CASE REPORT PRIMARY LYMPHOEPITHELIOMA-LIKE CARCINOMA OF MINOR SALIVARY GLAND: A CASE REPORT WITH IMMUNOHISTOCHEMICAL AND IN SITU HYBRIDIZATION STUDIES
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1 CASE REPORT Dennis H. Kraus, MD, Section Editor PRIMARY LYMPHOEPITHELIOMA-LIKE CARCINOMA OF MINOR SALIVARY GLAND: A CASE REPORT WITH IMMUNOHISTOCHEMICAL AND IN SITU HYBRIDIZATION STUDIES Sheng-Yun Lu, MD, 1 Chao-Cheng Huang, MD, 1 Ching-Yeh Hsiung, MD, 2 Hock-Liew Eng, MD, 1 Hsuan-Ying Huang, MD 1 1 Department of Pathology, Chang Gung Memorial Hospital, Kaohsiung Medical Center, No.123, Ta-Pei Rd., Niao-song Township, Kaohsiung County 833, Taiwan. a @yahoo.com 2 Department of Radiation Oncology, Chang Gung University and Memorial Hospital, Kaohsiung Medical Center, Kaohsiung, Taiwan Accepted 25 May 2005 Published online 20 October 2005 in Wiley InterScience ( DOI: /hed Abstract: Background. Lymphoepithelioma-like carcinomas (LEC) of salivary glands represent rare epithelial malignancies, with most cases affecting the parotid gland. To our knowledge, there was only one LEC arising from the minor salivary gland described in the English-language literature. Methods. We report the second LEC of the minor salivary gland in the buccal area of a 50-year-old Taiwanese woman, who underwent surgical resection and adjuvant radiotherapy and remained alive and well after 120 months of follow-up. Histologically, irregular tumor nests of undifferentiated epithelial cells with syncytial cell boundaries were found embedded within rich lymphoplasmacytic stroma. The tumor cells also showed strong c-kit expression and evidence of Epstein-Barr virus (EBV) infection. Conclusions. Our case suggests potential pathogenic implications of both c-kit and EBV in LEC of the minor salivary gland that can be cured by the combination of surgery and radiotherapy and has a very favorable long-term prognosis. A 2005 Wiley Periodicals, Inc. Head Neck 28: , 2006 Correspondence to: H.-Y. Huang B 2005 Wiley Periodicals, Inc. Keywords: lymphoepithelioma-like carcinoma; minor salivary gland; Epstein-Barr virus; c-kit Lymphoepithelioma-like carcinoma (LEC), also referred to as malignant lymphoepithelial lesions or undifferentiated carcinoma with lymphoid stroma, has a marked racial predilection for Southeastern Chinese and Eskimos. It is considered the malignant counterpart of benign lymphoepithelial lesion (BLE) and histologically indistinguishable from the similarly named neoplasms of nasopharyngeal origin. Two thirds of LECs arise de novo, whereas the remaining third develop in the setting of a preceding or concurrent BLE. As with LEC of nasopharyngeal origin, Epstein-Barr virus (EBV) has been strongly implicated in the oncogenesis of LECs, which can be detected by variable methods, including in situ hybridization for EBV-encoded small RNAs (EBER) mrna. c-kit (CD117) is a transmembrane receptor type tyrosine kinase that is structurally and 182 Lymphoepithelioma-Like Carcinoma of Minor Salivary Gland
2 functionally analogous to platelet-derived growth factor and colony-stimulating factor-1 receptors. c-kit expression has been previously documented in a wide variety of human neoplasms resulting either from constitutional mutation of various exons in the c-kit gene or from paracrine/autocrine loop feedback pathways. A recent study indicated that c-kit is highly frequently expressed in a handful of LECs of major salivary glands, raising the possibility that c-kit might also confer growth advantage on LECs. To date, only one case of an intraoral LEC of presumed minor salivary gland origin, affecting a 69-year-old white woman, has been reported in the English-language literature. 1 It was associated with concurrent BLE and neck lymph metastasis at initial diagnosis. In this report, we describe the second LEC of the minor salivary gland that occurred in an Asian patient without associated BLE in conjunction with immunohistochemical and EBV studies. CASE REPORT A 50-year-old woman was initially seen with a progressively enlarged, painless, firm mass beneath the right buccal mucosa for 1 year without a history of smoking, alcohol, or beetle nut consumption or relevant systemic disease. The overlying mucosa of the tumor was unremarkable. The CT scan revealed neither enlarged neck lymph nodes nor abnormality of the nasopharynx, lending further support for the primary nature of this tumor. She received wide local excision followed by adjuvant radiotherapy with a total dose of 6520 cgy with curative intent. The patient is alive with no evidence of disease after 120 months of long-term follow-up. FIGURE 1. (A) The tumor cells are arranged in nests with residual minor salivary glands on the left (hematoxylin eosin stain, original magnification 40), whereas (B) the overlying buccal mucosa is nondysplastic (hematoxylin eosin stain, original magnification 40). (C) At high magnification, the tumor is composed of syncytial epithelial cells featuring moderate nuclear pleomorphism and prominent nucleoli (hematoxylin eosin stain, original magnification 200). [Color figure can be viewed in the online issue, which is available at Lymphoepithelioma-Like Carcinoma of Minor Salivary Gland 183
