MALIGNANT TRANSFORMATION OF A BENIGN ONCOCYTOMA OF THE SUBMANDIBULAR GLAND: A CASE REPORT
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1 MALIGNANT TRANSFORMATION OF A BENIGN ONCOCYTOMA OF THE SUBMANDIBULAR GLAND: A CASE REPORT Tsung-Hsun Lee, 1 Yung-Song Lin, 1 Wen-Ying Lee, 2 Tai-Ching Wu, 3 and Shih-Lun Chang 1 Departments of 1 Otolaryngology, 2 Pathology, and 3 Radiology, Chi-Mei Medical Center, Tainan, Taiwan. Oncocytic carcinoma arising in the submandibular gland is an extremely rare tumor and only 11 cases have been reported previously. We report on a 51-year-old man with a previously benign oncocytoma in the submandibular gland that transformed from a benign morphology to malignant cellular atypia and mitosis. To our knowledge, the current report is the first published case of a malignant transformation from benign oncocytoma to oncocytic carcinoma of the submandibular gland. The proliferative activity of the tumor cells was evaluated immunohistochemically using antibodies against Ki-67. Key Words: benign oncocytoma, Ki-67 immunohistochemical stain, malignant transformation, oncocytic carcinoma, submandibular gland (Kaohsiung J Med Sci 2010;26:327 32) Salivary gland tumors are rare, comprising less than 3% of all neoplasms of the head and neck region. The majority of salivary tumors are located in the parotid gland (70%), followed by the minor salivary glands (22%) and the submandibular glands (8%) [1]. Oncocytic tumors comprise only 1% of all salivary gland tumors [2]. Oncocytic carcinomas are even more uncommon, representing 11% of all oncocytic salivary gland neoplasms, 0.5% of all epithelial salivary gland malignancies and 0.18% of all epithelial salivary gland tumors [3]. Oncocytic carcinoma arising in the salivary glands, first described by Bauer and Bauer in 1953, is a rare, predominantly oncocytic neoplasm [3,4]. Moreover, oncocytic carcinoma arising in the submandibular gland is an extremely rare tumor and Received: Sep 7, 2009 Accepted: Oct 13, 2009 Address correspondence and reprint requests to: Dr Shih-Lun Chang, Department of Otolaryngology, Chi-Mei Medical Center, 901 Chung Hwa Road, Yung Kung City 710, Tainan County, Taiwan. c @ms16.hinet.net only 11 cases have been reported to date [5]. We report a 51-year-old man with a previously benign oncocytoma in his submandibular gland that transformed from a benign morphology to malignant cellular atypia and mitosis. We performed immunohistochemical staining with antibodies against Ki-67 to qualify mitosis separately for clarity of the tumor. This study was approved by our Institutional Review Board (IRB ). CASE PRESENTATION A 51-year-old man presented with a recurrent mass in his left submandibular gland in August, 2008, and a prior diagnosis of benign oncocytoma in the same location. In February, 2005, he underwent total tumor ablation for the benign oncocytoma in his left submandibular gland. Pathological examination of the resected tissue of the earlier specimen revealed an encapsulated tumor (Figure 1A) composed of uniform oncocytes with fine chromatin and indistinct nucleoli (Figure 1B). Mitotic figures were rarely found. Kaohsiung J Med Sci June 2010 Vol 26 No Elsevier. All rights reserved.
2 T.H. Lee, Y.S. Lin, W.Y. Lee, et al A B Figure 1. (A) The tumor was well encapsulated (hematoxylin and eosin; original magnification, 100 ). (B) Uniform oncocytes with abundant eosinophilic granular cytoplasm, fine chromatin, indistinct nucleoli and rare mitoses (hematoxylin and eosin; original magnification, 400 ). Figure 2. (A) Axial computed tomography revealed a mass with central necrosis in the left submandibular region (arrows). (B) One enlarged lymph node was found anterior to the mass (arrow). At the current presentation, he had a painless swollen mass in the previously resected area. This lesion had been slowly growing for 4 months. On clinical examination, the mass was about cm in size, hard, rubbery and fixed. A palpable cervical lymphadenopathy was also found. The facial nerve and other cranial nerves functioned normally. Neck sonography revealed one well defined heterogeneous mass lesion in the left submandibular space, measuring cm in size. Several lymph nodes surrounding the tumor were swollen, with the largest one measuring about cm in size. Computed tomography of the neck demonstrated one enlarged mass lesion about 3.0 cm in diameter in the left submandibular 328 region (Figure 2A) and an enlarged lymph node, of about 1.4 cm in diameter, anterior to the submandibular mass (Figure 2B). Because recurrence of the oncocytoma was suspected, radical tumor resection with unilateral, modified neck dissection (levels I III) was performed in September Microscopically, the resected tumor revealed infiltrating growth and was composed of atypical oncocytes arranged in solid sheets. Marked nuclear atypia, cellular polymorphism and mitoses were observed (Figure 3A). Focal areas of necrosis were also found. The tumor had invaded the surrounding tissue, including the muscular tissue, perineural spaces and lymphatic vessels (Figure 3B). Three of the four lymph Kaohsiung J Med Sci June 2010 Vol 26 No 6
