Epithelial and endothelial damage induced by mechanical ventilation modes

Current Opinion in Critical Care

Volumn 20, Issue 1, 2014, Pages 17-24

  Suki, Béla ^a   Hubmayr, Rolf ^b  

^a Boston University   (United States)

^b MAYO CLINIC   (United States)

Author keywords

cell wounding; heterogeneity; lung injury; mechanics; stress failure

Indexed keywords

ADULT; FEMALE; HEMODYNAMICS; HUMANS; LUNG INJURY; MALE; OXIDATIVE STRESS; PULMONARY ALVEOLI; PULMONARY GAS EXCHANGE; RESPIRATION, ARTIFICIAL; RESPIRATORY DISTRESS SYNDROME, ADULT; RESPIRATORY MUCOSA; TIDAL VOLUME;

EID: 84895069998     PISSN: 10705295     EISSN: 15317072     Source Type: Journal    
DOI: 10.1097/MCC.0000000000000043     Document Type: Review

References (84)

1. Rubenfeld GD, Caldwell E, Peabody E, et al. Incidence and outcomes of acute lung injury. N Engl J Med 2005; 353:1685-1693.
2. Ferguson ND, Fan E, Camporota L, et al. The Berlin definition of ARDS: an expanded rationale, justification, and supplementary material. Intensive Care Med 2012; 38:1573-1582.
3. Zilberberg MD, Epstein SK. Acute lung injury in the medical ICU: comorbid conditions, age, etiology, and hospital outcome. Am J Respir Crit Care Med 1998; 157 (4 Pt 1):1159-1164.
4. Arroliga AC, Ghamra ZW, Perez Trepichio A, et al. Incidence of ARDS in an adult population of northeast Ohio. Chest 2002; 121:1972-1976.
5. The Acute Respiratory Distress Syndrome Network. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. N Engl J Med 2000; 342:1301- 1308.
6. Yilmaz M, Keegan MT, Iscimen R, et al. Toward the prevention of acute lung injury: protocol-guided limitation of large tidal volume ventilation and inappropriate transfusion. Crit Care Med 2007; 35:1660-1666.
7. Lin YC, Tambe DT, Park CY, et al. Mechanosensing of substrate thickness. Phys Rev E Stat Nonlin Soft Matter Phys 2013; 82 (4 Pt 1):041918.
8. Washko GR, O'Donnell CR, Loring SH. Volume-related and volume-independent effects of posture on esophageal and transpulmonary pressures in healthy subjects. J Appl Physiol 2006; 100:753-758.
9. Muscedere JG, Mullen JB, Gan K, Slutsky AS. Tidal ventilation at low airway pressures can augment lung injury. Am J Respir Crit Care Med 1994; 149:1327-1334.
10. Chu EK, Whitehead T, Slutsky AS. Effects of cyclic opening and closing at low- and high-volume ventilation on bronchoalveolar lavage cytokines. Crit Care Med 2004; 32:168-174.
11. Hussein O, Walters BJ, Stroetz RW, et al. Biophysical determinants of alveolar epithelial plasma membrane wounding associated with mechanical ventilation. Am J Physiol 2013; 305:L478-L484.
12. Otis DR Jr, Petak F, Hantos Z, et al. Airway closure and reopening assessed by the alveolar capsule oscillation technique. J Appl Physiol 1996; 80:2077- 2084.
13. Gattinoni L, Pesenti A. The concept of 'baby lung'. Intensive Care Med 2005; 31:776-784.
14. Carvalho AR, Pacheco SA, de Souza Rocha PV, et al. Detection of tidal recruitment/overdistension in lung-healthy mechanically ventilated patients under general anesthesia. Anesth Analg 2013; 116:677-684.
15. Zannin E,Dellaca RL, Kostic P, et al.Optimizing positive end-expiratory pressure by oscillatory mechanics minimizes tidal recruitment and distension: an experimental study in a lavage model of lung injury. Crit Care 2012; 16:R217.
16. Mascheroni D, Kolobow T, Fumagalli R, et al. Acute respiratory failure following pharmacologically induced hyperventilation: an experimental animal study. Intensive Care Med 1988; 15:8-14.
17. Veldhuizen RA, Welk B, Harbottle R, et al. Mechanical ventilation of isolated rat lungs changes the structure and biophysical properties of surfactant. J Appl Physiol 2002; 92:1169-1175.
18. Egan EA. Lung inflation, lung solute permeability, and alveolar edema. J Appl Physiol 1982; 53:121-125.
