Skip to main content
Top
Published in: Intensive Care Medicine 4/2004

01-04-2004 | Experimental

Infectious and inflammatory dissemination are affected by ventilation strategy in rats with unilateral pneumonia

Authors: Frédérique Schortgen, Lila Bouadma, Marie-Laure Joly-Guillou, Jean-Damien Ricard, Didier Dreyfuss, Georges Saumon

Published in: Intensive Care Medicine | Issue 4/2004

Login to get access

Abstract

Objective

To evaluate the effect of VT reduction and alveolar recruitment on systemic and contralateral dissemination of bacteria and inflammation during right-side pneumonia.

Design

Interventional animal study.

Setting

University hospital research laboratory.

Subjects

A total of 54 male Wistar rats.

Interventions

One day after right lung instillation of 1.4×107 Pseudomonas aeruginosa, rats were left unventilated or ventilated for 2 h at low VT (6 ml/kg) with different strategies of alveolar recruitment: no PEEP, 8 cm H2O PEEP, 8 cm H2O PEEP in a left lateral position, 3 cm H2O PEEP with partial liquid ventilation, or high VT (set such as end-inspiratory pressure was 30 cm H2O) without PEEP (ZEEP). After ventilation the lungs, spleen and liver were cultivated for bacterial counts. Global bacterial dissemination was scored considering the percentage of positive spleen, liver and left lung cultures. TNF-α was assayed in plasma before and after mechanical ventilation.

Measurements and results

All rats had right-side pneumonia with similar bacterial counts. All mechanical ventilation strategies, with the exception of low VT-PEEP 8, promoted contralateral lung dissemination. Overall bacterial dissemination was less in non-ventilated controls (22%) and low VT-PEEP 8 (22%) than in high VT-ZEEP (67%), low VT-PEEP 8 in left lateral position (59%) and low VT-ZEEP (56%) (p<0.05). Partial liquid ventilation prevented systemic bacterial translocation, but at the expense of contralateral bacterial seeding. Plasma TNF-α concentration increased significantly after mechanical ventilation with no PEEP at both high and low VT.

