Diaphragm Dysfunction in Critical Illness

Chest

Volumn 153, Issue 4, 2018, Pages 1040-1051

  Supinski, Gerald S ^a   Morris, Peter E ^a   Dhar, Sanjay ^a   Callahan, Leigh Ann ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

diaphragm weakness; ICU acquired weakness; mechanical ventilation; ultrasound

Indexed keywords

ENZYME ACTIVATOR; MAMMALIAN TARGET OF RAPAMYCIN ACTIVATOR; MYOSTATIN RECEPTOR ANTIBODY; RECEPTOR ANTIBODY; SEDATIVE AGENT; UNCLASSIFIED DRUG;

BREATHING; BREATHING MUSCLE; CRITICAL ILLNESS; CRITICALLY ILL PATIENT; DEATH; DIAPHRAGM DISEASE; HUMAN; HYPERVOLEMIA; INFLAMMATION; LUNG INJURY; MORBIDITY; MORTALITY; NEUROMUSCULAR DISEASE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY FAILURE; RESPIRATORY FUNCTION; REVIEW; SEPSIS; ARTIFICIAL VENTILATION; CROSS INFECTION; DIAGNOSTIC IMAGING; DIAPHRAGM; ECHOGRAPHY; ELECTROTHERAPY; INTENSIVE CARE; MAGNETOTHERAPY; MUSCLE DISEASE; MUSCLE WEAKNESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES;

CRITICAL CARE; CRITICAL ILLNESS; CROSS INFECTION; DIAPHRAGM; ELECTRIC STIMULATION THERAPY; HUMANS; MAGNETIC FIELD THERAPY; MUSCLE WEAKNESS; MUSCULAR DISEASES; RESPIRATION, ARTIFICIAL; RESPIRATORY INSUFFICIENCY; ULTRASONOGRAPHY;

EID: 85044135711     PISSN: 00123692     EISSN: 19313543     Source Type: Journal    
DOI: 10.1016/j.chest.2017.08.1157     Document Type: Review

References (84)

