LymphoepithelialCarcinomaoftheSalivaryGland:MorphologicPatternsandImagingFeaturesonCTandMRI - PDF Document

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  1. ORIGINALRESEARCH HEAD&NECK LymphoepithelialCarcinomaoftheSalivaryGland: MorphologicPatternsandImagingFeaturesonCTandMRI X. Ban, J. Wu, Y. Mo, Q. Yang, X. Liu, C. Xie, and R. Zhang ABSTRACT BACKGROUND AND PURPOSE: Lymphoepithelial carcinoma is a rare salivary gland lesion. We retrospectively reviewed CT and MR imaging features of salivary gland lymphoepithelial carcinoma to determine their imaging features and morphologic patterns. MATERIALS AND METHODS: The clinical data, CT, and MR imaging findings of 28 patients with histologically proved lymphoepithelial carcinoma of the salivary gland were retrospectively reviewed. Morphologic patterns of the lesions were categorized into 3 types on the basis of margin and shape. RESULTS: There were 17 men and 11 women with a mean age of 39.3 years; 96.4% of patients were positive for Epstein-Barr virus both on histologic staining and Epstein-Barr virus serology. Tumors were parotid in 18 patients, submandibular in 8 patients, sublingual in 1 patient, and palatal in 1 patient. Most tumors (57.1%) manifested as a partially or ill-defined mass with a lobulated or plaque-like shape. Homoge- neous enhancement was found in 16 patients, while heterogeneous enhancement was found in 12, including 4 patients with intratumoral necrosis.Invasionintoadjacentstructureswasfoundin5patients;60.7%ofpatientsexhibitedabnormallymphnodes,withnodalnecrosis in 3 patients. CONCLUSIONS: Thecharacteristiclobulatedorplaque-likeshape,withapartiallyorill-definedmargin,ofasalivaryglandmassassociated with ipsilateral lymphadenopathy may suggest a preoperative diagnosis of lymphoepithelial carcinoma. ABBREVIATIONS: EBER ? Epstein-Barr virus-encoded small RNA; LEC ? lymphoepithelial carcinoma L epithelial cells with marked infiltration of lymphoid cells in the stroma.1,2LEC most frequently occurs in the nasopharynx, but it also has been reported arising in various organs such as salivary glands, lungs, thymus, stomach, larynx, soft palate, uterus, bladder,andskin.1,3-5LECofthesalivarygland,firstdescribedby Hilderman et al in 1962,6is very rare and accounts for 0.3%?5.9% of malignant tumors of the salivary gland; it also has a striking geographic and ethnic distribution.1,7,8Most LECs of thesalivaryglandshavebeenreportedinInuit-YupikandChinese ymphoepithelial carcinoma (LEC) is an uncommon malig- nant neoplasm characterized by undifferentiated malignant populations, with a strong association with the Epstein-Barr vi- rus.5Theclinicalandpathologicfeatures,treatment,andprogno- sis of LEC of the salivary gland have been extensively re- ported.1,2,5,9Limited literature exists, however, describing the imaging features of LEC of the salivary gland. We retrospectively analyzed CT and MR imaging features in a seriesof28patientswithpathologicallyprovedsalivaryglandLEC to identify any distinct morphologic patterns and imaging fea- tures that could be useful for their diagnosis and differential diagnosis. MATERIALS AND METHODS Patients Twenty-eight patients with pathologically confirmed LEC of a major or minor salivary gland were enrolled retrospectively be- tween February 2001 and June 2012. This study was approved by our institutional review board, and patient informed consent was not required in accordance with the requirements of a retrospective study. Clinical data, including age, sex, clinical presentation, laboratory examinations, treatments, and out- comes, were reviewed. Received December 23, 2013; accepted after revision February 11, 2014. From the Medical Imaging and Minimally Invasive Interventional Center and State Key Laboratory of Oncology in Southern China, Cancer Center, Sun Yat-sen Uni- versity, Guangzhou, China. X. Ban and J. Wu contributed equally to this work. All authors have no conflict of interest. Please address correspondence to Rong Zhang, MD, No 651 Dongfeng Rd East, Medical Imaging and Minimally Invasive Interventional Center and State Key Labo- ratory of Oncology in Southern China, Cancer Center, Sun Yat-Sen University, Guangzhou, 510060, China; e-mail: zhangr@sysucc.org.cn http://dx.doi.org/10.3174/ajnr.A3940 1813 AJNR Am J Neuroradiol 35:1813–19 Sep 2014 www.ajnr.org

