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Breast Imaging |
1 From the Departments of Radiology (S.G.O., S.P.W., M.D.S.), Surgery (D.L.F.), and Radiation Oncology (L.J.S.) and the Hematology-Oncology Division (L.M.S.), University of Pennsylvania Medical Center, 3400 Spruce St, Philadelphia, PA 19104; and the Department of Anatomic Pathology, Mayo Clinic, Rochester, Minn (C.A.R.). Received July 8, 1998; revision requested August 18; final revision received October 22; accepted February 10, 1999. Address reprint requests to S.G.O. (e-mail: orel@oasis.rad.upenn.edu).
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: Between October 1993 and December 1997, 38 women with malignant axillary adenopathy and negative mammographic and physical examination findings underwent contrast material–enhanced MR imaging. Sixteen patients were excluded due to axillary tail cancer (n = 7), lack of follow-up (n = 4), second primary malignancy (n = 3), or chemotherapy before MR imaging (n = 2). The study population comprised the remaining 22 patients. Histopathologic findings were available in 20 patients; follow-up MR imaging findings were available in two patients.
RESULTS: MR imaging depicted a primary breast cancer in 19 patients (86%; identified at excisional biopsy or mastectomy in 17, resolved on follow-up MR images during treatment in two). MR imaging depicted 4–30-mm cancers (mean, 17 mm), which correlated closely with histopathologic size. Two patients (9%) had false-negative findings: (a) One had a 2-mm invasive ductal carcinoma, and (b) one had 17- and 20-mm invasive ductal carcinomas. Of the 19 patients, 11 underwent mastectomy, seven underwent breast-conservation therapy, and one did not undergo a surgical procedure.
CONCLUSION: MR imaging is very sensitive for the detection of mammographically and clinically occult breast cancer in patients with malignant axillary adenopathy. In these patients, MR imaging offers potential not only for cancer detection but also for staging the cancer within the breast, which may be useful for treatment planning.
Index terms: Breast neoplasms, diagnosis, 00.121412, 00.121415, 00.12143, 00.30 • Breast neoplasms, localization, 00.121412, 00.121415, 00.12143, 00.30 • Breast neoplasms, metastases, 997.33 • Breast neoplasms, MR, 00.121412, 00.121415, 00.12143, 00.30 • Breast neoplasms, staging, 00.30
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The most commonly used treatment in patients with axillary node metastases and an unknown primary site has been mastectomy and axillary node dissection (1–3). However, there can be a reluctance to perform "blind" mastectomy, since in approximately one-third of cases, no tumor is found at microscopic evaluation of the mastectomy specimen (4,5). Articles reporting the results of breast-conservation therapy in these patients have shown no survival difference between those who undergo mastectomy and those who do not, which supports the use of breast-conservation therapy with breast irradiation as an alternative to mastectomy (1,3,6–8). Yet, there is concern that in those patients with a relatively large occult tumor burden, whole-breast irradiation is unlikely to control the disease (3).
The ability of mammography to depict a primary breast cancer and define its extent in patients with axillary node metastases at presentation has been disappointing (4,6,8,9). The reported incidence of finding an occult breast cancer at mammography has ranged from 0% to 56% (3). In two series (6,9), when a primary tumor was found in the breast at microscopic examination, the mammogram was positive in only 29% and 35% of the cases. Findings of several studies now demonstrate the potential of magnetic resonance (MR) imaging to have greater sensitivity in the depiction of breast cancer than is possible with mammography, with multiple reported cases of MR imaging–detected mammographically and clinically occult carcinoma (10–15). The purpose of this study was to assess the usefulness of MR imaging of the breast in patients with axillary node metastases and negative clinical and mammographic findings at presentation.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Of the 38 patients, 16 were excluded from the study due to axillary tail cancer (n = 7), lack of follow-up (n = 4), a second primary nonipsilateral breast cancer (n = 3), or chemotherapy prior to MR imaging (n = 2). In the seven patients with axillary tail cancer, the tumor was removed prior to the MR imaging examination in four patients, was identified at MR imaging in two patients, and was not identified at MR imaging in one patient. MR imaging findings were negative in all four patients in whom surgical and/or clinical follow-up was not available. Among the three patients with a second nonipsilateral breast tumor, one patient had a contralateral breast tumor with identical histologic findings; among the other two patients, the tumors were metastatic melanoma and metastatic salivary gland tumor. In two of these three patients, the MR imaging findings were negative. In one patient, an enhancing lesion was identified and localized with MR imaging guidance but was proved to be fat necrosis. In the two patients who received chemotherapy prior to MR imaging, no abnormality was identified at MR imaging.
