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1 Breast Imaging Section, Department of Radiology, Memorial Sloan-Kettering
Cancer Center, 1275 York Ave., New York, NY 10021.
2 Medical Physics Section, Department of Radiology, Memorial Sloan-Kettering
Cancer Center, New York, NY 10021.
3 Clinical Genetics Service, Department of Medicine, Memorial Sloan-Kettering
Cancer Center, New York, NY 10021.
4 Breast Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center,
New York, NY 10021.
Received October 21, 2002;
accepted after revision December 31, 2002.
Address correspondence to E. A. Morris
(morrise{at}mskcc.org).
Abstract
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MATERIALS AND METHODS. Retrospective review was performed of the records of 367 consecutive women at high risk of developing breast cancer who had normal findings on mammography and their first breast MRI screening examination during a 2-year period. The frequency of recommending biopsy at the first screening MRI study and the biopsy results were reviewed.
RESULTS. Biopsy was recommended in 64 women (17%). Biopsy revealed cancer that was occult on mammography and physical examination in 14 (24%) of 59 women who had biopsy and in 14 (4%) of 367 women who underwent breast MRI screening. Histologic findings in 14 women with cancer were ductal carcinoma in situ in eight (57%) and infiltrating carcinoma in six (43%). The median size of infiltrating carcinoma was 0.4 cm (range, 0.1-1.2 cm). Two patients had nodes that were positive for cancer. Biopsy revealed high-risk lesions (atypical ductal hyperplasia, atypical lobular hyperplasia, lobular carcinoma in situ, or radial scar) in 13 (4%) of 367 women and other benign findings in 32 (9%) of 367 women who had MRI screening.
CONCLUSION. Among women at high risk of developing breast cancer, breast MRI led to a recommendation of biopsy in 17%. Cancer was found in 24% of women who underwent biopsy and in 4% of women who had breast MRI screening. More than half the MRI-detected cancers were ductal carcinoma in situ.
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Breast MRI has high sensitivity in breast cancer detection, reported to be as high as 94-100%, but lower specificity, 37-97% [9]. The high sensitivity of breast MRI is suitable for a screening test, but the lower specificity is problematic because it results in a large number of benign biopsies with their attendant costs in time, anxiety, and deformity, as well as their economic burden [10]. Few data address the frequency and positive predictive value of biopsy in breast MRI screening [11-16]. Furthermore, previous investigations have been few and most have included women with abnormal mammographic findings in the population undergoing MRI [11, 13, 14, 16]. Our study was undertaken in a larger population to determine the rate and results of biopsy in the first round of breast MRI screening in asymptomatic women with normal mammographic findings who were at a high risk of developing breast cancer.
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The 367 first high-risk screening breast MRI studies performed in these 367 women constitute 27% of 1336 breast MRI examinations performed during the study period. In addition to high-risk screening, other indications for breast MRI at our institution during the study period included evaluation of the extent of disease in women with known breast cancer, follow-up, and problem solving.
The 367 women in our study had a median age of 50 years (range, 23-82 years). None of these women had known synchronous breast cancer, defined as having occurred within 6 months before MRI. The median interval between mammography and MRI was 30 days (range, 0-270 days). In 355 women (97%), mammography was performed within 6 months of the breast MRI examination.
Breast MRI Technique
MRI examinations were performed with the patient prone in a 1.5-T
commercially available system (Sigma, General Electric Medical Systems,
Milwaukee, WI) using a dedicated surface breast coil
[17]. Our imaging sequence
includes a localizing sequence followed by a sagittal fat-suppressed
T2-weighted sequence (TR/TE, 4000/85). A T1-weighted three-dimensional,
fat-suppressed fast spoiled gradient-echo sequence (17/2.4; flip angle,
35°; bandwidth, 31.25 Hz) is then performed before and three times after a
rapid bolus injection of 0.1 mmol/L of gadopentetate dimeglumine (Magnevist,
Berlex, Wayne, NJ) per kilogram of body weight, delivered through an
indwelling IV catheter.
Image acquisition started after contrast material injection and saline bolus. Images were obtained sagittally for an acquisition time per volumetric acquisition of less than 3 min each. Total imaging time per breast, including three contrast-enhanced acquisitions, was approximately 20 min. Section thickness was 2-3 mm with no gap using a matrix of 256 x 192 and a field of view of 18-22 cm. Frequency was in the anteroposterior direction. After the examination, the unenhanced images were subtracted from the first contrast-enhanced images on a pixel-by-pixel basis.
