|Year : 2013 | Volume
| Issue : 3 | Page : 138-144
Intraoral myoepithelial tumors: A review and case reports
Meena Kulkarni1, Deepak Kulkarni2, B Sushma3, Yashwant Ingle4
1 Department of Oral Pathology and Microbiology, Dr. DY Patil Dental College and Hospital, Pune, Maharashtra, India
2 Department of Oral and Maxillofacial Surgery, Dr. DY Patil Dental College and Hospital, Pune, Maharashtra, India
3 Department of Oral and Maxillofacial Pathology, School of Dental Sciences, Krishna Dental College and Hospital, Karad, Maharashtra, India
4 Department of Oral Pathology and Microbiology, MA Rangoonwala College of Dental Science, Pune, Maharashtra, India
|Date of Submission||17-Feb-2013|
|Date of Acceptance||12-May-2013|
|Date of Web Publication||12-Dec-2013|
Department of Oral Pathology and Microbiology, Dr. D. Y. Patil Dental College and Hospital, Dr. D Y Patil Vidyapeeth, Pimpri, Pune 411 018, Maharashtra
Source of Support: None, Conflict of Interest: None
Myoepithelial cells that express both epithelial and smooth muscle phenotype have a potential to differentiate into various cytomorphologic forms such as spindle, plasmacytoid, epitheloid and clear cells. Salivary gland tumors composed entirely or almost exclusively of myoepithelial cells are referred to as myoepitheliomas. They may be benign or malignant in nature and about 90% of them are benign and only 10% are malignant. The palate is the most common intraoral site of occurrence for both the variants. In this paper, we report one case of myoepithelioma occurring on the palate and two cases of myoepithelial carcinomas, one seen on the palate and the other rare case seen on the alveolar mucosa, along with an elaborate review on benign and malignant myoepitheliomas of salivary glands along with their ultra-structural, cytological and immunohistochemical profiles.
Keywords: Alveolar ridge, myoepithelial carcinoma, myoepithelial cells, myoepithelioma, palate
|How to cite this article:|
Kulkarni M, Kulkarni D, Sushma B, Ingle Y. Intraoral myoepithelial tumors: A review and case reports. Indian J Oral Sci 2013;4:138-44
|How to cite this URL:|
Kulkarni M, Kulkarni D, Sushma B, Ingle Y. Intraoral myoepithelial tumors: A review and case reports. Indian J Oral Sci [serial online] 2013 [cited 2019 Nov 20];4:138-44. Available from: http://www.indjos.com/text.asp?2013/4/3/138/122965
| Introduction|| |
Myoepithelial cells are contractile cells, which express a dual epithelial and smooth muscle phenotype. , These are located around the terminal secretory units and intercalated ducts of the salivary gland and lies between the basal lamina and secretory acini connected by desmosomal junctions.  These cells are also known as "Basket cells" as their appearance is reminiscent of a basket cradling the secretory unit  or "Octopus sitting on the rock." In addition to their presence in major and minor salivary glands, they are also present in secretory portion of the sweat glands, apocrine glands,  duct of mammary glands, Bartholin's glands, mucous producing glands of the trachea, esophagus, prostate and lacrimal glands. Sciubba  suggested that the terminal tubule epithelial cell may serve as the stem or the precursor cell for the myoepithelial cell lineage. These cells are not clearly seen under the light microscope and can be readily detected using electron microscopy or by immunohistochemistry.  Recently, the new immunohistochemical markers such as p63 and maspin have shown to highlight the myoepithelial cell component in various intraoral myoepithelial tumors.  The myoepithelial cells have a potential to differentiate into various cytomorphologic forms such as spindle, plasmacytoid, epitheloid and clear cells.
Salivary gland tumors composed entirely or almost exclusively of myoepithelial cells are referred to as myoepitheliomas. , These are also known as myoepithelial adenomas or benign myoepithelial tumors. Myoepitheliomas are rare tumors that represent about 1-1.5% of the salivary gland tumors. ,, They may be benign or malignant in nature of which about 90% of them are benign and only 10% are malignant.  The malignant counterpart of myoepithelioma is known as myoepithelial carcinoma or malignant myoepithelioma. These tumors develop from pre-existing pleomorphic adenoma or arise de novo. ,,, The parotid gland is the most common site of occurrence for both the benign and malignant myoepitheliomas, whereas palate is the most common intraoral site. Both sexes are equally affected and the average age of occurrence is 9-85 years for benign myoepitheliomas  and above 50 years for myoepithelial carcinomas.  The other sites include submandibular gland, retromolar area, floor of the mouth, tongue  and soft palate.  The growth pattern varies from solid, myxoid or recticular and the component cells are spindle shaped, plasmacytoid, hyaline, clear or epitheliod. 
