Top

Published in:

01-04-2011 | Viewpoint

Beyond volutrauma in ARDS: the critical role of lung tissue deformation

Authors: Guillermo M Albaiceta, Lluis Blanch

Published in: Critical Care | Issue 2/2011

Abstract

Ventilator-induced lung injury (VILI) consists of tissue damage and a biological response resulting from the application of inappropriate mechanical forces to the lung parenchyma. The current paradigm attributes VILI to overstretching due to very high-volume ventilation (volutrauma) and cyclic changes in aeration due to very low-volume ventilation (atelectrauma); however, this model cannot explain some research findings. In the present review, we discuss the relevance of cyclic deformation of lung tissue as the main determinant of VILI. Parenchymal stability resulting from the interplay of respiratory parameters such as tidal volume, positive end-expiratory pressure or respiratory rate can explain the results of different clinical trials and experimental studies that do not fit with the classic volutrauma/atelectrauma model. Focusing on tissue deformation could lead to new bedside monitoring and ventilatory strategies.

Available only for authorised users

dos Santos CC, Slutsky AS: The contribution of biophysical lung injury to the development of biotrauma. Annu Rev Physiol 2006, 68: 585-618. 10.1146/annurev.physiol.68.072304.113443CrossRefPubMed

International consensus conferences in intensive care medicine. Ventilator-associated lung injury in ARDS. American Thoracic Society, European Society of Intensive Care Medicine, Societe de Reanimation Langue Francaise Intensive Care Med 1999, 25: 1444-1452. 10.1007/s001340051097

Brower RG, Shanholtz CB, Fessler HE, Shade DM, White P, Wiener CM, Teeter JG, Dodd-o JM, Almog Y, Piantadosi S: Prospective, randomized, controlled clinical trial comparing traditional versus reduced tidal volume ventilation in acute respiratory distress syndrome patients. Crit Care Med 1999, 27: 1492-1498. 10.1097/00003246-199908000-00015CrossRefPubMed

Amato MB, Barbas CS, Medeiros DM, Magaldi RB, Schettino GP, Lorenzi-Filho G, Kairalla RA, Deheinzelin D, Munoz C, Oliveira R, Takagaki TY, Carvalho CR: Effect of a protective-ventilation strategy on mortality in the acute respiratory distress syndrome. N Engl J Med 1998, 338: 347-354. 10.1056/NEJM199802053380602CrossRefPubMed

Brochard L, Roudot-Thoraval F, Roupie E, Delclaux C, Chastre J, Fernandez-Mondejar E, Clementi E, Mancebo J, Factor P, Matamis D, Ranieri M, Blanch L, Rodi G, Mentec H, Dreyfuss D, Ferrer M, Brun-Buisson C, Tobin M, Lemaire F: Tidal volume reduction for prevention of ventilator-induced lung injury in acute respiratory distress syndrome. The Multicenter Trail Group on Tidal Volume reduction in ARDS. Am J Respir Crit Care Med 1998, 158: 1831-1838.CrossRefPubMed

Stewart TE, Meade MO, Cook DJ, Granton JT, Hodder RV, Lapinsky SE, Mazer CD, McLean RF, Rogovein TS, Schouten BD, Todd TR, Slutsky AS: Evaluation of a ventilation strategy to prevent barotrauma in patients at high risk for acute respiratory distress syndrome. Pressure- and Volume-Limited Ventilation Strategy Group. N Engl J Med 1998, 338: 355-361. 10.1056/NEJM199802053380603CrossRefPubMed

Ranieri VM, Suter PM, Tortorella C, De Tullio R, Dayer JM, Brienza A, Bruno F, Slutsky AS: Effect of mechanical ventilation on inflammatory mediators in patients with acute respiratory distress syndrome: a randomized controlled trial. JAMA 1999, 282: 54-61. 10.1001/jama.282.1.54CrossRefPubMed

Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network N Engl J Med 2000, 342: 1301-1308. 10.1056/NEJM200005043421801

Brower RG, Lanken PN, MacIntyre N, Matthay MA, Morris A, Ancukiewicz M, Schoenfeld D, Thompson BT: Higher versus lower positive end-expiratory pressures in patients with the acute respiratory distress syndrome. N Engl J Med 2004, 351: 327-336. 10.1056/NEJMoa032193CrossRefPubMed

10.