Breast MRI Interpretation
Breast MRI examinations were interpreted according to previously described
criteria [18]. In our
practice, MRIs were interpreted by breast imaging specialists in conjunction
with clinical history and other breast imaging studies, including mammograms
and sonograms, when available. Level of suspicion was reported on a scale of
0-5, with 0 indicating additional imaging needed; 1, no abnormal enhancement;
2, benign enhancement; 3, probably benign, short-term follow-up recommended
(specified as either at different time in the patient's menstrual cycle or in
6 months); 4, suspicious; and 5, highly suggestive of malignancy. The
determination of level of suspicion was made by the individual radiologist on
the basis of individual experience and the literature
[18].
MRI-detected lesions referred for biopsy primarily included masses with spiculated or irregular margins, irregular shape, or heterogeneous or rim enhancement, and nonmass lesions showing linear or segmental enhancement. Other lesions were referred for biopsy at the discretion of the interpreting radiologist in conjunction with clinical history and other imaging studies. Tiny (1-mm) foci of enhancement or diffuse stippled enhancement generally did not prompt biopsy. Classification was based primarily on lesion morphology; however, kinetic features were visually assessed on the three contrast-enhanced image acquisitions, with quantitative kinetic curves generated in specific cases at the request of the interpreting radiologist.
For nonpalpable, mammographically occult, MRI-detected lesions warranting biopsy, correlative sonography was recommended at the discretion of the radiologist interpreting the MRI examination if it was thought that the lesion might be sonographically evident and amenable to sonographically guided biopsy. If the lesion was not seen on sonography, MRI-guided needle localization for surgical excision was performed using previously described methods [17].
Data Collection and Analysis
Records of the 367 women who underwent breast MRI screening were reviewed
to determine risk factors (prior breast cancer; family history; BRCA
status; biopsy-proven diagnosis of atypia, lobular carcinoma in situ, or
radial scar; or prior mantle radiation for Hodgkin's disease), menopausal
status, and mammographic parenchymal density
[2]. MRIs were reviewed by one
radiologist who was unaware of the pathology outcome, and lesions were
classified using previously described terminology
[18]. Mammograms were reviewed
to assess a mammographic correlate to the MRI-detected lesion. Pathology
records were reviewed to determine biopsy results, including stages of cancers
detected [19].
Data were recorded in a spreadsheet (Excel, Microsoft, Redmond, WA). Statistical analysis was performed with the chi-square and Fisher's exact tests using statistical software (Epi Info, Centers for Disease Control and Prevention, Atlanta, GA), with a p value of 0.05 considered significant. Exact confidence limits were calculated in accordance with the Geigy scientific tables [20].
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The biopsy method in 59 women was MRI-guided localization in 50 women, sonographically graphically guided core biopsy in five women, sonographically guided needle localization in three women, and sonographically guided fine-needle aspiration biopsy in one woman. Of the five women in whom biopsy was recommended for an MRI-detected lesion but not performed, two declined biopsy, two were scheduled for MRI-guided needle localization but the enhancing lesions were no longer evident, and one sought care elsewhere.
Biopsy Results: Patients
Biopsy revealed cancer that was occult on mammography and physical
examination in 14 women, constituting 24% (95% CI, 14-37%) of the 59 women who
had biopsy and 4% (95% CI, 2-6%) of the 367 women who had breast MRI screening
(Table 1). Cancer was found in
12 (24%) of 50 women who had MRI-guided needle localization versus two (22%)
of nine women who had sonographically guided biopsy (p = 1.0). The
two cancers with sonographic correlates were infiltrating carcinoma.
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Histologic findings in 14 women with MRI-detected cancers were ductal carcinoma in situ (DCIS) in eight (57%) and infiltrating carcinoma in six (43%) (Figs. 1, 2, 3A, 3B, 3C, 4A, 4B). Median size of infiltrating carcinoma was 0.4 cm (range, 0.1-1.2 cm); two had axillary metastases. The stage of MRI-detected cancer, known in 13 women, was stage 0 in eight women (62%), stage I in three (23%), and stage II in two (15%). Treatment for MRI-detected cancer, known in 13 women, was mastectomy in seven women (54%) and breast-conserving surgery in six (46%).
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Among 14 women with MRI-detected cancer, the median age was 50 years (range, 29-79 years). Median age was 49 years (range, 29-79 years) for the eight women with DCIS and 50 years (range, 42-69 years) for the six women with infiltrating carcinoma. The median interval between mammography and MRI in these 14 women was 11 days (range, 0-75 days). Thirteen (93%) of 14 women had a family history of breast cancer, including three with a family history of breast cancer in a first-degree relative. Nine women (64%) had both personal and family histories of breast cancer. Ten (71%) of 14 women had prior breast cancer at a median of 38 months (range, 11-180 months) before MRI. The MRI-detected cancer was in the treated breast in five (50%) and in the contralateral breast in five (50%). One of 14 women tested positive for BRCA2.
