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Breast Imaging |
1 From the Departments of Radiology (S.G.O., E.S.S., M.D.S.) and Surgery (B.J.C.), the Hospital of the University of Pennsylvania, 3400 Spruce St, Philadelphia, PA 19104; the Radiology Regional Center, Fort Myers, Fla (C.S.D.); and the Mayo Clinic, Division of Anatomic Pathology, Rochester, Minn (C.R.). From the 1998 RSNA scientific assembly. Received July 21, 1999; revision requested September 24; revision received October 29; accepted November 2. Address correspondence 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 February 1992 and December 1998, 23 patients with nipple discharge underwent contrast material–enhanced MR imaging at 1.5 T. Mammographic findings were negative in 22 of 23 patients and revealed asymmetry in one patient. Galactography was attempted in two patients, with negative findings in one patient and no success in the other. Fifteen of 23 patients underwent excisional biopsy—seven of 15 with MR imaging–guided localization, and one of 15 with mammographic localization. Eight of 23 patients were followed up clinically (range, 7–24 months; mean, 20 months).
RESULTS: In 11 of the 15 (73%) patients who underwent excisional biopsy, MR imaging findings correlated with histopathologic findings. MR imaging demonstrated four of six benign papillomas and one of two fibroadenomas as circumscribed, enhancing subareolar masses. Findings of one MR imaging examination were negative, and benign tissue was found at excisional biopsy. MR imaging findings were suspicious in six of the seven patients with excisional biopsy findings of malignancy (regional enhancement [n = 2], ductal enhancement [n = 2], peripherally enhancing mass [n = 1], and spiculated mass [n = 1]). In one of the seven patients, a benign-appearing intraductal mass was identified at MR imaging; excisional biopsy revealed a benign papilloma with an adjacent focus of DCIS.
CONCLUSION: MR imaging can help identify both benign and malignant causes of nipple discharge. It potentially offers a noninvasive alternative to galactography.
Index terms: Breast, abnormalities, 00.311, 00.312, 00.324, 00.71 • Breast, biopsy, 00.1261 • Breast, MR, 00.121412, 00.121415, 00.12143 • Breast neoplasms, MR, 00.311, 00.312, 00.324, 00.71
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The diagnostic imaging examination of patients with nipple discharge has included mammography, galactography, and, more recently, ultrasonography (US). We describe our experience with 23 patients with nipple discharge who underwent contrast material–enhanced magnetic resonance (MR) imaging of the breast. MR imaging has demonstrated the potential for increased sensitivity for cancer detection when compared with mammography and US. We sought to investigate the potential of MR imaging in patients with nipple discharge.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Five of the 23 patients underwent MR imaging as part of a research protocol for evaluating MR imaging in patients with an abnormal mammographic or clinical finding prior to excisional biopsy. Each of these five patients signed an internal review board–approved informed consent form. The remaining 18 patients underwent MR imaging during the routine clinical MR imaging schedule. They were not part of a research protocol.
All 23 patients underwent mammography prior to MR imaging. In 22 of 23 patients, mammographic results were negative (Breast Imaging Reporting and Data System [BI-RADS] [7] category 1 [n =16] or 2 [n = 6]). In one patient, mammography revealed an area of asymmetric increased density; because of the patient's history of bloody nipple discharge, this finding was reported as suspicious (BI-RADS category 4).
Four of 23 patients underwent US examination; two patients had negative findings, one had dilated subareolar ducts, and one had cysts.
Galactography was attempted in two of the 23 patients; one patient had an unsuccessful examination and the other had negative findings.
The nipple discharge was bloody in 15 patients, clear in five patients, and yellow in three patients. Cytologic evaluation of the nipple discharge was performed in five patients and revealed benign cells in four and adenocarcinoma in one. None of the patients had a palpable abnormality.
MR imaging was performed at 1.5 T (Signa; GE Medical Systems, Milwaukee, Wis). The available hardware and software evolved with time from a 5x system to a hybrid, premarket Echo-speed system (GE Medical Systems, Milwaukee, Wis) run at high speed to a standard, commercially available Echo-speed system. The software evolved from a 4.8 operating system to a 5.8 operating system. During this time, the imaging time after contrast material enhancement decreased from 3 minutes 30 seconds to 90 seconds (from three-dimensional, fast spoiled gradient-echo imaging to contrast-enhanced three-dimensional, fast spoiled gradient-echo imaging). At the time this article was written, the operating system did not differ from that which is available commercially.
Although the technique used to image the breast evolved over the 7-year period of the study, all examinations were performed with a home-built prototype phased-array multicoil, with the patient imaged in a prone position with the breast compressed gently between medial and lateral plates. The details of this coil have been described previously (8).
