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Primary Inflammatory Carcinoma of the Breast

Retrospective Review of Mammographic Findings

¹ Division of Diagnostic Imaging, Box 57, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030.
² Department of Breast Medical Oncology, Box 56, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030.

Received November 30, 1998; accepted after revision July 27, 1999.

 
Address correspondence to A. C. Kushwaha.

Abstract

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OBJECTIVE. Our goal was to describe the mammographic characteristics of primary inflammatory carcinoma of the breast.

MATERIALS AND METHODS. We identified the medical records of 43 women who participated in a chemotherapy protocol for primary inflammatory carcinoma of the breast between 1994 and 1997. Mammograms were available for review in 26 women (age range, 34-78 years; mean age, 56 years). Two radiologists independently reviewed the 26 mammograms obtained before patients underwent treatment. A third observer was the final arbiter when needed.

RESULTS. Mammographic findings included skin thickening in 24 patients (92%), diffusely increased density in 21 patients (81%), trabecular thickening in 16 patients (62%), axillary lymphadenopathy in 15 patients (58%), architectural distortion or focal asymmetric density in 13 patients (50%), and nipple retraction in 10 patients (38%). Malignant-appearing calcifications were seen in six patients (23%), and a mass was seen in four patients (15%).

CONCLUSION. Diffuse mammographic abnormalities such as skin thickening, increased density, trabecular thickening, and axillary lymphadenopathy are common at presentation in patients with primary inflammatory carcinoma of the breast. Mammographic masses and malignant-appearing calcifications are uncommon manifestations of this disease.

Introduction

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Inflammatory carcinoma of the breast is an infrequent form of invasive breast carcinoma that presents with rapid clinical onset of warmth, erythema, and edema of the breast. The definition of inflammatory carcinoma of the breast differs between studies and has often included locally advanced breast carcinoma with secondary inflammatory changes, which usually presents as a large mass with localized skin changes adjacent to the underlying mass [1, 2]. Other reports on the mammographic appearance of inflammatory carcinoma of the breast have yielded conflicting findings. These discrepancies may result from differences in the clinical definition of inflammatory carcinoma of the breast. In their report published in 1995, Buzdar et al. [3] suggest that primary inflammatory carcinoma of the breast and locally advanced carcinoma with secondary inflammatory changes are two distinct clinical entities with differing incidence trends and survival curves.

In this study, we examined the mammographic findings at clinical presentation in patients with primary inflammatory carcinoma of the breast. We aimed to describe the mammographic characteristics of primary inflammatory carcinoma of the breast. We performed this study because our recent experience with mammography of inflammatory carcinoma differed from that of other investigators [1, 2].

Materials and Methods

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We retrospectively reviewed the medical records of 43 patients with primary inflammatory carcinoma of the breast who had enrolled in a chemotherapy protocol at one institution between 1994 and 1997. All patients fulfilled the three clinical criteria required to enter the treatment protocol: erythema or increased warmth of the breast, skin edema or peau d'orange, and wheals or ridging of the skin. Each patient was examined by a radiation oncologist, a surgeon, and a medical oncologist in a multidisciplinary planning clinic before initiation of therapy. A history of rapid onset of clinical signs within 3 months of presentation was required to distinguish primary inflammatory carcinoma of the breast from locally advanced carcinoma with secondary lymphatic invasion (Cristofanilli M et al., presented at the American Society of Clinical Oncology meeting, May 1998). Patients with distant metastases were excluded from the treatment protocol (Cristofanilli M et al., ASCO meeting, May 1998). Mammograms obtained before the patients underwent treatment were available for review in 26 women, who ranged in age from 34 to 78 years (mean, 56 years). Seventeen women had right breast involvement, including one woman who had bilateral cancer at presentation with inflammatory carcinoma of the breast on the right side only. Nine women had left breast involvement. Pathology reports were available for all 26 patients.

Two radiologists independently reviewed the mammograms without knowledge of the clinical findings. The mammograms were assessed for skin thickening, diffusely increased density, trabecular thickening, vascular engorgement, nipple retraction, architectural distortion, masses, calcifications, and axillary lymphadenopathy. The findings were tabulated, and a third observer served as an arbiter when the two observers did not agree on a specific mammographic finding. During the mammogram review sessions, magnifying glasses, a light, and an oval mask were used to facilitate evaluation of the skin and the subcutaneous tissues.

