Case Report Aggressive invasive micropapillary salivary duct carcinoma of the parotid gland
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1 Pathology International 2008; 58: doi: /j x Case Report Aggressive invasive micropapillary salivary duct carcinoma of the parotid gland Hidetaka Yamamoto, 1 Hideoki Uryu, 2 Yuichi Segawa 1 and Masazumi Tsuneyoshi 1 1 Department of Anatomic Pathology, Pathological Sciences, Graduate School of Medical Sciences, Kyushu University and 2 Department of Head and Neck Surgery, National Kyushu Cancer Center, Fukuoka, Japan The presence of invasive micropapillary component has been reported to be associated with salivary duct carcinoma and poor outcomes. Herein is described a rare case of invasive micropapillary salivary duct carcinoma of the parotid gland in a 60-year-old man. The micropapillary component was approximately 70% of the area of the tumor. Squamous differentiation was focally seen adjacent to the micropapillary component. On immunohistochemistry the ordinary salivary duct carcinoma component was positive for gross cystic disease fluid protein-15 (GCDFP-15), androgen receptor (AR), and HER2/neu, whereas both micropapillary and squamous components were negative for GCDFP-15 and AR. Immunohistochemical staining for D2-40 highlighted the lymph vessel invasion of tumor cells. This patient developed metastases in the lymph nodes of the neck, and also in the liver, lung, and brain. The lymph nodes and liver metastases had both ordinary salivary duct carcinoma and micropapillary components. The patient died of tumor 11 months after the initial surgical operation. The results support that the presence of micropapillary component is associated with more aggressive behavior of salivary duct carcinoma. It is also important for pathologists to recognize that GCDFP-15 and AR expression can be reduced in micropapillary carcinoma in the differential diagnosis of metastatic tumor. Key words: immunohistochemistry, micropapillary, parotid gland, salivary duct carcinoma, squamous Salivary duct carcinoma is an aggressive adenocarcinoma that morphologically resembles high-grade ductal carcinoma of the breast. 1 A cribriform pattern with comedo necrosis is Correspondence: Hidetaka Yamamoto, MD, PhD, Department of Anatomic Pathology, Pathological Sciences, Graduate School of Medical Sciences, Kyushu University, Maidashi, Higashi-ku, Fukuoka , Japan. hidetaka@surgpath.med.kyushuu.ac.jp Received 14 September Accepted for publication 14 January typically seen in salivary duct carcinoma. There are some histological variants of salivary duct carcinoma: sarcomatoid, mucin-rich, and invasive micropapillary variants. 1 Nagao et al. reported 14 cases of invasive micropapillary salivary duct carcinoma that occurred in the parotid gland and that were associated with a more aggressive clinical course than ordinary salivary duct carcinoma. 2 After that report there has been no additional report of invasive micropapillary salivary duct carcinoma in the English-language literature. Here we describe an additional case of invasive micropapillary salivary duct carcinoma of the parotid. CLINICAL SUMMARY A 60-year-old Japanese man was admitted to hospital due to swelling of the left parotid region. There was no sign of facial nerve palsy. Radiological examination indicated a tumor in the left parotid gland, accompanied by swollen lymph nodes of the neck. Surgical resection of the parotid tumor together with lymph node dissection was performed. Local recurrence and liver metastasis of tumor occurred at 6 months after the initial operation. Chemotherapy with 5-fluorouracil and cisplatin had no effect on the recurrent tumor. Lung and brain metastases developed, and the patient died due to the tumor at 11 months after the initial operation. Autopsy was not performed. MATERIALS AND METHODS The excised specimen was fixed in a solution of 10% formaldehyde and embedded in paraffin. Four micrometer-thick sections were prepared and stained with HE. Immunohistochemical staining was performed with the primary antibodies as follows: low-molecular-weight cytokeratin (CAM5.2, Becton Dickinson, San Jose, CA, USA; dilution 20), pancytokeratin (AE1/AE3, Neomarkers, Fremont, CA, USA; dilution 40), cytokeratin (CK) 7 (OVT-TL12/30, Dako,
2 Micropapillary salivary duct carcinoma 323 Figure 1 Macroscopic appearance of invasive micropapillary salivary duct carcinoma. The cut surface is solid and whitish-gray in color. A focal yellowish portion corresponding to comedo necrosis is noted. Arrowheads indicate the intraparotid lymph nodes metastasized by carcinoma. Glostrup, Denmark; dilution 50), CK14 (LL002, Novocastra, Newcastle upon Tyne, UK; dilution 50), CK20 (Ks20.8, Dako, Glostrup, Denmark; dilution 50), high-molecular-weight cytokeratin (34bE12, Enzo Life Sciences, Farmingdale, NY, USA; dilution 50), epithelial membrane antigen (EMA; E29, Dako, Carpinteria, CA, USA; dilution 400), gross cystic disease fluid protein-15 (GCDFP-15; 23A3, Novocastra; dilution 20), androgen receptor (AR; AR27, Zymed Laboratories, South San Francisco, CA, USA; dilution 20), estrogen receptor (1D5, Dako, Carpinteria, CA, USA; dilution 2), progesterone receptor (PgR36, Dako, Carpinteria, CA, USA; dilution 6), and HER2/neu (rabbit polyclonal, Nichirei, Tokyo, Japan; dilution 200). The subsequent development of antibodybridge labeling using the Envision plus system (Dako, Carpinteria, CA, USA) with hematoxylin counterstaining was performed. RESULTS Macroscopically, the tumor was solid, whitish-gray, and focally yellow on cut surface, and was 2.3 cm in maximum diameter (Fig. 1). Intraparotid lymph node metastases were also present around the tumor. Histologically the tumor was composed of typical salivary duct carcinoma and invasive micropapillary component; the latter consisted of approximately 70% of the tumor area (Fig. 2a,b). The conventional salivary duct carcinoma area was composed of infiltrating growth of carcinoma cells arranged in nest or cribriform pattern with comedo necrosis. These carcinoma cells had abundant, eosinophilic cytoplasm, large pleomorphic nuclei and pleomorphic nucleoli. Focal dense sclerotic stroma was seen within the conventional salivary duct carcinoma, but there was no definite evidence of pre-existing pleomorphic adenoma. Invasive micropapillary carcinoma was characterized by morula-like cell clusters without fibrovascular cores surrounded by clear spaces (Fig. 2c). Squamous differentiation was focally seen adjacent to the micropapillary component (Fig. 2d). Immunohistochemistry results are given in Table 1. The EMA-positive reaction was stronger in peripheral cell membranes having an inside-out staining pattern in a b Figure 2 Histological appearance. (a) Transitional zone between the invasive micropapillary component (left lower) and the ordinary component (right upper) of salivary duct carcinoma. (b) The ordinary component has a nested pattern with comedo necrosis. (c) The invasive micropapillary component has small papillary clusters of carcinoma cells floating in the clear spaces. (d) Focal squamous differentiation is connected to the invasive micropapillary component. c d
3 324 H. Yamamoto et al. the micropapillary component (Fig. 3). Ordinary salivary duct carcinoma was positive for GCDFP-15 and AR, whereas both micropapillary and squamous components were negative for these markers (Fig. 4). Both ordinary salivary duct carcinoma and micropapillary components were positive for CK7 and HER2/neu, but negative for CK20. Immunohistochemical staining for D2-40 highlighted the lymph vessel invasion of tumor cells in part. But most of the clear spaces of the invasive micropapillary component were negative for D2-40. Myoepithelial or basal cells positive for CK14 focally surrounded conventional salivary duct carcinoma cells in a cribriform pattern, indicating intraductal spread. DISCUSSION Invasive micropapillary carcinoma component has been reported in the ovary, breast, colon, lung, and urinary bladder Figure 3 Immunohistochemical staining for epithelial membrane antigen (EMA). EMA is stained at the periphery of clusters of micropapillary carcinoma cells. a b c d e f Figure 4 Immunohistochemical staining for various markers in the different components. (a,b) Immunohistochemical staining for gross cystic disease fluid protein-15. (a) The ordinary component is positive, but (b) both invasive micropapillary and squamous components are negative. (c,d) Immunohistochemical staining for HER2/neu. (c) The ordinary component is positive, as is (d) the invasive micropapillary component, but the squamous component is negative. (e,f) Immunohistochemical staining for androgen receptor. (e) The ordinary component is positive, whereas (f) both invasive micropapillary and squamous components are negative.
4 Micropapillary salivary duct carcinoma 325 Table 1 Immunohistochemistry and histological components Marker SDC Micropapillary Squamous Cytokeratin (CAM5.2) + + Cytokeratin (AE1/AE3) Cytokeratin Cytokeratin 20 HMW-CK (34bE12) EMA + + Weak+ GCDFP-15 + Androgen receptor + Estrogen receptor Progesterone receptor HER2/neu + + EMA, epithelial membrane antigen; GCDFP-15, gross cystic disease fluid protein-15, HMW-CK, high-molecular-weight cytokeratin; SDC, salivary duct carcinoma. carcinomas. 3 9 Invasive micropapillary carcinomas have characteristic morphological features as shown by morulalike cell clusters without fibrovascular cores, surrounded by clear spaces. EMA is positive in peripheral cell membranes (so-called inside-out staining pattern). Clinically, the presence of invasive micropapillary component is associated with more aggressive behavior in these carcinomas. It has been reported that invasive micropapillary carcinoma of the breast is associated with frequent lymph vessel invasion and lymph node metastasis. 5 In salivary gland cancer this component can be seen in salivary duct carcinoma. Nagao et al. have reported 14 cases of invasive micropapillary variant of salivary duct carcinoma, most of which occurred together with lymph node metastasis (14/14), distant metastasis (9/14), and patient death (9/14). 2 The present patient died of metastatic carcinoma 11 months after the initial surgery followed by radiation therapy and chemotherapy. This finding indicates that invasive micropapillary salivary duct carcinoma is an aggressive tumor. The amount of invasive micropapillary component in salivary duct carcinoma ranges from 10% to >90%. 