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. 2003 Oct;79(936):569–574. doi: 10.1136/pmj.79.936.569

Serous effusions: diagnosis of malignancy beyond cytomorphology. An analytic review

S Mohanty 1, P Dey 1
PMCID: PMC1742845  PMID: 14612599

Abstract

In this brief review, the role of various ancillary techniques to detect malignancy in effusion fluid are evaluated and discussed. The data were collected from a large number of research articles published in various medical journals. The role of these techniques to increase the diagnostic accuracy in serous effusions is emphasised.

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Selected References

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  1. Anderson S., Shera K., Ihle J., Billman L., Goff B., Greer B., Tamimi H., McDougall J., Klingelhutz A. Telomerase activation in cervical cancer. Am J Pathol. 1997 Jul;151(1):25–31. [PMC free article] [PubMed] [Google Scholar]
  2. Ascoli V., Scalzo C. C., Taccogna S., Nardi F. The diagnostic value of thrombomodulin immunolocalization in serous effusions. Arch Pathol Lab Med. 1995 Dec;119(12):1136–1140. [PubMed] [Google Scholar]
  3. Bedrossian C. W., Bonsib S., Moran C. Differential diagnosis between mesothelioma and adenocarcinoma: a multimodal approach based on ultrastructure and immunocytochemistry. Semin Diagn Pathol. 1992 May;9(2):124–140. [PubMed] [Google Scholar]
  4. Berner H. S., Davidson B., Berner A., Risberg B., Nesland J. M. Differential expression of CD44s and CD44v3-10 in adenocarcinoma cells and reactive mesothelial cells in effusions. Virchows Arch. 2000 Apr;436(4):330–335. doi: 10.1007/s004280050455. [DOI] [PubMed] [Google Scholar]
  5. Blobel G. A., Moll R., Franke W. W., Kayser K. W., Gould V. E. The intermediate filament cytoskeleton of malignant mesotheliomas and its diagnostic significance. Am J Pathol. 1985 Nov;121(2):235–247. [PMC free article] [PubMed] [Google Scholar]
  6. Bodner S. M., Minna J. D., Jensen S. M., D'Amico D., Carbone D., Mitsudomi T., Fedorko J., Buchhagen D. L., Nau M. M., Gazdar A. F. Expression of mutant p53 proteins in lung cancer correlates with the class of p53 gene mutation. Oncogene. 1992 Apr;7(4):743–749. [PubMed] [Google Scholar]
  7. Callet N., Cohen-Solal Le Nir C. C., Berthelot E., Pichon M. F. Cancer of the uterine cervix: sensitivity and specificity of serum Cyfra 21.1 determinations. Eur J Gynaecol Oncol. 1998;19(1):50–56. [PubMed] [Google Scholar]
  8. Chang K., Pai L. H., Pass H., Pogrebniak H. W., Tsao M. S., Pastan I., Willingham M. C. Monoclonal antibody K1 reacts with epithelial mesothelioma but not with lung adenocarcinoma. Am J Surg Pathol. 1992 Mar;16(3):259–268. doi: 10.1097/00000478-199203000-00006. [DOI] [PubMed] [Google Scholar]
  9. Chang K., Pastan I., Willingham M. C. Frequent expression of the tumor antigen CAK1 in squamous-cell carcinomas. Int J Cancer. 1992 Jun 19;51(4):548–554. doi: 10.1002/ijc.2910510408. [DOI] [PubMed] [Google Scholar]
  10. Cibas E. S. Applications of flow cytometric DNA analysis to diagnostic cytology. Diagn Cytopathol. 1995 Aug;13(2):166–171. doi: 10.1002/dc.2840130219. [DOI] [PubMed] [Google Scholar]
