihood of histologic underestimation, imaging—histologic discordance, and rebiopsy [85]. Complete lesion removal may diminish the likelihood of subsequent growth on follow-up, reported to occur in 7-9% of lesions yielding benign results in prior studies of stereotactic 14-gauge automated core biopsy [70, 71]. The benefits of complete excision versus sampling should be assessed in future work, particularly with the development of new instruments for percutaneous biopsy that allow larger volume tissue acquisition.
Advanced Breast Biopsy Instrumentation
The ABBI system is a tissue acquisition device coupled with a stereotactic
table. It is available with a variety of cannula sizes ranging up to 2 cm. The
ABBI device can obtain a specimen extending from the subcutaneous tissue to
beyond the lesion, potentially removing the entirety of a small mammographic
target in a single specimen
[87].
In spite of initial enthusiasm regarding this device, the ABBI system has many disadvantages. The large volume of tissue obtained (reportedly up to 13 cm3) is likely to cause more scarring and deformity with little benefit to women with benign disease, who account for most women who come to biopsy. The 1.1% complication rate of ABBI biopsy [87] is significantly higher than the 0.2% [9] and 0.1% [60] complication rates for automated core and directional vacuum-assisted biopsy, respectively. For cancer diagnosed at ABBI biopsy, tumor has been present at the margins in 64-100%. Finally, the ABBI is substantially more expensive than other existing percutaneous biopsy technologies: the costs of tissue acquisition devices are approximately $15-25 for 14-gauge automated needles, more than $200 for 11-gauge vacuum-assisted probes, and more than $500 for ABBI cannulas. It has not yet been established that the ABBI has benefits that outweigh its disadvantages.
Epithelial Displacement
Displacement of benign or malignant epithelium into tissue away from the
target lesion may occur during a variety of breast needling procedures,
including fine-needle aspiration, core biopsy, directional vacuum-assisted
biopsy, local anesthetic injection, and suture placement
[67]. Epithelial displacement
can cause interpretive problems for the pathologist: displaced DCIS can mimic
infiltrating ductal carcinoma. Specific histologic findings suggesting
epithelial displacement include fragments of epithelium in artifactual spaces
in the breast parenchyma, morphologic evidence of a needle track (hemorrhage,
fat necrosis, inflammation, hemosiderin-laden macrophages, or granulation
tissue), and absence of surrounding tissue reaction such as one excepts to see
with infiltrating carcinomas. Epithelial displacement may be less frequent
after vacuum-assisted biopsy than after automated core biopsy
[67].
The largest study to address the issue of epithelial displacement at large-core needle breast biopsy was conducted by Diaz et al. [88]. In 352 surgical excision specimens in women with a prior diagnosis of cancer by large-core needle biopsy, Diaz et al. found displacement of malignant epithelium in 32%. The frequency of tumor displacement was 37% after automated gun biopsy, 38% after palpation-guided biopsy, and 23% after vacuum-assisted biopsy. Tumor displacement was seen in 42% of patients with an interval between biopsy and excision of less than 15 days, in 31% of patients with an interval of 15-28 days, and in 15% of tumors excised more than 28 days after core biopsy (p <0.005). The inverse relation between the amount of tumor displacement observed and time to excision suggests that tumor cells do not survive displacement.
Few data address the long-term impact of epithelial displacement. In a study of stagematched palpable invasive breast cancer treated by mastectomy, Berg and Robbins [89] noted no difference in 15-year survival between women whose cancer is diagnosed on aspiration biopsy and those whose cancer is diagnosed with open surgical biopsy. In a study of 74 women with nonpalpable breast cancer diagnosed by needle localization and surgical biopsy, Kopans et al. [90] reported no evidence of local recurrence attributable to needle localization. Mastectomy was performed in all the patients in the study of Berg and Robbins and most of the patients in the study of Kopans et al., limiting the conclusions that can be drawn about needle track recurrence. Additional study is needed to assess the clinical significance of epithelial displacement in the breast, including long-term follow-up of women with cancer diagnosed by percutaneous biopsy and treated with breast-conserving surgery.
