Skip to main content
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 1993;71(3):177–190. doi: 10.1007/BF00180100

Alveolar surfactant and adult respiratory distress syndrome

Pathogenetic role and therapeutic prospects

W Seeger 1, A Günther 1, H D Walmrath 1, F Grimminger 1, H G Lasch 1
PMCID: PMC7096084  PMID: 8481620

Summary

The adult respiratory distress syndrome (ARDS) is characterized by extended inflammatory processes in the lung microvascular, interstitial, and alveolar compartments, resulting in vasomotor disturbances, plasma leakage, cell injury, and complex gas exchange disturbances. Abnormalities in the alveolar surfactant system have long been implicated in the pathogenetic sequelae of this life-threatening syndrome. This hypothesis is supported by similarities in pulmonary failure between patients with ARDS and preterm babies with infant respiratory distress syndrome, known to be triggered primarily by lack of surfactant material. Mechanisms of surfactant alterations in ARDS include: (a) lack of surface-active compounds (phospholipids, apoproteins) due to reduced generation/release by diseased pneumocytes or to increased loss of material (this feature includes changes in the relative composition of the surfactant phospholipid and/or apoprotein profiles); (b) inhibition of surfactant function by plasma protein leakage (inhibitory potencies of different plasma proteins have been defined); (c) “incorporation” of surfactant phospholipids and apoproteins into polymerizing fibrin upon hyaline membrane formation; and (d) damage/inhibition of surfactant compounds by inflammatory mediators (proteases, oxidants, nonsurfactant lipids). Alterations in alveolar surfactant function may well contribute to a variety of pathophysiological key events encountered in ARDS. These include decrease in compliance, ventilation-perfusion mismatch including shunt flow due to altered gas flow distribution (atelectasis, partial alveolar collapse, small airway collapse), and lung edema formation. Moreover, more speculative at the present time, surfactant abnormalities may add to a reduction in alveolar host defense competence and an upregulation of inflammatory events under conditions of ARDS. Persistent atelectasis of surfactant-deficient and in particular fibrin-loaded alveoli may represent a key event to trigger fibroblast proliferation and fibrosis in late ARDS (“collapse induration”). Overall, the presently available data on surfactant abnormalities in ARDS lend credit to therapeutic trials with transbronchial surfactant administration. In addition to the classical goals of replacement therapy defined for preterm infants (rapid improvement in lung compliance and gas exchange), this approach will have to consider its impact on host defense competence and inflammatory and proliferative processes when applied in adults with respiratory failure.

Key words: Adult respiratory distress syndrome, Alveolar surfactant, Surfactant phospholipids, Surfactant apoproteins, Surfactant inhibition, Hyaline membranes

