Tuberculous Pleural Effusion and Tuberculous Empyema

ABSTRACT

Tuberculous pleuritis has increased worldwide, especially in developing countries, as a consequence of human immunodeficiency virus co-infection. Tuberculous pleuritis is a delayed hypersensitivity reaction against mycobacterial antigens in the pleural space. Mycobacteria are detected in less than 50% of pleural samples, but the characteristic pleural involvement, granulomas with or without caseous necrosis, is evident in 56 to 80% of cases from samples obtained by percutaneous pleural biopsy. Of several pleural fluid parameters studied, adenosine deaminase and interferon gamma (IFN-γ) have the best diagnostic yield, while polymerase chain reaction remains a promising test. Treatment of patients with tuberculous pleuritis is discussed.

Tuberculous empyema is a rare form of tuberculous pleuritis. It consists of a purulent infection of the pleural cavity with detectable bacilli in pleural fluid. Diagnosis is easily established clinically and bacteriologically. Treatment is to adequately drain the pleural space and achieve lung reexpansion, in conjunction with antituberculous chemotherapy. The efficacy of different surgical techniques is discussed.

KEYWORD

Tuberculous pleuritis - tuberculous empyema - diagnosis - treatment

REFERENCES

• 1 Raviglione M C, Snider D E, Kochi A. Global epidemiology of tuberculosis: morbidity and mortality of a worldwide epidemic.  JAMA . 1995;  273(3) 220-226
• 2 WHO. Global tuberculosis control 2000 . 
• 3 Aktogu S, Yorgancioglu A, Çirak K, Köse T, Dereli S M. Clinical spectrum of pulmonary and pleural tuberculosis: a report of 5480 cases.  Eur Respir J . 1996;  9 2031-2035
• 4 Batungwanayo J, Taelman H, Allen S, Bogaerts J, Kagame A, Van de Perre P. Pleural effusion, tuberculosis and HIV-1 infection in Kigali, Rwanda.  AIDS . 1993;  7 73-79
• 5 Grupo de trabajo de la P M I T. La tuberculosis en España: resultados del Proyecto Multicéntrico de Investigación sobre Tuberculosis (PMIT).  Med Clin (Barc) . 2000;  114 530-537
• 6 Mehta J B, Dutt A, Harvill L, Mathews K M. Epidemiology of extrapulmonary tuberculosis.  Chest . 1991;  99 1134-1138
• 7 Seibert A F, Haynes J, Middleton R, Bass J B. Tuberculous pleural effusion: twenty-year experience.  Chest . 1991;  99 883-886
• 8 Frye M D, Pozsik C J, Sahn S A. Tuberculous pleurisy is more common in AIDS than in non-AIDS patients with tuberculosis.  Chest . 1997;  112 393-397
• 9 Merino J M, Carpintero I, Alvarez T, Rodrigo J, Sánchez J, Coello J M. Tuberculous pleural effusion in children.  Chest . 1999;  115 26-30
• 10 Valdés L, Alvarez D, Valle J M, Pose A, San José E. The etiology of pleural effusions in an area with high incidence of tuberculosis.  Chest . 1996;  109 158-162
• 11 Richter C, Perenboom R, Mtoni I. Clinical features of HIV-seropositive and HIV-seronegative patients with tuberculous pleural effusion in Dar es Salaam, Tanzania.  Chest . 1994;  106 1471-1476
• 12 Marel M, Zrustová M, Stasny B, Light R W. The incidence of pleural effusion in a well-defined region: epidemiologic study in Central Bohemia.  Chest . 1993;  104 1486-1489
• 13 Saks A M, Posner R. Tuberculosis in HIV-positive patients in South Africa: a comparative radiological study with HIV-negative patients.  Clin Radiol . 1992;  46 387-390
• 14 Mlika-Cabanne N, Brauner M, Kamanfu G. Radiographic abnormalities in tuberculosis and risk of coexisting human immunodeficiency virus infection: methods and preliminary results from Bujumbura, Burundi.  Am J Respir Crit Care Med . 1995;  152 794-799