  11. Cibas E. S., Corson J. M., Pinkus G. S. The distinction of adenocarcinoma from malignant mesothelioma in cell blocks of effusions: the role of routine mucin histochemistry and immunohistochemical assessment of carcinoembryonic antigen, keratin proteins, epithelial membrane antigen, and milk fat globule-derived antigen. Hum Pathol. 1987 Jan;18(1):67–74. doi: 10.1016/s0046-8177(87)80196-x. [DOI] [PubMed] [Google Scholar]
  12. Clark S. P., Chou S. T., Martin T. J., Danks J. A. Parathyroid hormone-related protein antigen localization distinguishes between mesothelioma and adenocarcinoma of the lung. J Pathol. 1995 Jun;176(2):161–165. doi: 10.1002/path.1711760209. [DOI] [PubMed] [Google Scholar]
  13. Cote R. J., Jhanwar S. C., Novick S., Pellicer A. Genetic alterations of the p53 gene are a feature of malignant mesotheliomas. Cancer Res. 1991 Oct 1;51(19):5410–5416. [PubMed] [Google Scholar]
  14. Culty M., Miyake K., Kincade P. W., Sikorski E., Butcher E. C., Underhill C., Silorski E. The hyaluronate receptor is a member of the CD44 (H-CAM) family of cell surface glycoproteins. J Cell Biol. 1990 Dec;111(6 Pt 1):2765–2774. doi: 10.1083/jcb.111.6.2765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cunningham V. J., Markham N., Shroyer A. L., Shroyer K. R. Detection of telomerase expression in fine-needle aspirations and fluids. Diagn Cytopathol. 1998 Jun;18(6):431–436. doi: 10.1002/(sici)1097-0339(199806)18:6<431::aid-dc9>3.0.co;2-b. [DOI] [PubMed] [Google Scholar]
  16. Dalquen P., Baschiera B., Chaffard R., Dieterich H., Feichter G. E., Krmer K., Torhorst J. MIB-1 (Ki-67) immunostaining of breast cancer cells in cytologic smears. Acta Cytol. 1997 Mar-Apr;41(2):229–237. doi: 10.1159/000332448. [DOI] [PubMed] [Google Scholar]
  17. Davidson B., Goldberg I., Berner A., Nesland J. M., Givant-Horwitz V., Bryne M., Risberg B., Kristensen G. B., Tropé C. G., Kopolovic J. Expression of membrane-type 1, 2, and 3 matrix metalloproteinases messenger RNA in ovarian carcinoma cells in serous effusions. Am J Clin Pathol. 2001 Apr;115(4):517–524. doi: 10.1309/B1YX-L8DB-TGY1-7905. [DOI] [PubMed] [Google Scholar]
  18. Dejmek A., Yahata N., Ohyashiki K., Ebihara Y., Kakihana M., Hirano T., Kawate N., Kato H. In situ telomerase activity in pleural effusions: a promising marker for malignancy. Diagn Cytopathol. 2001 Jan;24(1):11–15. doi: 10.1002/1097-0339(200101)24:1<11::aid-dc1001>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
  19. Delahaye M., Hoogsteden H. C., Van der Kwast T. H. Immunocytochemistry of malignant mesothelioma: OV632 as a marker of malignant mesothelioma. J Pathol. 1991 Oct;165(2):137–143. doi: 10.1002/path.1711650209. [DOI] [PubMed] [Google Scholar]
  20. Doglioni C., Dei Tos A. P., Laurino L., Iuzzolino P., Chiarelli C., Celio M. R., Viale G. Calretinin: a novel immunocytochemical marker for mesothelioma. Am J Surg Pathol. 1996 Sep;20(9):1037–1046. doi: 10.1097/00000478-199609000-00001. [DOI] [PubMed] [Google Scholar]
  21. Donna A., Betta P. G., Bellingeri D., Tallarida F., Pavesi M., Pastormerlo M. Cytologic diagnosis of malignant mesothelioma in serous effusions using an antimesothelial-cell antibody. Diagn Cytopathol. 1992;8(4):361–365. doi: 10.1002/dc.2840080411. [DOI] [PubMed] [Google Scholar]
  22. Doweck I., Barak M., Greenberg E., Uri N., Kellner J., Lurie M., Gruener N. Cyfra 21-1. A new potential tumor marker for squamous cell carcinoma of head and neck. Arch Otolaryngol Head Neck Surg. 1995 Feb;121(2):177–181. doi: 10.1001/archotol.1995.01890020039009. [DOI] [PubMed] [Google Scholar]
