ARTICLE IN PRESS. Pathology Research and Practice 203 (2007)
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1 ARTICLE IN PRESS Pathology Research and Practice 203 (2007) TEACHING CASES Malignant adenomyoepithelioma of the breast with matrix production may be compatible with one variant form of matrix-producing carcinoma: A case report Kuniyuki Oka a,, Norimasa Sando b, Takuya Moriya c, Yasushi Yatabe d a Pathology, Mito Saiseikai General Hospital, Futabadai, Mito, Ibaraki , Japan b Surgery, Mito Saiseikai General Hospital, Mito, Ibaraki c Hospital Pathology, Tohoku University, Sendai, Miyagi d Department of Pathology Molecular Diagnostics, Aichi Cancer Center Hospital, Nagoya, Aichi, Japan Received 16 November 2006; accepted 18 April 2007 Abstract We examined a 77-year-old woman who suffered from a left breast tumor. She had undergone right mastectomy for invasive ductal carcinoma at 68 years of age, and rectal resection for mucinous carcinoma at the age of 74 years. The left breast tumor measured cm. Neoplastic cells consisted of atypical epithelial and myoepithelial cells. The former cells were polygonal and large. They were located in the periphery of the tumor, arranged in a ductal pattern, and expressed cytokeratins, S-100 protein, maspin, and MIC2. The latter cells were composed of dark cells which proliferated in a periductal pattern, and stellate cells which were located in the center of the tumor. They invaded the chondromyxoid tissues, and proliferated in a lace-like pattern. Atypical myoepithelial cells expressed vimentin, S-100 protein, maspin, and MIC2. We conclude that malignant adenomyoepithelioma of the breast with matrix production might be compatible with a variant form of matrix-producing carcinoma. r 2007 Elsevier GmbH. All rights reserved. Keywords: Malignant adenomyoepithelioma; Matrix-producing metaplastic carcinoma; Breast; Myoepithelial differentiation Introduction Metaplastic breast carcinomas comprise a heterogenous group of neoplasms with unknown histogenesis [2]. Wargotz and Norris [17] have subdivided metaplastic breast carcinomas into the following subtypes: matrixproducing carcinomas, metaplastic carcinomas with osteoclastic giant cells, and others: spindle cell carcinomas, carcinosarcomas, and squamous cell carcinomas of ductal origin. These five metaplastic breast carcinomas Corresponding author. Tel.: ; fax: address: oka-k@gb3.so-net.ne.jp (K. Oka). had no adenomyoepitheliomatous areas in any of their large series [17]. Matrix-producing metaplastic carcinomas are overt carcinomas and show a direct transition from glandular components to cartilaginous and/or osseous components or stromal matrices without an intervening spindle cell zone or osteoclastic giant cells [17]. Adenomyoepithelioma is usually benign and is predominantly of myoepithelial origin with additional glandular elements [11]. Malignant adenomyoepithelioma is rare and also biphasic, with myoepithelial, glandular and, rarely, sarcomatous elements [12]. The case described here is a 77-year-old woman who suffered from a left breast tumor. We discuss the /$ - see front matter r 2007 Elsevier GmbH. All rights reserved. doi: /j.prp
2 600 ARTICLE IN PRESS K. Oka et al. / Pathology Research and Practice 203 (2007) relationship between malignant adenomyoepithelioma of the breast with matrix-production and matrixproducing breast carcinoma, and report on neoplastic cells with a myoepithelial or basal phenotype. Case report and pathological results A Japanese woman having developed a right breast tumor underwent a right mastectomy at the age of 68 years in July She was diagnosed to have an invasive ductal carcinoma and scirrhous carcinoma. Furthermore, at the age of 74, a rectal tumor was resected in September 2002, diagnosed as mucinous carcinoma with lymph node metastases. She had a cerebral infarction attack in autumn In June 2005, the 77-year-old woman noticed a left breast tumor and underwent a core needle biopsy, followed by a left mastectomy in July A metastatic tumor in the thoracic wall was resected in February In March 2007, she is alive. Core needle