Intensive Care Medicine

, Volume 43, Issue 10, pp 1441–1452 | Cite as

Critical illness-associated diaphragm weakness

  • Martin DresEmail author
  • Ewan C. Goligher
  • Leo M. A. Heunks
  • Laurent J. Brochard


Diaphragm weakness is highly prevalent in critically ill patients. It may exist prior to ICU admission and may precipitate the need for mechanical ventilation but it also frequently develops during the ICU stay. Several risk factors for diaphragm weakness have been identified; among them sepsis and mechanical ventilation play central roles. We employ the term critical illness-associated diaphragm weakness to refer to the collective effects of all mechanisms of diaphragm injury and weakness occurring in critically ill patients. Critical illness-associated diaphragm weakness is consistently associated with poor outcomes including increased ICU mortality, difficult weaning, and prolonged duration of mechanical ventilation. Bedside techniques for assessing the respiratory muscles promise to improve detection of diaphragm weakness and enable preventive or curative strategies. Inspiratory muscle training and pharmacological interventions may improve respiratory muscle function but data on clinical outcomes remain limited.


Diaphragm dysfunction Respiratory muscle weakness Critically ill patients Diaphragm atrophy 



This work was supported by the Department of Critical Care Medicine, St. Michael’s Hospital, Toronto, Canada. LB holds the Keenan Chair in Acute Respiratory Failure and Critical Care Medicine.

Compliance with ethical standards

Conflicts of interest

MD gave lectures for Pulsion Medical Systems. LB’s research laboratory received research grants and/or equipment from Covidien, General Electric, Fisher Paykel, Maquet (with St. Michael’s Hospital), and Philips. LH received speakers fee from Maquet Critical Care and Orion Pharma. His lab received research grants from Orion Pharma and Liberate Medical. EG declares no conflict of interest.


MD was supported by the French Intensive Care Society, the Short-Term Fellowship Program of the European Respiratory Society, the Bernhard Dräger Award for advanced treatment of ARF of the European Society of Intensive Care Medicine, the Assistance Publique—Hôpitaux de Paris, and the Fondation pour la Recherche Médicale (FDM 20150734498).


