Avoiding Respiratory and Peripheral Muscle Injury During Mechanical Ventilation: Diaphragm-Protective Ventilation and Early Mobilization

Critical Care Clinics

Volumn 34, Issue 3, 2018, Pages 357-381

  Schreiber, Annia ^a   Bertoni, Michele ^b   Goligher, Ewan C ^c,d  

^a IRCCS   (Italy)

^b SPEDALI CIVILI   (Italy)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Intensive care unit; Limb muscle weakness; Mechanical ventilation; Respiratory muscle weakness; Ventilator dependence

Indexed keywords

ARTIFICIAL VENTILATION; BREATHING MUSCLE; CLINICAL OUTCOME; CONCENTRIC LOAD INDUCED INJURY; CRITICAL ILLNESS; CRITICALLY ILL PATIENT; ECCENTRIC LOAD INDUCED INJURY; HUMAN; LIMB WEAKNESS; LUNG VENTILATION; MOBILIZATION; MUSCLE ATROPHY; MUSCLE INJURY; MUSCLE TRAINING; NEUROMUSCULAR ELECTRICAL STIMULATION; NONHUMAN; NUTRITION; POLYNEUROPATHY; REHABILITATION CARE; RESPIRATORY TRACT INJURY; REVIEW; SEPSIS; ATROPHY; BREATHING EXERCISE; DIAPHRAGM; ELECTROTHERAPY; INJURIES; LIMB; MUSCLE WEAKNESS; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES;

ATROPHY; BREATHING EXERCISES; CRITICAL ILLNESS; DIAPHRAGM; EARLY AMBULATION; ELECTRIC STIMULATION THERAPY; EXTREMITIES; HUMANS; MUSCLE WEAKNESS; RESPIRATION, ARTIFICIAL;

EID: 85048293209     PISSN: 07490704     EISSN: 15578232     Source Type: Journal    
DOI: 10.1016/j.ccc.2018.03.005     Document Type: Review

References (127)

1. Esteban, A., Frutos-Vivar, F., Muriel, A., et al. Evolution of mortality over time in patients receiving mechanical ventilation. Am J Respir Crit Care Med 188:2 (2013), 220–230.
2. Doorduin, J., Van Hees, H.W.H., Van Der Hoeven, J.G., et al. Monitoring of the respiratory muscles in the critically ill. Am J Respir Crit Care Med 187:1 (2013), 20–27.
3. Dres, M., Goligher, E.C., Heunks, L.M.A., et al. Critical illness-associated diaphragm weakness. Intensive Care Med, 2017, 10.1007/s00134-017-4928-4.
4. Fan, E., Cheek, F., Chlan, L., 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 190:12 (2014), 1437–1446.
5. Stevens, R.D., Marshall, S.A., Cornblath, D.R., et al. A framework for diagnosing and classifying intensive care unit-acquired weakness. Crit Care Med 37:Suppl. 10 (2009), 299–308.
6. Demoule, A., Molinari, N., Jung, B., et al. Patterns of diaphragm function in critically ill patients receiving prolonged mechanical ventilation: a prospective longitudinal study. Ann Intensive Care, 6(1), 2016, 75.
7. Demoule, A., Jung, B., Prodanovic, H., et al. Diaphragm dysfunction on admission to the intensive care unit. prevalence, risk factors, and prognostic impact—a prospective study. Am J Respir Crit Care Med 188:2 (2013), 213–219.
8. Dres, M., Dube, B.P., Mayaux, J., et al. 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 195:1 (2017), 57–66.
9. Laghi, F., Cattapan, S.E., Jubran, A., et al. Is weaning failure caused by low-frequency fatigue of the diaphragm?. Am J Respir Crit Care Med 167 (2003), 120–127.
10. Jung, B., Moury, P.H., Mahul, M., et al. Diaphragmatic dysfunction in patients with ICU-acquired weakness and its impact on extubation failure. Intensive Care Med 42:5 (2016), 853–861.
