ICU-acquired weakness: Mechanisms of disability

Current Opinion in Critical Care

Volumn 18, Issue 5, 2012, Pages 509-517

  Santos, Claudia C Dos ^a   Batt, Jane ^a  

^a ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

Critical illness myopathy; Critical illness polyneuropathy; ICU acquired weakness; Mechanical ventilation; Multiorgan failure

Indexed keywords

AGE; AUTOPHAGY; BLOOD NERVE BARRIER; COMORBIDITY; CRITICAL ILLNESS; DISABILITY; INTENSIVE CARE UNIT; INTENSIVE CARE UNIT ACQUIRED WEAKNESS; MUSCLE ATROPHY; MUSCLE WEAKNESS; MYOPATHY; NEUROPATHY; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN DEGRADATION; REVIEW; WEAKNESS;

CRITICAL ILLNESS; DISABLED PERSONS; HUMANS; INTENSIVE CARE UNITS; MUSCLE WEAKNESS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; OXIDATIVE STRESS; PREVALENCE; PROTEOLYSIS; RESPIRATION, ARTIFICIAL; RISK FACTORS;

EID: 84865991495     PISSN: 10705295     EISSN: 15317072     Source Type: Journal    
DOI: 10.1097/MCC.0b013e328357cb5e     Document Type: Review

References (146)

1. Coleman ME, DeMayo F, Yin KC, et al. Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J Biol Chem 1995; 270: 12109-12116.
2. Florini JR, Ewton DZ, Magri KA. Hormones, growth factors, and myogenic differentiation. Annu Rev Physiol 1991; 53:201-216.
3. Musaro A, McCullagh K, Paul A, et al. Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 2001; 27:195-200. (Pubitemid 32157448)
4. Stewart CE, Rotwein P. Growth, differentiation, and survival: multiple physiological functions for insulin-like growth factors. Physiol Rev 1996; 76:1005-1026. (Pubitemid 26346814)
5. Turinsky J, Damrau-Abney A. Akt kinases and 2-deoxyglucose uptake in rat skeletal muscles in vivo: study with insulin and exercise. Am J Physiol 1999; 276:R277-R282. (Pubitemid 29061718)
6. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 2008; 23:160-170.
7. Yang ZZ, Tschopp O, Baudry A, et al. Physiological functions of protein kinase B/Akt. Biochem Soc Trans 2004; 32:350-354. (Pubitemid 38582126)
8. Gibson JN, Halliday D, Morrison WL, et al. Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci (Lond) 1987; 72:503-509. (Pubitemid 17022702)
9. Vesali RF, Cibicek N, Jakobsson T, et al. Protein metabolism in leg muscle following an endotoxin injection in healthy volunteers. Clin Sci (Lond) 2010; 118:421-427.
10. Vesali RF, Klaude M, Rooyackers O, Wernerman J. Amino acid metabolism in leg muscle after an endotoxin injection in healthy volunteers. Am J Physiol Endocrinol Metab 2005; 288:E360-E364. (Pubitemid 40110644)
11. Kumar V, Selby A, Rankin D, et al. Age-related differences in the doseresponse relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 2009; 587:211-217.
12. Rennie MJ. Anabolic resistance in critically ill patients. Crit Care Med 2009; 37:S398-S399.
13. Rennie MJ. Muscle protein turnover and the wasting due to injury and disease. Br Med Bull 1985; 41:257-264. (Pubitemid 15233306)
14. Biolo G, Fleming RY, Maggi SP, et al. Inverse regulation of protein turnover and amino acid transport in skeletal muscle of hypercatabolic patients. J Clin Endocrinol Metab 2002; 87:3378-3384. (Pubitemid 34816392)
15. Jespersen JG, Nedergaard A, Reitelseder S, et al. Activated protein synthesis and suppressed protein breakdown signaling in skeletal muscle of critically ill patients. PLoS One 2011; 6:e18090.
16. Constantin D, McCullough J, Mahajan RP, Greenhaff PL. Novel events in the molecular regulation of muscle mass in critically ill patients. J Physiol 2011; 589:3883-3895.