Villar J, Kacmarek RM, Perez-Mendez L, Aguirre-Jaime A: A high positive end-expiratory pressure, low tidal volume ventilatory strategy improves outcome in persistent acute respiratory distress syndrome: a randomized, controlled trial. Crit Care Med 2006, 34: 1311-1318. 10.1097/01.CCM.0000215598.84885.01CrossRefPubMed

11.

Mercat A, Richard JC, Vielle B, Jaber S, Osman D, Diehl JL, Lefrant JY, Prat G, Richecoeur J, Nieszkowska A, Gervais C, Baudot J, Bouadma L, Brochard L: Positive end-expiratory pressure setting in adults with acute lung injury and acute respiratory distress syndrome: a randomized controlled trial. JAMA 2008, 299: 646-655. 10.1001/jama.299.6.646CrossRefPubMed

12.

Meade MO, Cook DJ, Guyatt GH, Slutsky AS, Arabi YM, Cooper DJ, Davies AR, Hand LE, Zhou Q, Thabane L, Austin P, Lapinsky S, Baxter A, Russell J, Skrobik Y, Ronco JJ, Stewart TE: Ventilation strategy using low tidal volumes, recruitment maneuvers, and high positive end-expiratory pressure for acute lung injury and acute respiratory distress syndrome: a randomized controlled trial. JAMA 2008, 299: 637-645. 10.1001/jama.299.6.637CrossRefPubMed

13.

Talmor D, Sarge T, Malhotra A, O'Donnell CR, Ritz R, Lisbon A, Novack V, Loring SH: Mechanical ventilation guided by esophageal pressure in acute lung injury. N Engl J Med 2008, 359: 2095-2104. 10.1056/NEJMoa0708638PubMedCentralCrossRefPubMed

14.

Valenza F, Guglielmi M, Irace M, Porro GA, Sibilla S, Gattinoni L: Positive end-expiratory pressure delays the progression of lung injury during ventilator strategies involving high airway pressure and lung overdistention. Crit Care Med 2003, 31: 1993-1998. 10.1097/01.CCM.0000070401.65534.F9CrossRefPubMed

15.

Vlahakis NE, Hubmayr RD: Cellular stress failure in ventilator-injured lungs. Am J Respir Crit Care Med 2005, 171: 1328-1342. 10.1164/rccm.200408-1036SOPubMedCentralCrossRefPubMed

16.

Ridge KM, Linz L, Flitney FW, Kuczmarski ER, Chou YH, Omary MB, Sznajder JI, Goldman RD: Keratin 8 phosphorylation by protein kinase C delta regulates shear stress-mediated disassembly of keratin intermediate filaments in alveolar epithelial cells. J Biol Chem 2005, 280: 30400-30405. 10.1074/jbc.M504239200CrossRefPubMed

17.

Bilek AM, Dee KC, Gaver DP: Mechanisms of surface-tension-induced epithelial cell damage in a model of pulmonary airway reopening. J Appl Physiol 2003, 94: 770-783. 10.1063/1.1582234CrossRefPubMed

18.

Mead J, Takishima T, Leith D: Stress distribution in lungs: a model of pulmonary elasticity. J Appl Physiol 1970, 28: 596-608.PubMed

19.

Steinberg JM, Schiller HJ, Halter JM, Gatto LA, Lee HM, Pavone LA, Nieman GF: Alveolar instability causes early ventilator-induced lung injury independent of neutrophils. Am J Respir Crit Care Med 2004, 169: 57-63. 10.1164/rccm.200304-544OCCrossRefPubMed

20.

Manzano F, Fernandez-Mondejar E, Colmenero M, Poyatos ME, Rivera R, Machado J, Catalan I, Artigas A: Positive-end expiratory pressure reduces incidence of ventilator-associated pneumonia in nonhypoxemic patients. Crit Care Med 2008, 36: 2225-2231. 10.1097/CCM.0b013e31817b8a92CrossRefPubMed

21.

