MALIGNANT PLEURAL EFFUSION IN EGYPT

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1 MALIGNANT PLEURAL EFFUSION IN EGYPT Ahmed M. Abd El-Aziz 1, Hala M. N. Hosni 2, Mohamed F. Darweesh 3, Salma T. Hafez 4 1, 2, 3 Pathology Department, Faculty of Medicine, Cairo University, Egypt ABSTRACT Background: Malignant pleural effusions (MPEs) represent common and debilitating complications of a wide array of malignancies; virtually any malignant cell type can cause a MPE with metastatic adenocarcinoma being the most common tumor type.the diagnostic performance of the cytologic study of the fluid may be attributed to the fact that the cell population present in sediment is representative of a much larger surface area than that obtained by needle biopsy. Separating benign from malignant cellular changes may require meticulous screening, careful scrutiny of cellular features, and an understanding of the range of reactive changes. Aim of the work: To study cases of malignant pleural effusion in AL Kasr AL Aini Hospital. Methods: Pathology reports from malignant pleural effusion patients were obtained from the archives of the pathology department, cytology unit in Kasr AL Aini Hospital. Results: Non-mesothelioma (metastatic) cases are the most common cause of malignant pleural effusion. Recommendations: Use of immunohistochemical stains in differentiating adenocarcinoma from malignant mesothelioma. Key words: Malignant pleural effusion- Malignant Mesothelioma- Adenocarcinoma. 326

2 Ahmed M. Abd El-Aziz et al INTRODUCTION Pleural effusions are common problem resulting from accumulation of fluid in the pleural space. They reflect the presence of pleural, pulmonary, or extra pulmonary disease and are classified as either transudates or exudates (Moffet et al., 2009). Transudative effusions occur when the systemic factors influencing the formation and absorption of pleural fluid are altered such that pleural fluid accumulates. Most transudative pleural effusions are due to left ventricular failure or cirrhosis, so no need for pleural investigation but the systemic condition should be treated. While the most common causes of exudative effusions pleural effusions are malignancy, Para pneumonic effusions and empyema, tuberculosis and pulmonary embolus, so it is important to determine the local disease that is responsible for the effusion (Light 2007). Malignant pleural effusions (MPE) can result from primary malignancies of the pleura or from underlying intrathoracic or extrathoracic malignancies that reach the pleural space by hematogenous, lymphatic, or contiguous spread. Although virtually any malignant cell type can cause an MPE, more than 75% of MPEs are caused by neoplasms of the lung, breast, or ovary or by lymphomas (Awasthi et al., 2007). Regardless of the etiology of MPE, the median survival from clinical recognition is 4 months; however, prolonged survival is possible in some patients (Heffner et al., 2000). Metastatic adenocarcinoma is the most common tumor type. Malignant pleural mesothelioma (MPM) develops from malignant transformation of mesothelial cells in the pleural membranes. Malignant pleural mesothelioma is an uncommon neoplasm, associated usually with history of chronic asbestos exposure. The physical examination and chest radiographs will demonstrate a large pleural effusion in 80% to 90% of MPM (Ismail-Khan et al., 2006). 327

3 Pleural fluid cytology may yield a definitive diagnosis of MPM in 20% to 33% of patients. In additional to standard histology, special immunohistochemical stains may be necessary to make a definitive diagnosis of malignant pleural mesothelioma because of its histomorphologic similarities to adenocarcinoma. Mesothelioma is characterized by staining for calretinin in 88% and vimentin in 50% of patients. However, adenocarcinoma usually lacks these markers and instead stains positive for carcinoemberyonic antigen (84%) (Zellos and Sugarbaker 2002). The aim of our study is to detect the incidence of malignant pleural effusion, prevalence of mesothelioma as a cause of malignant pleural effusion with Statistical evaluation of clinical, patient data and cytological findings of value, as a guide in diagnosis of malignant pleural effusion. MATERIAL AND METHODS Material Clinical requests and cytology reports from 67 patients suffering from malignant pleural effusion were collected from the archives of the Cytology Unit, Pathology Department, Faculty of Medicine, Cairo University, in the period from April 2007 to September Data collected from cytology sheet included age and sex of patients as well as significant clinical and pathological data. Methods Patient slides stained by H&E, Papanicolaou and Giemsa were revised, categorized as mesothelioma and non-mesothelioma and photographed with Olympus digital camera ( EX 330 ) attached to an Olympus microscope model BX 51. Statistical methods Percentage calculations Descriptive analyses: bar and pie chart. 328