Abbreviations

ARDS

adult respiratory distress syndrome

IRDS

infant respiratory distrss syndrome

PC

phosphatidylcholine

PG

phosphatidylglycerol

PE

phosphatidylethanolamine

PS

phosphatidylserine

PI

phosphatidylinositol

Sph

spingomyelin

BAL

bronchoalveolar lavage

TNF

tumor necrosis factor

References

  • 1.Albert RK, Lakshminarayan S, Hildebrandt J, Kirk W. Increased surface tension favours pulmonary edema formation in anaesthetized dogs' lungs. J Clin Invest. 1979;63:1015–1018. doi: 10.1172/JCI109369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Allen JN, Herzyk DJ, Wewers MD. Surfactant suppresses interleukin-1 β and tumor necrosis factor-α release by human alveolar macrophages. Am Rev Respir Dis. 1992;145:A875. [Google Scholar]
  • 3.Ansfield MJ, Benson BJ. Identification of the immunosuppressive components of canine pulmonary surface active material. J Immunol. 1980;125:1093–1098. [PubMed] [Google Scholar]
  • 4.Ansfield MJ, Kaltreider HB, Benson BJ, Caldwell JL. Immunosuppressive activity of canine pulmonary surface active material. J Immunol. 1980;122:1062–1066. [PubMed] [Google Scholar]
  • 5.Ansfield MJ, Kaltreider HB, Benson NJ, Shalaby MR. Canine surface active material and pulmonary lymphocyte function studies with mixed-lymphocyte culture. Exp Lung Res. 1980;1:3–11. doi: 10.3109/01902148009057508. [DOI] [PubMed] [Google Scholar]
  • 6.Bachofen M, Weibel EF. Structural alterations of lung parenchyma in the adult respiratory distress syndrome. Clin Chest Med. 1982;3:35–56. [PubMed] [Google Scholar]
  • 7.Balis JU, Shelley SA, McCue MJ, Rappaport ES. Mechanisms of damage to the lung surfactant system. Ultrastructure and quantitation of normal and in vitro inactivated lung surfactant. Exp Mol Pathol. 1971;14:243–262. doi: 10.1016/0014-4800(71)90069-4. [DOI] [PubMed] [Google Scholar]
  • 8.Berggren P, Lachmann B, Curstedt T, Grossmann G, Robertson B. Gas exchange and lung morphology after surfactant replacement in experimental adult respiratory distress syndrome induced by repeated lung lavage. Acta Anaesthesiol Scand. 1986;30:321–328. doi: 10.1111/j.1399-6576.1986.tb02423.x. [DOI] [PubMed] [Google Scholar]
  • 9.Berry D, Ikegami M, Jobe A. Respiratory distress and surfactant inhibition following vagotomy in rabbits. J Appl Physiol. 1986;61:1741–1748. doi: 10.1152/jappl.1986.61.5.1741. [DOI] [PubMed] [Google Scholar]
  • 10.Bertozzi P, Astedt B, Zenzius L, Lynch K, LeMaire F, Zapol W, Chapman H. Depressed bronchoalveolar urokinase activity in patients with adult respiratory distress syndrome. N Engl J Med. 1990;322:890–897. doi: 10.1056/NEJM199003293221304. [DOI] [PubMed] [Google Scholar]
  • 11.Bredenberg CE, Paskanik AM, Nieman GF. High surface tension pulmonary edema. J Surg Res. 1983;34:515–523. doi: 10.1016/0022-4804(83)90104-x. [DOI] [PubMed] [Google Scholar]
  • 12.Burkhardt A. Alveolitis and collapse in the pathogenesis of pulmonary fibrosis. Am Rev Respir Dis. 1989;140:513–524. doi: 10.1164/ajrccm/140.2.513. [DOI] [PubMed] [Google Scholar]
  • 13.Chapman HA, Allen CL, Stone L. Abnormalities in pathways of alveolar fibrin turnover among patients with interstitiell lung disease. Am Rev Respir Dis. 1986;133:437–443. doi: 10.1164/arrd.1986.133.3.437. [DOI] [PubMed] [Google Scholar]
  • 14.Chapman HA, Reilly JJ, Kobzik L. Role of plasminogen activator in degradation of extracellular matrix protein by live human alveolar macrophages. Am Rev Respir Dis. 1988;137:412–419. doi: 10.1164/ajrccm/137.2.412. [DOI] [PubMed] [Google Scholar]
  • 15.Chapman HA, Bertozzi P, Sailor LZ, Nusrat AR. Alveolar macrophage urokinase receptors localize enzyme activity to the cell surface. Am J Physiol. 1990;259:L432–L438. doi: 10.1152/ajplung.1990.259.6.L432. [DOI] [PubMed] [Google Scholar]
  • 16.Christner P, Fein A, Goldberg S, Lippmann M, Abrams W, Weinbaum G. Collagenase in the lower respiratory tract of patients with adult respiratory distress syndrome. Am Rev Respir Dis. 1985;131:690–695. doi: 10.1164/arrd.1985.131.5.690. [DOI] [PubMed] [Google Scholar]
  • 17.Cochrane CG, Spragg R, Revak SD. Pathogenesis of the adult respiratory distress syndrome. J Clin Invest. 1983;71:754–761. doi: 10.1172/JCI110823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Cockshutt AM, Possmayer F. Lysophosphatidylcholine sensitizes lipid extracts of pulmonary surfactant to inhibition by serum proteins. Biochim Biophys Acta. 1991;1086:63–71. doi: 10.1016/0005-2760(91)90155-b. [DOI] [PubMed] [Google Scholar]
