Skip to main content
Log in

Bronchoalveolar lavage fluid characteristics of early intermediate and late phases of ARDS

Alterations in leukocytes, proteins, PAF and surfactant components

  • Original
  • Published:
Intensive Care Medicine Aims and scope Submit manuscript

Abstract

Objective To determine the concentration of proteins and phospholipids, markers of inflammatory reaction such as platelet-activating factor (PAF), and cell alterations in bronchoalveolar lavage (BAL) fluid during the evolution of the acute respiratory distress syndrome (ARDS).

Design Prospective controlled study.

Setting 14-bed medical-surgical intensive care unit in a 750-bed university teaching hospital.

Patients 19 mechanically ventilated patients, 9 patients with ARDS and 10 patients without cardiopulmonary disease (controls), were eligible for this study.

Interventions BAL was performed during the early, intermediate, and late phases of ARDS.

Measurements and results Total phospholipids and individual phospholipid classes of the surfactant, proteins, PAF, and cells were measured. High levels of PAF, an increase in neutrophils and proteins, and quantitative as well as qualitative alterations in phospholipids in BAL fluid were observed in ARDS patients compared to the control group. PAF, proteins, and neutrophils were higher in early ARDS than in intermediate or late ARDS. The surfactant pool increased in the early phase and decreased in the intermediate or late phase of the syndrome. The qualitative alterations of surfactant consist of reduced phospholipid content in the surfactant structures with good surface properties; moreover, there was a considerable decrease in the percentage of phosphatidylcholine and phosphatidylglycerol, followed by an increase in phosphatidylethanolamine, phosphatidylserine, phosphatidylinositol, and sphingomyelin in all three phases of ARDS compared to the control group. Lysophosphatidylcholine was detectable only in late ARDS.

Conclusion Total surfactant phospholipids, surfactant components, and inflammatory markers such as PAF, cells, and proteins were affected in patients with ARDS. These factors, undergoing quantitative alterations during the course of ARDS, could have a significant role in the pathogenesis and evolution of ARDS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bernard GR, Artigas BA, Brigham KL, Carlet J, Falke K, Hudson L, Lamy M, Legall JR, Morris A, Spragg R, the Consensus Committee (1994) The American-European Consensus Conference on ARDS. Am J Respir Crit Care Med 149: 818–824

    PubMed  CAS  Google Scholar 

  2. Rinaldo JE (1986) Mediation of ARDS by leukocytes. Clinical evidence and implication for therapy. Chest 89: 590–593

    Article  PubMed  CAS  Google Scholar 

  3. Suter PM, Suter S, Girardin E, Roux-Lombard P, Grau G, Dayer JM (1992) High bronchoalveolar level of tumor necrosis factor and its inhibitors, interleukin-1, interferon, and elastase, in patients with adult respiratory distress syndrome after trauma, shock, or sepsis. Am J Respir Crit Care Med 145:1016–1022

    CAS  Google Scholar 

  4. Martin C, Parazian L, Payan MJ, Saux P, Goutin F (1995) Pulmonary fibrosis correlates with outcome in adult respiratory distress syndrome. Chest 107:196–200

    Article  PubMed  CAS  Google Scholar 

  5. Voelkel NF, Stenmark KR, Reeves JT, Mathias MM, Murphy RC (1982) Non-immunologic production of leukotrienes induced by platelet-activating factor. Science 218: 286–288

    Article  PubMed  CAS  Google Scholar 

  6. Smith CS, Parker L, Shearer WT (1994) Cytokine regulation by platelet-activating factor in a human B cell line. J Immunol 153:3997–4005

    PubMed  CAS  Google Scholar 

  7. Tarbet EB, Stafforini DM, Elstad MR, Zimmerman GA, Mclntyre TM, Prescott SM (1991) Liver cells secrete the plasma form of platelet-activating factor acetylhydrolase. J Biol Chem 266: 16667–16673

