Cited by 193Intensive Care Unit Cognitive DisordersClinical Nutrition and GastroenterologyRespiratory Support and Mechanisms

Muscular weakness and muscle wasting in the critically ill

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Schefold, Joerg C., Wollersheim, Tobias, Grunow, Julius J., Luedi, Markus M., Z'Graggen, Werner J., Weber‐Carstens, Steffen·2020·Journal of Cachexia, Sarcopenia and Muscle

Abstract

Background: Muscular weakness and/or muscle wasting is recognized as a key medical problem in critically ill patients on intensive care units (ICUs) worldwide. Methods and Results: Intensive care unit‐acquired weakness (ICUAW) results from various diseases leading to critical illness and is observed in about 40% [1080/2686 patients, 95% confidence interval (CI): 38–42%] of mixed (medical–surgical) ICU patients. Muscle strength at ICU discharge is directly associated with mortality 5 years after discharge [hazard ratio 0.946, 95% CI: 0.928–0.968 per point increase in Medical Research Council (MRC) scores, P = 0.001]. ICUAW serves as umbrella term for the subgroups ‘critical illness myopathy’, ‘critical illness polyneuropathy’, and ‘critical illness polyneuromyopathy’, the latter distinguished using electrophysiology and/or biopsy studies. Diagnosing, studying, and developing treatments for ICUAW among the critically ill seems challenging due to the acuity and severity of the underlying heterogeneous diseases. Ventilator‐induced diaphragmatic dysfunction occurs in up to 80% ( n = 32/40) of ICUAW patients after mechanical ventilation and mostly results from distinct muscular pathologies, disuse, underlying critical illness, and/or effects imposed directly by mechanical ventilation. Swallowing disorders/dysphagia likely represent an additional (local) neuromuscular dysfunction/ICUAW sequelae and presents in 10.3% ( n = 96/933) of mixed medical–surgical ICU survivors, with 60.4% ( n = 58/96) of patients remaining dysphagia positive until hospital discharge. Key independent risk factors for dysphagia following mechanical ventilation are baseline neurological disease [odds ratio (OR) 4.45, 95% CI: 2.74–7.24, P < 0.01], emergency admission (OR 2.04, 95% CI: 1.15–3.59, P < 0.01), days on mechanical ventilation (OR 1.19, 95% CI: 1.06–1.34, P < 0.01), days on renal replacement therapy (OR 1.1, 95% CI: 1–1.23, P = 0.03), and disease severity (Acute Physiology and Chronic Health Evaluation II score within first 24 h; OR 1.03, 95% CI: 0.99–1.07, P < 0.01). Dysphagia positivity independently predicts 28‐day and 90‐day mortality (90‐day univariate hazard ratio: 3.74; 95% CI, 2.01–6.95; P < 0.001) and is associated with a 9.2% excess (all‐cause) mortality rate. Conclusions: Neuromuscular weakness and muscle wasting is observed in many survivors of critical illness. ICUAW, ventilator‐induced diaphragmatic dysfunction, and dysphagia are associated with complicated and prolonged ICU stay, impaired weaning from mechanical ventilation, impeded rehabilitative measures, and a considerable impact on morbidity and mortality is noted. Future research strategies should further explore underlying pathomechanisms and lead to development of causal treatment strategies.

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  • Prolonged bed rest is associated with health deficits and functional impairment.

    “Prolonged bed rest is associated with health deficits and functional impairment (1).”

    From Nonuniform loss of muscle strength and atrophy during bed rest: a systematic review (2021) · cites this paper as [1]

    The ICU-acquired weakness-associated complications section states that prolonged bed rest in critically ill patients increases the risk of comorbidities, supporting the health-deficits portion. The Introduction links impaired mobilization and prolonged bed rest as consequences of muscular weakness, but does not establish functional impairment as a consequence of bed rest. The claim also omits the paper’s critically ill patient context. (LLM, conf=0.82)

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  1. [1]Kramer CL. Intensive care unit‐acquired weakness. Neurol Clin 2017; 35: 723– 736. 28962810
  2. [2]Jolley SE, Bunnell AE, Hough CL. ICU‐acquired weakness. Chest 2016; 150: 1129– 1140. 27063347 PMC5103015
  3. [3]Schefold JC, Bierbrauer J, Weber‐Carstens S. Intensive care unit‐acquired weakness (ICUAW) and muscle wasting in critically ill patients with severe sepsis and septic shock. J Cachexia Sarcopenia Muscle 2010; 1: 147– 157. 21475702 PMC3060654
  4. [4]Hermans G, Van den Berghe G. Clinical review: intensive care unit acquired weakness. Crit Care 2015; 19: 274. 26242743 PMC4526175