The remaining 22 patients made up the study population. The women ranged in age from 37 to 66 years (mean age, 49 years). Diagnostic mammography was performed at an outside institution in 21 of the 22 patients and at the University of Pennsylvania Medical Center in one patient. Reports were available for all of the outside mammograms. Eighteen of the 21 outside mammograms and the one inside mammogram were available for review. All available mammograms were retrospectively reviewed by one radiologist (S.G.O.) experienced in breast imaging who had knowledge of the clinical history. The mammograms were reviewed to ensure that no suspicious findings (mass, microcalcifications, or architectural distortion) could be identified in either the breast ipsilateral to the malignant axillary nodes or the contralateral breast. The time from mammography to MR imaging examination was 0–84 days, with a mean of 40 days.
MR imaging was performed with a 1.5-T Signa system (GE Medical Systems, Milwaukee, Wis) equipped with a prototype high-performance gradient system. All patients were imaged in the prone position by using a specially designed compression multicoil array (16). Sagittal T1-weighed spin-echo (500–600/17 [repetition time msec/echo time msec]) and sagittal fat-suppressed T2-weighted fast spin-echo (4,000/120 [effective echo time]) imaging was performed with a 12–16-cm field of view, 3-mm section thickness, 1-mm gap, and a 256 x 256 matrix. The entire breast was then imaged before and following the bolus administration of 20 mL of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) with a sagittal three-dimensional-volume fat-suppressed fast spoiled gradient-recalled-echo sequence (minimum repetition time/minimum echo time, 18-cm field of view, 2-mm section thickness, no gap, and a 256 x 512 matrix). Regardless of weight, each patient received 20 mL of gadopentetate dimeglumine as a bolus injection followed by 20 mL of physiologic saline. Imaging was initiated during the saline injection.
The three-dimensional-volume fast spoiled gradient-recalled-echo sequence evolved, and the imaging time for each three-dimensional volume decreased from 3 minutes 30 seconds to 90 seconds. For the 90-second sequence, the entire breast volume was imaged four times (total of 6 minutes).
The MR images were read prospectively by two radiologists (S.G.O., M.D.S.) experienced in MR imaging of the breast. The studies were read collectively, and a consensus was reached in each case. The images were read with knowledge of the clinical history of axillary node metastases and the negative mammographic and physical examination findings. The mammograms were not available at the time the MR images were reviewed.
A lesion was considered suspicious if it was enhanced on the first (90-second) postcontrast image and was visualized as (a) a mass with at least partially ill-defined or irregular borders, (b) an area of linear or branching enhancement suggestive of ductal enhancement, or (c) an area of regional enhancement where the borders of the enhancing area were ill-defined or irregular or there was associated architectural distortion. Scattered punctate (1–3-mm) foci of enhancement, patchy enhancement of fibroglandular tissue with no architectural distortion, enhancing masses with circumscribed smooth or lobulated borders with or without internal septations, and masses that demonstrated no contrast material enhancement were classified as benign findings. These architectural features and an MR interpretation model incorporating multiple architectural features identified on breast MR images have been previously reported (17,18).
Seven patients underwent MR imaging–guided wire localization. The details of this procedure have been previously described (19).