17. Greenhaff PL, Karagounis LG, Peirce N, et al. Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am J Physiol Endocrinol Metab 2008; 295:E595-E604.
18. Wilkinson SB, Phillips SM, Atherton PJ, et al. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 2008; 586:3701-3717.
19. Attaix D, Ventadour S, Codran A, et al. The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem 2005; 41:173-186. (Pubitemid 41500978)
20. Attaix D, Bechet D. FoxO3 controls dangerous proteolytic liaisons. Cell Metab 2007; 6:425-427. (Pubitemid 350176297)
21. Saini A, Faulkner S, Al-Shanti N, Stewart C. Powerful signals for weak muscles. Ageing Res Rev 2009; 8:251-267.
22. Salanova M, Schiffl G, Puttmann B, et al. Molecular biomarkers monitoring human skeletal muscle fibres and microvasculature following long-term bed rest with and without countermeasures. J Anat 2008; 212:306-318. (Pubitemid 351325486)
23. Hicke L, Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 2003; 19:141-172. (Pubitemid 37487346)
24. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8:931-937. (Pubitemid 47622558)
25. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002; 82:373-428. (Pubitemid 34654457)
26. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007; 315:201-205. (Pubitemid 46166358)
27. Bodine SC, Latres E, Baumhueter S, et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001; 294:1704-1708. (Pubitemid 33104839)
28. Gomes MD, Lecker SH, Jagoe RT, et al. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 2001; 98:14440-14445. (Pubitemid 33121410)
29. Cohen S, Brault JJ, Gygi SP, et al. During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 2009; 185:1083-1095.
30. Lecker SH, Jagoe RT, Gilbert A, et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 2004; 18:39-51. (Pubitemid 38076464)
31. Jagoe RT, Lecker SH, Gomes M, Goldberg AL. Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB J 2002; 16:1697-1712. (Pubitemid 35345118)
32. Sandri M, Sandri C, Gilbert A, et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004; 117:399-412. (Pubitemid 38534545)
33. Kedar V, McDonough H, Arya R, et al. Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I. Proc Natl Acad Sci U S A 2004; 101:18135-18140. (Pubitemid 40054086)
34. Witt SH, Granzier H, Witt CC, Labeit S. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J Mol Biol 2005; 350:713-722. (Pubitemid 40848669)
35. Tintignac LA, Lagirand J, Batonnet S, et al. Degradation ofMyoD mediated by the SCF (MAFbx) ubiquitin ligase. J Biol Chem 2005; 280:2847-2856. (Pubitemid 40189393)
36. Doucet M, Russell AP, Leger B, et al. Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2007; 176:261-269. (Pubitemid 47195876)
37. Klaude M, Fredriksson K, Tjader I, et al. Proteasome proteolytic activity in skeletal muscle is increased in patients with sepsis. Clin Sci (Lond) 2007; 112:499-506. (Pubitemid 46762011)
38. Merritt EK, Cross JM, Bamman MM. Inflammatory and protein metabolism signaling responses in human skeletal muscle after burn injury. J Burn Care Res 2012; 33:291-297.
39. Plant PJ, Brooks D, Faughnan M, et al. Cellular markers of muscle atrophy in chronic obstructive pulmonary disease (COPD). Am J Respir Cell Mol Biol 2010; 42:461-471.
40. Roth GA, Moser B, Krenn C, et al. Heightened levels of circulating 20S proteasome in critically ill patients. Eur J Clin Invest 2005; 35:399-403. (Pubitemid 40826839)
41. Tiao G, Hobler S, Wang JJ, et al. Sepsis is associated with increased mRNAs of the ubiquitin-proteasome proteolytic pathway in human skeletal muscle. J Clin Invest 1997; 99:163-168. (Pubitemid 27053458)
42. de Boer MD, Selby A, Atherton P, et al. The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 2007; 585:241-251. (Pubitemid 350131116)
43. Jones SW, Hill RJ, Krasney PA, et al. Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 2004; 18:1025-1027. (Pubitemid 39561513)
44. Ogawa T, Furochi H, Mameoka M, et al. Ubiquitin ligase gene expression in healthy volunteers with 20-day bedrest. Muscle Nerve 2006; 34:463-469. (Pubitemid 44506715)
45. Batt J, Bain J, Goncalves J, et al. Differential gene expression profiling of short and long term denervated muscle. FASEB J 2006; 20:115-117. (Pubitemid 43100485)
46. Korolchuk VI, Menzies FM, Rubinsztein DC. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett 2010; 584:1393-1398.
