Fine Needle Aspiration of an Unusual Malignant Mixed Tumor in the Parotid Gland
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1 Fine Needle Aspiration of an Unusual Malignant Mixed Tumor in the Parotid Gland Xiu Yang, MD, PhD, 1 * Adam Cole, MD, 1 Maja Oktay, MD, PhD, 1 Richard Smith, MD, 2 Antonio Cajigas, MD, 1 Samer Khader, MD 1 Lab Med Spring 2014;45: DOI: /LMEKYOLQ2J5ZOO7O ABSTRACT Objective: The use of fine needle aspiration (FNA) biopsy in the triage of salivary gland tumors has been well established. The sensitivity and specificity of FNA biopsy for tumor diagnosis is generally very good. However, the diagnosis can be challenging due to the limited amount of tissue sampled, the occasional overlapping tumor morphology, and the presence of a malignant counterpart of a benign tumor. Methods: FNA biopsy was performed with ultrasound guidance. Airdried slides and alcohol-fixed slides were made for Diff-Quik staining and Papanicolaou staining, respectively. The syringes were rinsed and a cell block was prepared. The resected specimen was fixed in 10% formalin and processed by routine histology techniques. Results: We report a rare case of a salivary gland neoplasm with 2 distinct components: adenoid cystic carcinoma and pleomorphic Fine needle aspiration (FNA) cytology has been used to triage salivary gland lesions for quite some time. FNA biopsy is often the preferred procedure over a surgical core biopsy because it is convenient, cost efficient, and minimally invasive. For detection of salivary gland neoplasms, FNA has better than 90% sensitivity and Abbreviations FNA, fine needle aspiration; NOS, not otherwise specified; MRI, magnetic resonance imaging; Pap, Papanicolaou; PA, pleomorphic adenoma; carcinoma ex-pa, carcinoma ex-pleomorphic Adenoma; H&E, hematoxylin and eosin 1 Department of Pathology, Cytology Division; 2 Department of Otolaryngology, Head and Neck Surgery, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, New York State *To whom correspondence should be addressed. xiu.yang@louisville.edu adenoma. These 2 components are clearly identifiable in both cytological materials from fine needle aspiration and histological analysis of surgical resection. Conclusion: Pleomorphic adenoma is the most common salivary gland tumor for patients in all age groups. The characteristic cytological feature is fibrillary extracellular matrix intermixed with epithelial cells. Malignant transformation occurs in 5% to 10% of cases. Rarely, pleomorphic adenoma exists as one component of a hybrid tumor. The surgical resection will be needed in those cases. The final diagnosis relies on the combination of the clinical information, histological findings and molecular study. Keywords: fine needle aspiration, parotid gland, basaloid tumor, pleomorphic adenoma, adenoid cystic carcinoma specificity. For distinction between benign and malignant neoplasms, FNA has a sensitivity of 80% to 90%, and a specificity of more than 90%. 1 However, diagnosing salivary gland tumors by FNA can be challenging because of the limited amount of tissue acquired by FNA. In addition, overlapping histological features and the presence of a malignant counterpart of benign tumors also make the diagnosis difficult. Pleomorphic adenoma is the most common salivary gland tumor for patients in all age groups with a mean age of 46 years at the time of diagnosis. It accounts for 60% to 70% of all parotid gland tumors. There is a slight female preponderance of 1.9:1. Clinically, pleomorphic adenoma presents as a slow-growing, painless mass. Tumors are usually firm, mobile, and have a distinct smooth contour. The main concerns for pleomorphic adenoma are recurrence following surgical resection and risk of malignant transformation. Malignant transformation occurs in 5% to 10% of these neoplasms. The malignant component of this tumor always has an epithelial Spring 2014 Volume 45, Number 2 Lab Medicine 141
