Diaphragm atrophy and weakness in the absence of mitochondrial dysfunction in the critically Ill

American Journal of Respiratory and Critical Care Medicine

Volumn 196, Issue 12, 2017, Pages 1544-1558

  Van den Berg, Marloes ^a   Hooijman, Pleuni E ^a   Beishuizen, Albertus ^d   De Waard, Monique C ^b   Paul, Marinus A ^c   Hartemink, Koen J ^e   Van Hees, Hieronymus W H ^f   Lawlor, Michael W ^g   Brocca, Lorenza ^b   Bottinelli, Roberto ^b,h,j   Pellegrino, Maria A ^b,h,i   Stienen, Ger J M ^a,c   Heunks, Leo M A ^b   Wüst, Rob C I ^a,k   Ottenheijm, Coen A C ^a,l,m  

^a Amsterdam Infection and Immunity   (Netherlands)

^b Department of Intensive Care ^*  (United States)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d MEDISCH SPECTRUM TWENTE   (Netherlands)

^e ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

^f RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^g MEDICAL COLLEGE OF WISCONSIN   (United States)

^h Interdepartmental Center for Biology and Sport Medicine   (United States)

ⁱ UNIVERSITY OF PAVIA   (Italy)

^j IRCCS   (Italy)

^k ACADEMIC MEDICAL CENTER   (Netherlands)

^l UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^m VU UNIVERSITY MEDICAL CENTER   (Netherlands)

more..

Author keywords

Critically ill; Diaphragm weakness; Mechanical ventilation; Mitochondrial dysfunction; Oxidative stress

Indexed keywords

ADULT; AGED; ARTICLE; ARTIFICIAL VENTILATION; CELL STRUCTURE; CLINICAL ARTICLE; CRITICALLY ILL PATIENT; DIAPHRAGM DISEASE; DISEASE MARKER; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; HUMAN; LUNG BIOPSY; MALE; MIDDLE AGED; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE WEAKNESS; OXIDATIVE STRESS; PRIORITY JOURNAL; YOUNG ADULT; BIOPSY; CRITICAL ILLNESS; DIAPHRAGM; LUNG; MITOCHONDRION; PATHOLOGY; PATHOPHYSIOLOGY;

ADULT; AGED; BIOPSY; CRITICAL ILLNESS; DIAPHRAGM; FEMALE; HUMANS; LUNG; MALE; MIDDLE AGED; MITOCHONDRIA; MUSCLE WEAKNESS; MUSCULAR ATROPHY; OXIDATIVE STRESS; RESPIRATION, ARTIFICIAL; YOUNG ADULT;

EID: 85029879309     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201703-0501OC     Document Type: Article

References (55)

