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Underestimation of Atypical Ductal Hyperplasia at MRI-Guided 9-Gauge Vacuum-Assisted Breast Biopsy

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.

Received June 19, 2006; accepted after revision August 18, 2006.

 
Address correspondence to L. Liberman (libermal{at}mskcc.org).

Presented at the 2006 annual meeting of the American Roentgen Ray Society, Vancouver, BC, Canada.

Supported by a grant from the Breast Cancer Research Foundation.

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Abstract

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OBJECTIVE. The purposes of this study were to determine the frequency of diagnosis of atypical ductal hyperplasia (ADH) at MRI-guided 9-gauge vacuum-assisted breast biopsy and to assess the rate of underestimation of ADH at subsequent surgical excision.

MATERIALS AND METHODS. We conducted a retrospective review of medical records of 237 lesions consecutively detected with MRI and then subjected to MRI-guided 9-gauge vacuum-assisted breast biopsy during a 33-month period. Underestimated ADH was defined as a lesion yielding ADH at vacuum-assisted biopsy and cancer at surgery. Scientific tables were used to calculate 95% CI.

RESULTS. Histologic analysis of MRI-guided vacuum-assisted breast biopsy specimens yielded ADH without cancer in 15 (6%) of 237 lesions. Among 15 patients in whom vacuumassisted breast biopsy yielded ADH, the median age was 52 years (range, 46-68 years). The median number of specimens obtained was nine (range, 8-18 lesions). Median MRI lesion diameter was 1.3 cm (range, 0.7-7.0 cm). Among 15 MRI lesions, 10 (67%) were nonmasslike enhancement and five (33%) were masses. Surgical excision was performed on 13 lesions. Surgical histologic findings were malignancy in five (38%) of the cases, all ductal carcinoma in situ; high-risk lesion in six (46%) of the cases, including ADH without other high-risk lesions (n = 2), ADH and lobular carcinoma in situ (LCIS) (n = 1), ADH, LCIS, and papilloma (n =1), ADH and papilloma (n = 1), and LCIS (n = 1); and benign in two (15%) of the cases. These data indicated an ADH underestimation rate of 38% (95% CI, 14-68%).

CONCLUSION. ADH without cancer was encountered in 6% of MRI-guided 9-gauge vacuum-assisted breast biopsies. ADH at MRI-guided vacuum-assisted breast biopsy is an indication for surgical excision because of the high (38%) frequency of underestimation of these lesions.

Keywords: biopsy • breast • breast cancer • MRI • women's imaging

Introduction

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Atypical ductal hyperplasia (ADH) has been variably defined in the pathology literature as a lesion that has some but not all of the features of ductal carcinoma in situ (DCIS), a lesion that has all of the features of DCIS but involves only one duct, and a lesion that has all of the features of DCIS but measures less than 2 mm in diameter [1-3]. It is therefore possible for a sample obtained with a needle to contain DCIS but for the pathologist, using specific criteria, to diagnose only ADH. Furthermore, some lesions contain a combination of ADH and DCIS or of ADH, DCIS, and invasive cancer. In these lesions, it is possible to perform a needle biopsy for cancer and to retrieve only ADH in the specimen because of sampling error [4-6].

Underestimated ADH is defined as a lesion that yields ADH at needle biopsy but cancer at surgery [4]. The frequency of ADH underestimation at stereotactic biopsy performed with 14-gauge automated needles and with 11-gauge vacuum-assisted biopsy probes has been extensively studied [6-12]. The frequency of ADH underestimation is 50% (range, 20-56%) for stereotactic biopsy performed with a 14-gauge needle. This rate declines to 20% (range, 10-27%) for biopsy performed with an 11-gauge vacuum-assisted biopsy probe. Among lesions yielding ADH at stereotactic biopsy and cancer at surgery, approximately two thirds of the malignant tumors are DCIS.

MRI is being used increasingly to evaluate women with known breast cancer, high risk for development of breast cancer, and other specific clinical or imaging problems [13, 14]. MRI-guided vacuum-assisted biopsy is a safe and accurate alternative to MRI-guided needle localization and surgical biopsy for evaluation of mammographically occult MRI-detected lesions [15-20]. Few data address the frequency of ADH underestimation at MRI-guided vacuum-assisted biopsy. This study was undertaken to determine the frequency of diagnosis of ADH at MRI-guided vacuum-assisted biopsy and to assess the ADH underestimation rate (i.e., the proportion of lesions yielding ADH at MRI-guided vacuum-assisted biopsy that contain cancer at surgery).