• 15 Mlika-Cabanne N, Brauner M, Mugusi F. Radiographic abnormalities in tuberculosis and risk of coexisting human immunodeficiency virus infection: results from Dar-es-Salaam, Tanzania, and scoring system.  Am J Respir Crit Care Med . 1995;  152 786-793
• 16 Pozniak A L, MacLeod G A, Ndlovu D, Ross E, Mahari M, Weinberg J. Clinical and chest radiographic features of tuberculosis associated with human immunodeficiency virus in Zimbabwe.  Am J Respir Crit Care Med . 1995;  152 1558-1561
• 17 Caylà J A, Jansà J M, Artazcoz L, Plasència A, and the AIDS-TB Group. Predictors of AIDS in a cohort of HIV-infected patients with pulmonary or pleural tuberculosis.  Tubercle and Lung Disease . 1993;  74 113-120
• 18 Keiper M D, Beumont M, Elshami A, Langlotz C P, Miller W T. CD4 T lymphocyte count and the radiographic presentation of pulmonary tuberculosis: a study of the relationship between these factors in patients with human immunodeficiency virus infection.  Chest . 1995;  107 74-80
• 19 Stead W W, Eichenholz A, Stauss H-K. Operative and pathologic findings in twenty-four patients with syndrome of idiopathic pleurisy with effusion, presumably tuberculous.  Am Rev Tuberc Pulm Dis . 1955;  71 473-502
• 20 Cazzadori A, Di Perri G, Marocco S, Carlotto A, Adami T, Concia E. Tuberculous pleurisy after percutaneous needle biopsy of a pulmonary nodule.  Respir Med . 1994;  88 477-478
• 21 Antoniskis D, Amin K, Barnes P F. Pleuritis as a manifestation of reactivation tuberculosis.  Am J Med . 1990;  89 447-450
• 22 Gupta R C, Dixit R, Purohit S D, Saxena A. Devolopment of pleural effusion in patients during anti-tuberculous chemotherapy: analysis of twenty-nine cases with review of literature.  Indian J Chest Dis Allied Sci . 2000;  42 161-166
• 23 Widström O, Nilsson B S. Pleurisy induced by intrapleural BCG in immunized guinea pigs.  Eur J Respir Dis . 1982;  63 425-434
• 24 Leibowitz S, Kennedy L, Lessof M H. The tuberculin reaction in the pleural cavity and its suppression by antilymphocyte serum.  Br J exp Path . 1973;  54 152-162
• 25 Schlesinger L S, Bellinger-Kawahara C G, Payne N R, Horwitz M A. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3.  J Immunol . 1990;  144 2771-2780
• 26 Boom W H, Wallis R S, Chervenak K A. Human Mycobacterium tuberculosis-reactive CD4+ T-cell clones: heterogeneity in antigen recognition, cytokine production, and cytotoxicity for mononuclear phagocytes.  Infect Immun . 1991;  59 2737-2743
• 27 Morgan D A, Ruscetti F W, Gallo R. Selective in vitro growth of T lymphocytes from normal human bone marrows.  Science . 1976;  193 1007-1008
• 28 Kurasawa T, Shimokata K. Cooperation between accessory cells and T lymphocytes in patients with tuberculous pleurisy.  Chest . 1991;  100 1046-1052
• 29 Barnes P F, Fong S J, Brennan P J, Twomey P E, Mazumder A, Modlin R L. Local production of tumor necrosis factor and interferon gamma in tuberculous pleuritis.  J Immunol . 1990;  145 149-154
• 30 Barnes P F, Modlin A, Bikle D D, Adams J S. Transpleural gradient of 1,25-dihydroxyvitamin D in tuberculous pleuritis.  J Clin Invest . 1989;  83 1527-1532
• 31 Maeda J, Ueki N, Ohkawa T. Local production and localization of transforming growth factor-beta in tuberculous pleurisy.  Clin Exp Immunol . 1993;  92 32-38
• 32 Jonjic N, Peri G, Bernasconi S. Expression of adhesion molecules and chemotactic cytokines in cultured human mesothelial cells.  J Exp Med . 1992;  176 1165-1174
