Assisted mechanical ventilation promotes recovery of diaphragmatic thickness in critically ill patients: a prospective observational study
Alice Grassi, Daniela Ferlicca, Ermes Lupieri, Serena Calcinati, Silvia Francesconi, Vittoria Sala, Valentina Ormas, Elena Chiodaroli, Chiara Abbruzzese, Francesco Curto, Andrea Sanna, Massimo Zambon, Roberto Fumagalli, Giuseppe Foti, Giacomo Bellani, Alice Grassi, Daniela Ferlicca, Ermes Lupieri, Serena Calcinati, Silvia Francesconi, Vittoria Sala, Valentina Ormas, Elena Chiodaroli, Chiara Abbruzzese, Francesco Curto, Andrea Sanna, Massimo Zambon, Roberto Fumagalli, Giuseppe Foti, Giacomo Bellani
Abstract
Background: Diaphragm atrophy and dysfunction are consequences of mechanical ventilation and are determinants of clinical outcomes. We hypothesize that partial preservation of diaphragm function, such as during assisted modes of ventilation, will restore diaphragm thickness. We also aim to correlate the changes in diaphragm thickness and function to outcomes and clinical factors.
Methods: This is a prospective, multicentre, observational study. Patients mechanically ventilated for more than 48 h in controlled mode and eventually switched to assisted ventilation were enrolled. Diaphragm ultrasound and clinical data collection were performed every 48 h until discharge or death. A threshold of 10% was used to define thinning during controlled and recovery of thickness during assisted ventilation. Patients were also classified based on the level of diaphragm activity during assisted ventilation. We evaluated the association between changes in diaphragm thickness and activity and clinical outcomes and data, such as ventilation parameters.
Results: Sixty-two patients ventilated in controlled mode and then switched to the assisted mode of ventilation were enrolled. Diaphragm thickness significantly decreased during controlled ventilation (1.84 ± 0.44 to 1.49 ± 0.37 mm, p < 0.001) and was partially restored during assisted ventilation (1.49 ± 0.37 to 1.75 ± 0.43 mm, p < 0.001). A diaphragm thinning of more than 10% was associated with longer duration of controlled ventilation (10 [5, 15] versus 5 [4, 8.5] days, p = 0.004) and higher PEEP levels (12.6 ± 4 versus 10.4 ± 4 cmH2O, p = 0.034). An increase in diaphragm thickness of more than 10% during assisted ventilation was not associated with any clinical outcome but with lower respiratory rate (16.7 ± 3.2 versus 19.2 ± 4 bpm, p = 0.019) and Rapid Shallow Breathing Index (37 ± 11 versus 44 ± 13, p = 0.029) and with higher Pressure Muscle Index (2 [0.5, 3] versus 0.4 [0, 1.9], p = 0.024). Change in diaphragm thickness was not related to diaphragm function expressed as diaphragm thickening fraction.
Conclusion: Mode of ventilation affects diaphragm thickness, and preservation of diaphragmatic contraction, as during assisted modes, can partially reverse the muscle atrophy process. Avoiding a strenuous inspiratory work, as measured by Rapid Shallow Breathing Index and Pressure Muscle Index, may help diaphragm thickness restoration.
Keywords: Assisted mechanical ventilation; Diaphragm thickness; Diaphragm ultrasound.
Conflict of interest statement
The authors declare that they have no competing interests.
Figures
References
- Goligher EC, Dres M, Fan E, Rubenfeld GD, Scales DC, Herridge MS, et al. Mechanical ventilation-induced diaphragm atrophy strongly impacts clinical outcomes. Am J Respir Crit Care Med. 2017;197(2):204. doi: 10.1164/rccm.201703-0536OC.
- Goligher EC, Fan E, Herridge MS, Murray A, Vorona S, Brace D, et al. Evolution of diaphragm thickness during mechanical ventilation. Impact of inspiratory effort. Am J Respir Crit Care Med. 2015;192(9):1080. doi: 10.1164/rccm.201503-0620OC.
- Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothenberg P, et al. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med. 2008;358(13):1327. doi: 10.1056/NEJMoa070447.
- Orozco-Levi M, Lloreta J, Minguella J, Serrano S, Broquetas JM, Gea J. Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001;164(9):1734. doi: 10.1164/ajrccm.164.9.2011150.
- Pellegrini M, Hedenstierna G, Roneus A, Segelsjö M, Larsson A, Perchiazzi G. The diaphragm acts as a brake during expiration to prevent lung collapse. Am J Respir Crit Care Med. 2016;195(12):1608. doi: 10.1164/rccm.201605-0992OC.
