Structure to function: Muscle failure in critically ill patients

Journal of Physiology

Volumn 588, Issue 23, 2010, Pages 4641-4648

  Puthucheary, Zudin ^a   Montgomery, Hugh ^a   Moxham, John ^b   Harridge, Stephen ^b   Hart, Nicholas ^c  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; CRITICAL ILLNESS; HUMAN; MUSCLE ATROPHY; MUSCLE FUNCTION; MUSCLE MASS; MUSCLE WEAKNESS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SURVIVAL;

ANIMALS; CRITICAL ILLNESS; HUMANS; MUSCLE WEAKNESS; MUSCLE, SKELETAL; MUSCULAR ATROPHY;

EID: 78649718977     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.197632     Document Type: Review

References (99)

1. Ali NA, O'Brien JM Jr, et al (2008). Acquired weakness, handgrip strength, and mortality in critically ill patients. Am J Respir Crit Care Med 178, 261-268.
2. Arbeille P, Kerbeci P, et al (2009). Quantification of muscle volume by echography: comparison with MRI data on subjects in long-term bed rest. Ultrasound Med Biol 35, 1092-1097.
3. Baumgartner RN, Koehler KM, et al (1998). Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147, 755-763.
4. Bednarik J, Lukas Z, et al (2003). Critical Illness polyneuromyopathy: the electrophysiological components of a complex entity. Intensive Care Med 29, 1505-1514.
5. Berek K, Margreiter J, et al (1996). Polyneuropathies in critically ill patients: a prospective evaluation. Intensive Care Med 22, 849-855.
6. Biolo G, Fleming RY, et al (2002). Inverse regulation of protein turnover and amino acid transport in skeletal muscle of hypercatabolic patients. J Clin Endocrinol Metab 87, 3378-3384.
7. Bodine SC, Latres E, et al (2001a). Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708.
8. Bodine SC, Stitt TN, et al (2001b). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3, 1014-1019.
9. Bohe J, Low A, et al (2003). Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: a dose-response study. J Physiol 552, 315-324.
10. Bolton CF (2000). Evidence of neuromuscular dysfunction in the early stages of the systemic inflammatory response syndrome. Intensive Care Med 26, 1179-1180.
11. Bolton CF, Gilbert JJ, Hahn AF & Sibbald WJ (1984). Polyneuropathy in critically ill patients. J Neurol Neurosurg Psychiatry 47, 1223-1231.
12. Bone RC, Balk RA, et al (1992). Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 101, 1644-1655.
13. Cai D, Frantz JD, et al (2004). IKKβ/NF-κB activation causes severe muscle wasting in mice. Cell 119, 285-298.
14. Campbell IT, Watt T, et al (1995). Muscle thickness, measured with ultrasound, may be an indicator of lean tissue wasting in multiple organ failure in the presence of edema. Am J Clin Nutr 62, 533-539.
15. Caron AZ, Drouin G, et al (2009). A novel hindlimb immobilization procedure for studying skeletal muscle atrophy and recovery in mouse. J Appl Physiol 106, 2049-2059.
16. Cheung AM, Tansey CM, et al (2006). Two-year outcomes, health care use, and costs of survivors of acute respiratory distress syndrome. Am J Respir Crit Care Med 174, 538-544.
17. Coakley JH, Nagendran K, et al (1993). Preliminary observations on the neuromuscular abnormalities in patients with organ failure and sepsis. Intensive Care Med 19, 323-328.
18. Crossland H, Constantin-Teodosiu D, et al (2008). A potential role for Akt/FoXO signalling in both protein loss and the impairment of muscle carbohydrate oxidation during sepsis in rodent skeletal muscle. J Physiol 586, 5589-5600.
19. Crossland H, Constantin-Teodosiu D, et al (2010). Low-dose dexamethasone prevents endotoxaemia-induced muscle protein loss and impairment of carbohydrate oxidation in rat skeletal muscle. J Physiol 588, 1333-1347.
20. Daniels R (2009). Incidence, mortality and economic burden of sepsis "NHS Evidence - emergency and urgent care.
21. De Boer MD, Selby A, et al (2007). The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585, 241-251.
22. De Jonghe B, Sharshar T, et al (2002). Paresis acquired in the intensive care unit: a prospective multicenter study. JAMA 288, 2859-2867.
