Diagnostic Utility of MOC-31, HBME-1 and MOC-31mRNA in Distinguishing Between Carcinoma Cells and Reactive Mesothelial Cells in Pleural Effusions

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1 Diagnostic Utility of MOC-31, HBME-1 and MOC-31mRNA in Distinguishing Between Carcinoma Cells and Reactive Mesothelial Cells in Pleural Effusions Ying Sun, M.D., Guang-Ping Wu, Ph.D., Chang-Qing Fang, M.D., and Shu-Li Liu, M.D. Objective To evaluate the individual and combined diagnostic utility of MOC-31, HBME-1 and MOC-31mRNA in the differentiation of adenocarcinoma cells from reactive mesothelial cells in pleural effusions. Study Design To subject the cells from 293 pleural effusions to immunocytochemical staining for MOC-31 and HBME-1 and reverse transcriptase polymerase chain reaction for the expression of MOC-31. Results MOC-31 and MOC-31mRNA expression were significantly higher in the cancer cell group and in 3 subgrouped as adenocarcinoma, squamous cell carcinoma and small cell lung carcinoma than in the mesothelial cell group, whereas HBME-1 expression was obviously lower in those (p < The application of MOC-31 and HBME-1 for ICC in cell blocks is helpful in distinguishing cancer cells from reactive mesothelial cells. Nongynecologic Cytopathology 0.01). In single use, MOC-31mRNA had the highest sensitivity (90.8%) and accuracy (91.5%), whereas MOC-31 had the highest specificity (100%). When combinations of markers were evaluated together, MOC-31mRNA and HBME-1 gave a high diagnostic performance: sensitivity of 96.7% and accuracy of 95.2%, respectively. Conclusion The detection of MOC-31, HBME-1 and MOC-31- mrna is helpful in distinguishing between cancer and reactive mesothelial cells in pleural effusions. MOC- 31mRNA could be useful to the diagnosis of pleural micrometastasis. (Acta Cytol 2009;53: ) Keywords: immunocytochemistry, lung cancer, pleural effusion, reverse transcriptase polymerase chain reaction. From the Departments of Pathology, First Affiliated Hospital and College of Basic Medical Sciences, China Medical University, Shenyang, China. Dr. Sun is Ph.D. Student, Department of Pathology, First Affiliated Hospital and Department of Pathology, College of Basic Medical Sciences, China Medical University. Dr. Wu is Professor, Department of Pathology, First Affiliated Hospital and Department of Pathology, College of Basic Medical Sciences, China Medical University. Drs. Fang and Liu are Immunohistochemistry Technologists, Department of Pathology, College of Basic Medical Sciences, China Medical University. Supported by a grant from Shenyang Science & Technology Bureau (No ) and a grant from the Educational Department of Liaoning Province (No. 2004D164). Address correspondence to: Wu Guang-Ping, Ph.D., Department of Pathology, First Affiliated Hospital, and Department of Pathology, College of Basic Medical Sciences, China Medical University, Shenyang , China Financial Disclosure: The authors have no connection to any companies or products mentioned in this article. Received for publication July 31, Accepted for publication September 18, /09/ /$21.00/0 The International Academy of Cytology ACTA CYTOLOGICA 619

2 Sun et al Pleural effusions are commonly occurring complications produced by a wide variety of diseases. Approximately 20% of pleural effusions are caused by malignancy and in 10 50% of cancer patients may be the initial presentation. 1 One of the common difficulties in effusion cytology is the distinction between cancer cells and reactive mesothelial cells. Moreover, metastatic adenocarcinoma cells often are associated with prominent mesothelial hyperplasia, making the A combination of HBME-1 and MOC-31mRNA can significantly improve diagnostic accuracy. Table I Results of Marker Expressions in the Whole Population of Effusions diagnosis more difficult. Pleural effusion cytology findings are positive in only 60% of cases on average. 