Case 10. At gross examination, the parotid gland and the overlying skin were infiltrated by a whitish, firm mass with extensive necrosis.
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1 Case 10 Isabel Fonseca MD PhD Serviço de Anatomia Patológica, Instituto Português de Oncologia Francisco Gentil Lisboa & Instituto de Anatomia Patológica, Faculdade de Medicina de Lisboa, Portugal Case History An 81 year-old farmer presented with a parotid gland mass in He referred that the nodule was present for some years but with a rapid sudden growth in a few weeks after being hit by a tree branch. A 10 cm skin-infiltrating tumour and facial paralysis lead to a total parotidectomy. At gross examination, the parotid gland and the overlying skin were infiltrated by a whitish, firm mass with extensive necrosis. In low-power view, the gland was totally replaced by a mixed solid and cystic cell proliferation, some areas showing extensive keratinization with typical keratin pearls. The more solid areas were formed by aggregates of squamoid cells, with eccentric nuclei, some with clear cell cytoplasmic change. At the periphery of the tumour aggregates there was a rim of smaller cells, with scant cytoplasm and central, hyperchromatic nuclei. A population of mucin-producing cells, with signet-ring morphology, highlighted by PAS stain, was present being extensive in some areas. The areas with predominance of squamous differentiation also showed focal clear cell change, marked nuclear pleomorphism and high mitotic activity. In these areas, although present, mucin-producing cells were rare. Transition areas between the two patterns were present. The stroma was densely desmoplastic. There was perineural and vascular invasion. The original diagnosis was adenosquamous carcinoma but, upon review, the presence of typical mucoepidermoid carcinoma areas and transition areas to typical squamous areas changed the diagnosis to mucoepidermoid carcinoma with high-grade transformation. This 1
2 diagnosis was confirmed by the presence of MAML2 rearrangement using FISH analysis and immunohistochemistry. The patient did not receive further treatment and was well, without evidence of disease, 2 years after the diagnosis. Diagnosis Mucoepidermoid carcinoma (grade II) with high-grade transformation. Discussion This case allows the discussion of two relevant issues in salivary gland carcinoma pathology: (1) high-grade tumour transformation (also reported as tumour dedifferentiation) and (2) the use of biomarkers in routine clinical practice. High-grade transformation of salivary gland carcinoma High-grade transformation in salivary gland carcinomas is characterized by the presence of either poorly differentiated or undifferentiated areas in which epithelial, myoepithelial and mixed phenotypes are recognizable. This phenomenon can occur de novo or, most frequently, in the setting of a long-standing, often recurrent disease. Stanley and co-workers published the first report of high-grade transformation phenomenon in salivary carcinomas in 1988 in a case of acinic cell carcinoma. Since then, similar findings were reported in adenoid-cystic carcinoma, epithelial-myoepithelial carcinoma, polymorphous low-grade adenocarcinoma and clear cell carcinoma, NOS. This was also denominated as dedifferentiation but the term high-grade transformation is nowadays favoured. Despite the fact that high-grade transformation can occur in various salivary tumours types, either epithelial or myoepithelial, with different histogenesis it usually shows the morphological characteristics of poorly differentiated carcinoma or adenocarcinoma. Myoepithelial differentiation can be present and be highlighted by immunohistochemistry in biphasic tumours. However, as stated by Roy and co-workers the phenotype (epithelial or 2