  2. FIG 1. Morphologic patterns of salivary gland LECs. Type 1: Axial contrast-enhanced CT (A) and axial gadolinium-enhanced T1-weighted imaging (B) show round masses with well-defined margins located in the left parotid glands (arrows). Type 2: Axial contrast-enhanced CT (C) and axial gadolinium-enhanced T1-weighted imaging (D) show masses with plaque-like (C) and lobulated (D) shapes and partially defined margins located in the right parotid glands (arrows). Type 3: Axial contrast-enhanced CT shows masses with irregular shapes, ill-defined margins, and diffuse invasive growth (arrow) located in the left parotid (E) and right submandibular (F) glands, respectively. Normal submandibular gland tissue is displaced posteriorly and medially (arrowhead). Imaging Techniques All patients had cross-sectional imaging before therapy. Of 28 patients, 22 had CT examinations, 5 had MR imaging, and the remaining patient had both CT and MR imaging. Unenhanced andcontrast-enhancedCTandMRimagingwereperformedinall patients. CT was performed by using either 16-section CT (Brilliance TM16; Philips Healthcare, Best, the Netherlands) with an axial collimationof16?0.75mmanda1.2pitch(n?17)orbyusing dual-section CT (Twin FLASH; Philips Heathcare) with an axial collimation of 2 ? 1 mm and a 1.0 pitch (n ? 6). Other parame- ters included the following: section thickness/gap, 3/3 mm (n ? 17) or 5/5 mm (n ? 6); current, 250 mA; and voltage, 125 kV. Contrast-enhancedCTwasperformedafterintravenousinjection of iopromide at a dosage of 1.5 mL/kg of body weight (Ultravist 300; Schering, Berlin, Germany). MR imaging was performed on a 1.5T system (Signa Hori- zon LX, HighSpeed; GE Healthcare, Milwaukee, Wisconsin). The sequences included fast spin-echo T2-weighted images (TR/TE ? 2000/120 ms) in the axial plane; and spin-echo T1- weighted images (TR/TE ? 450/15 ms) in the axial, coronal, and sagittal planes. Others parameters included a matrix of 256 ? 256, FOV of 300?380 mm, and a section thickness/gap of 5/0.5 mm for the axial plane and 4/0.4 mm for the coronal and sagittal planes. Contrast-enhanced sagittal and transverse T1-weighted images and contrast-enhanced coronal T1- weighted images with fat suppression were obtained after in- travenous injection of gadopentetate dimeglumine (Magnev- ist; Schering, Berlin, Germany) at a dosage of 0.2 mmol/kg of body weight. The main parameters were the same as those used preinjection. Imaging Analysis All images were reviewed by 2 experienced radiologists (Y.M. and C.X.) by consensus. Tumors were evaluated with regard to the location, size, margin, shape, attenuation or signal inten- sity (compared with adjacent muscle on CT or T1WI and com- pared with the contralateral normal salivary gland on T2WI), lesion texture (homogeneous or heterogeneous; with or with- outcalcification,cysticareas,andnecrosis),patternanddegree of contrast enhancement, and involvement of adjacent struc- tures. Tumor size was measured in maximal dimensions on the transverseplane.Themarginofthelesionwasconsideredwell- defined if more than two-thirds of the margin was sharply demarcated from the surrounding tissue and ill-defined if less than one-third of the margin was sharply defined, while inter- mediate cases were considered partially defined. The shape of 1814 Ban Sep 2014 www.ajnr.org