• 33 Mohammed K A, Nasreen N, Ward M J, Mubarak K K, Rodriguez-Panadero F, Antony V B. Mycobacterium-mediated chemokine expression in pleural mesothelial cells: role of C-C chemokines in tuberculous pleurisy.  J Infect Dis . 1998;  178 1450-1456
• 34 Lorgat F, Keraan M M, Lukey P T, Ress S R. Evidence for in vivo generation of cytotoxic T cells: PPD-stimulated lymphocytes from tuberculous pleural effusions demonstrate enhanced cytotoxicity with accelerated kinetics of induction.  Am Rev Respir Dis . 1992;  145 418-423
• 35 Ota T, Okubo Y, Sekiguchi M. Analysis of immunologic mechanisms of high natural killer cell activity in tuberculous pleural effusions.  Am Rev Respir Dis . 1990;  142 29-33
• 36 Arruda S, Chalhoub M, Cardoso S, Barral-Netto M. Cell-mediated immune responses and cytotoxicity to mycobacterial antigens in patients with tuberculous pleurisy in Brazil.  Acta Trop . 1998;  71(1) 1-15
• 37 Hua C C, Chang L C, Chen Y C, Chang S C. Proinflammatory cytokines and fibrinolytic enzymes in tuberculous and malign pleural effusions.  Chest . 1999;  116(5) 1292-1296
• 38 Tsicopoulos A, Hamid Q, Varney V. Preferential messenger RNA expression of TH1-type cells (IFN-gamma+, IL-2+) in classical delayed-type (tuberculin) hypersensitivity reactions in human skin.  J Immunol . 1992;  148 2058-2061
• 39 Berger H W, Mejia E. Tuberculous pleurisy.  Chest . 1973;  63 88-92
• 40 Ellner J J. Supressor adherent cells in human tuberculosis.  J Immunol . 1978;  121 2573-2579
• 41 Rossi G A, Balbi B, Manca F. Tuberculous pleural effusions: evidence for a selective presence of PPD-specific T lymphocytes at site of inflammation in the early phase of the infection.  Am Rev Respir Dis . 1987;  136 575-579
• 42 Nasreen N, Mohammed K A, Ward M J, Antony V B. Mycobacterium-induced transmesothelial migration of monocytes into pleural space: role of intercellular adhesion molecule-1 in tuberculous pleurisy.  J Infect Dis . 1999;  180 1616-1623
• 43 Allen J C, Apicella M A. Experimental pleural effusion as a manifestation of delayed hypersensitivity to tuberculin PPD.  J Immunol . 1968;  101 481-487
• 44 Leckie W JH, Tothill P. Albumin turnover in pleural effusions.  Clin Sci . 1965;  29 339-352
• 45 Plans Bolibar C, Aranda Torres A, Roca Montanari A. Pleuritis tuberculosa: diagnostico histológico y bacteriológico en 310 pacientes.  Arch Bronconeumol . 1980;  16 106-110
• 46 Epstein D M, Kline L R, Albelda S M, Miller W T. Tuberculous pleural effusions.  Chest . 1987;  91 106-109
• 47 Trajman A, Neto E B, Belo M T. Pleural tuberculosis and human immunodeficiency virus co-infection.  Int J Tuberc Lung Dis . 1997;  1 498-501
• 48 Yilmaz M, Kumcuoglu Z, Utkaner G, Yalniz O, Erkmen G. Computed tomography findings of tuberculous pleurisy.  Int J Tuberc Lung Dis . 1998;  2 164-167
• 49 Relkin F, Aranda C P, Garay S M, Smith R, Berkowitz K A, Rom W N. Pleural tuberculosis and HIV infection.  Chest . 1994;  105 1338-1341
• 50 Ferrer J, Muñoz X, Orriols R, Light R W, Morell F. Evolution of idiopathic pleural effusion: a prospective, long-term follow-up study.  Chest . 1996;  109 1508-1513
• 51 Light R W, Erozan Y S, Ball W C. Cells in pleural fluid: their value in differential diagnosis.  Arch Intern Med . 1973;  132 854-860
• 52 Ellison E, Lapuerta P, Martin S E. Cytologic features of mycobacterial pleuritis: logistic regression and statistical analysis of a blinded, case-controlled study.  Diagn Cytopathol . 1998;  19 173-176