3 myoepithelial) identified within poorly differentiated areas appears to have no impact on the prognosis. Tumours with high-grade transformation are associated with increased risk of lymph node metastasis, local recurrence and distant progression as compared to those that do not exhibit it. This phenomenon is better documented in adenoid-cystic carcinoma where it mostly occurs in tumours arising in minor salivary glands, with a much higher (around 50%) incidence of nodal metastasis and poorer survival rates. In adenoid-cystic carcinoma, Seethala and co-workers proposed the following morphological criteria for the definition of high-grade transformation: increased nuclear size, solid growth pattern in a least one highpower field, desmoplastic stroma, presence of squamoid areas, increased mitotic activity with high Ki67 indexes, overexpression of p53 and loss of the myoepithelial cell elements. However, the small number of cases published in the literature does not allow their validation. High-grade transformation was reported in a similar number of acinic cell carcinomas and epithelial-myoepithelial carcinomas (around 50), in less than 10 cases of polymorphous lowgrade adenocarcinoma and in a single case of clear cell carcinoma NOS. Nagao and co-workers first reported high-grade transformation in MEC in 2003 describing an anaplastic, undifferentiated carcinoma component in an otherwise classical MEC. Since then, only one case was published by Subramaniam and co-workers recording the association of low-grade MEC with anaplastic and spindle cell carcinoma in a tracheal neoplasm of an 11 year-old girl. In the present case, the high-grade component displayed the morphology of poorly differentiated squamous cell carcinoma with extensive keratinization together with foci of anaplastic carcinoma. It is arguable that this case could represent a grade III MEC with marked anaplasia. However, the presence of areas with extensive keratinization (which is a known criterion for excluding the diagnosis of MEC) together with the presence of transition areas favour the interpretation that these findings represent high-grade transformation, in a tumour clinically suggestive of having arisen in a long-standing lesion. 3
4 The diagnosis of MEC was further confirmed by the demonstration of MAML2 rearrangement, which illustrates the usefulness of biomarkers for the classification of lesions with confounding morphology. As stated by Chenevert and co-workers, the routine use of fusion evaluation may allow to fine tune the amount of keratinisation permitted in MEC, drawing the line with the adenosquamous carcinoma and the squamous cell carcinoma, especially when they occur in mucosa lined sites. MAML2 rearrangement use in routine clinical practice MEC has a karyotypic profile, with recurrent rearrangements of chromosomal bands 11q21 and 19p13 that usually present as a balanced t(11;19) translocation, frequently as the sole cytogenetic alteration. This chromosomal rearrangement, cloned by Tonon and co-workers in 2003, creates a chimerical gene product that fuses the protein coding regions of CRTC1 exon1 in-frame with exons 2-5 of the MAML2 gene. More recently another variant fusion gene CRTC3-MAML2 was reported in MEC. The fusion oncogene activates both Notch target genes that are independent of ligands, and CREB-response genes. Although CRTC1-MAML2 fusion was initially reported exclusively in MEC arising in salivary glands and lung, it has also been found in tumours with MEC morphology located at other sites: skin, breast, thyroid and uterine cervix. The CRTC1-MAML2 fusion was also found in a subset of Warthin s tumours that show metaplastic squamous change. The study of a larger cohort of cases is needed to validate the use of CRTC1/3-MAML2 fusion. However, current