All examinations included sagittal, T1-weighted, spin-echo (repetition time msec/echo time msec [500/14]); T2-weighted, fat-suppressed, fast spin-echo (4,000/120); and T1-weighted, fat-suppressed, spoiled gradient-echo sequences before and after contrast material injection. The contrast-enhanced sequence was a three-dimensional, dynamic, fat-suppressed, fast spoiled gradient-echo sequence (minimum repetition time msec/minimum echo time msec; flip angle, 30°–90°; 28 sections obtained in a minimum of 1 minute 27 seconds and in a maximum of 2 minutes 52 seconds; a small field of view [160–180 mm]; large matrix [512 x 256]; and thin sections [2–3 mm, with no intersection gap]). In most patients, fat suppression was obtained by using a spectrally fat-selective inversion pulse. Contrast material (0.1 mmol per kilogram of body weight gadopentetate dimeglumine [Magnevist; Berlex, Wayne, NJ]) was injected intravenously over approximately 10 seconds and was followed by a normal saline flush; image acquisition was initiated immediately.
The MR images were read prospectively by a radiologist experienced in MR imaging of the breast (including S.G.O., M.D.S., and E.S.S.), and only the prospective readings were used for this study. The MR images—specifically, the fat-suppressed, spoiled gradient-echo, precontrast images—were assessed retrospectively (S.G.O.) for characterization of the contents of the ductal fluid. Ductal fluid was considered to be hemorrhagic or proteinaceous if it had higher signal intensity than the surrounding breast parenchyma on T1-weighted images. The images were read with knowledge of the clinical history of nipple discharge. The focal enhancement of the breast lesions was assessed qualitatively relative to the signal intensity of background glandular tissue on the first postcontrast images obtained at 3 minutes 30 seconds or at 90 seconds.
A lesion was considered suspicious for malignancy if it enhanced after contrast material administration and if it had at least partially irregular or ill-defined borders, had peripheral enhancement, or had linear or branching enhancement that was suggestive of ductal enhancement. Focal regional enhancement also was considered suspicious.
An enhancing lesion was considered likely to be benign if it had circumscribed borders or if it demonstrated minimal contrast material enhancement. Scattered punctate (1–3-mm) foci of enhancement or patchy diffuse enhancement of fibroglandular tissue with no architectural distortion were considered benign findings. These image interpretation criteria have been described previously (9,10). Since in our research experience with MR imaging of the breast we have not found the quantitative assessment of contrast material enhancement (ie, enhancement kinetic measurements such as rate and amplitude) to be useful in accurately discriminating benign from malignant lesions, we did not use enhancement kinetics for image interpretation (9).
Fifteen of the 23 patients underwent excisional biopsy after MR imaging. Seven of the 15 patients underwent preoperative MR imaging–guided localization. The details of this procedure have been described previously (11). One patient underwent preoperative mammographically guided wire localization of an area of asymmetry. Eight of the 23 patients were followed up clinically with subsequent physical examination and/or mammography and without surgical intervention (range of follow-up, 7–24 months; mean, 20 months).
In the pathology department, all breast specimens were marked with india ink. In cases where the lesion was localized with MR imaging guidance or with mammographic guidance, the area of concern was marked with a different color of india ink in contrast with the remainder of the specimen. A diagram delineating the relationship of the lesion to the hookwire (MR imaging–guided localization) or the mammogram of the specimen (mammographically guided localization) accompanied all specimens to the pathology department. In cases in which a nipple duct was dissected by the surgeon, a suture marked the distal duct end. The duct, usually dilated, was opened along its long axis and was examined grossly for any visible lesions. In all cases, the specimen was sectioned every 2–3 mm and was submitted in its entirety for microscopic examination.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Of the seven patients with malignant lesions, two had ductal carcinoma in situ (DCIS) with microinvasion (the DCIS was 12 mm in the first patient and was not measurable because of diffuse disease in the second patient), two had invasive ductal carcinoma with DCIS (15 and 7 mm), one had extensive DCIS that was not measurable because of diffuse disease, and one had DCIS that involved a 7-mm papilloma. In the patient in whom both benign and malignant lesions were identified, an incidental focus of DCIS was identified adjacent to a benign, 15-mm papilloma. In this patient, no residual DCIS was found at repeat excisional biopsy.