11. Kim, W.Y., Suh, H.J., Hong, S.B., et al. Diaphragm dysfunction assessed by ultrasonography: influence on weaning from mechanical ventilation. Crit Care Med 39:12 (2011), 2627–2630.
12. Ferrari, G., De Filippi, G., Elia, F., et al. Diaphragm ultrasound as a new index of discontinuation from mechanical ventilation. Crit Ultrasound J, 6(1), 2014, 10.1186/2036-7902-6-8.
13. Jiang, J.R., Tsai, T.H., Jerng, J.S., et al. Ultrasonographic evaluation of liver/spleen movements and extubation outcome. Chest 126:1 (2004), 179–185.
14. Hooijman, P.E., Beishuizen, A., Witt, C.C., et al. Diaphragm muscle fiber weakness and ubiquitin-proteasome activation in critically ill patients. Am J Respir Crit Care Med 191:10 (2015), 1126–1138.
15. Van den Berg, M., Hooijman, P.E., Beishuizen, A., et al. Diaphragm atrophy and weakness in the absence of mitochondrial dysfunction in the critically ill. Am J Respir Crit Care Med 196:12 (2017), 1544–1558.
16. Levine, S., Nguyen, T., Taylor, N., et al. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 358:13 (2008), 1327–1335.
17. Laghi, F., Shaikh, H.S., Morales, D., et al. Diaphragmatic neuromechanical coupling and mechanisms of hypercapnia during inspiratory loading. Respir Physiol Neurobiol 198:1 (2014), 32–41.
18. De Jonghe, B., Bastuji-Garin, S., Durand, M.-C., et al. Respiratory weakness is associated with limb weakness and delayed weaning in critical illness. Crit Care Med 35:9 (2007), 2007–2015.
19. De Jonghe, B., Sharshar, T., Lefaucheur, J., et al. Paresis acquired in the intensive care unit. JAMA 288:22 (2002), 2859–2867.
20. Hermans, G., Van Mechelen, H., Clerckx, B., 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 190:4 (2014), 410–420.
21. Leijten, F., Harinck-de Weerd, J.E., Poortvliet, D.C., et al. The role of polyneuropathy in motor convalescence after prolonged mechanical ventilation. JAMA 274:15 (1995), 1221–1225.
22. Garnacho-Montero, J., Madrazo-Osuna, J., García-Garmendia, J., et al. Critical illness polyneuropathy: risk factors and clinical consequences. A cohort study in septic patients. Intensive Care Med 27:8 (2001), 1288–1296.
23. Puthucheary, Z.A., Rawal, J., Mcphail, M., et al. Acute skeletal muscle wasting in critical illness. JAMA 310:15 (2013), 1591–1600.
24. Schepens, T., Verbrugghe, W., Dams, K., et al. The course of diaphragm atrophy in ventilated patients assessed with ultrasound: a longitudinal cohort study. Crit Care, 2015, 1–8, 10.1186/s13054-015-1141-0.
25. Goligher, E.C., Fan, E., Herridge, M.S., et al. Evolution of diaphragm thickness during mechanical ventilation: impact of inspiratory effort. Am J Respir Crit Care Med 192:9 (2015), 1080–1088.
26. Supinski, G.S., Ann Callahan, L., Diaphragm weakness in mechanically ventilated critically ill patients. Crit Care, 17(3), 2013, R120.
27. Adler, D., Dupuis-Lozeron, E., Richard, J.-C., et al. Does inspiratory muscle dysfunction predict readmission after intensive care unit discharge?. Am J Respir Crit Care Med 190:3 (2014), 347–349.
28. Medrinal, C., Prieur, G., Frenoy, É., et al. Respiratory weakness after mechanical ventilation is associated with one-year mortality - a prospective study. Crit Care 20:1 (2016), 1–7.
29. Goligher, E.C., Dres, M., Fan, E., et al. Mechanical ventilation–induced diaphragm atrophy strongly impacts clinical outcomes. Am J Respir Crit Care Med 197:2 (2018), 204–213.