• 53 Jones D, Lieb T, Narita M, Hollender E S, Pitchenik A E, Ashkin D. Mesothelial cells in tuberculous pleural effusions of HIV-infected patients.  Chest . 2000;  117 289-291
• 54 Bueno C E, Clemente G, Castro B C. Cytologic and bacteriologic analysis of fluid and pleural biopsy specimens with Cope's needle.  Arch Intern Med . 1990;  150 1190-1194
• 55 Valdes L, Alvarez D, San Jose E. Tuberculous pleurisy: a study of 254 patients.  Arch Intern Med . 1998;  158 2017-2021
• 56 Kirsch C M, Kroe D M, Azzi R L, Jensen W A, Kagawa F T, Wehner J H. The optimal number of pleural biopsy specimens for a diagnosis of tuberculous pleurisy.  Chest . 1997;  112 702-706
• 57 Heyderman R S, Makunike R, Muza T. Pleural tuberculosis in Harare, Zimbabwe: the relationship between human immunodeficiency virus, CD4 lymphocyte count, granuloma formation, and disseminated disease.  Trop Med International Health . 1998;  3 14-20
• 58 Maaertens G, Bateman E D. Tuberculous pleural effusions: increased culture yield with bedside inoculation of pleural fluid and poor diagnostic value of adenosine deaminase.  Thorax . 1991;  46 96-99
• 59 Cheng A F, Li M SK, Chan C Y. Evaluation of three culture media and their combinations for the isolation of Mycobacterium tuberculosis from pleural aspirates of patients with tuberculous pleurisy.  J Trop Med Hyg . 1994;  97 249-253
• 60 Cheng A FB, Tai V HB, Li M SK. Improved recovery of Mycobacterium tuberculosis from pleural aspirates: bedside inoculation, heparinized containers, and liquid culture media.  Scand J Infect Dis . 1999;  31 485-487
• 61 Walzl G, Wyser C, Smedema J, Corbett C, van de Wal B. Comparing the diagnostic yield of Abrams needle biopsy and thoracoscopy.  Am J Respir Crit Care Med . 1996;  153 A460
• 62 Valdés L, San José E, Alvarez D. Diagnosis of tuberculous pleurisy using the biologic parameters adenosine deaminase, lysozyme, and interferon gamma.  Chest . 1993;  103 458-465
• 63 Verea Hernando R H, Masa Jimenez F J, Dominguez Juncal L, Garcia-Buela J P, Martin Egana T M, Fontan Bueso J. Meaning and diagnostic value of determining the lysozyme level of pleural fluid.  Chest . 1987;  91 342-345
• 64 Ribera E, Ocaña I, Martinez-Vazquez J M, Rossell M, Español T, Ruibal A. High level of interferon gamma in tuberculous pleural effusion.  Chest . 1988;  93 308-311
• 65 Shimokata K, Saka H, Murate T, Hasegawa Y, Hasegawa T. Cytokine content in pleural effusion: comparison between tuberculous and carcinomatous pleurisy.  Chest . 1991;  99 1103-1107
• 66 Ito M, Kojiro N, Shirasaka T, Moriwaki Y, Tachibana I, Kobuku T. Elevated levels of soluble interleukin-2 receptors in tuberculous pleural effusions.  Chest . 1990;  97 1141-1143
• 67 Yew W W, Chan C Y, Kwas S Y, Cheung S W, French G L, Path E RC. Diagnosis of tuberculous pleural effusion by the detection of tuberculostearic acid in pleural aspirates.  Chest . 1991;  100 1261-1263
• 68 Shibagaki T, Hasegawa Y, Saito H, Yamori S, Shimokata K. Adenosine deaminase isozymes in tuberculous pleural effusion.  J Lab Clin Med . 1996;  127 348-352
• 69 Ungerer J PJ, Oosthuizen H M, Retief J H, Bissbort S H. Significance of adenosine deaminase activity and its isoenzymes in tuberculous effusions.  Chest . 1994;  106 33-37
• 70 Orriols R, Muñoz X, Drobnic M E, Ferrer J, Morell F. High adenosine deaminase activity in pleural effusion due to psittacosis.  Chest . 1992;  101 881-882