Biopsy Results: MRI Findings
Biopsy was performed for 79 MRI-detected lesions in 64 women (average, 1.2
lesions per woman; range, one to three lesions per woman). The median size of
MRI-detected lesions that underwent biopsy was 1.0 cm (range, 0.4-5.9 cm). The
median size of MRI-detected lesions yielding benign results was 0.9 cm (range,
0.4-4.9 cm), and the median size of MRI-detected lesions yielding carcinoma
was 1.3 cm (range, 0.5-5.9 cm).
Cancer was identified in 16 lesions, including 20% (95% CI, 12-31%) of 79 lesions that had biopsy. Among these 16 cancers, 10 (63%) were DCIS and six (38%) were infiltrating cancer (Table 2). These 16 malignant lesions occurred in 14 women, including one with multifocal cancer and one with synchronous bilateral MRI-detected cancers. The features with the highest positive predictive value were linear or ductal enhancement for nonmass lesions and spiculated margins for masses (Table 2). Cancer was more frequent among lesions classified as highly suggestive of malignancy than among those classified as suspicious (50% vs 18%, p = 0.09) (Table 3). Kinetic features and T2 signal intensity were not significant predictors of carcinoma (Table 3).
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Statistical Analysis
The positive predictive value of biopsy was significantly greater in women
with a family history of breast cancer than in women without such history (32%
vs 6%, p < 0.05) and in women with both a family history and a
personal history of breast cancer than in women without this combination (50%
vs 12%, p = 0.006) (Table
4). The positive predictive value of biopsy did not differ
significantly as a function of other factors, including menopausal status,
prior breast cancer (history, histology, stage, or treatment), or mammographic
parenchymal density (Table
4).
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The prevalence of MRI-detected cancer was significantly greater in women with a family history of breast cancer than in women without such history (6% vs < 1%, p = 0.02), in women who had undergone prior breast-conserving surgery for cancer than in women who had prior mastectomy (7% vs 2%, p < 0.05), and in women with both a family history and a personal history of breast cancer than in women without this combination (8% vs 2%, p < 0.02) (Table 4). No significant differences were observed in the prevalence of MRI-detected cancer as a function of other factors, including menopausal status, prior breast cancer stage or histology, or mammographic parenchymal density (Table 4).
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Screening mammography can detect breast cancers in high-risk women but has limitations, particularly in women with dense breasts that can obscure a cancerous lesion [21, 22]. Kopans [23] has estimated that if a group of 100 women with breast cancer are screened with mammography and clinical breast examination, 80 of the cancers will be detected, by mammography in 68 women (85%) and by physical examination in 12 (15%). Another 20 cancers will become palpable during the next year and will be diagnosed as interval cancers, which tend to be aggressive. Ancillary screening modalities can detect at least some of these interval cancers early, thereby decreasing breast cancer mortality [23], but such screening also generates additional biopsies of benign lesions, with the associated impact of false-positive results [10].
We present the largest study to date evaluating the use of breast MRI to screen women at high risk of developing breast cancer. Breast MRI can detect cancers that are mammographically and clinically occult [11-15] (Table 5). Of our asymptomatic high-risk women with normal mammographic findings who had breast MRI screening, biopsy was recommended in 17%. Biopsy revealed cancer that was occult to mammography and physical examination in 24% of women who had biopsy and in 4% of women who had breast MRI screening. The 4% prevalence of MRI-detected cancer in high-risk women in our study is comparable to the 2-7% prevalence of cancer detected only at MRI in prior reports [11-16] (Table 5). The 24% positive predictive value of biopsy is within the 18-88% range of positive predictive values for biopsy based on MRI findings in high-risk women [11-16] (Table 5) and within the 20-40% range of positive predictive values for mammographically guided needle localization and surgical excision in the general population [24].
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More than half (57%) of our MRI-detected, mammographically occult cancers were DCIS. In prior reports, DCIS has accounted for 0-43% of cancers detected by MRI screening in high-risk women (Table 5). The higher proportion of DCIS among MRI-detected cancers in our study may reflect our interpretation criteria, which emphasize lesion morphology, and our imaging parameters, which emphasize high resolution [18]. Although Ernster et al. [25] have suggested that detection of DCIS by screening may lead to overtreatment of an innocuous disease, published data do not support their contention. Previous investigators have shown that approximately 30% of women with untreated DCIS develop ipsilateral invasive breast cancer at long-term follow-up; among these, more than half develop distant metastases [26-28]. These studies show the potential for untreated DCIS to progress to invasive cancer with its associated morbidity and mortality, and support the usefulness of detecting and treating DCIS.