  23. Eisenstein B. I. The polymerase chain reaction. A new method of using molecular genetics for medical diagnosis. N Engl J Med. 1990 Jan 18;322(3):178–183. doi: 10.1056/NEJM199001183220307. [DOI] [PubMed] [Google Scholar]
  24. Eskelinen M. J., Lipponen P. K., Collan Y., Syrjänen K. J. The role of nucleolar organiser regions as prognostic factors in breast cancer. Eur J Cancer. 1991;27(8):989–992. doi: 10.1016/0277-5379(91)90265-f. [DOI] [PubMed] [Google Scholar]
  25. Esteban J. M., Sheibani K. DNA ploidy analysis of pleural mesotheliomas: its usefulness for their distinction from lung adenocarcinomas. Mod Pathol. 1992 Nov;5(6):626–630. [PubMed] [Google Scholar]
  26. Esteban J. M., Yokota S., Husain S., Battifora H. Immunocytochemical profile of benign and carcinomatous effusions. A practical approach to difficult diagnosis. Am J Clin Pathol. 1990 Dec;94(6):698–705. doi: 10.1093/ajcp/94.6.698. [DOI] [PubMed] [Google Scholar]
  27. Evans D. A., Thornthwaite J. T., Ng A. B., Sugarbaker E. V. DNA flow cytometry of pleural effusions. Comparison with pathology for the diagnosis of malignancy. Anal Quant Cytol. 1983 Mar;5(1):19–27. [PubMed] [Google Scholar]
  28. Fenton K. N., Richardson J. D. Diagnosis and management of malignant pleural effusions. Am J Surg. 1995 Jul;170(1):69–74. doi: 10.1016/s0002-9610(99)80257-8. [DOI] [PubMed] [Google Scholar]
  29. Ferroni P., Szpak C., Greiner J. W., Simpson J. F., Guadagni F., Johnston W. W., Colcher D. CA 72-4 radioimmunoassay in the diagnosis of malignant effusions. Comparison of various tumor markers. Int J Cancer. 1990 Sep 15;46(3):445–451. doi: 10.1002/ijc.2910460320. [DOI] [PubMed] [Google Scholar]
  30. Fetsch P. A., Abati A., Hijazi Y. M. Utility of the antibodies CA 19-9, HBME-1, and thrombomodulin in the diagnosis of malignant mesothelioma and adenocarcinoma in cytology. Cancer. 1998 Apr 25;84(2):101–108. doi: 10.1002/(sici)1097-0142(19980425)84:2<101::aid-cncr6>3.0.co;2-s. [DOI] [PubMed] [Google Scholar]
  31. Fiegl M., Kaufmann H., Zojer N., Schuster R., Wiener H., Müllauer L., Roka S., Huber H., Drach J. Malignant cell detection by fluorescence in situ hybridization (FISH) in effusions from patients with carcinoma. Hum Pathol. 2000 Apr;31(4):448–455. doi: 10.1053/hp.2000.6550. [DOI] [PubMed] [Google Scholar]
  32. Green L. K., Griffin J. Increased natural killer cells in fluids. A new, sensitive means of detecting carcinoma. Acta Cytol. 1996 Nov-Dec;40(6):1240–1245. doi: 10.1159/000333987. [DOI] [PubMed] [Google Scholar]
  33. Grem J. The prognostic importance of tumor markers in adenocarcinomas of the gastrointestinal tract. Curr Opin Oncol. 1997 Jul;9(4):380–387. doi: 10.1097/00001622-199709040-00012. [DOI] [PubMed] [Google Scholar]
  34. Guadagni F., Roselli M., Cosimelli M., Ferroni P., Spila A., Cavaliere F., Casaldi V., Wappner G., Abbolito M. R., Greiner J. W. CA 72-4 serum marker--a new tool in the management of carcinoma patients. Cancer Invest. 1995;13(2):227–238. doi: 10.3109/07357909509011692. [DOI] [PubMed] [Google Scholar]
  35. Hammar S. P., Bockus D. E., Remington F. L., Rohrbach K. A. Mucin-positive epithelial mesotheliomas: a histochemical, immunohistochemical, and ultrastructural comparison with mucin-producing pulmonary adenocarcinomas. Ultrastruct Pathol. 1996 Jul-Aug;20(4):293–325. doi: 10.3109/01913129609016331. [DOI] [PubMed] [Google Scholar]
