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© 1999 American Society for Clinical Oncology Utility of Magnetic Resonance Imaging in the Management of Breast Cancer: Evidence for Improved Preoperative StagingFrom the Departments of Surgery, Radiology, and Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, CA 94143. Address reprint requests to Laura J. Esserman, MD, MBA, Breast Care Center, UCSF/ Mount Zion Cancer Center, 2356 Sutter St, San Francisco, CA 94115–1714.
PURPOSE: The staging and treatment for breast cancer are changing; there is an increase in the incidence of ductal carcinoma-in-situ, the use of fine-needle aspiration and stereotactic biopsy for diagnosis, and the use of neoadjuvant chemotherapy. Thus, there is a need for a tool to assess more precisely the extent of cancer in the breast before surgery. To better plan surgical and chemotherapeutic interventions, we evaluated high-resolution magnetic resonance imaging (MRI) as such a tool. PATIENTS AND METHODS: Fifty-seven patients with 58 cases of breast cancer were evaluated preoperatively with MRI using a technique called the triple-acquisition rapid gradient echo technique to maximize anatomic detail. Imaging results were compared with mammography and subsequent pathology results. RESULTS: Magnetic resonance imaging correctly identified residual or primary cancer in 55 of 58 cases and accurately predicted the extent of the cancer in 54 of 58 cases. The anatomic extent was more accurately defined with MRI compared with mammography (98% v 55%). Magnetic resonance imaging added the greatest value in cases of multifocal disease. CONCLUSION: By applying MRI selectively to patients with a known diagnosis of cancer and focusing on defining the extent of malignant lesions, we were able to obtain clear and accurate anatomic information. Our results suggest that MRI could provide very valuable information for preoperative planning and single-stage resection in breast cancer. Based on preliminary data from our series, MRI would be valuable as a staging tool in the preoperative setting even if the cost is in the range of $1,300 to $2,000. It is already significantly less than the target cost, so it is reasonable to refine this technique for clinical use to help plan the most appropriate surgical intervention and possibly reduce costs as well. A careful prospective study is warranted to validate our findings.
SCREENING FOR AND EARLY clinical detection of breast cancer have led to the finding of tumors at an earlier clinical stage, which has clearly been shown to reduce mortality.1 Women with early breast cancer now have a choice of local therapy. Six randomized clinical trials have demonstrated that for women with stage I or stage II breast cancer, survival is equivalent regardless of whether patients undergo mastectomy or breast conservation.2-7 The majority of women will not die from breast cancer or suffer metastatic recurrence,1 but they will live for a long time with the sequelae of our treatment interventions. Now that we know that the choice of local therapy does not affect mortality, we must focus on ways to further minimize morbidity and the number of interventions for those who have this disease. The advent of fine-needle aspiration (FNA) and stereotactic core biopsy have enabled the diagnosis of breast cancer before a surgical biopsy. However, in these cases, information about tumor extent, traditionally provided by excisional biopsy, is not available. Resection margins that are clear of tumor are associated with the best local control for patients who choose breast conservation.8,9 The dilemma about margins is particularly problematic in patients with extensive intraductal carcinoma (EIC). The need for clear margins is also thought to be particularly important in noninvasive carcinoma or ductal carcinoma-in-situ.10 Multiple re-excisions and the accompanying anxiety could be reduced if we had better tools to define the extent of tumor before surgery. As many as 60% of patients require re-excision for breast conservation and many have several attempts for breast conservation before mastectomy.11 Thus, having a better idea of the extent of the tumor before surgery has significant potential for guiding patients who are making decisions about local therapy. In addition to having surgical options at the time of diagnosis, patients and physicians will now face the decision of whether to undergo neoadjuvant therapy before surgery. For women with T2 or T3 tumors, evidence from the National Surgical Adjuvant Breast and Bowel Project (NSABP)12 shows that by starting with adjuvant chemotherapy, 90% can expect a clinical response and 60% can achieve sufficient shrinkage to enable lumpectomy without adversely affecting their clinical outcomes. An accurate preoperative assessment will become increasingly important as this practice becomes widely adopted. Magnetic resonance imaging (MRI) may provide a window to visualize the extent of tumor involvement in breast tissue.13 What is needed is a technical focus on anatomic detail. We accomplished this using a new MRI method, a fast, high-resolution, three-dimensional imaging technique, for local staging. Much of breast MRI has focused on the ability to distinguish between benign and malignant disease14-16 and has emphasized high speed and contrast kinetics at the expense of detail and image quality. The diagnostic emphasis of these "dynamic" techniques may not compete with existing procedures that use mammography and/or sonography in combination with percutaneous needle biopsy. Our sequence technique was designed for patients with a known malignancy; thus, the primary goal was to maximize the potential to gain anatomic information. When applied in a focused manner, we believe that MRI can be an effective preoperative local staging tool for breast cancer. Magnetic resonance imaging would add value over mammography if it could reliably demonstrate the extent and location of the disease in the breast before surgical intervention. However, we must be careful not to introduce technology that just raises the cost of care or merely adds another procedure. Technology should be disseminated when its value is proven and when it is cost-effective. To see whether MRI has the potential for cost savings, we assessed the number, type, and cost of procedures that would have been saved with accurate preoperative staging by MRI. Although we did not perform a careful prospective trial to evaluate cost, we analyzed the change in surgical interventions and their attendant costs to determine an appropriate cost range for MRI where it would add value and not increase the cost of care. This information is included with our evaluation of MRI as an anatomic staging technique.