  3. Table 1: Clinical profiles of 28 patients with LEC of the salivary gland Table 2: Imaging characteristics of 28 patients with LEC of the salivary gland No. of Patients/ Values No. of Patients/ Values Characteristics Characteristics Sex Tumor location Parotid Submandibular gland Palate Sublingual gland Tumor size (cm) Tumor margin Partially defined Well-defined Ill-defined Morphologic patterns Type 1 Type 2 Type 3 Inner nature Necrosis Calcification Density on unenhanced CT (n ? 23) Slightly hypodense Isodensity Enhancement degree on CT (n ? 23) Poor Moderate Intense Signal intensity on MR imaging (n ? 6) T1WI Hyperintense Isointense T2WI Hypointense Hyperintense Enhancement degree on MR imaging (n ? 6) Poor Moderate Intense Inner nature after contrast enhancement Homogeneous Heterogeneous Adjacent structure invasion Bone destroyed Pathologic lymph nodes Female Male Age (mean) (yr) ?20 ?20 ? ?30 ?30 ? ?40 ?40 ? ?50 ?50 ? ?60 ?60 Symptom duration (mean) (mo) ?24 ?24 Epstein-Barr virus Positive Negative Clinical staging I II III IV Treatment Surgery Surgery and radiotherapy Surgery, radiotherapy, and chemotherapy Radiotherapy and chemotherapy Local recurrence Distant metastasis 11(39.3%) 17(60.7%) 12?60(39.3) 4(14.3%) 4(14.3%) 6(21.4%) 4(14.3%) 8(28.6%) 2(7.1%) 0.?120(25) 16(57.1%) 12(42.9%) 18(64.3%) 8(28.5%) 1(3.6%) 1(3.6%) 1.6?7(3.5) 13(46.4%) 5(17.9%) 10(35.7%) 5(17.9%) 16(57.1%) 7(25.0%) 27(96.4%) 1(3.6%) 4(14.3%) 0(0%) 1(3.6%) 7(25.0%) 8(28.5%) 12(42.9%) 19(82.6%) 4(17.4%) 6(26.1%) 14(56.5%) 3(17.4%) 7(25%) 18(64.2%) 2(7.2%) 1(3.6%) 3(10.7%) 4(14.3%) 1(16.7%) 5(83.3%) 4(66.7%) 2(33.3%) the lesion was classified as round/oval, lobulated, and/or irreg- ular. Patterns of enhancement were categorized as homoge- neous or heterogeneous. Cystic areas were defined as having relatively homogeneous low attenuation (?20 HU) without enhancement and with a relatively clear boundary, while ne- crotic areas were defined as having heterogeneous low attenu- ation without enhancement and with an unclear boundary. The degree of enhancement was graded as poor, moderate, and intense, with “poor” defined as attenuation or signal intensity lower than or similar to that of the adjacent muscle, “moder- ate” as greater than that of the muscle but lower than or similar to that of the contralateral normal submandibular gland, and “intense” as greater than that of the contralateral normal sub- mandibular gland. The morphologic patterns of tumors were categorized into 3 types according to the margin and shape of the lesions: In type 1, masseswereround/ovoidwithawell-definedmargin(Fig1A,-B); in type 2, masses showed a lobulated or plaque-like shape with a partially or ill-defined margin (Fig 1C, -D); and in type 3, masses showed an irregular shape with an ill-defined margin and diffuse invasive growth (Fig 1E, -F). The size, distribution, and attenuation or signal-intensity fea- tures of cervical lymphadenopathy were also evaluated. Cervical nodesweresubdividedaccordingtothespecificanatomicsubsites involved, and the assignment of level was predicated on imaging- based delineation of the cervical lymph nodes.10The diagnosis of nodeinvolvementwasdefinedonthebasisofcentralnecrosisand size criteria.11 1(16.7%) 4(66.6%) 1(16.7%) 16(57.1%) 12(42.9%) 5(17.9%) 2(7.1%) 17(60.7%) RESULTS Clinical Features Theclinicalprofilesof28patientswithLECofthesalivaryglandare summarizedinTable1.AllpatientsweresouthernChinese,with17 malesand11females,12–60yearsofage,withameanof39.3years. Of28patients,20presentedwithaslowlygrowing,palpablemassand 8 experienced a recent, rapidly growing mass. Four patients (3 with rapidlygrowingtumorsand1withaslowlygrowingtumor)hadpain or tenderness. One patient with a rapidly growing tumor had pro- gressive facial palsy. The duration of symptoms ranged from 0.2 months to 10 years (mean, 25 months), with 42.9% (12/28) of pa- tients having symptoms for ?2 years. Tumors were parotid in 18 patients, submandibular in 8 patients, sublingual in 1 patient, and arisingfromtheupperpalatein1patient.Onepatienthadahistory of non-Hodgkin lymphoma 8 years prior. Twenty-seven cases were positiveforEpstein-BarrvirusonEBER(Epstein-Barrvirus-encoded smallRNA)insituhybridization.Thepossibilityofametastasisfrom primary nasopharyngeal carcinoma was excluded in all cases by di- 1815 AJNR Am J Neuroradiol 35:1813–19 Sep 2014 www.ajnr.org