47. Mammucari C, Milan G, Romanello V, et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 2007; 6:458-471. (Pubitemid 350163055)
48. Mizushima N, Yamamoto A, Matsui M, et al. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15:1101-1111. (Pubitemid 38316219)
49. O'Leary MF, Hood DA. Denervation-induced oxidative stress and autophagy signaling in muscle. Autophagy 2009; 5:230-231.
50. Wang X, Blagden C, Fan J, et al. Runx1 prevents wasting, myofibrillar disorganization, and autophagy of skeletal muscle. Genes Dev 2005; 19:1715-1722. (Pubitemid 41058367)
51. Masiero E, Agatea L, Mammucari C, et al. Autophagy is required to maintain muscle mass. Cell Metab 2009; 10:507-515.
52. Lloyd TE. Novel therapeutic approaches for inclusion body myositis. Curr Opin Rheumatol 2010; 22:658-664.
53. Grumati P, Coletto L, Sabatelli P, et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 2010; 16:1313-1320.
54. Vanhorebeek I, Gunst J, Derde S, et al. Insufficient activation of autophagy allows cellular damage to accumulate in critically ill patients. J Clin Endocrinol Metab 2011; 96:E633-E645.
55. Hussain SN, Mofarrahi M, Sigala I, et al. Mechanical ventilation-induced diaphragm disuse in humans triggers autophagy. Am J Respir Crit Care Med 2010; 182:1377-1386.
56. Smith IJ, Lecker SH, Hasselgren PO. Calpain activity and muscle wasting in sepsis. Am J Physiol Endocrinol Metab 2008; 295:E762-E771.
57. Vinciguerra M, Musaro A, Rosenthal N. Regulation of muscle atrophy in aging and disease. Adv Exp Med Biol 2010; 694:211-233.
58. Williams AB, Decourten-Myers GM, Fischer JE, et al. Sepsis stimulates release of myofilaments in skeletal muscle by a calcium-dependent mechanism. FASEB J 1999; 13:1435-1443. (Pubitemid 29382511)
59. Reid MB, Moylan JS. Beyond atrophy: redox mechanisms of muscle dysfunction in chronic inflammatory disease. J Physiol 2011; 589:2171-2179.
60. Burke M, Reisler F, Harrington WF. Effect of bridging the two essential thiols of myosin on its spectral and actin-binding properties. Biochemistry 1976; 15:1923-1927.
61. Williams DL Jr, Swenson CA. Disulfide bridges in tropomyosin. Effect on ATPase activity of actomyosin. Eur J Biochem 1982; 127:495-499. (Pubitemid 13214664)
62. Putkey JA, Dotson DG, Mouawad P. Formation of inter-and intramolecular disulfide bonds can activate cardiac troponin C. J Biol Chem 1993; 268:6827-6830. (Pubitemid 23105554)
63. Liu DF, Wang D, Stracher A. The accessibility of the thiol groups on G-and F-actin of rabbit muscle. Biochem J 1990; 266:453-459. (Pubitemid 20090146)
64. Coirault C, Guellich A, Barbry T, et al. Oxidative stress of myosin contributes to skeletal muscle dysfunction in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 2007; 292:H1009-H1017.
65. Dalla LL, Ravara B, Gobbo V, et al. Skeletal muscle myofibrillar protein oxidation in heart failure and the protective effect of Carvedilol. J Mol Cell Cardiol 2005; 38:803-807. (Pubitemid 40591745)
66. van Hees HW, van der Heijden HF, Ottenheijm CA, et al. Diaphragm singlefiber weakness and loss of myosin in congestive heart failure rats. Am J Physiol Heart Circ Physiol 2007; 293:H819-H828. (Pubitemid 47105147)
67. Andrade FH, Reid MB, Westerblad H. Contractile response of skeletal muscle to low peroxide concentrations: myofibrillar calcium sensitivity as a likely target for redox-modulation. FASEB J 2001; 15:309-311.
