Comprehensive Physiology Wiley Online Library

Alveolar Surface Tension and Lung Surfactant

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Background
1.1 Early Contributors
1.2 Relevance of Alveolar Surface Film
1.3 Current Model of Lung Surfactant Action
2 Definition and Measurement of Surface Tension
2.1 Generation of Interfacial Tension
2.2 Methods
3 Adsorption and Spreading of Surfactant Films
3.1 Form of Surfactant
3.2 Factors Affecting Adsorption and Spreading
4 Properties of Films Related to Lung Surfactant
4.1 Low Surface Tension and Other Quasi‐Static Film Properties
4.2 Dynamic Film Properties
5 Influence of Surface Tension on Lung Pressure‐Volume Behavior
5.1 Static Properties
5.2 Dynamic Properties
6 Turnover and Recycling of Surfactant Components
6.1 Possible Recycling Paths
6.2 Local Monolayer Recycling
6.3 Extramonolayer Recycling Pathways
7 Summary of Lung Surfactant Properties
7.1 Rapid Adsorption and Spreading
7.2 Low Surface Tension When Film is Compressed
7.3 Stable Low Surface Tension
8 Future Considerations
Figure 1. Figure 1.

Langmuir film balance. Barrier rests on top of trough sidewalls. Moving it left compresses the surface film, lowering surface tension (raising the surface pressure). Compressed film pushes on mica float with a force proportional to difference between surface tensions in the clean and film‐covered surfaces. Float is kept in a null position by applying an opposing force, which is therefore a measure of film surface pressure. In many applications this force is supplied by a nulled torsion balance.

Figure 2. Figure 2.

Modified Wilhelmy film balance. Ends of barrier fit tightly against sidewalls of trough. Surface tension is lowered by moving barrier to left and compressing the film. This is sensed as a decreased force pulling on small, hydrophilic Wilhelmy dipping plate.

Figure 3. Figure 3.

Surface pressure vs. area for dipalmitoyl phosphatidylcholine monolayers at various temperatures. ▪, 34.6°C; Δ, 29.5°C; ▪, 26.0°C; ×, 21.1°C; ○, 16.8°C; △, 12.4°C; □, 6.2°C.

From Phillips and Chapman
Figure 4. Figure 4.

Surface pressure vs. area for dipalmitoyl phosphatidylcholine compressed to collapse pressures. Highest surface pressures at each temperature correspond to zero surface tension.

J. Goerke and J. Gonzales, unpublished observations
Figure 5. Figure 5.

Surface pressure vs. area for dog lung surfactant at 37°C. Surface pressure of 70 mN·m−1 corresponds to surface tension of 0 mN·m−1.

From King and Clements
Figure 6. Figure 6.

Volume vs. pressure from isolated rat (○) and cat (×) lungs. Surface tension was directly measured in lungs at selected points on deflation curve as indicated by arrows.

Rat data from Schürch et al. ; cat data from Schürch


Figure 1.

Langmuir film balance. Barrier rests on top of trough sidewalls. Moving it left compresses the surface film, lowering surface tension (raising the surface pressure). Compressed film pushes on mica float with a force proportional to difference between surface tensions in the clean and film‐covered surfaces. Float is kept in a null position by applying an opposing force, which is therefore a measure of film surface pressure. In many applications this force is supplied by a nulled torsion balance.



Figure 2.

Modified Wilhelmy film balance. Ends of barrier fit tightly against sidewalls of trough. Surface tension is lowered by moving barrier to left and compressing the film. This is sensed as a decreased force pulling on small, hydrophilic Wilhelmy dipping plate.



Figure 3.

Surface pressure vs. area for dipalmitoyl phosphatidylcholine monolayers at various temperatures. ▪, 34.6°C; Δ, 29.5°C; ▪, 26.0°C; ×, 21.1°C; ○, 16.8°C; △, 12.4°C; □, 6.2°C.

From Phillips and Chapman


Figure 4.

Surface pressure vs. area for dipalmitoyl phosphatidylcholine compressed to collapse pressures. Highest surface pressures at each temperature correspond to zero surface tension.

J. Goerke and J. Gonzales, unpublished observations


Figure 5.

Surface pressure vs. area for dog lung surfactant at 37°C. Surface pressure of 70 mN·m−1 corresponds to surface tension of 0 mN·m−1.

From King and Clements


Figure 6.

Volume vs. pressure from isolated rat (○) and cat (×) lungs. Surface tension was directly measured in lungs at selected points on deflation curve as indicated by arrows.