  1. 1.
    Laghi F, Cattapan SE, Jubran A et al (2003) Is weaning failure caused by low-frequency fatigue of the diaphragm? Am J Respir Crit Care Med 167:120–127. doi: 10.1164/rccm.200210-1246OC CrossRefPubMedGoogle Scholar
  2. 2.
    Demoule A, Jung B, Prodanovic H et al (2013) Diaphragm dysfunction on admission to the intensive care unit. Prevalence, risk factors, and prognostic impact—a prospective study. Am J Respir Crit Care Med 188:213–219. doi: 10.1164/rccm.201209-1668OC CrossRefPubMedGoogle Scholar
  3. 3.
    Jung B, Moury PH, Mahul M et al (2016) Diaphragmatic dysfunction in patients with ICU-acquired weakness and its impact on extubation failure. Intensive Care Med 42:853–861. doi: 10.1007/s00134-015-4125-2 CrossRefPubMedGoogle Scholar
  4. 4.
    Jaber S, Petrof BJ, Jung B et al (2011) Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med 183:364–371. doi: 10.1164/rccm.201004-0670OC CrossRefPubMedGoogle Scholar
  5. 5.
    Dres M, Dubé B-P, Mayaux J et al (2017) 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 195:57–66. doi: 10.1164/rccm.201602-0367OC CrossRefPubMedGoogle Scholar
  6. 6.
    Vassilakopoulos T, Petrof BJ (2004) Ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 169:336–341. doi: 10.1164/rccm.200304-489CP CrossRefPubMedGoogle Scholar
  7. 7.
    Gauthier AP, Verbanck S, Estenne M et al (1994) Three-dimensional reconstruction of the in vivo human diaphragm shape at different lung volumes. J Appl Physiol (1985) 76:495–506Google Scholar
  8. 8.
    American Thoracic Society/European Respiratory Society (2002) ATS/ERS statement on respiratory muscle testing. Am J Respir Crit Care Med 166:518–624. doi: 10.1164/rccm.166.4.518 CrossRefGoogle Scholar
  9. 9.
    Watson AC, Hughes PD, Louise Harris M 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 29:1325–1331CrossRefPubMedGoogle Scholar
  10. 10.
    Bellani G, Mauri T, Coppadoro A et al (2013) Estimation of patient’s inspiratory effort from the electrical activity of the diaphragm. Crit Care Med. doi: 10.1097/CCM.0b013e31827caba0 Google Scholar
  11. 11.
    Dres M, Schmidt M, Ferre A et al (2012) Diaphragm electromyographic activity as a predictor of weaning failure. Intensive Care Med 38:2017–2025. doi: 10.1007/s00134-012-2700-3 CrossRefPubMedGoogle Scholar
  12. 12.
    Ueki J, De Bruin PF, Pride NB (1995) In vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax 50:1157–1161CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Goligher EC, Laghi F, Detsky ME et al (2015) Measuring diaphragm thickness with ultrasound in mechanically ventilated patients: feasibility, reproducibility and validity. Intensive Care Med 41:642–649. doi: 10.1007/s00134-015-3687-3 CrossRefPubMedGoogle Scholar
  14. 14.
    Vivier E, Mekontso Dessap A, Dimassi S et al (2012) Diaphragm ultrasonography to estimate the work of breathing during non-invasive ventilation. Intensive Care Med 38:796–803. doi: 10.1007/s00134-012-2547-7 CrossRefPubMedGoogle Scholar
  15. 15.
    Gottesman E, McCool FD (1997) Ultrasound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med 155:1570–1574. doi: 10.1164/ajrccm.155.5.9154859 CrossRefPubMedGoogle Scholar
  16. 16.
    Dubé B-P, Dres M, Mayaux J et al (2017) Ultrasound evaluation of diaphragm function in mechanically ventilated patients: comparison to phrenic stimulation and prognostic implications. Thorax. doi: 10.1136/thoraxjnl-2016-209459 PubMedGoogle Scholar
  17. 17.
    Kim WY, Suh HJ, Hong S-B et al (2011) Diaphragm dysfunction assessed by ultrasonography: influence on weaning from mechanical ventilation. Crit Care Med 39:2627–2630. doi: 10.1097/CCM.0b013e3182266408 CrossRefPubMedGoogle Scholar
  18. 18.
