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DOI: 10.1148/radiol.2211991748
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(Radiology. 2001;221:132-136.)
© RSNA, 2001

Diagnosis Please

Case 39: Invasive Lobular Carcinoma1

Harmindar K. Gill, MD 2 and Wendie A. Berg, MD, PhD

1 From the Department of Radiology (H.K.G., W.A.B.) and Greenebaum Cancer Center (W.A.B.), University of Maryland School of Medicine, 419 W Redwood St, Ste 110, Baltimore, MD 21201. Received September 27, 1999; revision requested November 1; final revision received July 18, 2000; accepted August 2. Address correspondence to W.A.B. (e-mail: waberg@umaryland.edu).

Index terms: Breast, MR, 00.1214 • Breast neoplasms, 00.327 • Diagnosis Please


   HISTORY
TOP
 HISTORY
IMAGING FINDINGS
 DISCUSSION
 REFERENCES
 
The patient was a 43-year-old woman, otherwise healthy, who presented with a palpable mass in the entire upper right breast, centered at the 12-o’clock position. She also had vague thickening of the upper left breast at the radiologist’s clinical examination.


   IMAGING FINDINGS
TOP
 HISTORY
 IMAGING FINDINGS
DISCUSSION
 REFERENCES
 
Preliminary clinical examination findings demonstrated a broad, approximately 7 x 8-cm area of palpable thickening in the upper right breast extending from the 9- through the 3-o’clock position. Bilateral mediolateral oblique and craniocaudal mammograms (Fig 1a, Fig 1b) and spot compression of the palpable area in the right breast (Fig 1c) showed dense tissue with no discrete abnormalities. Sonography of the upper right breast revealed numerous irregular hypoechoic masses from the 11- to the 3-o’clock position that were not discrete and demonstrated moderate posterior acoustic shadowing suggestive of invasive lobular carcinoma (ILC) (Fig 2a). Sonography of the left breast was also performed in a region of mildly palpable thickening felt by the radiologist at the 12-o’clock position, and the findings included an indistinct, approximately 17-mm focus of decreased echogenicity with moderate posterior acoustic shadowing (Fig 2b) that was also considered suspicious for cancer.



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  		Figure 1a. Bilateral (a) mediolateral oblique and (b) craniocaudal mammograms show dense breasts bilaterally with no discrete abnormal findings. A metallic marker was placed on the palpable abnormality in the right breast. (c) Spot compression of the palpable abnormality in the right breast shows dense tissue with no discrete findings.

 


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  		Figure 1b. Bilateral (a) mediolateral oblique and (b) craniocaudal mammograms show dense breasts bilaterally with no discrete abnormal findings. A metallic marker was placed on the palpable abnormality in the right breast. (c) Spot compression of the palpable abnormality in the right breast shows dense tissue with no discrete findings.

 


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  		Figure 1c. Bilateral (a) mediolateral oblique and (b) craniocaudal mammograms show dense breasts bilaterally with no discrete abnormal findings. A metallic marker was placed on the palpable abnormality in the right breast. (c) Spot compression of the palpable abnormality in the right breast shows dense tissue with no discrete findings.

 


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  		Figure 2a. (a) Antiradial sonogram of the palpable abnormality in the right breast reveals numerous irregular hypoechoic masses from the 11- to the 3-o’clock position with moderate posterior acoustic shadowing, the largest of which is shown (arrow). Results of a core-needle biopsy showed ILC. (b) Antiradial sonogram of the mildly palpable thickening of the left breast reveals an indistinct approximately 17-mm focus of decreased echogenicity (arrow) with moderate posterior acoustic shadowing, which showed fibrosis at core-needle biopsy.

 


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  		Figure 2b. (a) Antiradial sonogram of the palpable abnormality in the right breast reveals numerous irregular hypoechoic masses from the 11- to the 3-o’clock position with moderate posterior acoustic shadowing, the largest of which is shown (arrow). Results of a core-needle biopsy showed ILC. (b) Antiradial sonogram of the mildly palpable thickening of the left breast reveals an indistinct approximately 17-mm focus of decreased echogenicity (arrow) with moderate posterior acoustic shadowing, which showed fibrosis at core-needle biopsy.

 
Sonographically guided core-needle biopsy of the suspicious mass at the 12-o’clock position in the right breast with a 14-gauge automated biopsy gun revealed ILC. Sonographically guided core-needle biopsy of the suspicious area in the left breast, which revealed fibrosis, was also performed with a 14-gauge automated gun.

