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MR Imaging Features of Infiltrating Lobular Carcinoma of the Breast

Histopathologic Correlation

¹ Department of Radiology, Box 0628, University of California San Francisco, 505 Parnassus Ave., San Francisco, CA 94143-0628.
² Department of Radiology, Stanford University Medical Center, 300 Pasteur Dr., Stanford, CA 94305.

Received July 16, 2001; accepted after revision October 26, 2001.

 
Address correspondence to A. Qayyum.

Abstract

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OBJECTIVE. Our study aimed to correlate the dynamic contrast-enhanced MR appearance of infiltrating lobular carcinoma of the breast with histopathologic findings.

MATERIALS AND METHODS. We retrospectively reviewed the high-resolution, fat-suppressed and dynamic contrast-enhanced MR images of 13 of 20 women diagnosed with pathologically proven infiltrating lobular carcinoma of the breast. Twelve of the 13 women presented with breast symptoms and underwent mammography. Five of the women also had breast sonography. MR imaging was performed for evaluation of disease extent before the patients underwent modified radical mastectomy (n = 11) or lumpectomy (n = 2). Three experienced radiologists reviewed the MR scans. The tumor pattern types described on imaging were correlated with a detailed analysis of the pathology.

RESULTS. We found three patterns of infiltrating lobular carcinoma on MR imaging. The tumor pattern on imaging correlated with pathologic tumor morphology. We found the following patterns of infiltrating lobular carcinoma: a solitary mass with irregular margins (n = 4) that corresponded to the same appearance at pathology; multiple lesions, either connected by enhancing strands (n = 6) or separated by nonenhancing intervening tissue (n = 2), that correlated with the pathologic appearance of noncontiguous tumor foci, with malignant cells streaming in single-file fashion in the breast stroma or small tumor aggregates separated by normal tissue; and enhancing septa only, which were correlated with the histopathologic appearance of tumor cells streaming in the breast stroma (n = 1).

CONCLUSION. Infiltrating lobular carcinoma may be detected on MR imaging as solitary or multiple lesions that correspond to tumor morphology on pathologic examination. The appearance of multiple lesions or of enhancing fibroglandular breast elements on MR imaging is suggestive of infiltrating lobular carcinoma.

Introduction

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Infiltrating lobular carcinoma of the breast, which constitutes 7-15% of invasive breast cancers [1,2,3,4], presents a diagnostic challenge because of its variable presentation on imaging and clinical examination. It is postulated that the histologic characteristics of infiltrating lobular carcinoma are responsible for the imaging difficulties. Typically these tumors show a single-file infiltration of malignant cells [1, 5, 6] through the breast stroma with a relative paucity of desmoplastic response, hemorrhage, necrosis, or calcification [6].

The sensitivities in the detection of infiltrating lobular carcinoma have been reported as 57-81% for mammography [3, 4, 7,8,9,10] and 68% for sonography [3, 8]. Butler et al. [3] reported sonographic sensitivity of 87%, but they included cases of mixed infiltrating lobular carcinoma and invasive ductal carcinoma.

Contrast-enhanced MR imaging of the breast is extremely sensitive in the detection of breast cancer [11,12,13,14,15,16,17,18,19,20,21,22,23,24], but few studies have focused on MR imaging of lobular breast cancer. Rodenko et al. [1] correlated the pathologic extent of infiltrating lobular carcinoma in 20 patients with MR imaging and mammographic findings using high-resolution scans and nondynamic gadolinium-enhanced imaging. They reported 85% MR imaging correlation versus 32% mammographic correlation with pathology. The mammographic sensitivity in their study is much lower than that in the larger trials; however, they reported disease extent rather than detection alone. Weinstein et al. [25] reported more extensive tumor burden detection on MR imaging than on conventional imaging in seven of 18 patients with infiltrating lobular carcinoma.

We evaluated 13 women with pure infiltrating lobular carcinoma using both high-resolution scans and dynamic imaging to gain a better understanding of the MR imaging features. Prior work has looked closely at the MR imaging patterns of enhancement associated with infiltrating lobular carcinoma, but we also looked at dynamic imaging, with the goal of better differentiating between normal and abnormal breast tissue and, thereby, better assessing disease extent.

