Clear Cell Neoplasms of Salivary Glands: A Diagnostic Challenge.


Journal

Advances in anatomic pathology
ISSN: 1533-4031
Titre abrégé: Adv Anat Pathol
Pays: United States
ID NLM: 9435676

Informations de publication

Date de publication:
01 Jul 2022
Historique:
pubmed: 8 3 2022
medline: 10 6 2022
entrez: 7 3 2022
Statut: ppublish

Résumé

This review focuses on the heterogenous group of clear cell neoplasms of salivary glands and attempts to identify major differential diagnostic features. Within the head and neck region, clear cells are found most commonly in salivary gland tumors, but may also be seen in tumors of squamous or odontogenic epithelial origin, primary or metastatic carcinomas, benign or malignant melanocytic lesions, or benign or malignant mesenchymal tumors. Clear cells occur fairly commonly among a wide variety of salivary gland neoplasms, but mostly they constitute only a minor component of the tumor cell population. Clear cells represent a major diagnostic feature in two salivary gland neoplasms, epithelial-myoepithelial carcinoma and hyalinizing clear cell carcinoma. In addition, salivary gland neoplasms composed predominantly of clear cells could also include clear cell variants of other salivary neoplasms, such as mucoepidermoid carcinoma and myoepithelial carcinoma, but their tumor type-specific histologic features may only be available in limited nonclear cell areas of the tumor. Diagnosing predominantly clear cell salivary gland tumors is difficult because the immunoprofiles and morphologic features may overlap and the same tumor entity may also have a wide range of other histologic presentations. Many salivary gland tumors are characterized by tumor type-specific genomic alterations, particularly gene fusions of the ETV6 gene in secretory carcinoma, the MYB and MYBL1 genes in adenoid cystic carcinoma, the MAML2 gene in mucoepidermoid carcinoma, the EWSR1 gene in hyalinizing clear cell carcinoma, and others. Thus, along with conventional histopathologic examination and immunoprofiling, molecular and genetic tests may be important in the diagnosis of salivary gland clear cell tumors by demonstrating genetic alterations specific to them.

Identifiants

pubmed: 35249992
doi: 10.1097/PAP.0000000000000339
pii: 00125480-202207000-00004
doi:

Substances chimiques

Biomarkers, Tumor 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

217-226

Informations de copyright

Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.

Déclaration de conflit d'intérêts

The authors have no funding or conflicts of interest to disclose.