  4. 1), lung (n ? 1), and liver (n ? 2) from 7 to 77 months after surgery. Imaging Findings The imaging characteristics of 28 patients are summarized in Table 2. Twenty-eight primary tumor masses were found in 28 patients.Lesionsweresolitaryandunilat- eral in all 28 patients. The parotid gland was the most frequent location (18 of 28 patients,64.3%)withlesionsinthesuper- ficial lobe in 11 patients, in the deep lobe in 1 patient, and in the superficial and deep lobes in 6 patients. Other less com- monly involved locations were the sub- mandibular gland (28.5%, n ? 8) (Fig 2), thesublingualgland(3.6%,n?1)(Fig3), and the palate (3.6%, n ? 1) (Fig 4). The size of the lesions ranged from 1.6 to 7.0 cm, with a mean of 3.5 cm. Themarginwaspartiallydefinedin13 patients (46.4%), ill-defined in 10 pa- tients (35.7%), and well-defined in 5 pa- tients(17.9%).Ofthe13partiallydefined masses, 7 were lobulated, 3 were plaque- like, and 3 were irregular. Of the 10 ill- defined masses, 5 were lobulated, 1 was plaque-like, and 4 were irregular. All 5 well-defined masses were round/ovoid. Invasion of adjacent soft tissue was found in 5 patients, including 2 patients with boneerosion.Accordingtotheshapeand margin of the masses, the morphology of tumorscouldbeclassifiedinto3patterns. The most common pattern was type 2 (n ? 16, 57.1%), then type 3 (n ? 7, 25.0%) and type 1 (n ? 5, 17.9%). Nota- FIG 2. LEC of the right submandibular gland in a 53-year-old woman with a painless mass in the right neck for 1 year. Axial contrast-enhanced CT (A) shows an ill-defined mass in the right submandibular gland with heterogeneous moderate enhancement (arrow). An enlarged lymph node in level IIa is also noted and shows a homogeneous enhancement (arrowhead). Axial T2-weighted image (B) shows a heterogeneous slight hyperintensity mass with curvilinear and linear hypointensity within it (arrow) and an enlarged lymph node in level IIa (arrowhead). Gadolinium-enhanced axial T1-weighted image (C) and coronal T1-weighted image with fat saturation (D) show the mass with a heterogeneous enhancement with hypoenhanced strands within it. An enlarged region of the lymph node in level IIa is also noted and shows homoge- neous enhancement (arrowhead). rectexamination(n?28)andbiopsyofthenasopharynx(n?8)by using fiberoptic nasopharyngoscopy. Of our patients, 42.9% were classified as having stage IV, followed by stage III (28.5%), stage II (25.0%),andstageI(3.6%). Preoperativefine-needleaspirationcytologywasperformedin 7 patients. Two patients were correctly diagnosed as having LEC, 1patientwassuspiciousforhavingalymphoepitheliallesionwith malignancy, 1 patient was diagnosed as having benign reactive lymphoproliferation, and the other 3 patients were diagnosed as having metastatic poorly differentiated squamous carcinoma. Twenty-sevenof28patientsunderwentsurgicalresectiontocon- firm the definitive diagnosis. After surgery, 18 of 27 patients re- ceived postoperative radiation therapy to the gland area and the ipsilateral upper neck with a dose range from 50 to 65 Gy, while 2 patients received postoperative radiation therapy (50 Gy) and chemotherapy. Only 1 patient underwent radiation therapy (50 Gy) and chemotherapy without surgery. Patient follow-up ranged from 5 to 123 months (mean, 41 months). Local recurrence was found in 3 patients from 12 to 28 months after surgery. Four patients, including 2 patients with local recurrence, developed distant metastases to the brain (n ? bly, the shape and size of the lesion in the parotid glands may depend predominantly on the location of the lesion. All masses involving the superficial and deep lobes of the parotid gland were irregular(n?5)orlobulated(n?1).Additionally,almosthalfof the masses (n ? 