Rapid onset of specific diaphragm weakness in a healthy murine model of ventilator-induced diaphragmatic dysfunction

Anesthesiology

Volumn 117, Issue 3, 2012, Pages 560-567

  Mrozek, Segolene ^a   Jung, Boris ^a,b,c   Petrof, Basil J ^d   Pauly, Marion ^a   Roberge, Stephanie ^a   Lacampagne, Alain ^a   Cassan, Cécile ^a   Thireau, Jerome ^a   Molinari, Nicolas ^a   Futier, Emmanuel ^a   Scheuermann, Valerie ^a   Michel Constantin, Jean ^e   Matecki, Stefan ^f   Jaber, Samir ^a,b  

^a HÔPITAL ARNAUD DE VILLENEUVE   (France)

^b HÔPITAL SAINT ELOI   (France)

^c MCGILL UNIVERSITY   (Canada)

^d RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^e UNIV MONTPELLIER   (France)

^f UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CASPASE 3;

AIRWAY PRESSURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL GAS; ARTICLE; ARTIFICIAL VENTILATION; ATROPHY; BREATHING; CONTROLLED STUDY; DIAPHRAGM; DIAPHRAGM DISEASE; ENZYME ACTIVATION; EXTENSOR DIGITORUM LONGUS MUSCLE; HISTOLOGY; IMMUNOBLOTTING; LUNG HEMODYNAMICS; MALE; MOUSE; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; POSITIVE END EXPIRATORY PRESSURE; PRIORITY JOURNAL; PROTEIN DEGRADATION; SARCOLEMMA; VENTILATOR INDUCED DIAPHRAGMATIC DYSFUNCTION;

ANIMALS; CARBON DIOXIDE; DIAPHRAGM; DISEASE MODELS, ANIMAL; HEMODYNAMICS; MALE; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION; MUSCLE WEAKNESS; RESPIRATION; RESPIRATION, ARTIFICIAL; VENTILATORS, MECHANICAL;

EID: 84865599834     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e318261e7f8     Document Type: Article

References (42)

