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Lymphoepithelioma-Like Carcinoma of the Urinary Tract: a Clinicopathological Study of 30 Pure and Mixed Cases

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Lymphoepithelioma-Like Carcinoma of the Urinary Tract: a Clinicopathological Study of 30 Pure and Mixed Cases Modern Pathology (2007) 20, 828–834 & 2007 USCAP, Inc All rights reserved 0893-3952/07 $30.00 www.modernpathology.org Lymphoepithelioma-like carcinoma of the urinary tract: a clinicopathological study of 30 pure and mixed cases Ecaterina F Tamas1, Matthew E Nielsen2, Mark P Schoenberg2 and Jonathan I Epstein1,2,3 1Department of Pathology, Johns Hopkins Hospital, Baltimore, MD, USA; 2Department of Urology, Johns Hopkins Hospital, Baltimore, MD, USA and 3Department of Oncology, Johns Hopkins Hospital, Baltimore, MD, USA We studied 28 cases of lymphoepithelioma-like carcinoma of the bladder, one case in the renal pelvis, and one in the urethra. The mean age of the patients was 67.6 years with 21 (70%) males. Seventeen cases (56.7%) were pure with the remaining mixed with other patterns of carcinoma, including invasive urothelial carcinoma (n ¼ 10), invasive adenocarcinoma (n ¼ 3), and squamous cell carcinoma (n ¼ 2). The surface demonstrated carcinoma in situ (CIS) in six cases, noninvasive high-grade papillary urothelial carcinoma in three cases, and in situ adenocarcinoma in one case. In 19/30 (66%) cases, there was a heavy lymphocytic infiltrate and in the remaining 11/30 (34%) cases a mixed inflammatory infiltrate. None of the 26 cases labeled for EBV-encoded RNA by in situ hybridization. Tumor stages at presentation were: seven cases T1 (23%); 14 cases T2 (47%); seven cases T3 (23%); and two cases T4 (7%). Treatment consisted of radical cystectomy in 13/30 cases (43%); partial cystectomy in 4/30 cases (13%); nephrectomy in one case (3%), and transurethral resection often followed by radiation or chemotherapy in 12/30 (40%) cases. The mean follow up for patients without progression was 31 months. Eight of 27 cases with follow-up (30%) cases had tumor recurrence, with seven patients having metastases. In cases treated with cystectomy, the 5-year actuarial recurrence-free risk was 59% (62 and 57%, for pure and mixed cases, respectively). Lymphoepithelioma-like carcinoma, whether in pure or mixed form, has a similar prognosis to ordinary urothelial carcinoma when treated by cystectomy. Of the three pure cases treated by chemotherapy, two were free of disease at 4 and 65 months and the third had recurrent disease at 17 months. Given the association of lymphoepithelioma-like carcinoma with urothelial carcinoma in 47% of our cases and its propensity for multifocality, partial cystectomy would typically be ill advised for lymphoepithelioma-like carcinoma. Modern Pathology (2007) 20, 828–834; doi:10.1038/modpathol.3800823; published online 1 June 2007 Keywords: lymphoepithelioma; lymphoepithelioma-like; urothelial carcinoma; EBV encoded RNA; EBER Lymphoepithelioma is a form of undifferentiated reported in the renal pelvis, ureter, and urethra.5,8 carcinoma primarily described in the nasopharynx Lymphoepithelioma-like carcinoma of the urinary in Asian patients. In this location, there is a close bladder, first reported by Zuckerberg et al in 1991, is pathogenetic link of carcinoma to Epstein–Barr virus uncommon with a reported incidence between 0.4 (EBV). Carcinomas with similar histological features and 1.3% of all bladder carcinomas.12 Prior to the arising outside the nasopharynx are called lym- current series, the largest report in the literature phoepithelioma-like carcinoma. Lymphoepithelio- was a study of 13 cases by Lopez-Beltran et al.11 ma-like carcinoma has been described in a variety Although it has been suggested that lymphoepithe- of organs including salivary glands, thymus, lung, lioma-like carcinoma of the bladder is associated skin, stomach, uterine cervix, breast, prostate, and with a more favorable prognosis compared to the urinary tract.1–15 conventional invasive urothelial carcinoma, there In the urinary tract, they typically arise in the have been relatively few small studies on lympho- urinary bladder, although isolated cases have been epithelioma-like carcinoma in the literature to date.1,5,8,12 Correspondence: Dr JI Epstein, MD, Department of Pathology, Johns Hopkins Hospital, 401 N Broadway Street, Room 2242, Weinberg Building, Baltimore, MD 21231, USA. Materials and methods E-mail: [email protected] Received 9 February 2007; revised 2 April 2007; accepted 3 April Thirty cases of lymphoepithelioma-like carcinoma 2007; published online 1 June 2007 arising in the urinary tract were retrieved from the Lymphoepithelioma-like carcinoma of the urinary tract EF Tamas et al 829 consultation files of one of the authors and the than one non-lymphoepithelioma-like carcinoma archival files of Surgical Pathology at The Johns component). In addition to lymphoepithelioma-like