23. De Jonghe BM, Bastuji-Garin S, Durand MC, Malissin I, Rodrigues P, Cerf C, Outin H, Sharshar T; for Groupe de Reflexion et d'Etude des Neuromyopathies En Reanimation (2007). Respiratory weakness is associated with limb weakness and delayed weaning in critical illness. Crit Care Med 39, 2007-2015.
24. Doucet M, Russell AP, et al (2007). Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 176, 261-269.
25. Duchateau J & Hainaut K (1987). Electrical and mechanical changes in immobilized human muscle. J Appl Physiol 62, 2168-2173.
26. Edwards RH, Young A, et al (1977). Human skeletal muscle function: description of tests and normal values. Clin Sci Mol Med 52, 283-290.
27. Essen P, McNurlan MA, et al (1998). Tissue protein synthesis rates in critically ill patients. Crit Care Med 26, 92-100.
28. Ferrando AA, Lane HW, et al (1996). Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol Endocrinol Metab 270, E627-633.
29. Forsberg AM, Nilsson E, et al (1991). Muscle composition in relation to age and sex. Clin Sci (Lond) 81, 249-256.
30. Fredriksson K, Tjäder I, et al (2008). Dysregulation of mitochondrial dynamics and the muscle transcriptome in ICU patients suffering from sepsis induced multiple organ failure. PLoS One 3, e3686.
31. Fryburg DA, Jahn LA, et al (1995). Insulin and insulin-like growth factor-I enhance human skeletal muscle protein anabolism during hyperaminoacidemia by different mechanisms. J Clin Invest 96, 1722-1729.
32. Gamrin L, Andersson K, et al (1997). Longitudinal changes of biochemical parameters in muscle during critical illness. Metabolism 46, 756-762.
33. Gamrin L, Essen P, et al (1996). A descriptive study of skeletal muscle metabolism in critically ill patients: free amino acids, energy-rich phosphates, protein, nucleic acids, fat, water, and electrolytes. Crit Care Med 24, 575-583.
34. Gatzen C, Scheltings M, et al. (1992). Growth hormone attenuates the abnormal distribution of water in critically ill surgical patients. Surgery 112, 181-87.
35. Gerovasili V, Stefanidis K, et al (2009). Electrical muscle stimulation preserves the muscle mass of critically ill patients: a randomized study. Crit Care 13, R161.
36. Gibson JN, Halliday D, et al (1987). Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci (Lond) 72, 503-509.
37. Gibson JN, Poyser NL, et al (1991). Muscle protein synthesis in patients with rheumatoid arthritis: effect of chronic corticosteroid therapy on prostaglandin F2 alpha availability. Eur J Clin Invest 21, 406-412.
38. Gimson AE (1987). Hepatic dysfunction during bacterial sepsis. Intensive Care Med 13, 162-166.
39. Glover EI, Phillips SM, et al (2008). Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 586, 6049-6061.
40. Gosker HR, Kubat B, et al (2003). Myopathological features in skeletal muscle of patients with chronic obstructive pulmonary disease. Eur Respir J 22, 280-285.
41. Greenhaff PL, Karagounis LG, et al (2008). Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am J Physiol Endocrinol Metab 295, E595-604.
42. Griffiths RD & Hall JB (2009). Exploring intensive care unit-acquired weakness. Preface. Crit Care Med 37(Suppl), S295.
43. Gruther W, Zorn BTC, Paternostro-Sluga T, Quittan M, Fialka-Moser V, Spiss C, Kainberger F & Crevenna R (2008). Muscle wasting in intensive care patients: ultrasound observation of the m. quadriceps femoris muscle layer. J Rehabil Med 40, 185-189.
44. Hamburg NM, McMackin CJ, et al (2007). Physical inactivity rapidly induces insulin resistance and microvascular dysfunction in healthy volunteers. Arterioscler Thromb Vasc Biol 27, 2650-2656.
45. Hammarqvist F, Von Der Decken A, et al (1994). Stress hormone and amino acid infusion in healthy volunteers: short-term effects on protein synthesis and amino acid metabolism in skeletal muscle. Metabolism 43, 1158-1163.