  5. [5]Friedrich O, Reid MB, Van den Berghe G, Vanhorebeek I, Hermans G, Rich MM, et al. The sick and the weak: neuropathies/myopathies in the critically ill. Physiol Rev 2015; 95: 1025– 1109. 26133937 PMC4491544
  6. [6]Ali NA, O'Brien JM Jr, Hoffmann SP, Phillips G, Garland A, Finley JC, et al. Acquired weakness, handgrip strength, and mortality in critically ill patients. Am J Respir Crit Care Med 2008; 178: 261– 268. 18511703
  7. [7]Zorowitz RD. ICU‐acquired weakness: a rehabilitation perspective of diagnosis, treatment, and functional management. Chest 2016; 150: 966– 971. 27312737
  8. [8]Herridge MS, Tansey CM, Matte A, Tomlinson G, Diaz‐Granados N, Cooper A, et al. Functional disability 5 years after acute respiratory distress syndrome. N Engl J Med 2011; 364: 1293– 1304. 21470008
  9. [9]Van Aerde N, Meersseman P, Debaveye Y, Wilmer A, Gunst J, Casaer MP, et al. Five‐year impact of ICU‐acquired neuromuscular complications: a prospective, observational study. Intensive Care Med 2020; 1– 10. 31970446
  10. [10]Puthucheary ZA, Rawal J, McPhail M, Connolly B, Ratnayake G, Chan P, et al. Acute skeletal muscle wasting in critical illness. JAMA 2013; 310: 1591– 1600. 24108501
  11. [11]Fan E, Cheek F, Chlan L, Gosselink R, Hart N, Herridge MS, et al. An official American Thoracic Society Clinical Practice guideline: the diagnosis of intensive care unit‐acquired weakness in adults. Am J Respir Crit Care Med 2014; 190: 1437– 1446. 25496103
  12. [12]Latronico N, Herridge M, Hopkins RO, Angus D, Hart N, Hermans G, et al. The ICM research agenda on intensive care unit‐acquired weakness. Intensive Care Med 2017; 43: 1270– 1281. 28289812
  13. [13]Appleton RT, Kinsella J, Quasim T. The incidence of intensive care unit‐acquired weakness syndromes: a systematic review. J Intensive Care Soc 2015; 16: 126– 136. 28979394 PMC5606476
  14. [14]Stevens RD, Marshall SA, Cornblath DR, Hoke A, Needham DM, de Jonghe B, et al. A framework for diagnosing and classifying intensive care unit‐acquired weakness. Crit Care Med 2009; 37: S299– S308. 20046114
  15. [15]Berger D, Bloechlinger S, von Haehling S, Doehner W, Takala J, Z'Graggen WJ, et al. Dysfunction of respiratory muscles in critically ill patients on the intensive care unit. J Cachexia Sarcopenia Muscle 2016; 7: 403– 412. 27030815 PMC4788634
  16. [16]Latronico N, Fenzi F, Recupero D, Guarneri B, Tomelleri G, Tonin P, et al. Critical illness myopathy and neuropathy. Lancet 1996; 347: 1579– 1582. 8667865
  17. [17]Latronico N, Bolton CF. Critical illness polyneuropathy and myopathy: a major cause of muscle weakness and paralysis. Lancet Neurol 2011; 10: 931– 941. 21939902
  18. [18]Latronico N, Filosto M, Fagoni N, Gheza L, Guarneri B, Todeschini A, et al. Small nerve fiber pathology in critical illness. PLoS ONE 2013; 8: e75696. 24098716 PMC3787101
  19. [19]Skorna M, Kopacik R, Vlckova E, Adamova B, Kostalova M, Bednarik J. Small‐nerve‐fiber pathology in critical illness documented by serial skin biopsies. Muscle Nerve 2015; 52: 28– 33. 25307783
  20. [20]Jaber S, Petrof BJ, Jung B, Chanques G, Berthet JP, Rabuel C, et al. Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med 2011; 183: 364– 371. 20813887
  21. [21]Koch S, Bierbrauer J, Haas K, Wolter S, Grosskreutz J, Luft FC, et al. Critical illness polyneuropathy in ICU patients is related to reduced motor nerve excitability caused by reduced sodium permeability. Intensive Care Med Exp 2016; 4: 10. 27207148 PMC4875580
  22. [22]Lang CH, Frost RA. Sepsis‐induced suppression of skeletal muscle translation initiation mediated by tumor necrosis factor alpha. Metabolism 2007; 56: 49– 57. 17161226
  23. [23]Van den Berghe G, Schoonheydt K, Becx P, Bruyninckx F, Wouters PJ. Insulin therapy protects the central and peripheral nervous system of intensive care patients. Neurology 2005; 64: 1348– 1353. 15851721
  24. [24]Larsson L, Friedrich O. Critical illness myopathy (CIM) and ventilator‐induced diaphragm muscle dysfunction (VIDD): acquired myopathies affecting contractile proteins. Compr Physiol 2016; 7: 105– 112. 28135001
  25. [26]Callahan LA, Supinski GS. Sepsis‐induced myopathy. Crit Care Med 2009; 37: S354– S367. 20046121 PMC3967515
  26. [27]Jung B, Moury PH, Mahul M, de Jong A, Galia F, Prades A, et al. Diaphragmatic dysfunction in patients with ICU‐acquired weakness and its impact on extubation failure. Intensive Care Med 2016; 42: 853– 861. 26572511
  27. [28]Vassilakopoulos T, Roussos C, Zakynthinos S. Weaning from mechanical ventilation. J Crit Care 1999; 14: 39– 62. 10102723
  28. [29]Ackermann KA, Brander L, Tuchscherer D, Schroder R, Jakob SM, Takala J, et al. Esophageal versus surface recording of diaphragm compound muscle action potential. Muscle Nerve 2015; 51: 598– 600. 25598146