1. Wolthuis EK, Choi G, Dessing MC, Bresser P, Lutter R, Dzoljic M, van der Poll T, Vroom MB, Hollmann M, Schultz MJ: Mechanical ventilation with lower tidal volumes and positive end-expiratory pressure prevents pulmonary inflammation in patients without preexisting lung injury. ANESTHESIOLOGY 2008; 108:46-54
2. Capdevila X, Lopez S, Bernard N, Rabischong E, Ramonatxo M, Martinazzo G, Prefaut C: Effects of controlled mechanical ventilation on respiratory muscle contractile properties in rabbits. Intensive Care Med 2003; 29:103-10
3. Gayan-Ramirez G, de Paepe K, Cadot P, Decramer M: Detrimental effects of short-term mechanical ventilation on diaphragm function and IGF-I mRNA in rats. Intensive Care Med 2003; 29:825-33
4. Jaber S, Sebbane M, Koechlin C, Hayot M, Capdevila X, Eledjam JJ, Prefaut C, Ramonatxo M, Matecki S: Effects of short vs. prolonged mechanical ventilation on antioxidant systems in piglet diaphragm. Intensive Care Med 2005; 31:1427-33
5. Le Bourdelles G, Viires N, Boczkowski J, Seta N, Pavlovic D, Aubier M: Effects of mechanical ventilation on diaphragmatic contractile properties in rats. Am J Respir Crit Care Med 1994; 149:1539-44
6. Sassoon CS, Caiozzo VJ, Manka A, Sieck GC: Altered diaphragm contractile properties with controlled mechanical ventilation. J Appl Physiol 2002; 92:2585-95
7. Yang L, Luo J, Bourdon J, Lin MC, Gottfried SB, Petrof BJ: Controlled mechanical ventilation leads to remodeling of the rat diaphragm. Am J Respir Crit Care Med 2002; 166:1135-40
8. Hermans G, Agten A, Testelmans D, Decramer M, Gayan-Ramirez G: Increased duration of mechanical ventilation is associated with decreased diaphragmatic force: A prospective observational study. Crit Care 2010; 14:R127.
9. Hussain SN, Mofarrahi M, Sigala I, Kim HC, Vassilakopoulos T, Maltais F, Bellenis I, Chaturvedi R, Gottfried SB, Metrakos P, Dania-lou G, Matecki S, Jaber S, Petrof BJ, Goldberg P: Mechanical ventilation-induced diaphragm disuse in humans triggers au-tophagy. Am J Respir Crit Care Med 2010; 182:1377-86
10. Jaber S, Petrof BJ, Jung B, Chanques G, Berthet JP, Rabuel C, Bouyabrine H, Courouble P, Koechlin-Ramonatxo C, Seb-bane M, Similowski T, Scheuermann V, Mebazaa A, Capdevila X, Mornet D, Mercier J, Lacampagne A, Philips A, Matecki S: Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med 2011; 183:364-71
11. Levine S, Biswas C, Dierov J, Barsotti R, Shrager JB, Nguyen T, Sonnad S, Kucharchzuk JC, Kaiser LR, Singhal S, Budak MT: Increased proteolysis, myosin depletion, and atrophic AKT-FOXO signaling in human diaphragm disuse. Am J Re-spir Crit Care Med 2011; 183:483-90
12. Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothen-berg P, Zhu J, Sachdeva R, Sonnad S, Kaiser LR, Rubinstein NA, Powers SK, Shrager JB: Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 2008; 358:1327-35
13. Vassilakopoulos T, Petrof BJ: Ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 2004; 169:336-41
14. Schultz MJ: Weaning from mechanical ventilation: Stay poised between load and strength. ANESTHESIOLOGY 2010; 113:273-5
15. Goll DE, Thompson VF, Li H, Wei W, Cong J: The calpain system. Physiol Rev 2003; 83:731-801
16. Powers SK, Kavazis AN, McClung JM: Oxidative stress and disuse muscle atrophy. J Appl Physiol 2007; 102:2389-97
17. Jaber S, Jung B, Matecki S, Petrof B: Clinical review: Ventilator induced diaphragm dysfunction: Humans studies confirm animal model findings! Crit Care 2011; 15:206
18. Petrof BJ, Jaber S, Matecki S: Ventilator-induced diaphragmatic dysfunction. Curr Opin Crit Care 2010; 16:19-25
19. Tobin MJ, Laghi F, Jubran A: Narrative review: Ventilator-induced respiratory muscle weakness. Ann Intern Med 2010; 153:240-5
20. Powers SK, Shanely RA, Coombes JS, Koesterer TJ, McKenzie M, Van Gammeren D, Cicale M, Dodd SL: Mechanical ventilation results in progressive contractile dysfunction in the diaphragm. J Appl Physiol 2002; 92:1851-8
21. Maes K, Testelmans D, Powers S, Decramer M, Gayan-Ramirez G: Leupeptin inhibits ventilator-induced diaphragm dysfunction in rats. Am J Respir Crit Care Med 2007; 175:1134-8