  36. Hiyama E., Gollahon L., Kataoka T., Kuroi K., Yokoyama T., Gazdar A. F., Hiyama K., Piatyszek M. A., Shay J. W. Telomerase activity in human breast tumors. J Natl Cancer Inst. 1996 Jan 17;88(2):116–122. doi: 10.1093/jnci/88.2.116. [DOI] [PubMed] [Google Scholar]
  37. Hiyama E., Yokoyama T., Tatsumoto N., Hiyama K., Imamura Y., Murakami Y., Kodama T., Piatyszek M. A., Shay J. W., Matsuura Y. Telomerase activity in gastric cancer. Cancer Res. 1995 Aug 1;55(15):3258–3262. [PubMed] [Google Scholar]
  38. Hiyama K., Hiyama E., Ishioka S., Yamakido M., Inai K., Gazdar A. F., Piatyszek M. A., Shay J. W. Telomerase activity in small-cell and non-small-cell lung cancers. J Natl Cancer Inst. 1995 Jun 21;87(12):895–902. doi: 10.1093/jnci/87.12.895. [DOI] [PubMed] [Google Scholar]
  39. Jia D., Zhang Z., Liu S., Cheng S. [Study on interphase cytogenetic abnormalities in malignant cells in pleural fluids from lung cancer cases]. Zhonghua Yi Xue Yi Chuan Xue Za Zhi. 2000 Aug;17(4):244–247. [PubMed] [Google Scholar]
  40. Joensuu H., Klemi P. J., Eerola E. Diagnostic value of flow cytometric DNA determination combined with fine needle aspiration biopsy in thyroid tumors. Anal Quant Cytol Histol. 1987 Aug;9(4):328–334. [PubMed] [Google Scholar]
  41. Joseph M. G., Banerjee D., Harris P., Gibson S., McFadden R. G. Multiparameter flow cytometric DNA analysis of effusions: a prospective study of 36 cases compared with routine cytology and immunohistochemistry. Mod Pathol. 1995 Aug;8(6):686–693. [PubMed] [Google Scholar]
  42. Kafiri G., Thomas D. M., Shepherd N. A., Krausz T., Lane D. P., Hall P. A. p53 expression is common in malignant mesothelioma. Histopathology. 1992 Oct;21(4):331–334. doi: 10.1111/j.1365-2559.1992.tb00403.x. [DOI] [PubMed] [Google Scholar]
  43. Kayser K., Märkle C., Kugler C., Andre S., Schüring M. P., Zeng F. Y., Gabius H. J. Integrated nuclear fluorescence and expression of hormone-binding sites in malignant pleural effusions. Anal Quant Cytol Histol. 2000 Oct;22(5):364–372. [PubMed] [Google Scholar]
  44. Kennedy A. D., King G., Kerr K. M. HBME-1 and antithrombomodulin in the differential diagnosis of malignant mesothelioma of pleura. J Clin Pathol. 1997 Oct;50(10):859–862. doi: 10.1136/jcp.50.10.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kim N. W., Piatyszek M. A., Prowse K. R., Harley C. B., West M. D., Ho P. L., Coviello G. M., Wright W. E., Weinrich S. L., Shay J. W. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994 Dec 23;266(5193):2011–2015. doi: 10.1126/science.7605428. [DOI] [PubMed] [Google Scholar]
  46. Ko E. C., Jhala N. C., Shultz J. J., Chhieng D. C. Use of a panel of markers in the differential diagnosis of adenocarcinoma and reactive mesothelial cells in fluid cytology. Am J Clin Pathol. 2001 Nov;116(5):709–715. doi: 10.1309/PJ7H-A52V-M3XB-V94Y. [DOI] [PubMed] [Google Scholar]
  47. Kondi-Paphitis A., Addis B. J. Secretory component in pulmonary adenocarcinoma and mesothelioma. Histopathology. 1986 Dec;10(12):1279–1287. doi: 10.1111/j.1365-2559.1986.tb02571.x. [DOI] [PubMed] [Google Scholar]