Rat data from Schürch et al. ; cat data from Schürch
References
 1. Adam, N. K. The Physics and Chemistry of Surfaces. New York: Dover, 1968.
 2. Adams, F. H., and G. Enhorning. Surface properties of lung extracts. I. A dynamic alveolar model. Acta Physiol. Scand. 68: 23–27, 1966.
 3. Adams, F. H., B. Towers, A. B. Osher, M. Ikegami, T. Fujiwara, and M. Nozaki. Effects of tracheal instillation of natural surfactant in premature lambs. I. Clinical and autopsy findings. Pediatr. Res. 12: 841–848, 1978.
 4. Alarie, Y., M. A. Choby, and W. E. Poel. Alveolar instability following administration of fluorocarbon (Abstract). Toxicol. Appl. Pharmacol. 22: 306, 1972.
 5. Alarie, Y., and J. Quealy. Effects of trichlorotrifluoroethane on pressure‐volume curves in rat lungs (Abstract). Physiologist 15: 69, 1972.
 6. Albrecht, O., H. Gruler, and E. Sackmann. Pressure‐composition phase diagrams of cholesterol/lecithin, cholesterol/phosphatidic acid, and lecithin/phosphatidic acid mixed monolayers: a Langmuir film balance study. J. Colloid Interface Sci. 79: 319–338, 1981.
 7. Ardila, R., D. Potter, and J. Hildebrandt. Interfacial hysteresis in lung (Letter to the editor). J. Appl. Physiol. 37: 472, 1974.
 8. Avery, M. E. On replacing the surfactant. Pediatrics 65: 1126–1177, 1980.
 9. Avery, M. E., and J. Mead. Surface properties in relation to atelectasis and hyaline membrane disease. Am. J. Dis. Child. 97: 517–523, 1959.
 10. Bachofen, H., P. Gehr, and E. R. Weibel. Alterations of mechanical properties and morphology in excised rabbit lungs rinsed with a detergent. J. Appl. Physiol: Respirat. Environ. Exercise Physiol. 47: 1002–1010, 1979.
 11. Bangham, A. D., C. J. Morley, and M. C. Phillips. The physical properties of an effective lung surfactant. Biochim. Biophys. Acta 573: 552–556, 1979.
 12. Baritussio, A. G., M. W. Magoon, J. Goerke, and J. A. Clements. Precursor‐product relationship between rabbit type II cell lamellar bodies and alveolar surface active material: surfactant turnover time. Biochim. Biophys. Acta 666: 382–393, 1981.
 13. Benson, B. J., M. C. Williams, K. Sueishi, J. Goerke, and T. Sargeant. Role of calcium ions in the structure and function of pulmonary surfactant. Biochim. Biophys. Acta 793: 18–27, 1984.
 14. Berggren, P., G. Grossmann, R. Nilsson, S. Tollbom, and B. Robertson. A protein‐free physiologically active preparation of natural lung surfactant. IRCS J. Med. Sci. 9: 283–284, 1981.
 15. Bergman, B. Beta‐mimetics and the preterm neonatal lung. Acta Physiol. Scand. Suppl. 497: 1–52, 1981.
 16. Boggs, J. M., M. A. Moscarello, and D. Papahadjopoulos. Phase separation of acidic and neutral phospholipids induced by human myelin basic protein. Biochemistry 16: 5420–5426, 1977.
 17. Boggs, J. M., D. D. Wood, M. A. Moscarello, and D. Papahadjopoulos. Lipid phase separation induced by a hydrophobic protein in phosphatidylserine‐phosphatidylcholine vesicles. Biochemistry 16: 2325–2329, 1977.
 18. Brown, E. S. Isolation and assay of dipalmityl lecithin in lung extracts. Am. J. Physiol. 207: 402–406, 1964.
 19. Brown, E. S., R. P. Johnson, and J. A. Clements. Pulmonary surface tension. J. Appl. Physiol. 14: 717–720, 1959.
 20. Brown, M. S., P. T. Kovanen, and J. L. Goldstein. Regulation of cholesterol by lipoprotein receptors. Science 212: 628–635, 1981.
 21. Brumley, G., and J. D. Crapo. Oxygen‐adapted rats and lung‐disaturated lecithin. J. Pediatr. 95: 892–895, 1979.
 22. Brumley, G. W., W. A. Hodson, and M. E. Avery. Lung phospholipids and surface tension correlations in infants with and without hyaline membrane disease and in adults. Pediatrics 40: 13–19, 1967.
 23. Brumley, G. W., B. Tuggle, L. Luxner, and J. D. Crapo. Disaturated phosphatidylcholine in rat lungs with altered numbers of type II alveolar epithelial cells. Am. Rev. Respir. Dis. 119: 461–470, 1979.
 24. Buckingham, S., and M. E. Avery. Time of appearance of lung surfactant in the foetal mouse. Nature London 193: 688–689, 1962.
 25. Cadenhead, D. A., and B. M. J. Kellner. Some observations on monolayer spreading solvents with special reference to phospholipid monolayers. J. Colloid Interface Sci. 49: 143–145, 1974.
 26. Cadenhead, D. A., and F. Mueller‐Landau. Molecular accommodation and molecular interactions in mixed insoluble monomolecular films. J. Colloid Interface Sci. 78: 269–270, 1980.
 27. Cadenhead, D. A., and J. E. Osonka. The influence of ethanol on both condensed and expanded monomolecular films at the air‐water interface. J. Colbid Interface Sci. 33: 187–191, 1970.
 28. Chander, A., J. F. Strauss, and A. B. Fisher. Uptake of phosphatidylcholine (PC) by granular pneumocytes in primary culture (Abstract). Federation Proc. 40: 407, 1981.
 29. Chapman, D., N. F. Owens, M. C. Phillips, and D. A. Walker. Mixed monolayers of phospholipids and cholesterol. Biochim. Biophys. Acta 183: 458–465, 1969.
 30. Clements, J. A. Surface tension of lung extracts. Proc. Soc. Exp. Biol. Med. 95: 170–172, 1957.
 31. Clements, J. A. Pulmonary edema and permeability of alveolar membranes. Arch. Environ. Health 2: 280–283, 1961.
 32. Clements, J. A. Functions of the alveolar lining. Am. Rev. Respir. Dis. 115: 67–71, 1977.