biopsy revealed invasive ductal carcinoma. On operation, the tumor was located in the lower lateral quadrant area of the left breast and measured cm. The tumor was multilobulated, had circumscribed borders, appeared to be incompletely surrounded by a thin band of connective tissue, and infiltrated into the adjacent fatty tissue. Neoplastic cells consisted of atypical epithelial and myoepithelial cells invading the chondromyxoid tissue (Fig. 1a). The atypical epithelial cells were of large polygonal shape with prominent nucleoli, located in the periphery of the tumor, arranged in a ductal or acinar pattern (Fig. 1b), and expressed wide-spectrum keratin (Fig. 2a), cytokeratins (AE1/AE3, KL-1, CAM5.2, CK7), S-100 protein (Fig. 3a), maspin (Fig. 3b), and MIC2 (Fig. 3c). The atypical myoepithelial cells consisted of dark cells (Fig. 1b) and stellate cells (Fig. 1c), and had dense chromatin. The atypical dark cells were located in the periphery of the tumor, and proliferated in a periductal or myoepithelial-like pattern (Fig. 1b). The atypical stellate cells were located in the center of the tumor, and proliferated in a lace-like pattern in chondromyxoid matrix (Fig. 1c). These atypical myoepithelial cells expressed vimentin (Fig. 2b), S-100 protein (Fig. 3a), maspin (Fig. 3b), and MIC2 (Fig. 3c). Abnormal mitotic figures and apoptosis were frequently observed. A regional lymph node and a thoracic subcutaneous tumor proved to be metastases originating from the neoplastic cells. The extracellular matrix expressed alcian blue and colloidal iron stains, type IV collagen, fibronectin, and laminin, but not von Kossa stain and osteopontin. From the pathological findings, we diagnosed this lesion as a malignant adenomyoepithelioma with matrix production. Table 1 summarizes the morphologic, histochemical, and immunohistochemical findings of Fig. 1. Tumor consisted of a ductal pattern formed by atypical epithelial and myoepithelial cells (right area) and a lace-like pattern formed by atypical stellate cells that invaded the chondromyxoid tissue (left area) (1a). x100. Atypical epithelial cells showed a duct-like appearance. Atypical myoepithelial cells showed a periductal arrangement (1b, right area in Fig. 1a) Atypical stellate cells invaded the chondromyxoid tissue (1c, left area in Fig. 1a) Hematoxylin eosin stain.
3 ARTICLE IN PRESS K. Oka et al. / Pathology Research and Practice 203 (2007) Fig. 2. Atypical epithelial cells located in inner layer expressed wide spectrum keratin (2a). Atypical dark cells located in outer layer expressed vimentin (2b). Immunostain atypical epithelial and myoepithelial cells and the extracellular matrix. Discussion The present tumor consisted of atypical epithelial cells; ductal large cells, and atypical myoepithelial cells; periductal dark cells and stellate cells, and the chondromyxoid matrix in the central areas. It was absent for intervening spindle cells or osteoclastic giant cells. The present case was similar to that of matrix-producing metaplastic carcinoma. In general, matrix-producing metaplastic carcinoma of the breast had no adenomyoepitheliomatous areas [17]; therefore, we diagnosed the present case as malignant adenomyoepithelioma with matrix production. To our knowledge, two reports about malignant adenomyoepithelioma showing matrix production have already been described [12,13]. Sugano et al. [13] have Fig. 3. Atypical epithelial cells and atypical dark and stellate cells expressed S-100 protein (3a), maspin (3b), and MIC2 (3c). Immunostain reported two cases of malignant adenomyoepithelioma of the breast with a non-tubular and matrix-producing variant. Their cases showed marked myoepithelial differentiation without overt tubular differentiation, and their patterns were quite different from those of matrix-producing metaplastic carcinoma or malignant
