The role of ventilation-induced surfactant dysfunction and atelectasis in causing acute respiratory distress syndrome

American Journal of Respiratory and Critical Care Medicine

Volumn 185, Issue 7, 2012, Pages 702-708

  Albert, Richard K ^a,b  

^a DENVER HEALTH AND HOSPITAL AUTHORITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

ARDS; Atelectasis; Surfactant

Indexed keywords

LUNG SURFACTANT;

ADULT RESPIRATORY DISTRESS SYNDROME; ARTIFICIAL VENTILATION; ATELECTASIS; DISEASE ASSOCIATION; HUMAN; IATROGENIC DISEASE; INFLAMMATION; LUNG ALVEOLUS SURFACE TENSION; LUNG GAS EXCHANGE; PATHOPHYSIOLOGY; PATIENT CARE; PATIENT POSITIONING; PATIENT SAFETY; POSITIVE END EXPIRATORY PRESSURE; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SEDATION; VENTILATOR INDUCED LUNG INJURY;

CONSCIOUS SEDATION; HUMANS; IATROGENIC DISEASE; LUNG; POSITIVE-PRESSURE RESPIRATION; PRONE POSITION; PULMONARY ATELECTASIS; PULMONARY SURFACTANTS; RESPIRATION, ARTIFICIAL; RESPIRATORY DISTRESS SYNDROME, ADULT; SUPINE POSITION; SURFACE TENSION;

EID: 84859485519     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201109-1667PP     Document Type: Review

References (84)