- Lindqvist J, van den Berg M, van der Pijl R, Hooijman PE, Beishuizen A, Elshof J, et al. Positive end-expiratory pressure ventilation induces longitudinal atrophy in diaphragm fibers. Am J Respir Crit Care Med. 2018;198(4):472. doi: 10.1164/rccm.201709-1917OC.
- Schepens T, Goligher EC. Lung- and diaphragm-protective ventilation in acute respiratory distress syndrome: rationale and challenges. Anesthesiology. 2019;130(4):620. doi: 10.1097/ALN.0000000000002605.
- Schepens T, Dres M, Heunks L, Goligher EC. Diaphragm-protective mechanical ventilation. Curr Opin Crit Care. 2018;25(1):77. doi: 10.1097/MCC.0000000000000578.
- Dres M, Goligher EC, Dubé B-P, Morawiec E, Dangers L, Reuter D, et al. Diaphragm function and weaning from mechanical ventilation: an ultrasound and phrenic nerve stimulation clinical study. Ann Intensive Care. 2018;8(1):53. doi: 10.1186/s13613-018-0401-y.
- Bellani G, Grassi A, Sosio S, Gatti S, Kavanagh BP, Pesenti A, et al. Driving pressure is associated with outcome during assisted ventilation in acute respiratory distress syndrome. Anesthesiology. 2019;131(3):594. doi: 10.1097/ALN.0000000000002846.
- Martin AD, Joseph A-M, Beaver TM, Smith BK, Martin TD, Berg K, et al. Effect of intermittent phrenic nerve stimulation during cardiothoracic surgery on mitochondrial respiration in the human diaphragm. Crit Care Med. 2013;42(2):e152. doi: 10.1097/CCM.0b013e3182a63fdf.
- Ahn B, Beaver T, Martin T, Hess P, Brumback BA, Ahmed S, et al. Phrenic nerve stimulation increases human diaphragm fiber force after cardiothoracic surgery. Am J Respir Crit Care Med. 2014;190(7):837. doi: 10.1164/rccm.201405-0993LE.
- Futier E, Constantin J-M, Combaret L, Mosoni L, Roszyk L, Sapin V, et al. Pressure support ventilation attenuates ventilator-induced protein modifications in the diaphragm. Crit Care. 2008;12(5):R116. doi: 10.1186/cc7010.
- Sassoon CSH, Zhu E, Caiozzo VJ. Assist-control mechanical ventilation attenuates ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med. 2004;170(6):626. doi: 10.1164/rccm.200401-042OC.
- Marin-Corral J, Dot I, Boguña M, Cecchini L, Zapatero A, Gracia MP, et al. Structural differences in the diaphragm of patients following controlled vs assisted and spontaneous mechanical ventilation. Intensive Care Med. 2019;45(4):488. doi: 10.1007/s00134-019-05566-5.
- Arabi YM, Aldawood AS, Al-Dorzi HM, Tamim HM, Haddad SH, Jones G, et al. Permissive underfeeding or standard enteral feeding in high- and low-nutritional-risk critically ill adults. Post hoc analysis of the PermiT Trial. Am J Respir Crit Care Med. 2016;195(5):652. doi: 10.1164/rccm.201605-1012OC.
- Devoto G, Gallo F, Marchello C, Racchi O, Garbarini R, Bonassi S, et al. Prealbumin serum concentrations as a useful tool in the assessment of malnutrition in hospitalized patients. Clin Chem. 2006;52(12):2281. doi: 10.1373/clinchem.2006.080366.
- Bellani G, Grassi A, Sosio S, Foti G. Plateau and driving pressure in the presence of spontaneous breathing. Intensive Care Med. 2018;45(1):97. doi: 10.1007/s00134-018-5311-9.
- Foti G, Cereda M, Banfi G, Pelosi P, Fumagalli R, Pesenti A. End-inspiratory airway occlusion: a method to assess the pressure developed by inspiratory muscles in patients with acute lung injury undergoing pressure support. Am J Respir Crit Care Med. 1997;156(4 Pt 1):1210. doi: 10.1164/ajrccm.156.4.96-02031.
- Yang KL, Tobin MJ. A prospective study of indexes predicting the outcome of trials of weaning from mechanical ventilation. N Engl J Med. 1991;324(21):1445. doi: 10.1056/NEJM199105233242101.