In this paper, we report one case of myoepithelioma and two cases of myoepithelial carcinomas seen intra-orally, along with an extensive review on myoepithelial neoplasms of salivary glands.
| Case Reports|| |
A 67-year-old male reported to Department of Oral Medicine, D Y Patil Dental College and Hospital, Dr D Y Patil Vidyapeeth, Pune with a complaint of painless palatal swelling of 5 years duration. On intraoral examination, the swelling was ovoid in shape, measuring 5 cm × 4 cm in dimension, soft to firm in consistency and was not tender on palpation [Figure 1]a. The overlying surface was not ulcerated. A computed tomography (CT) revealed a well-defined mass located in the posterior portion of palate extending into the nasopharynx measuring approximately 2.38 cm × 2.56 cm in dimension [Figure 1]b. Hematological investigations were done which revealed values within normal limits. Lacking a sure diagnosis, an incisional biopsy was performed under general anesthesia and histopathological diagnosis was made as myoepithelioma.
|Figure 1: Case 1 - (a) Clinical photograph showing intraoral sessile swelling on the left side of the palate with a smooth surface. (b) Computed tomograph showing a large, well circumscribed radiopaque lesion on the left side of maxilla extending posterioinferiorly into the nasopharynx. (c) Photomicrograph showing sheets of plasmacytoid cells with indistinct cell borders and intercellular pinkish, hyaline, basement membrane material. There is no evidence of cellular or nuclear pleomorphism or acini formation (d) Photomicrograph showing sheets of plasmacytoid cells which exhibit typical eccentric hyperchromatic nucleus with regular nuclear borders and abundant eosinophilic, amorphous pink cytoplasm. There is an absence of abnormal mitosis or bizarre cells or acini formation|
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Photomicrograph with ×10 revealed sheets of plasmacytoid cells with indistinct cell borders and intercellular basement membrane like material. There was no evidence of cellular or nuclear pleomorphism or acinus formation [Figure 1]c. Under ×40 magnification, these sheets of plasmacytoid cells exhibited typical eccentric hyperchromatic nucleus with abundant eosinophilic, amorphous pink cytoplasm [Figure 1]d. These features classically represented the picture of myoepithelioma. There was no history of recurrence till date.
A 42-year-old male presented with the history of pain and swelling on the right side of the lower jaw since 1 year. On intraoral examination, the swelling was located on the alveolar mucosa, well circumscribed having an ulcerated surface, soft in consistency, ovoid in shape measuring about 5 cm × 7 cm in dimension and was tender on palpation [Figure 2]a. Orthopantomograph revealed a large lytic lesion with erosion of the right side of the mandible [Figure 2]b. Blood investigations were within normal limits. Incisional biopsy was performed under general anesthesia.
Though the literature refers palate as the most common location with multi-nodular growth pattern for this tumor, the present case showed involvement of the alveolar mucosa with no multi-nodular growth pattern.
|Figure 2: Case 2 - (a) Clinical photograph showing an intraoral swelling on the vestibular zone of the right lower jaw with central, rough, irregular ulcerated surface. (b) A cropped orthopantomograph showing a large, well circumscribed radiolucent lesion on the right side of the mandible. (c) Photomicrograph showing highly cellular areas admixed with pinkish eosinophilic intercellular basement membrane material. The cellular borders are indistinct with few cells with clear cytoplasm. (d) Photomicrograph showing the tumor cells positive for cytokeratin 19 as a dark brownish blackish discoloration at nuclear membrane. (e) Photomicrograph showing tumor cells positive for S 100|
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Photomicrograph under ×10 demonstrated highly cellular areas admixed with pinkish eosinophilic intercellular basement membrane material. The cellular borders were indistinct with few cells exhibiting clear cytoplasm [Figure 2]c. Cellular and nuclear pleomorphism was evident. Nuclei were large and vesicular with prominent nucleoli. Mitotic figures were numerous with focal areas showing abnormal mitosis. Immunohistochemical profile was done using cytokeratin (CK) 19 and S-100 which showed positivity for both [Figure 2]d and e. The overall impression was myoepithelial carcinoma.