  48. Kumar N. U., Dey P., Mondal A. K., Singh S. K., Vohra H. DNA flow cytometry and bladder irrigation cytology in detection of bladder carcinoma. Diagn Cytopathol. 2001 Mar;24(3):153–156. doi: 10.1002/1097-0339(200103)24:3<153::aid-dc1032>3.0.co;2-p. [DOI] [PubMed] [Google Scholar]
  49. Laurini J. A., Garcia A., Elsner B., Bellotti M., Rescia C. Relation between natural killer cells and neoplastic cells in serous fluids. Diagn Cytopathol. 2000 Jun;22(6):347–350. doi: 10.1002/(sici)1097-0339(200006)22:6<347::aid-dc4>3.0.co;2-t. [DOI] [PubMed] [Google Scholar]
  50. Leers M. P., Aarts M. M., Theunissen P. H. E-cadherin and calretinin: a useful combination of immunochemical markers for differentiation between mesothelioma and metastatic adenocarcinoma. Histopathology. 1998 Mar;32(3):209–216. doi: 10.1046/j.1365-2559.1998.00349.x. [DOI] [PubMed] [Google Scholar]
  51. Levine A. J., Momand J., Finlay C. A. The p53 tumour suppressor gene. Nature. 1991 Jun 6;351(6326):453–456. doi: 10.1038/351453a0. [DOI] [PubMed] [Google Scholar]
  52. Magyarosy E., Martin W. J., Chu E. W., Martin S. E. Differential diagnostic significance of the paucity of HLA-I antigens on metastatic breast carcinoma cells in effusions. Pathol Oncol Res. 1999;5(1):32–35. doi: 10.1053/paor.1999.0032. [DOI] [PubMed] [Google Scholar]
  53. Mairinger T., Gschwendtner A., Toetsch M., Prior C., Fend F. Automated cell differentiation of bronchoalveolar lavage samples with two-step image analysis. Anal Quant Cytol Histol. 1996 Dec;18(6):453–460. [PubMed] [Google Scholar]
  54. Mason M. R., Bedrossian C. W., Fahey C. A. Value of immunocytochemistry in the study of malignant effusions. Diagn Cytopathol. 1987 Sep;3(3):215–221. doi: 10.1002/dc.2840030308. [DOI] [PubMed] [Google Scholar]
  55. Mayall F., Heryet A., Manga D., Kriegeskotten A. p53 immunostaining is a highly specific and moderately sensitive marker of malignancy in serous fluid cytology. Cytopathology. 1997 Feb;8(1):9–12. doi: 10.1046/j.1365-2303.1997.42575425.x. [DOI] [PubMed] [Google Scholar]
  56. Miller C. J., McGhee J. R., Gardner M. B. Mucosal immunity, HIV transmission, and AIDS. Lab Invest. 1993 Feb;68(2):129–145. [PubMed] [Google Scholar]
  57. Motherby H., Nadjari B., Friegel P., Kohaus J., Ramp U., Böcking A. Diagnostic accuracy of effusion cytology. Diagn Cytopathol. 1999 Jun;20(6):350–357. doi: 10.1002/(sici)1097-0339(199906)20:6<350::aid-dc5>3.0.co;2-7. [DOI] [PubMed] [Google Scholar]
  58. Mourad W. A., Erkman-Balis B., Livingston S., Shoukri M., Cox C. E., Nicosia S. V., Rowlands D. T., Jr Argyrophilic nucleolar organizer regions in breast carcinoma. Correlation with DNA flow cytometry, histopathology, and lymph node status. Cancer. 1992 Apr 1;69(7):1739–1744. doi: 10.1002/1097-0142(19920401)69:7<1739::aid-cncr2820690715>3.0.co;2-9. [DOI] [PubMed] [Google Scholar]
  59. Mu X. C., Brien T. P., Ross J. S., Lowry C. V., McKenna B. J. Telomerase activity in benign and malignant cytologic fluids. Cancer. 1999 Apr 25;87(2):93–99. [PubMed] [Google Scholar]
  60. Mullick S. S., Green L. K., Ramzy I., Brown R. W., Smith D., Gondo M. M., Cagle P. T. p53 gene product in pleural effusions. Practical use in distinguishing benign from malignant cells. Acta Cytol. 1996 Sep-Oct;40(5):855–860. doi: 10.1159/000333991. [DOI] [PubMed] [Google Scholar]
  61. Nance K. V., Silverman J. F. Immunocytochemical panel for the identification of malignant cells in serous effusions. Am J Clin Pathol. 1991 Jun;95(6):867–874. doi: 10.1093/ajcp/95.6.867. [DOI] [PubMed] [Google Scholar]