Wolthuis EK, Vlaar AP, Choi G, Roelofs JJ, Juffermans NP, Schultz MJ: Mechanical ventilation using non-injurious ventilation settings causes lung injury in the absence of pre-existing lung injury in healthy mice. Crit Care 2009, 13: R1. 10.1186/cc7688PubMedCentralCrossRefPubMed

22.

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. 10.1007/BF00255628CrossRefPubMed

23.

Wrigge H, Uhlig U, Zinserling J, Behrends-Callsen E, Ottersbach G, Fischer M, Uhlig S, Putensen C: The effects of different ventilatory settings on pulmonary and systemic inflammatory responses during major surgery. Anesth Analg 2004, 98: 775-781. 10.1213/01.ANE.0000100663.11852.BFCrossRefPubMed

24.

Wrigge H, Zinserling J, Stuber F, von Spiegel T, Hering R, Wetegrove S, Hoeft A, Putensen C: Effects of mechanical ventilation on release of cytokines into systemic circulation in patients with normal pulmonary function. Anesthesiology 2000, 93: 1413-1417. 10.1097/00000542-200012000-00012CrossRefPubMed

25.

Michelet P, D'Journo XB, Roch A, Doddoli C, Marin V, Papazian L, Decamps I, Bregeon F, Thomas P, Auffray JP: Protective ventilation influences systemic inflammation after esophagectomy: a randomized controlled study. Anesthesiology 2006, 105: 911-919. 10.1097/00000542-200611000-00011CrossRefPubMed

26.

Wrigge H, Uhlig U, Baumgarten G, Menzenbach J, Zinserling J, Ernst M, Dromann D, Welz A, Uhlig S, Putensen C: Mechanical ventilation strategies and inflammatory responses to cardiac surgery: a prospective randomized clinical trial. Intensive Care Med 2005, 31: 1379-1387. 10.1007/s00134-005-2767-1CrossRefPubMed

27.

Schilling T, Kozian A, Huth C, Buhling F, Kretzschmar M, Welte T, Hachenberg T: The pulmonary immune effects of mechanical ventilation in patients undergoing thoracic surgery. Anesth Analg 2005, 101: 957-965. 10.1213/01.ane.0000172112.02902.77CrossRefPubMed

28.

Gajic O, Frutos-Vivar F, Esteban A, Hubmayr RD, Anzueto A: Ventilator settings as a risk factor for acute respiratory distress syndrome in mechanically ventilated patients. Intensive Care Med 2005, 31: 922-926. 10.1007/s00134-005-2625-1CrossRefPubMed

29.

Gajic O, Dara SI, Mendez JL, Adesanya AO, Festic E, Caples SM, Rana R, St Sauver JL, Lymp JF, Afessa B, Hubmayr RD: Ventilator-associated lung injury in patients without acute lung injury at the onset of mechanical ventilation. Crit Care Med 2004, 32: 1817-1824. 10.1097/01.CCM.0000133019.52531.30CrossRefPubMed

30.

Determann RM, Royakkers A, Wolthuis EK, Vlaar AP, Choi G, Paulus F, Hofstra JJ, de Graaff MJ, Korevaar JC, Schultz MJ: Ventilation with lower tidal volumes as compared with conventional tidal volumes for patients without acute lung injury: a preventive randomized controlled trial. Crit Care 2010, 14: R1. 10.1186/cc8230PubMedCentralCrossRefPubMed

31.

Pinheiro de Oliveira R, Hetzel MP, Dos Anjos Silva M, Dallegrave D, Friedman G: Mechanical ventilation with high tidal volume induces inflammation in patients without lung disease. Crit Care 2010, 14: R39. 10.1186/cc8919PubMedCentralCrossRefPubMed

32.

Fanelli V, Mascia L, Puntorieri V, Assenzio B, Elia V, Fornaro G, Martin EL, Bosco M, Delsedime L, Fiore T, Grasso S, Ranieri VM: Pulmonary atelectasis during low stretch ventilation: 'open lung' versus 'lung rest' strategy. Crit Care Med 2009, 37: 1046-1053. 10.1097/CCM.0b013e3181968e7eCrossRefPubMed

33.

Page B, Vieillard-Baron A, Beauchet A, Aegerter P, Prin S, Jardin F: Low stretch ventilation strategy in acute respiratory distress syndrome: eight years of clinical experience in a single center. Crit Care Med 2003, 31: 765-769. 10.1097/01.CCM.0000055402.68581.DCCrossRefPubMed

34.

Chiumello D, Carlesso E, Cadringher P, Caironi P, Valenza F, Polli F, Tallarini F, Cozzi P, Cressoni M, Colombo A, Marini JJ, Gattinoni L: Lung stress and strain during mechanical ventilation for acute respiratory distress syndrome. Am J Respir Crit Care Med 2008, 178: 346-355. 10.1164/rccm.200710-1589OCCrossRefPubMed

35.

Carney DE, Bredenberg CE, Schiller HJ, Picone AL, McCann UG, Gatto LA, Bailey G, Fillinger M, Nieman GF: The mechanism of lung volume change during mechanical ventilation. Am J Respir Crit Care Med 1999,160(5 Pt 1):1697-1702.CrossRef

36.

Perlman CE, Bhattacharya J: Alveolar expansion imaged by optical sectioning microscopy. J Appl Physiol 2007, 103: 1037-1044. 10.1152/japplphysiol.00160.2007CrossRefPubMed

37.

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. 10.1164/rccm.2001080-01CPCrossRefPubMed

38.

Halter JM, Steinberg JM, Gatto LA, DiRocco JD, Pavone LA, Schiller HJ, Albert S, Lee HM, Carney D, Nieman GF: Effect of positive end-expiratory pressure and tidal volume on lung injury induced by alveolar instability. Crit Care 2007, 11: R20. 10.1186/cc5695PubMedCentralCrossRefPubMed

39.

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.CrossRefPubMed

40.

Pavone LA, Albert S, Carney D, Gatto LA, Halter JM, Nieman GF: Injurious mechanical ventilation in the normal lung causes a progressive pathologic change in dynamic alveolar mechanics. Crit Care 2007, 11: R64. 10.1186/cc5940PubMedCentralCrossRefPubMed

41.

Terragni PP, Rosboch G, Tealdi A, Corno E, Menaldo E, Davini O, Gandini G, Herrmann P, Mascia L, Quintel M, Slutsky AS, Gattinoni L, Ranieri VM: Tidal hyperinflation during low tidal volume ventilation in acute respiratory distress syndrome. Am J Respir Crit Care Med 2007, 175: 160-166. 10.1164/rccm.200607-915OCCrossRefPubMed

42.

Grasso S, Stripoli T, De Michele M, Bruno F, Moschetta M, Angelelli G, Munno I, Ruggiero V, Anaclerio R, Cafarelli A, Driessen B, Fiore T: ARDSnet ventilatory protocol and alveolar hyperinflation: role of positive end-expiratory pressure. Am J Respir Crit Care Med 2007, 176: 761-767. 10.1164/rccm.200702-193OCCrossRefPubMed

43.

Caironi P, Cressoni M, Chiumello D, Ranieri M, Quintel M, Russo SG, Cornejo R, Bugedo G, Carlesso E, Russo R, Caspani L, Gattinoni L: Lung opening and closing during ventilation of acute respiratory distress syndrome. Am J Respir Crit Care Med 2009, 181: 578-586. 10.1164/rccm.200905-0787OCCrossRefPubMed

44.

Briel M, Meade M, Mercat A, Brower RG, Talmor D, Walter SD, Slutsky AS, Pullenayegum E, Zhou Q, Cook D, Brochard L, Richard JC, Lamontagne F, Bhatnagar N, Stewart TE, Guyatt G: Higher vs lower positive end-expiratory pressure in patients with acute lung injury and acute respiratory distress syndrome: systematic review and meta-analysis. JAMA 2010, 303: 865-873. 10.1001/jama.2010.218CrossRefPubMed

45.

Gattinoni L, Caironi P, Cressoni M, Chiumello D, Ranieri VM, Quintel M, Russo S, Patroniti N, Cornejo R, Bugedo G: Lung recruitment in patients with the acute respiratory distress syndrome. N Engl J Med 2006, 354: 1775-1786. 10.1056/NEJMoa052052CrossRefPubMed

46.