Références

Maiorano E, Altini M, Favia G. Clear cell tumors of the salivary glands, jaws, and oral mucosa. Semin Diagn Pathol. 1997;14:203–212.
Jain A, Shetty DC, Juneja S, et al. Molecular characterization of clear cell lesions of head and neck. J Clin Diagn Res. 2016;10:ZE18–ZE23.
Majewska H, Skálová A, Radecka K, et al. Renal clear cell carcinoma metastasis to salivary glands—a series of 9 cases: clinico-pathological study. Pol J Pathol. 2016;67:39–45.
Morita Y, Kashima K, Suzuki M, et al. Differential diagnosis between oral metastasis of renal cell carcinoma and salivary gland cancer. Diagnostics (Basel). 2021;11:506–519.
Weinreb I. Hyalinizing clear cell carcinoma of salivary gland: a review and update. Head Neck Pathol. 2013;7(suppl 1):S20–S29.
Skalova A, Stenman G, Simpson RHW, et al. The role of molecular testing in the differential diagnosis of salivary gland carcinomas. Am J Surg Pathol. 2018;42:11–27.
Stenman G. Fusion oncogenes in salivary gland tumors: molecular and clinical consequences. Head Neck Pathol. 2013;7:S12–S19.
Moutasim KA, Thomas GJ. Salivary gland tumours: update on molecular diagnostics. Diagn Histopathol. 2021;26:159–164.
Skalova A, Vanecek T, Sima R, et al. Mammary analogue secretory carcinoma of salivary glands, containing the ETV6-NTRK3 fusion gene: a hitherto undescribed salivary gland tumor entity. Am J Surg Pathol. 2010;34:599–608.
Skalova A, Vanecek T, Martinek P, et al. Molecular profiling of mammary analog secretory carcinoma revealed a subset of tumors harboring a novel ETV6-RET translocation: report of 10 cases. Am J Surg Pathol. 2018;42:234–246.
Majewska H, Skálová A, Stodulski D, et al. Mammary analogue secretory carcinoma of salivary glands: first retrospective study of a new entity in Poland with special reference to ETV6 gene rearrangement. Virchows Arch. 2015;466:245–254.
Fujii K, Murase T, Beppu S, et al. MYB, MYBL1, MYBL2 and NFIB gene alterations and MYC overexpression in salivary gland adenoid cystic carcinoma. Histopathology. 2017;71:823–834.
Jee KJ, Persson M, Heikinheimo K, et al. Genomic profiles and CRTC1-MAML2 fusion distinguish different subtypes of mucoepidermoid carcinoma. Mod Pathol. 2013;26:213–222.
Okumura Y, Miyabe S, Nakayama T, et al. Impact of CRTC1/3-MAML2 fusions on histological classification and prognosis of mucoepidermoid carcinoma. Histopathology. 2011;59:90–97.
Antonescu CR, Katabi N, Zhang L, et al. EWSR1-ATF1 fusion is a novel and consistent finding in hyalinizing clear-cell carcinoma of salivary gland. Genes Chromosomes Cancer. 2011;50:559–570.
Urano M, Nakaguro M, Yamamoto Y, et al. Diagnostic significance of HRAS mutations in epithelial-myoepithelial carcinomas exhibiting a broad histopathologic spectrum. Am J Surg Pathol. 2019;43:984–994.
Skálová A, Weinreb I, Hyrcza M, et al. Clear cell myoepithelial carcinoma of salivary glands showing EWSR1 rearrangement: molecular analysis of 94 salivary gland carcinomas with prominent clear cell component. Am J Surg Pathol. 2015;39:338–348.
Skálová A, Agaimy A, Vanecek T, et al. Molecular profiling of clear cell myoepithelial carcinoma of salivary glands with EWSR1 rearrangement identifies frequent PLAG1 gene fusions but no EWSR1 fusion transcripts. Am J Surg Pathol. 2021;45:1–13.
Batsakis JG. Clear cell tumors of salivary glands. Ann Otol Rhinol Laryngol. 1980;89(pt 1):196–197.
Simpson RHW, Sarsfield PT, Clarke T, et al. Clear cell carcinoma of minor salivary glands. Histopathology. 1990;17:433–438.
Milchgrub S, Gnepp DR, Vuitch F, et al. Hyalinizing clear cell carcinoma of salivary gland. Am J Surg Pathol. 1994;18:74–82.
Ellis G Barnes L, Eveson JW, Reichert P, Sidransky D. Clear cell carcinoma, not otherwise specified, eds. World Health Organization Classification of Tumours: Pathology and Genetics of Head and Neck Tumours. Lyon, France: IARC Press; 2005:227–228.
Ellis GLA, Auclair PL. AFIP Atlas of Tumor Pathology: Tumors of the Salivary Glands. Washington, DC: ARP Press; 2008:301–309.
Wenig BM, Bell D, Chiosea S, et al. El-Naggar AK, Chan JKC, Grandis J, Takata T, Slootweg PJ. Clear cell carcinoma, eds. WHO Classification of Head and Neck Tumours. Lyon, France: IARC Press; 2017:168–169.
WHO Classification of Tumours Editorial Board. Head and Neck Tumours. WHO Classification of Tumours Series, 5th ed.Lyon, France: International Agency for Research on Cancer; 2022:9.