Conclusions

Our results suggest that PEEP might reduce the risk of ventilation-induced bacterial and inflammatory mediator dissemination during pneumonia.
Appendix
Available only for authorised users
Literature
1.
go back to reference Dreyfuss D, Soler P, Saumon G (1995) Mechanical ventilation-induced pulmonary edema. Interaction with previous lung alterations. Am J Respir Crit Care Med 151:1568–1575PubMed Dreyfuss D, Soler P, Saumon G (1995) Mechanical ventilation-induced pulmonary edema. Interaction with previous lung alterations. Am J Respir Crit Care Med 151:1568–1575PubMed
2.
go back to reference Chiumello D, Pristine G, Slutsky AS (1999) Mechanical ventilation affects local and systemic cytokines in an animal model of acute respiratory distress syndrome. Am J Respir Crit Care Med 160:109–116PubMed Chiumello D, Pristine G, Slutsky AS (1999) Mechanical ventilation affects local and systemic cytokines in an animal model of acute respiratory distress syndrome. Am J Respir Crit Care Med 160:109–116PubMed
3.
go back to reference Bouadma L, Schortgen F, Ricard J, Saumon G, Dreyfuss D (2002) Effect of mechanical ventilation on lung and systemic inflammation during mesenteric ischemia-reperfusion in rats (abstract). Am J Respir Crit Care Med 165:A175 Bouadma L, Schortgen F, Ricard J, Saumon G, Dreyfuss D (2002) Effect of mechanical ventilation on lung and systemic inflammation during mesenteric ischemia-reperfusion in rats (abstract). Am J Respir Crit Care Med 165:A175
4.
go back to reference Dreyfuss D, Saumon G (1998) Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 157:294–323PubMed Dreyfuss D, Saumon G (1998) Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 157:294–323PubMed
5.
go back to reference Argiras EP, Blakeley CR, Dunnill MS, Otremski S, Sykes MK (1987) High PEEP decreases hyaline membrane formation in surfactant deficient lungs. Br J Anaesth 59:1278–1285PubMed Argiras EP, Blakeley CR, Dunnill MS, Otremski S, Sykes MK (1987) High PEEP decreases hyaline membrane formation in surfactant deficient lungs. Br J Anaesth 59:1278–1285PubMed
6.
go back to reference Muscedere JG, Mullen JB, Gan K, Slutsky AS (1994) Tidal ventilation at low airway pressures can augment lung injury. Am J Respir Crit Care Med 149:1327–1334PubMed Muscedere JG, Mullen JB, Gan K, Slutsky AS (1994) Tidal ventilation at low airway pressures can augment lung injury. Am J Respir Crit Care Med 149:1327–1334PubMed
7.
go back to reference The Acute Respiratory Distress Syndrome Network (2000) 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 342:1301–1308PubMed The Acute Respiratory Distress Syndrome Network (2000) 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 342:1301–1308PubMed
8.
go back to reference Artigas A, Bernard GR, Carlet J et al. (1998) The American-European Consensus Conference on ARDS, part 2. Ventilatory, pharmacologic, supportive therapy, study design strategies and issues related to recovery and remodeling. Intensive Care Med 24:378–398PubMed Artigas A, Bernard GR, Carlet J et al. (1998) The American-European Consensus Conference on ARDS, part 2. Ventilatory, pharmacologic, supportive therapy, study design strategies and issues related to recovery and remodeling. Intensive Care Med 24:378–398PubMed
9.
go back to reference Eichacker PQ, Gerstenberger EP, Banks SM, Cui X, Natanson C (2002) Meta-analysis of acute lung injury and acute respiratory distress syndrome trials testing low tidal volumes. Am J Respir Crit Care Med 166:1510–1514 Eichacker PQ, Gerstenberger EP, Banks SM, Cui X, Natanson C (2002) Meta-analysis of acute lung injury and acute respiratory distress syndrome trials testing low tidal volumes. Am J Respir Crit Care Med 166:1510–1514
10.
go back to reference Ranieri VM, Suter PM, Tortorella C et al. (1999) Effect of mechanical ventilation on inflammatory mediators in patients with acute respiratory distress syndrome: a randomized controlled tria. JAMA 282:54–61PubMed Ranieri VM, Suter PM, Tortorella C et al. (1999) Effect of mechanical ventilation on inflammatory mediators in patients with acute respiratory distress syndrome: a randomized controlled tria. JAMA 282:54–61PubMed