46. Harris ML, Luo YM, et al (2000). Adductor pollicis twitch tension assessed by magnetic stimulation of the ulnar nerve. Am J Respir Crit Care Med 162, 240-245.
47. Harris ML & Moxham J (1998). Measuring respiratory and limb muscle strength using magnetic stimulation. Br J Int Care 8, 21-28.
48. Haussinger D, Roth E, et al. (1993) Cellular hydration state: an important determinant of protein catabolism in health and disease. Lancet 341, 1330-32.
49. Helliwell TR, Wilkinson A, et al (1998). 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 24, 507-517.
50. Herridge MS, Cheung AM, et al (2003). One-year outcomes in survivors of the acute respiratory distress syndrome. N Engl J Med 348, 683-693.
51. Jackman RW & Kandarian SC. (2004). The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287, C834-843.
52. Jones SW, Hill RJ et al (2004). Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 18, 1025-1027.
53. Kandarian SC & Jackman RW (2006). Intracellular signaling during skeletal muscle atrophy. Muscle Nerve 33, 155-165.
54. Klaude M, Fredriksson K, et al (2007). Proteasome proteolytic activity in skeletal muscle is increased in patients with sepsis. Clin Sci (Lond) 112, 499-506.
55. Kleyweg RP, Van Der Meche FG, et al (1991). Interobserver agreement in the assessment of muscle strength and functional abilities in Guillain-Barre syndrome. Muscle Nerve 14, 1103-1109.
56. Kortebein P, Symons TB, et al (2008). Functional impact of 10 days of bed rest in healthy older adults. J Gerontol A Biol Sci Med Sci 63, 1076-1081.
57. Kumar V, Selby A, et al (2009). Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 587, 211-217.
58. Latronico N, Fenzi F, et al (1996). Critical illness myopathy and neuropathy. Lancet 347, 1579-1582.
59. Latronico N, Peli E, et al (2005). Critical illness myopathy and neuropathy. Curr Opin Crit Care 11, 126-132.
60. Lecker SH, Jagoe RT, et al (2004). Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18, 39-51.
61. Lecker SH, Solomon V, et al (1999). Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J Nutr 129(Suppl), 227S-237S.
62. Leger B, Senese R, et al (2009). Atrogin-1, MuRF1, and FoXO, as well as phosphorylated GSK-3β and 4E-BP1 are reduced in skeletal muscle of chronic spinal cord-injured patients. Muscle Nerve 40, 69-78.
63. Leger B, Vergani L, et al (2006). Human skeletal muscle atrophy in amyotrophic lateral sclerosis reveals a reduction in Akt and an increase in atrogin-1. FASEB J 20, 583-585.
64. Louard RJ, Fryburg DA, et al (1992). Insulin sensitivity of protein and glucose metabolism in human forearm skeletal muscle. J Clin Invest 90, 2348-2354.
65. Mancini DM, Walter G, et al (1992). Contribution of skeletal muscle atrophy to exercise intolerance and altered muscle metabolism in heart failure. Circulation 85, 1364-1373.
66. McNurlan MA, Sandgren A, et al (1996). Protein synthesis rates of skeletal muscle, lymphocytes, and albumin with stress hormone infusion in healthy man. Metabolism 45, 1388-1394.
67. Millward D (1980). Protein Turnover in Cardiac and Skeletal Muscle during Normal Growth and Hypertrophy. Elsevier/North Holland, Amsterdam
68. Moore DR, Tang JE, et al (2009). Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise. J Physiol 587, 897-904.
69. Murton AJ, Alamdari N, et al (2009). Effects of endotoxaemia on protein metabolism in rat fast-twitch skeletal muscle and myocardium. PLoS One 4, e6945.
70. Murton AJ, Constantin D, et al (2008). The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy. Biochim Biophys Acta 1782, 730-743.
71. NICE (2009). CG83 Critical Illness Rehabilitation: NICE Guideline.
72. Niskanen M, Kari A, et al (1996). Five-year survival after intensive care: comparison of 12, 180 patients with the general population. Finnish ICU Study Group. Crit Care Med 24, 1962-1967.
73. Polkey MI, Kyroussis D, et al (1996). Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve 19, 549-555.
74. Raguso CA, Kyle U, et al (2006). A 3-year longitudinal study on body composition changes in the elderly: role of physical exercise. Clin Nutr 25, 573-580.
