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Original Research |
1 Breast Imaging Section, Department of Radiology, Memorial Sloan-Kettering
Cancer Center, 1275 York Ave., New York, NY 10021.
2 Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY
10021.
3 Present address: Department of Radiology, Clinical Hospital Rijeka, Rijeka,
Croatia.
4 Present address: Department for Diagnostic and Interventional Radiology,
Clinic Hospital Split, Split, Croatia.
5 Present address: Department of Radiology, University Hospital Osijek, Osijek,
Croatia.
Received January 22, 2007;
accepted after revision March 15, 2007.
Address correspondence to L. Liberman
(libermal{at}mskcc.org).
Abstract
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MATERIALS AND METHODS. An institutional review board-approved retrospective review was performed of 373 consecutive lesions that had undergone MRI vacuum-assisted breast biopsy. In 34 lesions with subsequent surgery, vacuum-assisted breast biopsy yielded DCIS without frank microinvasion or invasion. DCIS underestimates were lesions for which vacuum-assisted breast biopsy yielded DCIS without frank microinvasion or invasion at biopsy and surgery yielded invasive cancer. Records and pathology findings were reviewed.
RESULTS. Among 34 lesions, vacuum-assisted breast biopsy histology was DCIS in 29 and DCIS with possible microinvasion in five. Of 29 lesions yielding DCIS at MRI vacuum-assisted breast biopsy, surgical excision revealed invasive cancer in five (17%; 95% CI, 6-36%). The DCIS underestimation rate was significantly higher in lesions 6 cm or larger versus smaller lesions (60% vs 8%, p = 0.02). MRI lesion type, kinetics, number of specimens, menopausal status, and target sampling versus excision did not significantly affect underestimation. Of five lesions yielding DCIS with possible microinvasion at MRI vacuum-assisted breast biopsy, surgery revealed invasive carcinoma in four (80%; 95% CI, 28-99%). DCIS underestimation was significantly more likely if MRI vacuum-assisted breast biopsy showed possible microinvasion than if it did not (80% vs 17%, p =0.01).
CONCLUSION. Underestimation occurred in 17% of lesions yielding DCIS and in 80% of lesions yielding DCIS with possible microinvasion at MRI vacuum-assisted breast biopsy. DCIS underestimation was significantly more likely in lesions measuring 6 cm or larger. No other patient or lesion factors significantly affected DCIS underestimation at MRI vacuum-assisted breast biopsy.
Keywords: biopsy • breast cancer • breast imaging • ductal carcinoma in situ • MRI
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MRI-guided vacuum assisted biopsy is being increasingly used as an alternative to surgical biopsy for the diagnosis of MRI-detected breast lesions that are suspicious or highly suggestive of malignancy. Prior reports have shown that MRI-guided vacuum-assisted breast biopsy is fast, safe, and accurate in the assessment of MRI-detected lesions of the breast [5-8]. Like stereotactic biopsy, MRI-guided vacuum-assisted breast biopsy may fail to completely characterize the target lesion in specific scenarios. Few data address the DCIS underestimation rate at MRI-guided breast biopsy. This study was performed to determine the DCIS underestimation rate at MRI-guided 9-gauge vacuum-assisted breast biopsy and to identify factors associated with DCIS underestimation.
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MRI Indications and Evaluation
At our institution, breast MRI is primarily used for high-risk screening
(e.g., in women with a genetic predisposition, a strong family history of
breast cancer, prior breast cancer, biopsy-proven diagnosis of atypical
hyperplasia or lobular carcinoma in situ, or prior mantle irradiation for
Hodgkin's disease), extent of disease assessment in the ipsilateral or
contralateral breast in a woman with biopsy-proven breast cancer, follow-up
after previous breast MRI, or problem solving. If a sonographic correlate for
the MRI-detected lesion is confidently identified, biopsy is usually performed
under sonographic guidance. For MRI-detected lesions that have no sonographic
correlates, that have vague sonographic findings that do not definitely
correlate with the MRI lesion, or that are better seen on MRI than sonography,
biopsy is usually performed under MRI guidance.
