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Early Effects of Short-Time Cigarette Smoking on the Human Lung: A Study of Bronchoalveolar Lavage Fluids

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Abstract

We investigated the early effects of cigarette smoking in healthy subjects by means of lung lavage, looking at markers of alveolar permeability, the alveolar cell profile, the immunophenotyping of macrophages and lymphocytes, and the level and profile of surfactant phospholipids. Bronchoal-veolar lavages (BAL) were performed in 33 healthy subjects [20 nonsmokers (nS), 13 moderate and short-time smokers (S)]. In the acellular supernatants we measured the markers of alveolar permeability (i.e., total proteins, albumin, albumin/urea), the alveolar epithelial lining fluid (AELF), the surfactant amounts and profile, and explored the blood lymphocytes by in vitro exposure. The cell pellet established the alveolar formula and a membrane mapping of macrophages (LFA-1 and HLA-DRII expression) and lymphocytes (CD4, CD8, LFA-1, HLA-DRII expression). We found no significant increase of alveolar permeability in our smokers, but an increased alveolar cellularity (more than 3-fold vs nS, P < 0.05) evenly distributed between sub-populations except for an enhanced number of eosinophils in smokers (P < 0.05 vs nS). Smokers’ alveolar macrophages had an overloaded cytoplasm, a decreased percentage of antigen-handling cell expression (HLA DRII: P < 0.05 vs nS) and a low percentage of cell to cell adhesion molecule expression (LFA-1: P < 0.05 vs nS). Smoking history and LFA-1 expression on alveolar macrophages were interrelated. Smokers’ alveolar lymphocyte subsets were more often T suppressor cells (CD8+) and had an increased percentage of antigen-presenting cell expression (HLA DRII: P < 0.05 vs nS). Smokers’ BAL fluid did not show the inhibitory control of phytohemagglutinin-induced lymphocyte proliferation present in nonsmokers’ fluids. Surfactant phospholipid amounts were similar, but phosphatidylethanolamine was raised and the ratio of phosphatidyicholine to sphingomyelin decreased in smokers (P<0.05 vs nS).

We observed specific cellular and biochemical alterations in the lung lavage of short-time smokers. Alveolar macrophage and lymphocyte expression of LFA-1 and HLA-DR II molecules was altered. Smokers’ alveolar fluids lost the physiologic regulatory control of T mitogen-induced lymphocyte proliferation. Membrane phospholipids released by cellular damage increased early in tobacco-exposed lung fluids. This profile of alterations may be an early and sensitive marker of smoking-induced lung damage.

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References

  1. Albelda SM, Buck CA (1990) Integrins and other cell adhesion molecules. FASEB J 4: 2868–2880

    PubMed  CAS  Google Scholar 

  2. Arnaout MA (1990) Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75:1037–1050

    PubMed  CAS  Google Scholar 

  3. Barlow Y, Lamb D (1985) The effect of cigarette smoking on cell number and cell proliferation on the alveolar walls of man. Thorax 40:214–218

    Google Scholar 

  4. Bartlett WC (1959) Phosphorus assay in column chromatography. J Biol Chem 234:466–468

    PubMed  CAS  Google Scholar 

  5. Baughman RP, Dohn MN (1992) Value of albumin to urea ratio in the bronchoalveolar fluid in assessing alveolar permeability. Eur Respir X In European respiratory review, 3rd International Conference on Bronchoalveolar Lavage Vienna: 18S.