1. Dos Santos CC, Slutsky AS. Mechanisms of ventilator-induced lung injury: a perspective. J Appl Physiol 2000;89:1645-1655.
2. Drinker CK, Hardenbergh MA. The effects of the supine position upon the ventilation of the lungs of dogs. Surgery 1947;24:113-118.
3. Wu N, Miller WF, Luhn NR. Studies of breathing in anesthesia. Anesthesiology 1956;17:696-707.
4. Bernstein L. The elastic pressure-volume curves of the lungs and thorax of the living rabbit. J Physiol 1957;138:473-487.
5. Mead J, Collier C. Relation of volume history of lungs to respiratory mechanics in anesthetized dogs. J Appl Physiol 1959;14:669-678.
6. Clements JA. Surface tension of lung extracts. Proc Soc Exp Biol Med 1957;95:170-172.
7. Clements JA, Hustead RF, Johnson RP, Gribetz I. Pulmonary surface tension and alveolar stability. J Appl Physiol 1961;16:444-450.
8. Clements JA, Tierney DF, Trahan HJ. Influence of kinetic behavior of surface films on pulmonary elasticity. Physiologist 1963;6:159.
9. Greenfield LJ, Ebert PA, Benson DW. Effect of positive pressure ventilation on surface tension proterties of lung extracts. Anesthesiology 1964;25:312-316.
10. Faridy EE, Permutt S, Riley RL. Effect of ventilation on surface forces in excised dogs' lungs. J Appl Physiol 1966;21:1453-1462.
11. McClenahan JB, Urtnowski A. Effect of ventilation on surfactant, and its turnover rate. J Appl Physiol 1967;23:215-220.
12. Forrest JB. The effect of hyperventilation on pulmonary surface activity. Br J Anaesth 1972;44:313-320.
13. Wyszogrodski I, Kyei-Aboagye K, Taeusch HW Jr, Avery ME. Surfactant inactivation by hyperventilation: conservation by end-expiratory pressure. J Appl Physiol 1975;38:461-466.
14. Brown ES, Johnson RP, Clements JA. Pulmonary surface tension. J Appl Physiol 1959;14:717-720.
15. Tierney DF, Johnson RP. Altered surface tension of lung extracts and lung mechanics. J Appl Physiol 1965;20:1253-1260.
16. Webb HH, Tierney DF. Experimental pulmonary edema due to intermittent positive pressure ventilation with high inflation pressures. Protection by positive end-expiratory pressure. Am Rev Respir Dis 1974;110:556-565.
17. Veldhuizen RAW, Marcou J, Yao L, McCaig L, Ito Y, Lewis JF. Alveolar surfactant aggregate conversion in ventilated normal and injured rabbits. Am J Physiol 1996;270: L152-1588.
18. Veldhuizen RQW, Welk B, Harbottle R, Hearn S, Nag K, Peterson N, Possmayer F. Mechanical ventilation of isolated rat lungs changes the structure and biophysical properties of surfactant. J Appl Physiol 2002;92:1169-1175. (Pubitemid 34670976)
19. Muscedere JG, Mullen JBM, Gan K, Slutsky AS. Tidal ventilation at low airway pressures can augment lung injury. Am J Respir Crit Care Med 1994;149:1327-1334. (Pubitemid 24147077)
20. Thet LA, Clerch L, Massaro GD, Massaro D. 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 1979;64:600-608. (Pubitemid 9235006)
21. D'Angelo E, Pecchiari M, Baraggia P, Saetta M, Balestro E, Milic-Emili J. Low volume ventilation causes peripheral airway injury and increased airway resistance in normal rabbits. J Appl Physiol 2002;92:949-956. (Pubitemid 34670946)
22. Young SL, Tierney DF, Clements JA. Mechanism of compliance change in excised rat lungs at low transpulmonary pressure. J Appl Physiol 1970;29:780-785.
23. Dock W. The evil sequelae of complete bed rest. JAMA 1944;125:1083-1085.
24. Drinker CK. Pulmonary edema and inflammation. An analysis of processes involved in the formation and removal of pulmonary transudates and exudates. Cambridge, MA: Harvard University Press; 1945. pp 3-106.
25. Strandberg A, Tokics L, Brismar B, Lundquist H, Hedenstierna G. Constitutional factors promoting development of atelectasis during anaesthesia. Acta Anaesthesiol Scand 1987;31:21-24. (Pubitemid 17227998)
