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MR Imaging of the Breast in Patients with Invasive Lobular Carcinoma

¹ Department of Radiology, The University of Pennsylvania Medical Center, 1 Silverstein Bldg., 3400 Spruce St., Philadelphia, PA 19104.
² University Radiology Group, Robert Wood Johnson University Hospital, 800 Ryders La., East Brunswick, NJ 08816.
³ Department of Pathology, The University of Pennsylvania Medical Center, Philadelphia, PA 19104.
⁴ Present address: Department of Anatomic Pathology, Mayo Clinic, 200 First St., S.W., Rochester, MN 55905.
⁵ Department of Surgery, Division of Surgical Oncology, The University of Pennsylvania Medical Center, Philadelphia, PA 19104.
⁶ Department of Radiation Oncology, The University of Pennsylvania Medical Center, Philadelphia, PA 19104.

Received April 25, 2000; accepted after revision July 7, 2000.

 
Presented at the annual meeting of the American Roentgen Ray Society, New Orleans, May 1999.

Supported in part by National Institutes of Health grant R01CA81047-01.

Address correspondence to S.P. Weinstein.

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. Our objective was to assess the usefulness of MR imaging in patients diagnosed with invasive lobular carcinoma of the breast.

MATERIALS AND METHODS. Between July 1993 and September 1999, 32 women (33 cases) diagnosed with pure invasive lobular carcinoma of the breast underwent contrast-enhanced MR imaging examination. One woman was excluded because of lack of follow-up. Correlation was made between the mammographic and sonographic findings, the MR imaging findings, and the final pathology results for the remaining 32 cases.

RESULTS.In 18 women who did not undergo excisional biopsy before the MR imaging, MR imaging showed more extensive tumor burden or the detection of the primary lesion that was occult on conventional imaging in seven (38.9%) of 18 women. In nine (50%) of 18 women, MR imaging performed equally as well as mammography and sonography. In one case (5.6%), MR imaging and mammography underestimated disease extent. In another patient (5.6%), MR imaging overestimated tumor burden, although mammography failed to show the cancer. In 14 patients who had excisional biopsy before the MR imaging, residual tumor was shown in eight women (57.1%) with extensive tumor or additional separate foci in five of the eight patients. In two cases (14.3%) that were interpreted as equivocal, residual tumor was shown in both cases on reexcision. In three cases (21.4%), the MR imaging was interpreted as negative, but microscopic tumor was shown around seroma on reexcision. False-positive enhancement was seen in one case (7.1%).

CONCLUSION. MR imaging showed more extensive tumor than conventional imaging and affected the clinical management in 16 (50%) of 32 patients with invasive lobular carcinoma.

Introduction

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Infiltrating lobular carcinoma, which represents 5-15% of all diagnosed breast carcinoma [1], may be a diagnostic challenge to the breast radiologist. First described in 1941 by Foote and Stewart [2], unique histologic growth patterns were noted, including a linear file arrangement of the cells and a planar growth pattern. These histologic patterns may account for the higher false-negative rate on mammography than for other types of invasive breast carcinoma [3]. The detection of invasive lobular carcinoma on mammography and sonography may be difficult because of its growth pattern and the resulting low density of the lesions. Krecke and Gisvold [3], in their retrospective study of invasive lobular carcinoma, reported that 46% of the false-negative results on mammograms failed to show any suspicious findings even in retrospect. On sonography, the range of sensitivity has been reported to be 68-87.7%, with the sensitivity for lesions smaller than 1 cm in the range of 25-85.7% [4, 5].

Given the wide variation of results in the literature of conventional breast imaging studies, there is a potential role for breast MR imaging in the examination of patients with invasive lobular carcinoma. Prior studies have already shown breast MR imaging to be a useful adjunct to mammography, with the capability of detecting mammographically occult disease and hence altering patient management [6, 7]. Little has been written assessing the usefulness of MR imaging, especially in patients with invasive lobular carcinoma [6]. The purpose of this study was to evaluate the efficacy of MR imaging in the detection and staging of the extent of disease compared with mammography and sonography in patients with pure invasive lobular carcinoma of the breast.