Albaiceta GM, Taboada F, Parra D, Luyando LH, Calvo J, Menendez R, Otero J: Tomographic study of the inflection points of the pressure-volume curve in acute lung injury. Am J Respir Crit Care Med 2004, 170: 1066-1072. 10.1164/rccm.200312-1644OCCrossRefPubMed

47.

Albaiceta GM, Luyando LH, Parra D, Menendez R, Calvo J, Pedreira PR, Taboada F: Inspiratory vs. expiratory pressure-volume curves to set end-expiratory pressure in acute lung injury. Intensive Care Med 2005, 31: 1370-1378. 10.1007/s00134-005-2746-6CrossRefPubMed

48.

Piacentini E, Lopez-Aguilar J, Garcia-Martin C, Villagra A, Saenz-Valiente A, Murias G, Fernandez-Segoviano P, Hotchkiss JR, Blanch L: Effects of vascular flow and PEEP in a multiple hit model of lung injury in isolated perfused rabbit lungs. J Trauma 2008, 65: 147-153. 10.1097/TA.0b013e31813e0904CrossRefPubMed

49.

Marini JJ, Hotchkiss JR, Broccard AF: Bench-to-bedside review: microvascular and airspace linkage in ventilator-induced lung injury. Crit Care 2003, 7: 435-444. 10.1186/cc2392PubMedCentralCrossRefPubMed

50.

Fu Z, Costello ML, Tsukimoto K, Prediletto R, Elliott AR, Mathieu-Costello O, West JB: High lung volume increases stress failure in pulmonary capillaries. J Appl Physiol 1992, 73: 123-133.PubMed

51.

Broccard AF, Vannay C, Feihl F, Schaller MD: Impact of low pulmonary vascular pressure on ventilator-induced lung injury. Crit Care Med 2002, 30: 2183-2190. 10.1097/00003246-200210000-00002CrossRefPubMed

52.

Hotchkiss JR, Blanch L, Murias G, Adams AB, Olson DA, Wangensteen OD, Leo PH, Marini JJ: Effects of decreased respiratory frequency on ventilator-induced lung injury. Am J Respir Crit Care Med 2000,161(2 Pt 1):463-468.CrossRefPubMed

53.

Lopez-Aguilar J, Piacentini E, Villagra A, Murias G, Pascotto S, Saenz-Valiente A, Fernandez-Segoviano P, Hotchkiss JR, Blanch L: Contributions of vascular flow and pulmonary capillary pressure to ventilator-induced lung injury. Crit Care Med 2006, 34: 1106-1112. 10.1097/01.CCM.0000205757.66971.DACrossRefPubMed

54.

Broccard AF, Hotchkiss JR, Kuwayama N, Olson DA, Jamal S, Wangensteen DO, Marini JJ: Consequences of vascular flow on lung injury induced by mechanical ventilation. Am J Respir Crit Care Med 1998,157(6 Pt 1):1935-1942.CrossRefPubMed

Title: Beyond volutrauma in ARDS: the critical role of lung tissue deformation
Authors: Guillermo M Albaiceta
Lluis Blanch
Publication date: 01-04-2011
Publisher: BioMed Central
Published in: Critical Care / Issue 2/2011
Electronic ISSN: 1364-8535
DOI: https://doi.org/10.1186/cc10052

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Beyond volutrauma in ARDS: the critical role of lung tissue deformation

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2011

The microcirculation of the critically ill pediatric patient

Can 'permissive' hypercapnia modulate the severity of sepsis-induced ALI/ARDS?

Blood transfusion and the lung: first do no harm?

Vascular pedicle width in acute lung injury: correlation with intravascular pressures and ability to discriminate fluid status

Combination of lung ultrasound (a comet-tail sign) and N-terminal pro-brain natriuretic peptide in differentiating acute heart failure from chronic obstructive pulmonary disease and asthma as cause of acute dyspnea in prehospital emergency setting

Erratum to: Bedside quantification of dead-space fraction using routine clinical data in patients with acute lung injury: secondary analysis of two prospective trials