  62. O'Leary T. J. Flow cytometry in diagnostic cytology. Diagn Cytopathol. 1998 Jan;18(1):41–46. doi: 10.1002/(sici)1097-0339(199801)18:1<41::aid-dc7>3.0.co;2-x. [DOI] [PubMed] [Google Scholar]
  63. Ordóez N. G. Value of cytokeratin 5/6 immunostaining in distinguishing epithelial mesothelioma of the pleura from lung adenocarcinoma. Am J Surg Pathol. 1998 Oct;22(10):1215–1221. doi: 10.1097/00000478-199810000-00006. [DOI] [PubMed] [Google Scholar]
  64. Picker L. J., Nakache M., Butcher E. C. Monoclonal antibodies to human lymphocyte homing receptors define a novel class of adhesion molecules on diverse cell types. J Cell Biol. 1989 Aug;109(2):927–937. doi: 10.1083/jcb.109.2.927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Plebani M., Basso D., Navaglia F., De Paoli M., Tommasini A., Cipriani A. Clinical evaluation of seven tumour markers in lung cancer diagnosis: can any combination improve the results? Br J Cancer. 1995 Jul;72(1):170–173. doi: 10.1038/bjc.1995.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Ploton D., Menager M., Jeannesson P., Himber G., Pigeon F., Adnet J. J. Improvement in the staining and in the visualization of the argyrophilic proteins of the nucleolar organizer region at the optical level. Histochem J. 1986 Jan;18(1):5–14. doi: 10.1007/BF01676192. [DOI] [PubMed] [Google Scholar]
  67. Pomjanski N., Motherby H., Buckstegge B., Knops K., Rohn B. L., Böcking A. Early diagnosis of mesothelioma in serous effusions using AgNOR analysis. Anal Quant Cytol Histol. 2001 Apr;23(2):151–160. [PubMed] [Google Scholar]
  68. Pujol J. L., Grenier J., Daurès J. P., Daver A., Pujol H., Michel F. B. Serum fragment of cytokeratin subunit 19 measured by CYFRA 21-1 immunoradiometric assay as a marker of lung cancer. Cancer Res. 1993 Jan 1;53(1):61–66. [PubMed] [Google Scholar]
  69. Rocher A. E., Blanco A. M., Palaoro L. A. Utilidad de la técnica de AgNOR en la interpretación de los derrames de cavidades serosas. Rev Med Chil. 2000 Sep;128(9):963–968. [PubMed] [Google Scholar]
  70. Rodrigues N. R., Rowan A., Smith M. E., Kerr I. B., Bodmer W. F., Gannon J. V., Lane D. P. p53 mutations in colorectal cancer. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7555–7559. doi: 10.1073/pnas.87.19.7555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Roggli V. L., Kolbeck J., Sanfilippo F., Shelburne J. D. Pathology of human mesothelioma. Etiologic and diagnostic considerations. Pathol Annu. 1987;22(Pt 2):91–131. [PubMed] [Google Scholar]
  72. Saha I., Dey P., Vhora H., Nijhawan R. Role of DNA flow cytometry and image cytometry on effusion fluid. Diagn Cytopathol. 2000 Feb;22(2):81–85. doi: 10.1002/(sici)1097-0339(200002)22:2<81::aid-dc4>3.0.co;2-c. [DOI] [PubMed] [Google Scholar]
  73. Sahin A. A., Ro J. Y., Brown R. W., Ordonez N. G., Cleary K. R., el-Naggar A. K., Wilson P., Ayala A. G. Assessment of Ki-67-derived tumor proliferative activity in colorectal adenocarcinomas. Mod Pathol. 1994 Jan;7(1):17–22. [PubMed] [Google Scholar]
  74. Sahn S. A. State of the art. The pleura. Am Rev Respir Dis. 1988 Jul;138(1):184–234. doi: 10.1164/ajrccm/138.1.184. [DOI] [PubMed] [Google Scholar]