Materials and Methods

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Patients
We reviewed images from 20 women ranging in age from 46 to 84 years (mean age, 55 years), who had been diagnosed with infiltrating lobular carcinoma between 1993 and 1999 and who had undergone MR imaging of the breast. Three of the women were excluded from the study because they had associated ductal carcinoma, and four women were excluded because their original pathology or imaging reports were not available for review. The MR scans of the remaining 13 women with pathologically proven pure infiltrating lobular carcinoma were reviewed.

Twelve of the patients with positive clinical findings had been referred for MR imaging: nine presented with a palpable breast mass, one complained of breast pain, one presented with periareolar skin changes, and one had nipple retraction. The 13th patient was referred after routine mammography. Before MR imaging, each patient had undergone mammography; findings in 12 patients showed suspicious or overtly malignant features. Five of the patients also had sonographic examinations preceding MR imaging, and a malignant lesion was reported in three of the five women. The clinical indications for MR imaging were for evaluation of tumor extent before surgery in 11 women and for MR imaging—guided biopsy or localization in two women.

Techniques
We obtained contrast-enhanced MR scans of the breast for each patient using a combined dynamic and high-spatial-resolution imaging protocol. A 1.5-T scanner (Signa Echospeed; General Electric Medical Systems, Milwaukee, WI) and a dedicated phased array breast coil (MRI Devices, Waukesha, WI) were used. Each dynamic scan consisted of rapid three-dimensional spoiled gradient-echo scans using a water-selective spectral-spatial excitation to suppress fat signal, an on-resonance binomial magnetization transfer pulse for fibroglandular tissue suppression, as well as an interleaved spiral k-space trajectory readout and partial k-space sampling in k—z direction to reduce the scanning time for the whole breast to 10 sec (TR/TE, 38/7; flip angle, 40°; effective matrix, 188 x 188; field of view, 20 cm; effective slice thickness, 4.5-6.0 mm). The dynamic scans were repeated 20 times, with bolus IV injection of 0.1 mmol/kg of gadolinium (gadopentetate dimeglumine [Magnevist], Berlex, Wayne, NJ; or Prohance, Bracco Diagnostics, Princeton, NJ) at a rate of 2.0 mL/sec followed by a 20-mL saline flush.

Immediately after the dynamic scans were obtained, corresponding to approximately 1.5-2.0 min after the start of enhancement in the breast, high-spatial-resolution, fat-nulled scanning was performed with centric phase encoding, using a three-dimensional water-selective spectral-spatial spoiled gradient-echo acquisition with an on-resonance 1-2-1 binomial magnetization transfer pulse (33/9; flip angle, 50°; matrix, 512 x 192; field of view, 20 cm; slice thickness, 1.5-2.0 mm; 60 slices per scan; scanning time, 6 min 12 sec) [26].

The high-resolution imaging was followed by acquisition of 26 additional dynamic scans to capture the washout phase of contrast enhancement, using the same three-dimensional spiral dynamic sequence. In one initial case, dynamic scanning was not performed, and three-dimensional water-selective spectral-spatial magnetization transfer imaging used sequential, not centric, phase encoding and a 256 x 192 matrix. In two other early cases, dynamic imaging consisted of rapid interleaved two-dimensional spiral imaging (960/7; flip angle, 90°; matrix, 188 x 188; field of view, 20 cm; slice thickness, 6-9 mm; 12 slices through the breast at each time point; 7.68 sec per set of 12 slices) repeated 56 times [19]. In these cases, high-resolution three-dimensional water-selective spectral-spatial magnetization transfer was thus delayed until approximately 6.5 min after the start of enhancement in the breast.

One of the patients underwent bilateral modified radical mastectomy, 10 patients underwent unilateral modified radical mastectomy, one patient underwent MR imaging—guided localization followed by lumpectomy, and one patient underwent MR imaging—guided core biopsies followed by lumpectomy.