2 appearance, often presenting as adenocarcinoma (salivary duct type or not otherwise specified, [NOS]). On rare occasions, the malignant component can present as adenoid cystic carcinoma, 2-4 which is one of the major differential diagnosis of pleomorphic adenoma. Adenoid cystic carcinoma accounts for 4.4% of salivary gland tumors. While this tumor is very rare in children, it affects a wide range of age groups with a peak incidence between the fifth and seventh decade. There is a slight female preponderance. Adenoid cystic carcinoma usually presents as a slow-growing but widely infiltrative mass, either mobile or fixed. Both pleomorphic adenoma and adenoid cystic carcinoma are matrix-producing neoplasms. Cytologically, pleomorphic adenoma shows a fibrillary extracellular matrix while adenoid cystic carcinoma displays a spherical or tubular extracellular matrix. However, 5% of pleomorphic adenomas present with an adenoid cystic-like matrix, which may cause confusion in the interpretation. We report a rare malignant salivary gland tumor composed of distinct regions of pleomorphic adenoma and adenoid cystic carcinoma on both cytological and histological evaluations. We discuss the differential diagnosis and possible relationship between the 2 components. Materials and Methods The patient was a 17-year-old male with an angle of jaw mass that had been present for about 1 year. The size of the mass remained the same during this period. The patient complained of jaw pain with a decrease in the range of motion. A 3 cm mass was identified in the left parotid gland by magnetic resonance imaging (MRI). An ultrasound-guided fine needle aspiration biopsy was performed using a 25-gauge needle (Becon, Dickinson and Company, Franklin Lakes, NJ, Cat No ) with plunger (Belpro Medical Inc., Montreal, CA). The aspirated material was smeared on glass slides. Some of the slides were air-dried for Diff-Quik staining (Siemens,Malvern, PA Cat No. B4132), and others were immersed in 95% alcohol for Papanicolaou (Pap) staining. The syringes were then rinsed with Hank s solution (HBSS, Gibco, Grand Island, NY) and a cell block was prepared. The resected specimen was fixed in 10% formalin, and was processed by routine histology techniques. Results Review of slides showed a salivary gland neoplasm composed of sheets and clusters of bland epithelial cells with an abundant extracellular matrix. On Diff-Quik stained slides, the majority of the extracellular matrix was dense, magenta-colored, and formed spherical and tubular structures (Images 1A and 1B). Basaloid cells with scant cytoplasm were noted at the periphery surrounding the matrix (Images 1A and B). In other regions of the same slides, the extracellular matrix appeared thin and fibrillary; it intermingled with basaloid cells (Images 1C and 1D). On Pap stained slides, the extracellular matrix appeared blue and translucent with either a spherical or fibrillary shape (Images 2A and 2B). The basaloid cells occasionally formed sharply demarcated trabecular or spherical structures (Image 2C). The differential diagnosis included pleomorphic adenoma, membranous monomorphic adenoma, and adenoid cystic carcinoma, among others. Cell block preparations showed cells with scant cytoplasm forming double-layered trabecular or tubular structures with myxoid matrix. Rare mitoses were noted (Image 2D inset). No classic cribriform (so called Swiss-cheese ) pattern, as seen in adenoid cystic carcinoma, was noted on the cell block. A parotid gland lobectomy, and regional lymph node dissection was performed 1 month later. Microscopically, the tumor contained areas characteristic of cellular pleomorphic adenoma, and other areas characteristic of adenoid cystic carcinoma. In areas characteristic of cellular pleomorphic adenoma, some atypical features were noted, including cells with open chromatin and prominent nucleoli, and increased mitotic activity (Images 3A and 3B). Focal hyalinized areas within pleophormic adenoma were also observed. In areas with unequivocal features of adenoid cystic carcinoma, tumor cells demonstrated various growth patterns including predominantly cribriform as well as tubular/glandular and solid areas (Image 3C). Cytological analysis revealed a combination of cell types including dominant basaloid cells and scattered identifiable true gland lining cells. Multifocal perineural invasions were also identified (Image 3D). There were no foci in which direct continuity or merging of the 2 distinct tumor types was observed. Discussion Diagnosis of pleomorphic adenoma based on cytological or surgical specimens is relatively straightforward 142 Lab Medicine Spring 2014 Volume 45, Number 2