    Hamnegåard CH, Wragg S, Kyroussis D et al (1995) Mouth pressure in response to magnetic stimulation of the phrenic nerves. Thorax 50:620–624CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Supinski GS, Callahan LA (2013) Diaphragm weakness in mechanically ventilated critically ill patients. Crit Care 17:R120. doi: 10.1186/cc12792 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Jiang J-R, Tsai T-H, Jerng J-S et al (2004) Ultrasonographic evaluation of liver/spleen movements and extubation outcome. Chest 126:179–185. doi: 10.1378/chest.126.1.179 CrossRefPubMedGoogle Scholar
  21. 21.
    Latronico N, Bolton CF (2011) Critical illness polyneuropathy and myopathy: a major cause of muscle weakness and paralysis. Lancet Neurol 10:931–941. doi: 10.1016/S1474-4422(11)70178-8 CrossRefPubMedGoogle Scholar
  22. 22.
    Fan E, Cheek F, Chlan L et al (2014) An official American Thoracic Society clinical practice guideline: the diagnosis of intensive care unit-acquired weakness in adults. Am J Respir Crit Care Med 190:1437–1446. doi: 10.1164/rccm.201411-2011ST CrossRefPubMedGoogle Scholar
  23. 23.
    Latronico N, Herridge M, Hopkins RO et al (2017) The ICM research agenda on intensive care unit-acquired weakness. Intensive Care Med. doi: 10.1007/s00134-017-4757-5 PubMedGoogle Scholar
  24. 24.
    Puthucheary ZA, Rawal J, McPhail M et al (2013) Acute skeletal muscle wasting in critical illness. JAMA 310:1591–1600. doi: 10.1001/jama.2013.278481 CrossRefPubMedGoogle Scholar
  25. 25.
    De Jonghe B, Sharshar T, Lefaucheur J-P et al (2002) Paresis acquired in the intensive care unit: a prospective multicenter study. JAMA 288:2859–2867CrossRefPubMedGoogle Scholar
  26. 26.
    Polla B, D’Antona G, Bottinelli R, Reggiani C (2004) Respiratory muscle fibres: specialisation and plasticity. Thorax 59:808–817. doi: 10.1136/thx.2003.009894 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Mrozek S, Jung B, Petrof BJ et al (2012) Rapid onset of specific diaphragm weakness in a healthy murine model of ventilator-induced diaphragmatic dysfunction. Anesthesiology 117:560–567. doi: 10.1097/ALN.0b013e318261e7f8 CrossRefPubMedGoogle Scholar
  28. 28.
    Levine S, Nguyen T, Taylor N et al (2008) Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 358:1327–1335. doi: 10.1056/NEJMoa070447 CrossRefPubMedGoogle Scholar
  29. 29.
    Laghi F, Tobin MJ (2003) Disorders of the respiratory muscles. Am J Respir Crit Care Med 168:10–48. doi: 10.1164/rccm.2206020 CrossRefPubMedGoogle Scholar
  30. 30.
    Friedrich O, Reid MB, Van den Berghe G et al (2015) The sick and the weak: neuropathies/myopathies in the critically ill. Physiol Rev 95:1025–1109. doi: 10.1152/physrev.00028.2014 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    De Jong A, Carreira S, Na N et al (2017) Diaphragmatic function is enhanced in fatty and diabetic fatty rats. PLoS One 12:e0174043. doi: 10.1371/journal.pone.0174043 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Juan G, Calverley P, Talamo C et al (1984) Effect of carbon dioxide on diaphragmatic function in human beings. N Engl J Med 310:874–879. doi: 10.1056/NEJM198404053101402 CrossRefPubMedGoogle Scholar
  33. 33.
    Rafferty GF, Lou Harris M, Polkey MI et al (1999) Effect of hypercapnia on maximal voluntary ventilation and diaphragm fatigue in normal humans. Am J Respir Crit Care Med 160:1567–1571. doi: 10.1164/ajrccm.160.5.9801114 CrossRefPubMedGoogle Scholar
  34. 34.
    Mador MJ, Wendel T, Kufel TJ (1997) Effect of acute hypercapnia on diaphragmatic and limb muscle contractility. Am J Respir Crit Care Med 155:1590–1595. doi: 10.1164/ajrccm.155.5.9154862 CrossRefPubMedGoogle Scholar
  35. 35.
    Michelet P, Carreira S, Demoule A et al (2015) Effects of acute respiratory and metabolic acidosis on diaphragm muscle obtained from rats. Anesthesiology 122:876–883. doi: 10.1097/ALN.0000000000000574 CrossRefPubMedGoogle Scholar
  36. 36.
    Aubier M, Trippenbach T, Roussos C (1981) Respiratory muscle fatigue during cardiogenic shock. J Appl Physiol 51:499–508PubMedGoogle Scholar