4 602 ARTICLE IN PRESS K. Oka et al. / Pathology Research and Practice 203 (2007) Table 1. Summary of the morphologic, histochemical, and immunohistochemical findings of atypical cells and matrix Epithelial Myoepithelial Ductal Dark Stellate Matrix Mitosis + + PAS + + Alcian blue Colloidal iron Fibronectin + Laminin + Type IV collagen + WSK EMA + Ber-EP4 7 AE1/AE3 + + KL-1 + CAM5.2 + CK7 + CK20 Vimentin + + S-100 protein Maspin a-sma p63 CD10 CK5/6 CK14 + CK17 34bE EGFR (HER1) HER2 ER PgR MIC2 (CD99) c-kit (CD117) PAS: periodic acid-schiff, WSK: wide spectrum keratin, EMA: epithelial membrane antigen, a-sma: a-smooth muscle actin, CK: cytokeratin, ER: estrogen receptor, PgR: progesterone receptor, EGFR: epidermal growth factor receptor. adenomyoepithelioma. The morphology of their tumors was somewhat different from that of the present tumor. In addition, in their cases, both polygonal and spindled cells expressed EMA, vimentin, and S-100 protein. However, in the present case, atypical epithelial cells expressed keratin, EMA, and S-100 protein. On the other hand, atypical myoepithelial cells expressed vimentin and S-100 protein. The differential diagnosis between these two diseases was difficult. The present case suggests an intimate association between matrixproducing metaplastic carcinoma and malignant adenomyoepithelioma with matrix-producing variant. Simpson et al. [12] have reported on a 50-year-old woman whose original tumor was diagnosed as an adenomyoepithelioma, and whose recurrent tumor was recognized as a sarcoma composed of mature and immature bone, osteoid, and partly calcified and dense collagen tissue. Their case was also somewhat different from ours. Matrix production, including cartilage, may be present in a variety of other breast tumors, including fibroadenoma, hamartoma, intraductal papilloma, ductal adenoma, and some malignant tumors, including phyllodes tumor and metaplastic carcinoma. Pleomorphic adenoma and carcinoma ex-pleomorphic adenoma in salivary gland-like tumors of the breast may be indistinguishable from a matrix-producing metaplastic carcinoma. Hayes et al. [1] have described three cases of carcinoma ex-pleomorphic adenoma of the breast. These showed transition from benign areas through low- or intermediate-grade areas to high-grade areas. The present case was a typically uniformly high-grade tumor throughout. First, reports that matrix-producing metaplastic carcinomas of the breast expressed S-100 protein have already been described [2,6,17]. Wargotz and Norris [17], investigating a large series of 26 matrix-producing metaplastic carcinomas, reported that the overt carcinoma cells tended to show diffuse S-100 immunoreactivity and that the metaplastic cells within the matrix had diffuse S-100 immunorreactivity. Popnikolov et al. [6] have also reported that eight of nine matrixproducing metaplastic carcinoma cases expressed S-100 protein. Next, maspin, known as mammary serpin, a unique serine proteinase inhibitor that has tumor suppressor activity, is expressed in normal mammary myoepithelial cells and plays a remarkable role in mammary development. Maspin expression defines a myoepithelial histogenesis in breast tumors [9]. Popikolov et al. [6] have reported that all eight matrix-producing metaplastic carcinomas moderately to strongly expressed maspin. Last, MIC2/CD99 is a transmembrane protein encoded by the MIC2 gene, characteristically expressed in the Ewing family of tumors/pnet. Besides these tumors, MIC2 is expressed in mature plasma cells of reactive lymph nodes, cortical thymocytes, pancreatic islet cells, granulosa cells of the ovary, and Sertoli cells of the testis. Recently, MIC2 expression was demonstrated in a broader range of neoplastic tissues, including some epithelial tumors. Milanezi et al. [4] have reported that four out of five metaplastic carcinomas expressed MIC-2 protein, three of them were matrix-producing metaplastic carcinoma. Walker and Carder [16] have also reported the utility of immunohistochemistry for MIC-2 in the identification of matrix-producing metaplastic carcinoma of the breast. Therefore, the S-100 protein, maspin, and MIC2 expressions may be the characteristics of matrixproducing metaplastic carcinoma of the breast. The present case may be compatible with one variant form of matrix-producing carcinoma due to the S-100 protein, maspin, and MIC2 expressions.