Patient Selection Any patient with a diagnosis of breast cancer and a planned surgical excision were eligible for the study. Proof of diagnosis came from pathologic material demonstrating breast cancer, ie, FNA demonstrating malignancy or high suspicion for malignancy, core biopsy (stereotactic or clinically directed) showing ductal carcinoma-in-situ (DCIS) or invasive breast cancer, or an excisional biopsy with positive surgical margins. Fifty-seven patients, accounting for 58 diagnoses, agreed to participate in the study, gave their informed consent, and were enrolled from June 1995 to September 1996. Patient age ranged from 32 to 70 years (mean age, 49 years). The tumor stages and diagnoses are listed in Table 1.
Magnetic Resonance Imaging Contrast-enhanced MRI of the breast was performed using a fast, fat-suppressed, three-dimensional technique called the triple-acquisition rapid gradient echo technique (TARGET) and signal enhancement ratio (SER) analysis17 (Hylton et al, submitted for publication). For TARGET imaging, three high-resolution, three-dimensional data sets are acquired, once before the injection of gadolinium contrast agent and twice in succession beginning with the injection of contrast (S0, S1, and S2). Images were acquired using pulse repetition time (TR), TR = 11 milliseconds, and echo delay time (TE), TE = 4.2 milliseconds, 256 x 192 matrix, 16- to 18-cm field of view, and 1- to 2-mm section thickness. Sixty-four sections were acquired with oversampling (number of repeated excitations [NEX] = 2) to avoid image aliasing with a scan time of 5.4 minutes. Magnetic resonance malignancies were identified by computer, using the following criteria: 80% or greater signal enhancement between the precontrast and first postcontrast image, and SER value less than or equal to 1, where SER is defined by the ratio of early to late enhancement ([S1-S0]/[S2-S0]). Above a threshold of 80% contrast enhancement, SER was found to provide the highest specificity for malignancy in a group of 157 patients undergoing biopsy for a suspicious breast abnormality.33 All of the measurements of tumor size, including MRI, were independently recorded. The MRI tumor size was calculated directly from the computer on the basis of enhancement. These measurements were recorded before surgery by Nola Hylton, and the investigator was blinded to mammographic results. All patients were scheduled for surgery of their breast abnormality and participated in the breast MRI study before going to the operating room. Breast MRI was performed on a General Electric 1.5-tesla Signa whole body imager, using a dual phased-array breast coil. Patients underwent imaging in the prone position, and frequency encoding along the anterior-posterior direction was used to minimize artifacts from respiration and cardiac motion. Gadolinium DTPA was administered at a dose of 0.1 mmol/kg body weight through an indwelling intravenous catheter placed at the start of the study. The contralateral breast was not imaged to maximize information and resolution from the affected breast.
Microscopic and Radiographic Tumor Extent When available, mammograms (50 cases) were reviewed retrospectively by one mammographer in a blind fashion. Size and extent of masses and calcifications were noted. In a blind re-review of 43 of the 50 cases, a single discrepant reading was found. In seven cases, for which films were not available for review, data were taken from the original mammogram reports. Mammographic and MR images were considered concordant on extent if image measurements were within 50% to 150% of the microscopic pathology measurement in the greatest dimension. There is no gold standard by which to judge the accuracy of imaging. Even pathologic size can be somewhat arbitrary when the microscopic tumor margins extend beyond the gross borders. The generous criterion of 50% to 150% was chosen to identify significant differences in concordance. Of the 58 tumors referred to our study for MR imaging, 50 showed residual tumor at final pathology. These cases were used to evaluate MRI and mammographic concordance with pathology. In five cases of re-excision, before or after neoadjuvant chemotherapy, mammograms were not repeated after the initial biopsy. Thus, there were 45 cases in which MR images and mammograms were evaluated for detection of malignancy and concordance with surgical pathology on the extent of disease.