Results

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The most frequent mammographic finding was skin thickening, which was present in 24 patients (92%) (Fig. 1). Diffusely increased density was present in 21 patients (81%) (Fig. 2A, 2B). Trabecular thickening was seen in 16 patients (62%) (Fig. 3A, 3B), of whom seven had trabecular thickening in the subcutaneous tissues only (Fig. 4). Fifteen patients (58%) had axillary lymphadenopathy (Fig. 2A, 2B), 13 patients (50%) had an area of architectural distortion or a focal asymmetric density (Fig. 2A, 2B), and 10 patients (38%) had nipple retraction. Six patients (23%) had malignant-appearing calcifications and eight patients (31%) had indeterminate calcifications. Indeterminate calcifications were not obviously malignant-appearing (fine linear or pleomorphic) or associated with benign disease (round or punctate) and could not be further characterized on the mammograms available for review. A mass was seen in four patients (15%) (Fig. 5A, 5B). Skin thickening in the medial aspect of the contralateral breast was seen in one patient (4%). Increased vascularity was not seen in any patients.

View larger version (100K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. —32-year-old woman with inflammatory carcinoma of the breast who presented with swollen left breast. Craniocaudal mammogram shows diffuse skin thickening (arrows).

View larger version (104K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —47-year-old woman who presented with 2-month history of breast erythema, ridging, peau d'orange, and poorly defined 6 x 5 cm palpable mass in right upper inner quadrant extending into right lower inner quadrant. Mediolateral oblique mammograms of the right (A) and left (B) breasts show diffusely increased density of right breast, architectural distortion in upper right breast (straight arrow, A), and abnormal axillary lymph node (curved arrow, A).

View larger version (98K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —47-year-old woman who presented with 2-month history of breast erythema, ridging, peau d'orange, and poorly defined 6 x 5 cm palpable mass in right upper inner quadrant extending into right lower inner quadrant. Mediolateral oblique mammograms of the right (A) and left (B) breasts show diffusely increased density of right breast, architectural distortion in upper right breast (straight arrow, A), and abnormal axillary lymph node (curved arrow, A).

View larger version (100K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —Trabecular thickening in 60-year-old woman with breast carcinoma who presented with axillary lymphadenopathy. Craniocaudal mammograms of right (A) and left (B) breasts show diffusely thickened Cooper's suspensory ligaments in left breast.

View larger version (95K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —Trabecular thickening in 60-year-old woman with breast carcinoma who presented with axillary lymphadenopathy. Craniocaudal mammograms of right (A) and left (B) breasts show diffusely thickened Cooper's suspensory ligaments in left breast.

View larger version (70K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4. —Trabecular thickening in subcutaneous breast tissue of 58-year-old woman who presented with 1-month history of left breast enlargement with erythema of inferior aspect of breast. Craniocaudal mammogram shows thickened reticular network of lymphatics in subcutaneous region (arrows).

View larger version (66K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A. —Inflammatory carcinoma of the breast with mass in 57-year-old woman who presented with erythema of right breast and slight nipple inversion. Craniocaudal mammogram of right breast shows diffusely increased density with 1.4-cm spiculated mass in outer breast (arrow).

View larger version (89K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B. —Inflammatory carcinoma of the breast with mass in 57-year-old woman who presented with erythema of right breast and slight nipple inversion. Mediolateral oblique mammogram of right breast shows 1.4-cm spiculated mass in upper breast (arrow) and abnormal lymph node in axilla (curved arrow).

Discussion

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Inflammatory carcinoma of the breast accounts for 1% of breast cancers [4]. The clinical diagnosis of primary inflammatory carcinoma of the breast requires erythema, warmth, skin edema, and dermal ridging with rapid clinical onset. Inflammatory carcinoma of the breast is usually poorly differentiated infiltrating ductal carcinoma. In the typical case, histopathologic evaluation of the skin reveals tumor emboli, dilated dermal lymphatic channels, and a lymphocytic reaction in the dermis localized around dilated vascular channels [5]. In some cases, however, dermal vascular or lymphatic invasion is inconspicuous. In this study, dermal lymphatic invasion or vascular invasion was seen in 13 patients (50%).

In the TNM staging system of the American Joint Committee on Cancer and the International Union Against Cancer, inflammatory carcinoma of the breast is classified as a stage IIIB breast carcinoma, and locally advanced carcinoma of the breast is also classified as stage IIIB. Although the 5-year 50% disease-free survival for patients with primary inflammatory carcinoma of the breast and for those with other stage IIIB breast carcinoma is similar (26-28 months), the 5-year 50% overall survival is significantly worse for patients with primary inflammatory carcinoma of the breast than for those with locally advanced carcinoma of the breast (36-40 months versus 50-52 months) [3, 6]. This discrepancy is probably a result of more aggressive treatment and subsequent morbid complications from therapy. At our institution, a distinction is made between primary inflammatory carcinoma of the breast and secondary inflammatory carcinoma of the breast in all treatment protocols.