5) located in the superficial lobe of the parotid glandwereround-ovoid,andallmasses(n?11)inthesuperficial lobe of the parotid gland were ?5 cm. On CT, 23 masses were detected in 23 patients. Compared with the adjacent muscle, lesions showed slight hypoattenuation in19patientsandisoattenuationin4patients.Necrosiswasdem- onstratedin14.3%of(n?4)ofpatientsonenhancedCT,andno calcificationwasfoundinanypatient.Aftertheadministrationof contrast,lesionsshowedpoorenhancementin6patients,moder- ate enhancement in 13 patients, and intense enhancement in 4 patients. Homogeneous enhancement was found in 14 patients, while heterogeneous enhancement was found in the other 9 patients. Six patients with 6 masses (parotid glands in 4 patients, sub- mandibular gland in 1, sublingual gland in 1) underwent MR imaging. On T1-weighted imaging, 1 patient had a lesion with a slighthyperintensesignaland5patientshadisointensesignal.On 1816 Ban Sep 2014 www.ajnr.org

  5. Cervical Lymphadenopathy The incidence of neck node involvement was found in 60.7% (17/28) of patients, including 10 patients (56%, 10/18) with primary lesions in the parotid glands; 6 patients(75%,6/8),inthesubmandibular gland; and 1 patient (100%, 1/1), in the palate. Cervical lymphadenopathy was unilateral in all patients. The locations of pathologic lymph nodes were consis- tent with anatomic drainage without skip metastasis. The intraparotid region andlevelIIbwereinvolvedin8patients, respectively; level IIa was involved in 7 patients; level Ib was involved in 3 pa- tients; and level III was involved in 1 patient. Necrosis of the lymph nodes was found in 3 patients (Fig 5B). Histopathologic Results The diagnosis of LEC was confirmed his- topathologically in all patients by using either surgical resection (n ? 27) or fine- needle aspiration cytology (n ? 1). Grossly, all 27 resected tumors were gen- erally grayish or reddish and firm. Calci- fication was not found in any case, while necrosis was found in 5 cases in these 27 gross specimens. Infiltration into adja- cent muscle was found in 3 patients, and bone erosion, in 2 patients. Histopatho- logic examinations commonly showed infiltrativesheets,nests,andcordsofneo- plastic epithelial cells separated by lym- phoid stroma (Fig 3C). Immunohisto- chemically, cytokeratin and p63 were positive in 28 and 16 patients, respec- tively.Twenty-seventumorsshowedpos- itive EBER in epithelial neoplastic cells and negative EBER in stromal lymphoid cells and surrounding normal salivary gland tissue (Fig 3D). The remaining tu- mor showed negative EBER in epithelial neoplastic cells, stromal lymphoid cells, and surrounding normal salivary gland tissue. FIG3. LECoftheleftsublingualglandina44-year-oldwomanwithapainfulmassinthemouth for 8 years. Axial T2-weighted imaging (A) shows a homogeneous slightly hypointensity mass with a partially defined margin in the left sublingual gland (arrow). Axial gadolinium-enhanced T1-weighted image (B) shows the mass with homogeneous moderate enhancement (arrow). Histopathologic examination (C) shows nests of neoplastic epithelial cells separated by abun- dant lymphoid stroma (hematoxylin-eosin, original magnification ? 100). In situ hybridization by using a digoxigenin-labeled EBER probe (D) shows the nuclei of the malignant epithelial cells strongly positive but negative in the surrounding lymphocytes (original magnifica- tion ? 