 33. Clements, J. A., E. S. Brown, and R. P. Johnson. Pulmonary surface tension and the mucus lining of the lungs: some theoretical considerations. J. Appl. Physiol. 12: 262–268, 1958.
 34. Clements, J. A., R. F. Hustead, R. P. Johnson, and I. Gribetz. Pulmonary surface tension and alveolar stability. J. Appl. Physiol. 16: 444–450, 1961.
 35. Clements, J. A., M. J. Oyarzún, and A. Baritussio. Secretion and clearance of lung surfactant: a brief review. Prog. Respir. Res. 15: 20–26, 1981.
 36. Clements, J. A., A. C. G. Platzker, D. F. Tierney, C. J. Hobel, R. K. Creasy, A. J. Margolis, D. W. Thibeault, W. H. Tooley, and W. Oh. Assessment of the risk of the respiratory‐distress syndrome by a rapid test for surfactant in amniotic fluid. N. Engl. J. Med. 286: 1077–1081, 1972.
 37. Clements, J. A., and D. F. Tierney. Alveolar instability associated with altered surface tension. In: Handbook of Physiology. Respiration, edited by W. O. Fenn and H. Rahn. Washington, DC: Am. Physiol. Soc., 1965, sect. 3, vol. II, chapt. 69, p. 1565–1583.
 38. Crapo, J. D., B. E. Barry, H. A. Foscue, and J. Shelburne. Structural and biochemical changes in rat lungs occurring during exposures to lethal and adaptive doses of oxygen. Am. Rev. Respir. Dis. 122: 123–143, 1980.
 39. Darke, A., E. G. Finer, A. G. Floor, and M. C. Phillips. Complex and cluster formation in mixed lecithin cholesterol bilayers, cooperativity of motion in lipid systems. FEBS Lett. 18: 326–330, 1971.
 40. Davis, P. J., K. P. Coolbear, and K. M. W. Keough. Differential scanning calorimetric studies of the thermotropic phase behavior of membranes composed of dipalmitoyllecithin and mixed‐acid unsaturated lecithins. Can. J. Biochem. 58: 851–858, 1980.
 41. De Boer, J., I. J. Hermans, and C. A. P. Barker. Contribution of alveolar surface lining to lung mechanics. Analysis of in vivo measurements of air‐ and fluid‐filled lungs. Acta Physiol. Pharmacol. Neerl. 14: 231–249, 1967.
 42. DiAugustine, R. P. Lung concentric laminar organelle. Hydrolase activity and compositional analysis. J. Biol. Chem. 249: 584–593, 1974.
 43. Egan, E. A., R. M. Nelson, and R. E. Olver. Lung inflation and alveolar permeability to non‐electrolytes in the adult sheep in vivo. J. Physiol. London 260: 409–424, 1976.
 44. Egan, E. A., R. E. Olver, and L. B. Strang. Changes in non‐electrolyte permeability of alveoli and the absorption of lung liquid at the start of breathing in the lamb. J. Physiol. London 244: 161–179, 1975.
 45. Enhorning, G. Pulsating bubble technique for evaluating pulmonary surfactant. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 43: 198–203, 1977.
 46. Enhorning, G., and B. Robertson. Lung expansion in the premature rabbit fetus after tracheal deposition of surfactant. Pediatrics 50: 58–66, 1972.
 47. Evans, R. W., M. A. Williams, and J. Tinoco. Surface viscosities of phospholipids alone and with cholesterol in monolayers at the air‐water interface. Lipids 15: 524–533, 1980.
 48. Faridy, E. E. Effect of distension on release of surfactant in excised dogs' lungs. Respir. Physiol. 27: 99–114, 1976.
 49. Faridy, E. E. Fetal lung development in surgically induced prolonged gestation. Respir. Physiol. 45: 153–166, 1981.
 50. Farrell, E. E., M. A. Cox, J. Torday, K. Keough, M. Anton, and H. W. Taeusch. Criteria for exogenous surfactants (Abstract). Pediatr. Res. 15: 718, 1981.
 51. Finley, T. N., W. H. Tooley, E. W. Swenson, R. E. Gardner, and J. A. Clements. Pulmonary surface tension in experimental atelectasis. Am. Rev. Respir. Dis. 89: 372–378, 1964.
 52. Fisher, H. K., M. H. Hyman, and S. J. Ashcraft. Alveolar surfactant phospholipids are not cleared via trachea (Abstract). Federation Proc. 38: 1373, 1979.
 53. Florence, R. T., and W. D. Harkins. Molecular interaction in mixed monolayers. II. Unstable mixtures with unsaturated fatty acids. J. Chem. Phys. 6: 856–860, 1938.
 54. Fujiwara, T., H. Maeta, S. Chida, and T. Morita. Surface properties of artificial surfactant in comparison with natural and synthetic surfactant lipids (Abstract). IRCS Med. Sci. 7: 311, 1979.
 55. Fujiwara, T., H. Maeta, S. Chida, and T. Morita. Improved lung‐thorax compliance and prevention of neonatal pulmonary lesion in prematurely delivered rabbit neonates subjected to IPPV after tracheal instillation of artificial surfactant (Abstract). IRCS Med. Sci. 7: 313, 1979.
 56. Fujiwara, T., H. Maeta, S. Chida, T. Morita, Y. Watabe, and T. Abe. Artificial surfactant therapy in hyaline membrane disease. Lancet 1: 55–59, 1980.
 57. Gaines, G. L. Insoluble Monolayers at Liquid‐Gas Interfaces. New York: Wiley, 1966.
 58. Geiger, K., M. L. Gallagher, and J. Hedley‐Whyte. Cellular distribution and clearance of aerosolized dipalmitoyl lecithin. J. Appl. Physiol. 39: 759–766, 1975.
 59. Gershfeld, N. L. Thermodynamics and experimental methods for equilibrium studies with lipid monolayers. In: Methods in Membrane Biology, edited by E. D. Korn. New York: Plenum, 1974, p. 69–104.
 60. Gil, J., H. Bachofen, P. Gehr, and E. R. Weibel. Alveolar volume‐surface area relation in air‐ and saline‐filled lungs fixed by vascular perfusion. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 47: 990–1001, 1979.