26. Klingstedt C, Hedenstierna G, Lundquist H, Strandberg A, Tlkics L, Brismar B. The influence of body position and differential ventilation on lung dimensions and atelectasis formation in anaesthetized man. Acta Anaesthesiol Scand 1990;34:315-322. (Pubitemid 20247529)
27. Hedenstierna G, Tokics L, Lundquist H, Andersson T, Strandberg A, Brismar B. Phrenic nerve stimulation during halothane anesthesia. Effects on atelectasis. Anesthesiology 1994;80:751-760. (Pubitemid 24128937)
28. Rothen HU, Sporre B, Engberg G, Wegenius G, Reber A, Hedenstierna G. Prevention of atelectasis during general anaesthesia. Lancet 1995;345:1387-1391.
29. Neumann P, Rothen HU, Berglund JE, Valtysson J, Magnusson A, Hedenstierna G. Positive end-expiratory pressure prevents atelectasis during general anaesthesia even in the presence of a high inspired oxygen concentration. Acta Anaesthesiol Scand 1999;43:295-301. (Pubitemid 29109475)
30. Tokics L, Hedenstierna G, Strandberg A, Brismar B, Lundquist H. Lung collapse and gas exchange during general anesthesia: effects of spontaneous breathing, muscle paralysis, and positive end-expiratory pressure. Anesthesiology 1987;66:157-167. (Pubitemid 17014445)
31. Froese AB, Bryan AC. Effects of anesthesia and paralysis on diaphragmatic mechanics in man. Anesthesiology 1974;41:242-254.
32. Hoffman EA. Effect of body orientation on regional lung expansion: a computed tomographic approach. J Appl Physiol 1985;59:468-480. (Pubitemid 15249875)
33. Mutoh T, Lamm WJE, Hildebrandt J, Albert RK. Abdominal distension alters regional pleural pressures and chest wall mechanics in pigs in vivo. J Appl Physiol 1991;70:2611-2618.
34. Albert RK, Hubmayr RD. The prone position eliminates compression of the lungs by the heart. Am J Respir Crit Care Med 2000;161:1660-1665. (Pubitemid 30329045)
35. Coker PJ, Hernandez LA, Peevy K, Adkins K, Parker JC. Increased sensitivity to mechanical ventilation after surfactant inactivation in young rabbit lungs. Crit Care Med 1992;20:635-640.
36. Taskar V, John J, Evander E, Robertson B, Jonson B. Surfactant dysfunction makes lungs vulnerable to repetitive collapse and reexpansion. Am J Respir Crit Care Med 1997;155:313-320. (Pubitemid 27053182)
37. Bilek AM, Dee CY, Gaver DP III. Mechanisms of surface-tension-induced epithelial cell damage in a model of pulmonary airway reopening. J Appl Physiol 2003;94:770-783. (Pubitemid 36158257)
38. Ikegami J, Whitsett JA, Martis PC, Weaver TE. Reversibility of lung inflammation caused by SP-B deficiency. Am J Physiol Lung Cell Mol Physiol 2005;289:L962-L970. (Pubitemid 41681331)
39. Verbrugge SJC, Vasquez di Anda G, Gommers D, Neggers SJMM, Sorm V, Bohm S, Lachmann B. Exogenous surfactant preserves lung function and reduces alveolar Evans blue dye influx in a rat model of ventilation-induced lung injury. Anesthesiology 1998;89:467-474. (Pubitemid 28373437)
40. Maruscak AA, Vockeroth DW, Girardi B, Sheikh T, Possmayer F, Lewis JF, Veldhuizen RAW. Alterations to surfactant precede physiological deterioration during high tidal volume ventilation. Am J Physiol Lung Cell Mol Physiol 2008;294:L974-L983.
41. Welk B, Malloy JL, Joseph M, Yao L-J, Velduizen RQW. Surfactant treatment for ventilation-induced lung injury in rats: effects on lung compliance and cytokines. Exp Lung Res 2001;27:505-520. (Pubitemid 32826508)
42. D'Angelo E, Pecchiari M, Gentile G. Dependence of lung injury on surface tension during low-volume ventilation in normal open-chest rabbits. J Appl Physiol 2007;102:174-182. (Pubitemid 46089764)
43. Yamashita C, Forbes A, Tessolini JM, Yao L-J, Lewis JF, Veldhuizen RAW. Protective effects of elevated endogenous surfactant pools to injurions mechanical ventilation. Am J Physiol Lung Cell Mol Physiol 2008;294:L724-L732. (Pubitemid 351520105)
44. Walker MG, Tessolini JM, McCaig L, Yao L-J, Lewis JF, Veldhuizen RAW. Elevated endogenous surfactant reduces inflammation in an acute lung injury model. Exp Lung Res 2009;35:591-604.