5 ARTICLE IN PRESS K. Oka et al. / Pathology Research and Practice 203 (2007) Nielsen et al. [5] have proposed an immunochemical panel comprising estrogen receptor (ER), epidermal growth factor receptor (EGFR, HER1), HER2, and CK 5/6, which could be used to identify breast carcinomas with a basal-like phenotype. Reis-Filho et al. [10] have reported that 16 of 18 matrix-producing metaplastic carcinomas showed the typical immunoprofile of basallike tumors (ER-, HER2-, EGFR+ and/or CK5/6+), and one of the two remaining carcinomas expressed CK14. They concluded that matrix-producing metaplastic carcinomas of the breast are basal-like tumors. By contrast, the present case was negative for ER, EGFR, HER2, CK5, CK5/6, and CK14. Therefore, it was considered a myoepithelial phenotype. Rakha et al. [8] reported that the basal phenotype breast carcinomas (expressing CK5/6 and/or CK14) rather than the myoepithelial phenotype carcinomas (expressing SMA and/or p63) had a poor prognosis. Tsuda et al. [15] have reported that of seven matrixproducing metaplastic carcinomas, seven (100%) expressed EGFR, and 0 expressed HER2. Leibl et al. [3] also observed that matrix-producing metaplastic carcinomas expressed EGFR, but not HER2. The EGFR positivity and HER2 negativity in neoplastic cells might be characteristic for matrix-producing metaplastic carcinoma. However, by contrast, the present case was consistently negative for EGFR and HER2. Breast ductal tissues have two parenchymal cell layers: an inner luminal cell layer formed luminal/ glandular cells and an outer cell layer juxtaposed to the basement membrane, termed basal cell layer. The basal cell layer is formed by morphologically heterogeneous cells that appear either cuboidal or spindle-shaped, depending on their location and the hormonal status of the tissue. These basal cells can be distinguished from basal cells in stratified squamous epithelium because they exhibit features of both epithelial and smooth muscle cells. Therefore, the term myoepithelial cells was applied. Myoepithelial cells express high-molecular weight (basal associated) cytokeratins (CKs) and smooth muscle markers [8]. CK5, CK14, CK17, and 34bE12 are basal cell-type cytokeratins and are expressed in basal epitheliums [2,7]. On the other hand, S-100 protein, maspin, a-smooth muscle actin, p63, CD10, smooth muscle myosin heavy chain, calponin, caldesmon, and sigma are myoepithelial markers and are expressed in myoepithelial cells [2,9]. Matrixproducing metaplastic carcinomas consistently showed features of basal/myoepithelial differentiation. In the present case, both atypical epithelial and myoepithelial cells expressed S-100 protein and maspin; myoepithelial cell markers. Atypical myoepithelial cells did not consistently express CK14 and 34bE12,basalcellmarkers.In addition, Ber-EP4 marks the basal cells of basal cell carcinoma and basal cell adenocarcinoma [14]. In the present case, atypical epithelial cells were weakly or faintly positive for Ber-EP4; on the other hand, atypical dark and stellate cells were consistently negative for Ber- EP4. Therefore, alternatively, we considered that the neoplastic cells of the present case had myoepithelial markers, but no basal markers that implied myoepithelial differentiation. There remains the problem that in the present case, neither atypical epithelial nor myoepithelial cells consistently expressed a-smooth muscle actin, CD10, and p63. Acknowledgments This study was supported by a grant-in