 61. Gil, J., and O. K. Reiss. Isolation and characterization of lamellar bodies and tubular myelin from rat lung homogenates. J. Cell Biol. 58: 152–171, 1973.
 62. Gil, J., and E. R. Weibel. Morphological study of pressure‐volume hysteresis in rat lungs fixed by vascular perfusion. Respir. Physiol. 15: 190–213, 1972.
 63. Gilbert, D. B., C. Tanford, and J. A. Reynolds. Cholesterol in aqueous solution: hydrophobicity and self‐association. Biochemistry 14: 444–448, 1975.
 64. Glatz, T. H., M. Ikegami, and A. Jobe. Degradation and reutilization of alveolar surfactant (Abstract). Pediatr. Res. 14: 642, 1980.
 65. Goerke, J. Lung surfactant. Biochim. Biophys. Acta 344: 241–261, 1974.
 66. Goerke, J. Factors affecting adsorption of lipids related to lung surfactant at the air‐water interface (Abstract). Physiologist 24 (4): 104, 1981.
 67. Goerke, J., and J. Gonzales. Temperature dependence of dipalmitoyl phosphatidylcholine monolayer stability. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 51: 1108–1114, 1981.
 68. Goerke, J., H. H. Harper, and M. Borowitz. The interaction of calcium with monolayers of stearic and oleic acid. In: Surface Chemistry of Biological Systems, edited by M. Blank. New York: Plenum, 1970, p. 23–35.
 69. Goldfischer, S., Y. Kikkawa, and L. Hoffman. The demonstration of acid hydrolase activities in the inclusion bodies of type II alveolar cells and other lysosomes in the rabbit lung. J. Histochem. Cytochem. 16: 102–109, 1968.
 70. Grant, C. W. M., S. Hong‐Wei Wu, and H. M. McConnell. Lateral phase separations in binary lipid mixtures: correlation between spin label and freeze‐fracture electron microscopic studies. Biochim. Biophys. Acta 363: 151–158, 1974.
 71. Gross, N. J. Mechanical properties of mouse lungs: effects of degassing on normal, hyperoxic, and irradiated lungs. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 51: 391–398, 1981.
 72. Gruenwald, P., R. P. Johnson, R. F. Hustead, and J. A. Clements. Correlation of mechanical properties of infant lungs with surface activity of extracts. Proc. Soc. Exp. Biol. Med. 109: 369–371, 1962.
 73. Hallman, M., B. L. Epstein, and L. Gluck. Analysis of labeling and clearance of lung surfactant phospholipids in rabbit. Evidence of bi‐directional surfactant flux between lamellar bodies and alveolar lavage. J. Clin. Invest. 68: 742–751, 1981.
 74. Hallman, M., T. A. Merritt, H. Schneider, B. L. Epstein, F. Mannino, D. K. Edwards, and L. Gluck. Isolation of human surfactant from amniotic fluid and a pilot study of its efficacy in respiratory distress syndrome. Pediatrics 71: 473–482, 1983.
 75. Hassett, R. J., R. L. Sanders, A. E. Vatter, and O. K. Reiss. Lamellar bodies: isolation from rat lung, stability and conversion to tubular myelin figures (Abstract). Federation Proc. 36: 615, 1977.
 76. Hauser, H., C. Hinckley, J. Krebs, B. Levine, M. Phillips, and R. Williams. The interaction of ions with phosphatidylcholine bilayers. Biochim. Biophys. Acta 468: 364–377, 1977.
 77. Hauser, H., and M. C. Phillips. Ion‐binding to phospholipids. Interaction of calcium and lanthanide ions with phosphatidylcholine (lecithin) J Bur. J. Biochem. 58: 133–144, 1975.
 78. Hawco, M. W., K. P. Coolbear, P. J. Davis, and K. M. W. Keough. Exclusion of fluid lipid during compression of monolayers of mixtures of dipalmitoylphosphatidylcholine with some other phosphatidylcholines. Biochim. Biophys. Acta 646: 185–187, 1981.
 79. Hawco, M. W., P. J. Davis, and K. M. W. Keough. Lipid fluidity in lung surfactant: monolayers of saturated and unsaturated lecithins. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 51: 509–515, 1981.
 80. Heath, M. F., and W. Jacobson. Phospholipases A1 and A2 in lamellar inclusion bodies of the alveolar epithelium of rabbit lung. Biochim. Biophys. Acta 441: 443–452, 1976.
 81. Hildebran, J. N., J. Goerke, and J. A. Clements. Pulmonary surface film stability and composition. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 47: 604–611, 1979.
 82. Hildebran, J. N., J. Goerke, and J. A. Clements. Surfactant release in excised rat lung is stimulated by air inflation. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 51: 905–910, 1981.
 83. Hills, B. A. What is the true role of surfactant in the lung? Thorax 36: 1–4, 1981.
 84. Horn, L. W. Evaluation of some alternative mechanisms for interface‐related stress relaxation in lung. Respir. Physiol. 34: 345–357, 1978.
 85. Horn, L. W., and S. H. Davis. Apparent surface tension hysteresis of a dynamical system. J. Colloid Interface Sci. 51: 459–476, 1975.
 86. Ikegami, M., T. Hesterberg, M. Nozaki, and F. H. Adams. Restoration of lung pressure‐volume characteristics with surfactant: comparison of nebulization versus instillation and natural versus synthetic surfactant. Pediatr. Res. 11: 178–182, 1977.
 87. Ikegami, M., A. Jobe, and T. Glatz. Surface activity following natural surfactant treatment in premature lambs. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 51: 306–312, 1981.
 88. Ikegami, M., A. H. Jobe, and H. C. Jacobs. Characterization of a protein from immature lambs that inhibits surfactant function (Abstract). Clin. Res. 31: 141, 1983.