Biopsy Radiologists
At our institution, biopsies are performed with a 9-gauge MRI-compatible
vacuum-assisted breast biopsy device (Automated Tissue Excision and Collection
[ATEC], Suros Surgical Systems). In this study, biopsies were performed by one
of 14 radiologists specializing in breast imaging. All radiologists had prior
experience in breast MRI and percutaneous biopsies under stereotactic and
sonographic guidance. Three radiologists had performed a median of five
(range, 1-22) MRI-guided vacuum-assisted breast biopsies before this study;
the remainder had observed or assisted one or more experienced
radiologists.
Positioning and Biopsy
After giving informed consent for MRI-guided biopsies, the patient was
positioned prone in the 1.5-T magnet (Signa, GE Healthcare). A dedicated
breast surface coil and breast biopsy device were used, either the Biopsy
Breast Array Coil (Model BBC, MRI Devices [now In vivo, Intermagnetics]) or
the Open Breast Coil (Model OBC-63, MRI Devices [now In vivo]) with a
grid-localizing system (Biopsy Positioning Device, model MR-BI-160, MRI
Devices [now In vivo]). The MRI biopsy technique has been previously described
[5-8].
The biopsy site was marked with a titanium clip (TriMark, Suros Systems).
After biopsy, the breast was compressed with ice, sterile strips were applied,
a two-view digital mammogram was obtained to document clip placement, and a
sterile gauze bandage was applied. Postbiopsy instructions were given verbally
and in writing, and the patient was told when she would be contacted with
biopsy results.
Pathology Methods and Definitions
Pathology slides of vacuum-assisted breast biopsy and surgery were
reviewed. "Pure" DCIS was defined as a neoplastic intraductal
lesion characterized by increased epithelial proliferation, with subtle to
marked cellular atypia [9].
"DCIS with micro-invasion" was defined as tumor cells, singly or
in clusters, infiltrating the periductal stroma or occasionally as a
projection of neoplastic cells through a disrupted basement membrane in
continuity with the DCIS, measuring equal to or less than 1 mm in greatest
dimension [10]. Foci of
microinvasion tend to be accompanied by a stromal reaction consisting of
scattered chronic inflammatory cells arranged with pale staining loose arrays
of new collagen.
Stromal inflammatory response surrounding DCIS can make definitive diagnosis of microinvasion difficult. Serial sections and myoepithelial immunohistochemical markers may be helpful in problematic cases [10, 11]. However, not all cases are resolvable, and these foci were diagnosed as "DCIS with possible microinvasion." "Invasive ductal carcinoma" was defined as tumor cells larger than normal epithelium that invade through the basement membrane into the adjacent stroma and have a metastatic potential. Invasive ductal carcinoma can assume a variety of patterns, from diffuse sheets with a solid nonglandular architecture, a cord of cells, single-file infiltration, well-developed tubules, or a mixture of all of these. The cells vary in size and shape, with nuclei that may be regular and uniform or highly pleomorphic; few or many mitoses nay be present [9]. A "DCIS underestimate" was defined as a lesion yielding DCIS without frank microinvasion or invasion at vacuum-assisted breast biopsy and with microinvasion or invasive cancer at surgery.
The vacuum-assisted breast biopsy tissue cores were placed in cassettes, up to three cores per cassette for routine tissue processing. Excisional biopsy specimens were oriented by the surgeon and the margins were inked by the pathologist. For mastectomy specimens the following were routinely sampled: biopsy site, nipple and skin, deep margin, and two random sections per quadrant. If the mastectomy was performed for DCIS, then four sections per quadrant were submitted in addition to the biopsy site and other routine sections. All tissue samples were routinely fixed in 4% neutral buffered formalin and embedded in paraffin. Histologic assessment was performed on 4- to 5-µm-thick H and E-stained sections; three level sections were examined from each cassette of the vacuum-assisted breast biopsy tissue cores and one level section from each cassette of the surgical specimens (excision, mastectomy).