Twenty of the 22 patients underwent surgery following the MR imaging examination and prior to treatment with chemotherapy: excisional biopsy in nine patients, mastectomy in 10 patients, and excisional biopsy followed by mastectomy in one patient. In each of the patients who underwent surgery, the MR imaging findings were correlated with the histopathologic findings. In two of the 22 patients, surgery was not performed prior to treatment with chemotherapy. Both patients were followed up with sequential MR imaging examinations. One of the two patients subsequently underwent mastectomy following chemotherapy.
For excisional biopsy, including MR-guided wire localization, the specimen and the radiograph of the specimen were delivered to the pathology laboratory. In MR-guided wire localization cases, a radiologic-histopathologic correlation sheet accompanied the specimen to further clarify the relationship between the wire and the region of interest. The specimen was oriented by the surgeon, and the area of interest designated by the radiologist was inked with one color. The specimen was then measured, inked with several colors to correspond to the margins, and sectioned every 2–3 mm. Any lesion or lesions of interest were measured and photographed, and the entire specimen was submitted for histopathologic examination.
In cases in which mastectomy was performed, standard gross examination, including measurements, application of ink, sectioning, and lymph node dissection, was performed. Mastectomy specimens were sectioned every 0.5–1.0 cm, and each section was closely examined and palpated. Sections of tumor and all suspicious areas, with notation of the quadrant, were submitted for examination. In cases where the breast parenchyma was grossly unremarkable, a minimum of 12–15 sections were submitted for histopathologic examination. For all cases, two to three sections from the four quadrants, one section from the deep margin of resection, two sections of nipple, and all lymph nodes were microscopically examined.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In 19 (86%) of the 22 patients, a primary breast cancer was detected on MR images; the cancer was confirmed at excisional biopsy or mastectomy in 17 patients and had resolved on follow-up MR images obtained during chemotherapy in two patients. Of the 19 patients with MR imaging–detected cancers, 17 had cancers that appeared as a focal enhancing mass with spiculated (n = 5) or irregular (n = 12) borders (Figs 1–3). The enhancement pattern was homogeneous in nine patients and peripheral in eight patients. In the 17 patients with focal enhancing lesions, the lesions ranged in size from 5 to 30 mm, with a mean size of 17 mm. In two of the 19 patients, the enhancement was multifocal throughout the breast in one patient and in one quadrant in the second patient (Figs 4, 5). Due to the multifocality of the enhancement, an accurate measurement of tumor size was not possible.
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In two of the 19 women in whom a suspicious lesion was identified on MR images, the lesion had resolved on MR images obtained during chemotherapy. In the first woman, an enhancing, irregular, 1.5-cm mass was identified on MR images. The mass appeared unchanged on follow-up MR images at 3 and 4 months but was no longer identified on follow-up MR images at 7 months (Fig 6). In the second woman, an enhancing, spiculated, 1.5-cm mass was identified at MR imaging. The lesion was not identified on follow-up MR images obtained at 3 months. Mastectomy was performed 7 months following the initial MR imaging, after the completion of chemotherapy, and no tumor was found in the breast.
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In two women, the only enhancing lesion or lesions proved to be false-positive. In the first woman, MR imaging–guided wire localization and excisional biopsy of an irregular 5-mm enhancing lesion revealed fibrocystic changes at histopathologic review. At mastectomy following chemotherapy, no tumor was found within the breast. In the second woman, MR imaging–guided wire localization and excisional biopsy of two irregular enhancing lesions (5 and 7 mm) revealed atypical ductal hyperplasia. Subsequent mastectomy revealed a 2-mm infiltrating ductal carcinoma. The location of the infiltrating carcinoma did not clearly correspond to the location of the MR imaging–detected lesions.
Two women had false-negative findings. In the first woman, two invasive ductal carcinomas were found at mastectomy and measured 17 mm in the lateral part of the breast and 20 mm in the axillary tail. At retrospective review of the MR images, the lateral lesion was not visible, and the axillary tail was not included in the field of view of the examination. The lesion in the second woman was described with the false-positive findings earlier; MR imaging–guided localization and excisional biopsy revealed atypical ductal hyperplasia, and a 2-mm infiltrating ductal carcinoma was found at mastectomy.