2 Thus, many additional methods have been evaluated to improve the diagnostic accuracy and avoid invasive diagnostic techniques. MOC-31 is a monoclonal antibody that recognizes an epithelial cell adhesion molecule (Ep-CAM), also known as human pan-carcinoma-associated epithelial glycoprotein-2 (EGP-2). 3 It has been shown that this antibody is useful in distinguishing mesothelial cells from metastatic adenocarcinoma in both tissue biopsies 4 and body fluids. 5 HBME-1 is an antibody raised against cultured mesothelioma cells and recognizes an antigen on the microvillus surface. 6 HBME-1 has also been presented as a mesothelial cell marker. 7 It has been reported that immunocytochemistry (ICC) and reverse transcriptase polymerase chain reaction (RT-PCR) technique were used to make the distinction between cancer cells and reactive mesothelial cells. 5,8 However, RT-PCR was less intensively used in serous effusions, although it provides excellent material for molecular analysis. In the present study, we combined ICC with RT-PCR for distinguishing between carcinoma cells and reactive mesothelial cells in pleural effusion specimens. Patients and Methods Patients The study was conducted according to the regulations of the institutional review boards at China Medical University. A total of 293 pleural samples were collected from the patients at the Laboratory of Cytopathology of the First Affiliated Hospital of China Medical University from April 2006 to October There were 156 males (53.2%) and 137 females (46.8%). Samples consisted of 217 carcinomas from a variety of primary sites and 76 benign diseases (Table I). The diagnosis of primary tumor and metastatic lung cancer was based on the histologic findings of biopsy or/and cytologic analysis. The patients who had a suspicious cytologic dignosis were rechecked or followed for identifying the presence of cancer cells. Seventy-six benign diseases were diagnosed by laboratory and clinical findings (reactions to antibiotics or antituberculous drugs) and/or cytologic analysis and histologic findings. Preparation of Cells from Plerual Effusions All specimens were received as fresh effusions, with a volume range of 20 2,000 ml. The specimens were centrifuged for 30 minutes at 2,000 g at 4 C. The resulting pellet was used for the preparation of 2 cytologic smears (alcohol fixed and Papanicolaou stained). The rest of the pellet was divided into 2 parts. One was used for preparation of the paraffin-embedded cell block. Another was stored at 70 C for subsequent No. of No. of positive cases (%) Cause cases MOC-31 HBME-1 MOC-31mRNA Malignancy (76.0) 25 (11.5) 197 (90.8) AcA (74.8) 19 (11.9) 144 (90.6) Lung Breast Gastric Squamous cell carcinoma (78.7) 6 (12.8) 42 (89.4) Lung Esophagus Small cell lung carcinoma 11 9 (81.8) 0 (0) 11 (100) Benign 76 0 (0) 72 (94.7) 5 (6.6) Parapneumonic Tuberculosis Congestive heart failure ACTA CYTOLOGICA Volume 53 Number 6 November December 2009

3 Diagnostic Utility of MOC-31 RT-PCR analysis. Immunocytochemistry For MOC-31 and HBME-1 staining, 2 4-μm sections were cut from every cell block, deparaffinized in xylene and rehydrated through graded alcohols. Sections were stained in an automated immunostainer (Ventana ES, Ventana Medical System, Inc., Tuscon, Arizona, U.S.A.) according to the manufacturer s instructions. As primary antibodies we used human pancarcinoma-associated epithelial glycoprotein-2 (clone MOC-31, prediluted; Maixin Bio, FuZhou, China) and human mesothelial cell (clone HBME-1, prediluted; Maixin Bio). For MOC-31, slides were first treated with the pepsin (DIG-3009; Maixin Bio) for 15 minutes at room temperature. The signal was detected using streptavidin-peroxidase, with 3,3- diaminobenzidine as the chromogen and hematoxylin as the counterstain. Two cytopathologists blindly assessed the immunostaining without knowledge of the immunocytochemical evaluation made by the other cytopathologist and without knowledge of the diagnosis. A positive result was defined as the presence of stain in > 10% of tumor cells in a malignant effusion or in > 10% of mesothelial cells in a reactive effusion. Membranous and/or cytoplasmic reactivity was regarded as MOC-31 positive, and only membranous reactivity was regarded as HBME-1 positive. Positive and negative controls were performed on each staining run. The grading of the immunostaining was performed on a sliding scale of 1+ to 4+ according to the percentage of reactive cells (negative = 0 10%, 1+ = 11 25%, 2+ = 26 50%, 3+ = 51 75%, 4+ = %). Reverse Transcriptase Polymerase Chain Reaction Total RNA extraction from the cell pellets was performed with Trizol (Gibco, Life Technologies, Rockville, Maryland, U.S.A.). RT-PCR was performed with 0.5 μg of total RNA using the TaKaRa RNA PCR KiT (AMV), version 3.0 (TaKaRa Biotechnology Co., Ltd, Dalian, Liaoning, China) and pairs of primers for MOC-31 and β-actin. Forward and reverse primers for MOC-31 and housekeeping gene β- actin were designed as follows: MOC-31 primers (forward 5 -AATAATCGTCAATGCCAGTGTA-3, reverse 5 -ATCGCAGTCAGGATCATAAAGC-3 ), β-actin primers (forward 5 -GGCATGGGTCA- GAAGGATTCC-3, reverse 5 -ATGTCACGCAC- GATTTCCCGC-3 ). The cdna synthesis was performed at 40 C for 30 minutes. After heat inactivation at 99 C for 5 minutes, 10 μl of cdna was subjected to PCR analysis. After a denaturing step at 94 C for 2 minutes, PCR was done at 94 C for 30 seconds, at the annealing temperature for 40 seconds and at 72 C for 4 minutes for 29 cycles. PCR products were separated by electrophoresis on a 1.7% agarose gel. DNA fragments were visualized and photographed under ultraviolet light with ethidium bromide staining. A 100-bp DNA ladder (TaKaRa Biotechnology Co., Ltd) was used as a size marker. Statistical Analysis Statistical analysis was performed using the χ 2 test or Fisher s exact test when theoretical effectiveness was insufficient. The level of statistical significance was set at p < The utility of each marker was determined by means of sensitivity, specificity and accuracy. Diagnostic values of the combination of ICC and RT-PCR results were calculated in parallel. Results Results of the marker assay in malignant group and benign group effusions are shown in Table I. MOC- 31 and MOC-31mRNA expression were significantly higher in carcinoma than in the benign disease group, whereas HBME-1 expression was significantly lower in the carcinoma than benign disease group (p < 0.01). MOC-31 staining was predominantly membranous with very weak cytoplasmic staining in cancer cells and no background staining (Figure 1). No cases of benign diseases (0%) reacted positively with MOC-31. HBME-1 showed strong membranous staining in mesothelial cells (Figure 2). The presence of MOC- 31mRNA was confirmed by a simultaneous round of RT-PCR using the housekeeping gene β-actin. Examples are shown in Figure 3. Table I also shows the marker expression in pleural Figure 1 Carcinoma cells showing immunoreactivity for MOC-31 in pleural fluid of a patient with lung cancer. The cancer cells show an atypical glandular cavity-like distribution with intense cytomembrane staining, whereas the reactive mesothelial cells present display negative staining (streptavidin-peroxidase, 400). Volume 53 Number 6 November December 2009 ACTA CYTOLOGICA 621