• 71 Petterson T, Ojala K, Weber T H. Adenosine deaminase in the diagnosis of pleural effusions.  Acta Med Scand . 1984;  215 299-304
• 72 Ocaña I, Martinez-Vazquez J M, Segura R M, Fernandez-DeSevilla T, Capdevila J A. Adenosine deaminase in pleural fluids: test for diagnosis of tuberculous pleural effusion.  Chest . 1983;  84 51-53
• 73 Maritz F J, Malan C, Le Roux I. Adenosine deaminase estimations in the differentiation of pleural effusions.  SA Med J . 1982;  62 556-558
• 74 Ena J, Valls V, Pérez de Oteyza C, Enríquez de Salamanca R. Utilidad y limitaciones de la adenosina desaminasa en el diagnóstico de la pleuresía tuberculosa: estudio metaanalítico.  Med Clin (Barc) . 1990;  95 333-335
• 75 Valdés L, Alvarez D, San Jose E. Value of adenosine deaminase in the diagnosis of tuberculous pleural effusions in young patients in a region of high prevalence of tuberculosis.  Thorax . 1995;  50 600-603
• 76 Burgess L J, Maritz F J, Le Roux I, Frans Taljaard J J. Use of adenosine deaminase as a diagnostic tool for tuberculous pleurisy.  Thorax . 1995;  50 672-674
• 77 Riantawan P, Chaowalit P, Wongsangiem M, Rojanaraweewong P. Diagnostic value of pleural fluid adenosine deaminase in tuberculous pleuritis with reference to HIV coinfection and a bayesian analysis.  Chest . 1999;  116 97-103
• 78 Nathan C F, Murray H W, Wiebe M E, Rubin B Y. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity.  J Exp Med . 1983;  158 670-689
• 79 Aoki Y, Katoh O, Nakanishi Y, Kuroki S, Yamada H. A comparison study of IFN-gamma, ADA, and CA125 as the diagnostic parameters in tuberculous pleuritis.  Respir Med . 1994;  88 139-143
• 80 Villena V, López-Encuentra A, Echave-Sustaeta J, Martín-Escribano P, Ortuño-de Solo B, Estenoz-Alfaro J. Interferon-gamma in 388 immunocompromised and immunocompetent patients for diagnosing pleural tuberculosis.  Eur Respir J . 1996;  9 2635-2639
• 81 Söderbloom T, Nyberg P, Teppo A M, Klockars M, Riska H, Petterson T. Pleural fluid interferon-gamma and tumour necrosis factor-alfa in tuberculous and rheumatoid pleurisy.  Eur Respir J . 1996;  9 1652-1655
• 82 Ogawa K, Koga H, Hirakata Y, Tomono K, Fashiro T, Kohno S. Differential diagnosis of tuberculous pleurisy by measurement of cytokine concentrations in pleural effusion.  Tuber Lung Dis . 1997;  78 29-34
• 83 Wongtim S, Silachamroon U, Ruxrungtham K. Interferon gamma for diagnosing tuberculous pleural effusions.  Thorax . 1999;  54 921-924
• 84 Levy H, Wayne L G, Anderson B E, Barnes P F, Light R W. Antimycobacterial antibody levels in pleural fluid reflect passive diffusion from serum.  Chest . 1990;  97 1144-1147
• 85 Van Vooren P J, Farber C M, De Bruyn J, Yernault J C. Antimycobacterial antibodies in pleural effusions.  Chest . 1990;  97 88-90
• 86 Chin D P, Yajko D M, Hadley W K. Clinical utility of a commercial test based on the polymerase chain reaction for detecting Mycobacterium tuberculosis in respiratory specimens.  Am J Respir Crit Care Med . 1995;  151 1872-1877
• 87 de Wit D, Maaertens G, Steyn L. A comparative study of the polymerase chain reaction and conventional procedures for the diagnosis of tuberculous pleural effusion.  Tubercle Lung Dis . 1992;  73 262-267
• 88 de Lassence A, Lecossier D, Pierre C, Cadranel J, Stern M, Hance A J. Detection of mycobacterial DNA in pleural fluid from patients with tuberculous pleurisy by means of the polymerase chain reaction: comparison of two protocols.  Thorax . 1992;  47 265-269
