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Original Research |
1 Breast Imaging Section, Department of Radiology, Memorial Sloan-Kettering
Cancer Center, 1275 York Ave., New York, NY 10065.
2 Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York,
NY.
Received January 28, 2008;
accepted after revision April 19, 2008.
Address correspondence to L. Liberman
(libermal{at}mskcc.org).
Abstract
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MATERIALS AND METHODS. With the approval of our institutional review board, retrospective review was performed of 416 consecutive lesions that underwent MRI-guided 9-gauge vacuum-assisted biopsy, of which 76 (18%) yielded cancer. Medical and pathology records were reviewed.
RESULTS. Vacuum-assisted biopsy histology in 76 cancers was ductal
carcinoma in situ in 39 (51%) and invasive cancer in 37 (49%). Median MRI
lesion size in these 76 cancers was 1.2 cm (range, 0.4–8.0 cm). The
median number of samples obtained was 12 (range, 6–24 samples). Among 76
cancers, the MRI target was completely excised in 23 (30% [95% CI,
20–42%]), sampled in 52 (69% [57–79%]), and possibly missed in one
(1% [0–7%]). Complete MRI target excision rather than sampling was
significantly more likely in lesions 
1 cm than in lesions >1 cm (18/34
= 53% vs 5/41 = 12%; p < 0.001). Surgery, performed in 67 of 76
cancers, showed residual cancer in 55 (82% [71–90%]). The residual
cancer rate was significantly lower if the MRI target was completely excised
rather than sampled (14/22 = 64% vs 40/44 = 91%; p < 0.02).
CONCLUSION. Complete excision of the MRI target occurred in 30% of breast cancers diagnosed at MRI-guided vacuum-assisted biopsy. Among cancers in which the MRI target was percutaneously excised, surgery yielded residual cancer in 64%. Complete removal of the MRI target does not ensure complete histologic excision of the cancer.
Keywords: breast cancer • breast MRI • biopsy
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MRI-guided vacuum-assisted biopsy is a fast, safe, and accurate alternative to surgical biopsy for the histologic diagnosis of MRI-detected breast lesions [4–9]. Few data address the residual cancer rate in completely excised MRI target lesions at MRI-guided vacuum-assisted biopsy. This study was performed to determine the frequency of complete percutaneous excision of the MRI target in lesions yielding cancer at MRI-guided biopsy and to identify the residual cancer rate at surgery in these lesions. The ability to accurately predict the histologic presence or absence of residual cancer on the basis of imaging studies is particularly important in light of the ongoing development of techniques for percutaneous ablation of breast cancer.
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MRI Indications, Technique, and Evaluation
At our institution, breast MRI is primarily used for high-risk screening
(e.g., in women with a genetic predisposition, 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 proven breast cancer, follow-up after previous breast
MRI, or problem solving.
During the study period, breast MRI examinations at our center were performed with the patient prone in a 1.5-T magnet (Signa, GE Healthcare) using a dedicated breast surface coil [5]. The protocol included a localizing sequence followed by a sagittal fat-suppressed T2-weighted sequence (TR/TE, 4,000/85). A T1-weighted 3D fat-suppressed fast spoiled gradient-echo sequence (17/2.4; flip angle, 35°; bandwidth, 31.25 MHz) was then performed before and three times after the rapid injection of a bolus of 0.1 mmol/L of gadopentetate dimeglumine (Magnevist, Bayer Health Care, formerly Berlex) per kilogram of body weight. Section thickness was 2–3 mm without a gap using a matrix of 256 x 192 and a field of view of 18–22 cm. After the examination, the unenhanced images were subtracted from the first contrast-enhanced images on a pixel-by-pixel basis.
For MRI-detected lesions that are suspicious or highly suggestive of malignancy with a definitive mammographic or sonographic correlate that can be targeted for biopsy, biopsy is usually performed under stereotactic or sonographic guidance. For MRI-detected lesions warranting biopsy that lack mammographic or sonographic correlates, biopsy is performed under MRI guidance.
Biopsy
Biopsies were performed with a 9-gauge MRI-compatible vacuum-assisted
biopsy device (Automated Tissue Excision and Collection [ATEC], Suros Surgical
Systems). The biopsies in this study were each performed by one of 15
radiologists specializing in breast imaging. All radiologists had experience
in breast MRI and percutaneous biopsy under stereotactic, sonographic, and MRI
guidance.
