Overview of ventilator-induced lung injury mechanisms

Current Opinion in Critical Care

Volumn 11, Issue 1, 2005, Pages 82-86

  Lionetti, Vincenzo ^a   Recchia, Fabio A ^a   Ranieri, V Marco ^b  

^a Settore di Scienze Mediche   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Apoptosis; Inflammation; Necrosis; Polymorphonuclear cells; Ventilator induced lung injury

Indexed keywords

ADULT RESPIRATORY DISTRESS SYNDROME; APOPTOSIS; ARTIFICIAL VENTILATION; ENDOTHELIUM CELL; HUMAN; IMMUNE RESPONSE; IMMUNITY; INFLAMMATION; LUNG ALVEOLUS EPITHELIUM; LUNG INJURY; MECHANOTRANSDUCTION; MYOTATIC REFLEX; NECROSIS; NEUTROPHIL; REVIEW; SAFETY; SIGNAL TRANSDUCTION; SURVIVAL RATE; VASCULAR ENDOTHELIUM; VENTILATOR;

ANIMALS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HUMANS; INFLAMMATION; LUNG; NECROSIS; NEUTROPHILS; RESPIRATION, ARTIFICIAL; RESPIRATORY DISTRESS SYNDROME, ADULT; RESPIRATORY MUCOSA; STRESS, MECHANICAL; VENTILATORS, MECHANICAL;

EID: 13644261364     PISSN: 10705295     EISSN: None     Source Type: Journal    
DOI: 10.1097/00075198-200502000-00013     Document Type: Review

References (54)