4 Ahmed M. Abd El-Aziz et al RESULTS Malignant pleural effusions, archived cases were reviewed, in the period from April 2007 to September The number of malignant pleural effusions cases was 67 and diagnosed in the Cytology Unit, Pathology Department, Faculty of Medicine, Cairo University. The common age group for malignant pleural effusion patients was (52 61 years) presenting (16 patients, 24.6%). As illustrated in table (1). Table (1): Age distribution among studied cases of malignant pleural effusion * Age was not recorded in two cases. Age (years) Group Number (n) Percentage % % % % % % % % Total % Female predominance was observed among the studied cases of malignant pleural effusion, they represented 61.2 % of cases and the ratio of females to males was 1.6:1 (41 female: 26 males). 329

5 The majority of studied cases of malignant pleural effusion were metastatic (83.6%) while only 11 cases (16.4%) diagnosed as mesothelioma. As illustrated in table (2). Table (2): Incidence of mesothelioma in the studied cases. Type of malignancy No. of cases Percentage (n) (%) Mesothelioma Metastatic Total The cases with metastatic type (56 cases) were further categorized according to their origin of metastasis as following: (21.4%) were metastatic from breast cancer, (17.8%) lymphoma, (5.4%) considered as adenocarcinoma, (3.6%) were bronchoalveolar carcinoma, (3.6%) were lung small cell carcinoma, only (1.8%) was bronchogenic carcinoma, (1.8%) papillary carcinoma and (1.8%) signet ring carcinoma and finally the origin of metastasis for 24 cases were not identified. As illustrated in table (3). 330

6 Ahmed M. Abd El-Aziz et al Table (3): Classification of cases with metastatic pleural effusion Origin of metastasis(primary tumor) No. of each cases (n) Percentage of each type Unidentified % Breast cancer % Lymphoma % Adenocarcinoma 3 5.4% Bronchoalveolar carcinoma 2 3.6% Small cell carcinoma 2 3.6% Bronchogenic carcinoma 1 1.8% Papillary cell carcinoma 1 1.8% Signet ring carcinoma 1 1.8% Total % 331

7 Figure (1)Malignant pleural effusion showing group of malignant mesothelial cells with pleomorphic nuclei and fluffy or burry outline, note hemorrhagic background, Mesothelioma, H&E x 200) Figure (2) Malignant pleural effusion showing group of malignant mesothelial cells with marked cellular and nuclear pleomorphic nuclei, Mesothelioma, (Pap x 1000) 332

8 Ahmed M. Abd El-Aziz et al Figure (3) Malignant pleural effusion showing ball of malignant mesothelial cells with irregular outline, Mesothelioma, (Pap x 200) Figure (4) Malignant pleural effusion showing 3D balls of malignant cells with smooth outline, note hemorrhagic background, adenocarcinoma H&E x 200) 333

9 Figure (5) Malignant pleural effusion showing m3d balls of malignant cells with overlapping nuclei, adenocarcinoma H&E x 400) Figure (6) Malignant pleural effusion showing malignant large vacuolated cells with peripherally flattened nuclei, Signet cell carcinoma H&E x 200) 334

10 Ahmed M. Abd El-Aziz et al Figure (7) Malignant pleural effusion showing malignant epithelial cells arranged in linear pattern Indian file lobular carcinoma Pap x 200) Figure (8) Malignant pleural effusion showing an irregular group of malignant cells with pleomorphic nucleus and prominent nucleoli, Bronchoalveolar carcinoma Pap x 400) 335

11 Figure (9) Malignant pleural effusion showing an irregular group of malignant cells with pleomorphic nucleus, Small cell carcinoma H&E x 400) Concerning the side of pleural effusion, there were 51 cases with the side of the pleural effusion known while the side of effusion was not recorded in 16 cases. Regarding to the available 51 cases, there were 30 cases (58.8 %) with right pleural effusion, 19 cases (28.4 %) with left sided pleural effusion and 2 cases with bilateral pleural effusion. There were 32 cases (47.8 %) with hemorrhagic pleural effusion while the remaining 35 cases (52.2%) showed non-hemorrhagic pleural effusion fluid. Concerning the volume of pleural fluid needed for accurate diagnosis of cases of malignant pleural effusion, the volume of collected samples was found to be concentrated at the volume between 2 to 20 cc while in 3 cases volume was not recoded. 336