1. 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.
2. Jaber S, Petrof BJ, Jung B, Chanques G, Berthet JP, Rabuel C, Bouyabrine H, Courouble P, Koechlin-Ramonatxo C, Sebbane M, et al. Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med 2011; 183:364-371.
3. Watson AC, Hughes PD, Louise Harris M, 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 2001;29:1325-1331.
4. McClung JM, Whidden MA, Kavazis AN, Falk DJ, Deruisseau KC, Powers SK. Redox regulation of diaphragm proteolysis during mechanical ventilation. Am J Physiol Regul Integr Comp Physiol 2008;294:R1608-R1617.
5. 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;46:842-850.
6. 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 1985;2010: 1376-1382.
7. 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 2011;39:1749-1759.
8. Gottesman E, McCool FD. Ultrasound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med 1997;155:1570-1574.
9. Chan DC. Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet 2012;46:265-287.
10. Goligher EC, Fan E, Herridge MS, Murray A, Vorona S, Brace D, Rittayamai N, Lanys A, Tomlinson G, Singh JM, et al. Evolution of diaphragm thickness during mechanical ventilation: impact of inspiratory effort. Am J Respir Crit Care Med 2015;192: 1080-1088.
11. Dres M, Dubé BP, Mayaux J, Delemazure J, Reuter D, Brochard L, Similowski T, Demoule A. Coexistence and impact of limb muscle and diaphragm weakness at time of liberation from mechanical ventilation in medical intensive care unit patients. Am J Respir Crit Care Med 2017;195:57-66.
12. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010;141: 280-289.
13. Liu X, Weaver D, Shirihai O, Hajnóczky G. Mitochondrial “kiss-and-run”: interplay between mitochondrial motility and fusion-fission dynamics. EMBO J 2009;28:3074-3089.
14. Chen H, Chomyn A, Chan DC. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 2005;280: 26185-26192.
15. Supinski GS, Callahan LA. Diaphragm weakness in mechanically ventilated critically ill patients. Crit Care 2013;17:R120.
16. Esteban A, Anzueto A, Frutos F, Alía I, Brochard L, Stewart TE, Benito S, Epstein SK, Apezteguía C, Nightingale P, et al.; Mechanical Ventilation International Study Group. Characteristics and outcomes in adult patients receiving mechanical ventilation: a 28-day international study. JAMA 2002;287:345-355.
17. Hooijman PE, Beishuizen A, Witt CC, de Waard MC, Girbes AR, Spoelstra-de Man AM, Niessen HW, Manders E, van Hees HW, van den Brom CE, et al. Diaphragm muscle fiber weakness and ubiquitin-proteasome activation in critically ill patients. Am J Respir Crit Care Med 2015;191: 1126-1138.
18. Demoule A, Jung B, Prodanovic H, Molinari N, Chanques G, Coirault C, Matecki S, Duguet A, Similowski T, Jaber S. Diaphragm dysfunction on admission to the intensive care unit: prevalence, risk factors, and prognostic impact-a prospective study. Am J Respir Crit Care Med 2013;188:213-219.
19. Hooijman PE, Beishuizen A, de Waard MC, de Man FS, Vermeijden JW, Steenvoorde P, Bouwman RA, Lommen W, van Hees HW, Heunks LM, et al. Diaphragm fiber strength is reduced in critically ill patients and restored by a troponin activator. Am J Respir Crit Care Med 2014; 189:863-865.
20. van den Berg M, Hooijman PE, Beishuizen A, de Waard MC, Girbes ARJ, Spoelstra-de Man A, Zaremba R, Lawlor MW, Stienen GJM, Hartemink KJ, et al. Late-breaking abstract: disturbed mitochondrial dynamics and network in diaphragm muscle fibers of mechanically ventilated critically ill patients [abstract]. Eur Respir J 2015;46(Suppl 59):PA850.
21. Jheng HF, Tsai PJ, Guo SM, Kuo LH, Chang CS, Su IJ, Chang CR, Tsai YS. Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol Cell Biol 2012;32: 309-319.
