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10.1245/ASO.2003.03.016
Annals of Surgical Oncology 10:1048-1053 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Magnetic Resonance Imaging Detects Unsuspected Disease in Patients With Invasive Lobular Cancer

M.L. Quan, MD, L. Sclafani, MD, A.S. Heerdt, MD, J.V. Fey, MPH, E.A. Morris, MD and P.I. Borgen, MD

From the Breast Service, Department of Surgery (MLQ, LS, ASH, JVF, PIB), and the Breast Imaging Section, Department of Radiology (EAM), Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Lisa Sclafani, MD, Breast Service, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021; Fax: 631-864-3827; E-mail: sclafanl{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Predicting the extent of disease in the breasts of patients with invasive lobular cancer (ILC) can be difficult because of the limits of physical examination and standard imaging. We determined the utility of magnetic resonance imaging (MRI) in finding otherwise unsuspected cancer in the ipsilateral or contralateral breast of patients with ILC.

Methods: Through database review of all breast MRIs performed between January 1, 1999, and December 30, 2002, we identified patients with newly diagnosed ILC who underwent an MRI for extent-of-disease evaluation or contralateral screening. MRI findings separate from the primary tumor were biopsied and correlated with pathology by using MRI-guided biopsy.

Results: Sixty-two patients were identified. In all, 59 ipsilateral and 57 contralateral studies were performed. Suspicious lesions separate from the primary tumor were found by MRI in 38 (61%) of 62 patients. Eight patients were excluded from further analysis (seven elected mastectomy without biopsy; one had an unguided excision). Nineteen of 51 patients with an ipsilateral finding underwent MRI-guided biopsy, which revealed cancer in 11, or 22% of those imaged. Twenty of 53 patients with a contralateral finding underwent MRI-guided biopsy, which revealed cancer in 5, or 9% of those imaged.

Conclusions: MRI of the breast identifies unsuspected multicentric or contralateral cancer in patients with ILC. These findings support the use of MRI in selected patients with ILC, particularly in the ipsilateral breast.

Key Words: Invasive lobular cancer • Magnetic resonance imaging • Image-guided biopsy • Occult cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although invasive lobular cancer (ILC) constitutes only 10% to 14% of all malignancies of the breast,1,2 its unique presentation, tendency toward multicentricity,3 and associated higher incidence of synchronous contralateral disease3,4 have generated special interest in its management. Standard screening methods such as mammography, ultrasound (U/S), and physical examination have lower sensitivities for detecting lobular cancer compared with other invasive breast cancers. The sensitivity of detecting ILC has been reported to be as low as 57% to 76% for mammography5,6 and 25% to 87% for U/S.7,8 Physical examination can also be difficult because of vague findings, such as thickening or induration, as opposed to a discrete nodule, particularly in early disease. Difficulties with all three of these diagnostic methods have been attributed to the growth of tumor cells in single lines throughout the stroma, resulting in subtle physical findings.9

Magnetic resonance imaging (MRI) relies on physiologic rather than physical changes and, therefore, has provided new promise for evaluation of the breast and, potentially, for improved detection of ILC.10 Recent studies have documented that the sensitivity of MRI in detecting malignancy in the breast ranges from 80% to 100%.11–15 The limitation of MRI, however, is its lower specificity (range, 37%–97%), which results in high false-positive rates.13,16,17 Currently, the role of breast MRI is being evaluated to better define those patients most likely to benefit from its use. In this study, we attempted to determine the utility of MRI in characterizing the extent of ipsilateral cancer and identifying contralateral cancer in patients with ILC.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Through a database review of all breast MRIs performed at our institution between January 1, 1999, and December 30, 2002, we identified 62 patients with newly diagnosed ILC who had an MRI as part of an extent-of-disease work-up of the ipsilateral breast or to screen the contralateral breast. The diagnosis of ILC was determined before the MRI by either core or excisional biopsy. Patients who did not have pathology assessed at our institution were excluded. Clinical and radiological findings were correlated to identify patients who had additional lesions identified initially by MRI. To correlate MRI findings with pathology, we evaluated only those patients and lesions in which preoperative MRI needle localization or MRI-prompted U/S-guided biopsy was performed.