 89. Ito, T., and S. I. Ohnishi. Ca2+‐induced lateral phase separations in phosphatidic acid‐phosphatidylcholine membranes. Biochim. Biophys. Acta 352: 29–37, 1974.
 90. Ito, T., S. Ohnishi, M. Ishinaga, and M. Kito. Synthesis of a new phosphatidylserine spin‐label and calcium‐induced lateral phase separation in phosphatidylserine‐phosphatidylcholine membranes. Biochemistry 14: 3064–3069, 1975.
 91. Jacob, J., M. Hallman, and L. Gluck. Phosphatidylinositol (PI) and phosphatidylglycerol (PG) enhance surface properties of lecithin (PC) (Abstract). Pediatr. Res. 14: 644, 1980.
 92. Jacob, J., M. Hallman, and L. Gluck. The effect of phosphatidylglycerol (PG) and phosphatidyl inositol (PI) on dipalmitoyl lecithin (DPPC) monolayer (Abstract). Pediatr. Res. 14: 644, 1980.
 93. King, R. J., and J. A. Clements. Surface active materials from dog lung. I. Method of isolation. Am. J. Physiol. 223: 707–714, 1972.
 94. King, R. J., and J. A. Clements. Surface active materials from dog lung. II. Composition and physiological correlations. Am. J. Physiol. 223: 715–726, 1972.
 95. King, R. J., and J. A. Clements. Surface active materials from dog lung. III. Thermal analysis. Am. J. Physiol. 223: 727–733, 1972.
 96. King, R. J., and J. A. Clements. Lipid synthesis and surfactant turnover in the lungs. In: Handbook of Physiology. Circulation and Nonrespiratory Functions, edited by A. P. Fishman and A. B. Fisher. Bethesda, MD: Am. Physiol. Soc., 1985, sect. 3, vol. I, chapt. 8, p. 309–336.
 97. King, R. J., and M. C. MacBeth. Physicochemical properties of dipalmitoyl phosphatidylcholine after interaction with an apoprotein of pulmonary surfactant. Biochim. Biophys. Acta 557: 86–101, 1979.
 98. King, R. J., and M. C. MacBeth. Interaction of the lipid and protein components of pulmonary surfactant. Role of phosphatidylglycerol and calcium. Biochim. Biophys. Acta 647: 159–168, 1981.
 99. King, R. J., H. Martin, D. Mitts, and F. M. Holmstrom. Metabolism of the apoproteins in pulmonary surfactant. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 42: 483–491, 1977.
 100. Kitterman, J. A., P. L. Ballard, J. A. Clements, E. J. Mescher, and W. H. Tooley. Tracheal fluid in fetal lambs: spontaneous decrease prior to birth. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 47: 985–989, 1979.
 101. Klass, D. J. Dibutyryl cyclic GMP and hyperventilation promote rat lung phospholipid release. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 47: 285–289, 1979.
 102. Knoebel, L. K. Secretion and action of digestive juices; absorption. In: Physiology (4th ed.), edited by E. W. Selkurt. Boston, MA: Little, Brown, 1976, p. 654–658.
 103. Lau, M.‐J., and K. M. W. Keough. Lipid composition of lung and lung lavage fluid from map turtles (Malaclemys geographica) maintained at different environmental temperatures. Can. J. Biochem. 59: 208–219, 1981.
 104. Lee, A. G. Lipid phase transitions and phase diagrams: mixtures involving lipids. Biochim. Biophys. Acta 472: 285–344, 1977.
 105. Lempert, J., and P. T. Macklem. Effect of temperature on rabbit lung surfactant and pressure‐volume hysteresis. J. Appl. Physiol. 31: 380–385, 1971.
 106. Magoon, M. W., A. G. Baritussio, J. Goerke, and J. A. Clements. Precursor‐product (PP) relationship between rabbit type II cell lamellar bodies (LB) and alveolar surface active material (SAM) and SAM turnover time (τ) (Abstract). Federation Proc. 40: 407, 1981.
 107. Magoon, M. W., J. R. Wright, A. Baritussio, M. C. Williams, J. Goerke, B. J. Benson, R. L. Hamilton, and J. A. Clements. Subfractionation of lung surfactant. Implication for metabolism and surface activity. Biochim. Biophys. Acta 750: 18–31, 1983.
 108. Mason, R. J. Lipid metabolism. In: Lung Biology in Health and Disease. The Biochemical Basis of Pulmonary Function, edited by R. G. Crystal. New York: Dekker, 1976, vol. 2, p. 127–169.
 109. Massaro, D. Clinical implications of the effect of breathing pattern on the lung. Am. Thorac. Soc. News 6: 30–35, 1980.
 110. Massaro, D., L. Clerch, and G. D. Massaro. Effect of temperature and ventilatory rate of excised rat lungs on aggregation of surfactant (Abstract). Federation Proc. 39: 1065, 1980.
 111. Massaro, D., L. Clerch, and G. D. Massaro. Surfactant aggregation in rat lungs: influence of temperature and ventilation. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 51: 646–653, 1981.
 112. McBain, J. W., and C. W. Humphreys. The microtome method of the determination of the absolute amount of adsorption. J. Phys. Chem. 36: 300–311, 1932.
 113. McClenahan, J. B., R. Mussenden, and J. D. Ohlsen. Effect of ethanol on surfactant of ventilated lungs. J. Appl. Physiol. 27: 90–95, 1969.
 114. McClenahan, J. B., and A. Urtnowski. Effect of ventilation on surfactant, and its turnover rate. J. Appl. Physiol. 23: 215–220, 1967.
 115. McLean, L. R., and M. C. Phillips. Mechanism of cholesterol and phosphatidylcholine exchange or transfer between unilamellar vesicles. Biochemistry 20: 2893–2900, 1981.
 116. Mead, J., and C. Collier. Relation of volume history of lungs to respiratory mechanics in anesthetized dogs. J. Appl. Physiol. 14: 669–678, 1959.