In 11 (73%) of the 15 cases with surgical confirmation, the MR imaging findings correlated with the histopathologic findings. MR imaging prospectively demonstrated four of the six benign papillomas found at excisional biopsy. In each case, a circumscribed subareolar mass with variable enhancement within a fluid-filled duct was identified. The enhancement ranged from minimal and patchy to marked and homogeneous. The masses were 4–15 mm (mean, 8 mm). The two papillomas not identified at MR imaging measured 5 and 7 mm. In one of these two cases, a high-signal-intensity, fluid-filled duct that may have obscured the papilloma was identified on both the pre- and postcontrast images. There was no clear explanation for the second missed papilloma. In all six, fluid-filled ducts were identified. In two cases, the fluid had high signal intensity on T1-weighted images, which suggested hemorrhage or proteinaceous content. In the other four cases, despite patient histories of bloody nipple discharge, the fluid had low signal intensity on T1-weighted images.
MR imaging demonstrated one of two fibroadenomas found at excisional biopsy. In this case, a 10-mm, circumscribed, lobulated, homogeneously enhancing mass in the subareolar breast was identified. The mass had a benign appearance but had no MR imaging features—that is, internal septations—that allowed for a prospective diagnosis of fibroadenoma. In the other case, enhancing subareolar ducts were identified that raised the possibility of DCIS, but MR imaging-guided localization and excisional biopsy revealed a 7-mm fibroadenoma. In each case, at histologic review, the fibroadenoma was not associated clearly with an abnormal duct and therefore was believed to be an incidental finding.
In the final benign case, MR images were interpreted as normal, and no focal lesion was found at excisional biopsy.
In six of seven patients in whom excisional biopsy revealed DCIS and/or invasive carcinoma, MR imaging demonstrated a suspicious enhancing lesion. In four of the six patients, needle localization was performed with MR imaging guidance. In the two patients in whom DCIS with microinvasion was found at excisional biopsy, MR imaging revealed focal, regional enhancement. In both patients, fluid-filled ducts extending to the enhancing area were identified (Fig 1). Despite a history of bloody nipple discharge in both patients, the fluid had high signal intensity in the first patient and had low signal intensity in the second patient on T1-weighted images.
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The one false-negative malignancy was a single focus of DCIS identified near the margin of a surgical specimen that contained a benign, 15-mm papilloma. In this case, MR imaging revealed a minimally enhancing, circumscribed, 15-mm, subareolar mass that was consistent with benign papilloma within a dilated, low-signal-intensity, fluid-filled duct.
Eight patients did not undergo a surgical procedure. In all eight patients, MR images were interpreted as normal. At the time this article was written, the patients had been followed up for 7–24 months (mean, 20 months). Five of the eight patients underwent follow-up mammography; three had negative findings at 24 months, and two had negative findings at 18 months. Of these five patients, three noted no further nipple discharge, and one noted a decrease in the discharge. The remaining three patients (ages 24, 27, and 42 years) did not undergo mammographic follow-up. All three patients noted no further nipple discharge at 7, 17, and 23 months.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Investigators in most reported series of which we are aware have evaluated MR imaging either as a method to differentiate benign from malignant lesions detected initially at physical examination or at mammography or as a method to stage suspected or known breast cancer (21,22). On the basis of the promising results of these studies, it has been suggested that MR imaging can be used as an adjunctive imaging tool in a capacity similar to that of breast US for the further examination of patients with an equivocal mammographic or palpable abnormality (21,22).
While there is a growing body of evidence that MR imaging can be used to detect underlying mammographically and clinically occult invasive breast cancer, relatively little is known about the potential of MR imaging for detecting mammographically and clinically occult intraductal disease, either DCIS or a benign abnormality—specifically, intraductal papilloma. There are several reported cases of MR imaging–detected, mammographically and clinically occult DCIS (18,19). On the basis of this experience, it appears that MR imaging, in addition to being highly sensitive for the detection of invasive breast cancer, has the potential for being highly sensitive for the detection of intraductal disease and thus might be useful for the examination of patients with nipple discharge.
Nipple discharge, while usually benign in origin, raises concern in both patients and clinicians because of the possibility of an underlying malignancy as the cause (1). The imaging examination of patients with clinically important nipple discharge—spontaneous, unilateral discharge in which the fluid is bloody, serous, or clear—historically has included mammography and galactography. In the clinical setting of nipple discharge, mammographic findings have been reported to be positive in 50%–90% of patients with malignancy and in less than 50% of patients with a benign papilloma (2,3). In our study, mammographic findings were abnormal in only one (4%) of 23 patients. In this patient, an asymmetric area was identified that proved to be DCIS at needle localization and at excisional biopsy.