  29. [30]Tuchscherer D, Z'Graggen WJ, Passath C, Takala J, Sinderby C, Brander L. Neurally adjusted ventilatory assist in patients with critical illness‐associated polyneuromyopathy. Intensive Care Med 2011; 37: 1951– 1961. 22048718
  30. [31]Zuercher P, Moret CS, Dziewas R, Schefold JC. Dysphagia in the intensive care unit: epidemiology, mechanisms, and clinical management. Crit Care 2019; 23: 103. 30922363 PMC6438038
  31. [32]Zuercher P, Dziewas R, Schefold JC. Dysphagia in the intensive care unit: a (multidisciplinary) call to action. Intensive Care Med 2020; 46: 554– 556. 31996956
  32. [33]Schefold JC, Berger D, Zurcher P, Lensch M, Perren A, Jakob SM, et al. Dysphagia in mechanically ventilated ICU patients (DYnAMICS): a prospective observational trial. Crit Care Med 2017; 45: 2061– 2069. 29023260
  33. [34]Zuercher P, Schenk NV, Moret C, Berger D, Abegglen R, Schefold JC. Risk factors for dysphagia in ICU patients after invasive mechanical ventilation. Chest 2020. 32525018
  34. [35]Perren A, Zurcher P, Schefold JC. Clinical approaches to assess post‐extubation dysphagia (PED) in the critically ill. Dysphagia 2019; 34: 475– 486. 30684017
  35. [36]Zuercher P, Dziewas R, Schefold JC. Dysphagia in critical care: focus on therapeutical interventions. Intensive Care Med 2020. 32696191
  36. [37]Brodsky MB, Pandian V, Needham DM. Post‐extubation dysphagia: a problem needing multidisciplinary efforts. Intensive Care Med 2020; 46: 93– 96. 31768568 PMC7219527
  37. [38]Zuercher P, Moret C, Schefold JC. Dysphagia in the intensive care unit in Switzerland (DICE)—results of a national survey on the current standard of care. Swiss Med Wkly 2019; 149: w20111. 31330036
  38. [39]van Snippenburg W, Kroner A, Flim M, Hofhuis J, Buise M, Hemler R, et al. Awareness and management of dysphagia in Dutch intensive care units: a nationwide survey. Dysphagia 2019; 34: 220– 228. 30069599
  39. [40]Marian T, Dunser M, Citerio G, Kokofer A, Dziewas R. Are intensive care physicians aware of dysphagia? The MAD (ICU) survey results. Intensive Care Med 2018; 44: 973– 975. 29737377
  40. [41]De Jonghe B, Sharshar T, Lefaucheur JP, Authier FJ, Durand‐Zaleski I, Boussarsar M, et al. Paresis acquired in the intensive care unit: a prospective multicenter study. JAMA 2002; 288: 2859– 2867. 12472328
  41. [42]Kress JP, Hall JB. ICU‐acquired weakness and recovery from critical illness. N Engl J Med 2014; 371: 287– 288. 25014703
  42. [43]Hermans G, Clerckx B, Vanhullebusch T, Segers J, Vanpee G, Robbeets C, et al. Interobserver agreement of Medical Research Council sum‐score and handgrip strength in the intensive care unit. Muscle Nerve 2012; 45: 18– 25. 22190301
  43. [44]Hough CL, Lieu BK, Caldwell ES. Manual muscle strength testing of critically ill patients: feasibility and interobserver agreement. Crit Care 2011; 15: R43. 21276225 PMC3221972
  44. [45]Connolly BA, Jones GD, Curtis AA, Murphy PB, Douiri A, Hopkinson NS, et al. Clinical predictive value of manual muscle strength testing during critical illness: an observational cohort study. Crit Care 2013; 17: R229. 24112540 PMC4057053
  45. [46]Howard RS, Tan SV, Z'Graggen WJ. Weakness on the intensive care unit. Pract Neurol 2008; 8: 280– 295. 18796583
  46. [47]Rich MM, Bird SJ, Raps EC, McCluskey LF, Teener JW. Direct muscle stimulation in acute quadriplegic myopathy. Muscle Nerve 1997; 20: 665– 673. 9149072
  47. [48]Latronico N, Bertolini G, Guarneri B, Botteri M, Peli E, Andreoletti S, et al. Simplified electrophysiological evaluation of peripheral nerves in critically ill patients: the Italian multi‐centre CRIMYNE study. Crit Care 2007; 11: R11. 17254336 PMC2151880
  48. [49]Latronico N, Nattino G, Guarneri B, Fagoni N, Amantini A, Bertolini G, et al. Validation of the peroneal nerve test to diagnose critical illness polyneuropathy and myopathy in the intensive care unit: the multicentre Italian CRIMYNE‐2 diagnostic accuracy study. F1000Research 2014; 3: 127. 25309729 PMC4184363
  49. [50]Z'Graggen WJ, Bostock H. Velocity recovery cycles of human muscle action potentials and their sensitivity to ischemia. Muscle Nerve 2009; 39: 616– 626. 19229874
  50. [51]Z'Graggen WJ, Brander L, Tuchscherer D, Scheidegger O, Takala J, Bostock H. Muscle membrane dysfunction in critical illness myopathy assessed by velocity recovery cycles. Clin Neurophysiol 2011; 122: 834– 841. 21044861
  51. [52]Cunningham JN Jr, Carter NW, Rector FC Jr, Seldin DW. Resting transmembrane potential difference of skeletal muscle in normal subjects and severely ill patients. J Clin Invest 1971; 50: 49– 59. 5101298 PMC291892
