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1
Department of Radiology, Dr. Daniel den Hoed Cancer Center, University
Hospital Rotterdam, Groene Hilledijk 301, 3075 EA Rotterdam, the
Netherlands.
2
Department of Surgery, Dr. Daniel den Hoed Cancer Center, University Hospital
Rotterdam, 3075 EA Rotterdam, the Netherlands.
Received July 23, 1999;
accepted after revision September 20, 1999.
Address correspondence to I.-M. A. Obdeijn.
Abstract
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SUBJECTS AND METHODS. Thirty-one women with metastatic adenocarcinoma in their axillary lymph nodes originating from an unknown primary site underwent MR imaging of the breast because physical examination and mammography findings were normal. Twenty of the 31 women had no history of malignancy, 10 had been previously treated for contralateral breast cancer, and one patient had nodal metastases in the contralateral axilla at the time breast cancer was detected. When a contrast-enhancing lesion was revealed on MR imaging of the breast, sonography and fine-needle aspiration cytology were also performed.
RESULTS. MR imaging revealed the primary breast cancer in eight (40%) of the 20 patients without a history of malignancy. MR imaging of the breast revealed a second primary cancer in three (27%) of the 11 patients with previous or simultaneous breast cancer. All lesions were identified with sonography and verified by cytology and histology.
CONCLUSION. In women with axillary lymph node metastases from adenocarcinoma, MR imaging of the breast should be added to clinical examination and mammography before defining the breast cancer as occult. The combined approach of MR imaging, sonography, and aspiration fine-needle cytology is a good alternative to the MR imaging—guided biopsy.
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A potential source of metastatic adenocarcinoma in axillary lymph nodes is a previously treated carcinoma of the contralateral breast; however, patients with a previous history of breast cancer also have a significantly higher risk (as much as 2-6 times) of developing a second primary cancer in the other breast. In these patients, knowing whether the lymph node cancer metastasis originated from the first malignancy or from a second primary cancer in the other breast is important [5, 6].
Several groups of investigators have shown that MR imaging can reveal a mammographically and clinically occult breast cancer [7,8,9,10,11,12,13]; however, in each study, the number of patients was small. Morris et al. [11] found the occult malignancy with MR imaging in nine of 12 patients presenting with axillary metastases of an unknown primary cancer. Beatty et al. [12] found the occult breast cancer in 15 of 20 patients presenting with axillary nodal metastases. Davis et al. [9] also found occult breast cancer and performed wire localization using MR imaging. Identification of an otherwise occult malignancy with MR imaging leads to optimal therapeutic decisions and dispels the patient's uncertainty.
The aim of our study was to evaluate the combined role of MR imaging, sonography, and cytology in patients with axillary metastases as clinical evidence of a possible occult breast cancer and in patients with previous or simultaneous breast cancer and contralateral axillary nodal metastases. MR imaging combined with sonographically guided biopsy was investigated as an alternative to MR imaging-guided biopsy, which is a more extensive, less cost-effective, and less available method.
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In this study, the histopathologic findings of all axillary masses were lymph nodes containing metastases from an adenocarcinoma, possibly originating from a primary breast cancer. Pathology of the lymph nodes was evaluated by fine-needle aspiration cytology (three patients) or by histologic examination of the surgically excised lymph node (28 patients). In 25 of these 28 patients, a histologic examination was performed instead of an axillary lymph node dissection.
Twenty patients had no history of malignancy. In the 10 patients with a history of contralateral breast cancer, the metastatic lymph node became evident after a period of 3-17 years. Another patient had lymph node metastasis in the contralateral axilla at the time breast cancer was detected.
MR imaging of the breast was performed in the patients with no history of malignancy because clinical examination and mammographic findings were interpreted as negative. In patients with previous or simultaneous contralateral breast cancer, MR imaging of the breast was performed to exclude or detect a second primary cancer.
Sixteen patients were referred to us from other hospitals for MR imaging of the breast. Physical examination and mammography were performed at those hospitals. We reviewed the mammograms at the time of the MR imaging. In our hospital, mammography was performed on a Senographe 600T unit (General Electric Medical Systems, Milwaukee, WI) with a Kodak film-screen combination (Eastman Kodak, Rochester, NY). Standard oblique and craniocaudal projections were obtained with additional magnification views when necessary. The mammography of 15 patients revealed dense mammographic fibroglandular tissue; 16 patients had mild to moderate fibroglandular breasts.
All patients underwent MR imaging of the breast at our institution, performed with a 1.5-T MR imaging system (Vision; Siemens, Erlangen, Germany). Before scanning, venous access was established in a cubital vein through which a bolus of contrast material, consisting of 20 ml of gadopentate dimeglumine (Magnevist; Schering, Berlin, Germany) was administered during the examination. The women lay prone with the breasts suspended in a double breast surface coil.