Galactography, in which contrast material is injected into the draining duct system, has been advocated as a method for lesion identification in patients with nipple discharge (2,5,23–27). It has been suggested that galactography can be used to locate the lesion, which allows for more conservative surgical excision (24). In addition, preoperative galactography may increase the likelihood that a specific disease will be found at surgery (23). The utility of galactography, however, remains controversial. Many surgeons prefer to dissect the draining duct without preoperative galactography, while other surgeons use the galactogram as a "road map" to guide them to the lesion (1).
There also are limitations to galactography. While one or more intraductal filling defects may be identified, it usually is not possible to differentiate between carcinoma and papilloma at galactography (1). In addition, the discharge must be present on the day of galactography so that a cannula may be placed in the appropriate duct. This may not be possible in patients who complain of intermittent discharge that cannot be induced at galactography. Even when the discharge can be induced, cannula placement in the duct or injection of the contrast material beyond an obstructing lesion is not always successful.
Limitations of both mammography and galactography have spurred investigation into other potential adjunctive imaging examinations, which include US and MR imaging. The utility of breast US in the clinical setting of nipple discharge remains unclear. US-guided galactography as an alternative technique when conventional galactography is unsuccessful has been reported (28). US-guided fine-needle aspiration after galactography also has been described (29).
In the Hospital of the University of Pennsylvania's Breast Imaging Center, US is not incorporated routinely into the examination of patients who present with nipple discharge. In the present study, US was performed in only four of 23 patients. In two of these patients, abnormalities were identified: cysts in one patient and dilated subareolar ducts in one patient. In the patient with dilated ducts, subsequent MR imaging revealed an enhancing subareolar mass that was found to be a papilloma at excisional biopsy. Further investigation of breast US is needed to determine whether this imaging modality can play a clinically valuable role in the work-up of patients with nipple discharge.
To our knowledge, there has been very little published experience with MR imaging examination of patients with nipple discharge (30,31). Yoshimoto et al (30) reported on a single case of MR imaging-depicted, enhancing ducts that corresponded to areas of DCIS and microinvasion. In this case, contrast material was injected both intravenously and into the discharging duct.
Rovno et al (31), from the Hospital of the University of Pennsylvania, reported on the results of a retrospective review of the medical records of patients who underwent breast MR imaging and who subsequently underwent excisional biopsy, at which a papilloma was identified. In seven of seven patients with histories of spontaneous nipple discharge in whom papillomas were found at excisional biopsy, at retrospective review of the MR images, an enhancing, circumscribed, smooth or lobulated mass could be identified. Six of these seven patients were included in our study. In two of these six patients, the papillomas (5 and 7 mm) identified at retrospective review were not identified at the prospective reading. Possible reasons for the false-negative prospective readings in these patients are not clear but may have been the small size of the lesions, a high-signal-intensity duct potentially obscuring the lesion in one patient, or a learning curve in image interpretation. Rovno et al (31) also reported that in 16 patients in whom a papilloma was found at excisional biopsy in the absence of a history of nipple discharge, MR imaging did not demonstrate the papilloma at either prospective or retrospective review.
In our series of 23 patients who underwent MR imaging for the evaluation of nipple discharge, MR imaging demonstrated an abnormality in 12 (52%), and the MR imaging findings correlated with the histopathologic findings in 11 (73%) of the 15 patients who underwent excisional biopsy. In five of the 11 patients with abnormal MR images, a benign-appearing, circumscribed, enhancing subareolar mass was identified. At histologic examination, four had benign papillomas, and one had a fibroadenoma. Each papilloma was identified as an enhancing, circumscribed mass within a fluid-filled duct. Enhancement ranged from minimal and patchy to marked and homogeneous. The single fibroadenoma was visualized as a homogeneously enhancing, circumscribed, lobulated mass not associated with fluid-filled ducts. Of the eight patients with benign lesions (six with papillomas and two with fibroadenomas) identified at histologic examination, five (63%) had lesions that were detected prospectively at MR imaging.
In each of the remaining six patients with abnormal MR images, an enhancing lesion with MR imaging features suspicious for malignancy was identified. These features included regional enhancement in two patients, linear enhancement in two patients, a peripherally enhancing mass in one patient, and a spiculated mass in one patient. All six ([26%] of 23) patients were found to have a malignant lesion at excisional biopsy: DCIS in two patients, DCIS with microinvasion in two patients, and invasive ductal carcinoma with DCIS in two patients.
Of the seven ([30%] of 23) malignant lesions found at excisional biopsy, six (86%) were detected prospectively at MR imaging. The only patient who had false-negative findings of malignancy at MR imaging had an incidental single focus of DCIS that was identified at the margin of resection of an excisional biopsy specimen that contained a 15-mm papilloma. The papilloma was identified at MR imaging. In this patient, no residual DCIS was found at repeat excisional biopsy. Only one (14%) of the seven malignant lesions was detected at mammography.