3 Pathology. Grossly, the tumor, measuring cm, was yellowish white, firm, and multinodular in appearance. Microscopically, residual lobules of minor salivary glands were found juxtaposing or intermingling with several separated, various-sized tumor nodules (Figure 1A) beneath an intact nondysplastic stratified squamous epithelium (Figure 1B). The tumor was predominantly composed of large, polygonal, undifferentiated tumor cells with vesicular nuclei and prominent nucleoli that were arranged in cohesive nests within abundant lymphoplasmacytic infiltrates, focally forming germinal centers. The cell borders between adjacent cells were indistinct, creating a syncytial cytoplasmic appearance (Figure 1C). Mitotic figures averaged one to two per high-power field. Necrosis, keratinization, and benign lymphoepithelial lesions were all absent. Immunohistochemically, the tumor was diffusely positive for epithelial membrane antigen (EMA), AE1/AE3 cocktail, and CD117 (Figure 2A) but negative for cytokeratin 7, cytokeratin 20, and latent membrane protein-1 (LMP-1). The labeling indices of Ki-67 and p53 were approximately 10% and 25%, respectively. In situ hybridization for detection of EBV by use of EBER1-specific antisense oligoprobe disclosed abundant EBER1 in undifferentiated carcinoma (Figure 2B) but not in the surrounding lymphoid stroma. DISCUSSION Hilderman et al 2 were the first to recognize epithelial malignancy in the salivary gland showing features similar to those of BLE. Although LEC accounts for only 0.4% of all salivary gland neoplasms as reported by the Armed Forces Institute of Pathology Tumor Registry, 3 more than 100 cases have been described to date, with most affecting the parotid glands or, less commonly, the submandibular glands. 4,5 LEC accounted for 7% of all malignant salivary gland tumors in Taiwan, an incidence 14 times higher than in the Western population. Nevertheless, the presentation of primary LEC affecting the minor salivary gland was hitherto never described in Asians, except for one previous case derived from the same buccal area of an elderly white woman in the Englishlanguage literature. 1 As for malignancies of intraoral minor salivary glands, the most common histologic type is mucoepidermoid carcinoma followed by adenoid cystic carcinoma and adenocarcinoma, not otherwise specified, etc. 6 Therefore, this case represents an extremely rare type of carcinoma of the minor salivary glands. More than 40% of patients with LECs originating from the major salivary glands have metastases to lymph nodes at presentation, 20% have local recurrences or lymph node metastases develop, and approximately 20% eventually experience distant metastases within 3 years after therapy. 3 The clinical stage of disease has a significant impact on prognosis, because advanced disease in the form of large size or lymph node metastases corresponds to poor survival. The favorable outcome observed in our minor salivary gland LEC can be mostly ascribed to the early stage at initial presentation. However, accurate survival rates in patients with LECs of the sali- FIGURE 2. Tumor cells are strongly positive for both c-kit (A) (immunohistochemical stain, original magnification 400) and EBV-encoded small RNA-1 (B) (in situ hybridization, original magnification 400). Note the surrounding lymphocytes are negative. [Color figure can be viewed in the online issue, which is available at Lymphoepithelioma-Like Carcinoma of Minor Salivary Gland
4 vary glands are difficult to estimate because of insufficient follow-up or various therapeutic approaches in previously reported cases. A recent study from Taiwan demonstrated that the 5-year actuarial survival rate could be as high as 80% if combination therapy with surgical resection, neck dissection, and adjuvant radiation was used. 7 Several studies have demonstrated EBV genome in human carcinomas, particularly for those with morphologic features of LEC in various anatomic sites, such as the nasopharynx, salivary gland, lung, thymus, stomach, and gallbladder. 8 Although EBV-associated LECs of salivary glands were first reported by Salmundsen et al 9 in 1982 with use of complementary RNA-DNA filter hybridization, EBER in situ hybridization had been regarded as the gold standard for the identification of EBV within a given neoplasm. Unlike EBV nuclear antigen and LMPs, EBER is theoretically expressed in all three types of EBV latent infection. EBV-infected cells usually contain a large number of EBER copies, on the order of 10 6 to 10 7 copies per cell; therefore, EBER in situ hybridization should be the most sensitive method to detect any type of EBV in tumor cells. 