 117. Mead, J., J. L. Whittenberger, and E. P. Radford, Jr. Surface tension as a factor in pulmonary volume‐pressure hysteresis. J. Appl. Physiol. 10: 191–196, 1957.
 118. Meban, C. Surface viscosity of surfactant films from human lungs. Respir. Physiol. 33: 219–227, 1978.
 119. Meban, C. Physical properties of surfactant from the lungs of the tortoise Testudo hermanni. Comp. Biochem. Physiol. A 67: 253–257, 1980.
 120. Meban, C. Surface elastic properties of surfactant from the lungs of neonatal pigs. Biol. Neonate 37: 308–312, 1980.
 121. Meban, C. Effect of lipids and other substances on the adsorption of dipalmitoyl phosphatidylcholine. Pediatr. Res. 15: 1029–1031, 1981.
 122. Metcalfe, I. L., G. Enhorning, and F. Possmayer. Pulmonary surfactant‐associated proteins: their role in the expression of surface activity. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 49: 34–41, 1980.
 123. Morley, C. J., A. D. Bangham, P. Johnson, G. D. Thorburn, and G. Jenkin. Physical and physiological properties of dry lung surfactant. Nature London 271: 162–163, 1978.
 124. Morley, C. J., A. D. Bangham, N. Miller, and J. A. Davis. Dry artificial lung surfactant and its effect on very premature babies. Lancet 1: 64–68, 1981.
 125. Morley, C., B. Robertson, B. Lachmann, R. Nilsson, A. Bangham, G. Grossmann, and N. Miller. Artificial surfactant and natural surfactant. Comparative study of the effects on premature rabbit lungs. Arch. Dis. Child. 55: 758–765, 1980.
 126. Morris, G. S., J. A. Thliveris, and E. E. Faridy. Development of fetal rat lung during prolonged gestation. Respir. Physiol. 42: 263–285, 1980.
 127. Munder, J. W., and J. Swarbrick. Time‐dependent surface behavior of dipalmitoyllecithin and lung alveolar surfactant monolayers. Biochim. Biophys. Acta 291: 344–350, 1973.
 128. Nielson, D. W., J. Goerke, and J. A. Clements. Alveolar subphase pH in the lungs of anesthetized rabbits. Proc. Natl. Acad. Sci. USA 78: 7119–7123, 1981.
 129. Notter, R. H., S. Holcomb, and R. D. Mavis. Dynamic surface properties of phosphatidylglycerol‐dipalmitoyl phosphatidylcholine mixed films. Chem. Phys. Lipids 27: 305–319, 1980.
 130. Notter, R. H., and R. D. Mavis. Surface tension hysteresis in lung surfactant films: etiology and physiologic consequence (Abstract). Pediatr. Res. 15: 728, 1981.
 131. Notter, R. H., and P. E. Morrow. Pulmonary surfactant: a surface chemistry viewpoint. Ann. Biomed. Eng. 3: 119–159, 1975.
 132. Notter, R. H., D. L. Shapiro, R. Taubold, and J. Chen. Bilirubin interactions with phospholipid components of lung surfactant. Pediatr. Res. 16: 130–136, 1982.
 133. Notter, R. H., S. A. Tabak, S. Holcomb, and R. D. Mavis. Postcollapse dynamic surface pressure relaxation in binary surface films containing dipalmitoyl phosphatidylcholine. J. Colloid Interface Sci. 74: 370–377, 1980.
 134. Notter, R. H., S. A. Tabak, and R. D. Mavis. Surface properties of binary mixtures of some pulmonary surfactant components. J. Lipid Res. 21: 10–22, 1980.
 135. Notter, R. H., R. Taubold, and R. D. Mavis. Hysteresis in saturated phospholipid films and its potential relevance for lung function in vivo. Exp. Lung Res. 3: 109–127, 1982.
 136. O'Hare, K. H., J. K. Newman, A. E. Vatter, and O. K. Reiss. Esterases in developing and adult rat lung. II. An electrophoretic analysis. J. Histochem. Cytochem. 19: 116–123, 1971.
 137. O'Hare, K. H., O. K. Reiss, and A. E. Vatter. Esterases in developing and adult rat lung. I. Biochemical and electron microscopic observations. J. Histochem. Cytochem. 19: 97–115, 1971.
 138. Olver, R. E. Ion transport and water flow in the mammalian lung. In: Lung Liquids, edited by R. Porter and M. O'Connor. New York: Elsevier, 1976, p. 199–209. (Ciba Found. Symp. 38.).
 139. Olver, R. E., E. E. Schneeberger, and D. V. Walters. Epithelial solute permeability, ion transport and tight junction morphology in the developing lung of the foetal lamb. J. Physiol. London 315: 395–412, 1981.
 140. Olver, R. E., and L. B. Strang. Ion fluxes across the pulmonary epithelium and the secretion of lung liquid in the foetal lamb. J. Physiol. London. 241: 327–357, 1974.
 141. Oyarzún, M. J., and J. A. Clements. Ventilatory and cholinergic control of pulmonary surfactant in the rabbit. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 43: 39–45, 1977.
 142. Oyarzún, M. J., J. A. Clements, and A. Baritussio. Ventilation enhances pulmonary alveolar clearance of radioactive dipalmitoyl phosphatidylcholine in liposomes. Am. Rev. Respir. Dis. 121: 709–721, 1980.
 143. Pattle, R. E. Properties, function and origin of the alveolar lining layer. Nature London 175: 1125–1127, 1955.
 144. Pattle, R. E. Properties, function, and origin of the alveolar lining layer. Proc. R. Soc. London Ser. B 148: 217–240, 1958.
 145. Pattle, R. E. Slow collapse in vitro of the alveolar lining film. J. Physiol. London 284: 101–102, 1978.
 146. Pattle, R. E., C. Schock, and J. Battensby. Some effects of anaesthetics on lung surfactant. Br. J. Anaesth. 44: 1119–1127, 1972.
 147. Paul, G. W., R. J. Hassett, and O. K. Reiss. Formation of lung surfactant films from intact lamellar bodies. Proc. Natl. Acad. Sci. USA 74: 3617–3620, 1977.