30. Dos Santos, C., Hussain, S.N.A., Mathur, S., et al. Mechanisms of chronic muscle wasting and dysfunction after an intensive care unit stay: a pilot study. Am J Respir Crit Care Med 194:7 (2016), 821–830.
31. Herridge, M.S., Chu, L.M., Matte, A., et al. The RECOVER program: disability risk groups and 1-year outcome after 7 or more days of mechanical ventilation. Am J Respir Crit Care Med 194:7 (2016), 831–844.
32. Fan, E., Dowdy, D.W., Colantuoni, E., et al. Physical complications in acute lung injury survivors: a 2-year longitudinal prospective study. Crit Care Med 42:4 (2014), 849–859.
33. Bolton, C.F., Gilbert, J.J., Hahn, A.F., et al. Polyneuropathy in critically ill patients. J Neurol Neurosurg Psychiatry 47 (1984), 1223–1231.
34. Kress, J.P., Hall, J.B., ICU-acquired weakness and recovery from critical illness. N Engl J Med 370:17 (2014), 1626–1635.
35. Bolton, C.F., Neuromuscular manifestations of critical illness. Muscle Nerve 32:2 (2005), 140–163.
36. Asher, R.A.J., Dangers of going to bed. Br Med J 2:4536 (1947), 967–968.
37. Tesch, P.A., Lundberg, T.R., Fernandez-Gonzalo, R., Unilateral lower limb suspension: from subject selection to “omic” responses. J Appl Physiol 120:10 (2016), 1207–1214.
38. Jaber, S., Jung, B., Matecki, S., et al. Clinical review: ventilator-induced diaphragmatic dysfunction - human studies confirm animal model findings!. Crit Care, 15(2), 2011, 206.
39. Ottenheijm, C.A.C., Van Hees, H.W.H., Heunks, L.M.A., et al. Titin-based mechanosensing and signaling: role in diaphragm atrophy during unloading?. Am J Physiol Lung Cell Mol Physiol 300 (2011), L161–L166.
40. Picard, M., Jung, B., Liang, F., et al. Mitochondrial dysfunction and lipid accumulation in the human diaphragm during mechanical ventilation. Am J Respir Crit Care Med 186:11 (2012), 1140–1149.
41. Powers, S.K., Shanely, R.A., Coombes, J.S., et al. Mechanical ventilation results in progressive contractile dysfunction in the diaphragm. J Appl Physiol 92 (2002), 1851–1858.
42. Le Bourdelles, G., Viires, N., Boczkowski, J., et al. Effects of mechanical ventilation on diaphragmatic contractile properties in rats. Am J Respir Crit Care Med 149:6 (1994), 1539–1544.
43. Sassoon, C.S.H., Caiozzo, V.J., Manka, A., et al. Altered diaphragm contractile properties with controlled mechanical ventilation. J Appl Physiol 92:6 (2002), 2585–2595.
44. Yang, L., Luo, J., Bourdon, J., et al. Controlled mechanical ventilation leads to remodeling of the rat diaphragm. Am J Respir Crit Care Med 166:8 (2002), 1135–1140.
45. Anzueto, A., Peters, J.I., Tobin, M.J., et al. Effects of prolonged controlled mechanical ventilation on diaphragmatic function in healthy adult baboons. Crit Care Med 25:7 (1997), 1187–1190.
46. Radell, P.J., Remahl, S., Nichols, D.G., et al. Effects of prolonged mechanical ventilation and inactivity on piglet diaphragm function. Intensive Care Med 28:3 (2002), 358–364.
47. Jaber, S., Petrof, B.J., Jung, B., et al. Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med 183:3 (2011), 364–371.
48. Hooijman, P.E., Beishuizen, A., de Waard, M.C., et al. Diaphragm fiber strength is reduced in critically ill patients and restored by a troponin activator. Am J Respir Crit Care Med 189:7 (2014), 863–865.
49. Zambon, M., Beccaria, P., Matsuno, J., et al. Mechanical ventilation and diaphragmatic atrophy in critically ill patients: an ultrasound study. Crit Care Med 44:7 (2016), 1347–1352.