12 Ahmed M. Abd El-Aziz et al DISCUSSION The pleural space normally contains between 7 and 16 ml of fluid. Any accumulation of fluid in the pleural space is the result of an increased production exceeding the rate of fluid removal (Miserocchi 1997, Marios 2008). Pleural effusion as initial manifestation in a patient without accompanying symptoms is a major diagnostic problem. A large number of diseases may be the cause of pleural effusion. Different mechanisms are involved in the creation of pleural effusions. Time may be wasted before an accurate diagnosis is made in patients with pleural effusion, as the pleura is an inner cavity with no direct access, adding some difficulty to the diagnosis (Marios 2008). For exudates, malignancy, bacterial pleurisy and tuberculous effusions are the principle differential diagnosis (Chesnutt and Prendergast 2004).An exudative effusion has a higher probability of being malignant than transudative effusion, however, the finding is non-specific because of the multiple inflammatory causes of exudative effusions. It should be noted that 3 % to 10% of MPEs are transudates (Heffner and Klein 2008).Malignant Pleural effusions affects over 150,000 patients each year in the united states, often depriving patients with cancer of their quality of life, and is associated with significant health costs (Davies 2008). Effusions due to malignancy are frequently symptomatic, and in case of pleural space, may be the presenting sign of cancer (DeCamp et al., Reducing symptoms and improving quality of life is the primary goal of treatment in these patients. If a patient presents with respiratory distress, due to large size of the effusion, or mediastinal mass or both, thoracocentesis should be considered as the initial diagnostic and therapeutic procedure of choice (Pietsch et al., 1999). Pleural fluid cytology is the simplest definitive method to obtain a diagnosis of malignant effusion. Malignant effusions can be diagnosed by a single pleural fluid cytology specimen in 60 % of the cases for carcinomatous effusions but only 20-30% for mesothelioma. This yield is only slightly increased if repeated cytology 337

13 specimens are analyzed. The cytological yield is higher for adenocarcinoma (Marios 2008). Overall, the diagnostic yield of pleural cytology is dependent on such factors as the extent of disease and nature of primary malignancy (Antony et al., 2001). Immunohistochemical epithelial and glandular markers may help to confirm epithelial malignancy and differentiate mesothelioma from adenocarcinoma (Marios 2008). Metastatic adenocarcinoma, especially from primary lung and breast cancers, are the commonest causes (Lee et al., 2003). Malignant pleural mesothelioma (MPM) a fatal asbestos-associated malignancy originating from the pleura, is a solid, locally aggressive tumor that encases and invades the lung parenchyma in late stages of the disease causing clinically significant morbidities such as dyspnea and chest pain (Ismail Khan et al., 2006). Without treatment, MPM is associated with poor median survival, ranging from 4 to 12 months (Neragi-Miandoab 2006). The exact prevalence of malignant mesothelioma; is unknown but it is estimated that mesotheliomas represent less than 1% of all cancers. Its incidence is increasing, with an expected peak in the next years. Pleural malignant mesothelioma is the most common form of mesothelioma (Moore et al., 2008). Many risk factors have been identified as contributors to MPM pathogenesis (genetic, asbestos, and SV40 infection). Asbestos contribution to the pathogenesis of MPM is multifaceted with effects ranging from direct to indirect, genetic to molecular. Asbestos induces mutations in mesothelial cells. The more direct mechanism of injury includes deposition of asbestos fibers in the pleura and has a high like hood of causing cancer (Weiner and Neragi 2008). Asbestos fibers may also damage the mitotic spindle of cells and thereby disrupt mitosis, resulting in aneuploidy and DNA damage (Ault et al., 1995 and Kamp et al., 1995, Weiner and Neragi 2008).In a less direct fashion, asbestos can lead to the formation of reactive oxygen species (ROS). The production of ROS can be 338