Assessing the Impact of MRI on Surgical Decision Making
Cost Analysis
Details of the types of cancers studied are listed in Table 1. The majority of patients had invasive ductal cancers. Sixteen percent had an extensive intraductal component. Patients were recruited if they had a biopsy showing positive margins (n = 15 patients) or an FNA or stereotactic biopsy confirming a malignancy (n = 42 patients). In eight cases (14% of the series and 53% of those with positive margins), no residual tumor was found on MRI. In one case, in which there were two anatomically separate lesions, each of a different histologic type, the lesions were considered to be separate tumors for the purpose of analysis, except in the evaluation of the impact of MRI on surgical decision making.
MRI-Based Preoperative Staging
Figures 1, 2, and 3 show the detailed anatomic pictures that can be obtained with the MRI techniques described. Figure 1, A and B, shows the pre- and postcontrast MRI, respectively, of a cancer with central ductal portion and several surrounding foci of lobular disease in a young woman with dense breasts where the lesion was not visualized on mammography. Figure 1, C and D, shows pre- and postcontrast MRI, respectively, of a lesion that was palpable and visualized on both MRI and mammography, but the MRI also accurately identified two additional satellite lesions that showed contrast enhancement and therefore suggested tumor not appreciated clinically or mammographically. Figure 2, A and B, shows pre- and postcontrast views, respectively, of a breast cancer with an extensive intraductal component. Although the primary tumor was identified by mammography, the EIC component was only appreciated on the MR image. Figure 3, A and B, shows alternate methods of viewing the three-dimensional nature of the tumor with MRI, by showing a cut-away three-dimensional reconstruction in the lateral (Fig 3A) and cranial caudal (Fig 3B) projections.
Concordance of MRI and Mammography
Potential Impact of MRI on Patient Management
Figure 4 is a graphic representation of the anticipated charges potentially avoided by more accurate preoperative staging of breast cancer. The x-axis represents time in years, and the y-axis is cost in adjusted 1995 dollars. We itemized the costs of the procedures projected to be avoidable, using Medicare reimbursement rates. This total, $102,659, was divided by the total number of MRIs (n = 57) performed. The shaded area represents a 20% cost variance above and below the calculated cost saved per procedure, represented by the line and shading rising to the right. Providing a range also helps to adjust for variation in practice, such as radiation after excision of DCIS (for example, if all seven patients had chosen radiation, the minimum cost threshold for MRI would need to be lowered by $190). The cost of MRI, represented by the solid black line, is anticipated to decline over time because of the decreasing time required for image acquisition as the technique becomes better developed (see Fig 4). We adjusted the hourly rate for MRI to reflect the reduction in scan time associated with improvements in technology. Our estimates suggest that preoperative staging with MRI is within the range of costs that are incurred by unrecognized multifocal or microscopic spread, which necessitates one or more surgical procedures. This analysis estimates that the projected charges for MRI would be surpassed by the estimate of charges incurred but avoidable, using the information from preoperative MRI in 1994, when MR imaging time was projected to be just over 1 hour, assuming the information from MRI is reliable and accurate. All charges, including the hourly rates, were estimated by using the Medicare fee schedule. We used Medicare fee schedules as a proxy for cost in order to have a standard metric measure for estimating cost.