Data Collection and Analysis
Data collected for this study included indication for breast MRI, patient
age, menopausal status, MRI lesion type and kinetics, biopsy parameters, and
histologic results of vacuum-assisted biopsy and surgery. Breast MRI
examinations obtained at our institution before and after biopsy were
retrospectively reviewed and interpreted by one of 14 radiologists. Each MRI
lesion was classified by lesion type (mass, nonmass, or focus of enhancement)
and visual kinetic features (persistent, plateau, or washout) according to the
Breast Imaging Reporting and Data System (BI-RADS) breast MRI lexicon
[12]. Images were also
reviewed with a color kinetic analysis system (DynaCAD, In vivo,
Intermagnetics). MRI sequences obtained after tissue acquisition on the day of
the biopsy formed the basis for classification of completeness of excision of
the MRI target (excised, sampled, or possibly missed)
[12].
Data were entered into a computerized spread-sheet (Excel, Microsoft). Tests for statistical significance were performed with computerized statistical software (Epi-Info, Centers for Disease Control [CDC]) using the chi-square and Fisher's exact tests, with p < 0.05 considered significant. The 95% CIs were calculated using the Geigy scientific tables [13].
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DCIS (n = 29)
Patient and lesion features—The 29 lesions yielding DCIS at
MRI vacuum-assisted breast biopsy occurred in 29 women having a median age of
56 years (range, 36-75 years). Of the 29 DCIS lesions, 18 (62%) occurred in
postmenopausal women and 11 (38%) in premenopausal women. Indications for
breast MRI that led to the detection of these 29 lesions were high-risk
screening in 10 (34%), extent of disease assessment in nine (31%), problem
solving in seven (24%), and follow-up in three (10%). Among 29 lesions that
yielded DCIS at MRI vacuum-assisted breast biopsy, median lesion size was 1.5
cm (range, 0.4-8.0 cm). MRI lesion type was nonmass in 18 (62%) lesions, mass
in 10 (34%), and focus in one (3%) lesion. Median number of biopsy specimens
obtained, known in 25 lesions, was 10 (range, 6-20).
Surgical histology—Among 29 lesions yielding DCIS at MRI vacuum-assisted breast biopsy, surgical excision revealed invasive cancer in five (17%; 95% CI, 6-36%) (Table 1). Invasive cancer histologies (n =5) were invasive ductal in four (including one colloid cancer) and mixed invasive ductal and invasive lobular in one. The median histologic size of the four invasive ductal cancers was 0.3 cm (range, 0.1-1.5 cm); the lesion yielding mixed invasive ductal and invasive lobular carcinoma was multifocal, with invasive foci ranging in size from 0.2 to 0.7 cm. All five lesions with invasive cancer also had DCIS at surgery.
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Factors associated with underestimation— A significantly higher frequency of DCIS underestimation was seen in MRI lesions measuring 6 cm or larger as compared with smaller lesions (60% vs 8%, p = 0.02). A trend was seen toward a higher frequency of DCIS underestimation in lesions identified at MRI examinations performed for extent of disease assessment or follow-up as compared with high-risk screening or problem solving (42% vs 6%, p = 0.06). No significant difference in the likelihood of DCIS underestimation was observed as a function of MRI lesion type, kinetics, number of specimens obtained, menopausal status, or sampling versus excision of the target lesion (Table 2).
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DCIS with Possible Microinvasion (n = 5)
Patient and lesion features—The five lesions yielding DCIS
with possible microinvasion at MRI vacuum-assisted breast biopsy occurred in
five women having a median age of 46 years (range, 43-57 years). Four women
were postmenopausal and one was premenopausal. Indications for breast MRI were
high-risk screening in three, extent of disease assessment in one, and problem
solving in one. Among five lesions that yielded DCIS with possible
microinvasion at MRI vacuum-assisted breast biopsy, median lesion size was 2.5
cm (range, 0.9-4.5 cm). MRI lesion type was nonmass in four (80%) and mass in
one (20%). Median number of specimens, known in four lesions, was 12 (range,
10-12).