  52. [53]Ackermann KA, Bostock H, Brander L, Schroder R, Djafarzadeh S, Tuchscherer D, et al. Early changes of muscle membrane properties in porcine faecal peritonitis. Crit Care 2014; 18: 484. 25145497 PMC4159512
  53. [54]Boerio D, Correa TD, Jakob SM, Ackermann KA, Bostock H, Z'Graggen WJ. Muscle membrane properties in a pig sepsis model: effect of norepinephrine. Muscle Nerve 2018; 57: 808– 813. 29130505
  54. [55]Z'Graggen WJ, Lin CS, Howard RS, Beale RJ, Bostock H. Nerve excitability changes in critical illness polyneuropathy. Brain 2006; 129: 2461– 2470. 16901913
  55. [56]Dos Santos C, Hussain SN, Mathur S, Picard M, Herridge M, Correa J, et al. Mechanisms of chronic muscle wasting and dysfunction after an intensive care unit stay. A pilot study. Am J Respir Crit Care Med 2016; 194: 821– 830. 27058306
  56. [57]Wollersheim T, Woehlecke J, Krebs M, Hamati J, Lodka D, Luther‐Schroeder A, et al. Dynamics of myosin degradation in intensive care unit‐acquired weakness during severe critical illness. Intensive Care Med 2014; 40: 528– 538. 24531339
  57. [58]Helliwell TR, Wilkinson A, Griffiths RD, McClelland P, Palmer TE, Bone JM. Muscle fibre atrophy in critically ill patients is associated with the loss of myosin filaments and the presence of lysosomal enzymes and ubiquitin. Neuropathol Appl Neurobiol 1998; 24: 507– 517. 9888161
  58. [59]Sander HW, Golden M, Danon MJ. Quadriplegic areflexic ICU illness: selective thick filament loss and normal nerve histology. Muscle Nerve 2002; 26: 499– 505. 12362415
  59. [60]Gutmann L, Blumenthal D, Gutmann L, Schochet SS. Acute type II myofiber atrophy in critical illness. Neurology 1996; 46: 819– 821. 8618690
  60. [61]Hooijman PE, Beishuizen A, Witt CC, de Waard MC, Girbes AR, Spoelstra‐de Man AM, et al. Diaphragm muscle fiber weakness and ubiquitin‐proteasome activation in critically ill patients. Am J Respir Crit Care Med 2015; 191: 1126– 1138. 25760684 PMC4451621
  61. [62]Bierbrauer J, Koch S, Olbricht C, Hamati J, Lodka D, Schneider J, et al. Early type II fiber atrophy in intensive care unit patients with nonexcitable muscle membrane. Crit Care Med 2012; 40: 647– 650. 21963579
  62. [63]Helliwell TR, Coakley JH, Wagenmakers AJ, Griffiths RD, Campbell IT, Green CJ, et al. Necrotizing myopathy in critically‐ill patients. J Pathol 1991; 164: 307– 314. 1919868
  63. [64]Bolton CF, Gilbert JJ, Hahn AF, Sibbald WJ. Polyneuropathy in critically ill patients. J Neurol Neurosurg Psychiatry 1984; 47: 1223– 1231. 6094735 PMC1028091
  64. [65]Zochodne DW, Bolton CF, Wells GA, Gilbert JJ, Hahn AF, Brown JD, et al. Critical illness polyneuropathy. A complication of sepsis and multiple organ failure. Brain 1987; 110: 819– 841. 3651796
  65. [66]Coakley JH, Nagendran K, Honavar M, Hinds CJ. Preliminary observations on the neuromuscular abnormalities in patients with organ failure and sepsis. Intensive Care Med 1993; 19: 323– 328. 7755663
  66. [67]De Letter MA, van Doorn PA, Savelkoul HF, Laman JD, Schmitz PI, Op de Coul AA, et al. Critical illness polyneuropathy and myopathy (CIPNM): evidence for local immune activation by cytokine‐expression in the muscle tissue. J Neuroimmunol 2000; 106: 206– 213. 10814799
  67. [68]Stibler H, Edstrom L, Ahlbeck K, Remahl S, Ansved T. Electrophoretic determination of the myosin/actin ratio in the diagnosis of critical illness myopathy. Intensive Care Med 2003; 29: 1515– 1527. 12915938
  68. [69]Ahlbeck K, Fredriksson K, Rooyackers O, Maback G, Remahl S, Ansved T, et al. Signs of critical illness polyneuropathy and myopathy can be seen early in the ICU course. Acta Anaesthesiol Scand 2009; 53: 717– 723. 19388901
  69. [70]Danon MJ, Carpenter S. Myopathy with thick filament (myosin) loss following prolonged paralysis with vecuronium during steroid treatment. Muscle Nerve 1991; 14: 1131– 1139. 1684024
  70. [71]Derde S, Hermans G, Derese I, Guiza F, Hedstrom Y, Wouters PJ, et al. Muscle atrophy and preferential loss of myosin in prolonged critically ill patients. Crit Care Med 2012; 40: 79– 89. 21926599
  71. [72]Khaleeli AA, Edwards RH, Gohil K, McPhail G, Rennie MJ, Round J, et al. Corticosteroid myopathy: a clinical and pathological study. Clin Endocrinol (Oxf) 1983; 18: 155– 166. 6851197
  72. [74]Axer H, Grimm A, Pausch C, Teschner U, Zinke J, Eisenach S, et al. The impairment of small nerve fibers in severe sepsis and septic shock. Crit Care 2016; 20: 64. 26984636 PMC4793743
  73. [75]Rathke TWT, Krebs M, Schülke M, Weber‐Carstens S. Critically ill patients with icu‐acquired weakness show reduced density of myosin in electron microscope early after onset of critical illness. Intensive Care Med Exp 2015; 3: A44.