  37. 37.
    Aubier M, Viires N, Syllie G et al (1982) Respiratory muscle contribution to lactic acidosis in low cardiac output. Am Rev Respir Dis 126:648–652. doi: 10.1164/arrd.1982.126.4.648 PubMedGoogle Scholar
  38. 38.
    Viires N, Sillye G, Aubier M et al (1983) Regional blood flow distribution in dog during induced hypotension and low cardiac output. Spontaneous breathing versus artificial ventilation. J Clin Invest 72:935–947. doi: 10.1172/JCI111065 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Hussain SN, Simkus G, Roussos C (1985) Respiratory muscle fatigue: a cause of ventilatory failure in septic shock. J Appl Physiol (1985) 58:2033–2040Google Scholar
  40. 40.
    Leon A, Boczkowski J, Dureuil B et al (1992) Effects of endotoxic shock on diaphragmatic function in mechanically ventilated rats. J Appl Physiol (1985) 72:1466–1472Google Scholar
  41. 41.
    Boczkowski J, Dureuil B, Branger C et al (1988) Effects of sepsis on diaphragmatic function in rats. Am Rev Respir Dis 138:260–265. doi: 10.1164/ajrccm/138.2.260 CrossRefPubMedGoogle Scholar
  42. 42.
    Lanone S, Taillé C, Boczkowski J, Aubier M (2005) Diaphragmatic fatigue during sepsis and septic shock. Intensive Care Med 31:1611–1617. doi: 10.1007/s00134-005-2748-4 CrossRefPubMedGoogle Scholar
  43. 43.
    Shindoh C, Hida W, Ohkawara Y et al (1995) TNF-alpha mRNA expression in diaphragm muscle after endotoxin administration. Am J Respir Crit Care Med 152:1690–1696. doi: 10.1164/ajrccm.152.5.7582314 CrossRefPubMedGoogle Scholar
  44. 44.
    Ebihara S, Hussain SNA, Danialou G et al (2002) Mechanical ventilation protects against diaphragm injury in sepsis: interaction of oxidative and mechanical stresses. Am J Respir Crit Care Med 165:221–228. doi: 10.1164/ajrccm.165.2.2108041 CrossRefPubMedGoogle Scholar
  45. 45.
    Maes K, Stamiris A, Thomas D et al (2014) Effects of controlled mechanical ventilation on sepsis-induced diaphragm dysfunction in rats. Crit Care Med 42:e772–e782. doi: 10.1097/CCM.0000000000000685 CrossRefPubMedGoogle Scholar
  46. 46.
    Jung B, Nougaret S, Conseil M et al (2014) Sepsis is associated with a preferential diaphragmatic atrophy: a critically ill patient study using tridimensional computed tomography. Anesthesiology 120:1182–1191. doi: 10.1097/ALN.0000000000000201 CrossRefPubMedGoogle Scholar
  47. 47.
    Dureuil B, Viirès N, Cantineau JP et al (1986) Diaphragmatic contractility after upper abdominal surgery. J Appl Physiol (1985) 61:1775–1780Google Scholar
  48. 48.
    Diehl JL, Lofaso F, Deleuze P et al (1994) Clinically relevant diaphragmatic dysfunction after cardiac operations. J Thorac Cardiovasc Surg 107:487–498PubMedGoogle Scholar
  49. 49.
    Simonneau G, Vivien A, Sartene R et al (1983) Diaphragm dysfunction induced by upper abdominal surgery. Role of postoperative pain. Am Rev Respir Dis 128:899–903PubMedGoogle Scholar
  50. 50.
    Lerolle N, Guérot E, Dimassi S et al (2009) Ultrasonographic diagnostic criterion for severe diaphragmatic dysfunction after cardiac surgery. Chest 135:401–407. doi: 10.1378/chest.08-1531 CrossRefPubMedGoogle Scholar
  51. 51.
    Shaw IC, Mills GH, Turnbull D (2002) The effect of propofol on airway pressures generated by magnetic stimulation of the phrenic nerves. Intensive Care Med 28:891–897. doi: 10.1007/s00134-002-1347-x CrossRefPubMedGoogle Scholar
  52. 52.
    Hermans G, Agten A, Testelmans D et al (2010) Increased duration of mechanical ventilation is associated with decreased diaphragmatic force: a prospective observational study. Crit Care 14:R127. doi: 10.1186/cc9094 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Bouhemad B, Langeron O, Orliaguet G et al (2002) Effects of halothane and isoflurane on the contraction, relaxation and energetics of rat diaphragmatic muscle. Br J Anaesth 89:479–485CrossRefPubMedGoogle Scholar