3 A B C Image 1 A matrix-producing tumor shows features of both pleomorphic adenoma and adenoid cystic carcinoma (Diff-Quick stain, 40). A and B, The majority of the extracellular matrix forms spherical and tubular shapes with round smooth shape borders instead of frayed edges. Basaloid cells are surrounding the matrix. C and D, A magenta-colored fibrillary matrix mixed with isolated plump, oval to spindleshaped epithelial/myoepithelial cells. since they include a combination of epithelial cells with characteristic matrix material. However, there are several common features shared by pleomorphic adenomas and adenoid cystic carcinomas, that can complicate the differential diagnosis. For example, a sharply circumscribed cribriform pattern, although typical in adenoid cystic carcinoma, is also present in 5% of pleomorphic adenomas. At the cytological level, the matrix material in pleomorphic adenoma generally appears fibrillary. However, in a few areas of the tumor the matrix may be spherical, similar to the matrix observed in adenoid cystic carcinoma. If the spherical matrix is found only in D rare regions within an adequately sampled specimen, there is no significant concern. In resected surgical specimens, a well-circumscribed border versus infiltration and presence of perineural invasion will facilitate the final diagnosis. Immunohistochemical stains are rarely useful in distinguishing between pleomorphic adenoma and adenoid cystic carcinoma. For example, while C-kit (CD117) staining is moderately intense in luminal cells of pleomorphic adenoma, it also stains positively in duct-lining cells in adenoid cystic carcinoma. Similarly, the S-100 marker can be positive in both pleomorphic adenoma and adenoid cystic carcinoma. Spring 2014 Volume 45, Number 2 Lab Medicine 143
4 A B C D Image 2 A Pap stain reveals 2 distinct morphologies of the tumor. A, A pale blue, lucent tubular matrix with a sharp edge is surrounded by basaloid cells (Pap stain, 40). B, Basaloid cells are mixed with a thin fibrillary extracellular matrix. The lower left corner shows a denser pale-blue acellular cylinderous matrix (Pap stain, 40). C, A cluster of basaloid cells form a ribbon-like structure (Pap stain, 40). D, A cell block showed biphasic cells forming glandular and trabecular structures surrounding a fibromyxoid matrix (H&E stain, 20). Increased mitotic activity is noted (inset). We present an unusual case of a salivary gland tumor containing features of either pleomorphic adenoma or adenoid cystic carcinoma in distinct regions. This observation raises 2 possible scenarios that cannot be definitively resolved: a hybrid tumor vs. carcinoma expleomorphic adenoma (ex-pa). Carcinoma ex-pa occurs in about 6% of pleomorphic adenomas and usually occurs in the 6th or 7th decades, approximately 1 decade later than patients with pleomorphic adenomas. Clinically, carcinoma ex-pa usually presents as a rapidly enlarging mass in a long-standing tumor. The malignant component is usually poorly differentiated adenocarcinoma (salivary duct type or NOS). A few reports 2-4 suggest that adenoid cystic carcinoma is the malignant component in these mixed tumors. Evidence for pre-existing pleomorphic adenoma is sometimes hard to find. A thorough sampling, or a previously resected pleomorphic adenoma at the same location would be critical for making the diagnosis. Hyaline changes can be seen in some carcinomas, which could suggest a pre-existing pleomorphic adenoma. 144 Lab Medicine Spring 2014 Volume 45, Number 2