  74. [76]Leung TW, Wong KS, Hui AC, To KF, Lai ST, Ng WF, et al. Myopathic changes associated with severe acute respiratory syndrome: a postmortem case series. Arch Neurol 2005; 62: 1113– 1117. 16009768
  75. [78]Nanas S, Kritikos K, Angelopoulos E, Siafaka A, Tsikriki S, Poriazi M, et al. Predisposing factors for critical illness polyneuromyopathy in a multidisciplinary intensive care unit. Acta Neurol Scand 2008; 118: 175– 181. 18355395
  76. [79]Brunello AG, Haenggi M, Wigger O, Porta F, Takala J, Jakob SM. Usefulness of a clinical diagnosis of ICU‐acquired paresis to predict outcome in patients with SIRS and acute respiratory failure. Intensive Care Med 2010; 36: 66– 74. 19760204
  77. [80]de Letter MA, Schmitz PI, Visser LH, Verheul FA, Schellens RL, Op de Coul DA, et al. Risk factors for the development of polyneuropathy and myopathy in critically ill patients. Crit Care Med 2001; 29: 2281– 2286. 11801825
  78. [81]Hermans G, Casaer MP, Clerckx B, Guiza F, Vanhullebusch T, Derde S, et al. Effect of tolerating macronutrient deficit on the development of intensive‐care unit acquired weakness: a subanalysis of the EPaNIC trial. Lancet Respir Med 2013; 1: 621– 629. 24461665
  79. [82]Patel BK, Pohlman AS, Hall JB, Kress JP. Impact of early mobilization on glycemic control and ICU‐acquired weakness in critically ill patients who are mechanically ventilated. Chest 2014; 146: 583– 589. 25180722 PMC5831570
  80. [83]Bednarik J, Vondracek P, Dusek L, Moravcova E, Cundrle I. Risk factors for critical illness polyneuromyopathy. J Neurol 2005; 252: 343– 351. 15791390
  81. [84]van den Berghe G, Wouters P, Weekers F, Verwaest C, Bruyninckx F, Schetz M, et al. Intensive insulin therapy in critically ill patients. N Engl J Med 2001; 345: 1359– 1367. 11794168
  82. [85]Gardner AK, Ghita GL, Wang Z, Ozrazgat‐Baslanti T, Raymond SL, Mankowski RT, et al. The development of chronic critical illness determines physical function, quality of life, and long‐term survival among early survivors of sepsis in surgical ICUs. Crit Care Med 2019; 47: 566– 573. 30664526 PMC6422682
  83. [86]Stortz JA, Mira JC, Raymond SL, Loftus TJ, Ozrazgat‐Baslanti T, Wang Z, et al. Benchmarking clinical outcomes and the immunocatabolic phenotype of chronic critical illness after sepsis in surgical intensive care unit patients. J Trauma Acute Care Surgery 2018; 84: 342– 349. PMC5780256 29251709
  84. [87]Price DR, Mikkelsen ME, Umscheid CA, Armstrong EJ. Neuromuscular blocking agents and neuromuscular dysfunction acquired in critical illness: a systematic review and meta‐analysis. Crit Care Med 2016; 44: 2070– 2078. 27513545
  85. [88]Yang T, Li Z, Jiang L, Wang Y, Xi X. Risk factors for intensive care unit‐acquired weakness: a systematic review and meta‐analysis. Acta Neurol Scand 2018; 138: 104– 114. 29845614
  86. [89]Z'Graggen WJ, Schefold JC. Critical illness myopathy: glucocorticoids revisited? Acta physiologica 2019; 225: e13205. 30338655
  87. [90]Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 2013; 280: 4294– 4314. 23517348
  88. [91]Weber‐Carstens S, Schneider J, Wollersheim T, Assmann A, Bierbrauer J, Marg A, et al. Critical illness myopathy and GLUT4: significance of insulin and muscle contraction. Am J Respir Crit Care Med 2013; 187: 387– 396. 23239154
  89. [93]Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, et al. The IGF‐1/PI3K/Akt pathway prevents expression of muscle atrophy‐induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 2004; 14: 395– 403. 15125842
  90. [94]Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 1999; 96: 857– 868. 10102273
  91. [95]Lee JH, Budanov AV, Park EJ, Birse R, Kim TE, Perkins GA, et al. Sestrin as a feedback inhibitor of TOR that prevents age‐related pathologies. Science 2010; 327: 1223– 1228. 20203043 PMC2866632
  92. [96]Demontis F, Perrimon N. FOXO/4E‐BP signaling in Drosophila muscles regulates organism‐wide proteostasis during aging. Cell 2010; 143: 813– 825. 21111239 PMC3066043
  93. [97]Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, et al. Skeletal muscle FoxO1 (FKHR) transgenic mice have less skeletal muscle mass, down‐regulated type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 2004; 279: 41114– 41123. 15272020