A contrast material–enhanced magnetic resonance (MR) imaging examination was performed 42 days after the biopsy to evaluate the extent of disease and to plan treatment. Findings of MR imaging examination showed lobulated marked early enhancement of nearly the entire upper right breast that measured 7.3 x 5.5 x 5.0 cm and extended below the level of the nipple (Fig 3), which was compatible with cancer. The area in question in the left breast showed negligible enhancement, concordant with the core-needle biopsy finding of fibrosis.



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  		Figure 3. Coronal enhanced spoiled gradient-recalled MR image of both breasts (repetition time msec/echo time msec, 11/2; flip angle, 30°) 90 seconds after intravenous administration of 0.1 mmol per kilogram of body weight of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) shows lobulated marked early enhancement (arrowheads) of nearly entire upper right breast measuring 7.3 x 5.5 x 5.0 cm and extending below the level of the nipple. The 12-o’clock region in the left breast shows minimal enhancement (arrow). The same findings were evident on subtraction images. At bilateral mastectomy, ILC was confirmed throughout the upper right breast, and dense fibrosis was confirmed in the left breast.

 

   DISCUSSION
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 HISTORY
 IMAGING FINDINGS
 DISCUSSION
REFERENCES
 
Infiltrating or invasive lobular carcinoma is the diagnosis in 7%–10% of all breast cancer (1–3). ILC is characterized microscopically by similar cells forming linear invasive columns (2) that are loosely dispersed, whereas invasive ductal carcinoma (IDC) is more typically a discrete mass. ILC frequently invades the normal tissues without invoking the vigorous desmoplastic response that usually accompanies IDC. Cells of ILC often encircle ducts, thus preserving the architecture of the ducts (3). These histopathologic features tend to produce more subtle imaging findings with ILC than with IDC.

Mammographically, as in our patient, often no focal mass or clustered microcalcifications are evident, particularly in dense parenchyma. As a result, ILC tends to be larger than IDC at diagnosis, with an average size of 29 mm compared with 23 mm for IDC in one series (4). Hilleren et al (5) retrospectively reviewed 137 cases of ILC and found that 22 (16%) appeared mammographically occult or benign. Of those visible mammographically, more than one-third were seen as vague asymmetries, poorly defined opacities, or architectural distortions (5). In two series, ILC was better visualized in the craniocaudal view (5,6). Calcifications are often the earliest manifestation of ductal carcinomas but are uncommon in ILC. Calcifications were seen in only three (2%) of 137 ILCs in the series of Hilleren et al (5), in two (4%) of 52 in the series of Helvie et al (6), and in 83 (24%) of 341 in the series of LeGal et al (7). By comparison, calcifications were seen in 1,251 (41%) of 5,554 IDC in the latter series (7).

Because of the limitations of mammography in detecting ILC, other modalities, such as sonography and MR imaging, are being used in evaluating clinically suspicious findings and known cancers to assess the extent of disease. Paramagul et al (8) retrospectively reviewed the sonograms in 19 patients with ILC and found that all lesions were depicted, but only 13 (68%) appeared suspicious for malignancy. In a more recent and much larger series by Butler et al (9), 208 cases of ILC were reviewed. Of the 208 cases of ILC, 81 (39%) were mammographically subtle or invisible (9), and 71 (88%) of these 81 ILC were depicted sonographically; average tumor size was 2.5 cm. The most common sonographic appearance was a heterogeneous, hypoechoic mass with angular or ill-defined margins and posterior acoustic shadowing, which was seen in 49 (69%) of 71 sonographically visible cases (as seen in our patient). In another 12 (17%) of 71, focal shadowing without a discrete mass was revealed, and in 10 (14%) of 71, the tumor appeared as a lobulated, well-circumscribed mass (9).