19. Wray C, Mao Y, Pan J, et al. Claudin-4 augments alveolar epithelial barrier function and is induced in acute lung injury. Am J Physiol Lung Cell Mol Physiol 2009; 297:L219-L227.
20. Gajic O, Lee J, Doerr CH, et al. Ventilator-induced cell wounding and repair in the intact lung. Am J Respir Crit Care Med 2003; 167:1057-1063.
21. Pecchiari M, Monaco A, Koutsoukou A, D'Angelo E. Plasma membrane disruptions with different modes of injurious mechanical ventilation in normal rat lungs-. Crit Care Med 2012; 40:869-875.
22. Hubmayr RD. Perspective on lung injury and recruitment: a skeptical look at the opening and collapse story. Am J Respir Crit Care Med 2002; 165:1647- 1653.
23. Martynowicz MA, Minor TA, Walters BJ, Hubmayr RD. Regional expansion of oleic acid-injured lungs. Am J Respir Crit Care Med 1999; 160:250-258.
24. Brewer KK, Sakai H, Alencar AM, et al. Lung and alveolar wall elastic and hysteretic behavior in rats: Effects of in vivo elastase treatment. J Appl Physiol 2003; 95:1926-1936.
25. Azeloglu EU, Bhattacharya J, Costa KD. Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness. J Appl Physiol 2008; 105:652-661.
26. Hadi MF, Sander EA, Barocas VH. Multiscale model predicts tissue-level failure from collagen fiber-level damage. J Biomech Eng 2012; 134:091005.
27. Ritter MC, Jesudason R, Majumdar A, et al. A zipper network model of the failure mechanics of extracellular matrices. Proc Natl Acad Sci U S A 2009; 106:1081-1086.
28. Cavanaugh KJ Jr, Margulies SS. Measurement of stretch-induced loss of alveolar epithelial barrier integrity with a novel in vitro method. Am J Physiol Cell Physiol 2002; 283:C1801-C1808.
29. Vlahakis NE, Schroeder MA, Pagano RE, Hubmayr RD. Role of deformationinduced lipid trafficking in the prevention of plasma membrane stress failure. Am J Respir Crit Care Med 2002; 166:1282-1289.
30. West JB, Mathieu-Costello O. Stress failure of pulmonary capillaries in the intensive care setting. Schweiz Med Wochenschr 1992; 122:751-757.
31. West JB, Tsukimoto K, Mathieu-Costello O, Prediletto R. Stress failure in pulmonary capillaries. J Appl Physiol 1991; 70:1731-1742.
32. Perlman CE, Lederer DJ, Bhattacharya J. Micromechanics of alveolar edema. Am J Respir Cell Mol Biol 2011; 44:34-39.
33. Bilek AM, Dee KC, Gaver DP 3rd. Mechanisms of surface-tension-induced epithelial cell damage in a model of pulmonary airway reopening. J Appl Physiol 2003; 94:770-783.
34. Huh D, Fujioka H, Tung YC 3rd, et al. Acoustically detectable cellular-level lung injury induced by fluid mechanical stresses in microfluidic airway systems. Proc Natl Acad Sci U S A 2007; 104:18886-18891.
35. Van Citters KM, Hoffman BD, Massiera G, Crocker JC. The role of f-Actin and myosin in epithelial cell rheology. Biophys J 2006; 91:3946-3956.
36. Suki B, Stamenovic D, Hubmayr RD. Lung parenchymal mechanics. Compr Physiol 2011; 1:1317-1351.
37. Potard US, Butler JP, Wang N. Cytoskeletal mechanics in confluent epithelial cells probed through integrins and e-cadherins. Am J Physiol 1997; 272 (5 Pt 1):C1654-C1663.
38. Reiss LK, Uhlig U, Uhlig S. Models and mechanisms of acute lung injury caused by direct insults. Eur J Cell Biol 2012; 91:590-601.
39. Krause MF, Wiemann T, Reisner A, et al. Surfactant reduces extravascular lung water and invasion of polymorphonuclear leukocytes into the lung in a piglet model of airway lavage. Pulm Pharmacol Ther 2005; 18:129-139.
40. Hamanaka K, Jian MY, Weber DS, et al. Trpv4 initiates the acute calciumdependent permeability increase during ventilator-induced lung injury in isolated mouse lungs. Am J Physiol Lung Cell Mol Physiol 2007; 293:L923-L932.
