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Epithelial Lacrimal Gland Tumors Pathologic Classification and Current Understanding

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Epithelial Lacrimal Gland Tumors Pathologic Classification and Current Understanding CLINICAL SCIENCES Epithelial Lacrimal Gland Tumors Pathologic Classification and Current Understanding Ezekiel Weis, MD, MPH; Jack Rootman, MD; Thomas J. Joly, MD, PhD; Kenneth W. Berean, MD; Hind M. Al-Katan, MD; Sylvia Pasternak, MD; Giulio Bonavolontà, MD; Diego Strianese, MD; Peerooz Saeed, MD; Kenneth A. Feldman, MD; Sumalee Vangveeravong, MD; Jocelyne S. Lapointe, MD; Valerie A. White, MD, MHSc Objective: To apply the updated epithelial salivary gland mors were found to be unclassifiable with the updated classification scheme to a large cohort of lacrimal gland scheme, with 2 having histologically malignant features. tumors so as to provide an updated lacrimal gland tu- Deficiencies and variations in pathologic assessment were mor classification scheme. noted. Variation in the histologic findings of pleomor- phic adenoma and assessment of the extent of invasion of Methods: A retrospective multicenter cohort study of carcinoma ex pleomorphic adenoma were highlighted. 118 cases of epithelial neoplasia was undertaken. Main outcome measures included pathologic analysis, subtyp- Conclusions: The use of the more histologically di- ing, and survival. verse classification of salivary gland tumors can be suc- cessfully applied to the epithelial lacrimal gland neo- Results: Of 118 cases, 17 (14%) were reclassified using plasms. This expanded classification system led to the proposed expanded classification scheme based on the reclassifying 14% of cases. Currently, there are no con- current World Health Organization classification of sali- sistent pathologic standards for processing and evaluat- vary gland tumors. The most frequent neoplasms were pleo- ing these lesions. morphic adenoma and adenoid cystic carcinoma, of which we highlight more unusual histologic features. Three tu- Arch Ophthalmol. 2009;127(8):1016-1028 ACRIMAL GLAND LESIONS REP- showed an expanded classification based on resent 5% to 25% of orbital the 1992 WHO classification of salivary tumors, and the proportion in gland tumors. It is also clear that the sali- the literature that are epithe- vary gland classification has filtered into the lial range from 23% to 70% of lacrimal gland literature, which has de- Lbiopsied cases.1-6 Despite our current un- scribed many tumors analogous to their sali- derstanding that rational clinical manage- vary gland counterparts, including ductal ment of salivary and lacrimal gland tu- carcinoma,18-23 acinic cell carcinoma,24-27 pri- mors depends on specific histologic tumor mary squamous cell carcinoma,28-31 muco- typing,3-5,7-13 there has been no official up- epidermoid carcinoma,20,32-38 oncocytic car- date of the lacrimal gland tumor classifi- cinoma,39 polymorphous low-grade cation since the World Health Organiza- adenocarcinoma,5,40 myoepithelial carci- tion (WHO) publication of 1980.14 The noma,41-43 lymphoepithelial carcino- Armed Forces Institute of Pathology (AFIP) ma,44,45 epithelial-myoepithelial carcino- monograph on lacrimal gland tumors pub- ma,42 cystadenocarcinoma,46 primary lished in 1994 reviewed 39 cases but did sebaceous adenocarcinoma,5,47-53 basal cell not attempt a comprehensive reclassifica- adenocarcinoma,54 oncocytoma,55,56 cyst- tion.15 Our understanding of lacrimal gland adenoma,57 and myoepithelioma.5,43,58-62 tumors reflects the histologically similar but The purposes of our study are to re- more prevalent salivary gland tumors, the view the standards of histologic analysis classification of which has undergone sev- and propose an updated classification eral iterations since the introduction of the scheme based on a series of 118 cases from AFIP classification in 195316 to include 4 contributing institutions reviewed by a newly recognized tumor types correlating head and neck pathologist (K.W.B.) well Author Affiliations are listed at with biological behavior. In 2006 the AFIP versed in salivary gland tumor pathology the end of this article. monograph on lacrimal gland tumors17 and classification. (REPRINTED) ARCH OPHTHALMOL / VOL 127 (NO. 8), AUG 2009 WWW.ARCHOPHTHALMOL.COM 1016 ©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/01/2021 METHODS Table 1. Updated Diagnoses of 118 Epithelial Lacrimal Gland Tumors Using Proposed Salivary Gland Epithelial lacrimal gland neoplasms from 4 contributing insti- Classification Scheme tutions were reviewed for clinical profile, pathology, and out- come at the University of British Columbia, Vancouver, Brit- Cases, No. (%) ish Columbia, Canada. Only cases with pathology specimens Diagnosis (N=118) available for examination were included, resulting in a total of Pleomorphic adenoma 57 (48) 118 cases in the