Time course of diaphragm function recovery after controlled mechanical ventilation in rats

Journal of Applied Physiology

Volumn 115, Issue 6, 2013, Pages 775-784

  Thomas, Debby ^a   Maes, Karen ^a   Agten, Anouk ^a   Heunks, Leo ^b   Dekhuijzen, Richard ^b   Decramer, Marc ^a   Van Hees, Hieronymus ^b   Gayan Ramirez, Ghislaine ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Controlled mechanical ventilation; Diaphragm contractile properties; Inflammation; Protein synthesis; Reloading

Indexed keywords

CALPAIN; CARRIER PROTEIN; CASP3 PROTEIN, RAT; CASPASE 3; EIF4EBP1 PROTEIN, RAT; MUSCLE PROTEIN; PHOSPHOPROTEIN; PROTEIN KINASE B;

ANIMAL; ANIMAL MODEL; ARTICLE; ARTIFICIAL VENTILATION; BIOSYNTHESIS; CONTROLLED MECHANICAL VENTILATION; CONVALESCENCE; DIAPHRAGM; DIAPHRAGM CONTRACTILE PROPERTIES; INFLAMMATION; MALE; METABOLISM; MUSCLE ATROPHY; MUSCLE CONTRACTION; NEUTROPHIL; OXIDATIVE STRESS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; RAT; RELOADING; SKELETAL MUSCLE; TIME; WISTAR RAT;

CONTROLLED MECHANICAL VENTILATION; DIAPHRAGM CONTRACTILE PROPERTIES; INFLAMMATION; PROTEIN SYNTHESIS; RELOADING;

ANIMALS; CALPAIN; CARRIER PROTEINS; CASPASE 3; DIAPHRAGM; MALE; MODELS, ANIMAL; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCULAR ATROPHY; NEUTROPHILS; OXIDATIVE STRESS; PHOSPHOPROTEINS; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; RESPIRATION, ARTIFICIAL; TIME FACTORS; VENTILATOR WEANING;

EID: 84884236872     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00302.2012     Document Type: Article

References (49)

