Can diaphragmatic ultrasonography performed during the T-tube trial predict weaning failure? The role of diaphragmatic rapid shallow breathing index

Savino Spadaro, Salvatore Grasso, Tommaso Mauri, Francesca Dalla Corte, Valentina Alvisi, Riccardo Ragazzi, Valentina Cricca, Giulia Biondi, Rossella Di Mussi, Elisabetta Marangoni, Carlo Alberto Volta, Savino Spadaro, Salvatore Grasso, Tommaso Mauri, Francesca Dalla Corte, Valentina Alvisi, Riccardo Ragazzi, Valentina Cricca, Giulia Biondi, Rossella Di Mussi, Elisabetta Marangoni, Carlo Alberto Volta

Abstract

Background: The rapid shallow breathing index (RSBI), which is the ratio between respiratory rate (RR) and tidal volume (VT), is one of the most widely used indices to predict weaning outcome. Whereas the diaphragm plays a fundamental role in generating VT, in the case of diaphragmatic dysfunction the inspiratory accessory muscles may contribute. If this occurs during a weaning trial, delayed weaning failure is likely since the accessory muscles are more fatigable than the diaphragm. Hence, we hypothesised that the traditional RSBI could be implemented by substituting VT with the ultrasonographic evaluation of diaphragmatic displacement (DD). We named the new index the diaphragmatic-RSBI (D-RSBI). The aim of this study was to compare the ability of the traditional RSBI and D-RSBI to predict weaning failure in ready-to-wean patients.

Methods: We performed a prospective observational study. During a T-tube spontaneous breathing trial (SBT) we simultaneously evaluated right hemidiaphragm displacement (i.e., DD) by using M-mode ultrasonography as well as the RSBI. Outcome of the weaning attempt, length of mechanical ventilation, length of intensive care unit and hospital stay, and hospital mortality were recorded. Receiver operator characteristic (ROC) curves were used to evaluate the diagnostic accuracy of D-RSBI and RSBI.

Results: We enrolled 51 patients requiring mechanical ventilation for more than 48 h who were ready to perform a SBT. Most of the patients, 34 (66 %), were successfully weaned from mechanical ventilation. When considering the 17 patients that failed the weaning attempt, 11 (64 %) had to be reconnected to the ventilator during the SBT, three (18 %) had to be re-intubated within 48 h of extubation, and three (18 %) required non-invasive ventilation support within 48 h of extubation. The areas under the ROC curves for D-RSBI and RSBI were 0.89 and 0.72, respectively (P = 0.006).

Conclusions: D-RSBI (RR/DD) was more accurate than traditional RSBI (RR/VT) in predicting the weaning outcome.

Trial registration: Our clinical trial was retrospectively registered with ClinicalTrials.gov (identifier: NCT02696018 ). ClinicalTrials.gov processed our record on 25 February 2016.

Keywords: Diaphragmatic displacement; Rapid shallow breathing; Spontaneous breathing trial; Ultrasonography; Weaning.

Figures

Fig. 1
Fig. 1
Time-line of the study protocol. Patients requiring mechanical ventilation for at least 48 h (H) were consecutively included. After 30 min of a T-tube spontaneous breathing trial (SBT), patients breathing patterns were examined. We used a multimodal evaluation combining ultrasound evaluation of diaphragmatic displacement and spirometry. At the end of a 2-h SBT, the treating physician decided to extubate or to reinstitute mechanical ventilation without being aware of the results of the ultrasound exploration of the diaphragm. Weaning success was monitored for a 48-h follow-up period; the reinstitution of mechanical ventilation during or at the end of the SBT, reintubation within 48 h, or the use of non-invasive ventilation (NIV) within 48 h from extubation were registered as a failed weaning attempt
Fig. 2
Fig. 2
M-mode sonography of the diaphragm of a a representative patient with an impaired right diaphragmatic displacement (DD = 6 mm) and b a representative patient with a conserved right hemidiaphragm function (DD = 14.8 mm). DD was measured on the vertical axis of a frozen image from the baseline, at the end of expiration, to the point of maximum height of inspiration
Fig. 3
Fig. 3
Flow chart of the study. MV mechanical ventilation, NIV non-invasive ventilation, SBT spontaneous breathing trial
Fig. 4
Fig. 4
Correlation between diaphragmatic rapid shallow breathing index (D-RSBI) and traditional rapid shallow breathing index (RSBI)
Fig. 5
Fig. 5
Receiver operating characteristic (ROC) curve for diaphragmatic rapid shallow breathing index (D-RSBI) and traditional rapid shallow breathing index (RSBI). The D-RSBI curve is shown in black and the RSBI curve is presented by a grey dashed line