  94. [98]Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001; 294: 1704– 1708. 11679633
  95. [100]Langhans C, Weber‐Carstens S, Schmidt F, Hamati J, Kny M, Zhu X, et al. Inflammation‐induced acute phase response in skeletal muscle and critical illness myopathy. PLoS ONE 2014; 9: e92048. 24651840 PMC3961297
  96. [101]Friedland JS, Porter JC, Daryanani S, Bland JM, Screaton NJ, Vesely MJ, et al. Plasma proinflammatory cytokine concentrations, Acute Physiology and Chronic Health Evaluation (APACHE) III scores and survival in patients in an intensive care unit. Crit Care Med 1996; 24: 1775– 1781. 8917024
  97. [102]Majetschak M, Krehmeier U, Bardenheuer M, Denz C, Quintel M, Voggenreiter G, et al. Extracellular ubiquitin inhibits the TNF‐alpha response to endotoxin in peripheral blood mononuclear cells and regulates endotoxin hyporesponsiveness in critical illness. Blood 2003; 101: 1882– 1890. 12406900
  98. [103]Majetschak M, Borgermann J, Waydhas C, Obertacke U, Nast‐Kolb D, Schade FU. Whole blood tumor necrosis factor‐alpha production and its relation to systemic concentrations of interleukin 4, interleukin 10, and transforming growth factor‐beta1 in multiply injured blunt trauma victims. Crit Care Med 2000; 28: 1847– 1853. 10890631
  99. [104]Oliver JC, Bland LA, Oettinger CW, Arduino MJ, McAllister SK, Aguero SM, et al. Cytokine kinetics in an in vitro whole blood model following an endotoxin challenge. Lymphokine Cytokine Res 1993; 12: 115– 120. 8324076
  100. [105]Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, et al. The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone‐treated skeletal muscle. Cell Metab 2007; 6: 376– 385. 17983583
  101. [106]Shimizu N, Yoshikawa N, Ito N, Maruyama T, Suzuki Y, Takeda S, et al. Crosstalk between glucocorticoid receptor and nutritional sensor mTOR in skeletal muscle. Cell Metab 2011; 13: 170– 182. 21284984
  102. [108]Zimmers TA, Davies MV, Koniaris LG, Haynes P, Esquela AF, Tomkinson KN, et al. Induction of cachexia in mice by systemically administered myostatin. Science 2002; 296: 1486– 1488. 12029139
  103. [109]McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, et al. Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF‐kappaB‐independent, FoxO1‐dependent mechanism. J Cell Physiol 2006; 209: 501– 514. 16883577
  104. [111]Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 2007; 6: 458– 471. 18054315
  105. [112]Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6: 472– 483. 18054316
  106. [114]Vanhorebeek I, Gunst J, Derde S, Derese I, Boussemaere M, Guiza F, et al. Insufficient activation of autophagy allows cellular damage to accumulate in critically ill patients. J Clin Endocrinol Metab 2011; 96: E633– E645. 21270330
  107. [115]Mizock BA. Alterations in fuel metabolism in critical illness: hyperglycaemia. Best Pract Res Clin Endocrinol Metab 2001; 15: 533– 551. 11800522
  108. [116]Baron AD, Brechtel G, Wallace P, Edelman SV. Rates and tissue sites of non‐insulin‐ and insulin‐mediated glucose uptake in humans. Am J Physiol 1988; 255: E769– E774. 3059816
  109. [117]Zauner A, Nimmerrichter P, Anderwald C, Bischof M, Schiefermeier M, Ratheiser K, et al. Severity of insulin resistance in critically ill medical patients. Metabolism 2007; 56: 1– 5. 17161218
  110. [118]Huang S, Czech MP. The GLUT4 glucose transporter. Cell Metab 2007; 5: 237– 252. 17403369
  111. [119]Weber‐Carstens S, Koch S, Spuler S, Spies CD, Bubser F, Wernecke KD, et al. Nonexcitable muscle membrane predicts intensive care unit‐acquired paresis in mechanically ventilated, sedated patients. Crit Care Med 2009; 37: 2632– 2637. 19623045
  112. [120]Haeseler G, Foadi N, Wiegand E, Ahrens J, Krampfl K, Dengler R, et al. Endotoxin reduces availability of voltage‐gated human skeletal muscle sodium channels at depolarized membrane potentials. Crit Care Med 2008; 36: 1239– 1247. 18379251
  113. [121]Burtin C, Clerckx B, Robbeets C, Ferdinande P, Langer D, Troosters T, et al. Early exercise in critically ill patients enhances short‐term functional recovery. Crit Care Med 2009; 37: 2499– 2505. 19623052
  114. [122]Morris PE, Goad A, Thompson C, Taylor K, Harry B, Passmore L, et al. Early intensive care unit mobility therapy in the treatment of acute respiratory failure. Crit Care Med 2008; 36: 2238– 2243. 18596631