  6. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    PubMed  CAS  Google Scholar 

  7. Burke WMJ, Roberts CM, Bryant DH, Cairns D, Yeates M, Morgan GW, Martin BJ, Blake H, Penny R, Zaunders JJ, Breit SN (1992) Smoking-induced changes in epithelial lining fluid volume, cell density, and protein. Eur Respir J 5:780–784

    PubMed  CAS  Google Scholar 

  8. Catanzaro A, Richman P, Batcher S, Hallman M (1988) Immunomodulation by pulmonary surfactant. J Lab Clin Med 112:727–734

    PubMed  CAS  Google Scholar 

  9. Reuben M Cherniack (coordinator) (1990) Bronchoalveolar lavage constituents in healthy individuals, idiopathic pulmonary fibrosis, and selected comparison groups. Am Rev Respir Dis 141:S169-S202

    Google Scholar 

  10. Crystal RG, Reynolds HY, Kalica AR (1986) Bronchoalveolar lavage. The report of an international conference. Chest 90:122–131

    Article  PubMed  CAS  Google Scholar 

  11. Davis WB, Fells GA, Sun X-H, Gadek JE, Venet A, Crystal RG (1984). Eosinophilmediated injury to lung parenchymal cells and interstitial matrix. A possible role for eosinophils in chronic inflammatory disorders of the lower respiratory tract. J Clin Invest 74:269–278

    Article  PubMed  CAS  Google Scholar 

  12. Finlay TN, Ladman AJ (1972) Low yield of pulmonary surfactant in cigarette smokers. New Engl J Med 286:223–227

    Article  Google Scholar 

  13. Gérard H, Kohler F (1982) Cytological routine analysis in alveolar washing: contribution of some technical improvements. Acta Endosc 12:411–420

    Article  Google Scholar 

  14. Hallman M, Spragg R, Harreil JH, Moser KM, Gluck L (1982) Evidence of lung surfactant abnormality in respiratory failure. J Clin Invest 70:673–683

    Article  PubMed  CAS  Google Scholar 

  15. Hoogsteden HC, van Hal PThW, Wijkhuijs JM, Hop W, Verkaik APK, Hilvering C (1991) Expression of the CDU/CD 18 cell surface adhesion glycoprotein family on alveolar macrophages in smokers and nonsmokers. Chest 100:1567–1571

    Article  PubMed  CAS  Google Scholar 

  16. Hughes DA, Haslam PL (1990) 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. Eur Respir J 3:1128–1139

    PubMed  CAS  Google Scholar 

  17. Jones KP, Edwards JH, Reynolds SP, Peters TJ, Davies BH (1990) A comparison of albumin and urea as reference markers in bronchoalveolar lavage fluid from patients with interstitial lung diseases. Eur Respir J 3:152–156

    PubMed  CAS  Google Scholar 

  18. Laughter AH, Martin RR, Twomey JJ (1977) Lymphoproliferative responses to antigens mediated by human pulmonary alveolar macrophages. J Lab Clin Med 89:1326–1331

    PubMed  CAS  Google Scholar 

  19. Lehrer SB, Wilson MR, Salvaggio JE (1978) Immunogenic properties of tobacco smoke. J Allergy Clin Immunol, 62:368–370

    Article  PubMed  CAS  Google Scholar 

  20. LeMesurier SM, Lykle WJ, Stewart BW (1980) Reduced yields of pulmonary surfactant: patterns of response following administration of chemicals to rats by inhalation. Toxicol Lett 5:89–93

    Article  CAS  Google Scholar 

  21. Lesur O, Cantin AM, Tanswell AK, Melloni B, Beaulieu JF, Begin R (1992) Silica exposure induces cytotoxicity and proliferative activity of type II pneumocytes. Exp Lung Res 18:173–190

    Article  PubMed  CAS  Google Scholar 

  22. Lesur O, Melloni B, Cantin A, Begin R (1992) Silica-exposed lung fluids have a proliferative activity for type II epithelial cells: a study on human and sheep alveolar fluids. Exp Lung Res 18:635–656

    Google Scholar 

  23. Low RB, Davis GS, Giancola MS (1978) Biochemical analyses of bronchoalveolar lavage fluids of healthy human volunteer smokers and nonsmokers. Am Rev Respir Dis 118:863–875