1. 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.
2. The Acute Respiratory Distress Syndrome Network: Higher versus lower positive end-expiratory pressures in patients with the acute respiratory distress syndrome. N Engl J Med 2004; 351:327-336.
3. Dos Santos CC, Slutsky AS: Protective ventilation of patients with acute respiratory distress syndrome. Crit Care 2004; 8:145-147.
4. Ranieri VM, Suter PM, Tortorella C, et al. Effect of mechanical ventilation on inflammatory mediators in patients with acute respiratory distress syndrome: a randomized controlled trial. JAMA 1999; 282:54-61.
5. Uhlig S, Ranieri M, Slutsky AS: Biotrauma hypothesis of ventilator-induced lung injury. Am J Respir Crit Care Med 2004; 169:314-315.
6. Offner PJ, Moore EE: Lung injury severity scoring in the era of lung protective mechanical ventilation: the PaO2/FlO2 ratio. J Trauma 2003; 55:285-289.
7. Slutsky AS, Tremblay LN: Multiple system organ failure: is mechanical ventilation a contributing factor? Am J Respir Crit Care Med 1998; 157:1721-1725.
8. Gurkan OU, O'Donnell C, Brower R, et al. Differential effects of mechanical ventilatory strategy on lung injury and systemic organ inflammation in mice. Am J Physiol Lung Cell Mol Physiol 2003; 285:L710-L718.
9. Shimabukuro DW, Sawa T, Gropper MA: Injury and repair in lung and airways. Crit Care Med 2003; 31(8 Suppl):S524-S531. This review highlights a tutorial approach to understanding the mechanisms that result in acute inflammation of the lung. The authors describe the potential mechanisms of injury and repair in the lung affected by ALI/ARDS.
10. Waters CM, Sporn PH, Liu M, et al. Cellular biomechanics in the lung. Am J Physiol Lung Cell Mol Physiol 2002; 283:L503-L509.
11. Fisher JL, Margulies SS: Na(+)-K(+)-ATPase activity in alveolar epithelial cells increases with cyclic stretch. Am J Physiol Lung Cell Mol Physiol 2002; 283:L737-L746.
12. Kumar A, Lnu S, Malya R, et al. Mechanical stretch activates nuclear factor-kappaB, activator protein-1, and mitogen-activated protein kinases in lung parenchyma: implications in asthma. FASEB J 2003; 17:1800-1811.
13. 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; 162:357-362.
14. Fisher JL, Levitan I, Margulies SS: Plasma membrane surface increases with tonic stretch of alveolar epithelial cells. Am J Respir Cell Mol Biol 2004; 31:200-208. Using an alveolar epithelial cell stretch system, confocal microscopy, and fluorescent markers, the authors demonstrated the importance of additional phospholipid recruitment in plasma membrane expansion during tonic stretch of the attached basal surface. They demonstrated that this plasma membrane remodeling preponderates in the changes in cell surface shape and size demanded by stretching the cell, and, by using specific inhibitors, they showed that phospholipid insertion is unaffected by F-actin disassembly, ATP depletion, and calcium deprivation.
15. Sanchez-Esteban J, Wang Y, Gruppuso PA, et al. Mechanical stretch induces fetal type II cell differentiation via an epidermal growth factor receptor-extracellular-regulated protein kinase signaling pathway. Am J Respir Cell Mol Biol 2004; 30:76-83.
16. Tschumperlin DJ, Dai G, Maly IV, et al. Mechanotransduction through growth-factor shedding into the extracellular space. Nature 2004; 429:83-86. The authors demonstrated for the first time, in isolated perfused mouse lung model and normal human bronchial epithelial cells, that compressive stress shrinks the lateral intercellular space surrounding epithelial cells and triggers cellular signaling via autocrine binding of epidermal growth factor family ligands to the epidermal growth factor receptor, operating in a dynamically regulated extracellular volume. This establish a novel mechanotransduction system that is independent of force-dependent biochemical processes within the cell or cell membrane. In addition, they demonstrated by mathematical analysis that this mechanism is predictable.
17. Vlahakis NE, Hubmayr RD: Response of alveolar cells to mechanical stress. Curr Opin Crit Care 2003; 9:2-8. This is a comprehensive review of the effects of mechanical stretch on alveolar cells. The authors focused on the intracellular signal transduction pathways, the surfactant system, and cell injury and repair.
18. Bailey TC, Martin EL, Zhao L, et al. High oxygen concentrations predispose mouse lungs to the deleterious effects of high stretch ventilation. J Appl Physiol 2003; 94:975-982.
19. Hammerschmidt S, Kuhn H, Grasenack T, et al. Apoptosis and necrosis induced by cyclic mechanical stretching in alveolar type II cells. Am J Respir Cell Mol Biol 2004; 30:396-402.