41. Frank JA, Wray CM, McAuley DF, et al. Alveolar macrophages contribute to alveolar barrier dysfunction in ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol 2006; 291:L1191-L1198.
42. Birukova AA, Fu P, Xing J, et al. Mechanotransduction by gef-h1 as a novel mechanism of ventilator-induced vascular endothelial permeability. Am J Physiol Lung Cell Mol Physiol 2010; 298:L837-L848.
43. Yager D, Feldman H, Fung YC. Microscopic vs. macroscopic deformation of the pulmonary alveolar duct. J Appl Physiol 1992; 72:1348-1354.
44. Dreyfuss D, Basset G, Soler P, Saumon G. Intermittent positive-pressure hyperventilation with high inflation pressures produces pulmonary microvascular injury in rats. Am Rev Respir Dis 1985; 132:880-884.
45. Godin LM, Vergen J, Prakash YS, et al. Spatiotemporal dynamics of actin remodeling and endomembrane trafficking in alveolar epithelial type I cell wound healing. Am J Physiol 2013; 300:L615-L623.
46. Gil J, Bachofen H, Gehr P, Weibel ER. Alveolar volume-surface area relation in air- and saline-filled lungs fixed by vascular perfusion. J Appl Physiol 1979; 47:990-1001.
47. Tschumperlin DJ, Margulies SS. Alveolar epithelial surface area-volume relationship in isolated rat lungs. J Appl Physiol 1999; 86:2026-2033.
48. Stroetz RW, Vlahakis NE, Walters BJ, et al. Validation of a new live cell strain system: characterization of plasma membrane stress failure. J Appl Physiol 2001; 90:2361-2370.
49. Tschumperlin DJ, Margulies SS. Equibiaxial deformation-induced injury of alveolar epithelial cells in vitro. Am J Physiol 1998; 275 (6 Pt 1):L1173-L1183.
50. Oeckler RA, Lee WY, Park MG, et al. Determinants of plasma membrane wounding by deforming stress. Am J Physiol Lung Cell Mol Physiol 2010; 299:L826-L833.
51. Krishnan R, Klumpers DD, Park CY, et al. Substrate stiffening promotes endothelial monolayer disruption through enhanced physical forces. Am J Physiol Cell Physiol 2011; 300:C146-C154.
52. Roan E, Wilhelm K, Bada A, et al. Hyperoxia alters the mechanical properties of alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 2012; 302:L1235-L1241.
53. Charras GT, Coughlin M, Mitchison TJ, Mahadevan L. Life and times of a cellular bleb. Biophys J 2008; 94:1836-1853.
54. Gaver DP 3rd, Kute SM. A theoretical model study of the influence of fluid stresses on a cell adhering to a microchannel wall. Biophys J 1998; 75:721- 733.
55. DiPaolo BC, Lenormand G, Fredberg JJ, Margulies SS. Stretch magnitude and frequency-dependent actin cytoskeleton remodeling in alveolar epithelia. Am J Physiol Cell Physiol 2010; 299:C345-C353.
56. Mead J, Takishima T, Leith D. Stress distribution in lungs: a model of pulmonary elasticity. J Appl Physiol 1970; 28:596-608.
57. 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.
58. Protti A, Andreis DT, Iapichino GE, et al. High positive end-expiratory pressure: only a dam against oedema formation? Crit Care 2013; 17:R131.
59. Dreyfuss D, Saumon G. Role of tidal volume, FRC, and end-inspiratory volume in the development of pulmonary edema following mechanical ventilation. Am Rev Respir Dis 1993; 148:1194-1203.
60. Albert RK. The role of ventilation-induced surfactant dysfunction and atelectasis in causing acute respiratory distress syndrome. Am J Respir Crit Care Med 2012; 185:702-708.
61. Perez-Gil J, Weaver TE. Pulmonary surfactant pathophysiology: current models and open questions. Physiology (Bethesda) 2010; 25:132-141.
62. Fabry B, Maksym GN, Butler JP, et al. Time scale and other invariants of integrative mechanical behavior in living cells. Phys Rev E Stat Nonlin Soft Matter Phys 2003; 68 (4 Pt 1):041914.
63. Pelosi P, Negrini D. Extracellular matrix and mechanical ventilation in healthy lungs: back to baro/volotrauma? Curr Opin Crit Care 2008; 14:16-21.