Pharmacokinetic Analysis
Invasive tumors show rapid rates of contrast enhancement on dynamic imaging. The enhancement characteristics are attributed to tumor angiogenesis. The new tumor vessels are thought to have several unique properties that may account for the distribution of IV contrast material. These properties include increased tumor blood volume, arteriovenous shunting, altered capillary bed transit time, and increased capillary permeability [19]. K21 is a parameter used to distinguish invasive tumor tissue from benign tissue on the basis of enhancement pattern. K21 represents the rate of exchange of gadopentetate dimeglumine between the extracellular space and plasma. It is calculated mathematically by fitting dynamic enhancement data to a standard two-compartment pharmacokinetic model on a pixel-by-pixel basis using a non-linear gradient-expansion algorithm [19, 27, 28]. Malignant tissue shows a higher rate of exchange of contrast material than benign tissue. The combined wash-in and washout spiral data were linearly interpolated in the slice direction to create dynamic data at locations corresponding to each three-dimensional water-selective spectral-spatial magnetization transfer image [27].

The K21 parameter was used to generate color maps and to help differentiate invasive tumor from benign lesions. The K21 parameter was used for pharmacokinetic analysis in our study because of its high specificity in differentiating invasive carcinomas from other lesions [27, 28]. All calculations were performed using software (Interactive Data Language, version 3.6; Research Systems, Boulder, CO) and an Ultrapac computer (Sun Micro-systems, Mountain View, CA). The K21-value maps were used to generate color maps of the high-resolution three-dimensional water-selective spectral-spatial magnetization transfer images. Cyan was arbitrarily selected to represent the lowest K21 values, and yellow was selected to represent the highest K21 values using a nonobscuring algorithm [27] (Fig. 1A,1B,1C).

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —55-year-old woman with multiple infiltrating lobular carcinoma lesions. Sagittal three-dimensional water-selective spectral-spatial magnetization transfer MR image shows enhancing tumor clusters (arrows) with nonenhancing intervening tissue.

View larger version (77K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —55-year-old woman with multiple infiltrating lobular carcinoma lesions. Color parametric map of A shows yellow regions that correspond to tumor foci. K21 value maps are used to colorize high-resolution three-dimensional water-selective spectral-spatial magnetization transfer images with colors ranging from cyan (lowest values) to yellow (highest values).

View larger version (159K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —55-year-old woman with multiple infiltrating lobular carcinoma lesions. Photomicrograph shows foci of infiltrating lobular carcinoma (arrows) surrounded by benign breast tissue (B). Normal tissue separates infiltrating lobular carcinoma foci. (H and E, x200)

Color maps could not be produced in the one patient who did not undergo dynamic imaging. In this patient, the tumor was diagnosed on the basis of morphology and enhancement characteristics. Color parametric maps were not essential for recognizing tumor tissue, but they were helpful because of the color representation of the tumor enhancement pattern.

Three experienced radiologists independently reviewed the MR scans. Each radiologist was required to document the presence of solitary or multiple lesions and to describe the MR imaging findings in terms of criteria relating to lesion morphology, enhancement pattern, and extent of lesion. The morphologic criteria included lesion borders and shape. The lesion borders were categorized as well defined or ill defined, and the lesion shape was categorized as round, smoothly lobulated, or irregular. The enhancement pattern was categorized as homogeneous, heterogeneous, or rimlike. The presence or absence of secondary features of malignancy (skin thickening and chest wall invasion) was also noted.

The reviewers assessed the colorized images (in 12/13 patients) and subjectively rated the homogeneity of K21 values in each lesion. In addition, the colorized images were used to define regions of interest based on color representation of K21. Four regions were selected for each tumor: the region with the highest K21, the region with the lowest K21, the region with the most representative K21, and the K21 of the entire lesion.