20. Imai Y, Parodo J, Kajikawa O, et al. Injurious mechanical ventilation and end-organ epithelial cell apoptosis and organ dysfunction in an experimental model of acute respiratory distress syndrome. JAMA 2003; 23-30;289:2104-2112. In an in vivo rabbit model, the authors showed for the first time that an injurious ventilatory strategy may lead to end-organ epithelial cell apoptosis, Fas-dependent and organ dysfunction (kidney and small intestine), with elevation of biochemical markers. They found a significant correlation between changes in soluble Fas ligand and changes in biochemical markers in patients with ARDS. This may partially explain the high rate of multiple organ dysfunction observed in patients with ARDS.
21. Vlahakis NE, Schroeder MA, Limper AH: Stretch induces cytokine release by alveolar epithelial cells in vitro. Am J Physiol 1999; 277:L167-L173.
22. Wilson MR, Choudhury S, Goddard ME, et al. High tidal volume upregulates intrapulmonary cytokines in an in vivo mouse model of ventilator- induced lung injury. J Appl Physiol 2003; 95:1385-1393.
23. Uhlig U, Fehrenbach H, Lachmann RA, et al. Phosphoinositide 3-OH kinase inhibition prevents ventilation-induced lung cell activation. Am J Respir Crit Care Med 2004; 169:201-208. Using an isolated perfused mouse lung model and an in vivo rat model, the authors focused on cell types and specific signaling mechanisms that are activated by ventilation with increased pressure/volume. This study provides evidence that after overventilation there is increased expression of interleukin-6 mRNA and NF-κB activation in alveolar macrophages and alveolar epithelial type II cells that is selectively inhibited by phosphoinositide 3-OH kinase inhibitor.
24. Bershadsky AD, Balaban NQ, Geiger B: Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 2003; 19:677-695.
25. Trepat X, Grabulosa M, Puig F, et al. Viscoelasticity of human alveolar epithelial cells subjected to stretch. Am J Physiol Lung Cell Mol Physiol 2004; 287:L1025-L1034. Using A549 cells, an inverted microscope, and an optical magnetic twisting cytometer, the authors showed that after equibiaxial stretch, which simulates mechanical ventilation, alveolar epithelial cells increase their plasma membrane viscoelasticity and stiffening in an energy-dependent and strain amplitude-dependent manner. They showed that cell stiffening is paralleled by a partial cell detachment from the substrate at high strain amplitudes, which could indicate that cell adhesions do not endure the increased tension and might contribute to the disruption of the alveolar barrier.
26. Mascarenhas MM, Day RM, Ochoa CD, et al. Low molecular weight hyaluronan from stretched lung enhances interleukin-8 expression. Am J Respir Cell Mol Biol 2004; 30:51-60.
27. Taylor KR, Trowbridge JM, Rudisill JA, et al. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J Biol Chem 2004; 279:17079-17084.
28. Orfanos SE, Mavrommati I, Korovesi I, et al. Pulmonary endothelium in acute lung injury: from basic science to the critically ill. Intensive Care Med 2004; 30:1702-1714. This is a wide-ranging review of the functions of pulmonary endothelium in ALI. The authors highlight the pathogenic mechanisms of pulmonary endothelial injury and their clinical implications in ALI/ARDS patients.
29. Czarny M, Liu J, Oh P, et al. Transient mechanoactivation of neutral sphingomyelinase in caveolae to generate ceramide. J Biol Chem 2003; 278:4424-4430.
30. Czarny M, Schnitzer JE: Neutral sphingomyelinase inhibitor scyphostatin prevents and ceramide mimics mechanotransduction in vascular endothelium. Am J Physiol Heart Circ Physiol 2004; 287:H1344-H1352. In an in vitro model using pulmonary endothelial cells, the authors extended their previous work focusing on the role of neutral sphingomyelinase and ceramides in mechanosignaling after endothelial deformation. In this study they established that after endothelial distension there is an activation of caveolar neutral sphingomyelinase as well as downstream tyrosine and mitogen-activated protein kinases by generation of the lipid second messenger ceramide.
31. Moore JE Jr, Burki E, Suciu A, et al. A device for subjecting vascular endothelial cells to both fluid shear stress and circumferential cyclic stretch. Ann Biomed Eng 1994; 22:416-422.
32. Haseneen NA, Vaday GG, Zucker S, et al. Mechanical stretch induces MMP-2 release and activation in lung endothelium: role of EMMPRIN. Am J Physiol Lung Cell Mol Physiol 2003; 284:L541-L547.
33. Kuebler WM, Uhlig U, Goldmann T, et al. Stretch activates nitric oxide production in pulmonary vascular endothelial cells in situ. Am J Respir Crit Care Med 2003; 168:1391-1398.