64. Tremblay LN, Slutsky AS. Ventilator-induced injury: from barotrauma to biotrauma. Proc Assoc Am Phys 1998; 110:482-488.
65. Protti A, Andreis DT, Monti M, et al. Lung stress and strain during mechanical ventilation: any difference between statics and dynamics? Crit Care Med 2013; 41:1046-1055.
66. Tschumperlin DJ, Oswari J, Margulies AS. Deformation-induced injury of alveolar epithelial cells. Effect of frequency, duration, and amplitude. Am J Respir Crit Care Med 2000; 162 (2 Pt 1):357-362.
67. Wellman TJ, Winkler T, Costa EL, et al. Effect of regional lung inflation on ventilation heterogeneity at different length scales during mechanical ventilation of normal sheep lungs. J Appl Physiol 2012; 113:947-957.
68. Marks JD, Luce JM, Lazar NM, et al. Effect of increases in lung volume on clearance of aerosolized solute from human lungs. J Appl Physiol 1985; 59:1242-1248.
69. Garcia CS, Abreu SC, Soares RM, et al. Pulmonary morphofunctional effects of mechanical ventilation with high inspiratory air flow. Crit Care Med 2008; 36:232-239.
70. Steimback PW, Oliveira GP, Rzezinski AF, et al. Effects of frequency and inspiratory plateau pressure during recruitment manoeuvres on lung and distal organs in acute lung injury. Intensive Care Med 2009; 35:1120-1128.
71. Barbas CS, de Matos GF, Okamoto V, et al. Lung recruitment maneuvers in acute respiratory distress syndrome. Respir Care Clin N Am 2003; 9:401- 418.
72. Thammanomai A, Hamakawa H, Bartolak-Suki E, Suki B. Combined effects of ventilation mode and positive end-expiratory pressure on mechanics, gas exchange and the epithelium in mice with acute lung injury. PLoS One 2013; 8:e53934.
73. Santiago VR, Rzezinski AF, Nardelli LM, et al. Recruitment maneuver in experimental acute lung injury: the role of alveolar collapse and edema. Crit Care Med 2010; 38:2207-2214.
74. Lefevre GR, Kowalski SE, Girling LG, et al. Improved arterial oxygenation after oleic acid lung injury in the pig using a computer-controlled mechanical ventilator. Am J Respir Crit Care Med 1996; 154:1567-1572.
75. Arold SP, Mora R, Lutchen KR, et al. Variable tidal volume ventilation improves lung mechanics and gas exchange in a rodent model of acute lung injury. Am J Respir Crit Care Med 2002; 165:366-371.
76. Arold SP, Suki B, Alencar AM, et al. Variable ventilation induces endogenous surfactant release in normal guinea pigs. Am J Physiol Lung Cell Mol Physiol 2003; 285:L370-L375.
77. Funk DJ, Graham MR, Girling LG, et al. A comparison of biologically variable ventilation to recruitment manoeuvres in a porcine model of acute lung injury. Respir Res 2004; 22:5.
78. Spieth PM, Carvalho AR, Pelosi P, et al. Variable tidal volumes improve lung protective ventilation strategies in experimental lung injury. Am J Respir Crit Care Med 2009; 179:684-693.
79. Suki B, Alencar AM, Sujeer MK, et al. Life-support system benefits from noise. Nature 1998; 393:127-128.
80. Arold SP, Bartolak-Suki E, Suki B. Variable stretch pattern enhances surfactant secretion in alveolar type ii cells in culture. Am J Physiol Lung Cell Mol Physiol 2009; 296:L574-L581.
81. John J, Taskar V, Evander E, et al. Additive nature of distension and surfactant perturbation on alveolocapillary permeability. Eur Respir J 1997; 10:192- 199.
82. Dubrovskyi O, Birukova AA, Birukov KG. Measurement of local permeability at subcellular level in cell models of agonist- and ventilator-induced lung injury. Lab Invest 2013; 93:254-263.
83. Birukova AA, Tian Y, Meliton A, et al. Stimulation of rho signaling by pathologic mechanical stretch is a 'second hit' to rho-independent lung injury induced by IL-6. Am J Physiol Lung Cell Mol Physiol 2012; 302:L965-L975.
84. Birukov KG. Small GTPases in mechanosensitive regulation of endothelial barrier. Microvasc Res 2009; 77:46-52.