11.
go back to reference Savel RH, Yao EC, Gropper MA (2001) Protective effects of low tidal volume ventilation in a rabbit model of Pseudomonas aeruginosa-induced acute lung injury. Crit Care Med 29:392–398CrossRefPubMed Savel RH, Yao EC, Gropper MA (2001) Protective effects of low tidal volume ventilation in a rabbit model of Pseudomonas aeruginosa-induced acute lung injury. Crit Care Med 29:392–398CrossRefPubMed
12.
go back to reference Slutsky AS, Tremblay LN (1998) Multiple system organ failure. Is mechanical ventilation a contributing factor? Am J Respir Crit Care Med 157:1721–1725PubMed Slutsky AS, Tremblay LN (1998) Multiple system organ failure. Is mechanical ventilation a contributing factor? Am J Respir Crit Care Med 157:1721–1725PubMed
13.
go back to reference Dreyfuss D, Ricard JD, Saumon G (2003) On the physiologic and clinical relevance of lung-borne cytokines during ventilator-induced lung injury. Am J Respir Crit Care Med 167:1467–1471CrossRefPubMed Dreyfuss D, Ricard JD, Saumon G (2003) On the physiologic and clinical relevance of lung-borne cytokines during ventilator-induced lung injury. Am J Respir Crit Care Med 167:1467–1471CrossRefPubMed
14.
go back to reference Verbrugge SJC, Sorm V, Veen A van ‘t, Mouton JW, Gommers D, Lachmann B (1998) Lung overinflation without positive end-expiratory pressure promotes bacteremia after experimental Klebsiella pneumoniae inoculation. Intensive Care Med 24:172–177PubMed Verbrugge SJC, Sorm V, Veen A van ‘t, Mouton JW, Gommers D, Lachmann B (1998) Lung overinflation without positive end-expiratory pressure promotes bacteremia after experimental Klebsiella pneumoniae inoculation. Intensive Care Med 24:172–177PubMed
15.
go back to reference Nahum A, Hoyt J, Schmitz L, Moody J, Shapiro R, Marini JJ (1997) Effect of mechanical ventilation strategy on dissemination of intratracheally instilled Escherichia coli in dogs. Crit Care Med 25:1733–1743PubMed Nahum A, Hoyt J, Schmitz L, Moody J, Shapiro R, Marini JJ (1997) Effect of mechanical ventilation strategy on dissemination of intratracheally instilled Escherichia coli in dogs. Crit Care Med 25:1733–1743PubMed
16.
go back to reference Murphy DB, Cregg N, Tremblay L et al. (2000) Adverse ventilatory strategy causes pulmonary-to-systemic translocation of endotoxin. Am J Respir Crit Care Med 162:27–33PubMed Murphy DB, Cregg N, Tremblay L et al. (2000) Adverse ventilatory strategy causes pulmonary-to-systemic translocation of endotoxin. Am J Respir Crit Care Med 162:27–33PubMed
17.
go back to reference Lin CY, Zhang H, Cheng KC, Slutsky AS (2003) Mechanical ventilation may increase susceptibility to the development of bacteremia. Crit Care Med 31:1429–1434CrossRefPubMed Lin CY, Zhang H, Cheng KC, Slutsky AS (2003) Mechanical ventilation may increase susceptibility to the development of bacteremia. Crit Care Med 31:1429–1434CrossRefPubMed
18.
go back to reference Seidenfeld JJ, Mullins RC 3rd, Fowler SR, Johanson WG Jr (1986) Bacterial infection and acute lung injury in hamsters. Am Rev Respir Dis 134:22–26PubMed Seidenfeld JJ, Mullins RC 3rd, Fowler SR, Johanson WG Jr (1986) Bacterial infection and acute lung injury in hamsters. Am Rev Respir Dis 134:22–26PubMed
19.
go back to reference Johanson WG Jr, Higuchi JH, Woods DE, Gomez P, Coalson JJ (1985) Dissemination of Pseudomonas aeruginosa during lung infection in hamsters. Role of oxygen-induced lung injury. Am Rev Respir Dis 132:358–361PubMed Johanson WG Jr, Higuchi JH, Woods DE, Gomez P, Coalson JJ (1985) Dissemination of Pseudomonas aeruginosa during lung infection in hamsters. Role of oxygen-induced lung injury. Am Rev Respir Dis 132:358–361PubMed
20.
go back to reference Cakar N, Akinci O, Tugrul S et el. (2002) Recruitment maneuver: does it promote bacterial translocation? Crit Care Med 30:2103–2106CrossRefPubMed Cakar N, Akinci O, Tugrul S et el. (2002) Recruitment maneuver: does it promote bacterial translocation? Crit Care Med 30:2103–2106CrossRefPubMed
