No Difference Between Mesothelioma and Pulmonary and Nonpulmonary Adenocarcinoma DO NOT DUPLICATE. Malignancy is a common cause of effusions of the

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1 NONGYNECOLOGIC CYTOPTHOLOGY CK5/6 in Effusions No Difference etween Mesothelioma and Pulmonary and Nonpulmonary denocarcinoma nnika Dejmek, M.D., Ph.D. Objective To test the performance of CK5/6 for the differentiation between mesothelioma, adenocarcinoma and benign mesothelial proliferations in effusion cytology. Study Design CK5/6 immunocytochemistry was applied to ethanol-fixed cytospin preparations from 74 benign and malignant effusions. Results Reactivity was seen in 7 of 8 mesotheliomas and in 9 of 11 benign mesothelial proliferations but also in 11 of 17 pulmonary adenocarcinomas and in 12 of 31 adenocarcinomas of nonpulmonary origin. Reactivity was also found in 3 of 5 non small cell lung carcinomas and 1 of 1 squamous carcinoma. Conclusion CK5/6 reactivity was found in a considerable proportion of metastatic adenocarcinomas of pulmonary and nonpulmonary origin. The high reactivity rate in pulmonary adenocarcinomas disagrees with the results obtained with histologic sections from solid tumor tissue, and CK5/6 seems to be of very limited value as an additional marker in effusion cytology. (cta Cytol 2008;52: ) lthough it cannot be ruled out that CK5/6 may add information when tested in an antibody panel, the results indicate that it is not a suitable marker in effusions. Keywords: adenocarcinoma, CK5/6, effusions, immunocytochemistry, mesothelioma. Malignancy is a common cause of effusions of the serous cavities. n effusion is often the first clinical manifestation in malignant mesothelioma, and in cases of metastatic carcinoma the primary tumor may still be unknown when an effusion develops. Immunocytochemistry is an established diagnostic tool in effusion cytology, and several antibodies and antibody panels have been recommended. 1 Keratins are a family of water-insoluble proteins of kd, present in virtually all epithelia. Different types of normal epithelia and epithelial tumors are characterized by different keratin patterns. Normal mesothelial cells with a mesenchymal phenotype express the low-molecular-weight keratins of simple epithelia. When the cells develop epithelial morphologic features, they also acquire high-molecular-weight keratins. This keratin pattern is also found in neoplastic mesothelial cells, whereas most adenocarcinomas express only low-molecular-weight keratins. 2,3 From the Department of Laboratory Medicine, Malmö University Hospital, Lund University, Malmö, Sweden. Dr. Dejmek is ssociate Professor. Supported by grants from the Malmö University Hospital Cancer Foundation. ddress correspondence to: nnika Dejmek, M.D., Ph.D., Department of Laboratory Medicine, Malmö University Hospital, Lund University, S Malmö, Sweden (annika.dejmek@med.lu.se). Financial Disclosure: The author has no connection to any companies or products mentioned in this article. Received for publication March 25, ccepted for publication ugust 7, /08/ /$21.00/0 The International cademy of Cytology CT CYTOLOGIC 579

2 Dejmek Thanks to the relatively selective expression of CK5 in mesothelial cells as compared to adenocarcinoma, CK5/6 has been proposed as a marker in the differentiation between mesothelioma and lung adenocarcinoma. Primary lung adenocarcinomas usually do not express CK5/6, whereas squamous carcinomas and many large cell carcinomas are CK5/6 positive. 