68. Vescovo G, Ravara B, Dalla LL. Skeletal muscle myofibrillar protein oxidation and exercise capacity in heart failure. Basic Res Cardiol 2008; 103:285-290.
69. Li X, Moody MR, Engel D, et al. Cardiac-specific overexpression of tumor necrosis factor-alpha causes oxidative stress and contractile dysfunction in mouse diaphragm. Circulation 2000; 102:1690-1696.
70. Hardin BJ, Campbell KS, Smith JD, et al. TNF-alpha acts via TNFR1 and muscle-derived oxidants to depress myofibrillar force in murine skeletal muscle. J Appl Physiol 2008; 104:694-699. (Pubitemid 351468797)
71. Reid MB, Lannergren J, Westerblad H. Respiratory and limb muscle weakness induced by tumor necrosis factor-alpha: involvement of muscle myofilaments. Am J Respir Crit Care Med 2002; 166:479-484.
72. Yende S, Waterer GW, Tolley EA, et al. Inflammatory markers are associated with ventilatory limitation and muscle dysfunction in obstructive lung disease in well functioning elderly subjects. Thorax 2006; 61:10-16. (Pubitemid 43106971)
73. Cicoira M, Bolger AP, Doehner W, et al. High tumour necrosis factor-alpha levels are associated with exercise intolerance and neurohormonal activation in chronic heart failure patients. Cytokine 2001; 15:80-86. (Pubitemid 34920508)
74. de Letter MA, Schmitz PI, Visser LH, et al. Risk factors for the development of polyneuropathy and myopathy in critically ill patients. Crit Care Med 2001; 29:2281-2286. (Pubitemid 34038159)
75. Weber-Carstens S, Deja M, Koch S, et al. Risk factors in critical illness myopathy during the early course of critical illness: a prospective observational study. Crit Care 2010; 14:R119.
76. Andersson DC, Marks AR. Fixing ryanodine receptor Ca leak: a novel therapeutic strategy for contractile failure in heart and skeletal muscle. Drug Discov Today Dis Mech 2010; 7:e151-e157.
77. Middlekauff HR. Making the case for skeletal myopathy as the major limitation of exercise capacity in heart failure. Circ Heart Fail 2010; 3:537-546.
78. Lehnart SE. Novel targets for treating heart and muscle disease: stabilizing ryanodine receptors and preventing intracellular calcium leak. Curr Opin Pharmacol 2007; 7:225-232. (Pubitemid 46404746)
79. Bellinger AM, Mongillo M, Marks AR. Stressed out: the skeletal muscle ryanodine receptor as a target of stress. J Clin Invest 2008; 118:445-453. (Pubitemid 351206532)
80. Green HJ, Burnett M, Duhamel TA, et al. Abnormal sarcoplasmic reticulum Ca2+-sequestering properties in skeletal muscle in chronic obstructive pulmonary disease. Am J Physiol Cell Physiol 2008; 295:C350-C357. (Pubitemid 352755763)
81. Haeseler G, Foadi N, Wiegand E, et al. Endotoxin reduces availability of voltage-gated human skeletal muscle sodium channels at depolarized membrane potentials. Crit Care Med 2008; 36:1239-1247. (Pubitemid 351482674)
82. Rossignol B, Gueret G, Pennec JP, et al. Effects of chronic sepsis on the voltage-gated sodium channel in isolated rat muscle fibers. Crit Care Med 2007; 35:351-357. (Pubitemid 46148521)
83. Teener JW, Rich MM. Dysregulation of sodium channel gating in critical illness myopathy. J Muscle Res Cell Motil 2006; 27:291-296. (Pubitemid 44325608)
84. Boczkowski J, Lisdero CL, Lanone S, et al. Endogenous peroxynitrite mediates mitochondrial dysfunction in rat diaphragm during endotoxemia. FASEB J 1999; 13:1637-1646.