34. Bhattacharya S, Sen N, Yiming MT, et al. High tidal volume ventilation induces proinflammatory signaling in rat lung endothelium. Am J Respir Cell Mol Biol 2003; 28:218-224.
35. Vanderbilt JN, Mager EM, Allen L, et al. CXC chemokines and their receptors are expressed in type II cells and upregulated following lung injury. Am J Respir Cell Mol Biol 2003; 29:661-668. In an in vitro model, using freshly isolated alveolar type II epithelial cells, the authors demonstrated that type II alveolar epithelial cells produce CXC chemokines (MIP-2) and their related receptor CXCR2 in response to lung injury. These observations support a central role for the type II cell as an immunologic effector cell in the alveolus.
36. Zhang H, Downey GP, Suter PM, et al. Conventional mechanical ventilation is associated with bronchoalveolar lavage-induced activation of polymorphonuclear leukocytes: a possible mechanism to explain the systemic consequences of ventilator-induced lung injury in patients with ARDS. Anesthesiology 2002; 97:1426-1433.
37. Kawano T, Mori S, Cybulsky M, et al. Effect of granulocyte depletion in a ventilated surfactant-depleted lung. J Appl Physiol 1987; 62:27-33.
38. Choudhury S, Wilson MR, Goddard ME, et al. Mechanisms of early pulmonary neutrophil sequestration in ventilator-induced lung injury in mice. Am J Physiol Lung Cell Mol Physiol 2004. In an in vivo mouse model of VILI, the authors provide the evidence for the first time that mechanical ventilatory stress initiates pulmonary PMN sequestration early in the course of VILI associated with stretch-induced inflammatory events leading to PMN stiffening and mediated by L-selectin.
39. Jafari B, Ouyang B, Li LF, et al. Intracellular glutathione in stretch-induced cytokine release from alveolar type-2 like cells. Respirology 2004; 9:43-53.
40. Kotani M, Kotani T, Ishizaka A, et al. Neutrophil depletion attenuates interleukin-8 production in mild-overstretch ventilated normal rabbit. Crit Care Med 2004; 32:514-519.
41. Belperio JA, Keane MP, Burdick MD, et al. Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury. J Clin Invest 2002; 110:1703-1716.
42. Steinberg JM, Schiller HJ, Halter JM, et al. Alveolar instability causes early ventilator-induced lung injury independent of neutrophils. Am J Respir Crit Care Med 2003; Oct 2 (Epub ahead of print). Using an in vivo pig model of VILI and in vivo video microscopy, the authors provide evidence for the first time that unstable alveoli are subjected to VILI by surfactant-dependent and neutrophil-independent mechanism. The magnitude of alveolar instability was quantified by computer image analysis.
43. Majno G, Joris I: Apoptosis, oncosis, and necrosis: an overview of cell death. Am J Pathol 1995; 146:3-15.
44. Nishino H, Nemoto N, Lu W, et al. Significance of apoptosis in morphogenesis of human lung development: light microscopic observation using in situ DNA end-labeling and ultrastructural study. Med Electron Microsc 1999; 32:57-61.
45. Bardales RH, Xie SS, Schaefer RF, et al. Apoptosis is a major pathway responsible for the resolution of type II pneumocytes in acute lung injury. Am J Pathol 1996; 149:845-852.
46. Fischer S, Cassivi SD, Xavier AM, et al. Cell death in human lung transplantation: apoptosis induction in human lungs during ischemia and after transplantation. Ann Surg 2000; 231:424-431.
47. Oudin S, Pugin J: Role of MAP kinase activation in interleukin-8 production by human BEAS-2B bronchial epithelial cells submitted to cyclic stretch. Am J Respir Cell Mol Biol 2002; 27:107-114.
48. Jo H, Sipos K, Go YM, et al. Differential effect of shear stress on extracellular signal-regulated kinase and N-terminal Jun kinase in endothelial cells. Gi2- and Gbeta/gamma-dependent signaling pathways. J Biol Chem 1997; 272:1395-1401.
49. Correa-Meyer E, Pesce L, Guerrero C, et al. Cyclic stretch activates ERK1/2 via G proteins and EGFR in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 2002; 282:L883-L891.
50. Cardone MH, Roy N, Stennicke HR, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998; 282:1318-1321.
51. Bonni A, Brunet A, West AE, et al. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 1999; 286:1358-1362.
52. Flaherty DM, Hinde SL, Monick MM, et al. Adenovirus vectors activate survival pathways in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004; 287:L393-L401.
53. Li LF, Ouyang B, Choukroun G, et al. Stretch-induced IL-8 depends on c-Jun NH2-terminal and nuclear factor-kappaB-inducing kinases. Am J Physiol Lung Cell Mol Physiol 2003; 285:L464-L475.
54. Young MP, Manning HL, Wilson DL, et al. Ventilation of patients with acute lung injury and acute respiratory distress syndrome: has new evidence changed clinical practice? Crit Care Med 2004; 32:1260-1265.