Our routine breast MRI protocol has been described previously.10 Briefly, using an immobilization/biopsy coil (MRI Devices, Waukesha, WI), we performed breast MRI on a 1.5-T GE Signa magnet (General Electric, Milwaukee, WI). We obtained initial T2-weighted images, and the entire breast was then imaged by using a fat-suppressed, three-dimensional T1-weighted sequence. Gadolinium was then administered (.1 mmol/kg), followed by repetition of the sequence three times. Slice thickness was 2 to 3 mm without a gap, depending on breast thickness in compression. Image acquisition took 90 to 120 seconds on average. Subtraction imaging was then performed in addition to fat suppression to evaluate possible enhancement of high-signal areas on the T1-weighted images. Prior mammograms and U/S examinations were used for comparison when available. Locations of prior surgery or areas of palpable findings were marked on the patient’s skin surface with vitamin E capsules for correlation with MRI findings. MRI findings were graded by using a lexicon in progress (similar to BI-RADS [American College of Radiology, Reston, VA] for mammography) to standardize readings.10,18

Patients underwent MRI-guided needle localization and surgical excision of any BI-RADS category 4– or 5–equivalent lesion, as assessed by MRI with the lexicon.18 All lesions biopsied were occult based on initial imaging and identified initially on MRI only. Directed U/S was performed at the discretion of the interpreting radiologist to determine whether the lesion was sonographically evident and, thereby, amenable to biopsy under U/S guidance. These patients were included in our analysis, because the biopsies were prompted by MRI. The remaining lesions were localized by using MRI-guided wire placement on the day of surgery, by using a commercially available grid-localizing system (Biopsy-System NMR NI 160; MRI Devices) and MRI–compatible hook wires, as described previously.19 Patients then underwent needle-localized excisional biopsy in the operating room, as well as definitive surgery for the primary cancer site. Pathology specimens were evaluated with standard fixation and hematoxylin and eosin staining. Sentinel lymph node (SLN) biopsy was performed when indicated on the basis of prior cancer diagnosis.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
During the study period, 354 patients presented with ILC to a surgeon at our institution. Of these, 62 patients underwent an MRI and were eligible for evaluation; 54 had bilateral breast MRI, and 8 had unilateral MRI only. Of the patients with unilateral breast MRI, five had the ipsilateral breast imaged to determine extent of disease, and three underwent contralateral imaging only because ipsilateral mastectomy was already planned. In total, 59 ipsilateral and 57 contralateral studies were performed in 62 patients. Patient characteristics and imaging characteristics of the primary tumor are listed in Tables 1 and 2Go, respectively. Diagnosis of ILC was based on core biopsy in 33 (53%) and on excisional biopsy in 29 (47%) of 62 patients. The pathology was classic ILC in 50 (81%) of patients evaluated, 10 (16%) were mixed ductal/lobular, and 2 (3%) were tubulolobular.


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  		TABLE 1. Patient characteristics—ILC and MRI (N = 62)
 

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  		TABLE 2. Imaging characteristics of the primary tumor (N = 62)
 
Of the 62 patients imaged, 38 (61%) had 63 additional suggestive lesions separate from the primary ILC, identified solely on MRI. Seven patients elected mastectomy without MRI biopsy, and one patient had an unguided excision of the MRI lesion because of positive margins. Six of the eight patients had additional areas of cancer found on final pathology. Two had findings of lobular carcinoma-in-situ or other benign findings. All eight of these patients were excluded from further analysis, because direct correlation between the MRI finding and pathology was not possible.

At the discretion of the interpreting radiologist, MRI-directed U/S was performed to determine whether the area of enhancement correlated with a sonographic finding. In 5 of 20 patients, directed U/S at the site of the MRI abnormality identified a corresponding lesion. Three of these patients went on to have U/S-guided core biopsies of these areas, of which two showed cancer. The other two patients underwent U/S-guided needle localization and surgical excision, and one showed an additional site of cancer. The other 25 patients underwent MRI-guided needle localization and surgical excision. Overall, 30 patients had 46 lesions separate from the primary tumor for which they underwent MRI-prompted core or needle-localized excisional biopsies at the time of surgery for the primary tumor. Overall results are summarized in Table 3.