  • 19.Cockshutt AM, Weitz J, Possmayer F. Pulmonary surfactant-associated protein A enhances the surface activity of lipid extract surfactant and reverses inhibition by blood proteins in vitro. Biochemistry. 1990;29:8424–8429. doi: 10.1021/bi00488a032. [DOI] [PubMed] [Google Scholar]
  • 20.Coonrod JD, Yoneda K. Detection and partial characterization of antibacterial factor(s) in alveolar lining material of rats. J Clin Invest. 1981;71:129–141. doi: 10.1172/JCI110741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Coonrod JD, Lester RL, Chi Hsu L. Characterization of the extracellular bactericidal factors of rat alveolar lining material. J Clin Invest. 1984;74:1269–1279. doi: 10.1172/JCI111537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Collaborative European Multicenter Study Group Surfactant replacement therapy for severe neonatal respiratory distress syndrome: an international randomized clinical trial. Pediatrics. 1988;82:683–691. [PubMed] [Google Scholar]
  • 23.Crouch E, Rust K, Marienchek W, Parghi D, Chang D, Persson A. Developmental expression of pulmonary surfactant protein D (SP-D) Am J Respir Cell Mol Biol. 1991;5:13–18. doi: 10.1165/ajrcmb/5.1.13. [DOI] [PubMed] [Google Scholar]
  • 24.Egan EA, Notter RN, Kwong MS, Shapiro DL. Natural and artificial lung surfactant replacement therapy in premature lambs. J Appl Physiol. 1983;55:875–883. doi: 10.1152/jappl.1983.55.3.875. [DOI] [PubMed] [Google Scholar]
  • 25.Evander E, Wollmer P, Jonson B, Lachmann B. Pulmonary clearance of inhaled 99mTc-DTPA: effects of surfactant depletion by lung lavage. J Appl Physiol. 1987;62:1611–1614. doi: 10.1152/jappl.1987.62.4.1611. [DOI] [PubMed] [Google Scholar]
  • 26.Froh D, Ballard PL, Williams MC, Gonzales J, Goerke J, Odom MW, Gonzales LW. Lamellar bodies of cultured human fetal lung: content of surfactant protein A (SP-A), surface film formation and structural transformation in vitro. Biochim Biophys Acta. 1990;1052:78–89. doi: 10.1016/0167-4889(90)90060-q. [DOI] [PubMed] [Google Scholar]
  • 27.Fuchimukai T, Fuchiwara T, Takahashi A, Enhorning G. Artificial pulmonary surfactant inhibited by proteins. J Appl Physiol. 1987;62:429–437. doi: 10.1152/jappl.1987.62.2.429. [DOI] [PubMed] [Google Scholar]
  • 28.Goerke J, Clements JA. Alveolar surface tension and lung surfactant. In: Macklem PT, Mead J, editors. Handbook of physiology. Bethesda: American Physiological Society; 1986. pp. 247–261. [Google Scholar]
  • 29.Gregory TJ, Longmore WJ, Moxlcy MA, Whitsett JA, Reed CR, Fowler AA, Hudson LD, Maunder RJ, Crim C, Hyers TM. Surfactant chemical composition and biophysical activity in acute respiratory distress syndrome. J Clin Invest. 1991;88:1976–1981. doi: 10.1172/JCI115523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Grimminger F, Becker G, Seeger W. High yield enzymatic conversion of intravascular leukotriene A4 in blood-free perfused lungs. J Immunol. 1988;141:2431–2436. [PubMed] [Google Scholar]
  • 31.Grimminger F, Menger M, Becker G, Seeger W. Potentiation of leukotriene generation following sequestration of neutrophils in isolated lungs. Blood. 1988;72:1687–1692. [PubMed] [Google Scholar]
  • 32.Grimminger F, Kreusler B, Schneider U, Becker G, Seeger W. Influence of microvascular adherence on neutrophil leukotriene generation - evidence for cooperative eicosanoid synthesis. J Immunol. 1990;144:1866–1872. [PubMed] [Google Scholar]
  • 33.Grimminger F, Kreusler B, Schneider U, von Witzleben E, Walmrath D, Neppert J, Seeger W. Human leukoagglutinating antibody evokes cooperative leukotriene synthesis in pulmonary microvasculature - model of transfusion-related acute lung injury (TRALI) Circ Res. 1991;68:503–512. doi: 10.1161/01.res.68.2.503. [DOI] [PubMed] [Google Scholar]
  • 34.Grimminger F, Sibelius U, Seeger W. Amplification of LTB4 generation in AM-PMN cocultures: transcellular 5-lipoxygenase metabolism. Am J Physiol. 1991;261:L195–L203. doi: 10.1152/ajplung.1991.261.2.L195. [DOI] [PubMed] [Google Scholar]
  • 35.Grimminger F, von Kürten I, Walmrath D, Seeger W. Type II alveolar epithelial eicosanoid metabolism — predominance of cyclooxygenase pathways, and transcellular lipoxygenase metabolism in co-culture with neutrophils. Am J Respir Cell Mol Biol. 1992;6:9–16. doi: 10.1165/ajrcmb/6.1.9. [DOI] [PubMed] [Google Scholar]
  • 36.Gross TJ, Simon RH, Sitrin RG. Tissue factor procoagulant expression by rat alveolar epithelial cells. Am J Respir Cell Mol Biol. 1992;6:397–403. doi: 10.1165/ajrcmb/6.4.397. [DOI] [PubMed] [Google Scholar]