 148. Phillips, M. C., and D. Chapman. Monolayer characteristics of saturated 1,2‐diacyl phosphatidylcholines (lecithins) and phosphatidylethanolamines at the air‐water interface. Biochim. Biophys. Acta 163: 301–313, 1968.
 149. Phillips, M. C., and E. G. Finer. The stoichiometry and dynamics of lecithin‐cholesterol clusters in bilayer membranes. Biochim. Biophys. Acta 356: 199–206, 1974.
 150. Phillips, M. C., D. E. Graham, and H. Hauser. Lateral compressibility and penetration into phospholipid monolayers and bilayer membranes. Nature London 254: 154–156, 1975.
 151. Phillips, M. C., and H. Hauser. Spreading of solid glycerides and phospholipids at the air‐water interface. J. Colloid Interface Sci. 49: 31–39, 1974.
 152. Platzker, A. C. G., J. A. Kitterman, E. J. Mescher, J. A. Clements, and W. H. Tooley. Surfactant in the lung and tracheal fluid of the fetal lamb and acceleration of its appearance by dexamethasone. Pediatrics 56: 554–561, 1975.
 153. Rabinovitch, W., R. F. Robertson, and S. G. Mason. Relaxation of surface pressure and collapse of unimolecular films of stearic acid. Can. J. Chem. 38: 1881–1890, 1960.
 154. Rabinowitz, J. L., T. Cardwell, and D. J. P. Bassett. Reutilization of fatty acid carbons for lung lipid synthesis. Am. J. Physiol. 240 (Endocrinol. Metab. 3): E435–E440, 1981.
 155. Radford, E. P., Jr. Method for estimating respiratory surface area of mammalian lungs from their physical characteristics. Proc. Soc. Exp. Biol. Med. 87: 58–61, 1954.
 156. Radford, E. P., Jr. Recent studies of mechanical properties of mammalian lungs. In: Tissue Elasticity, edited by J. W. Remington. Washington, DC: Am. Physiol. Soc., 1957, p. 177–190.
 157. Reifenrath, R. Chemical analysis of the lung alveolar surfactant obtained by alveolar micropuncture. Respir. Physiol. 19: 35–46, 1973.
 158. Ries, H. E., Jr., M. Matsumoto, N. Uyeda, and E. Suito. Electron microscopic studies of monolayers of lecithin. Adv. Chem. Ser. 144: 286–293, 1975.
 159. Robertson, B. Lung surfactant for replacement therapy. Clin. Physiol. 3: 97–110, 1983.
 160. Ryan, S. F., S. A. Hashim, G. Cernansky, C. R. Barrett, Jr., A. L. L. Bell, Jr., and D. F. Liau. Quantification of surfactant phospholipids in the dog lung. J. Lipid Res. 21: 1004–1014, 1980.
 161. Said, S. I., C. M. Banerjee, W. R. Harlan, Jr., and M. E. Avery. Pulmonary edema as a cause of surfactant deficiency. Jpn. Heart J. 8: 742–744, 1967.
 162. Sanders, R. L., R. J. Hassett, and A. E. Vatter. Isolation of lung lamellar bodies and their conversion to tubular myelin figures in vitro. Anat. Rec. 198: 485–501, 1980.
 163. Sanderson, R. J., and A. E. Vatter. A mode of formation of tubular myelin from lamellar bodies in the lung. J. Cell Biol. 74: 1027–1031, 1977.
 164. Scarpelli, E. M., S. Condorelli, G. Colacicco, and E. V. Cosmi. Lamb fetal pulmonary fluid. II. Fate of phosphatidylcholine. Pediatr. Res. 9: 195–201, 1975.
 165. Schulman, J. H., and A. H. Hughes. Monolayers of proteolytic enzymes and proteins. IV. Mixed monolayer films. Biochem. J. 29: 1243–1252, 1935.
 166. Schürch, S. Surface tension at low lung volumes: dependence on time and alveolar size. Respir. Physiol. 48: 339–355, 1982.
 167. Schürch, S., J. Goerke, and J. A. Clements. Direct determination of surface tension in the lung. Proc. Natl. Acad. Sci. USA 73: 4698–4702, 1976.
 168. Schürch, S., J. Goerke, and J. A. Clements. Direct determination of volume‐ and time‐dependence of alveolar surface tension in excised lungs. Proc. Natl. Acad. Sci. USA 75: 3417–3421, 1978.
 169. Schürch, S., and D. J. L. McIver. Surface tension at low lung volumes: dependence on time and alveolar size (Abstract). Biophys. J. 33, pt. 2: 201, 1981.
 170. Schürch, S. F., and M. R. Roach. Interference of bronchographic agents with lung surfactant. Respir. Physiol. 28: 99–117, 1976.
 171. Sekulic, S. M., J. Hamlin, R. Ellison, and L. Ellison. Pulmonary surfactant and lung circulation in experimental atelectasis. Am. Rev. Respir. Dis. 97: 69–75, 1968.
 172. Shannon, D. C., H. Kazemi, E. W. Merrill, K. A. Smith, and P. S.‐L. Wong. Restoration of volume‐pressure curves with a lecithin fog. J. Appl. Physiol. 28: 470–473, 1970.
 173. Slama, H., W. Schoedel, and E. Hansen. Bestimmung der Oberflaecheneigenschaften von Stoffen aus den Lungenalveolen mit einer Blasenmethode. Pfluegers Arch. 322: 355–363, 1971.
 174. Slama, H., W. Schoedel, and E. Hansen. Lung surfactant: film kinetics at the surface of an air bubble during prolonged oscillation of its volume. Respir. Physiol. 19: 233–243, 1973.
 175. Smith, R., and C. Tanford. The critical micelle concentration of l‐α‐dipalmitoylphosphatidylcholine in water and water‐methanol solutions. J. Mol. Biol. 67: 75–83, 1972.
 176. Smyth, J. A., I. L. Metcalfe, P. Duffty, F. Possmayer, M. H. Bryan, and G. Enhorning. Hyaline membrane disease treated with bovine surfactant. Pediatrics 71: 913–917, 1983.
 177. Steim, J. Synthetic substitutes for surfactant. In: Lung Mat uration and the Prevention of Hyaline Membrane Disease, edited by T. D. Moore. Columbus, OH: Ross Labs., 1976, p. 51–53.