14 Ahmed M. Abd El-Aziz et al catalysed by iron content of fibers or can occur through additional reactions on the fibre surface (Weiner and Neragi 2008).Macrophages that have phagocytosed asbestos fibers release ROS and lymphokines, which can damage DNA and possibly suppress the immune system (Choe et al., 1998, Rosenthal et al., 1999 and Weiner and Neragi 2008). Asbestos and/or the resulting ROS may also activate cell-signaling pathways (Zanella et al., 1996, Weiner and Neragi 2008). Asbestos has been recognized in Egypt since a long time as ancient Egyptians were using it in mummification. Mesothelioma in Egypt is mainly attributed to environmental origin with a high incidence of women and young adults affected. The incidence of mesothelioma is rising in Egypt. Epidemiological data for 635 malignant mesothelioma (MM) patients over 4 years in the third Millennium were collected from the National Cancer Institute (NCI), Cairo University and Abbassia Chest hospital. This number is more than four times the number diagnosed in the previous 11 years at NCI. A clinicopathological study was done for 100 malignant pleural mesothelioma (MPM) patients and showed that asbestos exposure and SV40 positivity were evident in 67% and 60% of cases, respectively. The median survival was 14.3 months and the 1 and 2 year survival rates were 60% and 27%, respectively. Asbestos in Cairo is a silent killer and measures toward eliminating it entirely or at least strictly controlling human contact with this dangerous carcinogen have to be taken in order to combat the coming epidemic of mesothelioma in Egypt (Gaafar and Eldin 2005). It is currently stated that the time periods elapsing between first exposure to asbestos and diagnosis of mesothelioma are years. (Bianchi et al., 2002). Some data indicate that an inverse relationship exist between intensity of exposure to asbestos and length of latency period (Bianchi and Bianchi 2007). Despite some inconsistencies, the data about the relationship between the duration of employment and risk of mesothelioma indicate that duration of exposure is important. (Numinen et al., 2003). 339

15 It may be assumed that generally the carcinogenic effects of asbestos are neutralized by the defence mechanisms. In a majority of cases, mesothelioma develops only when a relatively high cumulative dose is reached, and/ or surveillance system is impaired (Bianchi and Bianchi 2007). In many industrial countries a great concern exists about the future trend of mesothelioma epidemic. Various studies have been devoted to the prediction in this field (Hodgson et al., 2005). Predictions are difficult, since during the last decades phenomena of opposite sign have occurred. World asbestos production has progressively increased since 1960s and 1970s. However, limitations in the use of asbestos began in some European countries in 1960s and 1970s. Therefore it is legitimate to expect the effects of such reductions (Bianchi and Bianchi 2007). Malignancy is diagnosed in 50 % of patients referred for evaluation of pleural effusion (Abouzgeib et al., 2009). The diagnosis of malignancy is based on the finding of malignant cells in pleural fluid by cytologic examination. (Sallach et al., 2002). Various studies of the accuracy of cytologic diagnosis of malignant pleural effusions have been reported to range from 40 to 87% (Abouzgheib et al., 2009). Not all pleural effusions in patients with malignancy are caused by tumor implants in the pleura or pleural infiltration by malignancy (Sahn 1985, Sallach et al., 2002). Detailed study of cytomorphologic features of various metastatic malignant cells in pleural effusions provides definitive clues regarding the primary site. It is possible to diagnose the type and source of malignant tumor cells in serous effusions with overall accuracy of 50% (Kushwaha et al., 2008). Non- Hodgkin lymphoma with pleural effusions was positive on cytologic analysis in 75% of patients in one series, in contrast with 25% for Hodgkin lymphoma with pleural effusions in another (Sallach et al., 2002).Adenocarcinoma involving the pleura is 340