  • 37.Hall SB, Venkitaraman AR, Whitsett JA, Holm BA, Notter RH. Importance of hydrophobic apoproteins as constituents of clinical exogenous surfactants. Am Rev Respir Dis. 1992;145:24–30. doi: 10.1164/ajrccm/145.1.24. [DOI] [PubMed] [Google Scholar]
  • 38.Hallman M. Lung surfactant in respiratory distress syndrome. Acta Anaesthesiol Scand. 1991;35(Suppl 95):15–21. doi: 10.1111/j.1399-6576.1991.tb03395.x. [DOI] [PubMed] [Google Scholar]
  • 39.Hallman M, Spragg R, Harrell JH, Moser KM, Gluck L. Evidence of lung surfactant abnormality in respiratory failure. J Clin Invest. 1982;70:673–683. doi: 10.1172/JCI110662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Hallman M, Maasilta P, Kivisaari L, Mattson K. Changes in surfactant in bronchoalveolar lavage fluid after hemithorax irradiation in patients with mesothelioma. Am Rev Respir Dis. 1990;141:998–1005. doi: 10.1164/ajrccm/141.4_Pt_1.998. [DOI] [PubMed] [Google Scholar]
  • 41.Hamm H, Fabel H, Bartsch W. The surfactant system of the adult lung: physiology and clinical perspectives. Clin Investig. 1992;70:637–657. doi: 10.1007/BF00180279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Hawwood JL. Lung surfactant. Prog Lipid Res. 1987;26:211–256. doi: 10.1016/0163-7827(87)90004-x. [DOI] [PubMed] [Google Scholar]
  • 43.Hasday JD, Bachwich PR, Lynch JP, Sitrin RG. Procoagulant and plasminogen activator activities of bronchoalveolar fluid in patients with pulmonary sarcoidosis. Exp Lung Res. 1988;14:261–278. doi: 10.3109/01902148809115128. [DOI] [PubMed] [Google Scholar]
  • 44.Hasleton PS. Adult respiratory distress syndrome: a review. Histopathology. 1983;7:037–332. doi: 10.1111/j.1365-2559.1983.tb02247.x. [DOI] [PubMed] [Google Scholar]
  • 45.Hasleton PS. The lung parenchyma in burns. Histopathology. 1983;7:333–347. doi: 10.1111/j.1365-2559.1983.tb02248.x. [DOI] [PubMed] [Google Scholar]
  • 46.Hawgood S. Pulmonary surfactant apoproteins: a review of protein and genomic structure. Am J Physiol. 1989;257:L13–L22. doi: 10.1152/ajplung.1989.257.2.L13. [DOI] [PubMed] [Google Scholar]
  • 47.Hawgood S, Benson BJ, Schilling J, Damm D, Clements JA, White RT. Nucleotide and amino acid sequences of pulmonary surfactant protein SP 18 and evidence for cooperation between SP 18 and SP 28–36 in surfactant lipid adsorption. Proc Natl Acad Sci USA. 1987;84:66–70. doi: 10.1073/pnas.84.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Hayakawa H, Myrvik QN, St. Clair RW. Pulmonary surfactant inhibits priming of rabbit alveolar macrophages. Am Rev Respir Dis. 1989;140:1390–1397. doi: 10.1164/ajrccm/140.5.1390. [DOI] [PubMed] [Google Scholar]
  • 49.Hennes HM, Lee MB, Rimm AA, Shapiro DL. Surfactant replacement therapy in respiratory distress syndrome. Am J Dis Child. 1991;145:102–104. doi: 10.1001/archpedi.1991.02160010108027. [DOI] [PubMed] [Google Scholar]
  • 50.Holm BA, Notter RH. Effects of hemoglobin and cell membrane lipids on pulmonary surfactant activity. J Appl Physiol. 1987;63:1434–1442. doi: 10.1152/jappl.1987.63.4.1434. [DOI] [PubMed] [Google Scholar]
  • 51.Holm BA, Notter RH, Finkelstein JN. Surface property changes from interactions of albumin with natural lung surfactant and extracted lung lipids. Chem Phys Lipids. 1985;38:287–298. doi: 10.1016/0009-3084(85)90022-2. [DOI] [PubMed] [Google Scholar]
  • 52.Holm BA, Venkitaraman AR, Enhorning G, Notter RH. Biophysical inhibition of synthetic lung surfactants. Chem Phys Lipids. 1990;52:243–250. doi: 10.1016/0009-3084(90)90120-g. [DOI] [PubMed] [Google Scholar]
  • 53.Holm BA, Keicher L, Liu M, Sokolowski J, Enhorning G. Inhibition of pulmonary surfactant function by phospholipases. J Appl Physiol. 1991;71:317–321. doi: 10.1152/jappl.1991.71.1.317. [DOI] [PubMed] [Google Scholar]
  • 54.Huang YC, Fawcett TA, Moon RE, Fracia PJ, Simonson SG, Sane AC, Piantadosi CA, Young SL. Exogenous surfactant treatment improves VA/Q abnormalities in hyperoxic lung injury. Am Rev Respir Dis. 1992;145:A609. [Google Scholar]
  • 55.Idell S, Gonzalez KK, Bradford H, MacArthur CK, Fein AM, Maunder RJ, Garcia JGN, Griffith DE, Weiland J, Martin TR, McLarty J, Fair DS, Walsh PN, Colman RW. Procoagulant activity in bronchoalveolar lavage in the adult respiratory distress syndrome. Am Rev Respir Dis. 1987;136:1466–1474. doi: 10.1164/ajrccm/136.6.1466. [DOI] [PubMed] [Google Scholar]
  • 56.Idell S, Gonzalez KK, MacArthur CK, Gillies C, Walsh PN, McLarty J, Thrall RS. Bronchoalveolar lavage procoagulant activity in bleomycin induced lung injury in marmosets. Am Rev Respir Dis. 1987;136:124–133. doi: 10.1164/ajrccm/136.1.124. [DOI] [PubMed] [Google Scholar]