85. Brealey D, Karyampudi S, Jacques TS, et al. Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol 2004; 286:R491-R497. (Pubitemid 38252613)
86. Crouser ED, Julian MW, Blaho DV, Pfeiffer DR. Endotoxin-induced mitochondrial damage correlates with impaired respiratory activity. Crit Care Med 2002; 30:276-284. (Pubitemid 34158107)
87. Rooyackers OE, Hesselink MK, Wagenmakers AJ. Contraction failure of skeletal muscle of rats recovering from critical illness. Clin Sci (Lond) 1997; 92:189-195. (Pubitemid 27075722)
88. Rooyackers OE, Gijsen AP, Saris WH, et al. Derangement in aerobic and anaerobic energy metabolism in skeletal muscle of critically ill and recovering rats. Biochim Biophys Acta 1996; 1315:55-60. (Pubitemid 26047214)
89. Schumer W, Erve PR, Obernolte RP. Endotoxemic effect on cardiac and skeletal muscle mitochondria. Surg Gynecol Obstet 1971; 133:433-436.
90. Vanhorebeek I, De VR, Mesotten D, et al. Protection of hepatocyte mitochondrial ultrastructure and function by strict blood glucose control with insulin in critically ill patients. Lancet 2005; 365:53-59. (Pubitemid 40082146)
91. Brealey D, Brand M, Hargreaves I, et al. Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 2002; 360:219-223. (Pubitemid 34804650)
92. Carre JE, Orban JC, Re L, et al. Survival in critical illness is associated with early activation of mitochondrial biogenesis. Am J Respir Crit Care Med 2010; 182:745-751.
93. Fredriksson K, Tjader I, Keller P, et al. Dysregulation of mitochondrial dynamics and the muscle transcriptome in ICU patients suffering from sepsis induced multiple organ failure. PLoS One 2008; 3:e3686.
94. Powers SK, Hudson MB, Nelson WB, et al. Mitochondria-targeted antioxidants protect against mechanical ventilation-induced diaphragm weakness. Crit Care Med 2011; 39:1749-1759.
95. Hunter RB, Kandarian SC. Disruption of either the Nfkb1 or the Bcl3 gene inhibits skeletal muscle atrophy. J Clin Invest 2004; 114:1504-1511. (Pubitemid 40385580)
96. Koncarevic A, Jackman RW, Kandarian SC. The ubiquitin-protein ligase Nedd4 targets Notch1 in skeletal muscle and distinguishes the subset of atrophies caused by reduced muscle tension. FASEB J 2007; 21: 427-437. (Pubitemid 46213490)
97. Judge AR, Koncarevic A, Hunter RB, et al. Role for IkappaBalpha, but not c-Rel, in skeletal muscle atrophy. Am J Physiol Cell Physiol 2007; 292:C372-C382. (Pubitemid 46115145)
98. Ladner KJ, Caligiuri MA, Guttridge DC. Tumor necrosis factor-regulated biphasic activation of NF-kappa B is required for cytokine-induced loss of skeletal muscle gene products. J Biol Chem 2003; 278:2294-2303. (Pubitemid 36801299)
99. Li YP, Reid MB. NF-kappaB mediates the protein loss induced by TNF-alpha in differentiated skeletal muscle myotubes. Am J Physiol Regul Integr Comp Physiol 2000; 279:R1165-R1170.
100. Zhao J, Brault JJ, Schild A, et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6:472-483. (Pubitemid 350163056)
101. McFarlane C, Hennebry A, Thomas M, et al. Myostatin signals through Pax7 to regulate satellite cell self-renewal. Exp Cell Res 2008; 314:317-329. (Pubitemid 350225602)
102. McFarlane C, Plummer E, Thomas M, 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. (Pubitemid 44484641)
103. Durieux AC, Amirouche A, Banzet S, et al. Ectopic expression of myostatin induces atrophy of adult skeletal muscle by decreasing muscle gene expression. Endocrinology 2007; 148:3140-3147. (Pubitemid 46996985)
104. Sandri M, Lin J, Handschin C, et al. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci U S A 2006; 103:16260-16265. (Pubitemid 44715184)
105. Romanello V, Sandri M. Mitochondrial biogenesis and fragmentation as regulators of muscle protein degradation. Curr Hypertens Rep 2010; 12:433-439.