21.
go back to reference Dreyfuss D, Saumon G (1998) From ventilator-induced lung injury to multiple organ dysfunction? Intensive Care Med 24:102–104PubMed Dreyfuss D, Saumon G (1998) From ventilator-induced lung injury to multiple organ dysfunction? Intensive Care Med 24:102–104PubMed
22.
go back to reference Coalson JJ, Higuchi JH, Williams ML, Johanson WG Jr (1986) Morphologic and microbiologic features of Pseudomonas aeruginosa pneumonia in normal hamsters. Exp Mol Pathol 45:193–206PubMed Coalson JJ, Higuchi JH, Williams ML, Johanson WG Jr (1986) Morphologic and microbiologic features of Pseudomonas aeruginosa pneumonia in normal hamsters. Exp Mol Pathol 45:193–206PubMed
23.
go back to reference Warner AE, Molina RM, Brain JD (1987) Uptake of bloodborne bacteria by pulmonary intravascular macrophages and consequent inflammatory responses in sheep. Am Rev Respir Dis 136:683–690PubMed Warner AE, Molina RM, Brain JD (1987) Uptake of bloodborne bacteria by pulmonary intravascular macrophages and consequent inflammatory responses in sheep. Am Rev Respir Dis 136:683–690PubMed
24.
go back to reference Sawa T, Ohara M, Kurahashi K et al. (1998) In vitro cellular toxicity predicts Pseudomonas aeruginosa virulence in lung infections. Infect Immun 66:3242–3249PubMed Sawa T, Ohara M, Kurahashi K et al. (1998) In vitro cellular toxicity predicts Pseudomonas aeruginosa virulence in lung infections. Infect Immun 66:3242–3249PubMed
25.
go back to reference Kurahashi K, Kajikawa O, Sawa T et al. (1999) Pathogenesis of septic shock in Pseudomonas aeruginosa pneumonia. J Clin Invest 104:743–750PubMed Kurahashi K, Kajikawa O, Sawa T et al. (1999) Pathogenesis of septic shock in Pseudomonas aeruginosa pneumonia. J Clin Invest 104:743–750PubMed
26.
go back to reference Dreyfuss D, Basset G, Soler P, Saumon G (1985) Intermittent positive-pressure hyperventilation with high inflation pressures produces pulmonary microvascular injury in rats. Am Rev Respir Dis 132:880–884PubMed Dreyfuss D, Basset G, Soler P, Saumon G (1985) Intermittent positive-pressure hyperventilation with high inflation pressures produces pulmonary microvascular injury in rats. Am Rev Respir Dis 132:880–884PubMed
27.
go back to reference Richman PS, Wolfson MR, Shaffer TH (1993) Lung lavage with oxygenated perfluorochemical liquid in acute lung injury. Crit Care Med 21:768–774PubMed Richman PS, Wolfson MR, Shaffer TH (1993) Lung lavage with oxygenated perfluorochemical liquid in acute lung injury. Crit Care Med 21:768–774PubMed
28.
go back to reference Crouch EC (1998) Collectins and pulmonary host defense. Am J Respir Cell Mol Biol 19:177–201PubMed Crouch EC (1998) Collectins and pulmonary host defense. Am J Respir Cell Mol Biol 19:177–201PubMed
29.
go back to reference Ricard JD, Lemaire F (2001) Liquid ventilation. Curr Opin Crit Care 7:8–14 Ricard JD, Lemaire F (2001) Liquid ventilation. Curr Opin Crit Care 7:8–14
30.
go back to reference Thomassen MJ, Buhrow LT, Wiedemann HP (1997) Perflubron decreases inflammatory cytokine production by human alveolar macrophages. Crit Care Med 25:2045–2047PubMed Thomassen MJ, Buhrow LT, Wiedemann HP (1997) Perflubron decreases inflammatory cytokine production by human alveolar macrophages. Crit Care Med 25:2045–2047PubMed
31.
go back to reference Rezaiguia-Delclaux S, Yang K, Stephan F et al. (2003) Effect of partial liquid ventilation on bacterial clearance during Pseudomonas aeruginosa-induced lung injury in rats. Intensive Care Med 29:1151–1156CrossRefPubMed Rezaiguia-Delclaux S, Yang K, Stephan F et al. (2003) Effect of partial liquid ventilation on bacterial clearance during Pseudomonas aeruginosa-induced lung injury in rats. Intensive Care Med 29:1151–1156CrossRefPubMed
32.
go back to reference Dreyfuss D, Soler P, Basset G, Saumon G (1988) High inflation pressure pulmonary edema. Respective effects of high airway pressure, high tidal volume, and positive end-expiratory pressure. Am Rev Respir Dis 137:1159–1164PubMed Dreyfuss D, Soler P, Basset G, Saumon G (1988) High inflation pressure pulmonary edema. Respective effects of high airway pressure, high tidal volume, and positive end-expiratory pressure. Am Rev Respir Dis 137:1159–1164PubMed