combined series. Adenoid cystic carcinoma 38 (32) Carcinoma ex pleomorphic adenoma 9 (8) PATHOLOGIC ANALYSIS Adenocarcinoma 3 (3) Mucoepidermoid carcinoma 2 (2) All pathology specimens were evaluated by a single patholo- Lacrimal ductal carcinoma 2 (2) gist specializing in head and neck pathology (K.W.B.). Speci- Unclassifiable carcinoma 2 (2) mens were classified according to the most recent WHO sali- Unclassifiable neoplasm 1 (1) vary gland tumor classification.63 The amount of material Squamous cell carcinoma 1 (1) Myoepithelial carcinoma 1 (1) available varied, and initial review was based on hematoxylin- Myoepithelioma 1 (1) eosin–stained sections. Additional material, analysis with his- Oncocytoma 1 (1) tochemical and immunohistochemical stains, and a more com- Total 118 (102)a plete examination of the extent of the tumor were requested for any case in which the diagnosis was questionable. Initial a Artifactually greater than 100% owing to rounding to the nearest integer. review was performed with the pathologist blinded to the clini- cal history and original diagnosis. All of the cases with rare di- agnoses, with atypical findings, or in which the review diag- thelial and mesenchymal-like tissues.”63 The epithelial nosis differed from the original were submitted to a second cells form characteristic ductal structures with surround- review by a committee comprising the head and neck patholo- ing myoepithelial cells, which trail out gradually into gist (K.W.B.) and 2 ophthalmic pathologists (V.A.W. and J.R.). myxomatous mesenchyme (Figure 1A). All but 2 of the 57 cases of PA in our series easily fit this description and STATISTICAL ANALYSIS were diagnosed as such in the original pathology reports. Variable features typical of PA were systematically ana- Linear and logistic regression was used to compare baseline char- lyzed, including cellularity, presence of myxoid, chon- acteristics between different tumor subtypes and histologic find- droid, and hyaline stroma, and cellular characteristics in- ings. Clinical outcomes for adenoid cystic carcinoma were ana- cluding squamous metaplasia and presence of plasmacytoid lyzed using survival analysis in the form of the log-rank test. Ͻ cells. Other rare features were occasionally noted. Statistical significance was defined as P .05. Typical and infrequent features are summarized in Table 3 and shown in Figure 1. The mean diameter was RESULTS 24.5 mm, ranging from 10 to 40 mm. Mitotic figures were rarely detected. Tumor capsules varied from a few mi- The pathology specimens of 118 cases from 4 institu- crometers to a few hundred micrometers in thickness and tions were classified as shown in Table 1. This study was were incomplete in some. In 31 cases in which we had coordinated by the Orbit Clinic, University of British Co- adequate sections to analyze the full extent of the tu- lumbia. Forty cases from the University of British Colum- mor, 27 were found to border or invade the capsule and bia, 33 from the Department of Ophthalmology, Univer- 4 (including 3 not originally reported) extended beyond. sity of Naples, Naples, Italy, 33 from the Department of The review diagnosis differed from the original diag- Ophthalmology, University of Amsterdam, Amsterdam, the nosis in 2 cases. One case, originally diagnosed as nonin- Netherlands, and 12 from the Department of Ophthal- vasive carcinoma in PA, was on review considered a PA mology, Kaiser Permanente Medical Center, Harbor City, with epithelial atypia and oncocytic metaplasia not war- California, were enrolled. No interinstitution or intra- ranting a diagnosis of carcinoma. The second case, origi- institution standards for specimen sampling or handling nally diagnosed as acinic cell carcinoma, was considered were found. The most frequent diagnosis was pleomor- a variant PA with atypical features. phic adenoma (PA), followed by adenoid cystic carci- The 3 clinically recurrent tumors were characterized his- noma (ACC) and carcinoma ex pleomorphic adenoma tologically by multifocal and multinodular growth patterns. (CEPA). Three tumors were unclassifiable, 2 of which were The recurrences occurred at 23, 25, and 30 years after the considered to have histopathologically malignant fea- initial resection. In all 3 cases, the tumor formed numer- tures and the third of which was indeterminate. Of the 118 ous nodules generally composed predominantly of stroma cases, 17 were reclassified in this study (Table 2). with minor epithelial components. One tumor showed fo- cal calcification and another showed focal ossification. There BENIGN NEOPLASMS was no evidence of malignant transformation. Pleomorphic Adenoma Other Benign Tumors According to the AFIP salivary gland tumor classifica- A single case of myoepithelioma was identified.64 It was tion, the “essential diagnostic feature” of a PA, or be- well circumscribed and
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