16 Ahmed M. Abd El-Aziz et al more frequently positive on cytology than sarcoma (Sallach et al., 2002).Carcinoma that arises in the breast and metastasizes to the pleura is more likely to be associated with a positive pleural fluid cytology specimen than is carcinoma of the lung (Prakash and Reiman 1985, Shallach et al., 2002). Morphological differentiation of reactive mesothelial cells from adenocarcinoma cells in the pleural effusions can be a diagnostic challenge. Adenocarcinoma metastatic to the pleural membrane is often associated with prominent mesothelial hyperplasia and may result 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 cytological examination of pleural fluid are a serous problem. Such errors in diagnosis usually are caused by misinterpretation of adenocarcinoma cells as reactive mesothelial cells (Afify et al., 2005). It has long been a major diagnostic challenge to distinguish among reactive mesothelial cells (RMs), malignant mesotheliomas (MM), and adenocarcinoma (AC) in both cytologic and surgical pathologic specimens (Hiromi 1999). The rate of false-positive diagnosis also is significant and often caused by overinterpretation of reactive mesothelial cells as malignant cells (Politi et al., 2005). This study included 67 cases presented with malignant pleural effusions. The cases were classified as mesothelioma 11 (16.4%) cases and non-mesothelioma (metastatic) 56 (83.6%). From these results it was concluded that metastatic cases represent the majority of malignant pleural effusion cases. In the current study, the 56 metastatic cases were further categorized according to their origin as following: 12 cases (21.4%) breast carcinoma, 10 cases (17.8%) lymphoma, 3 cases (5.4%) adenocarcinoma, 2 cases (3.6%) broncho-alveolar carcinoma, 2 cases (3.6%) small cell carcinoma, 1 case (1.8%) bronchogenic carcinoma, 1 case (1.8%) papillary carcinoma and 1 case (1.8%) signet ring carcinoma and finally the origin of metastasis for 24 cases were not identified. In the study by Daste et al malignant (pleural and peritoneal) metastatic effusions cases, the primary site of adenocarcinoma were lung (12 cases), stomach 341

17 (6 cases), breast (3 cases), ovary (4 cases), pancreas (3 cases), uterus (3 cases) and intestine (1 case).the primary site was unknown in eight cases. In the current study, the common age group for malignant pleural effusion patients was (52 61 years) presenting (16 patients, 24.6%). Female predominance was observed among the studied cases of malignant pleural effusion, they represented 61.2 % of cases and the ratio of females to males was 1.6:1. Female predominance may be explained by large number of cases with metastatic breast carcinoma (42.8 %) included in the study. This finding is similar to what Khanij et al have recorded, where the study carried out on 25 cases of presenting with serous effusions showed also female predominance representing 19 (76%) out of 25 cases. Kushwaha et al also stated that malignant pleural effusion was found to affect females more than males (2.1:1). The incidence of malignant mesothelioma among Females was found to be more than in men presenting 6 out of 11, this may be attributed to para-occupational exposure, women having laundered their husbands clothes (Howel et al., 1999). A bloody pleural effusion is characteristic of many pleural effusions caused by malignancy (Cagle and Churg 2005). A single variable which strongly predicts malignancy is bloody fluid (Kushwaha et al., 2008). In the current study, the gross appearance of fluid was hemorrhagic in 32 cases (47.8 %) while the remaining 35 cases (52.2%) showed non-hemorrhagic pleural effusion fluid. This finding agrees with what observed by Kushwaha et al where 68.9% of hemorrhagic effusions were positive for malignancy and with what observed by Coceincao et al. (2001) where 73.4 % of malignant effusion cases were hemorrhagic. This means that all hemorrhagic fluids need not to be due to malignancy and non-hemorrhagic fluids can have malignant cells (Kushwaha et al., 2008). 342

18 Ahmed M. Abd El-Aziz et al In the current work, concerning the side of pleural effusion, there were 51 cases with the side of the pleural effusion known. Regarding to the available 51 cases, there were 30 cases (58.8 %) with right pleural effusion, 19 cases (28.4 %) with left sided pleural effusion and 2 cases with bilateral pleural effusion. Less well studied is the amount of pleural fluid that should be removed to diagnose pleural malignancy. Suggestions exist, but an actual answer to this question has not yet been determined. It is generally thought that larger volumes collected by thoracentesis will result in more accurate results. However, the more appealing alternative would be that the volume of pleural fluid aspirated is not a predictor of finding malignant cells when present (Sallach et al., 2002). In the current study, concerning the volume of pleural fluid needed for accurate diagnosis of cases of malignant pleural effusion, the volume of collected samples was found to be concentrated at the volume between 2 to 200 ml. Sahn stated in his 1985 article that approximately 75% of patients known to have carcinomatous pleurisy would have pleural effusions in the range of 500 to 2,000 ml of fluid, while 10% would present with effusions < 500 ml and 10% with massive effusions. Collection volumes for optimal diagnostic accuracy of several hundred millilitres (Sahn., 1993), 100 ml (Prakash and Reiman 1985), no less than 250 ml (Leff et al., 1987) and only 50 to 100 ml have all been suggested by Sallach et al but at last he suggested that submission of 10 ml of pleural appears adequate for cytological processing. It appears that, if malignant cells are present, they are equally likely to be identified on cytologic processing of small volumes of pleural fluid as with larger volumes. This means that the sensitivity of pleural fluid analysis for the diagnosis of pleural-based malignancy is not dependent on the volume of pleural fluid extracted during diagnostic thoracentesis. There may be other reasons to remove large volumes of pleural fluid when effusions are massive, such as an attempt to relieve dyspnea or allow better radiographic display of the underlying lung after large volume thoracentesis. Many variables have been associated with the ability to find malignant cells in pleural fluid among patients 343

