Effects of sigh during pressure control and pressure support ventilation in pulmonary and extrapulmonary mild acute lung injury

Lillian Moraes, Cíntia Lourenco Santos, Raquel Souza Santos, Fernanda Ferreira Cruz, Felipe Saddy, Marcelo Marcos Morales, Vera Luiza Capelozzi, Pedro Leme Silva, Marcelo Gama de Abreu, Cristiane Sousa Nascimento Baez Garcia, Paolo Pelosi, Patricia Rieken Macedo Rocco, Lillian Moraes, Cíntia Lourenco Santos, Raquel Souza Santos, Fernanda Ferreira Cruz, Felipe Saddy, Marcelo Marcos Morales, Vera Luiza Capelozzi, Pedro Leme Silva, Marcelo Gama de Abreu, Cristiane Sousa Nascimento Baez Garcia, Paolo Pelosi, Patricia Rieken Macedo Rocco

Abstract

Introduction: Sigh improves oxygenation and lung mechanics during pressure control ventilation (PCV) and pressure support ventilation (PSV) in patients with acute respiratory distress syndrome. However, so far, no study has evaluated the biological impact of sigh during PCV or PSV on the lung and distal organs in experimental pulmonary (p) and extrapulmonary (exp) mild acute lung injury (ALI).

Methods: In 48 Wistar rats, ALI was induced by Escherichia coli lipopolysaccharide either intratracheally (ALIp) or intraperitoneally (ALIexp). After 24 hours, animals were anesthetized and mechanically ventilated with PCV or PSV with a tidal volume of 6 mL/kg, FiO2 = 0.4, and PEEP = 5 cmH2O for 1 hour. Both ventilator strategies were then randomly assigned to receive periodic sighs (10 sighs/hour, Sigh) or not (non-Sigh, NS). Ventilatory and mechanical parameters, arterial blood gases, lung histology, interleukin (IL)-1β, IL-6, caspase-3, and type III procollagen (PCIII) mRNA expression in lung tissue, and number of apoptotic cells in lung, liver, and kidney specimens were analyzed.

Results: In both ALI etiologies: (1) PCV-Sigh and PSV-Sigh reduced transpulmonary pressure, and (2) PSV-Sigh reduced the respiratory drive compared to PSV-NS. In ALIp: (1) PCV-Sigh and PSV-Sigh decreased alveolar collapse as well as IL-1β, IL-6, caspase-3, and PCIII expressions in lung tissue, (2) PCV-Sigh increased alveolar-capillary membrane and endothelial cell damage, and (3) abnormal myofibril with Z-disk edema was greater in PCV-NS than PSV-NS. In ALIexp: (1) PSV-Sigh reduced alveolar collapse, but led to damage to alveolar-capillary membrane, as well as type II epithelial and endothelial cells, (2) PCV-Sigh and PSV-Sigh increased IL-1β, IL-6, caspase-3, and PCIII expressions, and (3) PCV-Sigh increased the number of apoptotic cells in the lung compared to PCV-NS.

Conclusions: In these models of mild ALIp and ALIexp, sigh reduced alveolar collapse and transpulmonary pressures during both PCV and PSV; however, improved lung protection only during PSV in ALIp.

Figures

Figure 1
Figure 1
Timeline representation of the experimental procedure. ALI, acute lung injury; FiO2, fraction of inspired oxygen; i.t., intratracheal; i.p., intraperitoneal; LPS, lipopolysaccharide; Paw, airway pressure; PCV, pressure-controlled ventilation; PEEP, positive end-expiratory pressure; PSV, pressure-support ventilation; RT-PCR, real-time reverse transcription polymerase chain reaction; VT, tidal volume; ZEEP, zero end-expiratory pressure.
Figure 2
Figure 2
Photomicrographs of lung parenchyma stained with hematoxylin and eosin. Photomicrographs are representative of data obtained from lung sections of six animals (original magnification, x200). ALIexp, extrapulmonary acute lung injury; ALIp, pulmonary acute lung injury; PCV, pressure-controlled ventilation; PSV, pressure support ventilation.
Figure 3
Figure 3
Volume fraction of the lung occupied by normal pulmonary areas, collapsed alveoli, and hyperinflated structures. Each bar represents the mean + standard deviation (SD) of six rats in each group. *Significantly different from PCV non-Sigh (P <0.05); **significantly different from PCV-Sigh (P <0.05); #significantly different from PSV non-Sigh (P <0.05). ALIexp, extrapulmonary acute lung injury; ALIp, pulmonary acute lung injury; NS, non-sigh; PCV, pressure-controlled ventilation; PSV, pressure support ventilation.
Figure 4
Figure 4
Electron microscopy of lung parenchyma in ALIp and ALIexp. Photomicrographs are representative of data obtained from lung sections of five animals per group. Type II epithelial cell (PII) damage with bizarre lamellar bodies (Lb) and apoptosis of epithelial (PII) and endothelial cells (End) are visible in all groups. In ALIp, PCV-Sigh was associated with greater endothelial cell damage as well as with interstitial edema (asterisks), whereas PSV-Sigh was associated with comparatively less alveolar-capillary damage. In ALIexp, the blood-gas barrier (Bgb) was thickened from edema in PSV-Sigh animals compared to PCV-Sigh and PSV-Non-Sigh animals. AS, intra-alveolar space; Cap, capillary; E, erythrocyte; ED, edema; IC, interstitial cell; Neu, neutrophil.
Figure 5
Figure 5
Electron microscopy of diaphragm specimens in ALIp and ALIexp. Photomicrographs are representative of data obtained from diaphragm sections of five animals per group. Sigh did not affect the diaphragmatic damage induced by LPS; however, in ALIp, PSV led to less damage than PCV. ALIp, pulmonary acute lung injury; ALIexp, extrapulmonary acute lung injury; LPS, Escherichia coli lipopolysaccharide; Mi, mitochondria; PCV, pressure-controlled ventilation; PSV, pressure support ventilation; Z, Z-disk.
Figure 6
Figure 6
Expression of biological markers. Real-time polymerase chain reaction analysis of biological markers associated with inflammation (interleukin (IL)-1β, IL-6), fibrogenesis (type III procollagen), and apoptosis (caspase-3). Relative gene expression was calculated as a ratio of the average gene expression levels compared with the reference gene (GAPDH) and expressed as fold change relative to PCV-NS (non-Sigh). Values are mean + standard deviation (SD) of five rats in each group. *Significantly different from PCV non-Sigh (P <0.05); **significantly different from PCV-Sigh (P <0.05); #significantly different from PSV non-Sigh (P <0.05). ALIp, pulmonary acute lung injury; ALIexp, extrapulmonary acute lung injury; PCV, pressure-controlled ventilation; PSV, pressure support ventilation; NS, non-Sigh.