106. Greer EL, Oskoui PR, Banko MR, et al. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 2007; 282:30107-30119. (Pubitemid 350035296)
107. Nakashima K, Yakabe Y. AMPK activation stimulates myofibrillar protein degradation and expression of atrophy-related ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem 2007; 71:1650-1656. (Pubitemid 47358716)
108. Braun TP, Zhu X, Szumowski M, et al. Central nervous system inflammation induces muscle atrophy via activation of the hypothalamic-pituitary-adrenal axis. J Exp Med 2011; 208:2449-2463.
109. Zink W, Kollmar R, Schwab S. Critical illness polyneuropathy and myopathy in the intensive care unit. Nat Rev Neurol 2009; 5:372-379.
110. Latronico N, Bolton CF. Critical illness polyneuropathy and myopathy: a major cause of muscle weakness and paralysis. Lancet Neurol 2011; 10:931-941.
111. Bolton CF, Young GB, Zochodne DW. The neurological complications of sepsis. Ann Neurol 1993; 33:94-100. (Pubitemid 23009915)
112. De JB, Sharshar T, Lefaucheur JP, et al. Paresis acquired in the intensive care unit: a prospective multicenter study. JAMA 2002; 288:2859-2867. (Pubitemid 35425072)
113. Fletcher SN, Kennedy DD, Ghosh IR, et al. Persistent neuromuscular and neurophysiologic abnormalities in long-term survivors of prolonged critical illness. Crit Care Med 2003; 31:1012-1016. (Pubitemid 36444406)
114. 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. (Pubitemid 23284794)
115. Kupfer Y, Namba T, Kaldawi E, Tessler S. Prolonged weakness after longterm infusion of vecuronium bromide. Ann Intern Med 1992; 117:484-486.
116. Hermans G, Vanhorebeek I, Derde S, Van den Berghe G. Metabolic aspects of critical illness polyneuromyopathy. Crit Care Med 2009; 37:S391-S397.
117. Ifergane G, Bersudsky M, Kachko L, Wirguin I. Induction of conduction block by Campylobacter jejuni lipopolysaccharides and focal neural insult. J Neurol Sci 2003; 213:11-14. (Pubitemid 36842859)
118. Bolton CF. Neuromuscular manifestations of critical illness. Muscle Nerve 2005; 32:140-163. (Pubitemid 41061488)
119. Bolton CF. Sepsis and the systemic inflammatory response syndrome: neuromuscular manifestations. Crit Care Med 1996; 24:1408-1416. (Pubitemid 26262418)
120. Dori A, Ifergane G, Saar-Levy T, et al. Readthrough acetylcholinesterase in inflammation-associated neuropathies. Life Sci 2007; 80:2369-2374. (Pubitemid 46818282)
121. Witt NJ, Zochodne DW, Bolton CF, et al. Peripheral nerve function in sepsis and multiple organ failure. Chest 1991; 99:176-184.
122. Zochodne DW, Bolton CF, Wells GA, et al. Critical illness polyneuropathy. A complication of sepsis and multiple organ failure. Brain 1987; 110 (Pt 4):819-841.
123. Op de Coul AA, Verheul GA, Leyten AC, et al. Critical illness polyneuromyopathy after artificial respiration. Clin Neurol Neurosurg 1991; 93:27-33.
124. Fenzi F, Latronico N, Refatti N, Rizzuto N. Enhanced expression of E-selectin on the vascular endothelium of peripheral nerve in critically ill patients with neuromuscular disorders. Acta Neuropathol 2003; 106:75-82. (Pubitemid 36806170)
125. Druschky A, Herkert M, Radespiel-Troger M, et al. Critical illness polyneuropathy: clinical findings and cell culture assay of neurotoxicity assessed by a prospective study. Intensive Care Med 2001; 27:686-693. (Pubitemid 32318330)
126. Hund E. Critical illness polyneuropathy. Curr Opin Neurol 2001; 14:649-653. (Pubitemid 32964586)
127. Fong Y, Moldawer LL, Marano M, et al. Cachectin/TNF or IL-1 alpha induces cachexia with redistribution of body proteins. Am J Physiol 1989; 256:R659-R665.