Materials and Methods

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The patient records were obtained from a breast MR imaging research database. A concurrent search was also made in the department of pathology database for all patients diagnosed with pure invasive lobular carcinoma. Cases of mixed lobular and ductal carcinoma were excluded from the study. The list of patients generated from the pathology department was correlated with the radiology department's database to assess which women had breast MR imaging performed before definitive therapy. Between July 1993 and September 1999, 31 patients (one patient had bilateral metachronous carcinoma) enrolled in one of the ongoing institutional review board-approved research protocols in the department. One patient underwent a clinical breast MR imaging examination because she did not qualify as a research candidate. To qualify as a research candidate, the patient needed to be scheduled for biopsy because of a suspicious mammographic or sonographic abnormality or because of a finding of clinical concern.

One woman was excluded from the study because of lack of follow-up. The remaining 31 patients (32 cases) made up the study population. The patients ranged in age from 32 to 69 years old, with a mean age of 53.1 years at the time of the diagnosis. Twenty-nine (29/31) patients had a diagnostic mammogram that was reviewed by a dedicated breast radiologist in our department at the time of clinical presentation. Twelve of these cases had mammography performed at our institution, and 20 had mammography performed at outside institutions. For the mammography performed elsewhere, a member of the breast imaging section of our department reviewed the mammograms at the time of clinical evaluation and dictated an official report for each case. At the time of the review, the outside report was available. For the two patients whose mammograms were not available for review, the outside mammogram reported a single solid mass in one patient and no suspicious findings in the second patient. Twelve (12/32) of the mammograms were available for retrospective evaluation. Eleven (11/32) women had sonographic evaluations performed. Seven (7/11) of the patients who had sonographic evaluations were imaged at our institution, and four of the 11 examinations were performed at outside institutions. All the sonograms were also interpreted by a breast radiologist at the time the patient presented for clinical examination. For the sonographic examinations performed elsewhere, the images were reviewed and an official report was dictated in conjunction with the mammogram. Seven (7/11) of the sonographic studies were available for retrospective review.

MR imaging of the breast was performed on a 1.5-T Signa system (General Electric Medical Systems, Milwaukee, WI). The women were placed in the prone position with the breast compressed in the medial to lateral position using a specially designed breast multicoil array. The MR imaging protocol evolved over time. With improved technology, the image acquisition times decreased. The following parameters were used in all the studies: sagittal T1-weighted spin-echo (TR range/TE, 500-600/17) and sagittal fat-suppressed T2-weighted fast spin-echo (TR/TE, 4000/120) sequences with a 12- to 16-cm field of view, 3-mm slice thickness, 1-mm gap, and a 256 x 256 matrix. The breast was imaged before and after the administration of gadopentetate dimeglumine (Magnevist; Berlex, Wayne, NJ) with a sagittal, three-dimensional volume fat-suppressed fast spoiled gradient-echo sequence (TR/TE, minimum/minimum), 18-cm field of view, 2-mm slice thickness, no gap, and a 256 x 512 matrix). Each patient received gadopentetate dimeglumine (0.1 mmol/kg) injected as a bolus followed by 20 mL of saline. Imaging began during the saline injection. The imaging time for each three-dimensional volume fast spoiled gradient-echo sequence was 90 sec. One set of unenhanced images was obtained. After the administration of gadopentetate dimeglumine, the entire breast was imaged twice in succession using the three-dimensional volume fast spoiled gradient-echo sequence.

Before the MR imaging, 14 cases had undergone excisional biopsy, 13 had no prior intervention performed, three had undergone fine-needle aspiration, and two had core needle biopsies. For the women who had already had excisional biopsy, MR imaging was obtained before reexcision to achieve positive or close margins. Twenty-six patients presented with a palpable breast mass, one patient had malignant axillary adenopathy on examination, and five women had no suspicious findings on physical examination.

The prospective MR interpretations were used in this study. The clinical findings and the mammographic and sonographic reports were available at the time of the review. A finding on MR imaging was considered suspicious if it enhanced in the first contrast-enhanced image and met at least one of the following criteria: a mass with ill-defined or irregular margins, a region of linear or branching enhancement, or an area of regional enhancement with poorly defined or irregular borders or architectural distortion. Imaging findings that were considered benign included scattered punctate foci of enhancement measuring 1-3 mm, patchy enhancement of fibroglandular tissue, circumscribed enhancing masses with smooth or macrolobulated borders, and masses that did not enhance [8, 9].