References

    1. El-Khatib MF, Bou-Khalil P. Clinical review: liberation from mechanical ventilation. Crit Care. 2008;12(4):221.
    1. Esteban A, Anzueto A, Frutos F, Alía I, Brochard L, Stewart TE, et al. Mechanical Ventilation International Study Group. Characteristics and outcomes in adult patients receiving mechanical ventilation: a 28-day international study. JAMA. 2002;287(3):345–55.
    1. Thille AW, Harrois A, Schortgen F, Brun-Buisson C, Brochard L. Outcomes of extubation failure in medical intensive care unit patients. Crit Care Med. 2011;39(12):2612–8.
    1. Vassilakopoulos T, Zakynthinos S, Roussos C. Respiratory muscles and weaning failure. Eur Respir J. 1996;9(11):2383–400.
    1. Jubran A, Tobin MJ. Pathophysiologic basis of acute respiratory distress in patients who fail a trial of weaning from mechanical ventilation. Am J Respir Crit Care Med. 1997;155(3):906–15.
    1. Capdevila X, Perrigault PF, Ramonatxo M, Roustan JP, Peray P, d’Athis F, Prefaut C. Changes in breathing pattern and respiratory muscle performance parameters during difficult weaning. Crit Care Med. 1998;26(1):79–87.
    1. Heunks LM, van der Hoeven JG. Clinical review: the ABC of weaning failure—a structured approach. Crit Care. 2010;14:245.
    1. McCool FD, Tzelepis GE. Dysfunction of the diaphragm. N Engl J Med. 2012;366(10):932–42.
    1. Jaber S, Petrof BJ, Jung B, Chanques G, Berthet JP, Rabuel C, et al. Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med. 2011;183(3):364–71.
    1. Laghi F, Tobin MJ. Disorders of the respiratory muscles. Am J Respir Crit Care Med. 2003;168(1):10–48.
    1. Hermans G, Agten A, Testelmans D, Decramer M, Gayan-Ramirez G. Increased duration of mechanical ventilation is associated with decreased diaphragmatic force: a prospective observational study. Crit Care. 2010;14(4):R127.
    1. Doorduin J, van Hees HW, van der Hoeven JG, Heunks LM. Monitoring of the respiratory muscles in the critically ill. Am J Respir Crit Care Med. 2013;187(1):20–7.
    1. Laghi F, Cattapan SE, Jubran A, Parthasarathy S, Warshawsky P, Choi YS, Tobin MJ. Is weaning failure caused by low-frequency fatigue of the diaphragm? Am J Respir Crit Care Med. 2003;167(2):120–7.
    1. Watson AC, Hughes PD, Louise Harris M, Hart N, Ware RJ, Wendon J, 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. 2001;29(7):1325–31.
    1. Matamis D, Soilemezi E, Tsagourias M, Akoumianaki E, Dimassi S, Boroli F, et al. Sonographic evaluation of the diaphragm in critically ill patients. Technique and clinical applications. Intensive Care Med. 2013;39(5):801–10.
    1. Boussuges A, Gole Y, Blanc P. Diaphragmatic motion studied by M-mode ultrasonography. Chest. 2009;135:391–400.
    1. Houston JG, Morris AD, Howie CA, Reid JL, McMillan N. Technical report: quantitative assessment of diaphragmatic movement—a reproducible method using ultrasound. Clin Radiol. 1992;46:405–7.
    1. Cohen E, Mier A, Heywood P, Murphy K, Boultbee J, Guz A. Excursion-volume relation of the right hemidiaphragm measured by ultrasonography and respiratory airflow measurements. Thorax. 1994;49(9):885–9.
    1. Kim WY, Suh HJ, Hong SB, Koh Y, Lim CM. Diaphragm dysfunction assessed by ultrasonography: influence on weaning from mechanical ventilation. Crit Care Med. 2011;39(12):2627–30.