    PubMed  CAS  Google Scholar 

  8. Johansson J, Curstedt T, Robertson B (1994) The protein of the surfactant system. Eur Respir J 7: 372–391

    Article  PubMed  CAS  Google Scholar 

  9. Van Golde LMG, Batenburg JJ, Robertson B (1988) The pulmonary surfactant system. Physiol Rev 68: 374–455.

    PubMed  Google Scholar 

  10. Fukuda Y, Ishizaki M, Masuda Y, Kimura G, Kawanami O, Masugi Y (1987) The role of intraalveolar fibrosis in the process of pulmonary structural remodelling in patients with diffuse alveolar damage. Am J Pathol 126:171–182

    PubMed  CAS  Google Scholar 

  11. Chestnutt AN, Matthay MA, Tibayan FA, Clark JG (1997) Early detection of type III procollagen peptide in acute lung injury. Am J Resp Crit Care Med 156:840–845

    Google Scholar 

  12. Murray JF, Matthay MA, Luce J (1988) An expanded definition of adult respiratory distress syndrome. Am J Respir Crit Care Med l38:720–724

    Google Scholar 

  13. Nakos G, Pneumatikos J, Tsangaris H, Telis K, Lekka ME (1997) Protein and phospholipids in BAL from patients with hydrostatic pulmonary edema. Am J Respir Crit Care Med 155: 945–951

    PubMed  CAS  Google Scholar 

  14. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275

    PubMed  CAS  Google Scholar 

  15. Doumas BT, Biggs HG (1972) Determination of serum albumin. In Cooper GA (ed) Standard methods of clinical chemistry, vol 1. Academic Press, New York, p 175

    Google Scholar 

  16. 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 

  17. Bartlett GR (1959) Phosphorus assays in column chromatography. J Biol Chem 234:466–468

    PubMed  CAS  Google Scholar 

  18. Bossant M-J, Ninio E, Delautier D, Benveniste J (1990) Bioassay of paf-acether by rabbit platelet aggregation. In Murphy RC, Fitzpatrick FA (eds) Methods Enzymol 187:125–130

    Article  PubMed  CAS  Google Scholar 

  19. Tselepis AD, Lekka ML, Tsoukatos DA (1991) PAF-acetyhydrolase activity in tetrahymena puriformis cells. FEBS Lett 288:147–150

    Article  PubMed  CAS  Google Scholar 

  20. Goodman RB, Strieter RM, Martin DP, Steinberg KP, Milberg JA, Maunder RJ, Kunkel SL, Walz A, Hudson LD, Martin TR (1996) Inflammatory cytokines in patients with persistence of the acute respiratory distress syndrome. Am J Respir Crit Care Med 154: 602–611

    PubMed  CAS  Google Scholar 

  21. Steinberg KP, Milberg JA, Martin TR, Maunder RJ, Cockrill BA, Hudson LD (1994) Evolution of bronchoalveolar cells populations in adult respiratory distress syndrome. Am J Respir Crit Care Med 150:113–122

    PubMed  CAS  Google Scholar 

  22. Von Wiehert P, Joseph K, Muller B, Frank WM (1993) Bronchoalveolar lavage. Quantification of intraalveolar fluid. Am J Respir Crit Care Med 147: 148–152

    Google Scholar 

  23. Marcy TW, Merrill WW, Rancin JA, Reynolds HV (1987) Limitations of using urea to quantify epithelial fluid recovered by bronchoalveolar lavage. Am J Respir Crit Care Med 135: 1276–1280

    CAS  Google Scholar 

  24. Pittet JF, Mackersie RC, Martin TR, Matthay MA (1997) Biological markers of acute lung injury: prognostic and pathogenetic significance. Am J Respir Crit Care Med 155:1187–1205

    PubMed  CAS  Google Scholar 

  25. Matthay MA, Berthiaume Y, Staub NC (1985) Long-term clearance of liquid and protein of unanesthetized sheep. J Appl Physiol 59: 928–934

    PubMed  CAS  Google Scholar 

  26. Stremler KE, Stafforini DM, Prescott SM, Mclntyre TM (1991) Human plasma platelet-activating factor acetylhydrolase. J Biol Chem 266:11095–11103

    PubMed  CAS  Google Scholar 

  27. Evans TW, Chung KF, Rogers DF, Barnes PJ (1987) Effect of platelet-activating factor on airway vascular permeability: possible mechanism. J Appl Physiol 63: 479–484

    PubMed  CAS  Google Scholar 

  28. Sakai A, Chang S, Voelkel NF (1989) Importance of vasoconstriction in lipid mediator-induced pulmonary edema. J Appl Physiol 66: 2667–2674

    Article  PubMed  CAS  Google Scholar 

  29. Matsumoto K, Taki F, Yasuhiro Y, Taniguchi H, Takagi K (1992) Platelet-activating factor in bronchoalveolar lavage fluid of patients with adult respiratory distress syndrome. Clin Exp Pharmacol Physiol 19: 509–515

    Article  PubMed  CAS  Google Scholar 

  30. Windsor ACJ, Walsh CJ, Mullen PG, Cook DJ, Fisher BJ, Blocher CR, Leeper-Woodford SK, Sugerman HJ, Fowler AA (1993) Tumor necrosis factor-α blockade prevents neutrophil CD18 receptor upregulation and attenuates acute lung injury in porcine sepsis without inhibition of neutrophil oxygen radical generation. J Clin Invest 91: 1459–1468

    Article  PubMed  CAS  Google Scholar 

  31. Harada A, Sekido N, Akasoshi T, Wada T, Mukaida N, Matsushina K (1994) Essential involvement of interleukin-8 in acute inflammation. J Leukoc Biol 56: 559–564

    PubMed  CAS  Google Scholar 

  32. Haslam PL, Turton CWG, Lukoszek A, Salsbury AJ, Dewar A, Collins JV, Turner-Warwick M (1980) Bronchoalveolar lavage fluid cell counts in cryptogenic fibrosing alveolitis and their relation to therapy. Thorax 35: 328–339

    Article  PubMed  CAS  Google Scholar 

  33. Gregory TJ, Longmore WJ, Moxley MA, Whitsett JA, Reed CR, Fowler AA, Hudson LD, Maunder RJ, Crim C, Myers TM (1991) Surfactant chemical composition and biophysical activity in acute respiratory distress syndrome. J Clin Invest 65:1976–1981

    Article  Google Scholar 

  34. Pison U, Seeger W, Buchhorn R, Jokat R, Brand M, Obertacke U, Neuhof H, Schmit-Neuerburg K-P (1989) Surfactant abnormalities in patients with respiratory failure after multiple trauma. Am J Respir Crit Care Med 140: 1033–1039

    CAS  Google Scholar 

  35. Clander A, Fisher AB (1990) Regulation of lung surfactant secretion. Am J Physiol 258:L241-L251

    Google Scholar 

  36. Wright JR, Dodds LG (1991) Regulation of pulmonary surfactant secretion and clearance. Annu Rev Physiol 53: 395–414

    Article  PubMed  CAS  Google Scholar 

  37. Oyarzun MJ, Clements JA (1978) Control of lung surfactant by ventilation, adrenergic mediators and prostaglandins in the rabbit. Am J Respir Crit Care Med 117: 879–891

    CAS  Google Scholar 

  38. Frankel RA, Narahara H, Eguchi H, Toyoshima K, Johnston JM (1993) Metabolism of hexadecanol by rat type II pneumonocytes. Biochem Biophys Res Commun 196: 885–891

    Article  Google Scholar 

  39. Kikkawa Y, Smith F (1983) Cellular and biochemical aspects of pulmonary surfactant in health and disease. Lab Invest 49:122–139

    PubMed  CAS  Google Scholar 

  40. Veldhuizen RAW, McCaig LA, Akino T, Lewis JF (1995) Pulmonary surfactant subfractions in patients with the acute respiratory distress syndrome. Am J Respir Crit Care Med 152:1867–1871

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. Nakos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nakos, G., Kitsiouli, E.I., Tsangaris, I. et al. Bronchoalveolar lavage fluid characteristics of early intermediate and late phases of ARDS. Intensive Care Med 24, 296–303 (1998). https://doi.org/10.1007/s001340050571

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s001340050571

Key words

Navigation