50. Goligher, E.C., Laghi, F., Detsky, M.E., et al. Measuring diaphragm thickness with ultrasound in mechanically ventilated patients: feasibility, reproducibility and validity. Intensive Care Med, 2015, 10.1007/s00134-015-3687-3.
51. Puthucheary, Z., Harridge, S., Hart, N., Skeletal muscle dysfunction in critical care: wasting, weakness, and rehabilitation strategies. Crit Care Med 38:10 (2010), 676–682.
52. Jiang, T., Reid, W.D., Road, J.D., Delayed diaphragm injury and diaphragm force production. Crit Care Med 157 (1998), 736–742.
53. Reid, W.D., Huang, J., Bryson, S., et al. Diaphragm injury and myofibrillar structure induced by resistive loading. J Appl Physiol 76:1 (1994), 176–184.
54. Laghi, F., D'Alfonso, N., Tobin, M.J., Pattern of recovery from diaphragmatic fatigue over 24 hours. J Appl Physiol 79:2 (1995), 539–546.
55. Lin, M.C., Ebihara, S., Dwairi, Q.E.L., et al. Diaphragm sarcolemmal injury is induced by sepsis and alleviated by nitric oxide synthase inhibition. Am J Respir Crit Care Med 158:5 pt I (1998), 1656–1663.
56. Ebihara, S., Hussain, S.N.A., Danialou, G., et al. Mechanical ventilation protects against diaphragm injury in sepsis: interaction of oxidative and mechanical stresses. Am J Respir Crit Care Med 165:2 (2002), 221–228.
57. Orozco-levi, M., Lloreta, J., Minguella, J., et al. Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164 (2001), 1734–1739.
58. Damas, F., Phillips, S.M., Lixandrão, M.E., et al. Early resistance training-induced increases in muscle cross-sectional area are concomitant with edema-induced muscle swelling. Eur J Appl Physiol 116:1 (2016), 49–56.
59. Proske, U., Morgan, D.L., Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptations and clinical applications. J Physiol 537:2 (2001), 333–345.
60. Topulos, G.P., Reid, M.B., Leith, D.E., Pliometric activity of inspiratory muscles: maximal pressure-flow curves. J Appl Physiol 62:1 (1987), 322–327.
61. Gea, J., Zhu, E., Galdiz, J.B., et al. Functional consequences of eccentric contractions of the diaphragm. Arch Bronconeumol 45:2 (2009), 68–74 [in Spanish].
62. Sieck, G.C., Ferreira, L.F., Reid, M.B., et al. Mechanical properties of respiratory muscles. Compr Physiol 3:4 (2013), 1553–1567.
63. Baydur, A., Decay of inspiratory muscle pressure during expiration in anesthetized kyphoscoliosis patients. J Appl Physiol 72:2 (1992), 712–720.
64. Pellegrini, M., Hedenstierna, G., Roneus, A., et al. The diaphragm acts as a brake during expiration to prevent lung collapse. Am J Respir Crit Care Med 195:12 (2017), 1608–1616.
65. Thille, A.W., Rodriguez, P., Cabello, B., et al. Patient-ventilator asynchrony during assisted mechanical ventilation. Intensive Care Med 32:10 (2006), 1515–1522.
66. Akoumianaki, E., Lyazidi, A., Rey, N., et al. Mechanical ventilation-induced reverse-triggered breaths a frequently unrecognized form of neuromechanical coupling. Chest 143:4 (2013), 927–938.
67. Boczkowski, J., Lanone, S., Ungureanu-Longrois, D., et al. Induction of diaphragmatic nitric oxide synthase after endotoxin administration in rats: role on diaphragmatic contractile dysfunction. J Clin Invest 98:7 (1996), 1550–1559.
68. Supinski, G.S., Wang, W., Callahan, L.A., Caspase and calpain activation both contribute to sepsis-induced diaphragmatic weakness. J Appl Physiol 107:5 (2009), 1389–1396.