    PubMed  CAS  Google Scholar 

  24. Mourad W, Geha RS, Chatila T (1990) Engagement of major histocompatibility complex class II molecules induces sustained, lymphocyte function-associated molecule 1-dependent cell adhesion. J Exp Med 172:1513–1516

    Article  PubMed  CAS  Google Scholar 

  25. Moy VT, Brian AA (1992) Signaling by lymphocyte function-associated antigen 1 (LFA-1) in B cells: enhanced antigen presentation after stimulation through LFA-1. J Exp Med 175:1–7

    Article  PubMed  CAS  Google Scholar 

  26. Natali PC, De Martino C, Quaranta V (1981) Expression of la-like antigens in normal human nonlymphoid tissues. Transplantation 31:75–78

    Article  PubMed  CAS  Google Scholar 

  27. Ødum N, Yoshizumi H, Okamoto Y, Kamikawaji N, Kimura A, Nishimura Y, Sasazuki T (1992) Signal transduction by HLA class II molecules in human T cells: induction of LFA-1 dependent and independent adhesion. Human Immunol 35:71–84.

    Article  Google Scholar 

  28. Pankow W, Neumann K, Rüschoff J, Schröder R, von Wiehert P (1991) Reduction in HLA-DR antigen density on alveolar macrophages of smokers. Lung 169:255–262

    Article  PubMed  CAS  Google Scholar 

  29. Pesce MA, Strande CS (1973) A new micromethod for determination of protein in cerebrospinal fluid and urine. Clin Chem 19/11:1265–1267

    Google Scholar 

  30. Reynolds HY (1987) Bronchoalveolar lavage. Am Rev Respir Dis 135:250–263

    PubMed  CAS  Google Scholar 

  31. Reynolds HY, Chrétien J (1984) Respiratory tract fluids: analysis of content and contempory use in understanding lung disease. Dis Mon 5:1–103

    Article  Google Scholar 

  32. Rooney SA (1985) The surfactant system and lung phospholipid biochemistry. Am Rev Respir Dis 131:439–460

    PubMed  CAS  Google Scholar 

  33. Rouser G, Siakatos AN, Fleischer S (1966) Quantitative analysis of phospholipids by thin layer chromatography and phosphorus analysis of spot. Lipids 1:85–86

    Article  PubMed  CAS  Google Scholar 

  34. Schaberg T, Lauer C, Lode H, Fisher J, Haller H (1992) Increased number of alveolar macro-phages expressing adhesion molecules of the leukocyte adhesion molecule family in smoking subjects. Am Rev Respir Dis 146:1287–1293

    PubMed  CAS  Google Scholar 

  35. Springer TA (1990) Adhesion receptors of the immune system. Nature (Lond.) 346:425–427

    Article  CAS  Google Scholar 

  36. Taylor RG, Gross E, Joyce H, Holland F, Pride NB (1985) Smoking, allergy, and the differential white blood cell count. Thorax 40:17–22

    Article  PubMed  CAS  Google Scholar 

  37. Unuanue ER, Beller DI, Lu CY, Allen PM (1984) Antigen presentation: comments on its regulation and mechanisms. J Immunol 132:1–5

    Google Scholar 

  38. Warr GA (1979) The biology of normal human bronchoalveolar cells. INSERM 84:137–158

    Google Scholar 

  39. Warr GA, Martin RR, Gentry LO (1976) Alterations in pulmonary alveolar macrophages from young cigarette smokers. Bull Int Union Tuberc 51:531–537

    Google Scholar 

  40. Wilsher ML, Hughes DA, Haslam PL (1988) Immunoregulatory properties of pulmonary surfactant: influence of variations in the phospholipid profile. Clin Exp Immunol 73:117–122

    PubMed  CAS  Google Scholar 

Download references

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Mancini, N.M., Béné, M.C., Gérard, H. et al. Early Effects of Short-Time Cigarette Smoking on the Human Lung: A Study of Bronchoalveolar Lavage Fluids. Lung 171, 277–291 (1993). https://doi.org/10.1007/BF03215871

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