33.
go back to reference Lee JH, Del Sorbo L, Khine AA et al. (2003) Modulation of bacterial growth by TNF-{alpha} in vitro and in vivo. Am J Respir Crit Care Med (in press) Lee JH, Del Sorbo L, Khine AA et al. (2003) Modulation of bacterial growth by TNF-{alpha} in vitro and in vivo. Am J Respir Crit Care Med (in press)
34.
go back to reference Koch T, Duncker HP, Axt R, Schiefer HG, Ackern K van, Neuhof H (1993) Alterations of bacterial clearance induced by endotoxin and tumor necrosis factor. Infect Immun 61:3143–3148PubMed Koch T, Duncker HP, Axt R, Schiefer HG, Ackern K van, Neuhof H (1993) Alterations of bacterial clearance induced by endotoxin and tumor necrosis factor. Infect Immun 61:3143–3148PubMed
35.
go back to reference Bonten MJ, Froon AH, Gaillard C et al. (1997) The systemic inflammatory response in the development of ventilator-associated pneumonia. Am J Respir Crit Care Med 156:1105–1113PubMed Bonten MJ, Froon AH, Gaillard C et al. (1997) The systemic inflammatory response in the development of ventilator-associated pneumonia. Am J Respir Crit Care Med 156:1105–1113PubMed
36.
go back to reference Rello J, Mirelis B, Alonso C, Prats G (1991) Lack of usefulness of blood cultures to diagnose ventilator-associated pneumonia. Eur Respir J 4:1020PubMed Rello J, Mirelis B, Alonso C, Prats G (1991) Lack of usefulness of blood cultures to diagnose ventilator-associated pneumonia. Eur Respir J 4:1020PubMed
37.
go back to reference Wang E, Ouellet N, Simard M, Fillion I, Bergeron Y, Beauchamp D, Bergeron MG (2001) Pulmonary and systemic host response to Streptococcus pneumoniae and Klebsiella pneumoniae bacteremia in normal and immunosuppressed mice. Infect Immun 69:5294–5304CrossRefPubMed Wang E, Ouellet N, Simard M, Fillion I, Bergeron Y, Beauchamp D, Bergeron MG (2001) Pulmonary and systemic host response to Streptococcus pneumoniae and Klebsiella pneumoniae bacteremia in normal and immunosuppressed mice. Infect Immun 69:5294–5304CrossRefPubMed
38.
go back to reference Dehoux MS, Boutten A, Ostinelli J et al. (1994) Compartmentalized cytokine production within the human lung in unilateral pneumonia. Am J Respir Crit Care Med 150:710–716PubMed Dehoux MS, Boutten A, Ostinelli J et al. (1994) Compartmentalized cytokine production within the human lung in unilateral pneumonia. Am J Respir Crit Care Med 150:710–716PubMed
39.
go back to reference Tutor JD, Mason CM, Dobard E, Beckerman RC, Summer WR, Nelson S (1994) Loss of compartmentalization of alveolar tumor necrosis factor after lung injury. Am J Respir Crit Care Med 149:1107–1111PubMed Tutor JD, Mason CM, Dobard E, Beckerman RC, Summer WR, Nelson S (1994) Loss of compartmentalization of alveolar tumor necrosis factor after lung injury. Am J Respir Crit Care Med 149:1107–1111PubMed
40.
go back to reference Kawamae K, Pristine G, Chiumello D, Tremblay LN, Slutsky AS (2000) Partial liquid ventilation decreases serum tumor necrosis factor-alpha concentrations in a rat acid aspiration lung injury model. Crit Care Med 28:479–483 Kawamae K, Pristine G, Chiumello D, Tremblay LN, Slutsky AS (2000) Partial liquid ventilation decreases serum tumor necrosis factor-alpha concentrations in a rat acid aspiration lung injury model. Crit Care Med 28:479–483
Metadata
Title
Infectious and inflammatory dissemination are affected by ventilation strategy in rats with unilateral pneumonia
Authors
Frédérique Schortgen
Lila Bouadma
Marie-Laure Joly-Guillou
Jean-Damien Ricard
Didier Dreyfuss
Georges Saumon
Publication date
01-04-2004
Publisher
Springer-Verlag
Published in
Intensive Care Medicine / Issue 4/2004
Print ISSN: 0342-4642
Electronic ISSN: 1432-1238
DOI
https://doi.org/10.1007/s00134-003-2147-7

Other articles of this Issue 4/2004

Intensive Care Medicine 4/2004 Go to the issue

Announcements

April 2004