22. Picard M, Azuelos I, Jung B, Giordano C, Matecki S, Hussain S, White K, Li T, Liang F, Benedetti A, et al. Mechanical ventilation triggers abnormal mitochondrial dynamics and morphology in the diaphragm. J Appl Physiol 1985;2015:1161-1171.
23. Liu R, Jin P, Yu L, Wang Y, Han L, Shi T, Li X. Impaired mitochondrial dynamics and bioenergetics in diabetic skeletal muscle. PLoS One 2014;9:e92810.
24. Wüst RC, Helmes M, Stienen GJ. Rapid changes in NADH and flavin autofluorescence in rat cardiac trabeculae reveal large mitochondrial complex II reserve capacity. J Physiol 2015;593:1829-1840.
25. Wüst RC, Myers DS, Stones R, Benoist D, Robinson PA, Boyle JP, Peers C, White E, Rossiter HB. Regional skeletal muscle remodeling and mitochondrial dysfunction in right ventricular heart failure. Am J Physiol Heart Circ Physiol 2012;302:H402-H411.
26. Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothenberg P, Zhu J, Sachdeva R, Sonnad S, Kaiser LR, et al. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 2008;358:1327-1335.
27. Wüst RC, de Vries HJ, Wintjes LT, Rodenburg RJ, Niessen HW, Stienen GJ. Mitochondrial complex I dysfunction and altered NAD(P)H kinetics in rat myocardium in cardiac right ventricular hypertrophy and failure. Cardiovasc Res 2016;111:362-372.
28. Hussain SN, Mofarrahi M, Sigala I, Kim HC, Vassilakopoulos T, Maltais F, Bellenis I, Chaturvedi R, Gottfried SB, Metrakos P, et al. Mechanical ventilation-induced diaphragm disuse in humans triggers autophagy. Am J Respir Crit Care Med 2010;182:1377-1386.
29. Cannavino J, Brocca L, Sandri M, Bottinelli R, Pellegrino MA. PGC1-a over-expression prevents metabolic alterations and soleus muscle atrophy in hindlimb unloaded mice. J Physiol 2014; 592:4575-4589.
30. Picard M, Jung B, Liang F, Azuelos I, Hussain S, Goldberg P, Godin R, Danialou G, Chaturvedi R, Rygiel K, et al. Mitochondrial dysfunction and lipid accumulation in the human diaphragm during mechanical ventilation. Am J Respir Crit Care Med 2012;186:1140-1149.
31. Schellekens WJ, van Hees HW, Linkels M, Dekhuijzen PN, Scheffer GJ, van der Hoeven JG, Heunks LM. Levosimendan affects oxidative and inflammatory pathways in the diaphragm of ventilated endotoxemic mice. Crit Care 2015;19:69.
32. Ottenheijm CA, Heunks LM, Geraedts MC, Dekhuijzen PN. Hypoxia-induced skeletal muscle fiber dysfunction: role for reactive nitrogen species. Am J Physiol Lung Cell Mol Physiol 2006;290: L127-L135.
33. Zhu X, Heunks LM, Versteeg EM, van der Heijden HF, Ennen L, van Kuppevelt TH, Vina J, Dekhuijzen PN. Hypoxia-induced dysfunction of rat diaphragm: role of peroxynitrite. Am J Physiol Lung Cell Mol Physiol 2005;288:L16-L26.
34. Brocca L, Pellegrino MA, Desaphy JF, Pierno S, Camerino DC, Bottinelli R. Is oxidative stress a cause or consequence of disuse muscle atrophy in mice? A proteomic approach in hindlimb-unloaded mice. Exp Physiol 2010;95:331-350.
35. Cannavino J, Brocca L, Sandri M, Grassi B, Bottinelli R, Pellegrino MA. The role of alterations in mitochondrial dynamics and PGC-1a over-expression in fast muscle atrophy following hindlimb unloading. J Physiol 2015;593:1981-1995.
36. Liu Y, Wan Q, Guan Q, Gao L, Zhao J. High-fat diet feeding impairs both the expression and activity of AMPKa in rats’ skeletal muscle. Biochem Biophys Res Commun 2006;339:701-707.
37. Kraegen EW, Saha AK, Preston E, Wilks D, Hoy AJ, Cooney GJ, Ruderman NB. Increased malonyl-CoA and diacylglycerol content and reduced AMPK activity accompany insulin resistance induced by glucose infusion in muscle and liver of rats. Am J Physiol Endocrinol Metab 2006;290:E471-E479.
38. Schepens T, Verbrugghe W, Dams K, Corthouts B, Parizel PM, Jorens PG. The course of diaphragm atrophy in ventilated patients assessed with ultrasound: a longitudinal cohort study. Crit Care 2015;19:422.