3-8 Most studies have been performed on formalinfixed histologic sections, but the performance of CK5/6 as a diagnostic marker in effusions has so far attracted little interest. Therefore, CK5/6 was applied to a series of clinical malignant and benign effusions. Materials and Methods The study comprised 74 effusions (11 mesothelial proliferations, 8 mesotheliomas, 48 adenocarcinomas, 5 non small cell lung carcinomas, 1 renal carcinoma and 1 squamous carcinoma) analyzed at the Department of Laboratory Medicine, Malmö University Hospital, from February 2001 through September 2002 and for which an unequivocal final diagnosis could be established. To avoid bias towards cytologically easy cases, all effusions from the serous cavities containing mesothelial or epitheliallike cells regardless of cellular atypia were included. Thus, the metastatic tumors comprised the whole range of clearly malignant to cytologically atypical cases. The final diagnoses were based on all available morphologic, radiologic and clinical information (biopsy and/or autopsy if performed, cytologic examination of material from the primary tumor and/or metastases, clinical and radiologic information, and follow-up). From all fluids hematoxylin-eosin and Giemsastained smears were processed for morphologic evaluation. The immunocytochemical staining was performed on cytospin preparations from fresh fluids. The slides were immediately fixed in 95% ethanol, and all immunostaining were performed with Dako Tech-Mate 500 PLUS (Dakopatts, Älvsjö, Sweden) using the alkaline phosphatase anti alkaline phosphatase method (ChemMate Detection Kit no. K5000, Dako Cytomation, Glostrup, Denmark) to visualize the antigen-antibody complex. The CK5/6 antibody from Dakopatts was used. The slides were first evaluated by an experienced cytotechnologist in accordance with the routine of the laboratory and then on 2 different occasions by the author. The intensity of cytoplasmic immunostaining was estimated, and the proportion of stained cells was evaluated semiquantitatively. The reactivity was assigned to 3 groups: 2 = moderate or strong reactivity seen in most cells (> 70%), 1 = moderate or strong reactivity in part of the cell population (> 5% but < 70%) and 0. ll weak reactivity was considered negative (= 0). Staining in areas with degenerated cells and proteinaceous background was not considered in the evaluation. For all cases a negative control was included. Giemsa-stained cytospin preparation was always included to facilitate the identification of the relevant cells. Results The results for all cases, grouped according to tumor type, are given in Table I. majority of the mesothelial proliferations (9 of 11) and mesotheliomas (7 of 8) showed moderate or strong cytoplasmic CK5/6 staining in at least part of the cell population (Figure 1). However, reactivity was also found in 11 of 17 adenocarcinomas originating in lung and 12 of 31 adenocarcinomas of other origins (Figures 2 and 3). Three of five non small cell lung carcinomas were positive, as was 1 of 1 squamous carcinoma. No morphologic differences were observed between the positive and negative adenocarcinomas. s for the proportion of cases showing reactivity in most cells, there was no difference between benign and malignant cases (3 of 9 vs. 22 of 33, χ 2 test, p = 0.71), between benign cases and mesotheliomas (3 of 9 vs. 5/7, χ 2 test, p = 0.13) and between mesotheliomas and all other malignancies (5 of 7 vs. 17 of 26, χ 2 test, p = 0.76). Table I Reactivity to CK5/6 in Mesothelial Proliferations, Mesotheliomas and denocarcinomas in Effusions CK5/6 reactivity ll positivity Diagnosis Negative 1 2 (1 and 2) Mesothelial proliferation /11 Mesothelioma /8 Lung carcinoma denocarcinoma /17 Non small cell lung carcinoma /5 denocarcinoma sites other than lung /31 reast /8 Ovary serous /10 Ovary/peritoneum serous /4 Stomach /5 Prostate /1 Pancreas /2 Endometrium /1 Kidney carcinoma /1 Squamous carcinoma (maxilla) /1 ll cases / CT CYTOLOGIC Volume 52 Number 5 September October 2008

3 CK5/6 in Effusions Discussion Keratin 5 and 6 are found in many nonkeratinizing stratified squamous epithelia. CK5 is also expressed in so-called complex epithelia, especially basal cells of the breast, airways, prostate, urothelium, vagina and endometrium. 2 CK5/6 has been recommended for the differentiation between mesothelioma and pulmonary adenocarcinoma. In this study the sensitivity figures for mesotheliomas were similar to those reported for histologic specimens. 