  • 57.Idell S, Peterson BT, Gonzalez KK, Gray LD, Bach R, McLarty J, Fair DS. Local abnormalities of coagulation and fibrinolysis and alveolar fibrin deposition in sheep with oleic acid-induced lung injury. Am Rev Respir Dis. 1988;138:1282–1294. doi: 10.1164/ajrccm/138.5.1282. [DOI] [PubMed] [Google Scholar]
  • 58.Idell S, James KK, Gillies C, Fair DS, Thrall RS. Abnormalities of pathways of fibrin turnover in lung lavage of rats with oleic acid and bleomycin-induced lung injury support alveolar fibrin deposition. Am J Pathol. 1989;135:387–399. [PMC free article] [PubMed] [Google Scholar]
  • 59.Idell S, James KK, Levin EG, Schwartz BS, Manchanda N, Maunder RJ, Martin TR, McLarty J, Fair DS. Local abnormalities in coagulation and fibrinolytic pathways predispose to alveolar fibrin deposition in the adult respiratory distress syndrome. J Clin Invest. 1989;84:695–705. doi: 10.1172/JCI114217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Idell S, Peters J, James KK, Fair DS, Coalson JJ. Local abnormalities of coagulation and fibrinolytic pathways that promote alveolar fibrin deposition in the lungs of baboons with diffuse alveolar damage. J Clin Invest. 1989;84:181–193. doi: 10.1172/JCI114139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Idell S, Koenig KB, Fair DS, Martin TR, McLarty J, Maunder RJ. Serial abnormalities of fibrin turnover in evolving adult respiratory distress syndrome. Am J Physiol. 1991;261:L240–L248. doi: 10.1152/ajplung.1991.261.4.L240. [DOI] [PubMed] [Google Scholar]
  • 62.Ikegami M, Agata Y, Elkady T, Hallman M, Berry D, Jobe A. Comparison of four surfactants: in vitro surface properties and responses of preterm lambs to treatment at birth. Pediatrics. 1987;79:39–46. [PubMed] [Google Scholar]
  • 63.Ikegami M, Jobe AH, Tabor BL, Rider ED, Lewis JF. Lung albumin recovery in surfactant-treated preterm ventilated lambs. Am Rev Respir Dis. 1992;145:1005–1008. doi: 10.1164/ajrccm/145.5.1005. [DOI] [PubMed] [Google Scholar]
  • 64.van Iwaarden JF, Welmers B, Verhoef J, Haagsman HP, van Golde LMG. Pulmonary surfactant protein A enhances the host-defense mechanism of rat alveolar macrophages. Am J Respir Cell Mol Biol. 1990;2:91–98. doi: 10.1165/ajrcmb/2.1.91. [DOI] [PubMed] [Google Scholar]
  • 65.van Iwaarden JF, van Strijp JAG, Erbskamp MJM, Welmers AC, Verhoef J, van Golde LMG. Surfactant protein A is opsonin in phagocytosis of herpes simplex virus type 1 by rat alveolar macrophages. Am J Physiol. 1991;261:L204–L209. doi: 10.1152/ajplung.1991.261.2.L204. [DOI] [PubMed] [Google Scholar]
  • 66.van Iwaarden JF, Shimizu H, van Golde PHM, Voelker DR, van Golde LMG. Rat surfactant protein D enhances the production of oxygen radicals by rat alveolar macrophages. Biochem J. 1992;286:5–8. doi: 10.1042/bj2860005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.Jackson LK. Idiopathic pulmonary fibrosis. Clin Chest Med. 1982;3:579–592. [PubMed] [Google Scholar]
  • 68.Jefferies AL, Coates G, O'Brodovich H. Pulmonary epithelial permeability in hyaline-membrane disease. N Engl J Med. 1984;311:1075–1080. doi: 10.1056/NEJM198410253111703. [DOI] [PubMed] [Google Scholar]
  • 69.Joka T, Obertacke U. Neue medikamentöse Behandlung im ARDS: Effekt einer intrabronchialen xenogenen Surfactantapplikation. Z Herz- Thorax- Gefäßchirurgie. 1989;3:21–24. [Google Scholar]
  • 70.Kaneko T, Sato T, Katsuya H, Miyauchi Y. Surfactant therapy for pulmonary edema due to intratracheally injected bile acid. Crit Care Med. 1990;18:77–83. doi: 10.1097/00003246-199001000-00017. [DOI] [PubMed] [Google Scholar]
  • 71.King RJ, MacBeth MC. Interaction of the lipid and protein components of pulmonary surfactant. Role of phosphatidylglycerol and calcium. Biochim Biophys Acta. 1981;647:159–168. doi: 10.1016/0005-2736(81)90242-x. [DOI] [PubMed] [Google Scholar]
  • 72.Kobayashi T, Ganzuka M, Taniguchi J, Nitta K, Murakami S. Lung lavage and surfactant replacement for hydrochloric acid aspiration in rabbits. Acta Anaesthesiol Scand. 1990;34:216–221. doi: 10.1111/j.1399-6576.1990.tb03073.x. [DOI] [PubMed] [Google Scholar]
  • 73.Kobayashi T, Nitta K, Ganzuka M, Inui S, Grossmann G, Robertson B. Inactivation of exogenous surfactant by pulmonary edema fluid. Pediatr Res. 1991;29:353–356. doi: 10.1203/00006450-199104000-00005. [DOI] [PubMed] [Google Scholar]
  • 74.Kuroki Y, Mason R, Voelker D. Pulmonary surfactant apoprotein A structure and modulation of surfactant secretion by rat alveolar type II cells. J Biol Chem. 1988;263:3388–3394. [PubMed] [Google Scholar]