69. Laghi, F., Tobin, M.J., State of the art disorders of the respiratory muscles. Am J Respir Crit Care Med 168 (2003), 10–48.
70. Hermans, G., Agten, A., Testelmans, D., et al. Increased duration of mechanical ventilation is associated with decreased diaphragmatic force: a prospective observational study. Crit Care, 14(4), 2010, 10.1186/cc9094.
71. Testelmans, D., Maes, K., Wouters, P., et al. Infusions of rocuronium and cisatracurium exert different effects on rat diaphragm function. Intensive Care Med 33:5 (2007), 872–879.
72. Papazian, L., Forel, J.-M., Gacouin, A., et al. Neuromuscular blockers in early acute respiratory distress syndrome. N Engl J Med 363:12 (2010), 1107–1116.
73. Schakman, O., Gilson, H., Thissen, J.P., Mechanisms of glucocorticoid-induced myopathy. J Endocrinol 197:1 (2008), 1–10.
74. Maes, K., Agten, A., Smuder, A., et al. Corticosteroid effects on ventilator-induced diaphragm dysfunction in anesthetized rats depend on the dose administered. Respir Res, 11(1), 2010, 178.
75. Michelet, P., Carreira, S., Demoule, A., et al. Effects of acute respiratory and metabolic acidosis on diaphragm muscle obtained from rats. Anesthesiology 122:4 (2015), 876–883.
76. Schellekens, W.J.M., van Hees, H.W.H., Kox, M., et al. Hypercapnia attenuates ventilator-induced diaphragm atrophy and modulates dysfunction. Crit Care 18:1 (2014), 1–9.
77. Jung, B., Sebbane, M., Goff, C.L., et al. Moderate and prolonged hypercapnic acidosis may protect against ventilator-induced diaphragmatic dysfunction in healthy piglet: an in vivo study. Crit Care 17:1 (2013), 1–8.
78. Callahan, L., Supinski, G.S., Hyperglycemia and acquired weakness in critically ill patients: potential mechanisms. Crit Care, 13(2), 2009, 125.
79. Lewis, M.I., Feinberg, A.T., Fournier, M., IGF-I and/or growth hormone preserve diaphragm fiber size with moderate malnutrition. J Appl Physiol 85:1 (1998), 189–197.
80. Barr, J., Fraser, G.L., Puntillo, K., et al. Clinical practice guidelines for the management of pain, agitation, and delirium in adult patients in the intensive care unit. Crit Care Med, 2013, 263–306, 10.1097/CCM.0b013e3182783b72.
81. Bailey, P., Thomsen, G.E., Spuhler, V.J., et al. Early activity is feasible and safe in respiratory failure patients. Crit Care Med 35:1 (2007), 139–145.
82. Turner, D.A., Cheifetz, I.M., Rehder, K.J., et al. Active rehabilitation and physical therapy during extracorporeal membrane oxygenation while awaiting lung transplantation: a practical approach. Crit Care Med 39:12 (2011), 2593–2598.
83. Griffiths, R.D., Palmer, T.E., Helliwell, T., et al. Effect of passive stretching on the wasting of muscle in the critically ill. Nutrition 11:5 (1995), 428–432.
84. Schweickert, W.D., Pohlman, M.C., Pohlman, A.S., et al. Early physical and occupational therapy in mechanically ventilated, critically ill patients: a randomised controlled trial. Lancet 373:9678 (2009), 1874–1882.
85. Denehy, L., Skinner, E.H., Edbrooke, L., et al. Exercise rehabilitation for patients with critical illness: a randomized controlled trial with 12 months of follow-up. Crit Care, 17(4), 2013, R156.
86. Morris, P.E., Berry, M.J., Files, D.C., et al. Standardized rehabilitation and hospital length of stay among patients with acute respiratory failure a randomized clinical trial. JAMA 315:24 (2016), 2694–2702.
87. Moss, M., Nordon-craft, A., Malone, D., et al. A randomized trial of an intensive physical therapy program for patients with acute respiratory failure. Am J Respir Crit Care Med 193 (2016), 1101–1110.