After an initial localizer, a fat-suppressed short tau inversion recovery (STIR) T2 turbo spin-echo sequence was performed with the following scan parameters: field of view, 350 x 350 mm; contiguous axial slice, 5-mm thickness; matrix size, 256 x 256; TR/TE, 9128/60 msec; scan time, 3 min 11 sec; acquisitions, one; inversion time delay, 150 msec; echo-train length, 11; and flip angle, 180°. Next, gradient-echo T1-weighted imaging was performed, initially with a two-dimensional fast low-angle shot (FLASH) sequence (15 patients). Since January 1997, a three-dimensional FLASH sequence (16 patients) has been performed before and 1, 3, and 5 min after contrast administration. The two-dimensional scan parameters were field of view, 320 x 320 mm; axial slice, 4-mm thickness; matrix size, 256 x 256; TR/TE, 290/5; scan time, 1 min; acquisitions, one; and flip angle, 90°. The three-dimensional scan parameters were field of view, 160 x 320 mm; coronal slice acquisition effective slice, 1.5-mm thickness; and reformatted axial slice, 4-mm thickness; matrix size, 256 x 256; TR/TE, 8.1/4; scan time, 1 min 26 sec; acquisitions, one; and flip angle, 20°. Subtraction images were obtained with the use of a software subtraction function.
The breast MR images were interpreted by consensus of two radiologists who were aware of the clinical history and mammographic information. Any regional or focal contrast enhancement in the breast was considered abnormal and possibly malignant. Regional enhancement was defined as an area of enhancement without discrete borders. The border characteristics of focal enhancing lesions were examined. Ill-defined, irregular, or spiculated borders and peripheral enhancement were considered suggestive of malignancy. MR imaging was followed by sonography when regional or focal enhancement was seen and by fine-needle aspiration cytology when a lesion was identified. The biopsy technique used was similar to that described by Fornage [14]. For sonography of the breast, a 128XP/(ART) unit (Acuson, Mountain View, CA) with a 7.5-MHz linear array transducer was used. Three patients underwent sonography before MR imaging. In patients with negative MR imaging findings, the follow-up period was 12-53 months (mean, 25 months).
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In total, MR imaging revealed breast cancer in 11 (36%) of the 31 patients. In these patients, MR imaging showed 11 enhancing lesions in nine patients (two patients each had two lesions) and two enhancing areas in two patients. These patients underwent subsequent MR imaging—guided sonography. All 13 lesions were identified on sonography so that fine-needle aspiration cytology could be performed. Malignancy was proven in all patients. In three patients, no lesions were found on sonography before MR imaging; however, lesions were seen on subsequent MR imaging-guided sonography. If breast conservation therapy was preferred by the patient, lumpectomy was performed after sonographic localization, depending on the histologic findings.
Infiltrating ductal carcinoma was diagnosed in nine patients; infiltrating lobular carcinoma was found in two patients. In four patients, the malignancy was multifocal or diffusely growing. The range in size of the lesions was 6-50 mm (mean, 16 mm).
After initial retrospective mammographic evaluation, malignancy was identifiable as a nonsuspicious density in one patient and as a small cluster of microcalcifications in another. In the two patients with a large infiltrating lobular carcinoma (diameter, 50 mm), the tumor was vaguely palpable after MR imaging identification. Of the 20 patients with negative MR imaging findings, further clinical workup (physical examinations and CT) revealed a bronchogenic adenocarcinoma in three patients and a melanoma in one patient. On follow-up, breast cancer manifested as a palpable lesion (10 mm) in only one patient, 8 months after the MR imaging. In a retrospective analysis, the MR imaging findings of this patient were interpreted as negative.
In the remaining 15 patients with negative MR imaging findings, no malignancy became evident during the follow-up period. Thirteen of these patients were treated with axillary lymph node dissection, 12 of 15 patients received hormonal therapy or chemotherapy, and eight of 15 patients received radiation therapy. A mastectomy was performed in one patient and the mastectomy specimen showed no malignancy.
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In the past, the standard therapy for these occult primary cancers, staged as TX N1 M0 (stage II), has been mastectomy and axillary lymph node dissection, with or without radiation therapy; however, the patient survival rate is not improved with mastectomy [16, 17] and the prognosis in this stage is determined by the number of nodes involved and the biologic behavior. When the primary tumor in the breast can be detected, it is possible to choose optimal local treatment. The detection of a second primary cancer in patients previously treated for contralateral breast cancer determines the prognosis and offers the opportunity for optimal local treatment in this patient group as well.
MR imaging of the breast is the examination with the highest sensitivity for the detection of invasive breast cancer (91-95%) [18,19,20,21]; therefore, MR imaging of the breast is advocated to identify otherwise occult cancers in patients with or without a history of breast cancer. In the future, when MR imaging can detect occult primary cancers, breast-sparing approaches to treatment will be more often considered for these otherwise occult malignancies. In addition, when a tumor is detected on MR imaging in patients undergoing neoadjuvant chemotherapy rather than surgery as first-line treatment, tumor response can be monitored with follow-up MR imaging.