128. Verheul GA, de Jongh-Leuvenink J, Op de Coul AA, et al. Tumor necrosis factor and interleukin-6 in critical illness polyneuromyopathy. Clin Neurol Neurosurg 1994; 96:300-304. (Pubitemid 24357061)
129. Shimizu F, Sano Y, Haruki H, Kanda T. Advanced glycation end-products induce basement membrane hypertrophy in endoneurial microvessels and disrupt the blood-nerve barrier by stimulating the release of TGF-beta and vascular endothelial growth factor (VEGF) by pericytes. Diabetologia 2011; 54:1517-1526.
130. Miniati M, Monti S, Basta G, et al. Soluble receptor for advanced glycation end products in COPD: relationship with emphysema and chronic cor pulmonale -a case-control study. Respir Res 2011; 12:37.
131. Jabaudon M, Futier E, Roszyk L, et al. Soluble form of the receptor for advanced glycation end products is a marker of acute lung injury but not of severe sepsis in critically ill patients. Crit Care Med 2011; 39:480-488.
132. Creagh-Brown BC, Quinlan GJ, Evans TW, Burke-Gaffney A. The RAGE axis in systemic inflammation, acute lung injury and myocardial dysfunction: an important therapeutic target? Intensive Care Med 2010; 36:1644-1656.
133. Calfee CS, Ware LB, Eisner MD, et al. Plasma receptor for advanced glycation end products and clinical outcomes in acute lung injury. Thorax 2008; 63:1083-1089.
134. Yosef N, Xia RH, Ubogu EE. Development and characterization of a novel human in vitro blood-nerve barrier model using primary endoneurial endothelial cells. J Neuropathol Exp Neurol 2010; 69:82-97.
135. Shah KK, Yang L, Abbruscato TJ. In vitro models of the blood-brain barrier. Methods Mol Biol 2012; 814:431-449.
136. Hatherell K, Couraud PO, Romero IA, et al. Development of a three-dimensional, all-human in vitro model of the blood-brain barrier using mono-, co-, and tri-cultivation Transwell models. J Neurosci Methods 2011; 199:223-229.
137. Wessig C. Detection of blood-nerve barrier permeability by magnetic resonance imaging. Methods Mol Biol 2011; 686:267-271.
138. Kiernan MC, Walters RJ, Andersen KV, et al. Nerve excitability changes in chronic renal failure indicate membrane depolarization due to hyperkalaemia. Brain 2002; 125:1366-1378. (Pubitemid 34587145)
139. Krishnan AV, Phoon RK, Pussell BA, et al. Altered motor nerve excitability in end-stage kidney disease. Brain 2005; 128:2164-2174. (Pubitemid 41253283)
140. Z'Graggen WJ, Lin CS, Howard RS, et al. Nerve excitability changes in critical illness polyneuropathy. Brain 2006; 129:2461-2470. (Pubitemid 44522130)
141. Kiernan MC, Bostock H. Effects of membrane polarization and ischaemia on the excitability properties of human motor axons. Brain 2000; 123 (Pt 12): 2542-2551.
142. Cannon SC, Bean BP. Sodium channels gone wild: resurgent current from neuronal and muscle channelopathies. J Clin Invest 2010; 120:80-83.
143. Novak KR, Nardelli P, Cope TC, et al. Inactivation of sodium channels underlies reversible neuropathy during critical illness in rats. J Clin Invest 2009; 119:1150-1158.
144. Waldhausen E, Mingers B, Lippers P, Keser G. Critical illness polyneuropathy due to parenteral nutrition. Intensive Care Med 1997; 23:922-923.
145. Marino PL, Millili JJ. Possible role of dietary lipids in critical illness polyneuropathy. Intensive Care Med 1998; 24:87. (Pubitemid 28190797)
146. Van den Berghe G, Wouters P, Weekers F, et al. Intensive insulin therapy in critically ill patients. N Engl J Med 2001; 345:1359-1367.