100). FIG 4. LEC of the right upper palate in a 38-year-old man with a rapidly growing mass in the upper palate for approximately 8 months. Axial contrast-enhanced CT (A) shows the mass with aheterogeneousmoderateenhancement(arrow).Sagittal(B)contrast-enhancedCTshowsthe mass with heterogeneous moderate enhancement (arrow) and bone destruction. DISCUSSION LEC of the salivary gland, which has been referred to as undifferentiated carcinoma T2-weighted imaging, 4 patients had hypointense signal (Fig 3A) and 2 patients had slightly hyperintense signal. After the admin- istration of contrast, imaging of 1 patient showed poor enhance- ment,thatof4patientsshowedmoderateenhancement,andthat in 1 patient showed intense enhancement. Homogeneous en- hancement was found in 3 patients, and heterogeneous enhance- ment was found in 3 patients. Cystic/necrotic areas were not found in any of the 6 patients. with lymphoid stroma, malignant lymphoepithelial lesion, ma- lignant lymphoepithelioma, and lymphoepithelial-like carci- noma,1,7is a rare undifferentiated carcinoma with prominent lymphoid stroma and ultrastructural features of squamous cell carcinoma. Increasingly investigators have demonstrated that LEC of the salivary gland is strongly associated with Epstein-Barr virus in endemic areas such as Greenland, Southeast Asia, and Alaska.12Inourstudy,all28patientsweresouthernChinese,and 1817 AJNR Am J Neuroradiol 35:1813–19 Sep 2014 www.ajnr.org

  6. Ahujaetal16reportedimagingfindingsof LECsinminorsalivaryglandsin4casesin 1999. LECs of the salivary glands in our se- ries tended to involve the parotid gland with an ill-defined or partially ill-defined margin. Most LECs in the salivary glands showed slight hypoattenuation on CT, isointense signal on T1WI, and hypoin- tense signal on T2-weighted imaging, with moderate enhancement. Unfortu- nately, these CT and MR imaging charac- teristicsarenonspecificanddonotallowa definitive discrimination from other ma- lignant tumors of the salivary glands. However, most of the lesions had homo- geneous attenuation/signal intensity on unenhanced CT and MR imaging; no le- sionsexhibitedcysticdegenerationorcal- FIG 5. LEC of the right parotid gland in a 38-year-old man with painless masses in the right parotid regions for approximately 3 years. Axial contrast-enhanced CT (A) shows an ill-defined mass located in the right parotid gland (arrow) with heterogeneous enhancement and much intratumoral necrosis (arrowhead). Axial contrast-enhanced CT (B) shows multiple enlarged nodes (arrow) in the intraparotid region and level IIa, with obvious necrosis (arrowhead). 96.4% of tumors were positive for Epstein-Barr virus by using EBERinsituhybridization.Ourresultssupporttheassociationof Epstein-Barr virus with salivary gland LEC. In our series, LEC of the salivary gland predominantly occurred in the parotid gland (64.3%), followed by the submandibular gland (28.5%). The mean agewas39.3years,withamalepredominance(1.5:1).Aslowlygrow- ing,palpablemasswaspresentin71.4%ofpatients,and28.6%pre- sented with a recent, rapidly growing mass. Almost half of our pa- tients (42.9%) experienced a duration of symptoms of ?2 years, indicatingthatLECsofthesalivaryglandshadarelativelylongdura- tion of symptoms compared with other malignant tumors in the salivaryglands,consistentwithpriorreports.1,2,7 Treatment for LEC of the salivary gland includes surgical ex- cision, radiation therapy, and chemotherapy. At present, surgical excision followed by postoperative radiation therapy is consid- eredthetreatmentofchoiceforLECofthesalivarygland,andthe 5-year survival rate is reported to range from 50% to 90%.2,7The prognosis of salivary gland LEC is reported as better than that in other types of undifferentiated carcinoma of the salivary gland.13 The incidence of local recurrence and distant metastasis has var- ied in previous studies. The reported local recurrence rate ranged from 0% to 28.9%.5,7In our cases, 27 patients under- went a surgical excision and 18 patients underwent postoper- ative radiation