1. Doorduin, J., van Hees, H.W., 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.
2. Heunks, L.M., Doorduin, J., van der Hoeven, J.G., Monitoring and preventing diaphragm injury. Curr Opin Crit Care 21:1 (2015), 34–41.
3. 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 167:2 (2003), 120–127.
4. Watson, A.C., Hughes, P.D., Louise Harris, M., 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.
5. 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(9), 2010, R127.
6. Supinski, G.S., Callahan, L.A., Diaphragm weakness in mechanically ventilated critically ill patients. Crit Care, 17(3), 2013, R120.
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. Luo, Y.M., Hart, N., Mustfa, N., et al. Reproducibility of twitch and sniff transdiaphragmatic pressures. Respir Physiol Neurobiol 132:3 (2002), 301–306.
9. 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 195:3 (2017), 57–66.
10. 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.
11. Tobin, M.J., Laghi, F., Jubran, A., Ventilatory failure, ventilator support, and ventilator weaning. Compr Physiol 2:4 (2012), 2871–2921.
12. Laghi, F., Tobin, M.J., Disorders of the respiratory muscles. Am J Respir Crit Care Med 168:1 (2003), 10–48.
13. Oo, T., Watt, J.W., Soni, B.M., et al. Delayed diaphragm recovery in 12 patients after high cervical spinal cord injury. A retrospective review of the diaphragm status of 107 patients ventilated after acute spinal cord injury. Spinal Cord 37:2 (1999), 117–122.
14. Efthimiou, J., Butler, J., Woodham, C., et al. Diaphragm paralysis following cardiac surgery: role of phrenic nerve cold injury. Ann Thorac Surg 52:4 (1991), 1005–1008.
15. Yang, K.L., Tobin, M.J., A prospective study of indexes predicting the outcome of trials of weaning from mechanical ventilation. N Engl J Med 324:21 (1991), 1445–1450.
16. Shaikh, H., Morales, D., Laghi, F., Weaning from mechanical ventilation. Semin Respir Crit Care Med 35:4 (2014), 451–468.
17. Rosenow, E.C. III, Engel, A.G., Acid maltase deficiency in adults presenting as respiratory failure. Am J Med 64:3 (1978), 485–491.
18. McCool, F.D., Tzelepis, G.E., Dysfunction of the diaphragm. N Engl J Med 366:10 (2012), 932–942.
19. Howard, R.S., Respiratory failure because of neuromuscular disease. Curr Opin Neurol 29:5 (2016), 592–601.
20. van Doorn, P.A., Ruts, L., Jacobs, B.C., Clinical features, pathogenesis, and treatment of Guillain-Barre syndrome. Lancet Neurol 7:10 (2008), 939–950.
21. Mellies, U., Lofaso, F., Pompe disease: a neuromuscular disease with respiratory muscle involvement. Respir Med 103:4 (2009), 477–484.
22. Keunen, R.W., Lambregts, P.C., Op de Coul, A.A., et al. Respiratory failure as initial symptom of acid maltase deficiency. J Neurol Neurosurg Psychiatry 47:5 (1984), 549–552.
23. 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.
24. Supinski, G.S., Westgate, P., Callahan, L.A., Correlation of maximal inspiratory pressure to transdiaphragmatic twitch pressure in intensive care unit patients. Crit Care, 20, 2016, 77.
25. Aubier, M., Murciano, D., Lecocguic, Y., et al. Effect of hypophosphatemia on diaphragmatic contractility in patients with acute respiratory failure. N Engl J Med 313:7 (1985), 420–424.
26. Martinez, F.J., Bermudez-Gomez, M., Celli, B.R., Hypothyroidism. A reversible cause of diaphragmatic dysfunction. Chest 96:5 (1989), 1059–1063.
27. Petrof, B.J., Hussain, S.N., Ventilator-induced diaphragmatic dysfunction: what have we learned?. Curr Opin Crit Care 22:1 (2016), 67–72.
28. Powers, S.K., Shanely, R.A., Coombes, J.S., et al. Mechanical ventilation results in progressive contractile dysfunction in the diaphragm. J Appl Physiol 92:5 (2002), 1851–1858.
29. 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.
30. Knisely, A.S., Leal, S.M., Singer, D.B., Abnormalities of diaphragmatic muscle in neonates with ventilated lungs. J Pediatr 113:6 (1988), 1074–1077.
31. 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.
32. Hussain, S.N., Cornachione, A.S., Guichon, C., et al. Prolonged controlled mechanical ventilation in humans triggers myofibrillar contractile dysfunction and myofilament protein loss in the diaphragm. Thorax 71:5 (2016), 436–445.