  • 75.Lamm WJE, Albert RK. Surfactant replacement improves lung recoil in rabbit lungs after acid aspiration. Am Rev Respir Dis. 1990;142:1279–1283. doi: 10.1164/ajrccm/142.6_Pt_1.1279. [DOI] [PubMed] [Google Scholar]
  • 76.Lee CT, Fein AM, Lippmann M, Holtzman H, Kimbel P, Weinbaum G. Elastolytic activity in pulmonary lavage fluid from patients with adult respiratory distress syndrome. N Engl J Med. 1981;304:192–196. doi: 10.1056/NEJM198101223040402. [DOI] [PubMed] [Google Scholar]
  • 77.Lewis JF, Ikegami M, Higuchi R, Jobe A, Absolom D. Nebulized vs. instilled exogenous surfactant in an adult injury model. J Appl Physiol. 1991;71:1270–1276. doi: 10.1152/jappl.1991.71.4.1270. [DOI] [PubMed] [Google Scholar]
  • 78.Lewis JF, Ikegami M, Jobe AH. Metabolism of exogenously administered surfactant in the acutely injured lungs of adult rabbits. Am Rev Respir Dis. 1992;145:19–23. doi: 10.1164/ajrccm/145.1.19. [DOI] [PubMed] [Google Scholar]
  • 79.Nakstadt B, Boye NP, Lyberg T. Procoagulant activities in human alveolar macrophages. Eur J Respir Dis. 1987;71:459–471. [PubMed] [Google Scholar]
  • 80.Nakstad B, Lydberg T, Skjonsberg OH, Boye NP. Local activation of the coagulation and fibrinolysis systems in lung disease. Thromb Res. 1990;57:827–838. doi: 10.1016/0049-3848(90)90150-b. [DOI] [PubMed] [Google Scholar]
  • 81.Nieman GF, Bredenberg CE. High surface tension pulmonary edema induced by detergent aerosol. J Appl Physiol. 1985;58:129–136. doi: 10.1152/jappl.1985.58.1.129. [DOI] [PubMed] [Google Scholar]
  • 82.Nieman GF, Goyette D, Paskanik A, Brendenberg C. Surfactant displacement by plasma lavage results in pulmonary edema. Surgery. 1990;107:677–683. [PubMed] [Google Scholar]
  • 83.Notter RH, Shaprio DL, Ohning B, Whitsett JA. Biophysical activity of synthetic phospholipids combined with purified lung surfactant 6000 dalton apoprotein. Chem Phys Lipids. 1987;44:1–17. doi: 10.1016/0009-3084(87)90002-8. [DOI] [PubMed] [Google Scholar]
  • 84.O'Brodovich HM, Weitz JI, Possmayer F. Effect of fibrinogen degradation products and lung ground substance on surface function. Biol Neonate. 1990;57:325–333. doi: 10.1159/000243209. [DOI] [PubMed] [Google Scholar]
  • 85.Persson A, Chang D, Rust K, Moxley M, Longmore W, Crouch E. Purification and biochemical characterization of CP4 (SP-D), a collagenous surfactant-associated protein. Biochemistry. 1989;28:6361–6367. doi: 10.1021/bi00441a031. [DOI] [PubMed] [Google Scholar]
  • 86.Petty TL, Silvers GW, Paul GW, Stanford RE. Abnormalities in lung elastic properties and surfactant function in adult respiratory distress syndrome. Chest. 1979;75:571–574. doi: 10.1378/chest.75.5.571. [DOI] [PubMed] [Google Scholar]
  • 87.Pison U, Seeger W, Buchhorn R, Joka T, Brand M, Obertacke U, Neuhof H, Schmit-Neuerburg KP. Surfactant abnormalities in patients with respiratory failure after multiple trauma. Am Rev Respir Dis. 1989;140:1033–1039. doi: 10.1164/ajrccm/140.4.1033. [DOI] [PubMed] [Google Scholar]
  • 88.Pison U, Tam EK, Caughey GH, Hawgood S. Proteolytic inactivation of dog lung surfactant-associated proteins by neutrophil elastase. Biochim Biophys Acta. 1989;992:251–257. doi: 10.1016/0304-4165(89)90082-2. [DOI] [PubMed] [Google Scholar]
  • 89.Pison U, Obertacke U, Seeger W, Hawgood S (1992) Surfactant protein A (SP-A) is decreased in acute parenchymal lung injury associated with polytrauma. Eur J Clin Invest [DOI] [PubMed]
  • 90.Possmayer F. A proposed nomenclature for pulmonary surfactant-associated proteins. Am Rev Respir Dis. 1988;138:990–996. doi: 10.1164/ajrccm/138.4.990. [DOI] [PubMed] [Google Scholar]
  • 91.Pratt P. The lung: structure, function, and disease. Baltimore: Williams and Wilkins; 1977. pp. 45–57. [Google Scholar]
  • 92.Revak SD, Merritt TA, Hallman M, Cochrane CG. Reconstitution of surfactant activity using purified human apoprotein and phospholipid measured in vitro and in vivo. Am Rev Respir Dis. 1986;134:1258–1265. doi: 10.1164/arrd.1986.134.5.1258. [DOI] [PubMed] [Google Scholar]
  • 93.Revak SD, Merritt TA, Degryse E, Stefani L, Courtney M, Hallman M, Cochrane CG. Use of human surfactant low molecular apoproteins in the reconstitution of surfactant biologic activity. J Clin Invest. 1988;81:826–833. doi: 10.1172/JCI113391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94.Reynolds HY. Pulmonary host defenses — state of the art. Chest. 1989;95:223S–230S. [Google Scholar]