- Telias I, Damiani F, Brochard L. The airway occlusion pressure (P0.1) to monitor respiratory drive during mechanical ventilation: increasing awareness of a not-so-new problem. Intensive Care Med. 2018;44(9):1532. doi: 10.1007/s00134-018-5045-8.
- Goligher EC, Laghi F, Detsky ME, Farias P, Murray A, Brace D, et al. Measuring diaphragm thickness with ultrasound in mechanically ventilated patients: feasibility, reproducibility and validity. Intensive Care Med. 2015;41(4):734. doi: 10.1007/s00134-015-3724-2.
- McCool FD, Benditt JO, Conomos P, Anderson L, Sherman CB, Hoppin FG. Variability of diaphragm structure among healthy individuals. Am J Respir Crit Care Med. 1997;155(4):1323. doi: 10.1164/ajrccm.155.4.9105074.
- Cohen J. Statistical power analysis for the behavioral sciences: (2nd ed.). Mahwah: Lawrence Erlbaum Associates; (1988).
- Schepens T, Verbrugghe W, Dams K, Corthouts B, Parizel PM, Jorens PG. The course of diaphragm atrophy in ventilated patients assessed with ultrasound: a longitudinal cohort study. Crit Care. 2015;19:422.
- Zambon M, Beccaria P, Matsuno J, Gemma M, Frati E, Colombo S, et al. Mechanical ventilation and diaphragmatic atrophy in critically ill patients: an ultrasound study. Crit Care Med. 2016;44(7):1347. doi: 10.1097/CCM.0000000000001657.
- Grosu HB, Lee YI, Lee J, Eden E, Eikermann M, Rose KM. Diaphragm muscle thinning in patients who are mechanically ventilated. Chest. 2013;142(6):1455.
- Jung B, Constantin J-M, Rossel N, Le Goff C, Sebbane M, Coisel Y, et al. Adaptive support ventilation prevents ventilator-induced diaphragmatic dysfunction in piglet: an in vivo and in vitro study. Anesthesiology. 2010;112(6):1435. doi: 10.1097/ALN.0b013e3181d7b036.
- Umbrello M, Formenti P, Longhi D, Galimberti A, Piva I, Pezzi A, et al. Diaphragm ultrasound as indicator of respiratory effort in critically ill patients undergoing assisted mechanical ventilation: a pilot clinical study. Crit Care. 2015;19:161. doi: 10.1186/s13054-015-0894-9.
- DiNino E, Gartman EJ, Sethi JM, McCool FD. Diaphragm ultrasound as a predictor of successful extubation from mechanical ventilation. Thorax. 2013;69(5):423.
- Dres M, Dubé B-P, Mayaux J, Delemazure J, Reuter D, Brochard L, 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. 2016;195(1):57. doi: 10.1164/rccm.201602-0367OC.
- Rittayamai N, Hemvimon S, Chierakul N. The evolution of diaphragm activity and function determined by ultrasound during spontaneous breathing trials. J Crit Care. 2019;51(02):133. doi: 10.1016/j.jcrc.2019.02.016.
- Vivier E, Muller M, Putegnat J-B, Steyer J, Barrau S, Boissier F, et al. Inability of diaphragm ultrasound to predict extubation failure: a multicenter study. Chest. 2019;155(6):1131. doi: 10.1016/j.chest.2019.03.004.
- Gottesman E, McCool FD. Ultrasound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med. 1997;155(5):1570.
- Ferrari G, De Filippi G, Elia F, Panero F, Volpicelli G, Aprà F. Diaphragm ultrasound as a new index of discontinuation from mechanical ventilation. Crit Ultrasound J. 2014;6(1):8. doi: 10.1186/2036-7902-6-8.
- Rezoagli E, Bellani G. How I set up positive end-expiratory pressure: evidence- and physiology-based! Crit Care. 2019;23(1):412. doi: 10.1186/s13054-019-2695-z.
- Morais CCA, Koyama Y, Yoshida T, Plens GM, Gomes S, Lima CAS, et al. High positive end-expiratory pressure renders spontaneous effort noninjurious. Am J Respir Crit Care Med. 2018;197(10):1285. doi: 10.1164/rccm.201706-1244OC.
- Goligher EC, Brochard LJ, Reid WD, Fan E, Saarela O, Slutsky AS, et al. Diaphragmatic myotrauma: a mediator of prolonged ventilation and poor patient outcomes in acute respiratory failure. Lancet Respir Med. 2018;7(1):90. doi: 10.1016/S2213-2600(18)30366-7.
Source: PubMed