A 63-year-old female reported to Department of Oral Medicine, D Y Patil Dental College, Pune with a complaint of difficulty in swallowing and a swelling on the palate since 1-2 months. The patient was edentulous and was using complete dentures. On intraoral examination, the swelling was well circumscribed with a smooth surface and with no ulceration of the overlying mucosa. The swelling was round to oval in shape, soft to firm in consistency and slightly tender on palpation measuring about 5 cm × 6 cm in dimension [Figure 3]a. CT of the maxilla revealed a well-defined soft tissue density lesion along the soft palate projecting into the oropharynx. The lesion measured approximately 31 mm × 24 mm in dimension. There was no bony destruction of the hard palate. The bony walls of the maxillary sinus and the pterygoid plates were intact [Figure 3]b. No significant localized lymphadenopathy was seen. Incisional biopsy was performed and a diagnosis of myoepithelial neoplasm was given. The patient underwent surgical excision and the excisional biopsy was reported as myoepithelial carcinoma.
|Figure 3: Case 3 - (a) Clinical photograph showing an intraoral sessile swelling on the palate. (b) Orthopantomograph showing a well-defined rounded enhancing soft tissue density lesion along the soft palate projecting into the oropharynx with no bony destruction of the hard palate. (c) Photomicrograph showing tumor with moderate cellular as well as nuclear pleomorphism, high mitotic activity in the tumor cells admixed with intercellular basement membrane material. (d) Photomicroghaph showing moderately pleomorphic tumor cells with ill-defined cell borders and high N/C ratio. At places hyperchromatic nuclei, irregular nuclear borders, prominent nucleoli, increased mitotic activity and clear cytoplasm are evident|
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Most of the literature shows that these tumors develop in patients with multiple recurrences of benign myoepithelioma or from pre-existing pleomorphic adenoma, but in our case there was no such previous history.
Photomicrograph under ×10 demonstrated neoplastic cells with moderate cellular and nuclear pleomorphism, high mitotic activity in the tumor cells admixed with intercellular basement membrane material [Figure 3]c. Under ×40, the pleomorphic tumor cells demonstrated indistinct cell borders, high nuclear-cytoplasmic ratio, vesicular hyperchromatic nuclei, irregular nuclear borders, prominent nucleoli and clear cytoplasm [Figure 3]d. Basement membrane material was evident in between neoplastic cells. The histopathological features were consistent with those of malignant myoepithelioma.
| Discussion|| |
The term myoepithelioma was first introduced by Sheldon in 1943. ,, World Health Organization (WHO) defined myoepithelioma as "a benign salivary gland tumor composed almost exclusively of sheets, islands or cords of cells with myoepithelial differentiation that may exhibit spindle, plasmacytoid, epitheliod or clear cytoplasmic features". 
Myoepitheliomas are recognized as a histologically separate entity by the WHO since 1991. Some authors such as Simpson Batsakis et al. considered these tumors as monomorphic variant of pleomorphic adenoma. Few others described these tumors to be composed purely of myoepithelial cells as in monomorphic adenoma.  However, according to Dardick et al. these tumors do not show ductal differentiation histologically as seen in pleomorphic adenomas.
Myoepitheliomas are rare tumors that represent about 1-1.5% of the salivary gland tumors. ,, The parotid gland is the most common site and palate is the most common intraoral site of occurrence. There is no significant gender predilection. The age of occurrence for myoepitheliomas is 9-85 years with the mean average being 44 years and for myoepithelial carcinoma is above 50 years. These tumors occur rarely in children. There is no clear etiological factor identified for these tumors.
Majority of the myoepitheliomas are characterized by asymptomatic, slowly growing mass. Macroscopically, these tumors appear as well circumscribed and are frequently encapsulated. The parotid gland myoepitheliomas are usually encapsulated whereas the minor salivary gland myoepitheliomas are partially encapsulated or sometimes non-encapsulated.  They usually measure about 3-5 cm in diameter. These solid masses are grayish white or show a yellow tan having a smooth outline. ,
Histopathologically, myoepithelioma is composed exclusively of modified myoepithelial cells in which the phenotypic expression of the normal myoepithelial cells are altered. These cells are arranged in the form of sheets and islands of various proportions of spindle, plasmacytoid, epitheliod and clear cells with no ductal differentaiation. Among these, the spindle type is the most common and the clear cell type is the least common. 
The spindle type consists of proliferation of spindle shaped cells with central fusiform or cigar shaped nuclei and eosinophilic cytoplasm. The nuclei of these cells show delicately dispersed chromatin and a thin nuclear envelope that occupies most of the cell body. They tend to be bipolar with eosinophilic granular or fibrillar cytoplasm. In the solid areas of the tumors, these cells assume a swirling interdigitating pattern with orthogonally arranged cell clusters.  Few cases also show pseudomicrocystic pattern with less compact arrangement of individual cells.