aid from Mito Saiseikai General Hospital (MSGH), Mito, Ibaraki, and TAKE-TOSHI Medical Research Fund, Oyama, Tochigi, Japan. The authors thank Mrs. S. Koyamatsu, Mr. T. Kawasaki, Miss T. Tobita, Mr. N. Yonekawa, Mr. M, Okano and Mrs. M. Miyauchi (Pathology, MSGH) for their skillful technical assistance. References [1] M. Hayes, D. Lesack, C. Girardet, M. del Vecchio, V. Eusebi, Carcinoma ex-pleomorphic adenoma of the breast. Report of three cases suggesting a relationship to metaplastic carcinoma of the matrix-producing type, Virchows Arch. 446 (2005) [2] S. Leibl, M. Gogg-Kammerer, A. Sommersacher, H. Denk, F. Moinfar, Metaplatic breast carcinomas: are they of myoepithelial differentiation? Immunohistochemical profile of the sarcomatoid subtype using novel myoepithelial markers, Am. J. Surg. Pathol. 29 (2005) [3] S. Leibl, F. Moinfar, Metaplastic breast carcinomas are negative for Her-2 but frequently express EGFR (Her-1): potential relevance to adjuvant treatment with EGFR tyrosine kinase inhibitors?, J. Clin. Pathol. 58 (2005) [4] F. Milanezi, E.M. Pereira, F.V. Ferreira, D. Leitão, F.C. Schmitt, CD99/MIC-2 surface protein expression in breast carcinomas, Histopathology 39 (2001) [5] T.O. Nielsen, F.D. Hsu, K. Jensen, et al., Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma, Clin. Cancer Res. 10 (2004) [6] N.K. Popnikolov, A.G. Ayala, K. Graves, Z. Gatalica, Benign myoepithelial tumors of the breast have immunophenotypic characteristics similar to metaplastic matrixproducing and spindle cell carcinomas, Am. J. Clin. Pathol. 120 (2003) [7] P.E. Purkis, J.B. Steel, I.C. Mackenzie, W.B. Nathrath, I.M. Leigh, E.B. Lane, Antibody markers of basal cells in complex epithelia, J. Cell Sci. 97 (1990) [8] E.A. Rakha, T.C. Putti, D.M. Abd El-Rehim, et al., Morphological and immunophenotypic analysis of breast carcinomas with basal myoepithelial differentiation, J. Pathol. 208 (2006)
6 604 ARTICLE IN PRESS K. Oka et al. / Pathology Research and Practice 203 (2007) [9] J.S. Reis-Filho, F. Milanezi, P. Silv, F.C. Schmitt, Maspin expression in myoepithelial tumors of the breast, Pathol. Res. Pract. 197 (2001) [10] J.S. Reis-Filho, F. Milanezi, D. Steele, et al., Metaplastic breast carcinomas are basal-like tumours, Histopathology 49 (2006) [11] P.P. Rosen, Adenomyoepithelioma of the breast, Human Pathol. 18 (1987) [12] R.H. Simpson, N. Cope, A. Skalova, M. Michal, Malignant adenomyoepithelioma of the breast with mixed osteogenic, spindle cell, and carcinomatous differentiation, Am. J. Surg. Pathol. 22 (1998) [13] I. Sugano, T. Nagao, Y. Tajima, et al., Malignant adenomyoepithelioma of the breast: a non-tubular and matrix-producing variant, Pathol. Int. 51 (2001) [14] P.E. Swanson, M.M. Fitzzpatrick, J.H. Ritter, E.J. Glusac, M.R. Wick, Immunohistologic differential diagnosis of basal cell carcinoma, squamous cell carcinoma, and trichoepithelioma in small cutaneous biopsy specimens, J. Cutan. Pathol. 25 (1998) [15] H. Tsuda, Y. Tani, J. Weisenberger, et al., Frequent KIT and epidermal growth factor receptor overexpressions in undifferentiated-type breast carcinomas with stem-celllike features, Cancer Sci. 96 (2005) [16] J.A. Walker, P.J. Carder, Utility of immunohistochemistry for CD99 in the identification of matrix-producing carcinoma of the breast, Histopathology 42 (2003) [17] E.S. Wargotz, H.J. Norris, Metaplastic carcinomas of the breast: I. Matrix-producing carcinoma,, Human Pathol. 20 (1989)
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