75. Rennie MJ (1985). Muscle protein turnover and the wasting due to injury and disease. Br Med Bull 41, 257-264.
76. Rennie MJ (2009). Anabolic resistance in critically ill patients. Crit Care Med 37(Suppl), S398-399.
77. Sacheck JM, Hyatt JP, et al (2007). Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21, 140-155.
78. Sandri M, Lin J, et al (2006). PGC-1α protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci U S A 103, 16260-1625.
79. Schweickert WD, Pohlman MC, et al (2009). Early physical and occupational therapy in mechanically ventilated, critically ill patients: a randomised controlled trial. Lancet 373, 1874-1882.
80. Seymour JM, Ward K, et al (2009). Ultrasound measurement of rectus femoris cross-sectional area and the relationship to quadriceps strength in chronic obstructive pulmonary disease. Thorax 64, 418-423.
81. Sharshar T, Bastuji-Garin S, et al (2009). Presence and severity of intensive care unit-acquired paresis at time of awakening are associated with increased intensive care unit and hospital mortality. Crit Care Med 37, 3047-3053.
82. Smith GI, Atherton P, et al (2008). Differences in muscle protein synthesis and anabolic signaling in the postabsorptive state and in response to food in 65-80 year old men and women. PLoS One 3, e1875.
83. Soop M, Forsberg E, et al (1989). Muscle alkali-soluble protein, carnitine, water and electrolytes in patients with persistent post-operative infection. Clin Nutr 8, 237-245.
84. Stitt TN, Drujan D, et al (2004). The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14, 395-403.
85. Strom T, Martinussen T, et al (2010). A protocol of no sedation for critically ill patients receiving mechanical ventilation: a randomised trial. Lancet 375, 475-480.
86. Swallow EB, Gosker HR, et al (2007). A novel technique for nonvolitional assessment of quadriceps muscle endurance in humans. J Appl Physiol 103, 739-746.
87. Tennila A, Salmi T, et al (2000). Early signs of critical illness polyneuropathy in ICU patients with systemic inflammatory response syndrome or sepsis. Intensive Care Med 26, 1360-1363.
88. Tiao G, Hobler S, et al (1997). Sepsis is associated with increased mRNAs of the ubiquitin-proteasome proteolytic pathway in human skeletal muscle. J Clin Invest 99, 163-168.
89. Tipton KD, Borsheim E, et al (2003). Acute response of net muscle protein balance reflects 24-h balance after exercise and amino acid ingestion. Am J Physiol Endocrinol Metab 284, E76-89.
90. Tipton, KD, Elliott TA, et al (2007). Stimulation of net muscle protein synthesis by whey protein ingestion before and after exercise. Am J Physiol Endocrinol Metab 292, E71-76.
91. Tomanek RJ & Lund DD (1974). Degeneration of different types of skeletal muscle fibres. II. Immobilization. J Anat 118, 531-541.
92. Trouillet J-L, Scheimberg A, et al (1996). Long-term outcome and quality of life of patients requireing multi-disciplinary intensive care unit admissions after cardiac operations. J Thorac Cardiovasc Surg 112, 926-934.
93. Vesali RF, Cibicek N, et al (2009). Protein metabolism in leg muscle following an endotoxin injection in healthy volunteers. Clin Sci (Lond) 118, 421-427.
94. Vesali RF, Klaude M, et al (2005). Amino acid metabolism in leg muscle after an endotoxin injection in healthy volunteers. Am J Physiol Endocrinol Metab 288, E360-364.
95. Vincent MR (2010). Clinical review: Scoring systems in the critically ill. Crit Care 14, 207.
96. 2+-activated, and ubiquitin-proteasome proteolytic pathways. J Clin Invest 97, 1610-1617.
97. Volpi E, Sheffield-Moore M, et al (2001). Basal muscle amino acid kinetics and protein synthesis in healthy young and older men. JAMA 286, 1206-1212.
98. Waddell DS, Baehr LM, et al (2008). The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am J Physiol Endocrinol Metab 295, E785-797.
99. Watson, AC, Hughes PD, et al (2001). 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.