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Pleural Tuberculosis Copyright ERS Journals Ltd 1997 Eur Respir J 1997; 10: 942–947 European Respiratory Journal DOI: 10.1183/09031936.97.10040942 ISSN 0903 - 1936 Printed in UK - all rights reserved SERIES 'THE PLEURA' Edited by H. Hamm and R.W. Light Number 4 in this Series Pleural tuberculosis J. Ferrer Pleural tuberculosis. J. Ferrer. ©ERS Journals Ltd 1997. Correspondence: J. Ferrer ABSTRACT: Tuberculous pleural effusions occur in up to 30% of patients with Servei de Pneumologia tuberculosis. It appears that the percentage of patients with pleural effusion is Hospital General Universitari Vall d’Hebron comparable in human immunodeficiency virus (HIV)-positive and HIV-negative E-08035 Barcelona individuals, although there is some evidence that HIV-positive patients with CD4+ Spain -1 counts <200 cells·mL are less likely to have a tuberculous pleural effusion. Keywords: Adenosine deaminase There has recently been a considerable amount of research dealing with the pleural effusion immunology of tuberculous pleurisy. At present, we have more evidence that acti- tuberculosis vated cells produce cytokines in a complex pleural response to mycobacteria. Intramacrophage elimination of mycobacterial antigens, granuloma formation, Received: March 14 1996 direct neutralization of mycobacteria and fibrosis are the main facets of this reac- Accepted after revision September 29 1996 tion. With respect to diagnosis, adenosine deaminase and interferon gamma in pleural fluid have proved to be useful tests. Detection of mycobacterial deoxyribonucleic acid (DNA) by the polymerase chain reaction is an interesting test, but its useful- ness in the diagnosis of tuberculous pleurisy needs further confirmation. The rec- ommended treatment for tuberculous pleurisy is a 6 month regimen of isoniazid and rifampicin, with the addition of pyrazinamide in the first 2 months. HIV patients may require a longer treatment. The general use of corticosteroids is not recommended at this time, but they can be used in individuals who are markedly symptomatic. Eur Respir J 1997; 10: 942–947. Incidence [3, 4]. The fact that HIV infection affects mainly young adults could explain the high frequency of pleurisy in The clinical importance of tuberculosis in general and HIV patients with tuberculosis, since young people tend of tuberculous pleural effusion in particular is not the to have primary disease. same worldwide. Of the 8 million people who develop- ed tuberculosis in 1990, 95% lived in developing coun- tries [1]. In sub-Saharan Africa, 15 million new cases Pathogenesis of tuberculosis are expected over the next 5 yrs [2]. The frequency of pleural effusion in these tuberculous patients The current hypothesis for the pathogenesis of pri- is currently approximately 31% [3]. mary tuberculous pleural effusion is that a subpleural It seems that co-infection with human immunodefi- caseous focus in the lung ruptures into the pleural space ciency virus (HIV) is the main factor responsible for 6–12 weeks after a primary infection [7]. Mycobacterial this increase in tuberculosis and tuberculous pleurisy. antigens enter the pleural space and interact with T-cells In Burundi and Tanzania, 60% of patients with tuber- previously sensitized to mycobacteria, resulting in a culous pleural effusion were HIV-positive [3, 4]. Initial delayed hypersensitivity reaction and the accumulation data suggest that HIV patients tend to develop tuber- of fluid. It seems that this reaction of the pleura aug- culous pleurisy in the early stages of immunosuppres- ments the entry of fluid into the pleural space by in- sion. In one report, the prevalence of pleural effusion creasing the permeability of pleural capillaries to serum in tuberculous HIV patients with CD4+ T-lymphocyte proteins [8], and thereby increasing the oncotic pressure (helper-inducer) counts >200 cells·mL-1 was 27%, while in the pleural fluid. Involvement of the lymphatic sys- it was only 10% in HIV patients with tuberculosis and tem probably also contributes to the accumulation of CD4+ T-lymphocyte counts <200 cells·mL-1 [5]. There pleural fluid. An impaired clearance of proteins from are contradictory data regarding the frequency of pleurisy the pleural space has been reported in human tubercu- in HIV-positive and HIV-negative patients with tuber- lous effusions [9]. It is known that the clearance of pro- culosis. One study in South Africa reported a higher fre- teins and fluid from the pleural space is carried out by quency in HIV-positive patients [6], but several other lymphatics in the parietal pleura. Fluid gains access to studies in Central Africa could find no such differences the lymphatics through openings in the parietal pleura Previous articles in this series: No. 1: G. Miserocchi. Physiology and pathophysiology