There is clearly room for improvement in local disease management. Patients preferring breast preservation are often faced with biopsy results that demonstrate surgically and pathologically unrecognized disease at the margins, even when margins are inspected grossly by experienced pathologists. In such cases, it can be difficult to determine whether re-resection will be successful. Re-resection is surprisingly common. In a recent randomized clinical trial, Recht et al11 found that 67% to 69% of women underwent re-resection between 1984 and 1992. For patients with only a focally positive margin, lumpectomy and radiation can lead to acceptable local control rates.9 The problem is knowing whether there is more disease remaining. In patients with a diagnosis of DCIS, a review of 62 sequential cases of DCIS at our institution revealed that only 19% had one procedure and that 81% of patients required more than one procedure for adequate excision (H. Wilkie, personal communication, September 1997). Before FNA for palpable masses and stereotactic core biopsy for mammographic lesions were widely used, re-resection could be performed at the time of lymph node dissection or mastectomy. However, with the advent of better preoperative diagnoses and the increasingly common clinical scenario where axillary dissection is not performed (thus eliminating a second trip to the operating room), it is becoming more important to develop noninvasive tools to predict resectability from both the patient quality and cost-effective perspectives. Recent interest in MRI of the breast stems from reports that malignant lesions are enhanced significantly after contrast injection while benign lesions show little or no enhancement.16,19-26 Numerous studies indicate that breast MRI is sensitive to small cancers in the breast, at sizes smaller than 1 cm,20,21,27 and can successfully image the dense breast.16,19-21 In one study, MRI detected 80% of all tumor foci, whereas mammography detected 20% when compared with thin-slice pathology of mastectomy specimens.27 Harms et al16 reported that in 35 patients, 100% of multifocal cancers, confirmed by serial sectioning of mastectomy specimens, were visualized by MRI.28 Orel et al15 found many more tumors with MRI than with mammography in their series of 176 patients, 57 of whom had cancer. Thirty-four percent of patients with cancer had one or more tumors that could not be seen with mammography. Twenty percent had unsuspected multifocal disease that was found on MR images but not on mammograms. However, MRI has demonstrated only moderate specificity, and thus it cannot be used alone as a test for malignancy.16,19-21,29 Mammography is an excellent screening tool and is likely to continue to be the test of choice for the asymptomatic breast.29 However, MRI, if carefully developed, has the potential to be the tool of choice for evaluating the symptomatic breast. With this goal in mind, we focused our technical development on "staging" the breast, providing crisp anatomic detail and, therefore, maximum clinical information about size and extent of disease. Diagnostic applications rely on contrast kinetics and emphasize scan speed, often at the sacrifice of spatial detail. When using MRI for staging, the parameters can be changed because the diagnosis of cancer has been established; thus, the focus of MRI can be on maximizing image quality rather than on differential kinetics of contrast uptake. The TARGET staging technique involves the acquisition of three sequential images, ie, one precontrast and two postcontrast images. This technique is designed for high spatial resolution for maximum anatomic clarity while maintaining sensitivity to small and multifocal lesions.19,20,30,31 The result is much greater anatomic detail, which allows identification of multifocal or microscopically extensive tumors. A potential barrier to wide adoption of MRI is the difficulty in image interpretation and reader variability. An anatomic technique such as TARGET, described in this article, helps to address both of these problems. First, the clarity of the images improves one's ability to evaluate the films. Second, the use of computer algorithms to assess tumor size by objective criteria will minimize reader variability and make MRI a more robust and clinically useful tool. We found that MRI was much more accurate than mammography in identifying the extent of disease (98% v 54%), although both identify known tumors (98% v 84% for MRI and mammography, respectively). We have also found that MRI has the greatest added value for identifying the presence and extent of multifocal tumors. When either MRI or mammography identified the lesion, the greatest differential between MRI and mammography was seen for multifocal lesions (Table 3). A prospective study with larger numbers for each pattern of tumor spread will be needed to verify our findings and is currently under development. Other investigators have also found that MRI is useful for documenting multifocal lesions. Recently, Boetes et al32 from the Netherlands described their experience using magnetization-prepared rapid gradient echo sequence (MP-RAGE) with and without contrast in 60 patients undergoing mastectomy for breast cancer. Magnetic resonance imaging was 96% successful in identifying the index tumor lesion, compared with a 90% success rate for mammography and an 85% success rate for ultrasonography. Mammography and ultrasonography underestimated size by 14% and 18%, respectively. In cases in which the index lesion was multifocal, MRI was clearly better in showing additional foci of tumor when compared with mammography and ultrasonography (100% v 31% v 38%, respectively). One of the greatest potential impacts of MRI technology is the ability to determine, before surgery, the extent of DCIS. More work is necessary, but this is a very promising application. In the 13 cases in which DCIS was the only diagnosis, we were able to accurately identify the extent of disease in 85% of