All patients underwent surgery after MR imaging. Thirteen cases had excisional biopsy followed by mastectomy, 10 had excisional biopsy, six underwent mastectomy, two had fine-needle aspiration biopsy followed by mastectomy, and one had a core needle biopsy and a subsequent mastectomy. For nonpalpable lesions that were detectable on either mammography or sonography, needle localization was performed before the excisional biopsy. MR imaging—guided wire localization was performed for nonpalpable MR imaging-detected abnormalities in seven women. The details of this procedure have been previously reported [10]. Specimen radiographs were obtained for the wire-guided biopsies. The grid location of the region of interest on the specimen radiograph, if visible, was marked for the pathologist. For excisional biopsies, including MR imaging—guided wire localizations, the specimen and the specimen radiograph were delivered to the pathology laboratory. A radiologic—pathologic correlation sheet accompanied the specimen in MR-guided wire localization cases to show the relationship between the wire and the region of interest. Excision of the palpable lesions was guided by physical examination, and a specimen radiograph was not obtained. The surgeon oriented the specimen. The region of interest designated by the radiologist was inked with one color, then the specimen was inked with several different colors to indicate the margins. The specimen was measured and sectioned every 2-3 mm. The entire specimen was submitted for histopathologic examination.

In the patients having mastectomy, the standard gross examination was performed. After measurements were obtained and the specimens inked, the mastectomy specimens were sectioned every 0.5 cm with careful evaluation of each slice. Sections of the tumor and additional suspicious areas were submitted for evaluation. A minimum of 12-15 sections was submitted for histopathologic analysis if no gross abnormality was noted. For each mastectomy patient, two to three sections from the tumor, two sections from each of the four quadrants, one section from the deep margin of resection, two sections of the nipple, and all lymph nodes were microscopically evaluated. The imaging findings (mammography, sonography, and MR imaging) were correlated with the final pathology results.

Results

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The densities of the breast tissue on mammography of the 32 cases were heterogeneously dense (n = 16), scattered (n = 8), extremely dense (n = 4), fatty (n = 2), and not available (n = 2). Mammography, obtained before any biopsy, did not detect the invasive lobular carcinoma in 17 (53.1%) of 32 cases. In two (6.2%) of these cases, needle localization and excisional biopsy were performed for calcifications. In the first case, the calcifications were found on pathology to be incidental. In the second case, the calcifications represented ductal carcinoma in situ. In both cases, final pathology from the excisional biopsy revealed invasive lobular carcinoma that was not detected on mammography. In 15 (46.9%) of 32 cases, a mammographic finding was present, as described in Table 1. In three cases (9.4%, 3/32), the mammographic findings were negative, but sonography detected the suspicious findings.

A total of 11 patients had sonographic examinations, the results of which are given in Table 2. In six of 11 cases, a mammographic abnormality corresponded to the sonographic finding. In three of 11 cases, the mammographic findings were negative, with positive findings only on sonography.

The pathologic size of the lesions ranged from 1 mm to diffuse multifocal tumor, making measurement difficult. The mean size of the tumor, including only the cases that were amenable to measurement (n = 20), was 1.7 cm. The tumor was difficult to measure because of its diffuse nature in 12 cases.

Fourteen patients had excisional biopsy before MR imaging of the breast (Table 3). The biopsy status of the patients at the time of the MR imaging is summarized in Table 4. The findings on MR imaging are listed in Table 5. On the contrast-enhanced images, a thin rim of enhancement around the seroma was not considered suspicious. Thick or nodular enhancement was considered suspicious for residual tumor around the biopsy site. In nine (64.3%) of 14 patients, MR imaging showed findings consistent with residual disease. Extensive enhancement was seen in four of these cases, and a second focus distant from the biopsy cavity was seen in one case. The extent of disease found at pathology correlated with extent of disease identified on MR imaging. Mastectomy was performed in these five patients. All five of these women had negative mammographic findings before their initial excisional biopsy. In two (14.3%) of 14 cases, the degree of contrast enhancement was interpreted as equivocal, residual tumor versus granulation tissue. Tumor was present in both cases on reexcision. In one case, a residual invasive lobular carcinoma measured 1.0 x 0.7 x 0.3 cm, and in the second case a 5-mm tubular carcinoma was present. Both patients underwent reexcision followed by breast conservation therapy. In three (21.4%) of 14 cases, the MR imaging findings were interpreted as negative, but residual microscopic tumor was present adjacent to the seroma. In one patient, a 1-mm invasive lobular carcinoma was present on mastectomy. The mammographic findings in this patient, before the initial excisional biopsy, had been negative. Reexcision in two cases revealed 10 foci of invasive lobular carcinoma ranging in size from 0.1 to 5 mm in one patient, and a single focus of invasive lobular carcinoma on a high-power field in the second patient. In both patients, mammography before the initial excisional biopsy had revealed a discrete mass. One false-positive case was seen on MR imaging in which suspicious contrast enhancement was identified around the seroma, but reexcision revealed no residual carcinoma.

