Journal of Critical Care
Volume 22, Issue 4 , Pages 305-313 , December 2007

Hypercapnic acidosis modulates inflammation, lung mechanics, and edema in the isolated perfused lung

  • Hilde R. De Smet, BSc

      Affiliations

    • Flinders University, Bedford Park, South Australia 5042, Australia
    • Corresponding Author InformationCorresponding author. Department of Physiology, Flinders Medical Center, Bedford Park, SA 5042, Australia.
  • ,
  • Andrew D. Bersten, MD

      Affiliations

    • Flinders University, Bedford Park, South Australia 5042, Australia
    • Flinders Medical Center, Bedford Park, South Australia 5042, Australia
  • ,
  • Heather A. Barr, MSc

      Affiliations

    • Flinders University, Bedford Park, South Australia 5042, Australia
  • ,
  • Ian R. Doyle, PhD

      Affiliations

    • Flinders University, Bedford Park, South Australia 5042, Australia

References 

  1. Dreyfuss D, Saumon G. Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med. 1998;157:294–323
  2. 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
  3. Montgomery AB, Stager MA, Carrico CJ, et al. Causes of mortality in patients with the adult respiratory distress syndrome. Am Rev Respir Dis. 1985;132:485–489
  4. Slutsky AS, Tremblay LN. Multiple system organ failure. Is mechanical ventilation a contributing factor?. Am J Respir Crit Care Med. 1998;157:1721–1725
  5. Nicholas TE, Power JH, Barr HA. The pulmonary consequences of a deep breath. Respir Physiol. 1982;49:315–324
  6. Houmes RJ, Bos JA, Lachmann B. Effect of different ventilator settings on lung mechanics: with special reference to the surfactant system. Appl Cardiopulm Pathophysiol. 1992;5:117–127
  7. ARDS Network . 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
  8. Laffey JG, Engelberts D, Kavanagh BP. Buffering hypercapnic acidosis worsens acute lung injury. Am J Respir Crit Care Med. 2000;161:141–146
  9. Broccard AF, Hotchkiss JR, Vannay C, et al. Protective effects of hypercapnic acidosis on ventilator-induced lung injury. Am J Respir Crit Care Med. 2001;164:802–806
  10. Shibata K, Cregg N, Engelberts D, et al. Hypercapnic acidosis may attenuate acute lung injury by inhibition of endogenous xanthine oxidase. Am J Respir Crit Care Med. 1998;158:1578–1584
  11. Laffey JG, Tanaka M, Engelberts D, et al. Therapeutic hypercapnia reduces pulmonary and systemic injury following in vivo lung reperfusion. Am J Respir Crit Care Med. 2000;162:2287–2294
  12. Sinclair SE, Kregenow DA, Lamm WJ, et al. Hypercapnic acidosis is protective in an in vivo model of ventilator-induced lung injury. Am J Respir Crit Care Med. 2002;166:403–408
  13. Laffey JG, Jankov RP, Engelberts D, et al. Effects of therapeutic hypercapnia on mesenteric ischemia-reperfusion injury. Am J Respir Crit Care Med. 2003;168:1383–1390
  14. Laffey JG, Honan D, Hopkins N, et al. Hypercapnic acidosis attenuates endotoxin-induced acute lung injury. Am J Respir Crit Care Med. 2004;169:46–56
  15. Laffey JG, O'Croinin D, McLoughlin P, et al. Permissive hypercapnia—role in protective lung ventilatory strategies. Intensive Care Med. 2004;30:347–356
  16. Feihl F, Perret C. Permissive hypercapnia. How permissive should we be?. Am J Respir Crit Care Med. 1994;150:1722–1737
  17. Davidson KG, Bersten AD, Barr HA, et al. Endotoxin induces respiratory failure and increases surfactant turnover and respiration independent of alveolocapillary injury in rats. Am J Respir Crit Care Med. 2002;165:1516–1525
  18. Davidson KG, Bersten AD, Barr HA, et al. Lung function, permeability, and surfactant composition in oleic acid–induced acute lung injury in rats. Am J Physiol. 2000;279:L1091–L1102
  19. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Med Sci. 1959;37:911–917
  20. Bartlett GR. Phosphorus assay in column chromatography. J Biol Chem. 1959;234:466–468
  21. Mason RJ, Nellenbogen J, Clements JA. Isolation of disaturated phosphatidylcholine with osmium tetroxide. J Lipid Res. 1976;17:281–284
  22. Power JH, Barr HA, Nicholas TE. Surfactant-associated 15- and 35-kDa proteins are concentrated in different organelles in rat lung tissue. Exp Lung Res. 1988;14:209–224
  23. Power JH, Jones ME, Barr HA, et al. Analysis of pulmonary phospholipid compartments in the unanesthetized rat during prolonged periods of hyperpnea. Exp Lung Res. 1986;11:105–128
  24. Lang JD, Figueroa M, Sanders KD, et al. Hypercapnia via reduced rate and tidal volume contributed to lipopolysaccharide-induced lung injury. Am J Respir Crit Care Med. 2005;171(2):147–157
  25. Dong P, Hosszu E, Hart P, et al. pH and LPS alters TNF-α release from alveolar type II cells. Am J Respir Crit Care Med. 2001;163:A276;[abstr]
  26. Dong P, Hosszu E, Hart P, et al. CO2 alters cytokine release from alveolar macrophages. Am J Respir Crit Care Med. 2002;165:A546;[abstr]