knowledge point to use this test as a tool regarding the differential diagnosis of MEC-like lesions that display mixed glandular and squamous morphology, show clear and oncocytic features, and arising in salivary glands, upper aerodigestive tract mucosa, odontogenic tissues and in non-head and neck region. This is also valid for head and neck central, intraosseous lesions. There is accumulated evidence in the literature that MEC is fusion-positive in around 60% of the cases, mostly grade I and grade II lesions. Moreover, fusion-positive MECs have a better prognosis, and it has been suggested by Okumura and co-workers that the presence of the CRTC1/3-MAML2 fusion has prognostic value that is independent of the histological grade and the clinical stage at presentation and defining a separate group of fusion-positive MEC 4
5 behaving favourably. These authors suggest that histological grading should only be used in fusion-negative cases, where low-grade tumours have a disease-free survival and overall survival similar to the fusion-positive cases. These findings are of major clinical relevance and may warrant the systematic evaluation of CRTC1/3-MAML2 fusion in all cases of MEC. References High-grade transformation of salivary carcinomas - Alos L, Carrillo R, Ramos J, Baez JM, Mallofre C, Fernandez PL, Cardesa A. High-grade carcinoma component in epithelial-myoepithelial carcinoma of salivary glands: clinicopathological, immunohistochemical and flow-cytometric study of three cases. Virchows Arch 1999; 434: Brandwein MS, Ivanov K, Wallace DI, Hille JJ, Wang B, Fahmy A, Bodian C, Urken ML, Gnepp DR, Huvos A, Lumerman H, Mills SE. Mucoepidermoid carcinoma. A clinicopathologic study of 80 patients with special reference to histological grading. Am J Surg Pathol 2001; 25: Cheuk W, Chan JK, Ngan RK. Dedifferentiation in adenoid cystic carcinoma of salivary gland: an uncommon complication associated with an accelerated clinical course. Am J Surg Pathol 1999; 23: Costa AF, Altemani A, Hermsen M. Current concepts on dedifferentiation/high-grade transformation in salivary gland tumors. Patholog Res Int 2011; 2011: Epub 2011 Aug 17 - Fonseca I, Félix A, Soares J. Dedifferentiation in salivary gland carcinomas. Am J Surg Pathol 2000; 24: Jin R, Craddock KJ, Irish JC, Perez-Ordonez B, Weinreb I. Recurrent hyalinizing clear cell carcinoma of the base of the tongue with high-grade transformation and EWSR1 gene rearrangement by FISH. Head Neck Pathol 2012; DOI: /s Luna MA. Salivary mucoepidermoid carcinoma: revisited. Adv Anat Pathol 2006; 13: Nagao T, Gaffey TA, Kay PA, Unni KK, Nascimento AG, Sebo TJ, Serizawa H, Minato H, Lewis JE. Dedifferentiation in low-grade mucoepidermoid carcinoma of the parotid gland. Hum Pathol 2003; 34: Pelkey TJ, Mills SE. Histologic transformation of polymorphous low-grade adenocarcinoma of salivary gland. Am J Clin Pathol 1999; 111:
6 - Seethala RR, Hunt JL, Baloch ZW, Livolsi VA, Leon Barnes E. Adenoid cystic carcinoma with highgrade transformation: a report of 11 cases and a review of the literature. Am J Surg Pathol 2007; 31: Simpson RH, Pereira EM, Ribeiro AC, Abdulkadir A, Reis-Filho JS. Polymorphous low-grade adenocarcinoma of the salivary glands with transformation to high-grade carcinoma. Histopathology 2002; 41: Stanley RJ, Weiland LH, Olsen KD, Pearson BW. Dedifferentiated acinic cell (acinous) carcinoma of the parotid gland. Otolaryngol Head Neck Surg 1988; 98: Subramaniam MM, Ng SB, Seah SB, Anuar D, Soong R, Lee VK. Molecular characterization of dedifferentiated mucoepidermoid carcinoma of the trachea using laser microdissection-based TP53 mutation analysis. Histopathology 2009; 55: CRTC1/3-MAML2 fusion in mucoepidermoid carcinoma - Behboudi A, Enlund F, Winnes M, Andrén Y, Nordkvist A, Leivo I, Flaberg E, Szekely