  54. 54.
    Veber B, Dureuil B, Viires N et al (1989) Effects of isoflurane on contractile properties of diaphragm. Anesthesiology 70:684–688CrossRefPubMedGoogle Scholar
  55. 55.
    Kress JP, Hall JB (2014) ICU-acquired weakness and recovery from critical illness. N Engl J Med 371:287–288. doi: 10.1056/NEJMc1406274 CrossRefPubMedGoogle Scholar
  56. 56.
    Sassoon CS, Caiozzo VJ (2009) Bench-to-bedside review: diaphragm muscle function in disuse and acute high-dose corticosteroid treatment. Crit Care 13:221. doi: 10.1186/cc7971 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Testelmans D, Maes K, Wouters P et al (2006) Rocuronium exacerbates mechanical ventilation-induced diaphragm dysfunction in rats. Crit Care Med 34:3018–3023. doi: 10.1097/01.CCM.0000245783.28478.AD CrossRefPubMedGoogle Scholar
  58. 58.
    Testelmans D, Maes K, Wouters P et al (2007) Infusions of rocuronium and cisatracurium exert different effects on rat diaphragm function. Intensive Care Med 33:872–879. doi: 10.1007/s00134-007-0584-4 CrossRefPubMedGoogle Scholar
  59. 59.
    Papazian L, Forel J-M, Gacouin A et al (2010) Neuromuscular blockers in early acute respiratory distress syndrome. N Engl J Med 363:1107–1116. doi: 10.1056/NEJMoa1005372 CrossRefPubMedGoogle Scholar
  60. 60.
    Le Bourdelles G, Viires N, Boczkowski J et al (1994) Effects of mechanical ventilation on diaphragmatic contractile properties in rats. Am J Respir Crit Care Med 149:1539–1544. doi: 10.1164/ajrccm.149.6.8004310 CrossRefPubMedGoogle Scholar
  61. 61.
    Sassoon CS, Caiozzo VJ, Manka A, Sieck GC (2002) Altered diaphragm contractile properties with controlled mechanical ventilation. J Appl Physiol 92:2585–2595. doi: 10.1152/japplphysiol.01213.2001 CrossRefPubMedGoogle Scholar
  62. 62.
    Powers SK, Shanely RA, Coombes JS et al (2002) Mechanical ventilation results in progressive contractile dysfunction in the diaphragm. J Appl Physiol 92:1851–1858. doi: 10.1152/japplphysiol.00881.2001 CrossRefPubMedGoogle Scholar
  63. 63.
    Anzueto A, Peters JI, Tobin MJ et al (1997) Effects of prolonged controlled mechanical ventilation on diaphragmatic function in healthy adult baboons. Crit Care Med 25:1187–1190CrossRefPubMedGoogle Scholar
  64. 64.
    Jung B, Constantin J-M, Rossel N et al (2010) Adaptive support ventilation prevents ventilator-induced diaphragmatic dysfunction in piglet: an in vivo and in vitro study. Anesthesiology 112:1435–1443. doi: 10.1097/ALN.0b013e3181d7b036 CrossRefPubMedGoogle Scholar
  65. 65.
    Knisely AS, Leal SM, Singer DB (1988) Abnormalities of diaphragmatic muscle in neonates with ventilated lungs. J Pediatr 113:1074–1077CrossRefPubMedGoogle Scholar
  66. 66.
    Hooijman PE, Beishuizen A, Witt CC et al (2015) Diaphragm muscle fiber weakness and ubiquitin–proteasome activation in critically ill patients. Am J Respir Crit Care Med 191:1126–1138. doi: 10.1164/rccm.201412-2214OC CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Picard M, Jung B, Liang F et al (2012) Mitochondrial dysfunction and lipid accumulation in the human diaphragm during mechanical ventilation. Am J Respir Crit Care Med 186:1140–1149. doi: 10.1164/rccm.201206-0982OC CrossRefPubMedGoogle Scholar
  68. 68.
    van den Berg M, Hooijman PE, Beishuizen A et al (2017) Diaphragm Atrophy and weakness in the absence of mitochondrial dysfunction in the critically ill. Am J Respir Crit Care Med. doi: 10.1164/rccm.201703-0501OC Google Scholar
  69. 69.
    Sieck GC, Mantilla CB (2013) CrossTalk opposing view: the diaphragm muscle does not atrophy as a result of inactivity. J Physiol 591:5259–5262. doi: 10.1113/jphysiol.2013.254698 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Goligher EC, Fan E, Herridge MS et al (2015) Evolution of diaphragm thickness during mechanical ventilation: impact of inspiratory effort. Am J Respir Crit Care Med. doi: 10.1164/rccm.201503-0620OC Google Scholar