Rebiopsy
In previous studies of percutaneous imaging-guided core breast biopsy, a
second biopsy was recommended in 9-18% of patients
[17,
62,
91,
92]. The most common reason
for rebiopsy after stereotactic core biopsy is a diagnosis of ADH, which
accounted for 16-56% of lesions referred for rebiopsy in prior reports
[62,
91,
92]. Other accepted reasons
for a second biopsy include possible phyllodes tumor (the most common reason
for rebiopsy after sonographically guided 14-gauge automated core biopsy in
one series [17]),
pathologist's recommendation, discordance between imaging and histologic
findings, and inadequate tissue (a rare event at percutaneous core biopsy)
[17,
62,
91,
92].
Controversy exists regarding the need for surgical excision after percutaneous core biopsy diagnosis of other specific entities [93] including papillary lesions [94], radial scar [70], atypical lobular hyperplasia [95,96,97], and lobular carcinoma in situ [95,96,97]. Because of the low frequency of each of these diagnoses, these issues may best be addressed by the cooperative efforts of multiple institutions. Philpotts et al. [62] found a significantly lower rebiopsy rate after stereotactic 11-gauge directional vacuum-assisted biopsy (9%) than after 14-gauge automated core biopsy (15%), suggesting that the larger volume of tissue or more contiguous sampling may provide more accurate lesion characterization and lower the rebiopsy rate.
Follow-Up
The extent of the radiologist's responsibilities for follow-up after
percutaneous biopsy has not yet been determined, but these responsibilities
exist. In the most complete follow-up study to date, with follow-up on 307
(99%) of 310 lesions yielding benign results at stereotactic 14-gauge
automated core biopsy, Jackman et al.
[70] reported a false-negative
diagnosis in two (1.2%) of 161 cancerous tumors. These missed cases of cancer
were detected by means of mammographic progression at 6 and 18 months after
biopsy. Lee et al. [71]
reported a false-negative diagnosis in two (2%) of 105 cancers, with the
missed cancer identified by means of interval change on mammograms obtained at
6 and 24 months after biopsy. These studies illustrate the importance of
follow-up after percutaneous breast biopsy.
The follow-up interval after a benign percutaneous biopsy diagnosis is not standardized. Suggested intervals to the first follow-up mammogram have ranged from 6 months [70] to 1 year [39], with some investigators suggesting a varied interval depending on the histologic findings (1 year for a specific benign diagnosis and 6 months for a nonspecific benign diagnosis) [71]. Patients often fail to comply with follow-up recommendations [98]. Protocols for tracking follow-up data often vary, but all require substantial allocation of time and resources. In spite of these difficulties, follow-up is essential [99]. As eloquently stated by Berlin [100]:
...responsibilities to track patients after percutaneous core biopsies are clearly being imposed on radiologists by society and the radiologic community itself. Whatever the extent of these responsibilities, they are greater today than they were yesterday, and they are likely to be greater tomorrow than they are today.
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Although advances have been made, much work remains to be done. Newer technologies should be assessed with respect to their accuracy, safety, and cost-effectiveness. Protocols must be developed to optimize the choice of biopsy method for different lesions. Long-term follow-up is needed to determine the impact of the newer biopsy technologies on the mammographic pattern, to better delineate the false-negative rate of percutaneous breast biopsy, and to clarify the biologic implications of epithelial displacement in the breast. Further investigation is necessary to define the appropriate clinical context for breast MR imaging and to develop technology for MR imaging—guided breast biopsy. And finally, the future may allow an expansion of the role of percutaneous techniques into the realm of therapy. Perhaps the day will come in the new millennium when we can offer a woman not only minimally invasive diagnosis but also minimally invasive treatment of her breast cancer.
Acknowledgments
I offer thanks to Steve Parker, for starting it all; to D. David Dershaw,
for creating a work environment that allows us to ask questions and seek
answers; to Michelle P. Sama, for photographic assistance; and to David C.
Perlman, for invaluable support in this and all things.
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