  27. Rai S, Engelberts D, Laffey JG, et al. Therapeutic hypercapnia is not protective in the in vivo surfactant-depleted rabbit lung. Pediatr Res. 2004;55:42–49
  28. Laffey JG, Engelberts D, Duggan M, et al. Carbon dioxide attenuates pulmonary impairment resulting from hyperventilation. Crit Care Med. 2003;31:2634–2640
  29. Takeshita K, Suzuki Y, Nishio K, et al. Hypercapnic acidosis attenuates endotoxin-induced nuclear factor–[kappa]B activation. Am J Respir Cell Mol Biol. 2003;29:124–132
  30. Laffey JG, Kavanagh BP. Carbon dioxide and the critically ill—too little of a good thing?. Lancet. 1999;354:1283–1286
  31. Ingenito EP, Tsai LW, Majumdar A, et al. On the role of surface tension in the pathophysiology of emphysema. Am J Respir Crit Care Med. 2005;171:300–304
  32. Dietl P, Haller T. Exocytosis of lung surfactant: from the secretory vesicle to the air-liquid interface. Annu Rev Physiol. 2005;67:595–621
  33. Rooney SA, Young SL, Mendelson CR. Molecular and cellular processing of lung surfactant. FASEB J. 1994;8:957–967
  34. Savov J, Silbajoris R, Young SL. Mechanical ventilation of rat lung: effect on surfactant forms. Am J Physiol. 1999;277:320–326
  35. Nicholas TE, Power JHT, Barr HA. Effect of pattern of breathing on subfractions of surfactant in tissue and alveolar compartments of the adult rat lung. Am J Respir Cell Mol Biol. 1990;3:251–258
  36. Jones ME, Barr HA, Nicholas TE. Turnover of cholesterol and dipalmitoylphosphatidylcholine in surfactant of adult rat lung. Lipids. 1993;28:173–179
  37. Power JH, Barr HA, Jones ME, et al. Changes in surfactant pools after a physiological increase in alveolar surfactant. J Appl Physiol. 1987;63:1902–1911
  38. Albert RK, Lakshminarayan S, Hildebrandt J, et al. Increased surface tension favors pulmonary edema formation in anesthetized dogs' lungs. J Clin Invest. 1979;63:1015–1018
  39. Evander E, Wollmer P, Valind S, et al. Biexponential pulmonary clearance of 99mTc-DTPA induced by detergent aerosol. J Appl Physiol. 1994;77:190–196
  40. Nakamura T, Malloy J, McCaig L, et al. Mechanical ventilation of isolated septic rat lungs: effects on surfactant and inflammatory cytokines. J Appl Physiol. 2001;91:811–820
  41. Tremblay L, Valenza F, Ribeiro SP, et al. Injurious ventilatory strategies increase cytokines and c-fos m-RNA expression in an isolated rat lung model. J Clin Invest. 1997;99:944–952
  42. Tremblay LN, Miatto D, Hamid Q, Govindarajan A, Slutsky AS. Injurious ventilation induces widespread pulmonary epithelial expression of tumor necrosis factor–alpha and interleukin-6 messenger RNA. Crit Care Med. 2002;30:1693–1700
  43. Ricard JD, Dreyfuss D, Saumon G. Production of inflammatory cytokines in ventilator-induced lung injury: a reappraisal. Am J Respir Crit Care Med. 2001;163:1176–1180
  44. Goodman RB, Strieter RM, Martin DP, et al. Inflammatory cytokines in patients with persistence of the acute respiratory distress syndrome. Am J Respir Crit Care Med. 1996;154:602–611
  45. Meduri GU, Kohler G, Headley S, Tolley E, Stentz F, Postlethwaite A. Inflammatory cytokines in the BAL of patients with ARDS. Persistent elevation over time predicts poor outcome. Chest. 1995;108:1303–1314
  46. Meduri GU, Headley S, Kohler G, et al. Persistent elevation of inflammatory cytokines predicts a poor outcome in ARDS. Plasma IL-1 beta and IL-6 levels are consistent and efficient predictors of outcome over time. Chest. 1995;107:1062–1073
  47. von Bethmann AN, Brasch F, Nusing R, et al. Hyperventilation induces release of cytokines from perfused mouse lung. Am J Respir Crit Care Med. 1998;157:263–272
  48. Chiumello D, Pristine G, Slutsky AS. Mechanical ventilation affects local and systemic cytokines in an animal model of acute respiratory distress syndrome. Am J Respir Crit Care Med. 1999;160:109–116
  49. Tutor JD, Mason CM, Dobard E, Beckerman RC, Summer WR, Nelson S. Loss of compartmentalization of alveolar tumor necrosis factor after lung injury. Am J Respir Crit Care Med. 1994;149:1107–1111
  50. Yoshikawa S, King JA, Lausch RN, Penton AM, Eyal FG, Parker JC. Acute ventilator-induced vascular permeability and cytokine responses in isolated and in situ mouse lungs. J Appl Physiol. 2004;97(6):2190–2199
  51. Doyle IR, Nicholas TE, Bersten AD. Partitioning lung and plasma proteins: circulating surfactant proteins as biomarkers of alveolocapillary permeability. Clin Exp Pharmacol Physiol. 1999;26:185–197

 This research was supported by the National Health and Medical Research Council of Australia (Canberra, Australian Capital Territory) through grant no. 229954.

PII: S0883-9441(06)00215-2

doi: 10.1016/j.jcrc.2006.12.002

Journal of Critical Care
Volume 22, Issue 4 , Pages 305-313 , December 2007