22. McClung JM, Kavazis AN, Whidden MA, DeRuisseau KC, Falk DJ, Criswell DS, Powers SK: Antioxidant administration attenuates mechanical ventilation-induced rat diaphragm muscle atrophy independent of protein kinase B (PKB Akt) signalling. J Physiol 2007; 585:203-15
23. Agten A, Maes K, Smuder A, Powers SK, Decramer M, Gayan-Ramirez G: N-acetylcysteine protects the rat diaphragm from the decreased contractility associated with controlled mechanical ventilation. Crit Care Med 2011; 39:777-82
24. Mulvaney DR, Merkel RA, Bergen WG: Skeletal muscle protein turnover in young male pigs. J Nutr 1985; 115:1057-64
25. Young V: Nutrition and Immunology. Edited by Gershwin M. New York, Humana Press, 2000, pp 49-65
26. Divangahi M, Matecki S, Dudley RW, Tuck SA, Bao W, Rad-zioch D, Comtois AS, Petrof BJ: Preferential diaphragmatic weakness during sustained Pseudomonas aeruginosa lung infection. Am J Respir Crit Care Med 2004; 169:679-86
27. Jung B, Constantin JM, Rossel N, Le Goff C, Sebbane M, Coisel Y, Chanques G, Futier E, Hugon G, Capdevila X, Petrof B, Matecki S, Jaber S: Adaptive support ventilation prevents ventilator-induced diaphragmatic dysfunction in piglet: An in vivo and in vitro study. ANESTHESIOLOGY 2010; 112:1435-43
28. Matecki S, Guibinga GH, Petrof BJ: Regenerative capacity of the dystrophic (mdx) diaphragm after induced injury. Am J Physiol Regul Integr Comp Physiol 2004; 287:R961-8
29. Jaber S, Jung B, Sebbane M, Ramonatxo M, Capdevila X, Mercier J, Eledjam JJ, Matecki S: Alteration of the piglet diaphragm contractility in vivo and its recovery after acute hypercapnia. ANESTHESIOLOGY 2008; 108:651-8
30. Boden AG, Harris MC, Parkes MJ: Apneic threshold for CO2 in the anesthetized rat: Fundamental properties under steady-state conditions. J Appl Physiol 1998; 85:898-907
31. Schwarte LA, Zuurbier CJ, Ince C: Mechanical ventilation of mice. Basic Res Cardiol 2000; 95:510-20
32. Schnader J, Howell S, Fitzgerald RS, Roussos C: Interaction of fatigue and hypercapnia in the canine diaphragm. J Appl Physiol 1988; 64:1636-43
33. Bernard N, Matecki S, Py G, Lopez S, Mercier J, Capdevila X: Effects of prolonged mechanical ventilation on respiratory muscle ultrastructure and mitochondrial respiration in rabbits. Intensive Care Med 2003; 29:111-8
34. Radell P, Edström L, Stibler H, Eriksson LI, Ansved T: Changes in diaphragm structure following prolonged mechanical ventilation in piglets. Acta Anaesthesiol Scand 2004; 48:430-7
35. McClung JM, Kavazis AN, DeRuisseau KC, Falk DJ, Deering MA, Lee Y, Sugiura T, Powers SK: Caspase-3 regulation of diaphragm myonuclear domain during mechanical ventilation-induced atrophy. Am J Respir Crit Care Med 2007; 175:150-9
36. Bellinger AM, Reiken S, Carlson C, Mongillo M, Liu X, Roth-man L, Matecki S, Lacampagne A, Marks AR: Hypernitrosy-lated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat Med 2009; 15:325-30
37. Ottenheijm CA, Heunks LM, Hafmans T, van der Ven PF, Benoist C, Zhou H, Labeit S, Granzier HL, Dekhuijzen PN: Titin and diaphragm dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006; 173:527-34
38. Bartoli M, Richard I: Calpains in muscle wasting. Int J Biochem Cell Biol 2005; 37:2115-33
39. Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE: Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 2004; 113:115-23
40. Pockros PJ, Schiff ER, Shiffman ML, McHutchison JG, Gish RG, Afdhal NH, Makhviladze M, Huyghe M, Hecht D, Olters-dorf T, Shapiro DA: Oral IDN-6556, an antiapoptotic caspase inhibitor, may lower aminotransferase activity in patients with chronic hepatitis C. Hepatology 2007; 46:324-9
41. Kavazis AN, Talbert EE, Smuder AJ, Hudson MB, Nelson WB, Powers SK: Mechanical ventilation induces diaphragmatic mitochondrial dysfunction and increased oxidant production. Free Radic Biol Med 2009; 46:842-50
42. Rennie MJ: Anabolic resistance in critically ill patients. Crit Care Med 2009; 37:S398-9