Although MR imaging of the breast has a high sensitivity, specificity is low and variable (37-86%) [18,19,20,21]. Signal-intensity curves of benign and malignant lesions often show a considerable overlap because strong contrast enhancement is seen not only in carcinomas but also in nonmalignant lesions and even in normal breast parenchyma [22,23,24]. In our institution, every enhancing lesion or region on MR imaging is considered possibly malignant and followed up with sonography to perform fine-needle aspiration cytology. The combination of MR imaging and cytology [25] provides a high sensitivity as well as a high specificity. In 11 (36%) of 31 patients, the occult carcinoma could be seen with MR imaging. All these lesions were identified with MR imaging—guided sonography, and malignancy was confirmed with subsequent fine-needle aspiration cytology. Some patients had already undergone sonography of the breast with negative findings before the MR imaging examination. With previous MR images for reference, the sonographer knows where to look for the lesions and consequently will find small carcinomas and carcinomas with less typical malignant features, confirming that sonography is most useful when performed on targeted areas [26, 27] (Fig. 2A,2B,2C,2D,2E,2F). One can start the search for an occult breast carcinoma with a less expensive sonographic screening, especially when MR imaging is not available; however, we agree with Jackson et al. [26] that sonography alone should not be used to examine breasts because, as a screening technique, sonography has unacceptably high false-positive and false-negative rates.
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Regional or focal contrast enhancement on MR imaging often represents benign breast tissue [24], but sonography would not reveal a lesion when screening this benign tissue. In our selected patient population, every lesion apparent on MR imaging could be identified and characterized with the combination of sonography and fine-needle aspiration cytology (e.g., no false-positive MR imaging findings). This substantially reduces the need for time- and cost-consuming MR imaging—guided biopsies in this particular patient category; however, not every enhancing lesion on MR imaging will be detected with sonography, partly because enhancing lesions do not represent pathology and partly because not all solid lesions are shown with sonography. Therefore, we advise referring the few patients with an unknown primary tumor and a suspicious lesion on MR imaging that cannot be identified on sonography to a center with MR imaging—guided sonography.
Detection of the malignancy determines the treatment policy. A lumpectomy, followed by irradiation, was performed (after sonographically guided localization) in five patients. Mastectomy was performed on three patients with multifocal malignancy. Three other patients underwent induction chemotherapy.
The MR imaging findings proved to be false-negative in one patient; a primary cancer with an origin other than the breast was found in four patients. In the remaining 15 patients, MR imaging of the breast did not depict a malignant lesion and no breast cancer or other primary cancer was found during follow-up. The occult primary breast carcinoma in patients presenting with axillary metastases is often very small [4, 28, 29] or not found; careful histologic examination of mastectomy specimens fails to show the carcinoma in 30-40% [30,31,32].
Compared with previously published studies, the MR imaging detection rate (67-86%) [8, 11,12,13] of mammographically and clinically occult tumors is low in this study; however, this study has a different patient population. First, in a cancer center, a higher percentage of patients present with metastatic tumor in the axillary lymph nodes as a symptom of an unknown primary cancer (of another origin). Secondly, a significant part of the studied patient group was known to have contralateral breast cancer. If no second primary breast cancer is found in the other breast on MR imaging, it is plausible that the metastatic tumor in the axillary lymph node is a metastasis of the previously discovered tumor; therefore, MR imaging detects fewer primary breast cancers in this patient population with previously detected cancer.
In our study, the T1-weighted sequences were performed with 4-mm-thick slices. This theoretically implies that very small lesions of 1- to 2-mm diameters can be missed; thus, the current MR imaging techniques have a limited detection capacity. In this study, follow-up showed one patient in whom such a small lesion was missed; however, the lesion size at the time of MR imaging remains unknown.
In four of 20 patients not known to have malignancy, an adenocarcinoma with an origin other than the breast was the cause of the axillary metastases. In three patients, a bronchogenic carcinoma was found, which indicates that workup should include a CT examination of the thorax.
In conclusion, in women with axillary lymph node metastases consistent with breast cancer, MR imaging of the breast should be added to clinical examination and mammography before defining the malignancy as an occult primary cancer. In this study, MR imaging detected an occult breast carcinoma in 40% of the patients without a history of breast cancer. MR imaging of the breast is also advocated in women with a previous or simultaneous breast cancer presenting with contralateral lymph node metastases to more reliably detect or exclude a second primary cancer. A second primary cancer was found in 27% of these patients. Only one of 20 patients with negative MR imaging findings showed breast cancer on clinical follow-up after 8 months.
In this study, all MR imaging lesions could be identified on sonography and therefore MR imaging—guided sonography followed by fine-needle aspiration cytology offered an excellent alternative to MR imaging—guided biopsy.
Identification of an otherwise occult breast cancer with MR imaging eliminates uncertainty about the primary site of the cancer and offers the opportunity for optimal treatment.
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