  71. 71.
    Grosu HB, Lee YI, Lee J et al (2012) Diaphragm muscle thinning in patients who are mechanically ventilated. Chest 142:1455–1460. doi: 10.1378/chest.11-1638 CrossRefPubMedGoogle Scholar
  72. 72.
    Schepens T, Verbrugghe W, Dams K et al (2015) The course of diaphragm atrophy in ventilated patients assessed with ultrasound: a longitudinal cohort study. Crit Care 19:422. doi: 10.1186/s13054-015-1141-0 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Jiang TX, Reid WD, Belcastro A, Road JD (1998) Load dependence of secondary diaphragm inflammation and injury after acute inspiratory loading. Am J Respir Crit Care Med 157:230–236. doi: 10.1164/ajrccm.157.1.9702051 CrossRefPubMedGoogle Scholar
  74. 74.
    Reid WD, Huang J, Bryson S et al (1994) Diaphragm injury and myofibrillar structure induced by resistive loading. J Appl Physiol (1985) 76:176–184Google Scholar
  75. 75.
    Laghi F, D’Alfonso N, Tobin MJ (1995) Pattern of recovery from diaphragmatic fatigue over 24 hours. J Appl Physiol (1985) 79:539–546Google Scholar
  76. 76.
    Orozco-Levi M, Lloreta J, Minguella J et al (2001) Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164:1734–1739. doi: 10.1164/ajrccm.164.9.2011150 CrossRefPubMedGoogle Scholar
  77. 77.
    Gea J, Zhu E, Gáldiz JB et al (2009) Functional consequences of eccentric contractions of the diaphragm. Arch Bronconeumol 45:68–74. doi: 10.1016/j.arbres.2008.04.003 PubMedGoogle Scholar
  78. 78.
    Pellegrini M, Hedenstierna G, Roneus A et al (2016) The diaphragm acts as a brake during expiration to prevent lung collapse. Am J Respir Crit Care Med. doi: 10.1164/rccm.201605-0992OC Google Scholar
  79. 79.
    Jaber S, Jung B, Sebbane M et al (2008) Alteration of the piglet diaphragm contractility in vivo and its recovery after acute hypercapnia. Anesthesiology 108:651–658. doi: 10.1097/ALN.0b013e31816725a6 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Jung B, Sebbane M, Le Goff C et al (2013) Moderate and prolonged hypercapnic acidosis may protect against ventilator-induced diaphragmatic dysfunction in healthy piglet: an in vivo study. Crit Care 17:R15. doi: 10.1186/cc12486 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Schellekens W-JM, van Hees HWH, Kox M et al (2014) Hypercapnia attenuates ventilator-induced diaphragm atrophy and modulates dysfunction. Crit Care 18:R28. doi: 10.1186/cc13719 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Demoule A, Molinari N, Jung B et al (2016) Patterns of diaphragm function in critically ill patients receiving prolonged mechanical ventilation: a prospective longitudinal study. Ann Intensive Care 6:75. doi: 10.1186/s13613-016-0179-8 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Adler D, Dupuis-Lozeron E, Richard J-C et al (2014) Does inspiratory muscle dysfunction predict readmission after intensive care unit discharge? Am J Respir Crit Care Med 190:347–350. doi: 10.1164/rccm.201404-0655LE CrossRefPubMedGoogle Scholar
  84. 84.
    Medrinal C, Prieur G, Frenoy É et al (2016) Respiratory weakness after mechanical ventilation is associated with one-year mortality—a prospective study. Crit Care 20:231. doi: 10.1186/s13054-016-1418-y CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Thille AW, Cabello B, Galia F et al (2008) Reduction of patient-ventilator asynchrony by reducing tidal volume during pressure-support ventilation. Intensive Care Med 34:1477–1486. doi: 10.1007/s00134-008-1121-9 CrossRefPubMedGoogle Scholar
  86. 86.
    Yoshida T, Torsani V, Gomes S et al (2013) Spontaneous effort causes occult pendelluft during mechanical ventilation. Am J Respir Crit Care Med 188:1420–1427. doi: 10.1164/rccm.201303-0539OC CrossRefPubMedGoogle Scholar
  87. 87.