45. Hedley-Whyte J, Laver MB, Bendizen HH. Effect of changes in tidal ventilation on physiologic shunting. Am J Physiol 1964;206:891-897.
46. Finley TN, Tooley WH, Swenson EW, Gardner RE, Clements JA. Pulmonary surface tension in experimental atelectasis. Am Rev Respir Dis 1964;89:372-378.
47. Hudson LD, Milberg JA, Anardi D, Maunder RJ. Clinical risks for development of the acute respiratory distress syndrome. Am J Respir Crit Care Med 1995;151:293-301.
48. Lewis JF, Ikegami M, Jobe AH. Altered surfactant function and metabolism in rabbits with acute lung injury. J Appl Physiol 1990;69:2303-2310.
49. Thammanomai A, Majumdar A, Bartolak-Suki E, Suki B. Effects of reduced tidal volume ventilation on pulmonary function in mice before and after acute lung injury. J Appl Physiol 2007;103:1551-1559. (Pubitemid 350033837)
50. Greene KE, Wright JR, Steinberg KP, Ruzinski JT, Caldwell E, Wong WB, Hull W, Whitsett JA, Akino T, Kuroki Y, et al. Serial changes in surfactant-associated proteins in lung and serum before and after onset of ARDS. Am J Respir Crit Care Med 1999;160:1843-1850. (Pubitemid 30004685)
51. Shambaugh GE, Harrison WG, Farrell JI. Treatment of the respiratory paralysis of poliomyletis in a respiratory chamber. JAMA 1930;94:1371-1373.
52. Ferris BG, Pollard DS. Effect of deep and quite breathing on pulmonary compliance in man. J Clin Invest 1959;39:143-149.
53. Egbert LD, Laver MB, Bendixen HH. Intermittent deep breaths and compliance during anesthesia in man. Anesthesiology 1963;24:57-60.
54. Bendixen HH, Hedley-Whyte J, Laver MB. Impaired oxygenation in surgical patients during general anesthesia with controlled ventilation. A concept of atelectasis. N Engl J Med 1963;269:991-996.
55. Laver MB, Morgan J, Bendixen HH, Radford EP. Lung volume, compliance and arterial oxygen tensions during controlled ventilation. J Appl Physiol 1964;19:725-733.
56. Caro CG, Butler J, DuBois AB. Some effects of restriction of chest cage expansion on pulmonary function in man: an experimental study. J Clin Invest 1960;39:573-583.
57. Pattle RE. Surface lining of lung alveoli. Physiol Rev 1965;45:48-79.
58. Nicholas TE, Barr HA. The release of surfactant in rat lung by brief periods of hyperventilation. Respir Physiol 1983;52:69-83. (Pubitemid 13124930)
59. Massaro GD, Massaro D. Morphologic evidence that large inflations of the lung stimulate secretion of surfactant. Am Rev Respir Dis 1983;127:235-236. (Pubitemid 13146552)
60. Hildebran JN, Goerke J, Clements JA. Surfactant release in excised rat lung is stimulated by air inflation. J Appl Physiol 1981;51:905-910. (Pubitemid 11007460)
61. Wirtz RW, Dobbs LG. Calcium mobilization and exocytosis after one mechanical stretch of lung epithelial cells. Science 1990;250:1266.
62. Oyarzun MJ, Iturriaga R, Donoso P, Dussaubat N, Santos M, Schiappacasse ME, Lathrop ME, Larrain C, Zapata P. Factors affecting distribution of alveolar surfactant during resting ventilation. Am J Physiol 1991;261:L210-L217.
63. Mutch WAC, Harms S, Graham MR, Kowalski SE, Girling LG, Lefevre GR. Biologically variable or naturally noisy mechanical ventilation recruits atelectactatic lung. Am J Respir Crit Care Med 2000;162:319-323. (Pubitemid 30469840)
64. Mutch WA, Eschun GM, Kowalski SE, Graham MR, Girling LG, Lefevre GR. Biologically variable ventilation prevents deterioration of gas exchange during prolonged anaesthesia. Br J Anaesth 2000;84:197-203. (Pubitemid 30060304)
65. Arold SP, Suki B, Alencar AM, Lutchen KR, Ingenito EP. Variable ventilation induces endogenous surfactant release in normal guinea pigs. Am J Physiol Lung Cell Mol Physiol 2000;285:370-375.