As stated previously, there is considerable limitation in the depiction of lobular carcinoma at mammography, since it often does not manifest as a definite mass or as microcalcifications, and it can appear benign sonographically. As such, contrast-enhanced MR imaging has been increasingly proposed as an adjunctive modality for depiction of ILC as well as of IDC, and it is particularly useful for defining the extent of disease within the breast prior to definitive treatment (10,11). Rodenko et al (12) reported MR imaging and mammography results in 20 patients with ILC. The extent of disease at pathologic examination correlated with that predicted with MR imaging findings in 85% of patients, compared with only a 32% correlation (P < .001) with mammographic studies (12). Similarly, Weinstein et al (13) performed preoperative MR imaging in 18 patients with ILC and found that in 16 (89%), the extent of disease identified at MR imaging correlated with that identified at pathologic examination. Further, the extent of tumor was correctly depicted with only MR imaging in 7 (39%) of 18 cases, with both mammography and MR imaging in nine (50%) of 18 cases, and with neither in one (6%) of 18 cases (13). Of the eight patients with more extensive tumor on the basis of MR imaging findings, surgical treatment was altered in all eight (100%) patients (13). Preoperative assessment with MR imaging may be particularly important for ILC, since the rate of positive margins at initial excision is higher than it is for IDC, and this rate exceeded 50% in one recent series (14). As in the patient presented, far greater size of tumor manifested by clinical and MR findings compared with sonography or mammography findings favors a diagnosis of ILC over IDC.

In earlier literature, researchers advocated mastectomy and axillary dissection in patients with ILC because of a high incidence of multicentricity and bilaterality (15,16). Findings in case studies by Mate et al (15) and du Toit et al (16) suggested that the rate of local recurrence after conservative surgery and radiation therapy was high, with a range of 25%–42% of patients with ILC, but the studies were limited by small numbers of patients. Investigators in more recent studies of stages I and II ILC report local recurrence rates of 3%–5% at 5 years and 7% at 10 years (17–20); these rates are comparable with those for IDC. Thus, breast-conserving surgery followed by radiation therapy appears to be appropriate for stage I or II ILC, provided the tumor size is accurately depicted preoperatively.

There is a greater rate of contralateral breast cancer in ILC compared with IDC. However, the risk does not warrant "mirror-image" contralateral biopsies or prophylactic contralateral mastectomy. The reported rate of contralateral breast cancer in most series is low in the first 5 years. In the largest series to date, Sastre-Garau et al (21) analyzed 726 cases of ILC and found a 5-year rate of bilateral cancer of 8% (4% synchronous and 4% metachronous tumors). Similarly, Lee et al (22) found a 10% rate of bilateral cancer after 10 years and interestingly showed a survival benefit in those with unilateral disease who underwent prophylactic contralateral mastectomy. In several other series, a 6.9% incidence of contralateral cancer was noted (4,17,19,20).

In our patient, the MR findings were equivocal in the contralateral breast, with a 70% increase in signal intensity in the first 90 seconds in a patchy distribution (Fig 3). Typically, malignancies show at least an 80% increase in signal intensity (23). In several series, the sensitivity of MR imaging in patients with known or suspected invasive cancer has been reported at 94%–96% (10,11,24), although the sensitivity for ductal carcinoma in situ may be less, with 10 (77%) of 13 depicted in one study (25). Indeed, ductal carcinoma in situ can show patchy or regional enhancement as was seen here (25,26). The negative predictive value of MR imaging is not fully established. The absence of enhancement in a visualized mass is unusual and predicts benignity, as does enhancement less than that of parenchyma, with a negative predictive value of 93%–100% (27,28).

Further, the sonographic findings were suspicious in the contralateral breast, and a diagnosis of focal fibrosis on the basis of findings of core-needle biopsy was not accepted as definitive. Indeed, Venta et al (29) describe focal fibrosis as typically manifesting as a circumscribed mass: marginal spiculation should be considered discordant with a diagnosis of fibrosis on the basis of findings of core-needle biopsy. Further, Berg et al (30) reported that 22 (32%) of 68 core specimens showing only focal fibrosis had actually missed the lesion and that such a result was particularly problematic in dense breast tissue. As such, this patient chose bilateral mastectomy out of her understanding of the limitations of imaging and even core-needle biopsy in depicting both current and any subsequent disease.

As documented at follow-up MR imaging, our patient failed to respond to three cycles of neoadjuvant chemotherapy with the following: doxorubicin hydrochloride (Adriamycin; Pharmacia & Upjohn, Kalamazoo, Mich), cyclophosphamide (Cytoxan; Bristol-Meyers Squibb, Princeton, NJ), and docetaxel (Taxotere; Aventis Pharmaceuticals, Bridgewater, NJ). Histopathologic findings confirmed extensive contiguous ILC in the entire upper right breast and extending to the 8-o’clock radius, consistent with the extent depicted at MR imaging, with six of six lymph nodes metastatic. Dense fibrosis was confirmed throughout the left breast.