5 A B C D Image 3 A resection specimen shows areas characteristic of both pleomorphic adenoma and adenoid cystic carcinoma, respectively. A, Tumor cells form glandular and trabecular structures that are intermingled with fibromyxoid matrix (H&E stain, 10). B, A high magnification image showing biphasic tumor cells. Some cells have open chromatin and prominent nucleoli, which is atypical for pleomorphic adenoma (H&E stain, 40). Increased mitotic activity is noted (inset). C, Tumor cells form a cribriform pattern, a typical appearance of adenoid cystic carcinoma (H&E stain, 20). D, Perineural invasion is noted (H&E stain, 40). On the other hand, a hybrid tumor at this site is extremely rare, accounting for less than 0.1% of all salivary gland tumors. 7 The criteria for diagnosing a hybrid tumor is the presence of 2 distinct and separated tumors in the same topographic area producing a single tumor mass. Adenoid cystic carcinoma has been reported to co-exist with other salivary gland tumors (hybrid tumor), such as salivary duct carcinoma Our patient was much younger than a typical patient with carcinoma ex-pleomorphic adenoma. In addition, he did not have a history of a long-standing mass, nor did he notice any rapid growth of the mass. Therefore, the likelihood of his tumor being carcinoma ex-pa was small. The final diagnosis relied on molecular studies. Although the nature of this lesion is not fully understood, proper clinical management and prognosis depended on the finding of an adenoid cystic carcinoma component. The 5-year survival rate of adenoid cystic carcinoma is 60%, and the 10-year survival rate is only 30%. Patients typically receive radiation therapy. Our patient did receive radiation Spring 2014 Volume 45, Number 2 Lab Medicine 145
6 therapy after surgery. He has been closely followed up for 2.5 years and he remains tumor-free. Conclusion Pleomorphic adenoma is the most common salivary gland tumor for patients in all age groups. The characteristic cytological feature is fibrillary extracellular matrix intermixed with epithelial cells. Malignant transformation occurs in 5% to 10% of cases. Rarely, pleomorphic adenoma exists as one component of a hybrid tumor. Surgical resection will be needed in those cases. The final diagnosis relies on the combination of the clinical information, histological findings and molecular study. LM References 1. Cibas ES, Ducatman BS. Cytology: diagnostic principles and clinical correlations.philadelphia, PA: Saunders, Elserier Inc. 2009; Ide F, Mischima K, Yamada H, Saito I. Adenoid cystic carcinoma ex pleomorphic adenoma of the parotid gland. Head & Neck Pathol. 2009;3: Brcheriou C, Baudin JP, Verola O. Adenoid cystic carcinoma on pleomorphic adenoma. Report of two cases. Rev Stomatol Chir Maxillofac. 1985;86: Geisinger KR, Reynolds GD, Vance RP, McGuirt WF. Adenoid cystic carcinoma arising in a pleomorphic adenoma of the parotid gland. An aspiration cytology and ultrastructural study. Acta Cytol. 1985;29: Manganaris A, Kiziridou A, Manganaris T. Unusual localization of an adenoid cystic carcinoma subsequent to superficial parotidectomy for a benign lesion. J Craniofac Surg. 2007;18: Gnepp DR. Malignant mixed tumor of the salivary glands: a review. Pathol Annu. 1993;28: Seifert G, Donath K. Hybrid tumors of salivary glands: definition and classification of five rare cases. Eur J Cancer B Oral Oncol. 1996;32: Croitoru CM, Suarez PA, Luna MA. Hybrid carcinoma of salivary glands. Report of 4 cases and review of the literature. Arch Pathol Lab Med. 1999;123: Nagao T, Sugano I, Ishida Y, Asoh A, Munakata S, Yamazaki K, et al. Hybrid carcinomas of the salivary glands: report of nine cases with a clinicopathologic, immunohistochemical, and p53 gene alteration analysis. Mod Pathol. 2002;15: Snyder ML, Paulino AF. Hybrid carcinoma of the salivary gland: salivary duct adenocarcinoma adenoid cystic carcinoma. Histopathology. 1999;35: To read this article online, scan the QR code, ascpjournals.org/content/45/2/141. full.pdf+html 146 Lab Medicine Spring 2014 Volume 45, Number 2
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