4 Sun et al Figure 2 Reactive mesothelial cells showing immunoreactivity for HBME-1 in pleural fluid. The cells show positive cytomembrane staining (streptavidin-peroxidase, 400). fluid of patients subgrouped as adenocarcinoma, squamous cell carcinoma and small cell lung cancer. MOC-31 stained 119 of 159 (74.8%) adenocarcinomas as well as 37 of 47 (78.7%) squamous carcinomas. Expression of Moc-31mRNA occurred in 144 of 159 (90.6%) adenocarcinomas and 42 of 47 (89.4%) squamous carcinomas. No statistically significant correlations were found between the positive ratio of adenocarcinomas and squamous carcinomas in assaying MOC-31 and MOC-31mRNA (p > 0.05). The positive rates of MOC-31mRNA were the highest in small cell lung carcinoma (100%). Table II depicts the sensitivity, specificity and accuracy of each marker, combinations of markers and cytology examination in pleural fluid. We used MOC- 31 and MOC-31mRNA for detecting carcinoma cells in the malignant pleural effusions and HBME-1 for detecting the mesothelial cells in benign pleural effusions, respectively for evaluating the efficiency of each diagnosis in differentiating malignant and benign effusions. In single use, MOC-31mRNA had the high- Table II Sensitivity, Specificity and Accuracy of MOC-31, HBME-1, MOC-31mRNA and Cytology in the Diagnosis of Pleural Effusions in Patients with Lung Cancer Sensitivity Specificity Accuracy Variable (%) (%) (%) Single MOC HBME MOC-31mRNA Combined MOC-31 + HBME MOC-31 + MOC-31mRNA HBME-1 + MOC-31mRNA Cytology est sensitivity (90.8%) and accuracy (91.5%), whereas MOC-31 had the highest specificity (100%). When combinations of markers were evaluated together, MOC-31mRNA and HBME-1 gave a high diagnostic performance: sensitivity of 96.7% and accuracy of 95.2%, respectively. Discussion Morphologic differentiation of reactive mesothelial cells from carcinoma cells in pleural effusions can be a diagnostic challenge. In particular, adenocarcinoma metastatic to the pleural membrane is often associated with prominent mesothelial hyperplasia and often results in diagnostic confusion. The difficulty is obviously greater when neoplastic cells show only slight atypia or when they are scarce in the effusion. False negative results of the cytologic examination of pleural fluid are a serious problem. Such errors in diagnosis usually are caused by misinterpretation of adenocarcinoma cells as reactive mesothelial cells. 9 The rate of false positive diagnoses also is significant and often caused by overinterpretation of reactive mesothelial cells as malignant cells. 5 ICC can greatly aid in such diagnostic dilemmas, but, currently, available markers have varying sensitivities and specificities for mesothelial cells or cells of epithelial differentiation. 10,11 Figure 3 RT-PCR for MOC-31 in pleural fluid. Ethidium bromide stained agarose gel: 100-bp molecular marker (lane M); pleural fluids from lung cancer (lanes 1 11); pleural fluids from benign disease (lanes 12 14). 622 ACTA CYTOLOGICA Volume 53 Number 6 November December 2009

5 Diagnostic Utility of MOC-31 Recently, PCR techniques have been evaluated largely for the detection of cancer cells in blood, bone and lymph nodes, and they have proven to be more sensitive than conventional techniques. 12,13 MOC-31 is a monoclonal antibody initially raised against a small cell carcinoma cell line. The antibody recognizes an epithelial cell adhesion molecule (Ep- CAM), also known as EGP-2. 4 MOC-31 is a reliable marker of epithelial cells. As there are not epithelial cells in benign pleural effusions, expression of MOC- 31 may indicate that the cancer cells metastasized to the pleural effusion from elsewhere. In our study, MOC-31 sensitivity was 76.0%, with 100% specificity in distinguishing cancer cells and reactive mesothelial cells. Our study showed that MOC-31 was a useful marker in diagnosing plural effusions with carcinoma. HBME-1 is a monoclonal antibody directed against the microvillous surface of mesothelial cells. It is a good marker in distinguishing between mesothelial cells and nonmesothelial cells in body fluids. 