Dardick I, Leong I. Clear cell carcinoma: review of its histomorphogenesis and classification as a squamous cell lesion. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009;108:399–405.
Hsieh MS, Wang H, Lee YH, et al. Re-evaluation of MAML2 fusion-negative mucoepidermoid carcinoma: a subgroup being actually hyalinizing clear cell carcinoma of the salivary gland with EWSR1 translocation. Hum Pathol. 2016;61:9–18.
Tanguay J, Weinreb I. What the EWSR1-ATF1 fusion has taught us about hyalinizing clear cell carcinoma. Head Neck Pathol. 2013;7:28–34.
Chapman E, Skalova A, Ptakova N, et al. Molecular profiling of hyalinizing clear cell carcinomas revealed a subset of tumors harboring a novel EWSR1-CREM fusion: report of 3 cases. Am J Surg Pathol. 2018;42:1182–1189.
Seethala RR. Oncocytic and apocrine epithelial myoepithelial carcinoma: novel variants of a challenging tumor. Head Neck Pathol. 2013;7(suppl 1):S77–S84.
Donath K, Seifert G, Schmitz R. Diagnosis and ultrastructure of the tubular carcinoma of salivary gland ducts. Epithelial-myoepithelial carcinoma of the intercalated ducts. Virchows Arch A Pathol Pathol Anat. 1972;356:16–31.
Corridan M. Glycogen-rich clear cell adenoma of the parotid gland. J Pathol Bacteriol. 1956;72:623–626.
Feyrter F. On glycogen-rich reticular adenoma of the salivary glands. Z Krebsforsch. 1963;65:446–454.
Saksela E, Tarkkanen J, Wartiovaara J. Parotid clear-cell adenoma of possible myoepithelial origin. Cancer. 1972;30:742–748.
Simpson RHW, Clarke TJ, Sarsfield PTL, et al. Epithelial-myoepithelial carcinoma of salivary glands. J Clin Pathol. 1991;44:419–423.
Seethala RR, Barnes EL, Hunt JL. Epithelial-myoepithelial carcinoma: a review of the clinicopathologic spectrum and immunophenotypic characteristics in 61 tumors of the salivary glands and upper aerodigestive tract. Am J Surg Pathol. 2007;31:44–57.
Nakaguro M, Nagao T. Epithelial-myoepithelial carcinoma. Surg Pathol Clin. 2021;14:97–109.
Terada T, Ikeuchi S, Inomoto C, et al. Mucoepidermoid carcinoma of the palate composed exclusively of clear cells (clear cell variant). Virchows Arch. 2004;445:541–543.
Yang S, Chen X. Calcifications in clear cell mucoepidermoid carcinomas. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109:274–275.
Tajima S, Namiki I, Koda K. A clear cell variant of mucoepidermoid carcinoma harboring CRTC1-MAML2 fusion gene found in buccal mucosa: report of a case showing a large clear cell component and lacking typical epidermoid cells and intermediate cells. Med Mol Morphol. 2017;50:117–121.
Seethala RR, Dacic S, Cieply K, et al. A reappraisal of the MECT1-MAML2 translocation in mucoepidermoid carcinomas. Am J Surg Pathol. 2010;34:213–222.
Okamura Y, Nakano S, Murase T, et al. Prognostic impact of CRTC1-MAML2 fusions in salivary gland mucoepidermoid carcinoma. A multi-institutional retrospective study. Cancer Sci. 2020;111:4195–4204.
Bishop JA, Cowan ML, Shum CH, et al. MAML2 rearrangements in variant forms of mucoepidermoid carcinoma: ancillary diagnostic testing for the ciliated and Warthin-like variants. Am J Surg Pathol. 2018;42:130–136.
Skálová A, Agaimy A, Stanowska O, et al. Molecular profiling of salivary oncocytic mucoepidermoid carcinomas helps to resolve differential diagnostic dilemma with low-grade oncocytic lesions. Am J Surg Pathol. 2020;44:1612–1622.
Kong M, Drill EN, Morris L, et al. Prognostic factors in myoepithelial carcinoma of salivary glands: a clinicopathologic study of 48 cases. Am J Surg Pathol. 2015;39:931–938.
Savera AT, Sloman A, Huvos AG, et al. Myoepithelial carcinoma of the salivary glands: a clinicopathologic study of 25 patients. Am J Surg Pathol. 2000;24:761–774.
Di Palma S, Guzzo M. Malignant myoepithelioma of salivary glands: clinicopathological features of ten cases. Virchows Arch A Pathol Anat Histopathol. 1993;423:389–396.
Xu B, Mneimneh W, Torrence DE, et al. Misinterpreted myoepithelial carcinoma of salivary gland: a challenging and potentially significant pitfall. Am J Surg Pathol. 2019;43:601–609.
Michal M, Skálová A, Simpson RH, et al. Clear cell malignant myoepithelioma of the salivary glands. Histopathology. 1996;28:309–315.
Zarbo RJ. Salivary gland neoplasia. A review for the practicing pathologist. Mod Pathol. 2002;15:298–323.