The percentage of patients with a malignant lesion in this study was higher than would be expected on the basis of the results of previous clinical and imaging examinations in patients with nipple discharge (1–6). This high rate of malignancy probably reflects a bias in patient referral for breast MR imaging. Eighteen of the 23 patients underwent MR imaging examinations as part of the routine clinical MR imaging schedule, not as part of a research protocol. In the five patients who underwent MR imaging as part of a research protocol, the entrance criterion was a suspicious mammographic or clinical abnormality for which excisional biopsy was planned. Referral for MR imaging was at the discretion of the patient's clinician and was, therefore, not random. However, only one of the seven patients with a malignant lesion had positive cytologic examination findings of the discharge. None of the remaining six patients had clinical or conventional imaging findings that suggested a malignant cause of the nipple discharge.
In addition to a potential patient selection bias, this study had other limitations. First, the number of patients who underwent excisional biopsy was small. Only one of nine patients with negative MR imaging findings underwent subsequent excisional biopsy. In this patient, benign breast tissue was found. Because patients with negative MR imaging findings may have been less likely to undergo excisional biopsy, the sensitivity of MR imaging was not known.
Second, the clinical follow-up in those patients who did not undergo a surgical procedure was limited, with a mean follow-up of 20 months. Optimal follow-up, whether mammographic or clinical, should be at least 2 years to establish the actual false-negative rate of the imaging examination (32). However, five of the eight patients who were followed up clinically underwent at least one subsequent mammographic examination, with negative findings, and seven of the eight patients reported resolution of or a decrease in the nipple discharge.
Another limitation of our study was its retrospective design, with a virtual lack of correlative imaging—in particular, galactography. In our study population, galactography was attempted in only two of 23 patients and was successful in only one patient. In this patient, galactographic results were negative, as were those of subsequent MR imaging. This patient did not undergo excisional biopsy. In the absence of galactograms in those patients with positive MR imaging results, we could not compare the results of MR imaging with those of galactography. The uncommon use of galactography in this series mostly likely was due to the referral patterns of the breast surgeons at the Hospital of the University of Pennsylvania who, historically, do not incorporate galactography routinely into their evaluation of patients with nipple discharge. Nevertheless, we continue to recommend galactography as the initial study of choice after mammographic results are negative in patients with nipple discharge.
There was an additional limitation of this study that was not in the study design but rather was in the ability to transfer MR imaging technology from a research center to clinical practice. While the technique for breast MR imaging evolved during the 7-year period in which these examinations were performed, most of the examinations were performed with a system that is now commercially available. However, there are two components of our breast MR imaging program that are not yet widely commercially available, namely, the breast coil—a multicoil compression array—and the MR imaging-guided biopsy and localization system. The advantages of the prototypic breast coil we used, including shorter imaging times, improved signal-to-noise ratio, and increased spatial resolution, have been reported on previously (8).
The MR imaging–guided biopsy and localization system is a critical component of the Hospital of the University of Pennsylvania's breast MR imaging program (11,18,20–22). While MR imaging-detected lesions potentially may be visualized with US, this will not always be the case; thus, an accurate method to localize and/or perform biopsy on a lesion that is detected only with MR imaging guidance is needed. Such systems have not, until now, been available commercially. However, MR imaging–guided localization and biopsy systems remain in development and are now becoming available commercially.
The results of this preliminary investigation of MR imaging in patients with nipple discharge suggest that MR imaging can be used as an adjunctive imaging modality for the identification of mammographically occult benign or malignant breast abnormalities. While MR imaging currently is less readily available and is more costly than galactography, it offers the potential for both increased sensitivity for the detection of intraductal and invasive carcinoma and increased specificity for the differentiation of benign from malignant causes. A prospective study comparing galactography, US, and MR imaging is needed to determine whether MR imaging can supply clinically valuable information that cannot be obtained with conventional imaging methods in patients with nipple discharge.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, S.G.O.; study concepts, S.G.O., M.D.S.; study design, S.G.O.; definition of intellectual content, S.G.O.; literature research, S.G.O., C.S.D.; clinical studies, B.J.C., S.G.O., M.D.S., E.S.S.; data acquisition, S.G.O., M.D.S., E.S.S.; data analysis, S.G.O., C.R.; manuscript preparation, S.G.O., E.S.S., C.R.; manuscript editing and review, B.J.C., S.G.O., E.S.S., C.R.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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