39. Fredriksson K, Hammarqvist F, Strigård K, Hultenby K, Ljungqvist O, Wernerman J, Rooyackers O. Derangements in mitochondrial metabolism in intercostal and leg muscle of critically ill patients with sepsis-induced multiple organ failure. Am J Physiol Endocrinol Metab 2006;291:E1044-E1050.
40. Pascual-Guardia S, Árbol F, Sánchez E, Casadevall C, Merlo V, Gea J, Barreiro E. [Inflammation and oxidative stress in respiratory and limb muscles of patients with severe sepsis] [article in Spanish]. Med Clin (Barc) 2013;141:194-200.
41. Emerling BM, Weinberg F, Snyder C, Burgess Z, Mutlu GM, Viollet B, Budinger GR, Chandel NS. Hypoxic activation of AMPK is dependent on mitochondrial ROS but independent of an increase in AMP/ATP ratio. Free Radic Biol Med 2009;46:1386-1391.
42. Tong JF, Yan X, Zhu MJ, Du M. AMP-activated protein kinase enhances the expression of muscle-specific ubiquitin ligases despite its activation of IGF-1/Akt signaling in C2C12 myotubes. J Cell Biochem 2009;108:458-468.
43. McKeown DW, Bonser RS, Kellum JA. Management of the heartbeating brain-dead organ donor. Br J Anaesth 2012;108:i96-i107.
44. Smith M. Physiologic changes during brain stem death: lessons for management of the organ donor. J Heart Lung Transplant 2004;23(9, Suppl):S217-S222.
45. Schellekens WJ, van Hees HW, Kox M, Linkels M, Acuña GL, Dekhuijzen PN, Scheffer GJ, van der Hoeven JG, Heunks LM. Hypercapnia attenuates ventilator-induced diaphragm atrophy and modulates dysfunction. Crit Care 2014;18:R28.
46. Flandin P, Donati Y, Barazzone-Argiroffo C, Muzzin P. Hyperoxia-mediated oxidative stress increases expression of UCP3 mRNA and protein in skeletal muscle. FEBS Lett 2005;579:3411-3415.
47. Eu JP, Hare JM, Hess DT, Skaf M, Sun J, Cardenas-Navina I, Sun QA, Dewhirst M, Meissner G, Stamler JS. Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide. Proc Natl Acad Sci USA 2003;100: 15229-15234.
48. Quality Standards Subcommittee of the American Academy of Neurology. Practice parameters for determining brain death in adults (summary statement). Neurology 1995;45:1012-1014.
49. Sassoon CS, Caiozzo VJ, Manka A, Sieck GC. Altered diaphragm contractile properties with controlled mechanical ventilation. J Appl Physiol 1985;2002:2585-2595.
50. Martin AD, Joseph AM, Beaver TM, Smith BK, Martin TD, Berg K, Hess PJ, Deoghare HV, Leeuwenburgh C. Effect of intermittent phrenic nerve stimulation during cardiothoracic surgery on mitochondrial respiration in the human diaphragm. Crit Care Med 2014;42:e152-e156.
51. Mankowski RT, Ahmed S, Beaver T, Dirain M, Han C, Hess P, Martin T, Smith BK, Someya S, Leeuwenburgh C, et al. Intraoperative hemidiaphragm electrical stimulation reduces oxidative stress and upregulates autophagy in surgery patients undergoing mechanical ventilation: exploratory study. J Transl Med 2016;14:305.
52. Esme H, Cemek M, Sezer M, Saglam H, Demir A, Melek H, Unlu M. High levels of oxidative stress in patients with advanced lung cancer. Respirology 2008;13:112-116.
53. Barreiro E, del Puerto-Nevado L, Puig-Vilanova E, Pérez-Rial S, Sánchez F, Martínez-Galán L, Rivera S, Gea J, González-Mangado N, Peces-Barba G. Cigarette smoke-induced oxidative stress in skeletal muscles of mice. Respir Physiol Neurobiol 2012; 182:9-17.
54. Rosenfeldt F, Wilson M, Lee G, Kure C, Ou R, Braun L, de Haan J. Oxidative stress in surgery in an ageing population: pathophysiology and therapy. Exp Gerontol 2013;48:45-54.
55. Ottenheijm CA, Heunks LM, Sieck GC, Zhan WZ, Jansen SM, Degens H, de Boo T, Dekhuijzen PN. Diaphragm dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2005; 172:200-205.