• 89 Querol J M, Mínguez J, García-Sánchez E, Farga M A, Gimeno C, García-de-Lomas J. Rapid diagnosis of pleural tuberculosis by polymerase chain reaction.  Am J Respir Crit Care Med . 1995;  152 1977-1981
• 90 Kuwano K, Minamide W, Kusunoki S. Evaluation of nested polymerase chain reaction for detecting mycobacterial DNA in pleural fluid.  Kansenshogaku Zasshi . 1995;  69 175-180
• 91 Villegas M V, Labrada L A, Gore Saravia N. Evaluation of polymerase chain reaction, adenosine deaminase, and interferon-gamma in pleural fluid for the differential diagnosis of pleural tuberculosis.  Chest . 2000;  118 1355-1364
• 92 Roper W H, Waring J J. Primary serofibrinous pleural effusion in military personnel.  Am Rev Tuberc . 1955;  71 616-635
• 93 Ormerod L P, McCarthy O R, Rudd R M, Horsfield N. Short course chemotherapy for tuberculous pleural effusion and culture negative pulmonary tuberculosis.  Tuberc Lung Dis . 1995;  76 25-27
• 94 Dutt A K, Moers D, Stead W W. Short-course chemotherapy for pleural tuberculosis: nine years' experience in routine treatment service.  Chest . 1986;  90 112-116
• 95 Dutt A K, Moers D, Stead W W. Tuberculous pleural effusion: 6-month therapy with isoniazid and rifampin.  Am Rev Respir Dis . 1992;  145 1429-1432
• 96 Cañete C, Galarza I, Granados A, Farrero E, Estopá R, Manresa F. Tuberculous pleural effusion: experience with six months of treatment with isoniazid and rifampicin.  Thorax . 1994;  49 1160-1161
• 97 Joint Tuberculosis Committee of the British Thoracic Society. Chemotherapy and management of tuberculosis in the United Kingdom: recommendations 1998.  Thorax . 1998;  53 536-548
• 98 Task Force of ERS, WHO, and the Europe Region of IUATLD. Tuberculosis management in Europe.  Eur Respir J . 1999;  14 978-992
• 99 Small P M, Schecter G F, Goodman P C, Sande M A, Chaisson R E, Hopewell P C. Treatment of tuberculosis in patients with advanced human immunodeficiency virus infection.  N Engl J Med . 1991;  324 289-294
• 100 Harries A D, Nyangulu D S, Banda H. Efficacy of an unsupervised ambulatory treatment regimen for smear-negative pulmonary tuberculosis and tuberculous pleural effusion in Malawi.  Int J Tuberc Lung Dis . 1999;  3 402-408
• 101 Banda H, Kang'ombe C, Harries A D. Mortality rates and recurrent rates of tuberculosis in patients with smear-negative pulmonary tuberculosis and tuberculous pleural effusion who have completed treatment.  Int J Tuberc Lung Dis . 2000;  4 968-974
• 102 Al-Majed S A. Study of paradoxical response to chemotherapy in tuberculous pleural effusion.  Respir Med . 1996;  90 211-214
• 103 Large S E, Levick R K. Aspiration in the treatment of primary tuberculous pleural effusion.  Br Med J . 1958;  1 1512-1514
• 104 De Pablo A, Villena V, Echave-Sustaeta J, López Encuentra A. Are pleural fluid parameters related to the development of residual pleural thickening in tuberculosis?.  Chest . 1997;  112 1293-1297
• 105 Barbas C S, Cukier A, de Varvalho R C, Barbas Filho V J, Light R W. The relationship between pleural fluid findings and the development of pleural thickening in patients with pleural tuberculosis.  Chest . 1991;  100 1264-1267
• 106 Lee C H, Wang W J, Lan R S, Tsai Y H, Chiang Y C. Corticosteroids in the treatment of tuberculous pleurisy: a double-blind, placebo-controlled, randomized study.  Chest . 1988;  94 1256-1259
• 107 Galarza I, Cañete C, Granados A, Estopá R, Manresa F. Randomized trial of corticosteroids in the treatment of tuberculous pleurisy.  Thorax . 1995;  50 1305-1307