Hopkins Hospital between 1990 and 2005 (16 carcinoma, the surface demonstrated carcinoma consults and 14 in-house cases). Lymphoepithelio- in situ (CIS) in six cases, noninvasive high-grade ma-like carcinoma was classified as pure when papillary urothelial carcinoma in three cases, and 100% of the tumor showed lymphoepithelioma-like in situ adenocarcinoma in one case (Figures 6 and carcinoma pattern, and mixed when associated with 7). Either invasive or noninvasive urothelial carci- usual infiltrating urothelial carcinoma, adenocarci- noma was associated with lymphoepithelioma-like noma, or squamous carcinoma. There were two carcinoma in 14/30 (47%) cases (Table 1). In 19/30 cases that were still considered pure lymphoepithe- (66%) cases, the inflammatory component consisted lioma-like carcinoma despite having rare foci of of a heavy lymphocytic infiltrate and in the remain- atypical morphology (see Results). ing 11/30 (34%) cases a mixed inflammatory Clinical follow up was possible in all cases, infiltrate composed of neutrophils, eosinophils, however 3/30 were recent cases with short follow- lymphocytes, histiocytes, and plasma cells (Figures up. Time to tumor recurrence was measured from 1 and 8). the date of cystectomy or in cases without cystect- All 28 cases studied expressed strong cytoplasmic omy from the date of the diagnostic tissue sampling. positivity for cytokeratin AE1/AE3 (Figure 9). None Recurrence-free survival risks were evaluated using of the 26 cases studied showed any labeling for Cox regression analysis (Stata, College Station, TX, EBER by in situ hybridization. USA). Tumor stages were as follows: seven cases T1 Immunohistochemical stains for cytokeratin AE1/ (23%); 14 cases T2 (47%); seven cases T3 (23%); and AE3 (Clone AE1/AE3 þ PCK26, Ventana) and EBV- two cases T4 (7%) (Table 1). Treatment consisted of encoded RNA (EBER) in situ hybridization (Epstein– cystoprostatectomy in 10/30 cases (33%); radical Barr Virus Probe, fluorescein conjugated, Vector cystectomy in 3/30 cases (10%); partial cystectomy Laboratories) were performed based on availability in 4/30 cases (13%); nephrectomy in one case (3%), of the blank slides. and transurethral resection (TUR) often followed by radiation or chemotherapy in 12/30 (40%) cases. All together, eight of 27 cases with follow-up (30%) Results cases had recurrence of tumor. Of the 27 patients, seven (26%) patients had metastases: three cases The mean age of the patients was 67.6 years (range: had lymph node metastasis and four cases had 44–90 years) with 21 (70%) males. The mean follow distant metastasis (lung (n ¼ 2); abdomen; skin, up for patients without progression was 32 months lymph nodes). The overall 5-year actuarial recur- (median: 34 months). The location of the tumor was rence-free risk was 69% (74 and 64% for pure and in the urinary bladder with the exception of one case mixed lymphoepithelioma-like carcinoma, respec- located in the renal pelvis and one case located in tively). In cases treated with cystectomy, the overall the urethra. 5-year actuarial recurrence-free risk was 59% (62 Seventeen cases (57%) had pure lymphoepithe- and 57%, for pure and mixed lymphoepithelioma- lioma-like carcinoma with the remaining cases like carcinoma, respectively). having lymphoepithelioma-like carcinoma with other patterns of carcinoma (Table 1). The epithelial component of lymphoepithelioma-like carcinoma Discussion consisted of nests and individual cells of undiffer- entiated carcinoma admixed with a prominent Lymphoepithelioma was originally described in the often-obscuring inflammatory infiltrate (Figures nasopharynx in Asian patients and was tightly 1–3). In two cases, o1% of the tumor had glandular associated with Epstein–Barr virus.1,11,12,16–18 The differentiation in an otherwise typical lymphoe- EBV-encoded RNA (EBER) is abundantly expressed pithelioma-like carcinoma, where the glandular in latently infected cells and in the malignant element merged with the typical lymphoepithelio- epithelial cells of nasopharyngeal carcinoma. The ma-like carcinoma and the glandular elements were function of EBER is still uncertain, but EBER heavily infiltrated by lymphocytes identical to transcripts provide a convenient marker of tumor— typical lymphoepithelioma-like carcinoma and in associated viral infection. In the nasopharynx, there contrast to adenocarcinoma associated with lym- is a strong association between p53 overexpression phocytes (Figure 4). In two other cases, the epi- and EBER status, and EBV-infected tumors are prone thelial component of lymphoepithelioma-like carci- to show an undifferentiated histology.16 noma was focally composed of clear cells (Figure 5). Similar morphological lesions have been reported Of the 13 cases without pure lymphoepithelioma- in the salivary glands, thymus, lung, skin, stomach, like carcinoma, the associated conventional carci- breast, genitourinary
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