of pleural fluid turnover. Eur Respir J 1997; 10: 219–225. No. 2: R.W. Light. Diagnostic principles in pleural disease. Eur Respir J 1997; 10: 476–481. No. 3: G.T. Kinasewitz. Transudative effusions. Eur Respir J 1997; 10: 714–718. PLEURAL TUBERCULOSIS 943 called stomata [10]. Since the parietal pleural is diffus- CD4+ cells. Paradoxically, however, up to 30% of pati- ely affected with pleural tuberculosis, damage to or obs- ents with tuberculous pleurisy have a negative PPD test truction of the stomata could be an important mechanism [11]. Since adherent suppressor cells are found in the leading to accumulation of pleural fluid. peripheral blood but not in the pleural fluid of tubercu- lous patients [17], these cells could suppress the activity of blood T-lymphocytes in tuberculin anergic patients. Immunology However, peripheral suppressor cells cannot be detect- ed in some PPD-negative patients with pleural tuber- It appears that tuberculous pleurisy is due to a delayed culosis. The PPD negativity in these patients has been hypersensitivity reaction rather than to a tuberculous in- attributed to compartmentalization of CD4+ T-lympho- fection. This hypothesis is supported by several facts. cytes in the pleural space [17]. Cultures of pleural specimens from patients with tuber- culous pleurisy are frequently negative [11]. A lympho- cytic pleurisy can be produced in sensitized guinea-pigs Diagnosis by the intrapleural instillation of heat-killed bacilli Cal- mette-Guérin (BCG) [12]. Moreover, pleural effusion It appears that in developed countries tuberculous also develops in nonsensitized animals who have received pleurisy is becoming a form of reactivation rather than cells from immunized animals [13]; and effusion does primary disease [28], and therefore the mean age of the not develop in sensitized animals if they are given anti- affected individual is much higher than it was 50 yrs lymphocyte serum [14]. ago [28]. The diagnosis of tuberculous pleurisy in older Neutrophils appear to be the first cells responding to individuals can be problematical, because these patients mycobacterial protein in the pleural space. In an animal tend to have other conditions that could be responsible model of purified protein derivative (tuberculin) (PPD)- for their pleural effusions, such as pleural malignancy. induced pleural effusion, neutrophils initially predom- Moreover, patients with tuberculous pleurisy do not have inate and are responsible for the recruitment of blood distinctive clinical symptoms. Fever, chest pain, weight monocytes [15]. Recent studies suggest that the meso- loss and other symptoms are present in patients with thelial cell plays a role in the recruitment of blood neu- tuberculous pleurisy as well as in patients with exuda- trophils and monocytes in tuberculous pleuritis [16]. tive effusions with other aetiologies. Initial data suggest After 3 days, lymphocytes are already predominant in that patients with tuberculous pleural effusion and HIV the tuberculous pleural fluid [12]. Most of the lympho- seropositivity have been symptomatic for a longer peri- cytes in a tuberculous pleural effusion are T-lympho- od, have additional symptoms (tachypnoea, fever, dys- cytes [17]. Lymphocytes are mainly CD4+ [17], with a pnoea, night sweat, fatigue, diarrhoea), and have more mean CD4:CD8 (helper:suppressor) ratio of about 4.3 hepatomegaly, splenomegaly and lymphadenopathy than in pleural fluid, and 1.6 in peripheral blood [18]. patients who are seronegative [29]. Recent studies provide a partial explanation of the immunological process in tuberculous pleurisy. After phagocytosing mycobacteria, macrophages act as anti- Tuberculin skin test gen-presenting cells to the T-lymphocytes, which become activated and promote differentiation of macrophages and The diagnostic evaluation of patients with tubercu- granuloma formation. Some components of the myco- lous pleurisy includes a tuberculin skin test. In popula- bacterial cell wall, such as protein/proteoglycans complex tions with a high prevalence of tuberculous infection, a and lipoarabidomannan, are able to stimulate macrophages positive skin test in a patient with a pleural exudate to produce tumour necrosis factor (TNF), a regulator of strongly suggests the diagnosis of tuberculosis, where- granuloma formation [19]. Activated pleural macrophages as the diagnostic value of a positive tuberculin skin test can also produce interleukin-1 (IL-1) [20]. Both TNF and in countries with a low prevalence of tuberculous pleurisy IL-1 are involved in lymphocyte activation. Upon expo- is lower. On the other hand, a negative tuberculin skin sure to PPD, pleural T-lymphocytes from patients with test does not rule out the diagnosis of tuberculous pleur- tuberculous pleurisy produce
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