Materials and Methods

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MRI Indications and Evaluation
Breast MRI, performed according to previously described technique [21], is used at our center for several indications. Breast MRI is performed for screening selected women at high risk for breast cancer, including women with genetic predisposition to breast cancer, a strong family history of breast cancer, previous breast cancer, a biopsy-proven diagnosis of atypical hyperplasia or lobular carcinoma in situ (LCIS), or previous mantle irradiation for Hodgkin's disease. It is also used for assessment of extent of disease in women with proven breast cancer, for follow-up after previous breast MRI, and for problem solving. For nonpalpable mammographically occult MRI-detected lesions warranting biopsy, correlative sonography is performed at the discretion of the interpreting radiologist. MRI-detected lesions that have sonographic correlates usually are subjected to biopsy under sonographic guidance. MRI-detected lesions that lack 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 usually are subjected to biopsy guided by MRI. The decision between MRI-guided needle localization for surgical biopsy and MRI-guided vacuum-assisted biopsy is made by the radiologist, referring clinician, and patient in consultation.

Biopsy Radiologists and Technique
Biopsies during the study period were performed with a 9-gauge MRI-compatible vacuum-assisted biopsy device (Automated Tissue Excision and Collection, Suros Surgical Systems). Biopsies were performed by one of 14 radiologists specialized in breast imaging. All biopsy radiologists had experience interpreting breast MR images and performing percutaneous breast biopsy under stereotactic and sonographic guidance. These radiologists had either performed or assisted in MRI-guided vacuum-assisted biopsies before serving as primary physician in the biopsy cases included in this study.

Biopsies were performed with the patient positioned prone in a 1.5-T MRI unit (Signa, GE Healthcare). A dedicated breast surface coil and biopsy compression device were used, either a biopsy breast array coil (model BBC, MRI Devices [now Invivo Corporation]) or an open breast coil (model OBC-63, MRI Devices [now Invivo Corporation]) with a grid-localizing system (Biopsy Positioning Device, model MR-BI-160, MRI Devices [now Invivo Corporation]). Biopsy was performed according to previously described technique [16]. The biopsy site was marked with a clip (Trimark, Suros) and cleansed and compressed with ice. Sterile strips were applied, and a postbiopsy two-view digital mammogram was obtained. The patient was given postbiopsy instructions and told when she would be contacted with the biopsy results.

Data Collection and Analysis
In a protocol approved by our institutional review board, we retrospectively reviewed the medical records on 237 lesions consecutively evaluated with MRI-guided vacuum-assisted biopsy during a 33-month period. Vacuum-assisted biopsy yielded benign histologic findings in 156 (66%) of the 237 lesions, high-risk findings in 37 (16%) of the lesions, and cancer in 44 (19%) of the lesions; cancer histology was DCIS in 24 and invasive carcinoma in 20. MRI lesion type in these 237 lesions, recorded by one of 14 radiologists before biopsy according to the BI-RADS breast MRI lexicon [22], was mass in 125 (53%) of the cases, nonmasslike enhancement in 105 (44%) of the cases, and focus in seven (3%) of the cases.

Lesions that yielded ADH at MRI-guided vacuum-assisted biopsy constituted the basis of this study. Data collected included indication for breast MRI, patient age, menopausal status, MRI lesion size, biopsy parameters, histologic results, number of previous MRI-guided vacuum-assisted biopsies performed by the biopsy radiologist, and complications. MRI examinations before, during, and after biopsy were reviewed. Data were entered in a spread-sheet program (Excel, Microsoft). Chi-square and Fisher's exact tests for statistical significance were performed with statistical software (Epi-Info, Centers for Disease Control and Prevention), and p < 0.05 was considered significant. Geigy scientific tables [23] were used to calculate 95% CI.

Results

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Patients, Indications for MRI, and Lesions
MRI-guided 9-gauge vacuum-assisted biopsy yielded ADH in 15 (6%) of 237 lesions. ADH was encountered in five (4%) of 125 mass lesions and 10 (10%) of 105 cases of nonmasslike enhancement (p = 0.16). These 15 ADH lesions occurred in 14 women with a median age of 52 years (range, 46-68 years). Among these 14 women, six (43%) previously had breast cancer (contralateral in four, ipsilateral in one, and bilateral in one) and six (43%) had synchronous breast cancer.