Biopsies were performed with the patient prone in a 1.5-T magnet (Signa, GE Healthcare) using a dedicated breast surface coil and breast biopsy device, either the Biopsy Breast Array Coil (model BBC, MRI Devices) or the Open Breast Coil (model OBC-63, MRI Devices) with a grid-localizing system (Biopsy Positioning Device, model MR-BI-160, MRI Devices). Essential elements of the biopsy technique included mark ing the expected location of the lesion with a vitamin E marker on the skin, an unenhanced axial localizing sequence, a sagittal contrast-enhanced sequence, calculation of lesion depth and determination of skin entry site, sterilization and anesthetization of the breast, placement of the probe through a sterile obturator, sagittal images to confirm obturator location, tissue acquisition, postacquisition sagittal images to confirm appropriate sampling, and marking the biopsy site with a titanium clip (TriMark, Suros Systems). These and other aspects of the MRI vacuum-assisted biopsy technique have been previously described in detail [5–8].
After biopsy, pressure with ice was held on the biopsy site until bleeding ceased and sterile strips were applied. Postbiopsy mammography (craniocaudal and 90° lateral views) of the breast was performed to confirm clip deployment. A pressure dressing was applied and the patient was given postbiopsy instructions verbally and in writing.
Data Collection and Analysis
Data collected for this study included patient age, MRI lesion size, number
of specimens, and histologic results of vacuum-assisted biopsy and surgery.
Breast MRI examinations obtained at our institution before and after biopsy
were reviewed and interpreted by one of 15 radiologists. Each MRI lesion was
classified by lesion type (mass, nonmass, or focus) according to the Breast
Imaging Reporting and Data System (BI-RADS) breast MRI lexicon
[10].
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) [10]. The MRI target was considered to have been excised if the target lesion was no longer evident and there was evidence of postbiopsy change (hematoma, air, or both) at the lesion site. The MRI target was considered sampled if a portion of the enhancing target lesion remained at the biopsy site. The MRI target was considered to have been possibly missed if postbiopsy images suggested that the target lesion was still present in its entirety, with postbiopsy changes separate from that site. For study purposes, atypical ductal hyperplasia (ADH), atypical lobular hyperplasia (ALH), lobular carcinoma in situ (LCIS), and papilloma were considered high-risk histologies.
Data were entered in a computerized spreadsheet (Excel, Microsoft). Tests for statistical significance were performed with computerized statistical software (Epi-Info, Centers for Disease Control and Prevention) 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 [11].
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Complete Excision of the MRI Target: Frequency and Associated Factors
Among 76 cancers diagnosed at MRI-guided vacuum-assisted biopsy, the MRI
target was completely excised in 23 (30% [95 CI, 20–42%]), sampled in 52
(69% [57–79%]), and possibly missed in one (1% [0–7%]). The median
size of the 23 lesions from which the MRI target was completely removed was
0.7 cm (range, 0.4–3.0 cm). The MRI lesion type was mass in 15, nonmass
in six, and focus in two. The median number of specimens obtained was 14
(range, 8–20 specimens). Vacuum-assisted biopsy histology was ductal
carcinoma in situ (DCIS) in 12 and invasive carcinoma in 11 (including five
invasive cancers that had associated DCIS at biopsy); invasive cancer
histology was ductal in nine and lobular in two.
Complete excision rather than sampling of the MRI target was significantly
more likely in lesions 1 cm rather than in those > 1 cm (p
< 0.001). The likelihood of complete excision of the MRI target did not
vary significantly as a function of the number of specimens obtained, MRI
lesion type, or vacuum-assisted biopsy cancer histology
(Table 2).
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Surgical Pathology
Surgery, performed at our center in 67 of 76 percutaneously diagnosed
cancers, revealed residual cancer in 55 (82% [71–90%]) of 67 cancers.
The lesion in which the MRI target was possibly missed at MRI-guided
vacuum-assisted biopsy was a 0.5-cm irregular enhancing mass for which biopsy
yielded DCIS; surgery revealed residual DCIS and a 0.3-cm infiltrating ductal
carcinoma.
The residual cancer rate was significantly lower if the MRI target was completely excised rather than sampled at vacuum-assisted biopsy (14/22 = 64% vs 40/44 = 91%; p < 0.02). There was a trend toward a lower residual cancer rate in MRI target lesions measuring 1 cm or less compared with lesions larger than 1 cm (23/32 = 72% vs 32/35 = 91%; p = 0.08). Among 17 cancers with an MRI lesion measuring 1 cm or less that had percutaneous removal of the MRI target followed by surgery, residual cancer was present at surgical histologic analysis in 10 (59%).
In 22 lesions that had percutaneous removal of the MRI target at biopsy followed by surgery, no features reliably predicted the presence of residual cancer at surgical histologic analysis (Table 3).