    1. Esteban A, Frutos F, Tobin MJ, Alía I, Solsona JF, Valverdú I, et al. A comparison of four methods of weaning patients from mechanical ventilation. Spanish Lung Failure Collaborative Group. N Engl J Med. 1995;332(6):345–50.
    1. Brochard L, Rauss A, Benito S, Conti G, Mancebo J, Rekik N, et al. Comparison of three methods of gradual withdrawal from ventilatory support during weaning from mechanical ventilation. Am J Respir Crit Care Med. 1994;150(4):896–903.
    1. Alvisi R, Volta CA, Righini ER, Capuzzo M, Ragazzi R, Verri M, et al. Predictors of weaning outcome in chronic obstructive pulmonary disease patients. Eur Respir J. 2000;15(4):656–62.
    1. Tobin MJ, Perez W, Guenther SM, Semmes BJ, Mador MJ, Allen SJ, et al. The pattern of breathing during successful and unsuccessful trials of weaning from mechanical ventilation. Am Rev Respir Dis. 1986;134(6):1111–8.
    1. 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):1445–50.
    1. Meade M, Guyatt G, Cook D, Griffith L, Sinuff T, Kergl C, et al. Predicting success in weaning from mechanical ventilation. Chest. 2001;120(6 Suppl):400S–24S.
    1. Lee KH, Hui KP, Chan TB, Tan WC, Lim TK. Rapid shallow breathing (frequency-tidal volume ratio) did not predict extubation outcome. Chest. 1994;105:540–3.
    1. Huang CT, Yu CJ. Conventional weaning parameters do not predict extubation outcome in intubated subjects requiring prolonged mechanical ventilation. Respir Care. 2013;58:1307–14.
    1. Savi A, Teixeira C, Silva JM, Borges LG, Pereira PA, Pinto KB, Gaúcho Weaning Study Group et al. Weaning predictors do not predict extubation failure in simple-to-wean patients. J Crit Care. 2012;27(2):221.
    1. Yan S, Lichros I, Zakynthinos S, Macklem PT. Effect of diaphragmatic fatigue on control of respiratory muscles and ventilation during CO2 rebreathing. J Appl Physiol. 1993;75(3):1364–70.
    1. Yan S, Sliwinski P, Gauthier AP, Lichros I, Zakynthinos S, Macklem PT. Effect of global inspiratory muscle fatigue on ventilatory and respiratory muscle responses to CO2. J Appl Physiol. 1993;75(3):1371–7.
    1. MacIntyre NR, Cook DJ, Ely EW, Jr, Epstein SK, Fink JB, Heffner JE, American College of Chest Physicians; American Association for Respiratory Care; American College of Critical Care Medicine et al. Evidence-based guidelines for weaning and discontinuing ventilatory support: a collective task force facilitated by the American College of Chest Physicians; the American Association for Respiratory Care; and the American College of Critical Care Medicine. Chest. 2001;120(6 Suppl):375S–95S.
    1. Boles JM, Bion J, Connors A, Herridge M, Marsh B, Melot C, et al. Weaning from mechanical ventilation. Eur Respir J. 2007;29(5):1033–56.
    1. Esteban A, Alía I, Tobin MJ, Gil A, Gordo F, Vallverdú I, et al. Effect of spontaneous breathing trial duration on outcome of attempts to discontinue mechanical ventilation. Spanish Lung Failure Collaborative Group. Am J Respir Crit Care Med. 1999;159(2):512–8.
    1. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, ATS/ERS Task Force et al. Standardisation of spirometry. Eur Respir J. 2005;26(2):319–38.
    1. American Thoracic Society/European Respiratory Society ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002;166(4):518–24.