33. Picard, M., Azuelos, I., Jung, B., et al. Mechanical ventilation triggers abnormal mitochondrial dynamics and morphology in the diaphragm. J Appl Physiol (1985) 118:9 (2015), 1161–1171.
34. Tang, H., Smith, I.J., Hussain, S.N., et al. The JAK-STAT pathway is critical in ventilator-induced diaphragm dysfunction. Mol Med 20 (2015), 579–589.
35. Matecki, S., Dridi, H., Jung, B., et al. Leaky ryanodine receptors contribute to diaphragmatic weakness during mechanical ventilation. Proc Natl Acad Sci U S A 113:32 (2016), 9069–9074.
36. 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.
37. Kavazis, A.N., Talbert, E.E., Smuder, A.J., et al. Mechanical ventilation induces diaphragmatic mitochondrial dysfunction and increased oxidant production. Free Radic Biol Med 46:6 (2009), 842–850.
38. DeRuisseau, K.C., Kavazis, A.N., Deering, M.A., et al. Mechanical ventilation induces alterations of the ubiquitin-proteasome pathway in the diaphragm. J Appl Physiol 98:4 (2005), 1314–1321.
39. Zergeroglu, M.A., McKenzie, M.J., Shanely, R.A., et al. Mechanical ventilation-induced oxidative stress in the diaphragm. J Appl Physiol 95:3 (2003), 1116–1124.
40. Nelson, W.B., Smuder, A.J., Hudson, M.B., et al. Cross-talk between the calpain and caspase-3 proteolytic systems in the diaphragm during prolonged mechanical ventilation. Crit Care Med 40:6 (2012), 1857–1863.
41. Hussain, S.N., Mofarrahi, M., Sigala, I., et al. Mechanical ventilation-induced diaphragm disuse in humans triggers autophagy. Am J Respir Crit Care Med 182:11 (2010), 1377–1386.
42. Gayan-Ramirez, G., Testelmans, D., Maes, K., et al. Intermittent spontaneous breathing protects the rat diaphragm from mechanical ventilation effects. Crit Care Med 33:12 (2005), 2804–2809.
43. Sassoon, C.S., Zhu, E., Caiozzo, V.J., Assist-control mechanical ventilation attenuates ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 170:6 (2004), 626–632.
44. Thomas, D., Maes, K., Agten, A., et al. Time course of diaphragm function recovery after controlled mechanical ventilation in rats. J Appl Physiol (1985) 115:6 (2013), 775–784.
45. Callahan, L.A., Supinski, G.S., Rapid and complete recovery in ventilator-induced diaphragm weakness—problem solved?. J Appl Physiol (1985) 115:6 (2013), 773–774.
46. Laghi, F., Sassoon, C.S., Weakness in the critically ill: “captain of the men of death” or sign of disease severity?. Am J Respir Crit Care Med 195:1 (2017), 7–9.
47. Supinski, G.S., Alimov, A.P., Wang, L., et al. Calcium-dependent phospholipase A2 modulates infection-induced diaphragm dysfunction. Am J Physiol Lung Cell Mol Physiol 310:10 (2016), L975–L984.
48. Supinski, G.S., Ji, X.Y., Callahan, L.A., p38 mitogen-activated protein kinase modulates endotoxin-induced diaphragm caspase activation. Am J Respir Cell Mol Biol 43:1 (2010), 121–127.
49. Supinski, G.S., Wang, L., Song, X.H., et al. Muscle-specific calpastatin overexpression prevents diaphragm weakness in cecal ligation puncture-induced sepsis. J Appl Physiol (1985) 117:8 (2014), 921–929.
50. 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.
51. Callahan, L.A., Supinski, G.S., Sepsis-induced myopathy. Crit Care Med 37:10 (2009), S354–S367.
52. Supinski, G.S., Alimov, A.P., Wang, L., et al. Neutral sphingomyelinase 2 is required for cytokine-induced skeletal muscle calpain activation. Am J Physiol Lung Cell Mol Physiol 309:6 (2015), L614–L624.
53. Callahan, L.A., Supinski, G.S., Sepsis induces diaphragm electron transport chain dysfunction and protein depletion. Am J Respir Crit Care Med 172:7 (2005), 861–868.
54. Callahan, L.A., Nethery, D., Stofan, D., et al. Free radical-induced contractile protein dysfunction in endotoxin-induced sepsis. Am J Respir Cell Mol Biol 24:2 (2001), 210–217.
55. Sarwal, A., Walker, F.O., Cartwright, M.S., Neuromuscular ultrasound for evaluation of the diaphragm. Muscle Nerve 47:3 (2013), 319–329.
56. Gerscovich, E.O., Cronan, M., McGahan, J.P., et al. Ultrasonographic evaluation of diaphragmatic motion. J Ultrasound Med 20:6 (2001), 597–604.
57. Zambon, M., Greco, M., Bocchino, S., et al. Assessment of diaphragmatic dysfunction in the critically ill patient with ultrasound: a systematic review. Intensive Care Med 43:1 (2017), 29–38.
58. Umbrello, M., Formenti, P., Ultrasonographic assessment of diaphragm function in critically ill subjects. Respir Care 61:4 (2016), 542–555.