10 More importantly, by direct visualization of positive cells, one can determine whether tumor cells or normal lymphocytes are positive for EBV. Leung et al 8 reported the presence of the virus in a clonal episomal form and the expression of LMP-1 viral oncoprotein, indicating a causative role of EBV in the oncogenesis of salivary gland LEC. However, in our case, we can demonstrate the presence of only EBER-1 but not the LMP protein. The c-kit proto-oncogene, mapped to chromosome 4q11-12, encodes for a type III tyrosine kinase receptor growth factor protein (CD117) belonging to the immunoglobulin gene superfamily. Two general mechanisms of c-kit activation in tumor cells have been described, including acquisition of activating mutations and autocrine or paracrine stimulation loops. 11 The former, characteristic of gastrointestinal stromal tumors (GISTs), germ cell tumors, and mast cell disorders, leads to constitutive activation of the receptor kinase activity in a ligand-independent manner, thus providing uncontrolled growthpromoting and antiapoptotic signals for tumor cells. In contrast, the autocrine/paracrine stimulation is an attractive alternate non-mutational pathway accounting for high-level expression of the kit kinase in a variety of cancers, such as small cell lung carcinoma, 12 Ewing sarcoma, 11 and thymic carcinoma. 13 Gleevec, a selective tyrosine kinase inhibitor, can potentially treat these malignancies, and the prognostic and therapeutic implication of c-kit expression has been recently suggested in small cell lung carcinoma 12 and Ewing sarcoma. 11 Among the salivary gland tumors assayed for c-kit expression, adenoid cystic carcinoma exhibited the highest frequency of reactivity as high as 80%, followed by lymphoepithelial carcinoma and myoepithelial carcinoma. 14 Therefore, we assume that the genetic and biologic aspects of c-kit expression in LECs of salivary gland origin are worth being further explored. CONCLUSION We have described an additional LEC of the minor salivary gland, which, using surgical excision with adjuvant radiotherapy, showed a satisfactory outcome after long-term follow-up. The tumor cells were strongly positive for EBER1 and c-kit protein, providing further insights into the tumorigenesis of salivary gland LECs. Acknowledgment. The authors thank Andrew G. Huvos, MD, at Memorial Sloan-Kettering Cancer Center for critical histologic review of the slides. REFERENCES 1. Worley NK, Daroca PJ Jr. Lymphoepithelial carcinoma of the minor salivary gland. Arch Otolaryngol Head Neck Surg 1997;123: Hilderman WC, Gordon JS, Large HL Jr, Carroll CF Jr. Malignant lymphoepithelial lesion with carcinomatous component apparently arising in parotid gland: A malignant counterpart of benign lymphoepithelial lesion? Cancer 1962;15: Ellis GL, Auclair PL. Atlas of tumor pathology: tumors of the salivary glands. Washington, DC: Armed Forces Institute of Pathology; p. 4. Abdulla AK, Mian MY. Lymphoepithelial carcinoma of salivary glands. Head Neck 1996;18: Jang SJ, Paik SS, Lee WM, et al. Lymphoepithelial carcinoma of the submandibular gland a case report. J Korean Med Sci 1997;12: Lopes MA, Kowalski LP, da Cunha Santos G, Paes de Almeida O. A clinicopathologic study of 196 intraoral minor salivary gland tumours. J Oral Pathol Med 1999; 28: Sheen TS, Tsai CC, Ko JY, Chang YL, Hsu MM. Undifferentiated carcinoma of the major salivary glands. Cancer 1997;80: Leung SY, Chung LP, Yuen ST, Ho CM, Wong MP, Chan SY. Lymphoepithelial carcinoma of the salivary gland: in situ detection of Epstein-Barr virus. J Clin Pathol 1995; 48: Lymphoepithelioma-Like Carcinoma of Minor Salivary Gland 185
5 9. Saemundsen AK, Albeck H, Hansen JP, et al. Epstein- Barr virus in nasopharyngeal and salivary gland carcinomas of Greenland Eskimos. Br J Cancer 1982;46: Iezzoni JC, Gaffey MJ, Weiss LM. The role of Epstein-Barr virus in lymphoepithelioma-like carcinomas. Am J Clin Pathol 1995;103: Scotlandi K, Manara MC, Strammiello R, et al. C-kit receptor expression in Ewing s sarcoma: lack of prognostic value but therapeutic targeting opportunities in appropriate conditions. J Clin Oncol 2003;21: Naeem M, Dahiya M, Clark JI, Creech SD, Alkan S. Analysis of c-kit protein expression in small-cell lung carcinoma and its implication for prognosis. Hum Pathol 2002;33: Pan CC, Chen PC, Chiang H. KIT (CD117) is frequently overexpressed in thymic carcinomas but is absent in thymomas. J Pathol 2004;202: Jeng YM, Lin CY, Hsu HC. Expression of the c-kit protein is associated with certain subtypes of salivary gland carcinoma. Cancer Lett 2000;154: Lymphoepithelioma-Like Carcinoma of Minor Salivary Gland
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