Results

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We found overall consensus among the three radiologists in lesion detection. Three major morphologic patterns were observed on MR imaging that correlated with the histologic appearance of infiltrating lobular carcinoma when reviewed by an experienced pathologist (Table 1). In four women, MR imaging showed a discrete solitary mass lesion with irregular margins. The histopathologic findings corroborated the MR imaging in all four of these women (Fig. 2A,2B). The second infiltrating lobular carcinoma pattern seen on MR imaging, which was found in eight women, was of multiple lesions. Lesions were observed either as multiple small enhancing foci connected by enhancing strands (Figs. 3 and 4A,4B) or as enhancing clusters with nonenhancing intervening tissue (Fig. 1A,1B,1C). The first type correlated pathologically with noncontiguous tumor foci with malignant cells streaming in a single-file fashion in the breast stroma (n = 6). The second type correlated with small tumor aggregates separated by normal tissue (n = 2). The third pattern on MR imaging was seen in one patient as enhancing septa without a discrete mass (Fig. 5). On pathology, this pattern correlated with the appearance of tumor cells streaming in the breast stroma. All tumors showed heterogeneous rather than homogenous enhancement, although one tumor showed poor enhancement. The enhancement of two solitary lesions was described as rimlike by two radiologists and as heterogeneous by the third radiologist. All three radiologists agreed on all the morphologic features of the remaining lesions. No obvious histologic features were predictive of the degree of enhancement. An enlarged axillary lymph node was present in one patient.

View larger version (124K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —47-year-old woman with solitary infiltrating lobular carcinoma. Sagittal three-dimensional water-selective spectral-spatial magnetization transfer MR image shows enhancing, solitary, irregular mass (arrow).

View larger version (137K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —47-year-old woman with solitary infiltrating lobular carcinoma. Photomicrograph shows solitary tumor mass (asterisk) with irregular margins. (H and E, x100)

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —69-year-old woman with noncontiguous tumor foci and malignant cells streaming in single-file fashion in breast stroma. Sagittal MR image shows tumor foci (asterisks) connected by enhancing strands (arrows).

View larger version (164K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —43-year-old woman with noncontiguous tumor foci and malignant cells streaming in single-file fashion in breast stroma. Photomicrograph shows tumor focus (arrows) with fibrous strand (S) extending from focus. (H and E, x100)

View larger version (197K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —43-year-old woman with noncontiguous tumor foci and malignant cells streaming in single-file fashion in breast stroma. Photomicrograph of fibrous strand shows classic histologic pattern of tumor cells in single-file arrangements. (H and E, x300)

View larger version (159K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5. —84-year-old woman with tumor cells streaming in breast stroma. Sagittal MR image shows enhancing septa (arrows) with no dominant focus of tumor.

The maximum K21 values ranged between 0.005 and 0.38. The K21 values were obtained by placing regions of interest over regions of suspected tumor enhancement. In certain instances, the lesions were small or linear, which may have affected the actual numbers obtained. Placement of regions of interest and selection of the most representative lesion were also difficult for infiltrating lesions without large masslike components. The small patient number and variation in imaging technique prevented accurate interpretation or statistical analysis of the K21 data. Variations between observers were caused in part by the size of the regions of interest selected. In view of the variables and the fact that small patient numbers made interpretation of the actual K21 data of uncertain value, emphasis was placed on morphologic features and patterns of enhancement. The three reviewers were in overall agreement on imaging features; the images of the final six patients were interpreted by consensus on this basis for logistic reasons.

Discussion

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The rate of false-negative interpretation of infiltrating lobular carcinoma on mammograms has been reported to be in the range of 19-43% [4, 7, 29]. Difficulty in detecting infiltrating lobular carcinoma has been attributed to two main factors. First, the opacity of infiltrating lobular carcinoma on mammograms is similar to that of the normal breast parenchyma [4, 7, 30], which may be the result of the relative paucity of desmoplastic response. The second factor is the single-file invasion pattern of the malignant cells. The percentage of infiltrating lobular carcinoma lesions reported to be associated with suspicious calcification varies. In the study by Hilleren et al. [7], 2% of infiltrating lobular carcinomas (3/137) showed suspicious calcifications. Krecke and Gisvold [4] found suspicious calcifications associated with only 1% of 185 pure infiltrating lobular carcinomas. Cornford et al. [2] cited a higher frequency of micro-calcifications: 28%. They included mixed invasive lobular and ductal tumors in the infiltrating lobular carcinomas category, which could account for the difference. Characteristically, the tumor cells are seen to surround the ducts without obstructing them. It is postulated that the lack of ductal invasion or obstruction may explain why microcalcifications are not often seen with these tumors [7]. A more recent study of 30 women, in which breast size on mammography was evaluated, reported an association between reduced breast size and diffuse infiltrating lobular carcinoma. The women with reduced breast size on mammography did not have a discrete mass on pathology but showed tumor with numerous microscopic skip areas [31].