Surgical histology—Among five lesions yielding DCIS with possible microinvasion at MRI vacuum-assisted breast biopsy, surgical excision revealed invasive cancer in four (80%; 95% CI, 28-99%); the remaining lesion yielded DCIS at surgery. Histologic sub-type was invasive ductal carcinoma in all four invasive cancers, including three not otherwise specified and one papillary. The median size of the three invasive cancers was 0.5 cm (range, 0.2-2.5 cm); the fourth invasive cancer was multifocal, with invasive foci ranging in size from 0.2 to 0.4 cm. All four invasive cancers had associated DCIS at surgery.
Factors associated with underestimation— The likelihood of DCIS underestimation was significantly higher in lesions in which MRI-guided vacuum-assisted breast biopsy yielded DCIS with possible microinvasion as compared with DCIS alone (80% vs 17%, p = 0.01). In the five lesions yielding DCIS with possible microinvasion at MRI-guided biopsy, no significant difference in DCIS underestimation rate was observed as a function of MRI lesion or patient features (Table 2).
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In our study, we found that among lesions yielding pure DCIS at 9-gauge MRI-guided vacuum-assisted breast biopsy, surgery revealed invasive carcinoma in 17% (Figs. 1A, 1B, 1C, 1D, 1E, 1F and 2A, 2B, 2C, 2D, 2E). The 17% DCIS underestimation rate is between the 11% rate reported at stereotactic 11-gauge vacuum-assisted biopsy and the 20% rate reported at stereotactic 14-gauge automated core biopsy [2, 3]. That the DCIS underestimation rate at MRI-guided 9-gauge vacuum-assisted breast biopsy is not lower than that observed at stereotactic 11-gauge vacuum-assisted breast biopsy, despite the use of a larger tissue acquisition device, probably reflects the high-risk status of the women undergoing breast MRI-guided biopsy. The prior probability of invasive breast cancer is higher in women referred for breast MRI than in the general population of women having stereotactic breast biopsy, and may be particularly high for the vascular lesions identified on the basis of MRI enhancement. This higher probability of invasive breast cancer likely contributes to the higher rate of histologic underestimation.
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Our data regarding the DCIS underestimation rate are consistent with smaller published series of lesions that underwent MRI-guided 9-gauge vacuum-assisted biopsy [5, 6, 8] (Table 3). In previous investigations that reported successful MRI-guided 9-gauge vacuum-assisted breast biopsy of a total of 150 lesions, MRI vacuum-assisted breast biopsy histology yielded DCIS in 22 (15%) lesions. Among 22 DCIS lesions diagnosed at MRI vacuum-assisted breast biopsy, surgery revealed invasive cancer in five (23%; range, 0-25%). Our DCIS underestimation rate of 17% in the 29 lesions yielding pure DCIS at MRI-guided 9-gauge vacuum-assisted breast biopsy is within the 0-25% range of DCIS underestimation rates observed in prior studies of MRI-guided 9-gauge vacuum-assisted breast biopsy [5, 6, 8]. Considering our study in conjunction with these prior reports, the DCIS underestimation rate at MRI-guided 9-gauge vacuum-assisted breast biopsy is 20% (95% CI, 10-33%) (Table 3).
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We found that most (60%) lesions 6 cm or larger that yielded DCIS at
vacuum-assisted breast biopsy had associated invasion at surgery. If invasion
is encountered at surgery that is not suspected on the basis of needle biopsy
results, the patient may need to return for a second operation (usually
sentinel node biopsy) to evaluate the axilla. To prevent this scenario, one
approach might be to perform biopsy of two distant sites in larger lesions, to
increase the chances of identifying associated invasion; unfortunately,
because of the tiny size and scattered distribution of most of the invasive
foci, multiple needle biopsies may not prevent DCIS underestimation
[17]. We suggest consideration
of sentinel node biopsy during definitive surgery for women with larger (e.g.,
6 cm) lesions yielding DCIS at MRI-guided vacuum-assisted breast biopsy.