  • 95.Rice WR, Ross GF, Singleton FM, Dingle S, Whitsett JA. Surfactant-associated protein inhibits phospholipid secretion from type II cells. J Appl Physiol. 1987;63:692–698. doi: 10.1152/jappl.1987.63.2.692. [DOI] [PubMed] [Google Scholar]
  • 96.Richman PS, Spragg RG, Robertson B, Merritt TA, Curstedt T. The adult respiratory distress syndrome: first trials with surfactant replacement. Eur Respir J. 1989;2(Suppl 3):109–111. [PubMed] [Google Scholar]
  • 97.Robertson B, Lachmann B. Experimental evaluation of surfactants for replacement therapy. Exp Lung Res. 1988;14:279–310. doi: 10.3109/01902148809087810. [DOI] [PubMed] [Google Scholar]
  • 98.Ross GF, Notter RH, Meuth J, Whitsett JA. Phospholipid binding and biophysical activity of pulmonary surfactant-associated protein (SAP)-35 and its non-collagenous COOH-terminal domains. J Biol Chem. 1986;261:14283–14291. [PubMed] [Google Scholar]
  • 99.Rüfer R, Stolz C. Inaktivierung von alveolären Oberflächenfilmen durch Erniedrigung der Oberflächen-spannung der Hypophase. Pflügers Arch. 1969;307:89–103. [PubMed] [Google Scholar]
  • 100.Ryan RM, Morris RE, Rice WR, Ciraolo G, Whitsett J. Binding and uptake of pulmonary surfactant protein (SP-A) by pulmonary type II epithelial cells. J Histochem Cytochem. 1989;37:429–440. doi: 10.1177/37.4.2926121. [DOI] [PubMed] [Google Scholar]
  • 101.Ryan SF, Ghassibi Y, Liau DF. Effects of activated polymorphonuclear leukocytes upon pulmonary surfactant in vitro. Am J Respir Cell Mol Biol. 1990;4:33–41. doi: 10.1165/ajrcmb/4.1.33. [DOI] [PubMed] [Google Scholar]
  • 102.Seeger W, Lasch HG. Septic lung. Rev Infect Dis. 1987;9:570–579. doi: 10.1093/clinids/9.supplement_5.s570. [DOI] [PubMed] [Google Scholar]
  • 103.Seeger W, Suttorp N. Role of membrane lipids in the pulmonary vascular abnormalities caused by bacterial toxins. Am Rev Respir Dis. 1988;136:462–466. doi: 10.1164/ajrccm/136.2.462. [DOI] [PubMed] [Google Scholar]
  • 104.Seeger W, Lepper H, Wolf HRD, Neuhof H. Alteration of surfactant function after exposure to oxidative stress and to oxygenated and native arachidonic acid in vitro. Biochim Biophys Acta. 1985;835:58–67. doi: 10.1016/0005-2760(85)90030-x. [DOI] [PubMed] [Google Scholar]
  • 105.Seeger W, Stöhr G, Wolf HRD, Neuhof H. Alteration of surfactant function due to protein leakage: special interaction with fibrin monomer. J Appl Physiol. 1985;58:326–338. doi: 10.1152/jappl.1985.58.2.326. [DOI] [PubMed] [Google Scholar]
  • 106.Seeger W, Walmrath D, Menger M, Neuhof H. Increased lung vascular permeability after arachidonic acid and hydrostatic challenge. J Appl Physiol. 1986;61:1781–1789. doi: 10.1152/jappl.1986.61.5.1781. [DOI] [PubMed] [Google Scholar]
  • 107.Seeger W, Hilbel J, Klapettek K, Pison U, Obertacke U, Joka T, Roka L. Procoagulant activity in bronchoalveolar lavage of severly traumatized patients — relation to the development of acute respiratory distress. Throm Res. 1991;61:53–64. doi: 10.1016/0049-3848(91)90168-v. [DOI] [PubMed] [Google Scholar]
  • 108.Seeger W, Thede C, Günther A, Grube C. Surface properties and sensitivity to protein-inhibition of a recombinant apoprotein C-based phospholipid mixture in vitro — comparison to natural surfactant. Biochim Biophys Acta. 1991;1081:45–52. doi: 10.1016/0005-2760(91)90248-g. [DOI] [PubMed] [Google Scholar]
  • 109.Seeger W, Günther A, Thede C. Differential sensitivity to fibrinogen-inhibition of SP-C versus SP-B based surfactants. Am J Physiol. 1992;262:L285–L291. doi: 10.1152/ajplung.1992.262.3.L286. [DOI] [PubMed] [Google Scholar]
  • 110.Shiffer K, Hawgood S, Düzgünes N, Goerke J. Interactions of the low molecular weight group of surfactant-associated proteins (SP 5-18) with pulmonary surfactant lipids. Biochemistry. 1988;27:2689–2695. doi: 10.1021/bi00408a008. [DOI] [PubMed] [Google Scholar]
  • 111.Speer CP, Götze B, Curstedt T, Robertson B. Phagocytic functions and tumor necrosis factor secretion of human monocytes exposed to natural porcine surfactant (Curosurf) Pediatr Res. 1991;30:69–74. doi: 10.1203/00006450-199107000-00015. [DOI] [PubMed] [Google Scholar]
  • 112.Spencer H. Pathology of the lung. 3rd edn. Philadelphia: Saunders; 1977. pp. 235–240. [Google Scholar]
  • 113.Strohmaier W, Redl H, Schlag G. Studies of the potential role of a semisynthetic surfactant preparation in an experimental aspiration trauma in rabbits. Exp Lung Res. 1990;16:101–110. doi: 10.3109/01902149009087875. [DOI] [PubMed] [Google Scholar]