59. Umbrello, M., Formenti, P., Longhi, D., et al. Diaphragm ultrasound as indicator of respiratory effort in critically ill patients undergoing assisted mechanical ventilation: a pilot clinical study. Crit Care, 19, 2015, 161.
60. Matamis, D., Soilemezi, E., Tsagourias, M., et al. Sonographic evaluation of the diaphragm in critically ill patients. Technique and clinical applications. Intensive Care Med 39:5 (2013), 801–810.
61. Boussuges, A., Gole, Y., Blanc, P., Diaphragmatic motion studied by m-mode ultrasonography: methods, reproducibility, and normal values. Chest 135:2 (2009), 391–400.
62. Cohn, D., Benditt, J.O., Eveloff, S., et al. Diaphragm thickening during inspiration. J Appl Physiol (1985) 83:1 (1997), 291–296.
63. 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.
64. 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, 41(4), 2015, 734.
65. Sarwal, A., Parry, S.M., Berry, M.J., et al. Interobserver reliability of quantitative muscle sonographic analysis in the critically ill population. J Ultrasound Med 34:7 (2015), 1191–1200.
66. Zambon, M., Beccaria, P., Matsuno, J., et al. Mechanical ventilation and diaphragmatic atrophy in critically ill patients: an ultrasound study. Crit Care Med 44 (2016), 1347–1352.
67. Blumhof, S., Wheeler, D., Thomas, K., et al. Change in diaphragmatic thickness during the respiratory cycle predicts extubation success at various levels of pressure support ventilation. Lung 194:4 (2016), 519–525.
68. Multz, A.S., Aldrich, T.K., Prezant, D.J., et al. Maximal inspiratory pressure is not a reliable test of inspiratory muscle strength in mechanically ventilated patients. Am Rev Respir Dis 142:3 (1990), 529–532.
69. Mills, G.H., Kyroussis, D., Hamnegard, C.H., et al. Cervical magnetic stimulation of the phrenic nerves in bilateral diaphragm paralysis. Am J Respir Crit Care Med 155:5 (1997), 1565–1569.
70. Mier, A., Brophy, C., Moxham, J., et al. Twitch pressures in the assessment of diaphragm weakness. Thorax 44:12 (1989), 990–996.
71. Demoule, A., Morelot-Panzini, C., Prodanovic, H., et al. Identification of prolonged phrenic nerve conduction time in the ICU: magnetic versus electrical stimulation. Intensive Care Med 37:12 (2011), 1962–1968.
72. Supinski, G.S., Callahan, L.A., Beta-hydroxy-beta-methylbutyrate (HMB) prevents sepsis-induced diaphragm dysfunction in mice. Respir Physiol Neurobiol 196 (2014), 63–68.
73. Wilkinson, D.J., Hossain, T., Hill, D.S., et al. Effects of leucine and its metabolite beta-hydroxy-beta-methylbutyrate on human skeletal muscle protein metabolism. J Physiol 591:11 (2013), 2911–2923.
74. Supinski, G.S., Vanags, J., Callahan, L.A., Eicosapentaenoic acid preserves diaphragm force generation following endotoxin administration. Crit Care, 14(2), 2010, R35.
75. Laufenberg, L.J., Kazi, A.A., Lang, C.H., Salutary effect of aurintricarboxylic acid on endotoxin- and sepsis-induced changes in muscle protein synthesis and inflammation. Shock 41:5 (2014), 420–428.
76. Aslan, G.K., Huseyinsinoglu, B.E., Oflazer, P., et al. Inspiratory muscle training in late-onset Pompe disease: the effects on pulmonary function tests, quality of life, and sleep quality. Lung 194:4 (2016), 555–561.
77. Martin, A.D., Smith, B.K., Davenport, P.D., et al. Inspiratory muscle strength training improves weaning outcome in failure to wean patients: a randomized trial. Crit Care, 15(2), 2011, R84.
78. 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.
79. 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.
80. 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 (2017), e691–e694.
81. Kaufman, M.R., Elkwood, A.I., Colicchio, A.R., et al. Functional restoration of diaphragmatic paralysis: an evaluation of phrenic nerve reconstruction. Ann Thorac Surg 97:1 (2014), 260–266.
82. Podgaetz, E., Garza-Castillon, R. Jr., Andrade, R.S., Best approach and benefit of plication for paralyzed diaphragm. Thorac Surg Clin 26:3 (2016), 333–346.
83. Kwak, T., Lazzaro, R., Pournik, H., et al. Robotic thoracoscopic plication for symptomatic diaphragm paralysis. J Robot Surg 6:4 (2012), 345–348.
84. Le Pimpec-Barthes, F., Legras, A., Arame, A., et al. Diaphragm pacing: the state of the art. J Thorac Dis 8:suppl 4 (2016), S376–S386.