3 Malignant change of submandibular oncocytoma A B Figure 3. (A) Atypical oncocytes with marked nuclear pleomorphism and prominent nucleoli (hematoxylin and eosin; original magnification, 400 ). (B) Muscular and lymphatic invasion (hematoxylin and eosin; original magnification, 400 ). A B Figure 4. (A) Ki-67 immunohistochemical stain of the patient s previous benign oncocytoma showing rare Ki-67-positive cells (< 1%) (original magnification, 400 ). (B) Ki-67 immunohistochemical stain of the patient s current tumor showing oncocytic carcinoma, with a high frequency of Ki-67-positive cells of up to 30% (original magnification, 400 ). nodes contained tumor metastases. Therefore, the diagnosis of oncocytic carcinoma was established. We performed immunohistochemical stains with antibodies against Ki-67 (MIB-1, DAKO) to evaluate the proliferative activity of the earlier and current tumors. The frequency of Ki-67-positive cells was lower (< 1%) in the patient s previous oncocytoma (Figure 4A) than in the current oncocytic carcinoma (15 30%) (Figure 4B). We assumed from these clinical and immunohistochemical findings that this malignant tumor had transformed from the previously benign oncocytoma. The patient received postoperative adjuvant radiotherapy in the left submandibular tumor bed (total 66 Gy), left submental space and ipsilateral neck (total 59.4 Gy). He had no evidence of recurrence after 6 months of follow-up. DISCUSSION The German pathologist Hürthle was the first researcher to describe oncocytes as components of normal canine thyroid glands in 1894 [6]. The term oncocyte was only coined in 1931 by Hamperl to describe cells within Warthin s tumor with abundant granular eosinophilic cytoplasm [7]. The predominant ultrastructural feature of oncocytes is marked mitochondrial hyperplasia [8]. Oncocytes have since been described in many human tissues, including the salivary gland, lacrimal gland, ocular caruncle, parathyroid, thyroid, pituitary, esophagus, liver, pancreas, kidneys, adrenals, testicles and ovaries [2 4,9,10]. The diagnostic criteria of oncocytic carcinoma are as follows: (1) no encapsulation; (2) local invasion; Kaohsiung J Med Sci June 2010 Vol 26 No 6 329
4 T.H. Lee, Y.S. Lin, W.Y. Lee, et al (3) cellular polymorphism with scattered mitosis; (4) perineural, vascular or lymphatic invasion; (5) regional lymph node metastases; and (6) distant metastases [4,10]. Our patient s tumor fulfilled all of these criteria, except for distant metastases. To our knowledge, the development of a secondary oncocytic carcinoma of the submandibular gland from a preexisting benign oncocytoma has not been reported previously. The proliferative activity of the oncocytic tumor cells was evaluated immunohistochemically with antibodies against Ki-67 (MIB-1). Ki-67, a non-histone protein localized on the long arm of human chromosomes, is abundantly expressed in proliferating cells, except during the G0 period of the cell cycle [11 13]. In normal salivary glands, Ki-67 is expressed in an extremely small number of cells [12]. The high frequency of Ki- 67-positive cells is closely associated with the grade and early recurrence of carcinoma in various subtypes of salivary gland tumors, including adenoid cystic carcinomas, mucoepidermoid carcinoma and acinic cell carcinoma [11,13]. There was a higher frequency of Ki-67-positive cells in the oncocytic carcinoma of our patient. The average frequency of Ki-67-positive cells was very low (< 1%) in the patient s previous benign oncocytoma, whereas up to 30% of the cells in the current oncocytic carcinoma were positive for Ki-67. The higher frequency of Ki-67-positive cells in the oncocytic carcinoma reflects active cell proliferation [11 14]. Ki-67 immunostaining is valuable to distinguish a benign oncocytoma from a oncocytic carcinoma [3,11,12 14]. The combination of total surgical resection of the tumor with a safe margin and neck dissection is widely accepted for treating oncocytic carcinoma [3]. Adjuvant radiotherapy is an effective method for improving local control. However, the survival rates of oncocytic carcinoma were not fully documented in retrospective studies, such as the Dutch International Cooperative study or the study by Laramore et al [15 18]. Chemotherapy is often considered in symptomatic patients. However, the response to chemotherapy does not predict survival, and the currently available chemotherapeutic agents do not provide