The plasmacytoid type is the most commonly encountered variant in the minor salivary glands and palate is the frequently involved intraoral site. It is characterized by round to ovoid cells with distinctive eosinophilic hyaline cytoplasm and eccentrically placed nuclei. These cells mainly occur in clusters in abundant mucoid stroma.
The epitheloid type is characterized by large polygonal cells with centrally located nuclei and eosinophilic cytoplasm. Focal areas of clearing in the cytoplasm is also seen.
The clear cell type, which is the rarest variant is characterized by polygonal cells with clear cytoplasm due to their glycogen content. These cells exhibit signet ring or lipoblast like appearance.
Cytologically, the smears of myoepitheliomas are characterized by sheets and small clusters of spindle, plamacytoid, epithelioid cells with moderate amounts of pale blue cytoplasm. The nuclei are rounded with a granular, evenly distributed chromatin and inconspicuous nucleoli. The extracellular matrix is composed of fibrillary material, which appears pale green when stained with papanicolaou stain. Glandular structures, tubule formations and chondroid matrix, mitosis, necrosis and cytologic atypia are all absent.  In case of myoepithelial carcinoma, all the above features with mitosis, necrosis and cytologic atypia are seen.
The cytology of various salivary gland tumors mimick myoepithelioma. For example, the aspirated material from polymorphous low grade adenocarcinoma (PLGA) yields cohesive sheets of epithelial cells admixed with myxoid stroma, which resembles myoepithelioma. The tumor cells palisading around the myxoid stroma is a characteristic feature of PLGA. This is generally not seen in case of myoepithelioma.  The smears from cystic Adenoid cystic carcinoma generally show polygonal cells with abundant granular cytoplasm and marked cell dissociation. The abundant myxoid fibrillary stroma commonly observed in myoepithelioma is not seen in Adenoid cystic carcinoma. 
Fine needle aspiration material from high-grade mucoepidermoid carcinoma and squamous cell carcinoma generally are differentiated from myoepithelioma, based on their marked cytologic atypia and/or evidence of keratinization. 
Ultra-structurally, both the spindle and plasmacytoid type reveal a scant collagenous stroma between cell clusters. Electron microscopic studies show that a thin basal lamina is usually present between the tumor cells and the supportive stroma. The organization of fibrils also differ in between the spindle and plasmacytoid type. In the spindle cell type, fibrils are arranged parallel to the long axis of the cell and measure approx. 6 nm in diameter with randomly dispersed focal densities. Focal densities along the thin filaments are noted only in this type. In the plasmacytoid type, fibrils and their dimension are same, but the overall organization of fibrils are disordered and do not exhibit focal densities as noted in the spindle type. The character of the filaments within myoepithelial cells is similar to that of the actin filaments of the skeletal and smooth muscle cells. Although some investigators suggest that the filaments within the spindle and plasmacytoid cells represent tonofilaments, the overall pattern showed a predominance of the actin proteins. 
Crystalloid structures are rarely observed in salivary gland tumors and there are three different types of crystalloids namely tyrosine rich crystalloids, oxalate crystalloids and collagenous crystalloids. In salivary gland neoplasms such as pleomorphic adenoma, myoepithelioma and myoepithelial carcinoma, the collagenous crystalloids which are composed of radially arranged needle shaped fibers are most commonly encountered. These structures are scattered throughout the connective tissue and are surrounded by myoepithelial cells. The origin of these crystalloids is not clear, but it has been suggested that type III collagen might be involved in its formation. They are also positive for type I collagen. X-ray microanalysis of the collagenous crystalloids showed up-regulation of sulphur in the electron dense parts of stroma as compared to other parts. 
Normal myoepithelial cells express positivity for AE1/AE3; CK 5, 6, 7; murine monoclonal antibody anti-cytokeratin CAM 5.2 and CK 14, S-100, glial fibrillary acidic protein (GFAP).  The tumor cells are positive for markers such as calponin, smooth muscle actin (SMA), muscle specific actin, smooth muscle myosin and p63. Combination of these markers provide a more definitive diagnosis of these tumors as there exsits a difference in positivity of these markers. For example, spindle cell type shows strong positivity for SMA whereas clear cell type shows negativity for SMA. Myoepithelial cells are negative for carcinoembryonic antigen, which suggests that they do not exhibit ductal differentiation. 