therapy. The local recurrence rate in this group was 10.7%. Of our patients, 14.3% developed distant metasta- sis to the lung, liver, and brain from 7 to 77 months after diagnosis, comparable with a distant metastasis rate of 2.9%?33.3% in previous studies.5,7,9 Fine-needle aspiration cytology is a primary diagnostic tool for salivary gland tumors,14,15but the diagnostic accuracy, sensi- tivity, and specificity of fine-needle aspiration cytology in the di- agnosis of salivary gland lesions are varied owing to diverse mor- phologic patterns and overlapping features between benign and malignant lesions. In a recent review, the diagnostic accuracy of fine-needleaspirationcytologywas78.6%in14patientswithLEC of salivary gland.15Thus, CT and MR imaging are still valuable tools for the diagnosis, preoperative evaluation, and biopsy guid- ance for patients with LEC. To our knowledge, however, only cification, even in a large mass; and most of our lesions (85.7%) lacked necrotic regions. These features are, in aggregate, different from those in other common primary malignant tumors of the salivary glands, including mucoepidermoid carcinoma and ade- noid cystic carcinoma because these more common malignant tumorstypicallyshowheterogeneousattenuationorsignalinten- sity with cystic change and necrosis.17-19Thus, an ill-defined or partially ill-defined mass without cystic regions or calcification and lacking necrosis is typically seen in salivary gland LEC. In our cases, salivary gland LECs could be classified into 3 morphologictypesonthebasisofthemarginandshape.Morpho- logicpatternsofsalivaryglandLECsareusefulforthedifferential diagnosisalongwithothersalivaryglandtumors.Types1(17.9%) and 3 (25.0%) in our series showed typical morphologic features of benign and malignant tumors in the salivary glands, respec- tively. Type 2 represented a mass with a lobulated/plaque-like shape and a partially or ill-defined margin. In this study, most tumors belonged to this type. Because most LECs in the salivary glands are less aggressive malignant tumors,7this pattern might bearelativelymorphologiccharacteristicofsalivaryglandLEC.In addition, previous studies had reported an incidence of lymph node metastases in salivary gland LEC ranging from 10% to 50%.2,7,20In our study, the incidence of lymph node metastases was up to 60.7%, which was higher than that in previous stud- ies.2,7,20Lymphadenopathy in our cases was unilateral, with the intraparotid region and level IIa the most commonly involved regions. Lymph node metastasis was found to spread along with anatomic drainage. No skip metastasis was present. Lymph node necrosis occurred sometimes, as demonstrated in a previous study.16 Thereareseverallimitationstoourstudy.First,asaretrospec- tivestudy,mostofourpatientsunderwentCTandonly6patients underwent MR imaging with conventional T1 and T2 sequences. Because MR imaging, particularly MR imaging with diffusion- weighted imaging or dynamic contrast-enhanced sequences, is regarded as a better technique for characterizing and delineating salivary gland lesions,21a study using these new techniques may beneededforfurtherdeterminingtheimagingfeaturesofsalivary 1818 Ban Sep 2014 www.ajnr.org

  7. gland LEC. Second, our patients had a follow-up from 5 to 123 months. Four patients had follow-up at ?12 months, which was less than the time to recurrence or distant metastasis in some other patients. Therefore, it was difficult to conclude the exact long-term recurrence and metastasis rates just on the basis of our data. noma of salivary gland: 69 cases with long-term follow-up. Head Neck 2013 Aug 22. [Epub ahead of print] 8. Nagao T, Ishida Y, Sugano I, et al. Epstein-Barr virus-associated undifferentiated carcinoma with lymphoid stroma of the salivary glandinJapanesepatients:comparisonwithbenignlymphoepithe- lial lesion. Cancer 1996;78:695–703 