 178. Tabak, S. A., R. H. Notter, J. S. Ultman, and S. M. Dinh. Relaxation effects in the surface pressure behavior of dipalmitoyl lecithin. J. Colloid Interface Sci. 60: 117–125, 1977.
 179. Tajima, K., and N. L. Gershfeld. Detection of low levels of lipid contamination of lecithin by equilibrium spreading pressures. J. Colloid Interface Sci. 81: 283–284, 1981.
 180. Taylor, F. B., and M. E. Abrams. Effect of surface active lipoprotein on clotting and fibrinolysis, and of fibrinogen on surface tension of surface active lipoprotein. Am. J. Med. 40: 346–350, 1966.
 181. Thet, L. A., L. Clerch, G. D. Massaro, and D. Massaro. Changes in sedimentation of surfactant in ventilated excised rat lungs. Physical alterations in surfactant associated with the development and reversal of atelectasis. J. Clin. Invest. 64: 600–608, 1979.
 182. Thompson, W. K., B. E. Marchak, A. B. Froese, and A. C. Bryan. High‐frequency oscillation compared with standard ventilation in pulmonary injury model. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 52: 543–548, 1982.
 183. Tierney, D. F., J. A. Clements, and H. J. Trahan. Rates of replacement of lecithins and alveolar instability in rat lungs. Am. J. Physiol. 213: 671–676, 1967.
 184. Traeuble, H., H. Eibl, and H. Sawada. Respiration—a critical phenomenon? Lipid phase transitions in the lung alveolar surfactant. Naturwissenschaften 61: 344–354, 1974.
 185. Trurnit, H. J. A theory and method for the spreading of protein monolayers. J. Colloid Sci. 15: 1–13, 1960.
 186. Valberg, P. A., and J. D. Brain. Lung surface tension and air space dimensions from multiple pressure‐volume curves. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 43: 730–738, 1977.
 187. Vawter, D. L., Y. C. Fung, and J. B. West. Elasticity of excised dog lung parenchyma. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 45: 261–269, 1978.
 188. Vawter, D. L., Y. C. Fung, and J. B. West. Constitutive equation of lung tissue elasticity. J. Biomech. Eng. 101: 38–45, 1979.
 189. Ververgaert, P. H. J. T., B. De Kruyff, A. J. Verkleij, J. F. Tocanne, and L. L. M. Van Deenen. Calorimetric and freeze‐etch study of the influence of Mg2+ on the thermotropic behaviour of phosphatidylglycerol. Chem. Phys. Lipids. 14: 97–101, 1975.
 190. Vilallonga, F. Surface chemistry of l‐alpha‐dipalmitoyl lecithin at the air‐water interface. Biochim. Biophys. Acta 163: 290–300, 1968.
 191. Von Neergaard, K. Neue Auffassungen über einen Grundbegriff der Atemmechanik. Die Retractionskraft der Lunge, abhängig von der Oberflaechenspannung in den Alveolen. Z. Gesamte. Exp. Med. 66: 373–394, 1929.
 192. Watkins, J. C. The surface properties of pure phospholipids in relation to those of lung extracts. Biochim. Biophys. Acta 152: 293–306, 1968.
 193. Weibel, E. R., G. S. Kistler, and G. Toendury. A stereologic electron microscope study of “tubular myelin figures” in alveolar fluids of rat lungs. Z. Zellforsch. Mikrosk. Anat. 69: 418–427, 1966.
 194. Weibel, E. R., P. Untersee, J. Gil, and M. Zulauf. Morphometric estimation of pulmonary diffusion capacity. VI. Effect of varying positive pressure inflation of air spaces. Respir. Physiol. 18: 285–308, 1973.
 195. Williams, J. V., D. F. Tierney, and H. R. Parker. Surface forces in the lung, atelectasis, and transpulmonary pressure. J. Appl. Physiol. 21: 819–827, 1966.
 196. Williams, M. C. Conversion of lamellar body membranes into tubular myelin in alveoli of fetal rat lungs. J. Cell Biol. 72: 260–277, 1977.
 197. Williams, M. C. Freeze‐fracture studies of tubular myelin and lamellar bodies in fetal and adult rat lungs. J. Ultrastruct. Res. 64: 352–361, 1978.
 198. Williams, M. C., and B. J. Benson. Immunocytochemical localization and identification of the major surfactant protein in adult rat lung. J. Histochem. Cytochem. 29: 291–305, 1981.
 199. Wilson, T. A. Relations among recoil pressure, surface area, and surface tension in the lung. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 50: 921–926, 1981.
 200. Wilson, T. A. Surface tension‐surface area curves calculated from pressure‐volume loops. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 53: 1512–1520, 1982.
 201. Woo, S. W., W. Berlin, U. Buech, and J. Hedley‐White. Altered perfusion, ventilation, anesthesia and lung‐surface forces in dogs. Anesthesiology 33: 411–418, 1970.
 202. Woodside, G. L., and A. J. Dalton. The ultrastructure of lung tissue from newborn and embryo mice. J. Ultrastruct. Res. 2: 28–54, 1958.
 203. Wyszogrodski, I., K. Kyei‐Aboagye, H. W. Taeusch, Jr., and M. E. Avery. Surfactant inactivation by hyperventilation: conservation by end‐expiratory pressure. J. Appl. Physiol. 38: 461–466, 1975.
 204. Young, S. L., D. F. Tierney, and J. A. Clements. Mechanism of compliance change in excised rat lungs at low transpulmonary pressure. J. Appl. Physiol. 29: 780–785, 1970.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

Jon Goerke, John A. Clements. Alveolar Surface Tension and Lung Surfactant. Compr Physiol 2011, Supplement 12: Handbook of Physiology, The Respiratory System, Mechanics of Breathing: 247-261. First published in print 1986. doi: 10.1002/cphy.cp030316