    Doorduin J, Nollet JL, Roesthuis LH et al (2016) Partial neuromuscular blockade during partial ventilatory support in sedated patients with high tidal volumes. Am J Respir Crit Care Med. doi: 10.1164/rccm.201605-1016OC Google Scholar
  88. 88.
    Iotti GA, Braschi A (2001) Closed-loop support of ventilatory workload: the P0.1 controller. Respir Care Clin N Am 7:441–464, ixGoogle Scholar
  89. 89.
    Carteaux G, Mancebo J, Mercat A et al (2013) Bedside adjustment of proportional assist ventilation to target a predefined range of respiratory effort. Crit Care Med 41:2125–2132. doi: 10.1097/CCM.0b013e31828a42e5 CrossRefPubMedGoogle Scholar
  90. 90.
    Reynolds SC, Meyyappan R, Thakkar V et al (2017) Mitigation of ventilator-induced diaphragm atrophy by transvenous phrenic nerve stimulation. Am J Respir Crit Care Med 195:339–348. doi: 10.1164/rccm.201502-0363OC PubMedGoogle Scholar
  91. 91.
    Martin AD, Joseph A-M, Beaver TM et al (2014) Effect of intermittent phrenic nerve stimulation during cardiothoracic surgery on mitochondrial respiration in the human diaphragm. Crit Care Med 42:e152–e156. doi: 10.1097/CCM.0b013e3182a63fdf CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Schellekens W-JM, van Hees HWH, Doorduin J et al (2016) Strategies to optimize respiratory muscle function in ICU patients. Crit Care 20:103. doi: 10.1186/s13054-016-1280-y CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Aubier M, Murciano D, Lecocguic Y et al (1985) Effect of hypophosphatemia on diaphragmatic contractility in patients with acute respiratory failure. N Engl J Med 313:420–424. doi: 10.1056/NEJM198508153130705 CrossRefPubMedGoogle Scholar
  94. 94.
    Alsumrain MH, Jawad SA, Imran NB et al (2010) Association of hypophosphatemia with failure-to-wean from mechanical ventilation. Ann Clin Lab Sci 40:144–148PubMedGoogle Scholar
  95. 95.
    Aubier M (1987) Effect of theophylline on diaphragmatic muscle function. Chest 92:27S–31SCrossRefPubMedGoogle Scholar
  96. 96.
    Doorduin J, Sinderby CA, Beck J et al (2012) The calcium sensitizer levosimendan improves human diaphragm function. Am J Respir Crit Care Med 185:90–95. doi: 10.1164/rccm.201107-1268OC CrossRefPubMedGoogle Scholar
  97. 97.
    Kim W-Y, Park SH, Kim WY et al (2016) Effect of theophylline on ventilator-induced diaphragmatic dysfunction. J Crit Care 33:145–150. doi: 10.1016/j.jcrc.2016.01.007 CrossRefPubMedGoogle Scholar
  98. 98.
    Martin AD, Smith BK, Davenport PD et al (2011) Inspiratory muscle strength training improves weaning outcome in failure to wean patients: a randomized trial. Crit Care 15:R84. doi: 10.1186/cc10081 CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    DiNino E, Gartman EJ, Sethi JM, McCool FD (2014) Diaphragm ultrasound as a predictor of successful extubation from mechanical ventilation. Thorax 69(5):423–427CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany and ESICM 2017

Authors and Affiliations

  • Martin Dres
    • 1
    • 2
    • 3
    Email author
  • Ewan C. Goligher
    • 4
    • 5
  • Leo M. A. Heunks
    • 6
  • Laurent J. Brochard
    • 3
    • 5
  1. 1.Neurophysiologie Respiratoire Expérimentale et CliniqueSorbonne Universités, UPMC Université Paris 06, INSERM, UMRS_1158ParisFrance
  2. 2.Service de Pneumologie et Réanimation Médicale, Groupe Hospitalier Pitié-Salpêtrière-Charles FoixLa Pitié Salpêtrière HospitalParis Cedex 13France
  3. 3.Keenan Research Centre for Biomedical Science, Li Ka Shing Knowledge InstituteSt. Michael’s HospitalTorontoCanada
  4. 4.Department of Medicine, Division of RespirologyUniversity Health Network and Sinai Health SystemTorontoCanada
  5. 5.Interdepartmental Division of Critical Care MedicineUniversity of TorontoTorontoCanada
  6. 6.Department of Intensive Care MedicineVU University Medical Centre AmsterdamAmsterdamThe Netherlands

Personalised recommendations