• 108 Wyser C, Walzl G, Smedema J P, Swart F, van Schalkwyk M E, van de Wal W B. Corticosteroids in the treatment of tuberculous pleurisy: a double-blind, placebo-controlled, randomized study.  Chest . 1996;  110 333-338
• 109 Matchaba P T, Volmink J. Steroids for treating tuberculous pleurisy. In: The Cochrane Library. Oxford: Update Software; 2001;issue 1
• 110 Light R W. Chylothorax and pseudochylothorax. In: Light RW, ed. Pleural Diseases Philadelphia, Pa: Lippincott, Williams & Wilkins; 2001: 327-343
• 111 Vennera M C, Moreno R, Cot J. Chylothorax and tuberculosis.  Thorax . 1983;  38 694-695
• 112 Mandal A K, Thadepalli H, Mandal A K, Chettipally U. Outcome of primary empyema thoracis: therapeutic and microbiologic aspects.  Ann Thorac Surg . 1998;  66 1782-1786
• 113 Jenssen A O. Chronic calcified pleural empyema.  Scan J Resp Dis . 1969;  50 19-27
• 114 Al-kattan K M. Management of tuberculous empyema.  Eur J Cardiothorac Surg . 2000;  17 251-254
• 115 Rogiers P, Verschakelen J, Knockaert D, Vanneste S. Occult tuberculous postpneumonectomy space empyema four years after lung resection.  Postgrad Med J . 1991;  67 672-674
• 116 Minami M, Kawauchi N, Yoshikawa K. Malignancy associated with chronic empyema: radiologic assessment.  Radiology . 1991;  178 417-423
• 117 Forouhi N G, Walker W, Leitch A G. Tuberculous empyema presenting 62 years after oleothorax: a case report.  Respir Med . 1994;  88 391-392
• 118 Iseman M D, Madsen L A. Chronic tuberculous empyema with bronchopleural fistula resulting in treatment failure and progressive drug resistance.  Chest . 1991;  100 124-127
• 119 Sindel E A. Empyema necessitatis.  Q Bull Sea View Hospital . 1940;  6 1-49
• 120 Glicklich M, Mendelson D S, Gendal E S, Teirstein A S. Tuberculous empyema necessitatis: computed tomography findings.  Clin Imag . 1990;  14 23-25
• 121 Bhatt G M, Austin H M. CT demonstration of empyema necessitatis.  J Comput Assist Tomogr . 1985;  9 1108-1109
• 122 Neihart R E, Hof D G. Successful nonsurgical treatment of tuberculous empyema in an irreducible pleural space.  Chest . 1985;  88 792-794
• 123 Elliot A M, Berning S E, Iseman M D, Peloquin C A. Failure of drug penetration and acquisition of drug resistance in chronic tuberculous empyema.  Tubercle Lung Dis . 1995;  76 463-467
• 124 Yim A PC. The role of video-assisted thoracoscopic surgery in the management of pulmonary tuberculosis.  Chest . 1996;  110 829-832
• 125 Nakaoka K, Nakahara K, Iioka S, Mori T, Sawamura K, Kawashima Y. Postoperative preservation of pulmonary function in patients with chronic empyema thoracis: a one-stage operation.  Ann Thorac Surg . 1989;  47 848-852
• 126 Ali S M, Siddiqui A A, McLaughlin J S. Open drainage of massive tuberculous empyema with progressive reexpansion of the lung: an old concept revisited.  Ann Thorac Surg . 1996;  62 218-223
• 127 Miller J I, Mansour K A, Nahai F, Jurkiewicz M J, Hatcher Jr R C. Single-stage complete muscle flap closure of the postpneumonectomy empyema space: a new method and possible solution to a disturbing complication.  Ann Thorac Surg . 1984;  38 227-231
• 128 Tatsumura T, Koyama S, Yamamoto K. A new technique for one-stage radical eradication of long-standing chronic thoracic empyema.  J Thorac Cardiovasc Surg . 1990;  99 410-415
• 129 Nomori H, Hasegawa T, Kobayashi R. The ``reversed'' latissimus dorsi muscle flap with conditioning delay for closure of a lower thoracic tuberculous empyema.  Thorac Cardiovasc Surgeon . 1994;  42 182-184