Cytogenetic studies by El-Naggar et al.  demonstrated structural alterations of chromosomes 1, 9, 12 and 13: t (1;12)(q25;q12), del (9)(q22.1;q22.3), del (13)(q12;q22) in parotid myoepitheliomas whereas Hungermann et al.  showed structural alterations involving chromosome 2, 4, 8. Mutations in p53 have also been observed by Weber et al. in 25% of myoepitheliomas. Vιkony et al.  demonstrated that p61INK4a pathway dysregulation was involved in the development of the myoepithelial tumors.
The differential diagnosis of myoepithelioma depends on the predominant cell type. In case of spindle type, the differential diagnosis includes neurilemmoma, fibroma, leiomyoma and extra-cranial meningioma. These lesions can be differentiated by using electron microscopy and immunohistochemistry. In case of plasmacytoid type, the differential diagnosis includes plasmacytoma and multiple myeloma.
The malignant counterpart of myoepithelioma is known as myoepithelial carcinoma or malignant myoepithelioma. It was first described by Stromeyer Barnes et al. in 1975. The tumor is included in the WHO classification of salivary gland neoplasms as a distinct clinicopathologic entity since 1991.
WHO defined myoepithelial carcinoma as a neoplasm composed entirely of myoepithelial differentiation characterized by infiltrative growth and potential for metastasis. It accounts for about less than 1% of all salivary gland tumors. It may develop in patients with multiple recurrences of benign myoepithelioma or from pre-existing pleomorphic adenoma or de novo.  The one arising from the pre-existing pleomorphic adenoma was thought to be an indication of low grade malignancy and that arising de novo was thought to be an indication of high grade malignancy.  Few authors proposed that those tumors showing ductal differentiation arose from carcinoma ex pleomorphic adenoma, whereas others considered them to be purely myoepithelial in origin. 
Clinically, the myoepithelial carcinoma show multi-nodular growth pattern. Tumor infiltration into adjacent normal tissue is the most important histological feature that distinguishes malignant from benign myoepithelial neoplasms and should be considered the minimum requirement for the diagnosis of myoepithelial carcinoma. The tumor size ranges from 2 cm to 10 cm in diameter. The parotid gland is the most common site and palate is the most common intraoral site of occurrence. Equal sex distribution is seen. Most of the cases occur after the age of 50. The cut surface is gray white and glassy. Some tumors may also show areas of necrosis, hemorrhage and cystic degeneration.
Histologically, it is characterized by tumor cells, which form solid, sheet like formations, trabeculae or reticular patterns within myxoid or hyaline stroma. The tumor cells are spindled, plasmacytoid, epitheloid and occasionally vacuolated with signet ring like appearance. The neoplastic nodules frequently have necrotic centers. Pseudocystic degeneration can occur. Sparse areas with squamous differentiation may also be found. High mitotic activity, cellular pleomorphism and necrosis are also seen.  No specific mitotic rate cutoffs exists but >7 mitosis per high power fields is proposed as criteria for diagnosis of malignancy.  It has been also been suggested that the assessment of the cell proliferative index Ki67 of more than 10% is diagnostic of myoepithelial carcinoma.  Multinucleated tumor giant cells were reported in 2 cases of myoepithelial carcinoma. 
The differential diagnosis of myoepithelial carcinoma also depends on the predominant cell type. In case of spindle type, the differential includes hemangiopericytoma, schwannoma, fibrosarcoma, leiomyosarcoma. Plasmacytoid type should be distinguished from plasmmacytoma, malignant melanoma and large cell lymphoma. Immunohistochemistry is required for differentiating these lesions. Myoepithelial carcinoma should be distinguished from metastatic tumor like renal cell carcinoma. These tumors show keratin, epithelial membrane antigen and vimentin positivity and are negative for S-100, actin and GFAP. 
The differentiating features between myoepithelioma and myoepithelial carcinoma is illustrated in the [Table 1].
|Table 1: Illustrates the differentiating features between myoepithelioma and myoepithelial carcinoma |
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The treatment for both the benign and malignant myoepithelioma includes wide surgical excision. Therapeutic neck dissection and radiotherapy are indicated in cases showing metastasis.
| Summary|| |
This article compiles three cases of intraoral myoepithelial tumors, of which one is a benign myoepithelioma located on the palate and one cases of myoepithelial carcinoma, one on the palate and the other on a very rare and unusual location on the alveolar mucosa. It also reviews myoepithelial tumors of salivary glands, differentiating features of the benign and the malignant myoepitheliomas along with the ultra-structural and cytological features and their immunohistochemical profile.
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[Figure 1], [Figure 2], [Figure 3]