Indications for breast MRI that led to the detection of the 15 ADH lesions included screening for high risk in six (40%), assessment of extent of disease in six (40%), problem solving in two (13%), and follow-up in one (7%) of the cases. Among the six lesions detected in assessment of extent of disease, the lesion was in the ipsilateral breast in three and in the contralateral breast in three cases. Among the six lesions detected at screening for high risk, four were found in women with previous breast-conserving surgery for breast cancer (one in the ipsilateral and three in the contralateral breast) and two in women with a family history of breast cancer.

The median size of the 15 MRI lesions was 1.3 cm (range, 0.7-7.0 cm). The median number of specimens obtained at biopsy, reported for 11 lesions, was nine (range, 8-18). The median time to perform biopsy was 31 minutes (range, 17-57 minutes). The median number of previous MRI-guided vacuum-assisted biopsies performed by the radiologists who biopsied the 15 ADH lesions was 21 (range, 1-55). No complications were encountered.

Surgical Histology
Surgical excision, recommended for all 15 lesions that yielded ADH at MRI-guided vacuum-assisted biopsy, was performed on 13 lesions. Surgical histologic examination yielded cancer in five (38%) of the lesions, all of which were DCIS; high-risk findings in six (46%) of the lesions; and benign findings in two (15%) of the lesions (Table 1). High-risk surgical histologic findings were ADH in five lesions (including one with LCIS, one with LCIS and papilloma, and one with papilloma) and LCIS in one lesion. Benign surgical histologic findings in two lesions were fibroadenoma in one and duct hyperplasia, sclerosing adenosis, and apocrine metaplasia in the other.

The five ADH lesions upgraded to DCIS at surgery included a variety of MRI lesion types (masses and nonmasslike enhancement), sizes (median, 1.0 cm; range, 0.7-2.8 cm), DCIS histologic features, and nuclear grades (Table 2). No significant difference was found in likelihood of ADH underestimation as a function of MRI lesion size, lesion type, synchronous or previous breast cancer, experience of biopsy radiologist, removal of imaging target, menopausal status, or number of specimens removed (Table 3).

Among 13 ADH lesions diagnosed with MRI-guided vacuum-assisted biopsy and subsequently managed with surgery, the ADH underestimation rate was 38% (5/13; 95% CI, 14-68%). If the two ADH lesions not managed surgically were included in the denominator as benign lesions, the ADH underestimation rate would be 33% (5/15; 95% CI, 12-62%).

Discussion

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The dissemination of breast MRI mandates the capability of biopsy under MRI guidance [16]. Among nonpalpable mammographically occult MRI-detected lesions referred for biopsy, as many as 75% lack a sonographic correlate [24], and therefore either preoperative localization for surgical biopsy or percutaneous biopsy under MRI guidance must be performed. Compared with surgery, percutaneous biopsy is faster and less invasive, does not cause scarring or deformity, and costs less [25]. Among percutaneous biopsy methods, MRI-guided vacuum-assisted biopsy has advantages over core biopsy because it is faster, more tissue is acquired, and complex histologic findings such as ADH and DCIS are characterized more accurately. These histologic findings are more frequently encountered among women at high risk undergoing breast MRI than in the general population [16, 26]. Knowledge of the rate of identification and underestimation of ADH lesions at MRI-guided vacuum-assisted biopsy would facilitate informed choices about biopsy methods.

Few previous reports of MRI-guided vacuum-assisted biopsy have stated the frequency of encountering ADH and the underestimation rate among ADH lesions (Table 4). In a European multiple-institution study [20] of 517 lesions on which MRI-guided 11-gauge vacuum-assisted biopsy was successful, ADH was encountered in 17 (3%) of the lesions. Surgery revealed cancer in five (29%; 95% CI, 10-56%) of these lesions, all of which were DCIS. In four U.S. studies [16-19] of MRI-guided 9-gauge vacuum-assisted biopsy in 245 lesions, ADH was encountered in 15 lesions, accounting for 15 (48%) of 31 high-risk lesions and 15 (6%) of all lesions subjected to MRI-guided vacuumassisted biopsy in these studies. Among 15 ADH lesions, surgery revealed cancer in six (40%; 95% CI, 16-68%), and all of the malignant tumors were DCIS. The frequencies of ADH underestimation did not differ significantly in published reports of MRI-guided vacuum-assisted biopsy with 9-gauge versus 11-gauge probes (p =0.8).