    1. Spadaro S, Marangoni E, Ragazzi R, Mojoli F, Verri M, Longo L, et al. A methodological approach for determination of maximal inspiratory pressure in patients undergoing invasive mechanical ventilation. Minerva Anestesiol. 2015;81(1):33–8.
    1. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44(3):837–45.
    1. Conti G, Montini L, Pennisi MA, Cavaliere F, Arcangeli A, Bocci MG, et al. A prospective, blinded evaluation of indexes proposed to predict weaning from mechanical ventilation. Intensive Care Med. 2004;30(5):830–6.
    1. Sellares J, Ferrer M, Cano E, Loureiro H, Valencia M, Torres A. Predictors of prolonged weaning and survival during ventilator weaning in a respiratory ICU. Intensive Care Med. 2011;37(5):775–84.
    1. Vallverdu I, Calaf N, Subirana M, Net A, Benito S, Mancebo J. Clinical characteristics, respiratory functional parameters, and outcome of a two-hour T-piece trial in patients weaning from mechanical ventilation. Am J Respir Crit Care Med. 1998;158:1855–62.
    1. 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.
    1. Milic-Emili J. Is weaning an art or a science? Am Rev Respir Dis. 1986;134(6):1107–8.
    1. 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;41:642–9.
    1. Testa A, Soldati G, Giannuzzi R, Berardi S, Portale G, Gentiloni Silveri N. Ultrasound M-mode assessment of diaphragmatic kinetics by anterior transverse scanning in healthy subjects. Ultrasound Med Biol. 2011;37(1):44–52.
    1. Demoule A, Jung B, Prodanovic H, Molinari N, Chanques G, Coirault C, 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. 2013;188(2):213–9.
    1. Jaber S, Jung B, Matecki S, Petrof BJ. Clinical review: ventilator-induced diaphragmatic dysfunction—human studies confirm animal model findings! Crit Care. 2011;15(2):206.
    1. 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):1327–35.
    1. Jung B, Nougaret S, Conseil M, Coisel Y, Futier E, Chanques G, et al. Sepsis is associated with a preferential diaphragmatic atrophy: a critically ill patient study using tridimensional computed tomography. Anesthesiology. 2014;120(5):1182–91.
    1. Vivier E, Mekontso Dessap A, Dimassi S, Vargas F, Lyazidi A, Thille AW, Brochard L. Diaphragm ultrasonography to estimate the work of breathing during non-invasive ventilation. Intensive Care Med. 2012;38(5):796–803.
    1. DiNino E, Gartman EJ, Sethi JM, McCool FD. Diaphragm ultrasound as a predictor of successful extubation from mechanical ventilation. Thorax. 2014;69(5):423–7.
    1. Lemaire F, Teboul JL, Cinotti L, Giotto G, Abrouk F, Steg G, et al. Acute left ventricular dysfunction during unsuccessful weaning from mechanical ventilation. Anesthesiology. 1988;69(2):171–9.
    1. Papanikolaou J, Makris D, Saranteas T, Karakitsos D, Zintzaras E, Karabinis A, Kostopanagiotou G, Zakynthinos E. New insights into weaning from mechanical ventilation: left ventricular diastolic dysfunction is a key player. Intensive Care Med. 2011;37(12):1976–85.
    1. Grasso S, Leone A, De Michele M, Anaclerio R, Cafarelli A, Ancona G, et al. Use of N-terminal pro-brain natriuretic peptide to detect acute cardiac dysfunction during weaning failure in difficult-to-wean patients with chronic obstructive pulmonary disease. Crit Care Med. 2007;35(1):96–105.
    1. Nyquist P, Stevens RD, Mirski MA. Neurologic injury and mechanical ventilation. Neurocrit Care. 2008;9(3):400–8.

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