88. Schaller, S.J., Anstey, M., Blobner, M., et al. Early, goal-directed mobilisation in the surgical intensive care unit: a randomised controlled trial. Lancet 388:10052 (2016), 1377–1388.
89. Tipping, C.J., Harrold, M., Holland, A., et al. The effects of active mobilisation and rehabilitation in ICU on mortality and function: a systematic review. Intensive Care Med 43:2 (2017), 171–183.
90. Jung, B., Constantin, J.-M., Rossel, N., et al. Adaptive support ventilation prevents ventilator-induced diaphragmatic dysfunction in piglet an in vivo and in vitro study. Anesthesiology 6 (2010), 1435–1443.
91. Mauri, T., Grasselli, G., Suriano, G., et al. Control of respiratory drive and effort in extracorporeal severe acute respiratory distress syndrome. Crit Care Med 125 (2016), 159–167.
92. Doorduin, J., Nollet, J.L., Roesthuis, L.H., et al. Partial neuromuscular blockade during partial ventilatory support in sedated patients with high tidal volumes. Am J Respir Crit Care Med 195:8 (2017), 1033–1042.
93. Karagiannidis, C., Lubnoow, M., Philipp, A., et al. Autoregulation of ventilation with neurally adjusted ventilatory assist on extracorporeal lung support. Intensive Care Med 36 (2010), 2038–2044.
94. Elkins, M., Dentice, R., Inspiratory muscle training facilitates weaning from mechanical ventilation among patients in the intensive care unit: a systematic review. J Physiother 61:3 (2015), 125–134.
95. Romer, L.M., McConnell, A.K., Specificity and reversibility of inspiratory muscle training. Med Sci Sports Exerc 35 (2003), 237–244.
96. Ayas, N.T., Cool, F.D.M.C., Gore, R., et al. Prevention of human diaphragm atrophy with short periods of electrical stimulation. Am J Respir Crit Care Med 159 (1999), 2018–2020.
97. Martin, A.D., Joseph, A.M., Beaver, T.M., et al. Effect of intermittent phrenic nerve stimulation during cardiothoracic surgery on mitochondrial respiration in the human diaphragm. Crit Care Med 42:2 (2014), e152–156.
98. Ahn, B., Beaver, T., Tomas, M., et al. Phrenic nerve stimulation increases human diaphragm fiber force after cardiothoracic surgery. Am J Respir Crit Care Med 190:7 (2014), 837–839.
99. Reynolds, S.C., Meyyappan, R., Thakkar, V., et al. Mitigation of ventilator-induced diaphragm atrophy by transvenous phrenic nerve stimulation. Am J Respir Crit Care Med 195:3 (2017), 339–348.
100. Reynolds, S., Ebner, A., Meffen, T., et al. Diaphragm activation in ventilated patients using a novel transvenous phrenic nerve pacing catheter. Crit Care Med 45:7 (2017), e691–e694.
101. Gibson, J.N., Smith, K., Rennie, M.J., Prevention of disuse muscle atrophy by means of electrical stimulation: maintenance of protein synthesis. Lancet 2:8614 (1988), 767–770.
102. Jolley, S.E., Bunnell, A.E., Hough, C.L., ICU-acquired weakness. Chest 150:5 (2016), 1129–1140.
103. Segers, J., Hermans, G., Bruyninckx, F., et al. Feasibility of neuromuscular electrical stimulation in critically ill patients. J Crit Care 29:6 (2014), 1082–1088.
104. Hermans, G., Casaer, M.P., Clerckx, B., 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 1 (2013), 621–629.
105. Powers, S.K., Hudson, M.B., Nelson, W.B., et al. Mitochondrial-targeted antioxidants protect against mechanical ventilation-induced diaphragm weakness. Crit Care Med 39:7 (2011), 1749–1759.
106. Agten, A., Maes, K., Smuder, A., et al. N-Acetylcysteine protects the rat diaphragm from the decreased contractility associated with controlled mechanical ventilation. Crit Care Med 39:4 (2011), 777–782.