19 who have a malignancy (Sahn 1985, Sallach et al., 2002). There was a 100% concordance between a 50-ml sample is cost-effective without any sacrifice of diagnostic yield. If more fluid is to be drained, the decision should be based on factors other than cytology (Abouzgheib et al., 2009) We concluded that Mesothelioma represents only 11 cases (16%) of malignant pleural effusions cases and non-mesothelioma (metastatic) were 84%. Females suffer more from malignant pleural effusion and present 61.2% of cases. The incidence of malignant mesothelioma among females was found to be more than in men presenting 6 out of 11 cases. Hemorrhagic effusions represent 52.2% of cases. Although highly suspicious for malignancy but not always indicative for malignancy as it may be due injury during sample collection. Sample volume was mostly < 200 ml and this represents 67.2 % of cases and this coincide with the literature saying that large volume of sample is not necessary and <50 ml of fluid is quite enough for diagnosis. The cytological diagnosis of pleural effusions can be difficult, and usually detects only 50-60% of malignant pleural effusions, especially in specimens containing abundant reactive mesothelial cells. The origin of 24 cases of non-mesothelioma (metastatic) could not be identified so the combination of cytology and pleural biopsy from any suspicious lesion will aid to decrease the diagnostic dilemmas and also allows the application of immunohistochemical techniques with much ease. Having full patient data e.g. history of malignancy, x-ray and CT scan reports will aid to have full picture and guide diagnosis. 344

20 Ahmed M. Abd El-Aziz et al REFRENCES 1. Abouzgeib, Lovett JK, McGavin CR. The rise and fall in incidence of malignant mesothelioma from a British naval dockyard, Occup Med 2009; 53: Afify AM, Stern R, Michael CW. Differentiation of mesothelioma from adenocarcinoma in serous effusions: the role of hyaluronic acid and CD44 localization. Diagn Cytopathol 2005; 32: Antony VB, Loddenkemper R, Astoul P, Boutin C, Goldstraw P, Hott J, Rodriguez Panadero F, Sahn SA. Management of malignant pleural effusions. Eur Respir J 2001; 18: Ault JG, Cole RW, Jensen CG, Jensen LC, Bachert LA, Rieder CL. Behavior of crocidolite asbestos during mitosis in living vertebrate lung epithelial cells. Cancer research 1995; 55(4): Awasthi A, Gupta N, Srinivasan R, Nijhawan R, Rajwanshi A. Cytopathological spectrum of unusual malignant pleural effusions at a tertiary care centre in north India. Cytopathol 2007; 18: Bianchi Claudio and Bianchi Tommaso. Malignant Mesothelioma: Global Incidence and Relationship with Asbestos. Industrial Health 2007; 45: Cagle PT, Churg A. Differential diagnosis of benign and malignant mesothelial proliferations on pleural biopsies. Arch Pathol Lab Med 2005; 129: Chesnutt C, Prendergast P: Finger clubbing in malignant mesothelioma and benign asbestos pleural disease. Respir Med 2004; 92: Choe N, Tanaka S, Kagan E: Asbestos fibers and interleukin-1 up regulate the formation of reactive nitrogen species in rat pleural mesothelial cells. Am J Respir Cell Mol Biol 1998; 19(2): Coceincao Q, Manoel B and Carlos E. Charactarizing subpopulations of neoplastic cells in effusion. Acta Cytol 2001; 45:

21 11. Daste G, Serve G, Maudy T and Vicent C. Immuno-phenotyping of mesothelial cells and carcinoma cells with monoclonal antibodies to cytokeratine, vimentin, CEA, EMA improve the cytodiagnosis of serous effusion. Cytopathology 1991; 2: Davies RJ. Pleural effusion: a structured approach to care. Oxford Pleural Diseases Unit, Oxford Centre for Respiratory Medicine, Churchill Hospital Oxford, UK., British Medical Bulletin 2008; 72: DeCamp MM, Metzer SJ, Swanson SJ, Sugarbaker DJ. Malignant effusion disease of the pleura and pericardium. Chest 1997; 112:291S-295S. 14. Gaafar RM, Eldin N H. Epidemic of mesothelioma in Egypt. Lung Cancer 2005; 49(suppl 1):S17-S Heffner JE, Klein JS. Recent Advances in the Diagnosis of and Management of Malignant Pleural Effusions. Mayo Clin Pro.2008; (2): Heffner JE, Nietert PJ, Barbieri C. Pleural fluid ph as a predictor of survival for patients with malignant pleural effusions. Chest 2000; 117: Hiromi JG, Cole RW, Jensen CG, Jensen LC, Bachert LA, Rieder CL. Behavior of crocidolite asbestos during mitosis in living vertebrate lung epithelial cells. Cancer research 1999; 55(4): Hodgson JT, McElvenny DM, Dartnton AJ, Price MJ, Peto J. The expected burden of mesothelioma mortality in Great Britain from 2002 to Br J Cancer 2005; 92: Ismail-Khan R, Robinson LA, Williams CC Jr, Garrett CR, Bepler G and Simon GR. Malignant pleural mesothelioma: a comprehensive review. Cancer Control 2006; 13: Ismail-Khan R, Robinson LA, Williams CC Jr, Garrett CR, Bepler G and Simon GR. Malignant pleural mesothelioma: a comprehensive review. Cancer Control 2006; 13:

22 Ahmed M. Abd El-Aziz et al 21. Kamp DW, Israbian VA, Preusen SE, Zhang CX, Weitzman SA: Asbestos causes DNA strand breaks in cultured pulmonary epithelial cells: role of iron-catalyzed free radicals. Am J physiol 1995; 268(3 Pt 1): Khanij R, Savita M and Hemlata G. Cytologic study of serous effusions with the aid of tumor markers. J Indian Med Associated 1999; 97: Kushwaha R, Shashikala P, Hiremath S, Basavaraj HG. Cells in pleural fluid and their value in differential diagnosis. J Cytol 2008; 25: Kushwaha R, Shashikala P, Hiremath S, Basavaraj HG. Cells in pleural fluid and their value in differential diagnosis. J Cytol 2008; 25: Lee YC, Conner BD, Branca P, Rogers JT, Rodriguez RM, Light RW. Variations in pleural fluid WBC count and differential counts with different sample containers and different methods. Chest 2003; 123: Leff A, Hopewell PC, Costello J. Pleural effusion from malignancy. Ann Intern Med 1987; 88: Light RW. Pleural effusions: The separation of Transudates and Exudates. Egypt J Bronch. December 2007; 1 no.1: Marios KN. The serous membranes in the cat. Electron microscopic observations. Anat Anz 2008; 178: Miserocchi G. Physiology and Pathophysiology of pleural fluid turnover. Eur Respir J 1997; 10: Moffett PU, Moffett BK, and Laber DA. Diagnosing and Managing Suspected Malignant Pleural Effusions, J Support Oncol 2009; 7: Moore AJ, Parker RJ and Wiggins J: Malignant mesothelioma. Orphanet J Rare Diseases 2008, 3: Neragi-Miandoab S: Multimodality approach in management of malignant pleural mesothelioma. Eur J Cardiothorac Surg 2006; 29(1): Numinen, Shih CS, Wang YT, Tseng GC, Hsu WH. Angiosarcoma with pulmonary metastasis presenting with spontaneous bilateral pneumothorax in an elderly man. J. Formos.Med. Assoc. 2003; 105:

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