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  		TABLE 3. Findings of MRI-prompted biopsies in patients with ILC
 
Ipsilateral Findings
Nineteen of 51 patients had an abnormality identified by MRI of the ipsilateral breast. Eleven of the 19 patients (58%) biopsied had an additional cancer separate from the primary cancer and identified by the MRI-guided biopsy. On pathology, 10 were ILC, and 1 was ductal carcinoma-in-situ (DCIS; Fig. 1). Six (54%) of the 11 patients went on to have completion mastectomy on the basis of the findings of the MRI-guided biopsy. Of all the assessable patients who had an ipsilateral MRI, 11 (22%) of 51 had an additional unsuspected malignancy identified.



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  		FIG. 1. Findings in patients undergoing ipsilateral breast magnetic resonance imaging (MRI). ILC, invasive lobular cancer; DCIS, ductal carcinoma-in-situ.

 
Contralateral Findings
Twenty of 53 patients had an abnormality identified by MRI of the contralateral breast. Five (25%) of the 20 patients who underwent a biopsy had an additional synchronous, otherwise occult malignancy identified by the MRI-guided biopsy. On pathology, one was ILC, two were invasive ductal carcinoma, and two were DCIS (Fig. 2). All three patients with invasive cancer went on to have SLN biopsy; SLN biopsy results were negative in two of the three patients. In the third patient, who had invasive ductal carcinoma, two of four SLNs were positive for micrometastases; this patient went on to have a completion axillary node dissection. One patient with invasive cancer had a re-excision because of a positive margin. Both patients with DCIS had positive margins on pathology. One elected re-excision, which was negative on pathology, and the other patient elected mastectomy. Of all the assessable patients who underwent a contralateral breast MRI, 5 (9%) of 53 had an unsuspected, otherwise occult malignancy identified.



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  		FIG. 2. Findings in patients undergoing contralateral breast magnetic resonance imaging (MRI). ILC, invasive lobular cancer; DCIS, ductal carcinoma-in-situ.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Although breast MRI is being used with increasing frequency for the screening and diagnosis of breast cancer, its utility and indications as a diagnostic modality are still being determined.10,13 The high sensitivity (80%–100%) for detecting abnormalities not identified by other diagnostic tools makes its use highly attractive.11–15 However, its lower specificity (37%–97%)13,16,17 for malignancy may lead to additional unnecessary surgery or further imaging.20 Studies have suggested that breast MRI is best used in situations in which there is a high probability of cancer, such as in a patient with known cancer.10,20

The ability of ILC to be identified by standard imaging, such as mammogram and U/S, is reportedly less than that for other invasive cancers.5–8,21 The classic growth pattern of single files of malignant cells spreading in a planar pattern often results in subtle infiltration of the normal breast parenchyma.9 Additionally, the classic desmoplastic reaction to surrounding tissues, which causes a mass effect, is less common, so findings are often limited to architectural distortion or vague thickenings. Tumor size is often underestimated with standard modalities.22 The higher incidence of multicentric and contralateral disease3,4 makes patients with ILC ideal candidates for a more sensitive diagnostic test, such as MRI.10

Relatively few studies have looked specifically at MRI in patients with ILC. Qayyum et al.23 correlated MRI findings in patients with known ILC to gain a better understanding of the type of enhancement that ILC produces on MRI. Thirteen patients with ILC were reviewed and found to have three patterns of abnormality on MRI: in eight, multiple enhancing masses; in four, presence of an irregular mass; and in one, enhancing septa without a dominant mass.23 Similarly, Weinstein et al.24 studied a series of 18 patients who underwent MRI before excision of ILC diagnosed on core biopsy or fine-needle aspiration. In all 18, MRI identified the primary tumor as a suspicious lesion, most as irregular masses, and the rest with abnormal enhancement. MRI was believed to be superior to conventional imaging in defining the extent of the tumor in 7 of the 18 patients. In the same study, Weinstein et al. reviewed 14 patients who had an excisional biopsy before MRI to evaluate extent of disease. MRI identified suspicious lesions in nine patients and was able to accurately predict residual disease in six, with one false-positive case. Overall, they concluded that MRI more accurately predicted the presence or extent of disease in 50% of patients evaluated.24