107. Travaline, J.M., Sudarshan, S., Roy, B.G., et al. Effect of N -acetylcysteine on human diaphragm strength and fatigability. Am J Respir Crit Care Med 156 (1997), 1567–1571.
108. Takala, J., Ruokonen, E., Webster, N.R., et al. Increased mortality associated with growth hormone treatment in critically ill adults. N Engl J Med 341 (1999), 785–792.
109. Schols, A.M.W.J., Soeters, P.B., Mostert, R.O.B., Physiologic effects of nutritional support and anabolic steroids in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 152 (1995), 1268–1274.
110. Almoosa, K.F., Gupta, A., Pedroza, C., et al. Low testosterone levels are frequent in patients with acute respiratory failure and are associated with poor outcomes. Endocr Pract 20:10 (2014), 1057–1063.
111. Kim, W.Y., Park, S.H., Kim, W.Y., et al. Effect of theophylline on ventilator-induced diaphragmatic dysfunction. J Crit Care 33 (2016), 145–150.
112. Doorduin, J., Sinderby, C.A., Beck, J., et al. The calcium sensitizer levosimendan improves human diaphragm function. Am J Respir Crit Care Med 185:1 (2012), 90–95.
113. van Hees, H.W.H., Dekhuijzen, P.N.R., Heunks, L.M.A., Levosimendan enhances force generation of diaphragm muscle from patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 179 (2009), 41–47.
114. Boussuges, A., Gole, Y., Blanc, P., Diaphragmatic motion studied by M-mode ultrasonography. Chest 135:2 (2009), 391–400.
115. Gottesman, E., Mccool, F.D., Ultrasound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med 155 (1997), 1570–1574.
116. Black, L.F., Hyatt, R.E., Maximal respiratory pressures: normal values and relationships to age and sex. Am Rev Respir Dis 99 (1969), 696–702.
117. Uldry, C., Fitting, J.W., Maximal values of sniff nasal inspiratory pressure in healthy subjects. Thorax 50:4 (1995), 371–375.
118. Gibson, G.J., Whitelaw, W., Siafakas, N., et al. American Thoracic Society/European Respiratory Society ATS/ERS statement on respiratory muscle testing. Am J Respir Crit Care Med 166 (2002), 518–624.
119. Watson, A.C., Hughes, P.D., Harris, M.L., et al. 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 29:7 (2001), 1325–1331.
120. Liu, L., Liu, H., Yang, Y., et al. Neuroventilatory efficiency and extubation readiness in critically ill patients. Crit Care, 16(4), 2012, R143.
121. Ali, N.A., O'Brien, J.M.J., Hoffmann, S.P., et al. Acquired weakness, handgrip strength, and mortality in critically ill patients. Am J Respir Crit Care Med 178:3 (2008), 261–268.
122. Connolly, B., Macbean, V., Crowley, C., et al. Ultrasound for the assessment of peripheral skeletal muscle architecture in critical illness: a systematic review. Crit Care Med 43:4 (2015), 897–905.
123. Laghi, F., Khan, N., Schnell, T., et al. New device for nonvolitional evaluation of quadriceps force in ventilated patients. Muscle Nerve, 2017, 1–8, 10.1002/mus.26026.
124. Latronico, N., Bolton, C.F., Care, N., Critical illness polyneuropathy and myopathy: a major cause of muscle weakness and paralysis. Lancet Neurol 10:10 (2011), 931–941.
125. Latronico, N., Nattino, G., Guarneri, B., 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. F1000Res, 2014, 10.12688/f1000research.3933.1.
126. Hulzebos, E.H.J., Helders, P.J.M., Favié N.J., et al. Muscle training to prevent postoperative pulmonary complications in high-risk. JAMA 296:15 (2006), 1851–1857.
127. Latronico, N., Herridge, M., Hopkins, R.O., et al. The ICM research agenda on intensive care unit-acquired weakness. Intensive Care Med 43:9 (2017), 1270–1281.