1. 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 39: 777-782, 2011.
2. Agten A, Maes K, Thomas D, Cielen N, van Hees HW, Dekhuijzen RP, Decramer M, Gayan-Ramirez G. Bortezomib partially protects the rat diaphragm from ventilator-induced diaphragm dysfunction. Crit Care Med 40: 2449-2455, 2012.
3. Andrianjafiniony T, Dupre-Aucouturier S, Letexier D, Couchoux H, Desplanches D. Oxidative stress, apoptosis, and proteolysis in skeletal muscle repair after unloading. Am J Physiol Cell Physiol 299: C307-C315, 2010.
4. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019, 2001.
5. Burkholder TJ, Lieber RL. Sarcomere length operating range of vertebrate muscles during movement. J Exp Biol 204: 1529-1536, 2001.
6. 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 29: 103-110, 2003.
7. Dumont N, Bouchard P, Frenette J. Neutrophil-induced skeletal muscle damage: a calculated and controlled response following hindlimb unloading and reloading. Am J Physiol Regul Integr Comp Physiol 295: R1831-R1838, 2008.
8. Dumont N, Frenette J. Macrophages protect against muscle atrophy and promote muscle recovery in vivo and in vitro: a mechanism partly dependent on the insulin-like growth factor-1 signaling molecule. Am J Pathol 176: 2228-2235, 2010.
9. Enns DL, Raastad T, Ugelstad I, Belcastro AN. Calpain/calpastatin activities and substrate depletion patterns during hindlimb unweighting and reweighting in skeletal muscle. Eur J Appl Physiol 100: 445-455, 2007.
10. Frenette J, Cai B, Tidball JG. Complement activation promotes muscle inflammation during modified muscle use. Am J Pathol 156: 2103-2110, 2000.
11. Frenette J, St-Pierre M, Cote CH, Mylona E, Pizza FX. Muscle impairment occurs rapidly and precedes inflammatory cell accumulation after mechanical loading. Am J Physiol Regul Integr Comp Physiol 282: R351-R357, 2002.
12. Frimel TN, Walter GA, Gibbs JD, Gaidosh GS, Vandenborne K. Noninvasive monitoring of muscle damage during reloading following limb disuse. Muscle Nerve 32: 605-612, 2005.
13. 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 29: 825-833, 2003.
14. Gayan-Ramirez G, Testelmans D, Maes K, Racz GZ, Cadot P, Zador E, Wuytack F, Decramer M. Intermittent spontaneous breathing protects the rat diaphragm from mechanical ventilation effects. Crit Care Med 33: 2804-2809, 2005.
15. Guillot C, Steinberg JG, Delliaux S, Kipson N, Jammes Y, Badier M. Physiological, histological and biochemical properties of rat skeletal muscles in response to hindlimb suspension. J Electromyogr Kinesiol 18: 276-283, 2008.
16. Haitsma JJ. Diaphragmatic dysfunction in mechanical ventilation. Curr Opin Anaesthesiol 24: 214-218, 2011.
17. 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 14: R127, 2010.
18. Hussain SN, Mofarrahi M, Sigala I, Kim HC, Vassilakopoulos T, Maltais F, Bellenis I, Chaturvedi R, Gottfried SB, Metrakos P, Danialou G, Matecki S, Jaber S, Petrof BJ, Goldberg P. Mechanical ventilation-induced diaphragm disuse in humans triggers autophagy. Am J Respir Crit Care Med 182: 1377-1386, 2010.
19. Itai Y, Kariya Y, Hoshino Y. Morphological changes in rat hindlimb muscle fibres during recovery from disuse atrophy. Acta Physiol Scand 181: 217-224, 2004.
20. Jaber S, Jung B, Matecki S, Petrof BJ. Clinical review: ventilatorinduced diaphragmatic dysfunction-human studies confirm animal model findings! Crit Care 15: 206, 2011.
21. Jaber S, Petrof BJ, Jung B, Chanques G, Berthet JP, Rabuel C, Bouyabrine H, Courouble P, Koechlin C, Sebbane 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 183: 364-371, 2011.
22. Laghi F, Cattapan SE, Jubran A, Parthasarathy S, Warshawsky P, Choi YS, Tobin MJ. Is weaning failure caused by low-frequency fatigue of the diaphragm? Am J Respir Crit Care Med 167: 120-127, 2003.
23. 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 149: 1539-1544, 1994.
24. 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 Respir Crit Care Med 183: 483-490, 2011.
25. Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothenberg 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 358: 1327-1335, 2008.
26. Maes K, Testelmans D, Cadot P, Deruisseau K, Powers SK, Decramer M, Gayan-Ramirez G. Effects of acute administration of corticosteroids during mechanical ventilation on rat diaphragm. Am J Respir Crit Care Med 178: 1219-1226, 2008.
27. 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 175: 1134-1138, 2007.
28. Petrof BJ, Jaber S, Matecki S. Ventilator-induced diaphragmatic dysfunction. Curr Opin Crit Care 16: 19-25, 2010.
29. Pottle D, Gosselin LE. Impact of mechanical load on functional recovery after muscle reloading. Med Sci Sports Exerc 32: 2012-2017, 2000.
30. Powers SK, Criswell D. Adaptive strategies of respiratory muscles in response to endurance exercise. Med Sci Sports Exerc 28: 1115-1122, 1996.
31. Powers SK, Hudson MB, Nelson WB, Talbert EE, Min K, Szeto HH, Kavazis AN, Smuder AJ. Mitochondria-targeted antioxidants protect against mechanical ventilation-induced diaphragm weakness. Crit Care Med 39: 1749-1759, 2011.
32. 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 92: 1851-1858, 2002.
33. Sassoon CS, Caiozzo VJ, Manka A, Sieck GC. Altered diaphragm contractile properties with controlled mechanical ventilation. J Appl Physiol 92: 2585-2595, 2002.
34. Schiaffino S, Mammucari C. Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1: 4, 2011.
35. Selsby JT, Rother S, Tsuda S, Pracash O, Quindry J, Dodd SL. Intermittent hyperthermia enhances skeletal muscle regrowth and attenuates oxidative damage following reloading. J Appl Physiol 102: 1702-1707, 2007.
36. Shanely RA, Van Gammeren D, DeRuisseau KC, Zergeroglu AM, McKenzie MJ, Yarasheski KE, Powers SK. Mechanical ventilation depresses protein synthesis in the rat diaphragm. Am J Respir Crit Care Med 170: 994-999, 2004.
37. Shanely RA, Zergeroglu MA, Lennon SL, Sugiura T, Yimlamai T, Enns D, Belcastro A, Powers SK. Mechanical ventilation-induced diaphragmatic atrophy is associated with oxidative injury and increased proteolytic activity. Am J Respir Crit Care Med 166: 1369-1374, 2002.
38. Taillandier D, Aurousseau E, Combaret L, Guezennec CY, Attaix D. Regulation of proteolysis during reloading of the unweighted soleus muscle. Int J Biochem Cell Biol 35: 665-675, 2003.
39. Tidball JG. Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288: R345-R353, 2005.
40. Tidball JG, Berchenko E, Frenette J. Macrophage invasion does not contribute to muscle membrane injury during inflammation. J Leukoc Biol 65: 492-498, 1999.
41. Tidball JG, Wehling-Henricks M. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J Physiol 578: 327-336, 2007.
42. Van Gammeren D, Falk DJ, DeRuisseau KC, Sellman JE, Decramer M, Powers SK. Reloading the diaphragm following mechanical ventilation does not promote injury. Chest 127: 2204-2210, 2005.
43. van Hees HW, Ottenheijm CA, Granzier HL, Dekhuijzen PN, Heunks LM. Heart failure decreases passive tension generation of rat diaphragm fibers. Int J Cardiol 141: 275-283, 2010.
44. van Hees HW, Schellekens WJ, ndrade Acuna GL, Linkels M, Hafmans T, Ottenheijm CA, Granzier HL, Scheffer GJ, van der Hoeven JG, Dekhuijzen PN, Heunks LM. Titin and diaphragm dysfunction in mechanically ventilated rats. Intensive Care Med 38: 702-709, 2012.
45. van Hees HW, van der Heijden HF, Ottenheijm CA, Heunks LM, Pigmans CJ, Verheugt FW, Brouwer RM, Dekhuijzen PN. Diaphragm single-fiber weakness and loss of myosin in congestive heart failure rats. Am J Physiol Heart Circ Physiol 293: H819-H828, 2007.
46. Watson AC, Hughes PD, Louise HM, Hart N, Ware RJ, Wendon J, Green M, Moxham J. Measurement of twitch transdiaphragmatic, esophageal, and endotracheal tube pressure with bilateral anterolateral magnetic phrenic nerve stimulation in patients in the intensive care unit. Crit Care Med 29: 1325-1331, 2001.
47. Whidden MA, Smuder AJ, Wu M, Hudson MB, Nelson WB, Powers SK. Oxidative stress is required for mechanical ventilation-induced protease activation in the diaphragm. J Appl Physiol 108: 1376-1382, 2010.
48. 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 166: 1135-1140, 2002.
49. Zuurbier CJ, Heslinga JW, Lee-de Groot MB, Van der Laarse WJ. Mean sarcomere length-force relationship of rat muscle fibre bundles. J Biomech 28: 83-87, 1995.