Rodenko et al.25 performed an elegant study in which 20 mastectomy specimens were serially sectioned in a sagittal plane and compared with sagittal images of the respective patient’s preoperative MRI. The authors were able to demonstrate excellent correlation between MRI and pathology, with 85% agreement by size and location, compared with 27% to 36% with mammography alone. In addition, the MRIs were read by three independent observers with 100% interobserver agreement, compared with 86% to 93% for the corresponding mammograms. The authors did note that although it was able to detect unsuspected skin extension not seen by mammography, MRI seemed to overestimate the presence of chest-wall invasion. MRI suggested multifocal disease in 11 patients, and, in fact, only nine patients had multiple lesions. Multifocality was demonstrated in only one patient on mammography.

These studies support the use of MRI in detecting the primary lesion in patients with ILC and demonstrate the ability of MRI to define the extent of disease more accurately than conventional imaging. We were interested in determining the ability of MRI to detect unsuspected malignancy separate from the primary tumor site or in the contralateral breast in patients with known ILC. To provide better correlation between the MRI findings and pathology, we included only lesions that were distinct from the known primary tumor, were otherwise occult, and had undergone MRI-prompted localization and biopsy.

Our detection of additional sites of cancer separate from the primary tumor in 58% of patients undergoing ipsilateral biopsy exceeds the accepted range of 23% to 34% for mammographically detected BI-RADS 4 lesions undergoing biopsy.18 Six patients underwent benign ipsilateral biopsies, however, for a false-positive rate of 42%. It is therefore important to biopsy lesions seen on MRI to confirm additional disease, and mastectomy should not be recommended solely on the basis of MRI findings. In 6 (54%) of 11 patients, breast conservation was performed despite the finding of additional cancer; in these cases, the surgeon was able to excise the disease along with the primary lesion while achieving clear margins.

The increased rate of synchronous contralateral breast cancers in patients with ILC is well described.3 In a previous study from our institution of patients with known ILC undergoing random contralateral biopsies, we found contralateral invasive breast cancer in 10% and noninvasive cancers in 6% of patients.26 In this series, contralateral cancer was detected in 5 (25%) of 20 patients undergoing biopsy and in 5 (9%) of all patients (n = 53) who underwent contralateral MRI. This is consistent with a study from our institution that evaluated MRI screening of the contralateral breast in women with recently diagnosed breast cancer of any pathology.27 In that study, unsuspected cancer was found in 20% of women with a suggestive contralateral MRI lesion who were undergoing biopsy and in 5% of all women who underwent a contralateral breast MRI.

The use of MRI did lead to unnecessary biopsies in approximately one third (21 of 62) of patients imaged. In addition, many patients underwent additional surgeries after multifocal or multicentric disease was found. We are currently evaluating a protocol for MRI-guided core biopsy. This should lead to fewer unnecessary operations in these patients and, by better delineating the disease before surgery, help to plan one-stage surgical procedures.

Given the small sample size in our study, we could not expect to predict a subgroup of patients who were more likely to have additional disease detected by MRI. Most of our patients (84%) had mammograms described as dense or extremely dense. This might indicate a selection bias by the ordering physician, because our cohort comprised only a small portion of all women presenting with ILC during the study period. With a larger series, however, variables such as menopausal state, breast density on mammogram, biopsy type, pathologic subtype, and detection method of the primary cancer could be evaluated as possible predictors of additional cancer on MRI. It is not entirely clear what the role of MRI in the fatty breast is, and further prospective study with the entire population is warranted. To the best of our knowledge, this is the first study to correlate MRI abnormalities directly with pathologic evaluation of tissue obtained with MRI-guided needle-localization biopsy in a large cohort of patients with ILC. Our results support the prospective study of MRI in patients with known ILC to identify additional disease separate from the primary lesion, as well as to screen the contralateral breast.


   FOOTNOTES
 
Patients with invasive lobular cancer who underwent magnetic resonance imaging (MRI) of the breast for extent-of-disease work-up or contralateral screening were evaluated to determine the utility of MRI in detecting unsuspected malignancy.

Received for publication March 6, 2003. Accepted for publication July 6, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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