9. LeungSY,ChungLP,YuenST,etal.Lymphoepithelialcarcinomaof the salivary gland: in situ detection of Epstein-Barr virus. J Clin Pathol 1995;48:1022–27 10. GorDM,LangerJE,LoevnerLA.Imagingofcervicallymphnodesin headandneckcancer:thebasics.RadiolClinNorthAm2006;44:101– 10, viii 11. van den Brekel MW, Stel HV, Castelijns JA, et al. Cervical lymph node metastasis: assessment of radiologic criteria. Radiology 1990;177:379–84 12. Tsai CC, Chen CL, Hsu HC. Expression of Epstein-Barr virus in carcinomasofmajorsalivaryglands:astrongassociationwithlym- phoepithelioma-like carcinoma. Hum Pathol 1996;27:258–62 13. LarbcharoensubN,TubtongN,PraneetvatakulV,etal.Epstein-Barr virusassociatedlymphoepithelialcarcinomaoftheparotidgland:a clinicopathological report of three cases. J Med Assoc Thai 2006; 89:1536–41 14. Singh Nanda KD, Mehta A, Nanda J. Fine-needle aspiration cytology: a reliable tool in the diagnosis of salivary gland lesions. J Oral Pathol Med 2012;41:106–12 15. Colella G, Cannavale R, Flamminio F, et al. Fine-needle aspiration cytology of salivary gland lesions: a systematic review. J Oral Max- illofac Surg 2010;68:2146–53 16. Ahuja AT, Teo PM, To KF, et al. Palatal lymphoepitheliomas and a review of head and neck lymphoepitheliomas. Clin Radiol 1999; 54:289–93 17. Lee YY, Wong KT, King AD, et al. Imaging of salivary gland tu- mours. Eur J Radiol 2008;66:419–36 18. Thoeny HC. Imaging of salivary gland tumours. Cancer Imaging 2007;7:52–62 19. Christe A, Waldherr C, Hallett R, et al. MR imaging of parotid tumors: typical lesion characteristics in MR imaging improve dis- crimination between benign and malignant disease. AJNR Am J Neuroradiol 2011;32:1202–07 20. BoschJD,KudrykWH,JohnsonGH.Themalignantlymphoepithe- lial lesion of the salivary glands. J Otolaryngol 1988;17:187–90 21. YabuuchiH,MatsuoY,KamitaniT,etal.Parotidglandtumors:can addition of diffusion-weighted MR imaging to dynamic contrast- enhanced MR imaging improve diagnostic accuracy in character- ization? Radiology 2008;249:909–16 CONCLUSIONS LEC of the salivary gland displays nonspecific attenuation or sig- nalintensityonCTorMRimaging.Itisdifficulttomakeareliable diagnosis of it on the basis of CT and MR images. However, clin- ically, it predominantly occurs in Inuit-Yupik and southern Chi- nese with a strong association with Epstein-Barr virus and a rela- tively long history. Imaging features, including an intraglandular mass with a lobulated/plaque-like shape and ill- or partially ill- definedmarginsbutwithoutcalcificationandnecrosis,accompa- niedbyipsilaterallymphadenopathy,suggestthediagnosisofsal- ivary gland LEC. REFERENCES 1. Schneider M, Rizzardi C. Lymphoepithelial carcinoma of the pa- rotid glands and its relationship with benign lymphoepithelial le- sions. Arch Pathol Lab Med 2008;132:278–82 2. Wang CP, Chang YL, Ko JY, et al. Lymphoepithelial carcinoma ver- sus large cell undifferentiated carcinoma of the major salivary glands. Cancer 2004;101:2020–27 3. Hsiung CY, Huang CC, Wang CJ, et al. Lymphoepithelioma-like carcinoma of salivary glands: treatment results and failure pat- terns. Br J Radiol 2006;79:52–55 4. Hoxworth JM, Hanks DK, Araoz PA, et al. Lymphoepithelioma-like carcinoma of the lung: radiologic features of an uncommon pri- marypulmonaryneoplasm.AJRAmJRoentgenol2006;186:1294–99 5. Kuo T, Hsueh C. Lymphoepithelioma-like salivary gland carci- noma in Taiwan: a clinicopathological study of nine cases demon- strating a strong association with Epstein-Barr virus. Histopathol- ogy 1997;31:75–82 6. Hilderman WC, Gordon JS, Large HL Jr, et al. Malignant lymphoe- pitheliallesionwithcarcinomatouscomponentapparentlyarising inparotidgland:amalignantcounterpartofbenignlymphoepithe- lial lesion? Cancer 1962;15:606–10 7. Ma H, Lin Y, Wang L, et al. Primary lymphoepithelioma-like carci- 1819 AJNR Am J Neuroradiol 35:1813–19 Sep 2014 www.ajnr.org