From the clinical, mammographic, and sonographic features, the other differential considerations for the right breast in this case included IDC, fibrosis, and diabetic mastopathy. Of these, the most likely was IDC, since it showed marked enhancement at MR imaging and shadowing at sonography, and IDC can be mammographically occult. As mentioned, the discrepancy in size on the basis of clinical and MR imaging findings, compared with mammographic and sonographic appearances, favors a diagnosis of ILC. Fibrosis may have similar findings sonographically and mammographically but will not show intense enhancement at MR imaging (31). Diabetic mastopathy will have similar findings clinically, mammographically, and sonographically (32), but our patient had no history of diabetes.

In conclusion, ILC is difficult to diagnose mammographically, and the use of both sonography and MR imaging to establish diagnosis is encouraged. Sonography is valuable in depicting mammographically subtle or occult ILC and in guiding biopsy but may underestimate the tumor size. MR imaging shows particular value in helping to diagnose ILC and to define the extent of disease prior to definitive treatment.

Our congratulations to the 50 individuals who submitted the most likely diagnosis (invasive lobular carcinoma) for Diagnosis Please, Case 39. The names and locations of the individuals, as submitted, are as follows:

Nabil Ammouri, MD, Zahle, Lebanon
William W. Beckett, Jr, MD, Dothan, Ala
A. R. Belknap, MD, Butte, Mont
Grazia Bitti, MD, Cagliari, Italy
R. James Brenner, MD, FACR, Santa Monica, Calif
Michael P. Buetow, MD, Okemos, Mich
Eithne Burke, MB, Raleigh, NC
Sinan Cakirer, Atasehir, Istanbul, Turkey
Tirso Cascajares Murillo, Los Mochis, Sin, Mexico
Daniel M. Chernoff, MD, Saratoga Springs, NY
Marc G. de Baets, MD, Lugano, Switzerland
Evaldo de Sousa Nóbrega, João Pessoa, Brazil
Kemal Demir, MD, Ataköy, Istanbul, Turkey
Dra. Estela Di Nella, Mar del Plata, Argentina
Arie Franco, MD, PhD, Livingston, NJ
Milton R. Fuentealba, MD, General Roca, Rio Negro, Argentina
Akira Fujikawa, Tokyo, Japan
Mark A. Guenin, MD, Harrisburg, Pa
Flavius Guglielmo, MD, Basking Ridge, NJ
Marc J. Homer, MD, Boston, Mass
Masako Kataoka, Sakyo, Kyoto, Japan
Douglas S. Katz, MD, Mineola, NY
Kevin M. Kelly, MD, Pasadena, Calif
Stefanos Lachanis, MD, Athens, Greece
Eduardo Lassalle, MD, Quilmes, Argentina
Paul Madsen, MD, Greendale, Wis
Tatsuya Ya Magen, Fukui, Japan
Tom Mahon, MD, Los Angeles, Calif
Bernard F. Masters III, MD, Mount Pleasant, SC
Manabu Minami, MD, Tokyo, Japan
Chuck Nicolette, Odessa, Tex
Sanford M. Ornstein, MD, Phoenix, Ariz
Dr. Roberto E. Perez Gautrin, Hermosillo, Sonora, Mexico
Shawn P. Quillin, MD, Charlotte, NC
Enrique Remartinez Escobar, MD, Melilla, Spain
Dennis Scholl, Gig Harbor, Wash
Steven M. Schultz, MD, Fort Worth, Tex
Matt Shapiro, MD, Lowell, Mass
Taro Shimono, MD, Osaka, Japan
Dr. Shivanand, New Delhi, India
Eleanor Smergel, MD, Philadelphia, Pa
Arlene Sussman, MD, Mineola, NY
Tapani Tikkakoski, MD, Kokkola, Finland
Martha K. Uhler, MD, San Antonio, Tex
Christopher Vittore, MD, Rockford, Ill
Edward Williams, Jersey, Channel Islands, United Kingdom
David J. Wright, MD, Lake Oswego, Ore
Stanko Yovichevich, MD, Sydney, New South Wales, Australia
Joe Yut, Olathe, Kan
Jeffrey H. Zapolsky, Oshkosh, Wis


   FOOTNOTES
 
2 Current address: Johns Hopkins University School of Medicine, Baltimore, Md. Back

Part 1 of this case appeared 4 months previously and may contain larger images.


   REFERENCES
TOP
 HISTORY
 IMAGING FINDINGS
 DISCUSSION
 REFERENCES
 

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