  115. [123]Connolly B, Salisbury L, O'Neill B, Geneen L, Douiri A, Grocott MP, et al. Exercise rehabilitation following intensive care unit discharge for recovery from critical illness: executive summary of a Cochrane Collaboration systematic review. J Cachexia Sarcopenia Muscle 2016; 7: 520– 526. 27891297 PMC5114628
  116. [125]Wollersheim T, Grunow JJ, Carbon NM, Haas K, Malleike J, Ramme SF, et al. Muscle wasting and function after muscle activation and early protocol‐based physiotherapy: an explorative trial. J Cachexia Sarcopenia Muscle 2019; 10: 734– 747. 31016887 PMC6711421
  117. [126]Fossat G, Baudin F, Courtes L, Bobet S, Dupont A, Bretagnol A, et al. Effect of in‐bed leg cycling and electrical stimulation of the quadriceps on global muscle strength in critically ill adults: a randomized clinical trial. JAMA 2018; 320: 368– 378. 30043066 PMC6583091
  118. [127]Hermans G, De Jonghe B, Bruyninckx F, Van den Berghe G. Interventions for preventing critical illness polyneuropathy and critical illness myopathy. Cochrane Database Syst Rev 2014; 1: CD006832. PMC7390458 24477672
  119. [128]Investigators N‐SS, Finfer S, Chittock DR, Su SY, Blair D, Foster D, et al. Intensive versus conventional glucose control in critically ill patients. N Engl J Med 2009; 360: 1283– 1297. 19318384
  120. [129]Griesdale DE, de Souza RJ, van Dam RM, Heyland DK, Cook DJ, Malhotra A, et al. Intensive insulin therapy and mortality among critically ill patients: a meta‐analysis including NICE‐SUGAR study data. CMAJ 2009; 180: 821– 827. 19318387 PMC2665940
  121. [130]van Gassel RJJ, Baggerman MR, van de Poll MCG. Metabolic aspects of muscle wasting during critical illness. Curr Opin Clin Nutr Metab Care 2020; 23: 96– 101. 31904602 PMC7015189
  122. [131]Fan E, Ciesla ND, Truong AD, Bhoopathi V, Zeger SL, Needham DM. Inter‐rater reliability of manual muscle strength testing in ICU survivors and simulated patients. Intensive Care Med 2010; 36: 1038– 1043. 20213068 PMC2891143
  123. [132]Parry SM, Berney S, Granger CL, Dunlop DL, Murphy L, El‐Ansary D, et al. A new two‐tier strength assessment approach to the diagnosis of weakness in intensive care: an observational study. Crit Care 2015; 19: 52. 25882719 PMC4344764
  124. [133]Van Aerde N, Meersseman P, Debaveye Y, Wilmer A, Gunst J, Casaer MP, et al. Five‐year impact of ICU‐acquired neuromuscular complications: a prospective, observational study. Intensive Care Med 2020; 46: 1184– 1193. 31970446
  125. [134]Vanpee G, Segers J, Van Mechelen H, Wouters P, Van den Berghe G, Hermans G, et al. The interobserver agreement of handheld dynamometry for muscle strength assessment in critically ill patients. Crit Care Med 2011; 39: 1929– 1934. 21572324
  126. [135]Alison JA, Kenny P, King MT, McKinley S, Aitken LM, Leslie GD, et al. Repeatability of the six‐minute walk test and relation to physical function in survivors of a critical illness. Phys Ther 2012; 92: 1556– 1563. 22577064
  127. [136]Denehy L, Nordon‐Craft A, Edbrooke L, Malone D, Berney S, Schenkman M, et al. Outcome measures report different aspects of patient function three months following critical care. Intensive Care Med 2014; 40: 1862– 1869. 25319384
  128. [137]Chan KS, Pfoh ER, Denehy L, Elliott D, Holland AE, Dinglas VD, et al. Construct validity and minimal important difference of 6‐minute walk distance in survivors of acute respiratory failure. Chest 2015; 147: 1316– 1326. 25742048 PMC4420183
  129. [138]Chrispin PS, Scotton H, Rogers J, Lloyd D, Ridley SA. Short Form 36 in the intensive care unit: assessment of acceptability, reliability and validity of the questionnaire. Anaesthesia 1997; 52: 15– 23. 9014540
  130. [139]Robinson KA, Davis WE, Dinglas VD, Mendez‐Tellez PA, Rabiee A, Sukrithan V, et al. A systematic review finds limited data on measurement properties of instruments measuring outcomes in adult intensive care unit survivors. J Clin Epidemiol 2017; 82: 37– 46. 27865899 PMC5325798
  131. [140]Turnbull AE, Rabiee A, Davis WE, Nasser MF, Venna VR, Lolitha R, et al. Outcome measurement in ICU survivorship research from 1970 to 2013: a scoping review of 425 publications. Crit Care Med 2016; 44: 1267– 1277. 26992067 PMC4911315