5,14 In the present study, HBME-1 sensitivity of detecting mesothelial cells achieved 94.7%; corresponding specificity was 88.5%. A difference in the staining pattern of HBME-1 between cells of mesothelial origin and adenocarcinoma cells was observed: the former appeared in a thick (bushy) membrane pattern, whereas the latter had a cytoplasmic staining pattern. It is advantageous to use for HBME-1 in distinguishing reactive mesothelial cells from cancer cells. RT-PCR method has been reported and recommended to facilitate the detection of few or single carcinoma cells in pleural effusions. 15,16 Our study confirmed that the sensitivity of RT-PCR is elevated as compared with ICC. MOC-31mRNA in detecing carcinoma cells achieved a very high sensitivity, 90.8%; corresponding specificity was 93.4%. Of the 197 carcinoma cell cases positive by RT-PCR, 32 were negative by ICC, whereas 165 cases positive by ICC were also positive by RT-PCR. The diagnostic sensitivity of carcinoma cells with RT-PCR was 90.8%, significantly higher than that with ICC (76.0%, p < 0.05). Earlier diagnosis of malignant pleural effusions thus may be established by means of detecting MOC- 31mRNA in occult cancer cells by RT-PCR. Vicidomini et al 17 demonstrated that patients with positive cytology always have poor prognosis and short survival. According to our study, we can infer that patients with expression of MOC-31mRNA have a high risk of pleural metastasis and recurrence. The existence of MOC-31mRNA indicates that there may be micrometastases on the pleura and that they can be considered a pretreated factor. Further studies might be used for monitoring the effects of therapy. In the current study, the positive rate of MOC-31 mrna was the highest in small cell lung carcinoma (100%), but definitive conclusions could not be made as there were fewer cases in the group. At present, there is an obvious limitation in the international TNM staging of non small cell lung carcinoma that was absent from the interpretation of occult tumor cells. 18,19 Additionally, the inclusion of the interpretation of occult micrometastases in the current TNM staging system is also recommended by the International Union Against Cancer. 20 Thus, detecting MOC-31mRNA in a pleural effusion can provide a supplement to TNM staging. In the current study, MOC-31mRNA sensitivity and accuracy achieved 90.8% and 91.5% respectively, which were superior to those of MOC-31. We conclude that the application of MOC-31 and HBME-1 for ICC in cell blocks is helpful in distinguishing cancer cells from reactive mesothelial cells. A combination of HBME-1 and MOC-31mRNA can significantly improve diagnostic accuracy. MOC- 31mRNA could be useful in the diagnosis of pleural micrometastasis. References 1. Monte SA, Ehya H, Lang WR: Positive effusion cytology as the initial presentation of malignancy. Acta Cytol 1987;31: Maskell NA, Butland RJA: BTS guidelines for the investigation of a unilateral pleural effusion in adults. Thorax (suppl 11) 2003;58:ii8 ii17 3. Ordóñez NG: Value of immunohistochemistry in distinguishing peritoneal mesothelioma from serous carcinoma of the ovary and peritoneum: A review and update. Adv Anat Pathol 2006;13: Oates J, Edwards C: HBME-1, MOC-31, WT1 and calretinin: An assessment of recently described markers for mesothelioma and adenocarcinoma. Histopathology 2000;36: Politi E, Kandaraki C, Apostolopoulou C, Kyritsi T, Koutselini H: Immunocytochemical