L, Mäkitie A, Grenman R, Mark J, Stenman G. Molecular classification of mucoepidermoid carcinomasprognostic significance of the MECT1-MAML2 fusion oncogene. Genes Chromosomes Cancer 2006; 45: Bell D, Luna MA, Weber RS, Kaye FJ, El-Naggar AK. CRTC1/MAML2 fusion transcript in Warthin's tumor and mucoepidermoid carcinoma: evidence for a common genetic association. Genes Chromosomes Cancer 2008; 47: Camelo-Piragua SI, Habib C, Kanamurri P, Lago CE, Mason HS, Otis CN. Mucoepidermoid carcinoma of the breast shares cytogenetic abnormality with mucoepidermoid carcinoma of the salivary glands: a case report with molecular analysis and review of the literature. Hum Pathol 2009; 40: Chenevert J, Barnes LE, Chiosea SI. Mucoepidermoid carcinoma: a five-decade journey. Virchows Arch 2011; 458: Enlund F, Behboudi A, Andrén Y, Oberg C, Lendahl U, Mark J, Stenman G. Altered Notch signalling resulting from expression of a WAMTP1-MAML2 gene fusion in mucoepidermoid carcinomas and benign Warthin's tumors. Exp Cell Res 2004; 292: Fehr A, Röser K, Heidorn K, Hallas C, Löning T, Bullerdiek J. A new type of MAML2 fusion in mucoepidermoid carcinoma. Genes Chromosomes Cancer 2008; 47:
7 - García JJ, Hunt JL, Weinreb I, McHugh JB, Barnes EL, Cieply K, Dacic S, Seethala RR. Fluorescence in situ hybridization for detection of MAML2 rearrangements in oncocytic mucoepidermoid carcinomas: utility as a diagnostic test. Hum Pathol 2011; 42: Lennerz JK, Perry A, Mills JC, Huettner PC, Pfeifer JD. Mucoepidermoid carcinoma of the cervix: another tumor with the t(11;19)-associated CRTC1-MAML2 gene fusion. Am J Surg Pathol 2009; 33: Martins C, Cavaco B, Tonon G, Kaye FJ, Soares J, Fonseca I. A study of MECT1-MAML2 in mucoepidermoid carcinoma and Warthin's tumor of salivary glands. J Mol Diagn 2004; 6: Nakayama T, Miyabe S, Okabe M, Sakuma H, Ijichi K, Hasegawa Y, Nagatsuka H, Shimozato K, Inagaki H. Clinicopathological significance of the CRTC3-MAML2 fusion transcript in mucoepidermoid carcinoma. Mod Pathol 2009; 22: Okabe M, Miyabe S, Nagatsuka H, Terada A, Hanai N, Yokoi M, Shimozato K, Eimoto T, Nakamura S, Nagai N, Hasegawa Y, Inagaki H. The MECT1-MAML2 fusion transcript defines a favourable subset of mucoepidermoid carcinoma: a molecular and clinicopathological study of 71 cases. Clin Cancer Res 2006; 12: Okumura Y, Miyabe S, Nakayama T, Fujiyoshi Y, Hattori H, Shimozato K, Inagaki H. Impact of CRTC1/3-MAML2 fusions on histological classification and prognosis of mucoepidermoid carcinoma. Histopathology 2011; 59: Schwarz S, Stiegler C, Müller M, Ettl T, Brockhoff G, Zenk J, Agaimy A. Salivary gland mucoepidermoid carcinoma is a clinically, morphologically and genetically heterogeneous entity: a clinicopathological study of 40 cases with emphasis on grading, histological variants and presence of the t(11;19) translocation. Histopathology 2011; 58: Seethala RR, Dacic S, Cieply K, Kelly LM, Nikiforova MN. A reappraisal of the MECT1/MAML2 translocation in salivary mucoepidermoid carcinomas. Am J Surg Pathol 2010; 34: Tirado Y, Williams MD, Hanna EY, Kaye FJ, Batsakis JG, El-Naggar AK. CRTC1/MAML2 fusion transcript in high-grade mucoepidermoid carcinomas of salivary and thyroid glands and Warthin's tumors: implications for histogenesis and biologic behavior. Genes Chromosomes Cancer 2007; 46: Tonon G, Modi S, Wu L, Kubo A, Coxon AB, Komiya T, O'Neil K, Stover K, El-Naggar A, Griffin JD, Kirsch IR, Kaye FJ. t(11;19)(q21;p13) translocation in mucoepidermoid carcinoma creates a novel fusion product that disrupts a Notch signalling pathway. Nat Genet 2003; 33:
8 - Wu L, Liu J, Gao P, Nakamura M, Cao Y, Shen H, Griffin JD. Transforming activity of MECT1- MAML2 fusion oncoprotein is mediated by constitutive CREB activation. EMBO J 2005; 24:
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