Ni H, Zhao P-Y, Wang X-T, et al. EWSR1 rearrangement is present in a subset of myoepithelial tumors of salivary glands with variable morphology and does not correlate with clinical behavior. Ann Diagn Pathol. 2017;28:19–23.
Dalin MG, Katabi N, Persson M, et al. Multi-dimensional genomic analysis of myoepithelial carcinoma identifies prevalent oncogenic gene fusions. Nat Commun. 2017;8:1197.
Damm DD, White DK, Geissler RH, et al. Benign solid oncocytoma of intraoral minor salivary glands. Oral Surg Oral Med Oral Pathol. 1989;67:84–86.
Ellis GL. Clear cell neoplasms in salivary glands: clearly a diagnostic challenge. Ann Diagn Pathol. 1998;2:61–78.
Ellis GL. “Clear cell” oncocytoma of salivary gland. Hum Pathol. 1988;19:862–867.
Bilodeau EA, Weinreb I, Antonescu CR, et al. Clear cell odontogenic carcinomas show EWSR1 rearrangements: a novel finding and biologic link to salivary clear cell carcinomas. Am J Surg Pathol. 2013;37:1001–1005.
Liu L, Zhang JW, Zhu NS, et al. Clear cell odontogenic carcinoma: a clinicopathological and immunocytochemical analysis. Pathol Oncol Res. 2020;26:1559–1564.
Vogels R, Baumhoer D, van Gorp J, et al. Clear cell odontogenic carcinoma: occurrence of EWSR1-CREB1 as alternative fusion gene to EWSR1-ATF1 . Head Neck Pathol. 2019;13:225–230.
Breik O, Higginson J, Al-Ajami AK, et al. Clear cell odontogenic carcinoma: first report of novel EWSR1-CREM fusion gene in case of long-term misdiagnosis. Head Neck Pathol. 2021;15:1391–1398.
Siriwardena BSMS, Speight PM, Franklin CD, et al. CEOT variants or entities: time for a rethink? A case series with review of the literature. Head Neck Pathol. 2021;15:186–201.
Eversole LR. On the diferential diagnosis of clear cell tumours of the head and neck. Eur J Cancer B Oral Oncol. 1993;29B:173–179.
Kuo T. Clear cell carcinoma of the skin. A variant of the squamous cell carcinoma that simulates sebaceous carcinoma. Am J Surg Pathol. 1980;4:573–583.
Lawal AO, Adisa AO, Olajide MA, et al. Clear cell variant of squamous cell carcinoma of skin: a report of a case. J Oral Maxillofac Pathol. 2013;17:110–112.
Obiorah IE, Ozdemirli M. Clear cell sarcoma in unusual sites mimicking metastatic melanoma. World J Clin Oncol. 2019;10:213–221.
Mesbah Ardakani N, Leslie C, Grieu-Iacopetta F, et al. Clinical and therapeutic implications of BRAF mutation heterogeneity in metastatic melanoma. Pigment Cell Melanoma Res. 2017;30:233–242.
Panagopoulos I, Mertens F, Isaksson M, et al. Absence of mutations of the BRAF gene in malignant melanoma of soft parts (clear cell sarcoma of tendons and aponeuroses). Cancer Genet Cytogenet. 2005;156:74–76.
Feasel PC, Cheah AL, Fritchie K, et al. Primary clear cell sarcoma of the head and neck: a case series with review of the literature. J Cutan Pathol. 2016;43:838–846.
Hicks MJ, Saldivar VA, Chintagumpala MM, et al. Malignant melanoma of soft parts involving the head and neck region: review of literature and case report. Ultrastruct Pathol. 1995;19:395–400.
Zhang L, Jia Z, Mao F, et al. Whole-exome sequencing identifies a somatic missense mutation of NBN in clear cell sarcoma of the salivary gland. Oncol Rep. 2016;35:3349–3356.
McHugh JB, Hoschar AP, Dvorakova M, et al. p63 immunohistochemistry differentiates salivary gland oncocytoma and oncocytic carcinoma from metastatic renal cell carcinoma. Head Neck Pathol. 2007;1:123–131.

Auteurs

Alena Skalova (A)

Departments of Pathology.

Ilmo Leivo (I)

Institute of Biomedicine, Pathology, University of Turku and Department of Pathology, Turku University Hospital, Turku, Finland.

Henrik Hellquist (H)

Epigenetics and Human Disease Laboratory, Department of Biomedical Sciences and Medicine, Algarve Biomedical Center (ABC), University of Algarve, Faro, Portugal.

Roderick H W Simpson (RHW)

Department of Anatomical Pathology, University of Calgary, Calgary, Alberta, Canada.

Vincent Vander Poorten (V)

Department of Oncology, Section Head and Neck Oncology, University Hospitals Leuven, KU Leuven, Leuven, Belgium.

Stefan M Willems (SM)

Department of Pathology and Medical Biology, University of Groningen, Groningen, The Netherlands.

Elaheh Mosaieby (E)

Departments of Pathology.
Molecular and Genetic Laboratory, Bioptic Laboratory Ltd, Plzen, Czech Republic.

David Slouka (D)

Otorhinolaryngology, Faculty of Medicine in Plzen, Charles University.

Alfio Ferlito (A)

International Head and Neck Scientific Group, Padua, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH