Skip to main content
NCBI home page
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2014 Jan 11;23(1):9–16. [Article in French] doi: 10.1007/s13546-014-0846-4

Dysfonction immunitaire induite par la ventilation mécanique

Ventilator-induced immune dysfunction

J M Tadié 1,✉, A Gacouin 1, Y Le Tulzo 1
PMCID: PMC7117828  PMID: 32288738

Abstract

Although mechanical ventilation is an essential support in patients admitted to the intensive care unit, clinical and experimental studies have shown that it could be harmful and could induce lung injury. Pulmonary and immune cells can convert mechanical stimuli into biological signals that will lead to inflammation. This sterile inflammation both locally and systemically will cause immunosuppression.

Keywords: Mechanical ventilation, Immune dysfunction, ARDS

Références

  • 1.Dreyfuss D, Saumon G. Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med. 1998;15:294–323. doi: 10.1164/ajrccm.157.1.9604014. [DOI] [PubMed] [Google Scholar]
  • 2.Vlahakis NE, Hubmayr RD. Cellular stress failure in ventilator-injured lungs. Am J Respir Crit Care Med. 2005;171:1328–1342. doi: 10.1164/rccm.200408-1036SO. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Jaecklin T, Otulakowski G, Kavanagh BP. Do soluble mediators cause ventilator-induced lung injury and multi-organ failure? Intensive Care Med. 2010;36:750–757. doi: 10.1007/s00134-010-1850-4. [DOI] [PubMed] [Google Scholar]
  • 4.Hotchkiss RS, Monneret G, Payen D. Sepsis-induced immunosuppression: from cellular dysfunctions to immunotherapy. Nat Rev Immunol. 2013;13:862–874. doi: 10.1038/nri3552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Vincent JL, Bihari DJ, Suter PM, et al. The prevalence of nosocomial infection in intensive care units in Europe. Results of the European Prevalence of Infection in Intensive Care (EPIC) Study. EPIC International Advisory Committee. JAMA. 1995;274:639–644. doi: 10.1001/jama.1995.03530080055041. [DOI] [PubMed] [Google Scholar]
  • 6.Slutsky AS, Ranieri VM. Ventilator-induced lung injury. N Engl J Med. 2013;369:2126–2136. doi: 10.1056/NEJMra1208707. [DOI] [PubMed] [Google Scholar]
  • 7.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. doi: 10.1056/NEJM200005043421801. [DOI] [PubMed] [Google Scholar]
  • 8.Mercat A, Richard JC, Vielle B, et al. Positive endexpiratory pressure setting in adults with acute lung injury and acute respiratory distress syndrome: a randomized controlled trial. JAMA. 2008;299:646–655. doi: 10.1001/jama.299.6.646. [DOI] [PubMed] [Google Scholar]
  • 9.Gattinoni L, Pesenti A, Avalli L, et al. Pressure-volume curve of total respiratory system in acute respiratory failure. Computed tomographic scan study. Am Rev Respir Dis. 1987;136:730–736. doi: 10.1164/ajrccm/136.3.730. [DOI] [PubMed] [Google Scholar]
  • 10.Jacob AM, Gaver DP., 3rd Atelectrauma disrupts pulmonary epithelial barrier integrity and alters the distribution of tight junction proteins ZO-1 and claudin 4. J Appl Physiol. 2012;113:1377–1387. doi: 10.1152/japplphysiol.01432.2011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Slutsky AS. Lung injury caused by mechanical ventilation. Chest. 1999;116:9S–15S. doi: 10.1378/chest.116.suppl_1.9S-a. [DOI] [PubMed] [Google Scholar]
  • 12.Pugin J. Molecular mechanisms of lung cell activation induced by cyclic stretch. Crit Care Med. 2003;31:S200–206. doi: 10.1097/01.CCM.0000057844.31307.ED. [DOI] [PubMed] [Google Scholar]
  • 13.Liu M, Tanswell AK, Post M. Mechanical force-induced signal transduction in lung cells. Am. J. Physiol. 1999;277:L667–683. doi: 10.1152/ajplung.1999.277.4.L667. [DOI] [PubMed] [Google Scholar]
  • 14.dos Santos CC, Slutsky AS. The contribution of biophysical lung injury to the development of biotrauma. Annu Rev Physiol. 2006;68:585–618. doi: 10.1146/annurev.physiol.68.072304.113443. [DOI] [PubMed] [Google Scholar]
  • 15.Chapman KE, Sinclair SE, Zhuang D, et al. Cyclic mechanical strain increases reactive oxygen species production in pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2008;38:362–370. doi: 10.1152/ajplung.00069.2005. [DOI] [PubMed] [Google Scholar]
  • 16.Pugin J, Dunn-Siegrist I, Dufour J, et al. Cyclic stretch of human lung cells induces an acidification and promotes bacterial growth. Am J Respir Cell Mol Biol. 2008;38:362–370. doi: 10.1165/rcmb.2007-0114OC. [DOI] [PubMed] [Google Scholar]
  • 17.Janmey PA. The cytoskeleton and cell signaling: component localization and mechanical coupling. Physiol Rev. 1998;78:763–781. doi: 10.1152/physrev.1998.78.3.763. [DOI] [PubMed] [Google Scholar]
  • 18.Zupancich E, Paparella D, Turani F, et al. Mechanical ventilation affects inflammatory mediators in patients undergoing cardiopulmonary bypass for cardiac surgery: a randomized clinical trial. J Thorac Cardiovasc Surg. 2005;130:378–383. doi: 10.1016/j.jtcvs.2004.11.061. [DOI] [PubMed] [Google Scholar]
  • 19.Emr B, Gatto LA, Roy S, et al. Airway pressure release ventilation prevents ventilator-induced lung injury in normal lungs. JAMA Surg. 2013;148:1005–1012. doi: 10.1001/jamasurg.2013.3746. [DOI] [PubMed] [Google Scholar]
  • 20.Pugin J, Dunn I, Jolliet P, et al. Activation of human macrophages by mechanical ventilation in vitro. Am J Physiol. 1998;275:L1040–1050. doi: 10.1152/ajplung.1998.275.6.L1040. [DOI] [PubMed] [Google Scholar]
  • 21.Tremblay LN, Miatto D, Hamid Q, et al. Injurious ventilation induces widespread pulmonary epithelial expression of tumor necrosis factor-α and interleukin-6 messenger RNA. Crit Care Med. 2002;30:1693–1700. doi: 10.1097/00003246-200208000-00003. [DOI] [PubMed] [Google Scholar]
  • 22.Martin TR, Frevert CW. Innate immunity in the lungs. Proc Am Thorac Soc. 2005;2:403–411. doi: 10.1513/pats.200508-090JS. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Opitz B, van Laak V, Eitel J, et al. Innate immune recognition in infectious and noninfectious diseases of the lung. Am J Respir Crit Care Med. 2010;181:1294–1309. doi: 10.1164/rccm.200909-1427SO. [DOI] [PubMed] [Google Scholar]
  • 24.Chastre J, Fagon JY. Ventilator-associated pneumonia. Am J Respir Crit Care Med. 2002;165:867–903. doi: 10.1164/ajrccm.165.7.2105078. [DOI] [PubMed] [Google Scholar]
  • 25.Grommes J, Soehnlein O. Contribution of neutrophils to acute lung injury. Mol Med. 2011;17:293–307. doi: 10.2119/molmed.2010.00138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.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. doi: 10.1172/JCI0215849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Ravichandran K S, Lorenz U. Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol. 2007;7:964–974. doi: 10.1038/nri2214. [DOI] [PubMed] [Google Scholar]
  • 28.Caudrillier A, Kessenbrock K, Gilliss BM, et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest. 2012;122:2661–2671. doi: 10.1172/JCI61303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol. 2007;81:1–5. doi: 10.1189/jlb.0306164. [DOI] [PubMed] [Google Scholar]
  • 30.Vaneker M, Joosten LA, Heunks LM, et al. Lowtidal-volume mechanical ventilation induces a toll-like receptor 4-dependent inflammatory response in healthy mice. Anesthesiology. 2008;109:465–472. doi: 10.1097/ALN.0b013e318182aef1. [DOI] [PubMed] [Google Scholar]
  • 31.Murray LA, Knight DA, McAlonan L, et al. Deleterious role of TLR3 during hyperoxia-induced acute lung injury. Am J Respir Crit Care Med. 2008;178:1227–1237. doi: 10.1164/rccm.200807-1020OC. [DOI] [PubMed] [Google Scholar]
  • 32.Kuipers MT, van der Poll T, Schultz MJ, et al. Benchto-bedside review: Damage-associated molecular patterns in the onset of ventilator-induced lung injury. Crit Care. 2011;15:235. doi: 10.1186/cc10437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Kuipers MT, Aslami H, Janczy JR, et al. Ventilator-induced lung injury is mediated by the NLRP3 inflammasome. Anesthesiology. 2012;116:1104–1115. doi: 10.1097/ALN.0b013e3182518bc0. [DOI] [PubMed] [Google Scholar]
  • 34.Wu J, Yan Z, Schwartz DE. Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury. J Immunol. 2013;190:3590–3599. doi: 10.4049/jimmunol.1200860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Reynolds PR, Schmidt RE, Kasteler SD, et al. Receptors for advanced glycation end products targeting protects against hyperoxia-induced lung injury in mice. Am J Respir Cell Moll Biol. 2010;42:545–551. doi: 10.1165/rcmb.2008-0265OC. [DOI] [PubMed] [Google Scholar]
  • 36.Agrawal A, Zhuo H, Brady S, et al. Pathogenetic and predictive value of biomarkers in patients with ALI and lower severity of illness: results from two clinical trials. Am J Physiol Lung Cell Mol Physiol. 2012;303:L634–639. doi: 10.1152/ajplung.00195.2012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol. 2011;29:139–162. doi: 10.1146/annurev-immunol-030409-101323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Chorny A, Anderson P, Gonzalez-Rey E, et al. Ghrelin protects against experimental sepsis by inhibiting high-mobility group box 1 release and by killing bacteria. J Immunol. 2008;180:8369–8377. doi: 10.4049/jimmunol.180.12.8369. [DOI] [PubMed] [Google Scholar]
  • 39.Tadie JM, Bae HB, Deshane JS, et al. TLR4 engagement inhibits AMPK activation through a HMGB1 dependent mechanism. Mol Med. 2012;18:659–668. doi: 10.2119/molmed.2011.00401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Tsung A, Klune JR, Zhang X, et al. HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. J Exp Med. 2007;204:2913–2923. doi: 10.1084/jem.20070247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Kim JY, Park JS, Strassheim D, et al. HMGB1 contributes to the development of acute lung injury after hemorrhage. Am J Physiol Lung Cell Mol Physiol. 2005;288:L958–L965. doi: 10.1152/ajplung.00359.2004. [DOI] [PubMed] [Google Scholar]
  • 42.Friggeri A, Yang Y, Banerjee S, et al. HMGB1 inhibits macrophage activity in efferocytosis through binding to the αvβ3-integrin. Am J Physiol Cell Physiol. 2010;299:C1267–C1276. doi: 10.1152/ajpcell.00152.2010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Sha Y, Zmijewski J, Xu Z, et al. HMGB1 develops enhanced proinflammatory activity by binding to cytokines. J Immunol. 2008;180:2531–2537. doi: 10.4049/jimmunol.180.4.2531. [DOI] [PubMed] [Google Scholar]
  • 44.Ogawa EN, Ishizaka A, Tasaka S, et al. Contribution of high-mobility group box-1 to the development of ventilatorinduced lung injury. Am J Respir Crit Care Med. 2006;174:400–407. doi: 10.1164/rccm.200605-699OC. [DOI] [PubMed] [Google Scholar]
  • 45.Shimazaki J, Matsumoto N, Ogura H, et al. Systemic involvement of HMGB1 and therapeutic effect of anti-HMGB1 antibody in a rat model of crush injury. Shock. 2012;37:634–638. doi: 10.1097/SHK.0b013e31824ed6b7. [DOI] [PubMed] [Google Scholar]
  • 46.Tadie JM, Bae HB, Jiang S, et al. HMGB1 can induce neutrophils extracellular traps through TLR4. Am J Physiol Lung Cell Mol Physiol. 2013;304:L342–349. doi: 10.1152/ajplung.00151.2012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13:463–469. doi: 10.1038/nm1565. [DOI] [PubMed] [Google Scholar]
  • 48.Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303:1532–1535. doi: 10.1126/science.1092385. [DOI] [PubMed] [Google Scholar]
  • 49.Mantovani A, Cassatella MA, Costantini C, et al. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11:519–531. doi: 10.1038/nri3024. [DOI] [PubMed] [Google Scholar]
  • 50.Tadié JM, Bae HB, Banerjee S, et al. Differential activation of RAGE by HMGB1 modulates neutrophil-associated NADPH oxidase activity and bacterial killing. Am J Physiol Cell Physiol. 2012;302:C249–256. doi: 10.1152/ajpcell.00302.2011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Barnay-Verdier S, Fattoum L, Borde C, et al. Emergence of autoantibodies to HMGB1 is associated with survival in patients with septic shock. Intensive Care Med. 2011;37:957–962. doi: 10.1007/s00134-011-2192-6. [DOI] [PubMed] [Google Scholar]
  • 52.Haitsma JJ, Uhlig S, Goggel R, et al. Ventilator-induced lung injury leads to loss of alveolar and systemic compartmentalization of tumor necrosis factor-α. Intensive Care Med. 2000;26:1515–1522. doi: 10.1007/s001340000648. [DOI] [PubMed] [Google Scholar]
  • 53.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;289:2104–2112. doi: 10.1001/jama.289.16.2104. [DOI] [PubMed] [Google Scholar]
  • 54.Limaye AP, Kirby KA, Rubenfeld GD, et al. Cytomegalovirus reactivation in critically ill immunocompetent patients. JAMA. 2008;300:413–422. doi: 10.1001/jama.2008.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Luyt CE, Combes A, Deback C, et al. Herpes simplex virus lung infection in patients undergoing prolonged mechanical ventilation. Am J Respir Crit Care Med. 2007;175:935–942. doi: 10.1164/rccm.200609-1322OC. [DOI] [PubMed] [Google Scholar]
  • 56.Verbrugge SJ, Sorm V, van’ t Veen A, et al. Lung overinflation without positive end-expiratory pressure promotes bacteremia after experimental Klebsiella pneumoniae inoculation. Intensive Care Med. 1998;24:172–177. doi: 10.1007/s001340050541. [DOI] [PubMed] [Google Scholar]
  • 57.Lin CY, Zhang H, Cheng KC, et al. Mechanical ventilation may increase susceptibility to the development of bacteremia. Crit Care Med. 2003;31:1429–1434. doi: 10.1097/01.CCM.0000063449.58029.81. [DOI] [PubMed] [Google Scholar]
  • 58.Futier E, Constantin JM, Paugam-Burtz C, et al. A trial of intraoperative low-tidal-volume ventilation in abdominal surgery. N Engl J Med. 2013;369:428–437. doi: 10.1056/NEJMoa1301082. [DOI] [PubMed] [Google Scholar]
  • 59.Emr B, Gatto LA, Roy S, et al. Airway pressure release ventilation prevents ventilator-induced lung injury in normal lungs. JAMA Surg. 2013;148:1005–1012. doi: 10.1001/jamasurg.2013.3746. [DOI] [PubMed] [Google Scholar]
  • 60.Plötz FB, Vreugdenhil HA, Slutsky AS, et al. Mechanical ventilation alters the immune response in children without lung pathology. Intensive Care Med. 2002;28:486–492. doi: 10.1007/s00134-002-1216-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Le Tulzo Y, Pangault C, Amiot L, et al. Monocyte human leukocyte antigen-DR transcriptional down-regulation by cortisol during septic shock. Am J Respir Crit Care Med. 2004;169:1144–1151. doi: 10.1164/rccm.200309-1329OC. [DOI] [PubMed] [Google Scholar]

Articles from Reanimation are provided here courtesy of Nature Publishing Group

RESOURCES