  • 114.Suzuki Y, Fujita Y, Kogishi K. Reconstitution of tubular myelin from synthetic lipids and proteins associated with pig pulmonary surfactant. Am Rev Respir Dis. 1989;140:75–81. doi: 10.1164/ajrccm/140.1.75. [DOI] [PubMed] [Google Scholar]
  • 115.Taylor FB, Abrams ME. Effect of surface active lipoprotein on clotting and fibrinolysis, and of fibrinogen on surface tension of surface active lipoprotein. Am J Med. 1966;40:346–350. [Google Scholar]
  • 116.Termer AJ, Robinson SL, Borchelt J, Wright JR. Human pulmonary surfactant protein (SP-A), a protein structurally homologous to C1q, can enhance FcR- and CR1-mediated phagocytosis. J Biol Chem. 1989;264:13923–13928. [PubMed] [Google Scholar]
  • 117.Tierney DF, Johnson RP. Altered surface tension of lung extracts and lung mechanics. J Appl Physiol. 1965;20:1253–1260. [Google Scholar]
  • 118.van Daal GJ, So KL, Gommers D, Eijking EP, Fiévez RB, Sprenger MJ, van Dam DW, Lachman B. Intratracheal surfactant administration restores gas exchange in experimental adult respiratory distress syndrome associated with viral pneumonia. Anesth Analg. 1991;72:589–595. [PubMed] [Google Scholar]
  • 119.van Daal GJ, Bos JAH, Eijking EP, Gommers D, Hannappel E, Lachmann B. Surfactant replacement therapy improves pulmonary mechanics in end-stage influenza A pneumonia in mice. Am Rev Respir Dis. 1992;145:859–863. doi: 10.1164/ajrccm/145.4_Pt_1.859. [DOI] [PubMed] [Google Scholar]
  • 120.van Golde LMG, Batenburg JJ, Robertson B. The pulmonary surfactant system: biochemical aspects and functional significance. Physiol Rev. 1988;68:374–455. doi: 10.1152/physrev.1988.68.2.374. [DOI] [PubMed] [Google Scholar]
  • 121.Venkitaraman AR, Baatz JE, Whitsett JA, Hall SB, Notter RH. Biophysical inhibition of synthetic phospholipid-lung surfactant apoprotein admixtures by plasma proteins. Chem Phys Lipids. 1991;57:49–57. doi: 10.1016/0009-3084(91)90048-g. [DOI] [PubMed] [Google Scholar]
  • 122.Warr RG, Hawgood S, Buckley DI, Crisp TM, Schilling J, Benson BJ, Ballard PL, Clements JA, White RT. Low molecular weight human pulmonary surfactant protein (SP5): isolation, characterization, and cDNA and amino acid sequences. Proc Natl Acad Sci USA. 1987;84:7915–7919. doi: 10.1073/pnas.84.22.7915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 123.Whitsett JA, Ohning BL, Ross G, Meuth J, Weaver T, Holm BA, Shapiro DL, Notter RH. Hydrophobic surfactant-associated protein in whole lung surfactant and its importance for biophysical activity in lung surfactant extracts used for replacement therapy. Pediatr Res. 1986;20:460–467. doi: 10.1203/00006450-198605000-00016. [DOI] [PubMed] [Google Scholar]
  • 124.von Wichert P, Temmesfeld M, Meyer W. Influence of septic shock upon phosphytidylcholine remodeling mechanism in rat lung. Biochim Biophys Acta. 1981;664:487–497. doi: 10.1016/0005-2760(81)90127-2. [DOI] [PubMed] [Google Scholar]
  • 125.Williams MC, Hawgood S, Hamilton RL. Changes in lipid structure produced by surfactant proteins SP-A, SP-B and SP-C. Am J Respir Cell Mol Biol. 1991;5:41–50. doi: 10.1165/ajrcmb/5.1.41. [DOI] [PubMed] [Google Scholar]
  • 126.Wispé JR, Clark JC, Warner BB, Fajardo D, Hull WE, Holtzman RB, Whitsett JA. Tumor necrosis factor-alpha inhibits expression of pulmonary surfactant protein. J Clin Invest. 1990;86:1954–1960. doi: 10.1172/JCI114929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 127.Yu SH, Possmayer F. Reconstitution of surfactant activity by using the 6 kDa apoprotein associated with pulmonary surfactant. Biochem J. 1986;236:85–89. doi: 10.1042/bj2360085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 128.Yu SH, Possmayer F. Comparative studies on the biophysical activities of the low-molecular-weight hydrophobic proteins purified from bovine pulmonary surfactant. Biochim Biophys Acta. 1988;961:337–350. doi: 10.1016/0005-2760(88)90081-1. [DOI] [PubMed] [Google Scholar]
  • 129.Zelter M, Escudies BJ, Hoeffel JM, Murray JF. Effects of aerosolized artificial surfactant on repeated oleic acid injury in sheep. Am Rev Respir Dis. 1990;141:1014–1019. doi: 10.1164/ajrccm/141.4_Pt_1.1014. [DOI] [PubMed] [Google Scholar]
  • 130.Günther A, Bleyl H, Seeger W (1992) Apoprotein-based synthetic surfactants inhibit plasmic cleavage of fibrinogen in vitro. (submitted) [DOI] [PubMed]
  • 131.Seeger W, Elssner A, Giinther A, Krämer HJ, Kalinowski HO (1992) Lung surfactant phospholipids associate with polymerizing fibrin - loss of surface activity. (submitted) [DOI] [PubMed]

Articles from The Clinical Investigator are provided here courtesy of Nature Publishing Group

RESOURCES