Eighteen of 32 patients had MR imaging before excisional biopsy (Table 6). Thirteen patients had no intervention performed before MR imaging. Two patients underwent core needle biopsy, and three patients had fine-needle aspiration. In nine (50%) of 18 cases, MR imaging performed equally as well as conventional imaging when compared with the final pathology results. In seven (38.9%) of 18 women, MR imaging revealed additional findings: additional foci of tumor separate from the primary lesion (n = 2), extensive multicentric disease not seen on mammography or sonography (n = 3), and a primary lesion that was occult on mammography and sonography (n = 2). In one (5.6%) of 18 patients, both MR imaging and mammography equally underestimated the disease extent. Mammography and MR imaging revealed a spiculated mass measuring 15 mm on mammography and 11 mm on MR imaging. Excisional biopsy and subsequent mastectomy revealed diffuse invasive lobular carcinoma spanning 8 cm. In one (5.6%) of 18 patients, MR imaging overestimated disease extent. The MR imaging showed multiple areas of abnormal contrast enhancement, with the largest area measuring 2.2 cm. Mammographic findings in this case were negative. Mastectomy revealed a single localized area of invasive lobular carcinoma of 3.5 cm corresponding to the dominant mass seen on the MR image, with lobular carcinoma in situ in the remainder of the breast. The patterns of MR imaging contrast enhancement are summarized in Table 7.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The potential of MR imaging of the breast to affect clinical management of patients diagnosed with breast carcinoma has been shown by multiple studies [6, 7, 11,12,13]. Conventional imaging for lobular carcinoma poses a greater challenge than for other histologic types of breast carcinoma. This has been attributed partly to the tumor growth pattern [3]. Additionally, invasive lobular carcinoma has a propensity (14-31%) to be multifocal [13, 14]. Therefore, even if one lesion is detected, additional lesions may potentially be occult on the routine imaging examination. Given the limitations of conventional mammography and sonography in the evaluation of invasive lobular carcinoma, MR imaging may be able to enhance the detection and staging of disease, thereby affecting patient management. This is particularly important when breast conservation is being considered. The presence of undetected macroscopic residual or multifocal disease could lead to failure of breast conservation because of recurrence. In a study of patients with invasive lobular carcinoma, Rodenko et al. [6] concluded that MR imaging defined the extent of disease, including the presence of multifocal and multicentric disease, better than mammography. Our results confirm the findings of Rodenko et al. that MR imaging has the potential to affect the management of women with invasive lobular carcinoma before excisional biopsy. Our findings also show that even in women who have already undergone excisional biopsy, MR imaging may provide valuable information, such as residual tumor that is confined to the biopsy site or the presence of extensive or multifocal disease. In our series, in 16 (50%) of 32 patients, MR imaging more accurately defined the extent of tumor than did conventional imaging. Diffuse tumor was identified in six patients, necessitating mastectomy (Fig. 1). Additionally, MR imaging either detected the mammographically occult primary lesion (Figs. 2A,2B,2C and 3A,3B,3C) or a second separate focus in another seven patients. Six of these patients then underwent mastectomy, although, because of the proximity of the lesions, breast conservation was possible in only one patient (Fig. 4A,4B,4C). In the remaining three patients, residual disease was identified on MR imaging at the margins of the excisional biopsy site.

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. —47-year-old woman with palpable left breast mass and negative findings on mammography. Sonography (not shown) revealed 2.5-cm mass corresponding to palpable mass. Sagittal fat-suppressed contrast-enhanced three-dimensional fast spoiled gradient-recalled echo MR image (TR/TE, 9.3/2.2) shows multiple enhancing masses in all quadrants. Additional masses were unsuspected. At mastectomy, invasive lobular carcinoma was found in all four quadrants.