Infiltrating lobular carcinoma is most commonly described on sonography as a heterogeneous hypoechoic mass with an irregular contour and posterior acoustic shadowing [3, 7, 30, 32]. Butler et al. [3] found 10 (12%) of 81 cases of infiltrating lobular carcinoma to be occult on sonography, and their study found focal shadowing without a discrete mass in 12 (15%) of 81 patients.

MR imaging is generally accepted as a more sensitive technique than mammography or sonography for the detection of breast tumors. The use of dynamic imaging and pharmacokinetic analysis of dynamic data has increased detection specificity [19, 33].

In our study, three basic patterns of infiltrating lobular carcinoma were observed on MR imaging. There was overall consensus among the reviewers in the number of lesions detected and the tumor extent, shape, and enhancement. The most common pattern, observed in eight of 13 patients, was of multiple enhancing foci with either connecting enhancing strands or nonenhancing intervening tissue. The histologic correlation of small tumor aggregates with or without single-file cell infiltration may be a contributing factor to the low density of these tumors on mammography and the lack of focal mass on sonography.

Our study further supports the findings of other authors in this relatively uncommon malignancy, including those of Weinstein et al. [25], who describe the following patterns on MR imaging in 18 women with infiltrating lobular carcinoma: a solitary mass, regions of linear branching enhancement, regions of enhancement with poorly defined borders or architectural distortion, and multifocal lesions.

Multifocal disease was diagnosed in most of the patients in our study, and it was treated with modified radical mastectomy. One patient with multifocal disease in one breast underwent bilateral modified radical mastectomy, and two patients with a solitary lesion underwent modified simple mastectomies. MR imaging is useful in assessing disease extent before surgery, but other factors, such as family history and patient and physician preference, also influence treatment selection.

The major limitation of our study was the small subject population, which precluded any statistical analysis. Some variation in the imaging parameters occurred over the 6-year period. Dynamic imaging was not performed in one of the patients, and it was therefore not possible to generate a color parametric map in this case. However, in that patient, contrast material was administered that enabled evaluation of areas of increased enhancement. The range of maximum K21 values in our study was of an order of magnitude less than that described for studies relating to invasive ductal carcinoma [19]. The significance of this difference is unclear, in view of the small patient population and the variation in scanning parameters. Variations occurred in the K21 data between observers and by each observer selecting regions of interest for maximum K21 and the most representative K21 values. Factors contributing to the variation in K21 data include variable imaging parameters, differences in size of regions of interest, and difficulty in selecting the most representative tumor focus for infiltrating lesions that did not have a large discrete mass lesion. The small patient population and the many factors influencing the K21 data prevent meaningful interpretation of the K21 data.

Although parametric maps are not essential, they are helpful in recognizing tumor because of the color representation of the rate of enhancement (Figs. 1A and 1B). Color mapping of the dynamic data did appear to facilitate the identification of malignant lesions, and it may be a useful tool for determining disease extent in the future.

In conclusion, dynamic MR imaging may be used for better delineation of disease extent in infiltrating lobular carcinoma of the breast than can be obtained with sonography or mammography, and it has a role in surgical planning. Infiltrating lobular carcinoma may be seen as a spiculated solitary lesion or as multiple lesions in the breast. Infiltrating lobular carcinoma should be suspected in the presence of multiple enhancing lesions with or without enhancing interconnecting septa or when a region of strandlike enhancement is present without a discrete or dominant focus on MR imaging.

References

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