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Immunohistochemical Differential Diagnosis Between Thymic Carcinoma and Type B3 Thymoma: Diagnostic Utility of Hypoxic Marker, GLUT-1, in Thymic Epithelial Neoplasms

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Immunohistochemical Differential Diagnosis Between Thymic Carcinoma and Type B3 Thymoma: Diagnostic Utility of Hypoxic Marker, GLUT-1, in Thymic Epithelial Neoplasms Modern Pathology (2009) 22, 1341–1350 & 2009 USCAP, Inc. All rights reserved 0893-3952/09 $32.00 1341 Immunohistochemical differential diagnosis between thymic carcinoma and type B3 thymoma: diagnostic utility of hypoxic marker, GLUT-1, in thymic epithelial neoplasms Masakazu Kojika1,2, Genichiro Ishii1, Junji Yoshida2, Mituyo Nishimura2, Tomoyuki Hishida2, Shu-ji Ota1, Yukinori Murata1, Kanji Nagai2 and Atsushi Ochiai1 1Pathology Division, Research Center for Innovative Oncology, National Cancer Center Hospital East, Kashiwa, Chiba, Japan and 2Thoracic Surgery Division, National Cancer Center Hospital East, Kashiwa, Chiba, Japan There are only a few immunohistochemical markers that are useful for differentiating thymic carcinomas from type B3 thymomas. The purpose of this study is to examine the additional markers that would be useful for differentiating between thymic carcinoma and thymoma type B3. We performed a tissue microarray analysis of surgically resected thymic tumor specimens from12 cases of thymic carcinoma, 7 cases of type B3 thymoma, and 68 cases of other types of thymoma. Immunostaining using 49 antibodies was scored based on staining intensity and the percentage of cells that stained positive. Seven proteins that were selected by the staining scores, namely, GLUT-1 (167 vs 4), CA-IX (110 vs 15), c-kit (162 vs 44), CD5 (33 vs 0), MUC-1 (54 vs 0), CEA (42 vs 0), and CK18 (110 vs 42), were significantly higher in the thymic carcinomas than in the type B3 thymomas. The staining sensitivity and specificity of the antibodies for thymic carcinoma were GLUT-1, sensitivity 72% and specificity 100%; CA-IX, 58 and 71%; c-kit, 72 and 85%; CD5, 33 and 100%; CK18, 58 and 71%; MUC-1, 25 and 100%; and CEA, 33 and 100%. Glucose transporter 1 (GLUT-1) is the best marker for thymic carcinoma because it had the highest sensitivity and specificity. Positive immunostaining for a combination of three markers, namely, GLUT-1, CD5, and CEA, enabled differentiation of thymic carcinoma with 91.6% sensitivity and 100% specificity. In conclusion, we identified GLUT-1 as an additional marker that will be useful for differentiating thymic carcinoma from type B3 thymoma, especially in biopsy specimens that have been crushed or are otherwise difficult to examine morphologically in thymic tumors. Modern Pathology (2009) 22, 1341–1350; doi:10.1038/modpathol.2009.105; published online 31 July 2009 Keywords: thymic carcinoma; thymoma; type B3 thymoma; GLUT-1; CA-IV The thymus is an immune-related organ, whose consist of tumor cells similar to carcinomas occur- network-forming epithelial cells are responsible for ring in other organs with infiltrating mature T cells. immature T-cell (thymocyte) growth, development, However, little is known about the pathogenesis of and differentiation. Thymic epithelial tumors are thymoma or thymic carcinomas. traditionally classified as thymomas and thymic In 1999, the World Health Organization (WHO) carcinomas. Thymomas consist of neoplastic epithe- published a classification of thymic epithelial lial cells and immature T cells intermingled in tumors that is based on the morphology of the variable proportions, whereas thymic carcinomas epithelial cells and the lymphocyte-to-epithelial cell ratio of the tumor. Thymic epithelial tumors are Correspondence: Dr A Ochiai, MD, PhD, Pathology Division, classified into five types: A, AB, B1, B2, and B3. In Research Center for Innovative Oncology, National Cancer type A the epithelial cells appear spindle-shaped or Center Hospital East, 6-5-1, Kashiwanoha, Kashiwa-City, Chiba oval, whereas in type B they are dendritic or plump, 277-8577, Japan. and tumors that combine these two morphologies E-mail: [email protected] Received 16 February 2009; revised and accepted 2 June 2009; are designated as type AB. Type B thymomas are published online 31 July 2009 subdivided into subtypes B1, B2, and B3, increasing www.modernpathology.org Thymic carcinoma and type B3 thymoma 1342 M Kojika et al with the ratio of atypia in the neoplastic cells. Type were stained using hematoxylin and eosin (H&E). B3 thymoma was predominantly epithelial type, The sections were reviewed by two pathologists with severe cellular atypia and a few immature T (MK, GI), according to the histological criteria cells around the tumor cells, and was considered to described in the WHO classification, and the be a borderline malignancy. On the other hand, all discrepancies were resolved by joint discussion of thymic carcinomas are classified as type C thymo- the slides while viewing with a multiheaded micro- mas. In 2004, the WHO classification of thymic scope. In addition to the morphological examination, tumors was revised and the term ‘type C thymoma’ we examined the sections for the presence of was replaced by ‘thymic carcinoma.’1,2 The validity immature T thymocyte using CD99 