women. Magnetic resonance imaging accurately determined the extent of disease in six of the seven cases in which residual disease was found after initial resection for DCIS. Six of the 13 had no residual disease, and five of the six were confirmed by MRI. One of our false-negative results was in a woman who had low-grade DCIS. The lesion was identified, but the percentage of enhancement was not sufficient to reach our threshold for cancer. The lower enhancement for low-grade DCIS may be a more accurate reflection of the biology of lesion, but a much larger series will be needed to establish a correlation. For women who desire both breast conservation and limited numbers of trips to the operating room, prior knowledge of DCIS extent would be invaluable; thus, further research in this area is warranted. If MRI can truly distinguish DCIS from invasive cancer, MRI could serve as a basis for new treatment interventions for DCIS. It should be noted, however, that more errors occurred in the DCIS group. Application of this technology to DCIS may be less accurate compared with invasive cancer, and more focused research in the area DCIS is required. False-positive results with MRI have been shown in fibrosis, inflammatory changes from a prior biopsy, atypical hyperplasia, and fibroadenoma or hematoma.14-16,28,29 We have described a potential solution to false-positive results through the analysis of differences in contrast-uptake behavior, as measured by a signal enhancement ratio, or SER value. Tumor and tissue patterns can be divided into gradual, sustained, or fast uptake and washout. We have found that gradual uptake, or low SER values, precludes a diagnosis of cancer13 (Hylton et al, submitted for publication). In an era of patient choice, accurate information is essential to help avoid the trauma of multiple resections or the disappointment associated with the absence of residual disease in a mastectomy specimen. We estimate that the information available by MRI would have had the potential to affect the decision making in 21 of our 57 patients. Orel et al15 also found that at least 11% of patients had their stage and treatment changed by MRI information, and when multifocal disease was present, MRI was much more accurate.32,33 We and others have found that MRI is particularly helpful for patients with multifocal disease. Although this study is not a prospective trial, our data give an indication of the value of conducting a trial of MRI for preoperative staging of breast cancer. Although this study represents one institution's experience with MRI, the patient population studied is highly representative of the kinds of patients seen within the community and at academic centers who are likely to benefit from MRI. The health care climate in the United States has made clear that if new technology is to be introduced and supported, the burden is on its proponents to demonstrate that it will add value and ultimately decrease costs of care. To demonstrate whether that potential exists, a model of financial impact was included. The purpose of this exercise is to determine whether the technology is in the economic range for the expected clinical value. The technology migration figure (Fig 4) shows the potential economic impact of the routine introduction of MRI. Our data do not show that MRI would be cost-effective in diagnostic management because we only imaged patients with known diagnoses of cancer. We can, however, estimate the range of costs that might be avoided with the use of MRI before surgery and use it as a guide to determine the economic feasibility of using MRI in a routine clinical setting. In particular, we can use a conservative cost savings estimate to help set a target cost for the dissemination of this new technology. Obviously, economic cost estimates represent only one dimension of savings. The ability to give patients an accurate idea of what surgical treatments are likely to be successful and the ability to avoid the trauma of multiple trips to the operating room are of great emotional benefit. A cautionary note must be added. MRI will only be successful if the technology is carefully deployed. First, the findings must be confirmed in a prospective trial. Second, we do not have the ability to easily localize and sample all of the areas that are enhanced with MRI. The development of stereotactic tools represents a complementary technology that must accompany MRI development if the clinical application of routine MRI is to be valuable and cost-effective. Third, our study was conducted on a high-field magnet (1.5 Tesla). Most interventional MR magnets operate at lower field strengths (< 0.5 Tesla). The TARGET imaging method may not be attainable at lower-field strength because of reduced image quality and/or longer scan times and the inability to use spectrally selective fat-suppression techniques. Fourth, utilization of machines will have a large impact on costs. The purchase of an MRI machine requires a large capital investment; thus, the cost of MR images will truly reflect the volume of patients regardless of what is charged. Cost reductions in MRI will be gained through experience (decreased interpretation time) and full utilization of the MRI machines. Rampant dissemination of many machines that may be underpowered and underutilized will prevent this technology from being clinically valuable and affordable. Before breast MRI is disseminated as an acceptable technology, a careful prospective trial is needed to validate the efficacy of MRI for preoperative staging of breast cancer, and the diagnostic imaging parameters must be standardized. We are currently starting such a prospective trial with a careful cost analysis to determine whether routine use of MRI is cost-effective. If MRI can be established as an accurate staging tool, it can be used to defray the cost and associated trauma of multiple procedures in women with breast cancer.
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ABSTRACT
INTRODUCTION