5-8 Reactivity was also seen in more than one third (39%) of all the adenocarcinomas from other primary Figure 1 Mesothelioma cells in pleural effusion. () Strong CK5/6 reactivity in all tumor cells (ethanol-fixed cytospin). () ir-dried, Giemsastained, routine smear ( and, 40). sites. When CK5/6 has been tested on histologic sections from formalin-fixed surgical specimens, reactivity in nonpulmonary adenocarcinomas has been reported. In a study of surgical specimens from 509 cases of epithelial neoplasms, Chu and Weiss 9 reported reactivity in 9% of nonpulmonary adenocarcinomas. The origins of the adenocarcinomas expressing CK5/6 were mainly endometrium, ovary, pancreas and breast. Ordonez 6 and Cury and coworkers 8 reported similar results, although their proportion of positive adenocarcinomas was slightly higher (15% and 14%, respectively). Marson and coworkers 10 reported reactivity in 3 of 37 adenocarcinomas (breast, Figure 2 Moderately differentiated lung adenocarcinoma in pleural effusion. () Strong CK5/6 reactivity in all tumor cells (ethanol-fixed cytospin). () ir-dried, Giemsa-stained, routine smear ( and, 40). Volume 52 Number 5 September October 2008 CT CYTOLOGIC 581

4 Dejmek Figure 3 Poorly differentiated lung adenocarcinoma in pleural effusion. () Dispersed tumor cells with strong CK5/6 reactivity (ethanol-fixed cytospin). () ir-dried, Giemsa-stained, routine smear ( and, 40). uterus and ovary) metastatic to lung. Kim and coworkers 11 reported CK6 reactivity in 28% of gastric adenocarcinomas tested. However, in the present study reactivity was also found in a considerable fraction of the lung adenocarcinomas tested (64%).These results are in disagreement with those obtained when CK5/6 has been applied to sections from solid tumor tissue. Clover and coworkers 5 studied CK5/6 reactivity in 27 lung adenocarcinomas and reported weak, equivocal reactivity in 4 cases only and patchy reactivity in 1 case. Chu and Weiss 9 reported reactivity in 1 of 21 lung adenocarcinomas. Only 1 previous study, conducted by Han and coworkers, 12 addressed the diagnostic utility of CK5/6 reactivity in cells in effusions. It was performed on formalin-fixed cell blocks, and the authors reported reactivity in 25% of the adenocarcinomas tested. The spectrum of positive nonpulmonary adenocarcinomas is to a great extent in agreement with the results reported on sections from surgical material, 6,8,9 but in contrast to those studies, Han and coworkers 12 reported a considerable fraction, 43%, of positive lung adenocarcinomas. This figure does not differ from the results of the present investigation (13 of 30 vs. 11 of 17, χ 2 test, p = 0.16). Thus, there is disagreement between the reported CK5/6 reactivity in histologic specimens from lung adenocarcinoma and the results obtained with effusions, as found in both this study and the study by Han and coworkers. 12 The reasons for discrepancies in reported immunoreactivity between different studies has been discussed in detail in a previous paper. 13 Discrepancies may be due to technical factors and to storage times and conditions The present study was performed on ethanol-fixed cytospin preparations from fresh effusions, a rapid and very reproducible technique, preserving antigens as well as morphologic features. Han and coworkers used formalin-fixed, paraffin-embedded cell blocks in their study but reported similar results for adenocarcinomas of pulmonary origin. Discrepancies between primary tumors, solid tissue metastases and metastatic cells shed into effusions may also be due to biologic differences. The immunophenotype may change during tumor progression, cells shed into effusions may reveal another immunophenotype than cells fixed in solid tissue, and late-stage tumor cells may represent aggressive subpopulations The recommendations of certain antibodies are often based on the results obtained with histologic sections, and the potential diagnostic consequences if the antibodies are applied to cytologic material are seldom stressed. Regardless of the reason for the reactivity found, it can be concluded that a considerable proportion of lung adenocarcinomas may be CK5/6 positive when immunocytochemistry is performed on cells in effusions. The results disagree with those previously reported for histologic sections from solid tumor tissue. lthough it cannot be ruled out that CK5/6 may add information when tested in an antibody panel, the results indicate that it is not a suitable marker in effusions. References 1. Fetsch P, bati : Immunocytochemistry in effusion cytology: contemporary review. Cancer (Cancer Cytopathol) 2001; 93: Moll R, Franke WW, Schiller DL, Geiger, Krepler R: The 582 CT CYTOLOGIC Volume 52 Number 5 September October 2008