sustained remission [19 21]. Previous reports showed that oncocytic carcinoma commonly recurred locally with subsequent lymph nodes metastases and the prognosis of most patients was poor [4]. Goode and Corio reported that oncocytic carcinoma of the salivary glands of less than cm in size had better prognoses than larger tumors [22]. In addition, patients who underwent aggressive initial surgical intervention had significantly better prognoses than those treated conservatively [11]. Meanwhile, Nakada et al concluded that distant metastasis appeared to be the most important prognostic feature of oncocytic carcinoma [23]. To our knowledge, immunohistochemical transformation from benign oncocytoma to oncocytic carcinoma of the submandibular gland has never been reported. Further investigation of the prognosis of patients with oncocytic carcinoma of the submandibular gland is warranted as more cases are reported. REFERENCES 1. Corcione L, Giordano G, Genetti L, et al. Oncocytic mucoepidermoid carcinoma of a submandibular gland: a case report and review of the literature. Int J Oral Maxillofac Surg 2007;36: Wu HHJ, Silvernagel SW. Fine-needle aspiration cytology of an oncocytic carcinoma of the submandibular gland. Diagn Cytopathol 1998;19: Guclu E, Oghan F, Ozturk O, et al. A rare malignancy of the parotid gland oncocytic carcinoma. Eur Arch Otorhinolaryngol 2005;262: Muramatsu T, Hashimoto S, Lee MW, et al. Oncocytic carcinoma arising in submandibular gland with immunohistochemical observations and review of the literature. Oral Oncol 2003;39: Lee JS, Choi JH, Oh YH. Oncocytic carcinoma arising in the submandibular gland with disseminated bone metastases. South Med J 2009;102: Hürthle K. Beitrage zur kenntnis de sekretionsvorganges in der schilddruse. Arch F D Ges Physiol 1894;56: Hamperl H. Beitrage zur normalen und pathologischen Histologie menschlicher Speicheldrusen. Z Mikr-Anat Forsch 1931;27:1. 8. Ferreiro JA, Stylopoulos N. Oncocytic differentiation in salivary gland tumours. J Laryngol Otol 1995;109: Capone RB, Ha P, Westra WH, et al. Oncocytic neoplasms of the parotid gland: A 16-year institutional review. Otolaryngol-Head Neck Surg 2002;126: Mizutari K, Naganishi H, Tanaka Y. Oncocytic carcinoma in the submandibular gland: report of a case based on anti-mitochondrial immunohistochemical observations. Auris Nasus Larynx 2005;32: Ito K, Tsukuda M, Kawabe R, et al. Benign and malignant oncocytoma of the salivary glands with an immunohistochemical evaluation of Ki-67. ORL 2000;62: Aoki T, Tsukinoki K, Karakida K, et al. Expression of cyclooxygenase-2, Bcl-2 and Ki-67 in pleomorphic adenoma with special reference to tumor proliferation and apoptosis. Oral Oncol 2004;40: Kaohsiung J Med Sci June 2010 Vol 26 No 6
5 Malignant change of submandibular oncocytoma 13. Katori H, Nozawa A, Tsukuda M. Increased expression of cyclooxygenase-2 and Ki-67 are associated with malignant transformation of pleomorphic adenoma. Auris Nasus Larynx 2007;34: Alves FA, Pires FR, de Almeida OP, et al. PCNA, Ki-67 and p53 expressions in submandibular salivary gland tumours. Int J Oral Maxillofac Surg 2004;33: Terhaard CH, Lubsen H, Van der Tweel I, et al. Salivary gland carcinoma: independent prognostic factors for locoregional control, distant metastases, and overall survival: results of the Dutch Head and Neck Oncology Cooperative Group. Head Neck 2004;26: Terhaard CH, Lubsen H, Rasch CR, et al. Dutch Head and Neck Oncology Cooperative Group. The role of radiotherapy in the treatment of malignant salivary gland tumors. Int J Radiat Oncol Biol Phys 2005;61: Douglas JG, Lee S, Laramore GE, et al. Neutron radiotherapy for the treatment of locally advanced major salivary gland tumors. Head Neck 1999;21: Douglas JG, Koh WJ, Laramore GE, et al. Treatment of salivary gland neoplasms with fast neutron radiotherapy. Arch Otolaryngol Head Neck Surg 2003;129: Rentschler R, Burgess MA, Byers R. Chemotherapy of malignant major salivary gland neoplasms: a 25-year review of MD Anderson Hospital experience. Cancer 1977;40: Vattemi E, Graiff C, Sava T, et al. Systemic therapies for recurrent and/or metastatic salivary gland cancers. Expert Rev Anticancer Ther 2008;8: Tanvetyanon T, Qin D, Padhya T, et al. Outcomes of postoperative concurrent chemoradiotherapy for locally advanced major salivary gland carcinoma. Arch Otolaryngol Head Neck Surg 2009;135: Goode RK, Corio RL. Oncocytic adenocarcinoma of salivary glands. Oral Surg Oral Med Oral Pathol 1988; 65: Nakada M, Nishizaki K, Akagi H, et al. Oncocytic carcinoma of the submandibular gland a case of report and literature review. J Oral Pathol Med 1998;27: Kaohsiung J Med Sci June 2010 Vol 26 No 6 331
6 Ki-67 Ki ;26: Kaohsiung J Med Sci June 2010 Vol 26 No 6
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