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Effect of Smoking on the Lipid Composition of Lung Lining Fluid And

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Effect of Smoking on the Lipid Composition of Lung Lining Fluid And Eur Resplr J 1990, 3, 1128- 1139 Effect of smoking on the lipid composition of lung lining fluid and relationship between immunostimulatory lipids, inflammatory cells and foamy macrophages in extrinsic allergic alveolitis D.A. Hughes, P.L. Haslam Effect of smoking on the lipid composition of lung lining fluid and relation· Cell Biology Group, Dept of Cardiothoracic Surgery, ship between immunostimulatory lipids, inflammatory cells and foamy National Heart and Lung Institute, Dovehouse Street, macrophages in extrinsic allergic alveolitis. DA. Hughes, P L. Has/am. London, UK. ABSTRACT: Normal lung lining nuld suppresses lymphoprollferative responses. This errect Is mediated by the major phospholipid compo­ Correspondence: Dr P.L. Haslam, Cell Biology nents, but minor lipid components can stimulate lympbocyte prolif­ Group, Dept of Cardiothoracic Surgery, National eration. Tbe aim of this study was to discover whether the changes In Heart and Lung Institute, Dovehouse Street, London lung Lipid composition reported ln patients with ntrlnslc allergic SW3 6LY, UK. alveoUtls (EAA) might lnnuence tbe levels or lymphocytes which occur In the lungs of these patlent.s. Since cigarette smokers are less suscep­ tible to EAA, we also Investigated the effect of smoking on the lipid Keywords: Bronchoalveolar lavage; cholesterol; composition of lung lining nuld. Lung lining nuld was sampled by cigarette smoking; extrinsic allergic alveolitis; foamy bronchoa.lveolar lavage (BAL) from 15 patients with EAA, and 9 non­ macrophages; lymphocytes; phospholipids; pulmo· nary surfactant. smokers and 13 smokers without lung disease. The smoking controls had Increases In phosphatldyletbanolamlne, sphingomyelin and phospbatldylglycerol, but lower levels of cholesterol and cholesterol:total Received: November 1989; accepted after revision phospholipid ratios compared with the nonsmoking controls. By contrast, August 28, 1990. the patients with EAA bad Increases In total phospholipid and sphin­ gomyelin; there were no smoking related decreases In cholesterol; and several patients bad levels or cholesterol and cbolesterol:total phos­ Supported by The Chest, Heart and Stroke pholipid ratios above the upper limit for the controls. In the BAL nulds Association. or the EAA patients, the levels·ml"1 or the lmmunostimulatory llplds sphingomyelin, phosphatldylethanolamlne, cholesterol and cholesterol esters correlated with the number·mJ·' of lymphocytes, mast cells, neutrophlls and "foamy" macrophages. Cholesterol levels (r,=0.82) and lymphocyte counts (r,=0.90) correlated most closely with "foamy" mac rophages (p<O.OOJ), s uggesting that uptake or cholesterol by macrophages may en.bance antigen-presenting function. These obser­ vations provide some support for the hypothesis that lnnammatory reactions In the lungs might be Influenced by the localllpld environment. Eur Respir J., 1990, 3, 1128-1139. Extrins ic alle rgic alveolitis (EAA) (synonym - their bronchoalveolar lavage (BAL) fluid, most hypersensitivity pneumonitis) is an innammatory notably a striking decrease in the levels of the major granulomato us response of the lungs to a wide range of phospholipid class found in the pulmonary surfactant inhaled organic antigens [ 1]. Lung biopsies from the system, phosphatidylcholine, with increases in patients demonstrate increased numbers of lymphocytes phosphatidylethanolamine and cholesterol. We have infilLrating the alveolar walls and septa [2], and recently reported that the lipid fraction of normal samples washed from the peripheral air spaces contain lung lining fluid obtained by BAL from humans, pigs strikingly increased numbers of T-lymphocytes (3, 4] and rabbits can suppress lymphocyte proliferation in which appear to be activated L5]. The factors determining a dose dependent manner [9] and A.NsFIE.I.D et al. [10] susceptibility to this disease are still poorly understood have reported similar findings using dogs. Furthermore, [6] . we have shown that while some lipid classes, The air spaces of the lungs are lined with a Lipid rich including phosphatidylcholine and phosphatidylglycerol, material containing components with surfactant prop­ suppress the induc tio n of lymphocyte responses, erties which prevent alveolar collapse at low lung others, namely cholestero l, sphingomye lin and volumes [7]. JouANEL et al. [8] reported that patients phosphatidylethanolamine, augment them [11, 12}. We with EAA have alterations in the lipid composition of have also shown that altering the relative proportions of LUNG LA V AGE LIPIDS IN EAA AND IN SMOKERS 1129 mixtures of these lipids in vitro can modulate the levels a standardized 240 ml (4x60 ml) lavage fluid intro­ of immunosuppression [1 1). It is, therefore, possible duction volume, subject to clinical constrainlS. Several that the aiLerations in the lipid composition of the lung earlier samples were also included and the introduction lining fluid reported in patienlS with EAA may lead to volume ranged from 