Of the 17 patients with a primary breast cancer identified on MR images and confirmed at surgery, 10 underwent mastectomy and seven underwent breast-conservation therapy. Of the two patients with a highly suspicious enhancing lesion that was identified on MR images and that resolved during treatment, one patient subsequently underwent mastectomy, and no tumor was found. The other patient did not undergo a surgical procedure.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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As axillary node presentation of a clinically occult breast cancer is relatively uncommon, there have been very few reports of MR imaging–detected cancers in their clinical setting that we know of (11,15,20–22). In to our knowledge the largest published series to date, Morris et al (15) reported the MR imaging findings in 12 women with biopsy-proved metastatic adenocarcinoma to the axillary lymph nodes. In their series, a primary breast cancer was identified on MR images in nine (75%) of the 12 patients. In eight of the nine patients, cancers were visualized as a focal mass ranging from 9 to 20 mm (mean, 13 mm), and one cancer was visualized as an area of regional enhancement. The histopathologic findings in this series were invasive ductal carcinoma in seven patients, invasive lobular carcinoma in one patient, and ductal carcinoma in situ in one patient.
In our series, a primary breast cancer was detected on MR images in 19 (86%) of 22 patients. The MR imaging findings were similar to those reported by Morris et al. The most common MR imaging finding was that of a focal mass with irregular or spiculated borders, which was identified in 17 of the 19 patients in their study. The size of these lesions was also similar to that found by Morris et al, with a mean of 17 mm. In all 17 patients, the focally enhancing lesions proved to be invasive ductal carcinoma. In the remaining two patients, MR imaging demonstrated multiple enhancing lesions; in both patients, multifocal invasive lobular carcinoma was found at surgery.
The results of our series along with those of Morris et al (15), despite relatively small numbers of patients, suggest that MR imaging can be used to identify a primary breast cancer with high sensitivity in patients with isolated axillary metastases at presentation. However, the detection of a primary breast cancer is valuable clinically only if it will in some way affect patient care. The treatment of patients with isolated axillary metastases at presentation remains controversial. These patients are presumed to harbor an occult carcinoma in the ipsilateral breast (1,3). Review of the literature shows that 55%–100% of patients have an occult breast cancer (6). The traditional treatment of choice for this group of patients is mastectomy and axillary node dissection, which continues to be the most frequent treatment option (1–3). Most studies have shown long-term survival with mastectomy to be at least comparable with that for stage II breast cancer (1,3,5,6,9).
There are now reports demonstrating equivalent survival for patients with axillary node metastases and unknown primary malignancy who undergo breast-conservation therapy with breast irradiation and for those who undergo mastectomy (6–8). However, the recurrence rate in the breast in this population is higher than in the population undergoing breast-conservation therapy with radiation following excisional biopsy of the primary breast cancer (3,7,8). In two series (7,8), the recurrence rates in the breast were 23% and 12%. The failure rate in the breast is consistent with the expected failure rate that is based on the inability to control gross tumor in the breast with standard doses of radiation (3). With the exception of these two series (7,8), there is minimal information about the outcome of treatment with definitive radiation as an alternative to mastectomy (3).
Treatment recommendations for patients with newly diagnosed breast cancer are based on many factors, perhaps the most important being the extent of cancer within the breast. For patients with isolated axillary metastases at presentation, the extent of cancer within the breast is not known. As MR imaging appears to be very sensitive for the detection of an ipsilateral breast cancer in this population, MR imaging in these patients may provide information to help guide treatment planning. While overall survival appears to be similar for patients undergoing breast irradiation and for patients undergoing mastectomy, the detection and staging of an ipsilateral breast cancer provides clinical information that can allow the surgeon, radiation oncologist, and medical oncologist to determine whether breast-conservation therapy is a reasonable treatment option or whether the size and/or histopathologic features suggest a high rate of local recurrence following radiation, which makes mastectomy a better treatment choice.