panel for distinguishing between carcinoma and reactive mesothelial cells in body cavity fluids. Diagn Cytopathol 2005;32: Miettinen M, Kovatich A: HBME-1, a monoclonal antibody useful in the differential diagnosis of mesothelioma, adenocarcinoma, and soft-tissue and bone tumors. Appl Immunohistochem 1995;3: Gümürdülü D, Zeren EH, Cagle PT, Gümürdülü D, Zeren EH, Cagle PT, Kayasel uk F, Alparslan N, Kocabas A, Tuncer I: Specificity of MOC-31 and HBME-1 immunohistochemistry in the differential diagnosis of adenocarcinoma and malignant mesothelioma: A study on environmental malignant mesothelioma cases from Turkish villages. Pathol Oncol Res 2002;8: Passebosc-Faure K, Li G, Lambert C, Cottier M, Gentil- Perret A, Fournel P, Pérol M, Genin C: Evaluation of a panel of molecular markers for the diagnosis of malignant serous effusions. Clin Cancer Res 2005;11: Afify AM, Stern R, Michael CW: Differentiation of mesothelioma from adenocarcinoma in serous effusions: The role of hyaluronic acid and CD44 localization. Diagn Cytopathol Volume 53 Number 6 November December 2009 ACTA CYTOLOGICA 623

6 Sun et al 2005;32: Ordonez NC: The immunohistochemical diagnosis of mesothelioma: A comparative study of epithelioid mesothelioma and lung adenocarcinoma. Am J Surg Pathol 2003;27: Yaziji H, Battifora H, Barry TS, Hwang HC, Bacchi CE, McIntosh MW, Kussick SJ, Gown AM: Evaluation of 12 antibodies for distinguishing epithelioid mesothelioma from adenocarcinoma: Identification of a three-antibody immunohistochemical panel with maximal sensitivity and specificity. Mod Pathol 2006;19: Gerhard M, Juhl H, Kalthoff H, Schreiber HW, Wagener C, Neumaier M: Specific detection of carcinoembryonic antigenexpressing tumor cells in bone marrow aspirates by polymerase chain reaction. J Clin Oncol 1994;12: Mori M, Mimori K, Ueo H, Tsuji K, Shiraishi T, Barnard GF, Sugimachi K, Akiyoshi T: Clinical significance of molecular detection of carcinoma cells in lymph nodes and peripheral blood by reverse transcription polymerase chain reaction in patients with gastrointestinal or breast carcinomas. J Clin Oncol 1998; 16: Lozano MD, Panizo A, Toledo GR, Sola JJ, Pardo-Mindán J: Immunocytochemistry in the differential diagnosis of serous effusions: A comparative evaluation of eight monoclonal antibodies in Papanicolaou stained smears. Cancer 2001;93: Yu CJ, Shew JY, Liaw YS, Kuo SH, Luh KT, Yang PC: Application of mucin quantitative competitive reverse transcription polymerase chain reaction in assisting the diagnosis of malignant pleural effusion. Am J Respir Crit Care Med 2001;164: Grünewald K, Haun M, Fiegl M, Urbanek M, Müller-Holzner E, Massoner A, Riha K, Propst A, Marth C, Gastl G: Mammaglobin expression in gynecologic malignancies and malignant effusions detected by nested reverse transcriptase-polymerase chain reaction. Lab Invest 2002;82: Vicidomini G, Santini M, Fiorello A, Parascandolo V, Calabrò B, Pastore V: Intraoperative pleural lavage: Is it a valid prognostic factor in lung cancer? Ann Thorac Surg 2005;79: Saintigny P, Coulon S, Kambouchner M, Ricci S, Martinot E, Danel C, Breau JL, Bernaudin JF: Real-time RT-PCR detection of CK19, CK7 and MUC1 mrna for diagnosis of lymph node micrometastases in non small cell lung carcinoma. Int J Cancer 2005;115: Dong Q, Huang J, Zhou Y, Li L, Bao G, Feng J, Sha H: Hematogenous dissemination of lung cancer cells during surgery: Quantitative detection by flow cytometry and prognostic significance. Lung Cancer 2002;37: Hermanek P, Hutter RV, Sobin LH, Wittekind C: International Union Against Cancer: Classification of isolated tumor cells and micrometastasis. Cancer 1999;86: ACTA CYTOLOGICA Volume 53 Number 6 November December 2009

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