View larger version (112K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A —49-year-old woman who had undergone ipsilateral lumpectomy yielding ductal carcinoma in situ (DCIS) 3 years earlier. Sagittal image from first T1-weighted 3D fat-suppressed fast spoiled gradient-echo sequence (TR/TE, 17/2.4; flip angle, 35°) after IV administration of gadopentetate dimeglumine shows susceptibility artifacts (black arrow) in area of previous lumpectomy. Suspicious focal enhancement (white arrow) is present at 12-o'clock axis.

View larger version (104K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B —49-year-old woman who had undergone ipsilateral lumpectomy yielding ductal carcinoma in situ (DCIS) 3 years earlier. Sagittal delayed MR image obtained after contrast injection shows susceptibility artifacts (black arrow) and washout (white arrow) from enhancement at 12-o'clock axis.

View larger version (66K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C —49-year-old woman who had undergone ipsilateral lumpectomy yielding ductal carcinoma in situ (DCIS) 3 years earlier. Sagittal delayed image obtained after contrast injection and after B shows susceptibility artifacts (black arrow) and that enhancement (white arrow) at 12-o'clock axis has become even less conspicuous, consistent with washout.

View larger version (96K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D —49-year-old woman who had undergone ipsilateral lumpectomy yielding ductal carcinoma in situ (DCIS) 3 years earlier. Sagittal image from T1-weighted 3D fat-suppressed fast spoiled gradient-echo sequence (17/2.4; flip angle, 35°) obtained after IV contrast injection on day of MRI-guided vacuum-assisted biopsy. Nipple and susceptibility artifacts (black arrow) serve as landmarks to show that biopsy obturator was placed at site of suspicious enhancement (white arrow). More background enhancement is evident on biopsy day because patient underwent imaging in different phase of menstrual cycle. Histologic examination of MRI vacuum-assisted breast biopsy specimens revealed foci of marked atypical ductal hyperplasia involving florid sclerosing adenosis. Histologic examination after surgical excision showed DCIS, solid and cribriform types, intermediate to high nuclear grade, apocrine cytologic features, and minimal necrosis, mostly involving sclerosing adenosis.

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A —52-year-old woman with family history of breast cancer who underwent high-risk-screening MRI. Sagittal image from T1-weighted 3D fat-suppressed fast spoiled gradient-echo sequence (TR/TE, 17/2.4; flip angle, 35°) after IV administration of gadopentetate dimeglumine shows area of clumped enhancement (arrow) in ductal distribution at 6-o'clock axis.

View larger version (140K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B —52-year-old woman with family history of breast cancer who underwent high-risk-screening MRI. Sagittal image from T1-weighted 3D fat-suppressed fast spoiled gradient-echo sequence (17/2.4; flip angle, 35°) after IV contrast administration on day of biopsy shows clumped ductal enhancement (arrow) at 6-o'clock axis. Round signal void within clumped enhancement is from biopsy obturator, which is in center of enhancement. Histologic examination of MRI vacuum-assisted breast biopsy specimens showed atypical ductal hyperplasia with adenosis and stromal fibrosis. Histologic examination of surgical specimen revealed ductal carcinoma in situ, solid and cribriform types, intermediate nuclear grade, in background of atypical ductal hyperplasia.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A —48-year-old woman with family history of breast cancer who underwent high-risk-screening MRI. Sagittal image from T1-weighted 3D fat-suppressed fast spoiled gradient-echo sequence (TR/TE, 17/2.4; flip angle, 35°) after IV administration of gadopentetate dimeglumine shows clumped ductal enhancement (arrow).

View larger version (117K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B —48-year-old woman with family history of breast cancer who underwent high-risk-screening MRI. Sagittal image from T1-weighted 3D fat-suppressed fast spoiled gradient-echo sequence (17/2.4; flip angle, 35°) after IV contrast administration on day of biopsy shows area of clumped ductal enhancement (black arrow). Round signal void (dotted arrow) within clumped enhancement is from biopsy obturator.

View larger version (101K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C —48-year-old woman with family history of breast cancer who underwent high-risk-screening MRI. Zoomed view of sagittal image in A shows individual clumps (arrows) of enhancement in more detail.