  75. Sakaguchi M., Virmani A. K., Ashfaq R., Rogers T. E., Rathi A., Liu Y., Kodagoda D., Cunningham H. T., Gazdar A. F. Development of a sensitive, specific reverse transcriptase polymerase chain reaction-based assay for epithelial tumour cells in effusions. Br J Cancer. 1999 Feb;79(3-4):416–422. doi: 10.1038/sj.bjc.6690065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Salama G., Miédougé M., Rouzaud P., Mauduyt M. A., Pujazon M. C., Vincent C., Carles P., Serre G. Evaluation of pleural CYFRA 21-1 and carcinoembryonic antigen in the diagnosis of malignant pleural effusions. Br J Cancer. 1998;77(3):472–476. doi: 10.1038/bjc.1998.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Saleh H., Bober P., Tabaczka P. Value of Ki67 immunostain in identification of malignancy in serous effusions. Diagn Cytopathol. 1999 Jan;20(1):24–28. doi: 10.1002/(sici)1097-0339(199901)20:1<24::aid-dc6>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
  78. Schneller J., Eppich E., Greenebaum E., Elequin F., Sherman A., Wersto R., Koss L. G. Flow cytometry and Feulgen cytophotometry in evaluation of effusions. Cancer. 1987 Apr 1;59(7):1307–1313. doi: 10.1002/1097-0142(19870401)59:7<1307::aid-cncr2820590713>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
  79. Silverman J. F., Nance K., Phillips B., Norris H. T. The use of immunoperoxidase panels for the cytologic diagnosis of malignancy in serous effusions. Diagn Cytopathol. 1987 Jun;3(2):134–140. doi: 10.1002/dc.2840030209. [DOI] [PubMed] [Google Scholar]
  80. Simsir A., Fetsch P., Mehta D., Zakowski M., Abati A. E-cadherin, N-cadherin, and calretinin in pleural effusions: the good, the bad, the worthless. Diagn Cytopathol. 1999 Mar;20(3):125–130. doi: 10.1002/(sici)1097-0339(199903)20:3<125::aid-dc3>3.0.co;2-v. [DOI] [PubMed] [Google Scholar]
  81. Skov B. G., Stahel R. A., Hirsch F. ME1-antibody labelling of primary bronchogenic tumours and extrapulmonary malignancies. Lung Cancer. 1994 Sep;11(3-4):221–227. doi: 10.1016/0169-5002(94)90542-8. [DOI] [PubMed] [Google Scholar]
  82. Sommerfeld H. J., Meeker A. K., Piatyszek M. A., Bova G. S., Shay J. W., Coffey D. S. Telomerase activity: a prevalent marker of malignant human prostate tissue. Cancer Res. 1996 Jan 1;56(1):218–222. [PubMed] [Google Scholar]
  83. Sujathan K., Kannan S., Pillai K. R., Chandralekha B., Amma N. S., Nair M. K. Significance of AgNOR count in differentiating malignant cells from reactive mesothelial cells in serous effusions. Acta Cytol. 1996 Jul-Aug;40(4):724–728. doi: 10.1159/000333946. [DOI] [PubMed] [Google Scholar]
  84. Sölétormos G., Nielsen D., Schiøler V., Skovsgaard T., Dombernowsky P. Tumor markers cancer antigen 15.3, carcinoembryonic antigen, and tissue polypeptide antigen for monitoring metastatic breast cancer during first-line chemotherapy and follow-up. Clin Chem. 1996 Apr;42(4):564–575. [PubMed] [Google Scholar]
  85. Thunnissen F. B., Buchholtz R. T., Woutersen D. P., Arends J. W., van der Putten H. W., ten Velde G. P. Clinical value of DNA image cytometry in effusions with atypia. Diagn Cytopathol. 1999 Aug;21(2):112–116. doi: 10.1002/(sici)1097-0339(199908)21:2<112::aid-dc6>3.0.co;2-d. [DOI] [PubMed] [Google Scholar]
  86. Thunnissen F. B., Peterse J. L., van Pel R., Jansen J. W., Laddé B. E., Arends J. W., Volovics A. Reliability of fine needle aspiration cytology for distinguishing between carcinoma, lymphoma and sarcoma; the influence of clinical information. Cytopathology. 1993;4(2):107–114. doi: 10.1111/j.1365-2303.1993.tb00522.x. [DOI] [PubMed] [Google Scholar]