View larger version (148K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —51-year-old woman with negative mammographic findings and palpable breast mass. Sagittal fat-suppressed contrast-enhanced three-dimensional fast spoiled gradient-recalled echo MR image (TR/TE, 9.3/2.2) reveals extensive contrast enhancement throughout breast.

View larger version (91K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —51-year-old woman with negative mammographic findings and palpable breast mass. Mammographic images from MR imaging—guided needle localization show dense breast tissue. A 9-cm invasive lobular carcinoma was found at mastectomy.

View larger version (95K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —51-year-old woman with negative mammographic findings and palpable breast mass. Mammographic images from MR imaging-guided needle localization show dense breast tissue. A 9-cm invasive lobular carcinoma was found at mastectomy.

View larger version (87K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —51-year-old woman with palpable breast mass. Mammograms reveal no suspicious findings, which was stable in comparison with prior studies. Sonography (not shown) did not show any suspicious findings.

View larger version (69K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —51-year-old woman with palpable breast mass. Mammograms reveal no suspicious findings, which was stable in comparison with prior studies. Sonography (not shown) did not show any suspicious findings.

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —51-year-old woman with palpable breast mass. Sagittal fat-suppressed contrast-enhanced three-dimensional fast spoiled gradient-recalled echo MR image (TR/TE, 9.3/2.2) reveals enhancing spiculated mass (arrow).

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —61-year-old woman with abnormal mammographic findings. Multiple sagittal fat-suppressed contrast-enhanced three-dimensional fast spoiled gradient-recalled echo MR images (TR/TE, 9.3/2.2) reveal focally enhancing dominant mass (arrows) in inferior breast. However, anterior and superior to this mass are additional areas of enhancement (arrows).

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —61-year-old woman with abnormal mammographic findings. Mammographic images from wire localization of dominant mass seen in A. On wide excisional biopsy, multiple foci of invasive lobular carcinoma were found.

View larger version (87K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —61-year-old woman with abnormal mammographic findings. Mammographic images from wire localization of dominant mass seen in A. On wide excisional biopsy, multiple foci of invasive lobular carcinoma were found.

One of the limitations of MR imaging of the breast has been reported to be false-positive enhancement [11, 15]. This limitation was also seen in two cases in our series. Although MR imaging showed areas of false-positive enhancement in the first case, it also showed the primary lesion, which mammography had failed to do. In the second false-positive case, enhancement of granulation tissue was mistaken for residual tumor.

Underestimation of disease and false-negative MR imaging results have been reported for invasive lobular carcinoma [6, 16]. In our series, MR imaging failed to detect residual tumor or underestimated tumor extent in four (12.5%) of 32 cases. In one case, both mammography and MR imaging underestimated tumor extent. Mammography and MR imaging showed a 1.5-cm and a 1.1-cm mass, respectively. Final pathology revealed diffuse invasive lobular carcinoma spanning 8 cm. The reason for the discrepancy is not clear. Boetes et al. [16] described a similar case of underestimation of tumor extent on MR imaging. The three missed lesions represented microscopic disease. Nonspecific foci of enhancement may be seen in MR imaging of the breast. This is a limitation of breast MR imaging that has been previously reported [11]. The significance of these areas of enhancement is not clear; similar enhancement may be seen in benign breast tissue [15]. Differentiating such findings from enhancement of a 2- to 3-mm carcinoma would be difficult, especially when the situation is confounded by changes after biopsy with contrast material uptake in granulation tissue, as in our three patients.

All our false-positive (n = 1) and false-negative (n = 3) findings were in patients who had excisional biopsy before their MR imaging. The limitation may lie in our inability to differentiate residual tumor from enhancement of granulation tissue or changes after biopsy.

Our results indicate that breast MR imaging may have a significant impact on the treatment of patients with invasive lobular carcinoma. Such patients are eligible for breast conservation [1, 17,18,19,20,21], although it is reported that these tumors have a propensity to be multifocal [13, 14]. The results of our study and the study by Rodenko et al. [6] show the ability of MR imaging to detect the primary lesion and additional foci as well as to define the extent of the tumor better than conventional imaging. Our results indicate that if breast conservation is being considered for patients with invasive lobular carcinoma, MR imaging of the breast can provide essential information for treatment planning and management.

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