In our series, the mean histopathologic lesion size was 17 mm, and in six women, the lesion measured less than 10 mm. In only two women was extensive cancer identified on MR images, and both women were proved to have multifocal invasive lobular carcinoma at mastectomy. Of the 17 patients with a primary breast cancer detected on MR images and surgically confirmed, seven (41%) underwent breast-conservation therapy. In these seven women, the information gained from the MR imaging study, namely the detection of a localized cancer on MR images, resulted in a change in clinical management; breast-conservation therapy was offered as an alternative to the traditional recommendation of mastectomy.
When breast cancer is suspected on an imaging study, the ability to offer lumpectomy with the potential for breast-conservation therapy is dependent on the localization of the suspicious lesion. In the setting of MR imaging–detected lesions, the lesion must either be localized with MR imaging guidance or be identified at mammography, US, or physical examination.
In our study, four of the eight excisional biopsies among the 17 patients with histopathologic proof were guided with MR imaging, while the remaining four were guided with mammography, US, or palpation. In our breast center, MR imaging–guided wire localization is readily available (19). Thus, for the lesions that were ultimately localized with MR imaging guidance, an attempt was not made to localize the MR imaging–detected lesion with US. In the series reported on by Morris et al (15), an MR imaging–guided localization system was not available, and the authors were successful at identifying and localizing the MR imaging–detected lesion at US in six of nine patients. Ideally, an MR imaging–guided localization system should be available, as MR imaging–detected lesions may not be visible with US. However, as there is presently no commercially available MR imaging guiding system, directed US examination to the expected location of the MR imaging–detected lesion may allow for lesion identification and biopsy.
Two of the limitations of MR imaging previously reported (11,22), specifically, false-positive enhancement and the inability to document lesion removal following MR imaging–guided wire localization, were also present in this study. In six patients, a false-positive enhancing lesion was identified; in four patients, it occurred along with a true-positive enhancing lesion elsewhere in the breast. In two of these women, atypia was identified. There is, at the present time, no way to determine if a suspicious lesion localized with MR imaging is successfully removed at excisional biopsy unless cancer is found at histopathologic review. An MR imaging–compatible core biopsy system could both obviate a surgical procedure for a false-positive benign enhancing lesion and solve the problem of documenting lesion removal. Such systems are in development.
The clinical importance of a negative MR image in the setting of isolated axillary metastases is not clear. In this series, there were two patients with false-negative findings: one patient with two cancers measuring 17 and 20 mm and one patient with a cancer measuring 2 mm. The patient with the two cancers not identified on MR images was examined early in our study. In this patient, one of the cancers proved to be in the axillary tail, but the axillary tail was not included in the field of view of the MR imaging examination. With the present design of our breast coil, the axillary tail cannot always be compressed between the medial and lateral plates and is thereby excluded from the examination. Further coil development is needed so that the axillary tail can be fully evaluated.
The missed 2-mm cancer is our only recent false-negative case. Whether the axillary metastases in this case were secondary to this tiny cancer is not clear. Our inability to visualize the 2-mm cancer may reflect the ultimate imperfect sensitivity of MR imaging. In our experience, multiple, scattered 2–3-mm enhancing foci are often identified on diagnostic breast MR images both in patients with known breast cancer and in those with no known breast cancer. In patients who undergo subsequent MR imaging examinations, these tiny foci commonly resolve and new foci appear. In the presence of these enhancing foci, it may not always be possible to identify a 2- or 3-mm breast cancer. The negative predictive value of MR imaging remains unknown. Whether a negative MR image can be used to support breast-conservation therapy with breast irradiation as an alternative to mastectomy needs to be determined with additional investigation.
Our results, along with those previously reported, support the use of MR imaging for the evaluation of patients who have axillary node metastases at presentation and negative mammographic and clinical examination findings. In this patient population, MR imaging offers potential not only for the detection of a primary ipsilateral breast cancer but also for staging, which may be used to guide treatment planning. The identification of localized disease may offer some women the option of breast-conservation therapy as an alternative to mastectomy.
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Footnotes |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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