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Correlation between the presence of a residual MRI target lesion and histologic evidence of residual cancer at surgery is shown in Table 4. The presence of a residual MRI target lesion had a high positive predictive value for residual cancer (91%) but a poor negative predictive value (36%) and limited sensitivity (75%), specificity (67%), and accuracy (73%).
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MRI may provide more accurate correlation with the extent of carcinoma in the breast than mammography or sonography [12]. One can therefore hypothesize that complete percutaneous removal of the MRI target may enable accurate prediction of complete histologic excision of carcinoma.
Although numerous studies have evaluated percutaneous biopsy under MRI guidance, few data address the frequency of complete excision of the MRI target and whether complete removal of the imaging target correlates with complete histologic excision of cancer. In two prior studies of MRI-guided vacuum-assisted biopsy, complete excision of the imaging target occurred in 29–57% of all lesions; among 14 cancers in which the MRI target was percutaneously removed, surgery revealed residual cancer in seven (50%) [4, 7].
In our study, complete removal of the MRI target occurred in 30% of cancers that underwent MRI-guided 9-gauge vacuum-assisted biopsy and was significantly (p < 0.001) more likely in lesions measuring 1 cm or smaller than in larger lesions. The higher rate of complete removal of the imaging target in subcentimeter lesions is consistent with prior reports. In a study of stereotactic 11-gauge vacuum-assisted biopsy, the median size was 0.6 cm for lesions in which the mammographic target was excised versus 1.2 cm for lesions in which the mammographic target was sampled [1]. In a study of sonographically guided 11-gauge vacuum-assisted biopsy, complete removal of the sonographic target was significantly (p < 0.05) more likely in lesions measuring 1 cm or less than in larger lesions [2]. In another study reporting eight cancers in which the imaging target was removed at sonographically guided 11-gauge vacuum-assisted biopsy, all sonographic targets removed percutaneously measured 1 cm or less [3]. In a study of MRI-guided 11-gauge vacuum-assisted biopsy, all imaging targets removed were smaller than 1 cm [4]. For all guidance techniques studied to date, complete removal of the imaging target is more likely in lesions measuring 1 cm or less.
Among cancers in which the imaging target was removed at MRI-guided biopsy in our study, almost two thirds had residual cancer at surgery (Fig. 1A, 1B). This residual cancer rate is within the 50–79% range of residual cancer rates reported in studies in which the imaging target was excised at stereo tactic or sonographically guided biopsy [1–3]. Although the presence of a residual MRI target has high (91%) positive predictive value for residual carcinoma, the absence of a residual imaging target has poor (36%) negative predictive value. These find ings refute our hypothesis that assessment of the completeness of excision of the MRI target enables accurate prediction of the completeness of the histologic excision of breast cancer.
For several reasons, residual cancer may be present despite the apparent complete removal of the MRI target. First, the microscopic extent of cancer can exceed the extent of cancer delineated by imaging studies, even studies as sensitive as MRI. Second, there may be limitations in the assessment of complete removal of the imaging target on images obtained immediately after MRI biopsy. The presence of hematoma at the biopsy site (Fig. 2A, 2B), washout of contrast material from the lesion, and lesion movement (e.g., due to patient motion, anesthetic injection, or bleeding) may compromise assessment of the residual MRI target lesion. Suctioning out the biopsy cavity and reinjection of contrast material before obtaining postbiopsy images may assist in assessing the completeness of excision of the imaging target. Alternatively, bringing the patient back for reimaging on a subsequent day may increase the accuracy of assessment of the residual target lesion.
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Our findings have implications for the percutaneous treatment of breast cancer. Although MRI may provide more accurate assessment of the extent of breast cancer than other imaging techniques such as mammography and sonography, removal of all MRI evidence of cancer does not guarantee complete removal of breast cancer histologically. If techniques such as MRI-guided focused sonographic ablation [13] or other percutaneous techniques are to be used to treat breast cancer, it will be necessary to develop methods to more reliably predict the completeness of histologic tumor excision. Perhaps further improvements in MR spectroscopy [14, 15] may provide the methods necessary to accomplish this goal.
In conclusion, we found complete excision of the MRI target in 30% of cancers diagnosed by MRI-guided 9-gauge vacuum-assisted biopsy. The likelihood of complete removal of the imaging target was higher in subcentimeter lesions than in larger lesions. Among breast cancers from which the MRI target was percutaneously removed, most (64%) had residual cancer at surgery. Complete excision of the MRI target, like complete excision of the mammographic or sonographic target, does not ensure complete histologic excision of carcinoma. As we consider the possibility of percutaneous treatment of breast cancer, it will be necessary to develop methods to show not only that the imaging target been excised but also that the cancer has been removed in its entirety.
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