66. Arold SP, Mora R, Lutchen KR, Ingenito EP, Suki B. Variable tidal volume ventilation improves mechanics and gas exchange in a rodent model of acute lung injury. Am J Respir Crit Care Med 2002;165:366-371. (Pubitemid 34118510)
67. Boker A, Graham MR, Walley KR, McManus BM, Girling LG, Walker E, Lefevre GR, Mutch WA. Improved arterial oxygenation with biologically variable or fractal ventilation using low tidal volumes in a procine model of acute respiratory distress syndrome. Am J Respir Crit Care Med 2002;165:456-462. (Pubitemid 34165467)
68. Mutch WAC, Harms S, Lefevre GR, Graham MR, Girling LG, Kowalski SE. Biologically variable ventilation increases arterial oxygenation over that seen with positive end-expiratory pressure alone in a porcine model of acute respiratory distress syndrome. Crit Care Med 2000;28:2457-2464. (Pubitemid 30604454)
69. Pelosi P, Cadringher P, Bottino N, Panigada M, Carrieri F, Riva E. Sigh in acute respiratory distress syndrome. Am J Respir Crit Care Med 1999;159:872-880. (Pubitemid 29137788)
70. Patroniti N, Foti G, Cortinovis B, Maggioni E, Bigatello LM, Cereda M, Pesenti A. Sigh improves gas exchange and lung volume in patients with acute respiratory distress syndrome undergoing pressure support ventilation. Anesthesiology 2002;96:788-794. (Pubitemid 34266670)
71. Mascheroni D, Kolobow T, Fumagalli R, Moretti MP, Chen V, Buckhold D. Acute respiratory failure following pharmacologically induced hyperventilation: an experimental animal study. Intensive Care Med 1988;15:8-14. (Pubitemid 19012889)
72. Oyarzun MJ, Clements JA. Ventilatiory and cholinergic control of pulmonary surfactant in the rabbit. J Appl Physiol 1977;43:39-45. (Pubitemid 8169326)
73. Verbrugge SJC, Boghm SH, Gommers D, Zommerman LJI, Lachmann B. Surfactant impairment after mechanical ventilation with large alveolar surface area changes and effects of positive-end expiratory pressure. Br J Anaesth 1998;80:360-364. (Pubitemid 28105473)
74. Liu S, Margulies SS, Wilson TA. Deformation of the dog lung in the chest wall. J Appl Physiol 1990;68:1979-1987. (Pubitemid 20183086)
75. Hubmayr RD, Walters JB, Chevalier PA, Rodarte JR, Olson LE. Topographical distribution of regional lung volume in anesthetized dogs. J Appl Physiol 1983;54:1048-1056. (Pubitemid 13123922)
76. Wiener-Kronish JP, Gropper MA, Lai-Fook SJ. Pleural liquid pressure in dogs measured using a rib capsule. J Appl Physiol 1985;59:597-602. (Pubitemid 15248980)
77. Mutoh T, Guest RJ, Lamm WJE, Albert RK. Prone position alters the effect of volume overload on regional pleural pressures and improves hypoxemia in pigs in-vivo. Am Rev Respir Dis 1992;146:300-306.
78. Lai-Fook SJ, Beck KC, Sothorn PA. Pleural liquid pressure measured by micropipettes in rabbits. J Appl Physiol 1984;56:1633-1639. (Pubitemid 14122639)
79. Yang Q-H, Kaplowitz MR, Lai-Fook SJ. Regional variations in lung expansion in rabbits: prone vs supine positions. J Appl Physiol 1989;67:1371-1376. (Pubitemid 19276385)
80. Broccard AF, Shapiro RS, Schmitz LL, Ravenscraft SA, Marini JJ. Influence of prone position on the extent and distribution of lung injury in a high tidal volume oleic acid model of acute respiratory distress syndrome. Crit Care Med 1997;25:16-27.
81. Houseley E, Louzada N, Becklake MR. To sigh or not to sigh. Am Rev Respir Dis 1970;101:611-614.
82. Davis K, Branson RD, Campbell RS, Porembka DT, Johnson DJ. The addition of sighs during pressure support ventilation. Is there a benefit. Chest 1993;104:867-870. (Pubitemid 23268963)
83. Levine M, Gilbert R, Auchincloss JH Jr. A comparison of the effects of sighs, large tidal volumes, and positive end-expiratory pressure in assisted ventilation. Scand J Respir Dis 1972;53:101-108.
84. Pepe PE, Hudson LD, Carrico CJ. Early application of positive end-expiratory pressure in patients at risk for the adult respiratory distress syndrome. N Engl J Med 1984;311:281-286. (Pubitemid 14091205)