and terminal of this classification as a prognostic tool is a matter deoxynucleotidyl transferase immunostaining. of controversy, even if the preliminary studies are encouraging. It is sometimes difficult to make the differential diagnosis between thymoma type B3 and Construction of Tumor Tissue Microarrays thymic carcinoma histologically, especially when the Tissue microarrays were constructed according to biopsy specimen is small. Although immunoreactiv- the procedure described in previous reports.12–14 ity for CD5 and c-kit has been reported as a useful Briefly, the most representative tumor areas were marker for primary thymic carcinoma, but not for carefully selected and marked on the H&E-stained thymoma, the positive rate of CD5 and c-kit has been slide to construct the microarrays, and the tissue reported to be limited to over 50%;3–7 and as not all microarrays were assembled using a tissue arraying neoplastic cells in thymic carcinomas stain positive instrument (KIN-1; Azumaya, Tokyo, Japan).15 The for these markers,8–11 it will be necessary to identify microarray system consists of thin-walled stainless other diagnostic markers to make the differential steel needles approximately 2 mm in diameter, and a diagnosis more reliable. stylet for transferring and removing the contents of In this study, we used a tissue microarray with a the needle. The assembly is held in an x-y position large panel of antibodies to identify additional guide that is manually adjusted using digital micro- immunohistochemical markers to phenotypically meters. Core samples are retrieved from selected differentiate between thymic carcinomas and type areas of donor tissue and precisely arrayed in a new B3 thymomas. (recipient) paraffin block. Samples of the specimens were routinely obtained by collecting two replicate Materials and methods core samples of the tumor from different areas. The normal thymus tissue and liver tissue, used as the Case Selection positive/negative control, were arrayed in sample During the period from January 1992 to December paraffin blocks. 2006, a total of 94 patients with thymic epithelial tumors were treated at the National Cancer Center Hospital East, Chiba, Japan. All thymic epithelial Antibodies and Immunohistochemical Staining tumors, with a pathological diagnosis based on the The 49 antibodies used in this study are listed in classification schema of the third edition of the WHO Table 1. Immunohistochemical staining was per- classification, were reviewed, and 18 tumors were formed according to the procedure described in a diagnosed as type A thymoma, 27 as type B1 and 10 previous report.13 Tissue microarray donor blocks as type B2 thymoma, 12 as type AB thymoma, and 18 were cut into 4-mm sections and mounted on silane- as thymic carcinoma. The six cases of thymic coated slides. The sections were then deparaffinized carcinoma, and four cases of thymoma, for which in xylene and dehydrated in a graded alcohol series, an adequate tissue specimen was not available for and the endogenous peroxidase was blocked using pathological review, were excluded from the study, 3% hydrogen peroxide in absolute methyl alcohol. leaving a total of 84 cases of thymic epithelial tumor Heat-induced epitope retrieval was performed for for review. The tumors selected for tissue microarray 20 minutes at 951C using a 0.02-mol/l concentration analysis were: 10 cases of type A thymoma, 5 cases of of citrate buffer (pH 6.0). After allowing the slides to type B1 thymoma, 5 cases of type B2 thymoma, 7 cool at room temperature for 60 minutes, they were cases of type B3 thymoma, and 12 cases of thymic rinsed with deionized water and incubated over- carcinomas. The 12 cases of thymic carcinoma night with the primary antibodies. The slides were consisted of 6 cases of keratinizing carcinoma and 6 then washed thrice with phosphate-buffered saline cases non-keratinizing carcinoma. Representative and incubated with the EnVision þ System-HRP figures of type B3 thymoma and thymic carcinoma (Dako, Glostrup, Denmark). The reaction products are shown in Figure 1a, b, c, and d. were stained using diaminobenzidine and counter- stained using hematoxylin. Some antibodies Pathological Studies (Table 1) were used in an automated immunostainer (Ventana Medical Systems, Tucson, AZ, USA) after After fixing the specimens with 10% formalin and antigen retrieval by microwave heating and using embedding them in paraffin, serial 4-mm sections citrate buffer. Immunostaining was recorded as Modern Pathology (2009) 22, 1341–1350 Thymic carcinoma and type B3 thymoma M Kojika et al 1343 Figure 1 Preparation of tissue microarray using hematoxylin and eosin stain. (a) Histological features of type B3 thymoma. (b) Histological features of thymic carcinoma. (c) Histological features of type B3 thymoma (higher magnification). Severe cellular atypia with conspicuous nucleoli and a few immature T cells around the tumor cells are seen. (d) Histological features of thymic carcinoma (higher magnification). positive when more than 20% of the cancer cells as score for that tumor. The staining scores obtained exhibited intermediate or strong staining (staining for the two samples from the same specimen were intensity ¼ 2, 3).
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