  87. Toshima S., Arai T., Yasuda Y., Takaya T., Ito Y., Hayakawa K., Shibuya C., Yoshimi N., Shibayama M., Kashiki Y. Cytological diagnosis and telomerase activity of cells in effusions of body cavities. Oncol Rep. 1999 Jan-Feb;6(1):199–203. doi: 10.3892/or.6.1.199. [DOI] [PubMed] [Google Scholar]
  88. Villena V., López-Encuentra A., Echave-Sustaeta J., Martín-Escribano P., Ortuño-de-Solo B., Estenoz-Alfaro J. Diagnostic value of CA 72-4, carcinoembryonic antigen, CA 15-3, and CA 19-9 assay in pleural fluid. A study of 207 patients. Cancer. 1996 Aug 15;78(4):736–740. doi: 10.1002/(SICI)1097-0142(19960815)78:4<736::AID-CNCR7>3.0.CO;2-C. [DOI] [PubMed] [Google Scholar]
  89. Wang N. S. Electron microscopy in the diagnosis of pleural mesotheliomas. Cancer. 1973 May;31(5):1046–1054. doi: 10.1002/1097-0142(197305)31:5<1046::aid-cncr2820310502>3.0.co;2-p. [DOI] [PubMed] [Google Scholar]
  90. Warhol M. J., Hickey W. F., Corson J. M. Malignant mesothelioma: ultrastructural distinction from adenocarcinoma. Am J Surg Pathol. 1982 Jun;6(4):307–314. [PubMed] [Google Scholar]
  91. Wells W. A., Rainer R. O., Memoli V. A. Basic principles of image processing. Am J Clin Pathol. 1992 Nov;98(5):493–501. doi: 10.1093/ajcp/98.5.493. [DOI] [PubMed] [Google Scholar]
  92. Westermann A. M., Havik E., Postma F. R., Beijnen J. H., Dalesio O., Moolenaar W. H., Rodenhuis S. Malignant effusions contain lysophosphatidic acid (LPA)-like activity. Ann Oncol. 1998 Apr;9(4):437–442. doi: 10.1023/a:1008217129273. [DOI] [PubMed] [Google Scholar]
  93. Wolman S. R. Fluorescence in situ hybridization: a new tool for the pathologist. Hum Pathol. 1994 Jun;25(6):586–590. doi: 10.1016/0046-8177(94)90223-2. [DOI] [PubMed] [Google Scholar]
  94. Yanagawa H., Takeuchi E., Suzuki Y., Ohmoto Y., Bando H., Sone S. Vascular endothelial growth factor in malignant pleural effusion associated with lung cancer. Cancer Immunol Immunother. 1999 Oct;48(7):396–400. doi: 10.1007/s002620050592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Yang C. T., Lee M. H., Lan R. S., Chen J. K. Telomerase activity in pleural effusions: diagnostic significance. J Clin Oncol. 1998 Feb;16(2):567–573. doi: 10.1200/JCO.1998.16.2.567. [DOI] [PubMed] [Google Scholar]
  96. Zarbo R. J. Flow cytometric DNA analysis of effusions. A new test seeking validation. Am J Clin Pathol. 1991 Jan;95(1):2–4. doi: 10.1093/ajcp/95.1.2. [DOI] [PubMed] [Google Scholar]
  97. Zebrowski B. K., Yano S., Liu W., Shaheen R. M., Hicklin D. J., Putnam J. B., Jr, Ellis L. M. Vascular endothelial growth factor levels and induction of permeability in malignant pleural effusions. Clin Cancer Res. 1999 Nov;5(11):3364–3368. [PubMed] [Google Scholar]
  98. Zimmerman R. L., Fogt F., Bibbo M. Diagnostic utility of sialosyl-Tn in discriminating carcinomatous cells from benign mesothelium in body cavity effusions. Acta Cytol. 1999 Nov-Dec;43(6):1079–1084. doi: 10.1159/000331356. [DOI] [PubMed] [Google Scholar]
  99. Zoppi J. A., Pellicer E. M., Sundblad A. S. Diagnostic value of p53 protein in the study of serous effusions. Acta Cytol. 1995 Jul-Aug;39(4):721–724. [PubMed] [Google Scholar]

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