This recommendation is consistent with that of Klauber-Demore et al.
[18], who suggested that women
with biopsy-proven DCIS large enough to warrant mastectomy have sentinel node
biopsy during definitive surgery because of the high underestimation rate in
these larger lesions.
Although we found no significant difference in the DCIS underestimation rate as a function of MRI indication, we noted that analysis of biopsies performed in the extent-of-disease setting can be challenging, particularly in the ipsilateral breast. It is helpful if the surgeon meticulously labels the excised specimens, noting whether the specimen represents the index cancer or a separate MRI-detected area of enhancement, and indicating the precise location of the specimen in the breast (quadrant, clock position, and nipple-lesion distance divided by nipple-chest wall distance). Specimen labeling facilitates imaging-histologic correlation, which helps the radiologist in auditing performance and improving MRI interpretation and biopsy techniques. The low frequency of DCIS underestimation in lesions detected at high-risk screening reflects that the proportion of cancers that are DCIS is highest (up to 50%) in the high-risk screening setting [19].
MRI lesion type and kinetics were not significant predictors of DCIS underestimation. Prior studies of breast MRI have suggested that most malignant masses are invasive carcinoma and most malignant nonmass lesions are DCIS [20, 21]. Furthermore, recent investigations have shown that unlike invasive cancers, which frequently show washout kinetics, DCIS lesions often have plateau or persistent enhancement [22, 23]. On the basis of prior reports, one might have hypothesized that DCIS underestimation would be significantly more likely in masses versus nonmass lesions, and in lesions showing washout versus plateau or persistent kinetics; however, this hypothesis is not supported by our data. MRI lesion type and kinetic patterns do not predict the DCIS underestimation rate, probably because most of our underestimates contained extensive DCIS with only small areas of invasion (median, 0.3 cm) at surgery.
Among lesions yielding DCIS with possible microinvasion at MRI-guided vacuum-assisted breast biopsy, 80% had invasive cancer at surgery. Of lesions yielding DCIS without frank microinvasion or invasion at MRI-guided 9-gauge breast biopsy, the likelihood of invasion at surgery was significantly higher if vacuum-assisted breast biopsy histology suggested "possible microinvasion." On the basis of this finding, we suggest consideration of sentinel node biopsy at the time of the initial excision in patients in whom MRI vacuum-assisted breast biopsy yields DCIS with possible microinvasion, to maximize the chance of a single therapeutic operation. Our data show that if sentinel node biopsy is not performed during the initial surgery in these patients, 80% will need to return for sentinel node biopsy later. Sentinel node biopsy has also been recommended for lesions yielding DCIS with definite microinvasion; among those lesions, sentinel node metastases are present in 10% [18].
In summary, surgery revealed invasive cancer in 17% of lesions for which
MRI-guided 9-gauge vacuum-assisted breast biopsy yielded "pure"
DCIS and in 80% of lesions for which MRI-guided 9-gauge vacuum-assisted breast
biopsy yielded DCIS with possible microinvasion. The relatively high DCIS
underestimation rate at MRI 9-gauge vacuum-assisted breast biopsy compared
with that reported at stereotactic 11-gauge biopsy, despite use of a larger
tissue acquisition device, may reflect the high prior probability of invasive
cancer in these vascular lesions in high-risk women. Sampling more than one
site in larger lesions (e.g., 6 cm) may diminish but will not prevent
DCIS underestimation. Performing sentinel lymph node biopsy during the initial
therapeutic surgery may be reasonable for lesions yielding DCIS at MRI-guided
vacuum-assisted breast biopsy if the MRI lesion is 6 cm or larger, if
mastectomy is planned, or if vacuum-assisted breast biopsy histology suggests
possible microinvasion. Further work is necessary with a larger group of
patients to identify additional factors associated with DCIS underestimation
at MRI-guided 9-gauge vacuum-assisted biopsy of the breast.
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