View larger version (143K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3D —48-year-old woman with family history of breast cancer who underwent high-risk-screening MRI. Photomicrograph of section from specimen obtained at MRI vacuum-assisted biopsy shows multiple small benign intraductal papillomas with sclerosis in background of fibrocystic changes with rare foci of atypical ductal hyperplasia. Individual small benign intraductal papillomas (arrows) correspond to clumped areas of enhancement (arrows, C). Histologic examination of surgical specimen revealed small benign intraductal papillomas with sclerosis, fibrocystic changes, and ductal hyperplasia with focal atypia. (H and E, x20)

Our ADH underestimation rate should be interpreted in the context of the percutaneous breast biopsy literature. The ADH underestimation rate at MRI-guided 9-gauge vacuum-assisted biopsy in our study was 38%, which is within the range of ADH underestimates reported in other studies [16-20] of MRI-guided vacuum-assisted biopsy. Our observed 38% ADH underestimation rate at MRI-guided vacuum-assisted biopsy was higher than expected on the basis of findings in previous studies of stereotactic 11-gauge vacuum-assisted biopsy. Those studies showed ADH underestimation rates of approximately 20%. We hypothesize that the higher frequency of ADH underestimation at MRI-guided than at stereotactic biopsy reflects the higher prior probability of breast cancer in the women at high risk undergoing breast MRI.

In a previous study [10] of 104 ADH lesions encountered at stereotactic 11-gauge vacuum-assisted biopsies, surgery revealed cancer in 22 (21%) of the lesions. Nineteen (86%) of those 22 cancers were DCIS, and three (14%) were invasive carcinoma. ADH underestimation was significantly (p < 0.02) less likely if there was no family history of breast cancer (16%), if the lesion was smaller than 1 cm (13%), and if the mammographic target was removed (8%). However, all subgroups of stereotactically diagnosed ADH lesions had a sufficiently high frequency of cancer to necessitate surgical biopsy. In our study, we found no significant predictors of ADH underestimation at MRI-guided vacuum-assisted biopsy. On the basis of our findings and the findings in the literature, surgical excision is warranted for lesions yielding ADH at MRI-guided vacuum-assisted biopsy, as it is warranted for ADH lesions found at stereotactic biopsy [27].

Among ADH underestimates at MRI-guided vacuum-assisted biopsy in our study and in the literature, all upgrades were to DCIS without invasion (Figs. 1A, 1B, 1C, 1D and 2A, 2B). In contrast, among ADH underestimates at stereotactic biopsy, most cancers found at surgery are DCIS, but 14-45% are invasive carcinoma [10-12]. Why are all ADH upgrades at MRI-guided vacuum-assisted biopsy DCIS without invasion? The most likely explanation is that if invasion is present, the lesion is more likely to have a sonographic correlate and be subjected to biopsy under sonographic rather than MRI guidance [24]. A second hypothesis is that study with a larger number of lesions may be necessary to detect invasive cancer, which represents the minority of ADH upgrades. A third hypothesis is that invasive carcinoma may be more readily apparent than DCIS at MRI and therefore easier to target for biopsy. Further work is needed to test these hypotheses. Even in our population, most surgical excisions of lesions yielding ADH at MRI-guided vacuum-assisted biopsy revealed histologic features that were not malignant but were benign or high risk (Fig. 3A, 3B, 3C, 3D).

In conclusion, we obtained a diagnosis of ADH in 6% of lesions subjected to MRI-guided 9-gauge vacuum-assisted biopsy. Among those ADH lesions, surgery revealed cancer in 38%, and all of the malignant tumors were DCIS. The ADH underestimation rate, which is comparable with that reported in other studies of MRI-guided 9-gauge vacuum-assisted biopsy, is higher than would be expected on the basis of results from stereotactic 11-gauge vacuum-assisted biopsy. The higher frequency of ADH underestimation at MRI-guided biopsy than at stereotactic biopsy probably reflects the higher risk of breast cancer among women undergoing breast MRI than in the general population. We found no significant predictors of ADH underestimation in our small study, but further study with a larger number of patients is needed. Our data indicate that the diagnosis of ADH at MRI-guided vacuum-assisted biopsy, like the diagnosis of ADH at stereotactic biopsy, warrants surgical excision.

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