180-360 ml. The mean (±so) a reduction in its immunosuppressive properties and introduction volume was 240±0 ml in the nonsmoker favour the developmem of localized lymphoproliferative controls, 263±71 ml in the nonsmokers with EAA, responses to inhaled antigens. The aim of this study 300±36 ml in the smoker controls and 291±54 ml in the was to test this hypothesis by examining whether the smokers with EAA. The mean (±so)% fluid recovery was lipid composition of lung lining Owd obtained by BAL 60±11% in the nonsmoker controls, and 43±6% in the from patienlS with EAA has any relationship with the nonsmokers with EAA, 46±19% in the smoker controls, numbers of cells, particularly lymphocytes, recovered and 46±16% in the smokers with EAA. Although the simultaneously in the fluid. We have also investigated mean fluid recovery volume was higher in the non­ the effects of smoking on lung lining flui d in view of smoker controls, there were no significant differences the reports that EAA is a disorder which appears to be either in introduction volumes or % fluid recovered more prevalent in nonsmokers [13-15]. between the groups (Mann-Whitncy U-tcst). The lavage procedure was performed using an Olympus fibreoptic bronchoscope introduced by the transnasal route after Methods premedication with papaveretum and atroprine and under local anaesthesia with lignocaine. Supplementary Subjects oxygen was administered throughout the procedure. The tip of the bronchoscope was wedged in the lateral Patients with EAA. Bronchoalveolar lavage samples were segment of the right lower lobe and lavage was per­ obtained from 15 patients with EAA, all of whom had formed using 4x60 ml aliquolS of normal saline buff­ histories of exposure to organic duslS and exposure­ ered to pH 7.0 with 8.4% sodium bicarbonate and related respiratory symptoms. Nine of the patients had prewarmed to 37°C. The aspirated fluid was collected episodic symptoms (breathlessness with or without into a sterile sillconized container and transported on febrille episodes) whilst six had chronic breathlessness. ice immediately to the laboratory. The BAL fluid was Specific precipitating antibodies to antigens of the dusts centrifuged at 300 g for 10 min at 4°C to sediment the were presem in the scrum of aJl patienlS (avian in 1 I cells, and the supematant fluid was divided into aliquots and moulds in four), and all but one had been exposed and immediately frozen and stored at -70°C. This sepa­ up to the time of admission for lavage. All had shown ration procedure was completed within 20 min post­ a reduction in lung function, in particular diffusing lavage to prevent the fluid from becoming contaminated capacity for carbon monioxide ( <80% mean predicted), with lipids from the membranes of cells which, if kept although one patient had normal lung function at the for more prolonged periods in saline, subsequently start time of lavage. All of the patients had shown diffuse to die in vitro. Our values for cell viabiJity, assessed by nodular shadows on their chest radiographs, although trypan blue exclusion within 20 min, were >98% for all two had normal radiographs at the time of lavage. One cell types except contaminating ciliated and squamous also had linear shadows suggestive of fibrosis. None epithelial cells from the airways. These stained with were receiving treatment at the time of lavage. The mean trypan blue but rarely exceeded 5% of the total cells age was 45±14 yrs (7 males, 8 females). Eight patients present. had never smoked and seven were cigarette smokers (3 ex-smokers and 4 current smokers). Lipid analysis Controls. As controls for this study, BAL samples were obtained from a group of nine healthy volunteers who Aliquots of BAL supematant were thawed at room had never smoked (seven males, two females, mean age temperature and analysed by the methods that we have 36±6 yrs). To evaluate the effect of cigarette smoking, described previously [17]. Total lipid extraction was a group of 13 current smoking controls were also studied carried out by the methanol-chloroform method of BwaH (1 1 males, two females, mean age 44±18 yrs). These and DYER [18]. The organic phase containing the lipids subjects had normal chest radiographs and were was separated off and taken down to dryness under undergoing bronchoscopy for investigation of cough or reduced pressure at 20°C in a rotary evaporator, minor haemoptysis. No abnormality was detected in any resuspcnded in chloroform-methanol (9: 1 v/v) to 40 mg case. Ethical approval was obtained for all lavage studies, lipid per ml , and stored under nitrogen at -70°C. The and all patients and controls gave their informed phospholipids present in each sample were determined consent. using the improved one dimensional thin layer chroma­ tography (TLC) system developed by Gu.FU.J..AN et al. [ 19], using silica gel plates (20 cm + 20 cm, K6; Bronchoalveolar lavage (BAL) Whatman, Clifton, NJ) and chloroform-methanol­ petroleum ether (bp 35-60°C) - acetic acid - boric acid BAL samples were obtained from each individual (40:20:30:10:1.8 vol/vol/vol/vol/wL) as the developing studied by the method that we have previously described solvent.
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