  132. [141]Connolly B, Denehy L, Hart N, Pattison N, Williamson P, Blackwood B. Physical rehabilitation core outcomes in critical illness (PRACTICE): protocol for development of a core outcome set. Trials 2018; 19: 294. 29801508 PMC5970518
  133. [142]Dinglas VD, Chessare CM, Davis WE, Parker A, Friedman LA, Colantuoni E, et al. Perspectives of survivors, families and researchers on key outcomes for research in acute respiratory failure. Thorax 2018; 73: 7– 12. 28756400 PMC7430927
  134. [143]Needham DM, Sepulveda KA, Dinglas VD, Chessare CM, Friedman LA, Bingham CO 3rd, et al. Core outcome measures for clinical research in acute respiratory failure survivors. An International Modified Delphi Consensus Study. Am J Respir Crit Care Med 2017; 196: 1122– 1130. 28537429 PMC5694837
  135. [145]Cheung AM, Tansey CM, Tomlinson G, Diaz‐Granados N, Matte A, Barr A, et al. Two‐year outcomes, health care use, and costs of survivors of acute respiratory distress syndrome. Am J Respir Crit Care Med 2006; 174: 538– 544. 16763220
  136. [147]Hermans G, Van Mechelen H, Clerckx B, Vanhullebusch T, Mesotten D, Wilmer A, et al. Acute outcomes and 1‐year mortality of intensive care unit‐acquired weakness. A cohort study and propensity‐matched analysis. Am J Respir Crit Care Med 2014; 190: 410– 420. 24825371
  137. [148]Rudis MI, Guslits BJ, Peterson EL, Hathaway SJ, Angus E, Beis S, et al. Economic impact of prolonged motor weakness complicating neuromuscular blockade in the intensive care unit. Crit Care Med 1996; 24: 1749– 1756. 8874316
  138. [149]Kamdar BB, Huang M, Dinglas VD, Colantuoni E, von Wachter TM, Hopkins RO, et al. Joblessness and lost earnings after acute respiratory distress syndrome in a 1‐year national multicenter study. Am J Respir Crit Care Med 2017; 196: 1012– 1020. 28448162 PMC5649982
  139. [150]Griffiths J, Hatch RA, Bishop J, Morgan K, Jenkinson C, Cuthbertson BH, et al. An exploration of social and economic outcome and associated health‐related quality of life after critical illness in general intensive care unit survivors: a 12‐month follow‐up study. Crit Care 2013; 17: R100. 23714692 PMC3706775
  140. [151]Ruhl AP, Lord RK, Panek JA, Colantuoni E, Sepulveda KA, Chong A, et al. Health care resource use and costs of two‐year survivors of acute lung injury. An observational cohort study. Ann Am Thorac Soc 2015; 12: 392– 401. 25594116 PMC4418317
  141. [152]von Haehling S, Morley JE, Coats AJS, Anker SD. Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2019. J Cachexia Sarcopenia Muscle 2019; 10: 1143– 1145. 31661195 PMC6818444

Cited by

Sorted by citations

Authors
Schefold, J. C., Wollersheim, T., Grunow, J. J., Luedi, M. M., Z'Graggen, W. J., & Weber‐Carstens, S.
Affiliations
  • University of Bern (CH)
  • Humboldt-Universität zu Berlin (DE)
Corresponding author
Schefold, Joerg C.
Venue
Journal of Cachexia, Sarcopenia and Muscle
Publisher
Wiley
Published
2020-09-07
Volume
11
Issue
6
Pages
1399-1412
ISSN
  • 2190-5991 (ISSN-L)
  • 2190-6009
OpenAlex
W3084022240
Cited by
193
References
9
Citations by year
2026: 38 · 2025: 44 · 2024: 36 · 2023: 37 · 2022: 26 · 2021: 11 · 2020: 1
FWCI
3.30
Type
journal article
Language
en
Open access
Locations
  • Journal of Cachexia Sarcopenia and Muscle (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by)
  • Open Access CRIS of the University of Bern
Topics
  • Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Intensive Care Unit Cognitive Disorders
  • Health Sciences › Nursing › Nutrition and Dietetics › Clinical Nutrition and Gastroenterology
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory Support and Mechanisms
Keywords
ICU-acquired weakness, critical illness myopathy, critical illness polyneuropathy, critical illness polyneuromyopathy, ventilator-induced diaphragm dysfunction, dysphagia, mechanical ventilation, muscle atrophy, muscle strength, mortality, risk factors, intensive care unit, post-ICU recovery, neuromuscular dysfunction, renal replacement therapy
MeSH terms
Female, Humans, Intensive Care Units, Male, Muscles, Muscular Diseases, Polyneuropathies, Critical Illness, Muscle Weakness

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