The mammographic characteristics of inflammatory carcinoma of the breast identified in this study were diffuse and often subtle. Skin thickening (Fig. 1) and diffusely increased density (Fig. 2A, 2B) were the most common findings, seen in 92% and 81% of patients, respectively. In most cases, proper use of a mask and a bright light was necessary to detect skin thickening as well as trabecular thickening and nipple retraction. Diffusely increased density, skin edema, and trabecular thickening are mammographic manifestations of the edema and lymphatic obstruction in inflammatory carcinoma of the breast. Contralateral skin thickening was seen in the medial breast of one patient. This patient had progressive disease while receiving neoadjuvant chemotherapy and died with liver metastases 6 months after the initial diagnosis of inflammatory carcinoma of the breast. The contralateral skin thickening may have represented crossed dermal metastases.

Axillary lymphadenopathy was seen in 15 patients (58%) (Fig. 2A, 2B). Architectural distortion or focal asymmetric densities were present in 13 patients (50%). We defined architectural distortion as distortion of the normal structures of the breast with no definite mass visible [7] (Fig. 2A, 2B). We defined a focal asymmetric density as asymmetry of tissue density with a similar shape on two views, but completely lacking borders and the conspicuity of a true mass [7].

In 1994, Dershaw et al. [1] reviewed the mammographic findings in inflammatory carcinoma of the breast from a group of 22 patients at Memorial Sloan-Kettering Cancer Center. In that study, 21 of 22 patients had masses or malignant-appearing calcifications identified on mammography. In 1997, Tardivon et al. [2] reviewed 92 cases: 57 patients had secondary inflammatory carcinoma of the breast and 35 patients had primary inflammatory carcinoma of the breast. These investigators did not separate the two clinical entities. In addition, these investigators identified opacities or malignant-appearing calcifications in 74% of patients.

The main difference between our study and those of Dershaw et al. [1] and Tardivon et al. [2] is the frequency with which masses and malignant-appearing calcifications were identified. In our study, masses, malignant-type calcifications, or both were present in 10 patients (38%). However, Dershaw et al. and Tardivon et al. identified masses, malignant-appearing calcifications, or both in 95% and 74% of their patients, respectively. The disparity between these findings and ours may result from their inclusion of patients in their study populations with locally advanced breast cancer who had preexisting clinical masses. In the study by Tardivon et al., 97% of patients presented with clinically palpable masses. Dershaw et al. described palpable masses in 82% of patients. In our study population, 12 patients (46%) presented with clinically palpable masses.

Our results agree with those reported in studies of inflammatory carcinoma of the breast by other investigators. For instance, in a study by Droulias et al. [8], 33 patients underwent mammography, and skin thickening was seen in all patients. On mammography, Droulias et al. found generally increased density in 27 patients (82%) and identified masses in 11 patients (33%). In the series of 12 patients described by Berger [9], increased density, skin thickening, and prominent subcutaneous lymphatic obstruction were the most common findings in inflammatory carcinoma of the breast. Berger did not discuss the frequency of masses or calcifications.

The concept of differentiating primary from secondary inflammatory carcinoma is relatively new, but this distinction is likely important for patient treatment and prognosis. In our study of primary inflammatory carcinoma, we found a lower incidence of clinically palpable masses, mammographically visible masses, and malignant-appearing calcifications than did investigators who included both primary and secondary inflammatory carcinoma cases in their studies. Our results support the concept that primary and secondary inflammatory carcinoma of the breast are two different disease processes. Further research will be necessary to determine the importance of distinguishing between primary and secondary inflammatory carcinoma.

Acknowledgments
 
We thank Mary Ann Waggoner for her secretarial support in preparation of this manuscript.

References

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4. Chang S, Parker SL, Pham T, Buzdar AU, Hursting SD. Inflammatory breast carcinoma incidence and survival: the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute, 1975-1992. Cancer 1998;82:2366-2372[Medline]
5. Rosen PP. Invasive mammary carcinoma. In: Harris JR, Lippman ME, Morrow M, Hellman S, eds. Diseases of the breast. Philadelphia: Lippincott-Raven, 1996:393-444
6. Koh EH, Buzdar AU, Ames FC, et al. Inflammatory carcinoma of the breast: results of a combined-modality approach—M.D. Anderson Cancer Center experience. Cancer Chemother Pharmacol 1990;27:94-100[Medline]
7. BI-RADS Committee. Illustrated breast imaging reporting and data system (Illustrated BI-RADS), 3rd ed. Reston, VA: American College of Radiology, 1998:121-139
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