5 CK5/6 in Effusions catalog of human cytokeratins: Patterns and expression in normal epithelia, tumors and cultured cells. Cell 1982;31: lobel G, Moll R, Franke WW, Kayser KW, Gould VE: The intermediate filament cytoskeleton of malignant mesotheliomas and its diagnostic significance. m J Pathol 1985;121: Moll R: Molecular diversity of cytokeratins: Significance for cell and tumor differentiation. cta Histochem (suppl 1) 1991; 41: Clover J, Oates J, Edwards C: nti-cytokeratin 5/6: positive marker for epithelial mesothelioma. Histopathology 1997; 31: Ordonez NG: Value of cytokeratin 5/6 immunostaining in distinguishing epithelial mesothelioma of the pleura from lung adenocarcinoma. m J Surg Pathol 1998;22: Ordonez NG: The immunohistochemical diagnosis of mesothelioma: comparative study of epithelioid mesothelioma and lung adenocarcinoma. m J Surg Pathol 2003;27: Cury PM, utcher DN, Fisher C, Corrin, Nicholson G: Value of the mesothelium-associated antibodies thrombomodulin, cytokeratin 5/6, calretinin, and cd44h in distinguishing epithelioid pleural mesothelioma from adenocarcinoma metastatic to the pleura. Mod Pathol 2000;13: Chu PG, Weiss LM: Expression of CK5/6 in epithelial neoplasms: n immunohistochemical study of 509 cases. Mod Pathol 2002;15: Marson VJ, Mazieres J, Groussard O, Garcia O, erjaud J, Dahan M, Carles P, Daste G: Expression of TTF-1 and cytokeratins in primary and secondary epithelial lung tumours: Correlation with histological type and grade. Histopathology 2004; 45: Kim M, Lee HS, Yang HK, Kim WH: Cytokeratin expression profile in gastric carcinomas. Hum Pathol 2004;35: Han J, Kim MK, Nam SJ, Yang JH: E-cadherin and cytokeratin subtype profiling in effusion cytology. J Korean Med Sci 2004;19: Dejmek J, Dejmek : The reactivity to CK5/6 antibody in tumor cells from non-small cell lung cancers shed into pleural effusions predicts survival. Oncol Rep 2006;15: Leong S: Pitfalls in diagnostic immunohistology. dv nat Pathol 2004;11: Shi SR, Cote RJ, Taylor JR: ntigen retrieval technique: Current perspectives. J Histochem Cytochem 2001;49: van den roek LJCM, van de Vijver MJ: ssessment of problems in diagnostic and research immunohistochemistry associated with epitope instability in stored paraffin sections. ppl Immunohistochem Mol Morphol 2000;8: Shidham V, Lindholm PF, Kajdacsy-alla, Chang CC, Komorowsky R: Methods of cytologic smear preparation and fixation: Effect on the immunoreactivity of commonly used anticytokeratin antibody E1/E3. cta Cytol 2000;44: Ramaekers FCS, Haag D, Kant, Moesker O, Jap PH, Vooijs GP: Coexpression of keratin- and vimentin-type intermediate filaments in human metastatic carcinoma cells. Proc Natl cad Sci US 1983;80: erner HS, Davidson, erner, Risberg, Kristensen G, Trope CG, Van de Putte G, Nesland JM: Expression of CD44 in effusions of patients diagnosed with serous ovarian carcinoma: Diagnostic and prognostic implications. Clin Exp Metastasis 2000;18: Davidson, Risberg, Goldberg I, Nesland JM, erner, Tropé CG, Kristensen G, ryne M, Reich R: Ets-1 mrn expression in effusions of serous ovarian carcinoma patients is a marker of poor outcome. m J Surg Pathol 2001;25: (erratum in: m J Surg Pathol 2002;26:539) 21. Davidson, Risberg, Reich R, erner : Effusion cytology in ovarian cancer: New molecular methods as aids to diagnosis and prognosis. Clin Lab Med 2003;23: Gemma, Takenaka K, Hosoya Y, Matuda K, Seike M, Kurimoto F, Ono Y, Uematsu K, Takeda Y, Hibino S, Yoshimura, Shibuya M, Kudoh S: ltered expression of several genes in highly metastatic subpopulations of a human pulmonary adenocarcinoma cell line. Eur J Cancer 2001;37: Volume 52 Number 5 September October 2008 CT CYTOLOGIC 583

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