2 In the present case this component was found to be approximately 70% of the area, but there is no definite association between the proportion of the invasive micropapillary component and the biological behavior of salivary duct carcinoma. 2 Likewise, such association has not been observed in invasive micropapillary carcinoma of the breast. 5 In the current case focal squamous differentiation was present adjacent to the micropapillary component. To the best of our knowledge, this is the first report regarding the presence of squamous component in invasive micropapillary salivary duct carcinoma. Salivary duct carcinoma frequently expresses GCDFP-15 and AR. 10 Nagao et al. have reported that invasive micropapillary salivary duct carcinomas express GCDFP-15 and AR in 10/12 (83%) and 9/12 (75%) cases, respectively. 2 Interestingly, in the present case ordinary salivary duct carcinoma was positive for GCDFP-15 and AR, but the invasive micropapillary component and squamous component were negative for both markers. This finding suggests that morphological change may be associated with phenotypic change in salivary duct carcinoma. In addition, negative staining for GCDFP-15 and AR in the metastatic foci of invasive micropapillary carcinoma can lead to difficulty in determination of the primary site because various organs of carcinoma have an invasive micropapillary pattern, as mentioned here. HER2/neu is a receptor tyrosine kinase, and its overexpression and/or gene amplification have been reported in various carcinomas, including breast and salivary gland. 11,12 Most salivary duct carcinomas express HER2/neu, and some of them are associated with HER2/neu gene amplification. 13,14 Nagao et al. have reported frequent expression of HER2/neu in invasive micropapillary salivary duct carcinoma, which is consistent with the present results. 2 It has been reported that HER2/neu overexpression is associated with a poor prognosis in salivary duct carcinoma. 15 Thus, overexpression of HER2/neu in the micropapillary component may contribute to highly aggressive behavior of this variant. Furthermore, this highly malignant tumor might respond to therapy with monoclonal antibody (Herceptin) directed against the extracellular domain of the HER2/neu protein. Further study is necessary to elucidate the clinical response to Herceptin therapy and its association with the levels of HER2/neu protein expression and gene amplification. REFERENCES 1 Brandwein-Gensler MS, Skalova A, Nagao T. Salivary duct carcinoma. In: Barnes L, Eveson JW, Reichart P, Sidransky D, eds. World Health Organization Classification of Tumours. Pathology and Genetics Head and Neck Tumours. Lyon: IARC Press, 2005; Nagao T, Gaffey TA, Visscher DW et al. Invasive micropapillary salivary duct carcinoma: A distinct histologic variant with biologic significance. Am J Surg Pathol 2004; 28: Prat J, De Nictolis M. Serous borderline tumors of the ovary: A long-term follow-up study of 137 cases, including 18 with a micropapillary pattern and 20 with microinvasion. Am J Surg Pathol 2002; 26: Siriaunkgul S, Tavassoli FA. Invasive micropapillary carcinoma of the breast. Mod Pathol 1993; 6: Nassar H, Wallis T, Andea A et al. Clinicopathologic analysis of invasive micropapillary differentiation in breast carcinoma. Mod Pathol 2001; 14: Kim MJ, Hong SM, Jang SJ et al. Invasive colorectal micropapillary carcinoma: An aggressive variant of adenocarcinoma. Hum Pathol 2006; 37: Amin MB, Tamboli P, Merchant SH et al. Micropapillary component in lung adenocarcinoma: A distinctive histologic feature with possible prognostic significance. Am J Surg Pathol 2002; 26: Amin MB, Ro JY, el-sharkawy T et al. Micropapillary variant of transitional cell carcinoma of the urinary bladder: Histologic pattern resembling ovarian papillary serous carcinoma. Am J Surg Pathol 1994; 18:
5 326 H. Yamamoto et al. 9 Samaratunga H, Khoo K. Micropapillary variant of urothelial carcinoma of the urinary bladder; a clinicopathological and immunohistochemical study. Histopathology 2004; 45: Kapadia SB, Barnes L. Expression of androgen receptor, gross cystic disease fluid protein, and CD44 in salivary duct carcinoma. Mod Pathol 1998; 11: Slamon DJ, Godolphin W, Jones LA et al. Studies of the HER- 2/neu proto-oncogene in human breast and ovarian cancer. Science 1989; 244: Ross JS, Fletcher JA. The HER-2/neu oncogene in breast cancer: Prognostic factor, predictive factor, and target for therapy. Stem Cells 1998; 16: Skalova A, Starek I, Vanecek T et al. Expression of HER-2/neu gene and protein in salivary duct carcinomas of parotid gland as revealed by fluorescence in-situ hybridization and immunohistochemistry. Histopathology 2003; 42: Felix A, El-Naggar AK, Press MF et al. Prognostic significance of biomarkers (c-erbb-2, p53, proliferating cell nuclear antigen, and DNA content) in salivary duct carcinoma. Hum Pathol 1996; 27: Jaehne M, Roeser K, Jaekel T, Schepers JD, Albert N, Loning T. Clinical and immunohistologic typing of salivary duct carcinoma: A report of 50 cases. Cancer 2005; 103:
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