Our data allow us to suggest subgroups of high-risk women most likely to benefit from breast MRI screening. The positive predictive value of biopsy based on MRI findings was significantly greater in women with a family history of breast cancer (positive predictive value, 32%), particularly among those women who had both a family history and a personal history of breast cancer (positive predictive value, 50%). In the first round of screening, MRI detected an otherwise occult cancer in 4% of all high-risk women in this study, in 6% of women with a family history of breast cancer, in 7% of women who had undergone prior breast-conserving surgery for breast cancer, and in 8% of women who had both a personal history and a family history of breast cancer. Breast MRI screening is likely to have the highest yield in women with both a family history and a personal history of breast cancer, particularly those previously treated with breast conservation.
Women with mutations in the BRCA1 or BRCA2 genes, who constituted 5% of our population, account for approximately 5-10% of women with breast cancer in the general population [3]. Lifetime breast cancer risks of up to 85% have been calculated for women with germline mutations in either BRCA1 or BRCA2, although other studies of less-selected groups have suggested that risks may be lower [3, 29]. Mammography may have lower sensitivity in detecting breast cancer in women with a genetic predisposition to breast cancer than in the general population [11, 30, 31]. Previous studies of women with genetic mutations or strong family histories of breast cancer have shown that MRI is more sensitive than mammography in detecting breast cancer in these women, with reported sensitivities of 33-50% for mammography and 86-100% for MRI [11, 13, 14]. Further study of MRI screening in women with genetic predisposition to breast cancer is needed.
Breast sonography has been suggested as a screening test for high-risk women with dense breasts [32-35]. MRI, however, has several advantages over sonography. The prevalence of cancer at MRI screening in high-risk women is 2-7% [11-15], significantly greater than the four to six per 1000 prevalence of cancer in high-risk women reported in prior studies of screening breast sonography [32, 33, 35]. In studies of high-risk women who have had sonography and MRI in addition to mammography, the 86-100% sensitivity of MRI was greater than the 13-43% sensitivity of sonography [11, 13, 16]. MRI is more sensitive than sonography in the detection of DCIS [36]: DCIS, which accounted for more than half the MRI-screening detected cancers in our study, accounted for only 0-17% of cancers detected at screening sonography in prior reports [11, 32-35]. The 18-88% positive predictive value of biopsy in studies of MRI screening [11-15] is significantly greater than the 7-14% positive predictive value of biopsy in studies of screening sonography [11, 32-35]. Breast sonography does retain some advantages, however, including widespread availability, ready access for biopsy procedures, speed, and lower cost.
Although MRI screening can detect otherwise occult breast cancers in high-risk women, several caveats should be remembered. MRI is expensive, and neither the technique nor the interpretive criteria are standardized; variability may occur in performance and interpretation [9]. MRI may not be feasible in some women, such as those with pacemakers, aneurysm clips, or claustrophobia [37]. Breast MRI screening should be performed in a setting in which it is possible to perform biopsy of lesions detected at MRI only; biopsy systems are commercially available but not yet widely used [17]. Breast MRI may result in benign biopsy findings, with the attendant cost and anxiety [10]: among high-risk women who have breast MRI screening, 3-15% have a subsequent biopsy yielding benign results [11-15]. Our data represent results from screening a high-risk population; MRI screening done on women with lower risk than those reported here might have a lower detection rate. Finally, the impact of MRI detection of cancer on survival has not yet been determined.
In conclusion, in our high-risk population that, to our knowledge, is the largest series to date, breast MRI led to a biopsy recommendation in 17% of women. Cancer was found in 24% of women who had biopsy and in 4% of women who had breast MRI screening. More than half the MRI-detected cancers were DCIS. Kopans [23] has stated that the only definitive proof of benefit of breast cancer screening comes from randomized controlled trials, with death as the end point [23]. Neither our study nor previous reports provide such proof, but trials of breast MRI screening are in progress. Further work, including refinements in technique and interpretation; long-term follow-up; and assessments of sensitivity, specificity, and cost effectiveness, is needed to define the role of breast MRI in screening women at high risk.
Acknowledgments
We thank Alicia Parlanti, Cathleen Cooper, Jeffrey Radeckje, and Flavia
Facio for their work in performing this study. Important technical assistance
came from Richard Fischer and Charles Nyman.
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