References

    1. Putensen C, Theuerkauf N, Zinserling J, Wrigge H, Pelosi P. Meta-analysis: ventilation strategies and outcomes of the acute respiratory distress syndrome and acute lung injury. Ann Intern Med. 2009;151:566–576. doi: 10.7326/0003-4819-151-8-200910200-00011.
    1. Pelosi P, Goldner M, McKibben A, Adams A, Eccher G, Caironi P, Losappio S, Gattinoni L, Marini JJ. Recruitment and derecruitment during acute respiratory failure: an experimental study. Am J Respir Crit Care Med. 2001;164:122–130. doi: 10.1164/ajrccm.164.1.2007010.
    1. Fan E, Wilcox ME, Brower RG, Stewart TE, Mehta S, Lapinsky SE, Meade MO, Ferguson ND. Recruitment maneuvers for acute lung injury: a systematic review. Am J Respir Crit Care Med. 2008;178:1156–1163. doi: 10.1164/rccm.200802-335OC.
    1. Pelosi P, Cadringher P, Bottino N, Panigada M, Carrieri F, Riva E, Lissoni A, Gattinoni L. Sigh in acute respiratory distress syndrome. Am J Respir Crit Care Med. 1999;159:872–880. doi: 10.1164/ajrccm.159.3.9802090.
    1. Foti G, Cereda M, Sparacino ME, De Marchi L, Villa F, Pesenti A. Effects of periodic lung recruitment maneuvers on gas exchange and respiratory mechanics in mechanically ventilated acute respiratory distress syndrome (ARDS) patients. Intensive Care Med. 2000;26:501–507. doi: 10.1007/s001340051196.
    1. 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. doi: 10.1097/00000542-200204000-00004.
    1. Brander L, Slutsky AS. Assisted spontaneous breathing during early acute lung injury. Crit Care. 2006;10:102. doi: 10.1186/cc3953.
    1. Riva DR, Oliveira MB, Rzezinski AF, Rangel G, Capelozzi VL, Zin WA, Morales MM, Pelosi P, Rocco PR. Recruitment maneuver in pulmonary and extrapulmonary experimental acute lung injury. Crit Care Med. 2008;36:1900–1908. doi: 10.1097/CCM.0b013e3181760e5d.
    1. Santos CL, Moraes L, Santos RS, Oliveira MG, Silva JD, Maron-Gutierrez T, Ornellas DS, Morales MM, Capelozzi VL, Jamel N, Pelosi P, Rocco PR, Garcia CS. Effects of different tidal volumes in pulmonary and extrapulmonary lung injury with or without intraabdominal hypertension. Intensive Care Med. 2012;38:499–508. doi: 10.1007/s00134-011-2451-6.
    1. Silva PL, Moraes L, Santos RS, Samary C, Ramos MB, Santos CL, Morales MM, Capelozzi VL, Garcia CS, de Abreu MG, Pelosi P, Marini JJ, Rocco PR. Recruitment maneuvers modulate epithelial and endothelial cell response according to acute lung injury etiology. Crit Care Med. 2013;41:e256–e265. doi: 10.1097/CCM.0b013e31828a3c13.
    1. Baydur A, Behrakis PK, Zin WA, Jaeger M, Milic-Emili J. A simple method for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis. 1982;126:788–791.
    1. Weibel ER. Models of Lung Disease-Microscopy and Structural Methods. 1990. Morphometry: stereological theory and practical methods; p. 247.
    1. Oliveira GP, Oliveira MB, Santos RS, Lima LD, Dias CM, Ab' Saber AM, Teodoro WR, Capelozzi VL, Gomes RN, Bozza PT, Pelosi P, Rocco PR. Intravenous glutamine decreases lung and distal organ injury in an experimental model of abdominal sepsis. Crit Care. 2009;13:R74. doi: 10.1186/cc7888.
    1. Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, Kuebler WM. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol. 2011;44:725–738. doi: 10.1165/rcmb.2009-0210ST.
    1. Steimback PW, Oliveira GP, Rzezinski AF, Silva PL, Garcia CS, Rangel G, Morales MM, Lapa ESJR, Capelozzi VL, Pelosi P, Rocco PR. 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. doi: 10.1007/s00134-009-1439-y.
    1. Guerin C, Debord S, Leray V, Delannoy B, Bayle F, Bourdin G, Richard JC. Efficacy and safety of recruitment maneuvers in acute respiratory distress syndrome. Ann Intensive Care. 2011;1:9. doi: 10.1186/2110-5820-1-9.
    1. 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. doi: 10.1097/CCM.0b013e3181968e7e.
    1. Chesnutt AN, Matthay MA, Tibayan FA, Clark JG. Early detection of type III procollagen peptide in acute lung injury. Pathogenetic and prognostic significance. Am J Respir Crit Care Med. 1997;156:840–845. doi: 10.1164/ajrccm.156.3.9701124.
    1. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, −3, −6, −7, −8, and −10 in a caspase-9-dependent manner. J Cell Biol. 1999;144:281–292. doi: 10.1083/jcb.144.2.281.
    1. Nacoti M, Spagnolli E, Bonanomi E, Barbanti C, Cereda M, Fumagalli R. Sigh improves gas exchange and respiratory mechanics in children undergoing pressure support after major surgery. Minerva Anestesiol. 2012;78:920–929.
    1. Perlman CE, Bhattacharya J. Alveolar expansion imaged by optical sectioning microscopy. J Appl Physiol (1985) 2007;103:1037–1044. doi: 10.1152/japplphysiol.00160.2007.
    1. Bhattacharya J, Matthay MA. Regulation and repair of the alveolar-capillary barrier in acute lung injury. Annu Rev Physiol. 2013;75:593–615. doi: 10.1146/annurev-physiol-030212-183756.
    1. Suki B, Hubmayr R. Epithelial and endothelial damage induced by mechanical ventilation modes. Curr Opin Crit Care. 2014;20:17–24. doi: 10.1097/MCC.0000000000000043.
    1. Galletly D, Larsen P. Ventilatory frequency variability in spontaneously breathing anaesthetized subjects. Br J Anaesth. 1999;83:552–563. doi: 10.1093/bja/83.4.552.
    1. Brack T, Jubran A, Tobin MJ. Dyspnea and decreased variability of breathing in patients with restrictive lung disease. Am J Respir Crit Care Med. 2002;165:1260–1264. doi: 10.1164/rccm.2201018.
    1. Passaro CP, Silva PL, Rzezinski AF, Abrantes S, Santiago VR, Nardelli L, Santos RS, Barbosa CM, Morales MM, Zin WA, Amato MB, Capelozzi VL, Pelosi P, Rocco PR. Pulmonary lesion induced by low and high positive end-expiratory pressure levels during protective ventilation in experimental acute lung injury. Crit Care Med. 2009;37:1011–1017. doi: 10.1097/CCM.0b013e3181962d85.
    1. Santiago VR, Rzezinski AF, Nardelli LM, Silva JD, Garcia CS, Maron-Gutierrez T, Ornellas DS, Morales MM, Capelozzi VL, Marini J, Pelosi P, Rocco PR. Recruitment maneuver in experimental acute lung injury: the role of alveolar collapse and edema. Crit Care Med. 2010;38:2207–2214. doi: 10.1097/CCM.0b013e3181f3e076.
    1. Saddy F, Oliveira GP, Garcia CS, Nardelli LM, Rzezinski AF, Ornellas DS, Morales MM, Capelozzi VL, Pelosi P, Rocco PR. Assisted ventilation modes reduce the expression of lung inflammatory and fibrogenic mediators in a model of mild acute lung injury. Intensive Care Med. 2010;36:1417–1426. doi: 10.1007/s00134-010-1808-6.
    1. Saddy F, Moraes L, Santos C, Oliveira G, Cruz F, Morales M, Capelozzi V, de Abreu M, Baez Garcia CS, Pelosi P, Rocco PR. Biphasic positive airway pressure minimizes biological impact on lung tissue in mild acute lung injury independent of etiology. Crit Care. 2013;17:R228. doi: 10.1186/cc13051.
    1. Laffey JG, O'Croinin D, McLoughlin P, Kavanagh BP. Permissive hypercapnia-role in protective lung ventilatory strategies. Intensive Care Med. 2004;30:347–356. doi: 10.1007/s00134-003-2051-1.

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel