Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 12  |  Issue : 2  |  Page : 218-225

Assessment of ventilator-induced diaphragmatic dysfunction in patients with chronic obstructive pulmonary disease using transthoracic ultrasonography


Chest Department, Faculty of Medicine, Assiut University Hospital, Assuit, Egypt

Date of Submission30-Sep-2017
Date of Acceptance22-Oct-2017
Date of Web Publication23-May-2018

Correspondence Address:
Shereen Farghaly
Chest Department, Faculty of Medicine, Assiut University Hospital, Assiut University Hospital, Assuit 7111
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ejb.ejb_99_17

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  Abstract 

Background Mechanical ventilation (MV) can cause progressive thinning of diaphragm muscle and hence progressive decrease in diaphragmatic function. We aimed to assess the rate at which diaphragm thickness (tdi) changed during MV and its effect on weaning outcome using transthoracic ultrasound (TUS) evaluation in patients with chronic obstructive pulmonary disease (COPD).
Patients and methods Thirty mechanically ventilated patients with COPD were enrolled in this cohort study. Baseline tdi was recorded within 24 h of MV after stoppage of sedation using TUS. The subsequent measurements were recorded on the third, fifth, and seventh day of MV and at the time of initiation of weaning.
Results There was a significant decrease in tdi at end expiration and at end inspiration by approximately 27.2 and 17% at third day of MV, respectively, and 35.5 and 18.5% at fifth day of MV, respectively, compared with baseline parameters. In the 10 patients who were still on ventilator till the seventh day, tdi were significantly lower compared with baseline recordings. Percentage of decrease of tdi at end inspiration from baseline recordings was significantly higher in patients with difficult weaning than in those with simple weaning. The optimum cutoff value of % of decline of tdi at end inspiration associated with difficult weaning was at least 10.6% giving 88.9% sensitivity and 83.3% specificity.
Conclusion MV is associated with gradual diaphragmatic atrophy which can be detected by TUS and could predict weaning outcome in mechanically ventilated patients with COPD.

Keywords: diaphragm, transthoracic ultrasonography, weaning


How to cite this article:
Farghaly S, Hasan AA, Makhlouf HA. Assessment of ventilator-induced diaphragmatic dysfunction in patients with chronic obstructive pulmonary disease using transthoracic ultrasonography. Egypt J Bronchol 2018;12:218-25

How to cite this URL:
Farghaly S, Hasan AA, Makhlouf HA. Assessment of ventilator-induced diaphragmatic dysfunction in patients with chronic obstructive pulmonary disease using transthoracic ultrasonography. Egypt J Bronchol [serial online] 2018 [cited 2018 Oct 22];12:218-25. Available from: http://www.ejbronchology.eg.net/text.asp?2018/12/2/218/233052


  Introduction Top


Mechanical ventilation (MV) is a lifesaver in patients with acute respiratory failure. However, prolonged mechanical ventilation can lead to serious problems [1],[2]. Of these problems, MV can impair diaphragm function [3],[4],[5], leading to ventilator-induced diaphragmatic dysfunction (VIDD) [6]. Full-support MV for a long time is suggested to increase protein breakdown and decrease protein synthesis in the diaphragm muscle resulting in diaphragm fiber atrophy [7],[8].

The diaphragm is considered the main inspiratory muscle [9]. Thus, problems including diaphragm dysfunction can impede discontinuation of MV and contribute to difficulty in weaning [10]. VIDD is expected to contribute to weaning problems [6],[11].

The tools commonly applied to assess diaphragmatic function cannot be routinely used in ICU. Fluoroscopy and computed tomography have the risk of radiation exposure. Transdiaphragmatic pressure measurement and phrenic nerve stimulation are limited by need of a special operator. Recently, ultrasonography has been considered an easily available, noninvasive, and safe bedside tool for assessment of diaphragm function [12]. Ultrasound can easily access diaphragm thickness (tdi) in its zone of apposition [13]. During inspiration (i.e. active phase of respiration), tdi could represent the contractile activity of the diaphragm [14],[15]. During expiration (i.e. resting state of respiration), decrease diaphragmatic muscle has also been considered an essential part of VIDD [6],[16].

So this study was conducted to assess the rate at which tdi changed during partial support mode of MV using transthoracic ultrasonography and its effect on weaning outcome in patients with chronic obstructive pulmonary disease (COPD).


  Patients and methods Top


This longitudinal cohort study was conducted in the ICU of chest department of a tertiary hospital over a 9-month period. Thirty mechanically ventilated patients with COPD were enrolled in the study. An informed consent was obtained from the patients or their relatives. The study was approved by the Faculty of Medicine Ethics Committee, Assiut University.

Inclusion and exclusion criteria

Patients with COPD (diagnosed by previous pulmonary function test in the past 6 months to have forced expiratory volume in 1 s/forced vital capacity <70%) who were anticipated to require MV for more than 72 h were included in the study. Morbidly obese patients (BMI>40); patients with suspicious diaphragmatic paralysis, previous history of diaphragmatic or neuromuscular disease, pneumothorax, pleural effusion; or those who previously underwent cardiothoracic surgery or pleurodesis were excluded from the study. Patients who were maintained on sedatives or muscle relaxants and those who required high PEEP (i.e. >5 cm H2O) were further excluded from the study.

Mechanical ventilation protocol

Patients with COPD enrolled in the study were ventilated on Puritan Bennett ventilator (NPB 840, Puritan-Bennett/Covidien, Carlsbad, California, USA). All patients enrolled in the study were sedated with the same sedation protocol [16],[17]. For rapid sequence intubation induction, we used intravascular dose 0.2 mg/kg of midazolam in addition to succinylcholine (1.5 to 2 mg/kg intravenous). Midazolam 0.05–0.3 mg/kg intravenous was used to maintain sedation for the first 6 h. Synchronized intermittent mechanical ventilation is the mode applied for initial setting. An initial tidal volume was set at 5–8 ml/kg of ideal body. Respiratory rate was initially adjusted at 8–12 breaths/min. The initial inspiration/expiration ratio and the inspiratory flow rate to start were 1 : 3 and 60 l/min, respectively. We generally applied PEEP of 3–5 cm H2O as a physiological PEEP [18].

Severity of illness assessment

Severity of illness on admission was assessed by severity of illness scores [19],[20],[21], and Charlson comorbidity index (CCI) was used to evaluate comorbidities [22].

Diaphragm ultrasound

In a semirecumbent position, diaphragm ultrasound (Samsung Medison Sono Ace R3 ultrasound system; Samsung Company, Seoul, South Korea) was done. The 7-MHz transducer was placed at the zone of apposition using B-mode image where the diaphragm muscle appeared as a hypoechoic structure between the diaphragmatic pleura and the peritoneal membrane [23],[24]. Images of tdi were taken during mandatory tidal breathing (i.e. we put the patient on assist-control volume controlled mode with fixed tidal volume) to ensure equal tidal volume during all consequent measurements. tdi (mm) was measured from the middle of the pleural line to the middle of the peritoneal line ([Figure 1]). Measures were recorded at the end of inspiration and end of expiration. In all enrolled patients, diaphragm ultrasound was performed within 24 h of MV after stoppage of sedation to prevent the possible effect of sedation on tdi especially at the end of inspiration. The subsequent measurements were recorded on the third, fifth, and seventh day of MV and at time of initiation of weaning process. Ultrasound was performed in all recordings by two pulmonologists, and the average of the measurement was recorded.
Figure 1 Transthoracic ultrasound applying B-mode using 7.5-MHz probe in the zone of apposition. The diaphragm thickness is measured from the middle of the pleural line to the middle of the peritoneal line (arrow).

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Weaning decision

When patients were considered ready for initiation of weaning process [25],[26], patients underwent spontaneous breathing trial (SBT). In patients who passed SBT and were successfully weaned off, weaning was considered simple weaning. Failure to pass the first SBT but weaning was achieved within 7 days of first SBT was considered difficult weaning. For patients who required more than three SBT or 7 days of weaning after the first SBT, it was considered prolonged weaning [27].

Statistical analysis

Statistical Package for the Social Sciences (SPSS, version 16) software produced by SPSS Inc. (Chicago, Illinois, USA) was used for analysis of results. Using tests of normality, data of all diaphragm ultrasound (tdi at end inspiration, tdi at end expiration, % of decline in tdi at end expiration, and % of decline in tdi at end inspiration) were detected to be nonparametric. They were presented in median and interquartile range and analyzed using Mann–Whitney U-test for comparison between two groups. Correlations of % of decline of tdi at end inspiration with disease assessment scores and electrolytes were done by Spearman’s correlation coefficient. Other results in this study were presented as mean±SD or number and percentage. The qualitative data were compared between the two groups using χ2-test, and the quantitative data were compared using Student’s t-test. P value less than 0.05 was considered significant.


  Results Top


The flowchart of patients who met the inclusion criteria is shown in [Figure 2]. Baseline diaphragm ultrasound parameters were recorded within 24 h of MV in all enrolled patients. Baseline demographic data are shown in [Table 1]. Median baseline tdi at end expiration (mm) and at end inspiration (mm) were 22 (17–30) and 37 (30–46), respectively. On day 3 of MV, a significant decrease in tdi was observed at end expiration and tdi at end inspiration by approximately 27.2 and 17%, respectively, versus baseline recordings [16 (11–22) vs. 22 (17–30), P=0.023; 29 (23–36) vs. 37 (30–46), P<0.001, respectively], as shown in [Figure 3]a. On fifth day of MV, continuous diaphragm ultrasound parameters were recorded in 22 patients. Diaphragm thickness was significantly decreased by 35.5% at end expiration and by 18.5% at end inspiration compared with their baseline parameters [16 (10–20) vs. 25 (20–30), P<0.001 and 32 (28–350 vs. 40 (36–48), P<0.001, respectively] ([Figure 3]b). In the 10 patients who were still on ventilator till the seventh day, tdi at end expiration and tdi at end inspiration were also significantly lower compared with their baseline recordings [19 (13–23) vs. 28 (24.25–30.25), P=0.005 and 36 (25.7–39.3) vs. 38 (33.75–44.75), P=0.012, respectively], as shown in [Figure 3]c.
Figure 2 Flowchart of patients who met inclusion criteria. COPD, chronic obstructive pulmonary disease; MV, mechanical ventilation.

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Table 1 Demographic data of the study group

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Figure 3 Serial measurement of tdi at end expiration and at end inspiration during mechanical ventilation.

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By recording diaphragm ultrasound parameters at time of initiation of weaning process, median tdi at end expiration and median tdi at end inspiration were lower in difficult or prolonged weaning than in those with simple weaning, but the results did not reach the statistical significance difference [11 (9.5–16.7) vs. 15.5 (10–23), P=0.123; 28 (22.7–30) vs. 31.5 (23–38), P=0.125, respectively]. However, % of decline of tdi at end inspiration from baseline recordings was significantly higher in patients with difficult or prolonged weaning than in those with simple weaning [37.3 (17.5–41.1) vs. 5.8 (0–7.9), P=0.003]. Moreover, other factors such as higher APACHE score and higher CCI (40.7±2.4 vs. 38.7±1.5, P=0.013; 5±0.9 vs. 3.9±0.6, P<0.001) were reported in patients with difficult or prolonged weaning compared with simple weaning group ([Table 2]). The optimum cutoff value of % of decline of tdi at end inspiration associated with difficult weaning was at least 10.6%, giving 88.9% sensitivity and 83.3% specificity and area under the curve of 0.815 (0.646–0.983) ([Figure 4]). Meanwhile, % of decline of tdi at end inspiration recorded at time of initiation of weaning process was found to be have significant negative correlation with baseline electrolyte levels including K level (r=−0.399, P=0.029), Ca (r=−0.575, P=0.001) and Mg (r=−0.555, P=0.001), but it showed no significant correlation with disease assessment severity scores (APACHE II, M SOFA, SAPS II, and CCI), baseline Hg, and baseline serum albumin ([Table 3]).
Table 2 Comparison of parameters between patients with simple and difficult or prolonged weaning (n=30)

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Figure 4 Reciprocal operating curve for % of decline of tdi at end inspiration at weaning time. The optimum cutoff value of % of decline of tdi at end inspiration associated with difficult or prolonged weaning was at least 10.6% giving 88.9% sensitivity and 83.3% specificity and area under the curve of 0.815 (0.646–0.983).

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Table 3 Correlation of % of decline of tdi at end inspiration at time of weaning and the base line parameters

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  Discussion Top


Failure of weaning had been commonly associated with diaphragm weakness [28],[29]. MV imposes variable degrees of muscular inactivity on the diaphragm [30], rapidly leading to VIDD. As the main finding of VIDD was decrease of tdi [6],[16], this study was designed to use bedside ultrasonography to detect rate of change in tdi during MV in patients with COPD using a partial support mode and its effect on weaning outcome.

The marked variation in baseline tdi of patients with COPD observed in our study (median baseline tdi at end expiration ranged from 17 to 30 mm) was previously demonstrated in previous studies. Arora and Rochester [31] observed decrease in diaphragm size compared with control and attributed that decrease was owing to nutritional status of patients, whereas Ishikawa and Hayes [32] found increase in parameters of diaphragm size in patients with COPD compared with control and attributed hypertrophy to increase work of breathing in patients with COPD.

At the resting state (end expiration), a significant decrease in tdi at end expiration by approximately 27.2% on third day of MV was detected. On the fifth day of MV, continuous decrease in tdi at end expiration by 35.5% was reported. Even in patients who were still mechanically ventilated till the seventh day, tdi at end expiration was significantly lower compared with baseline recordings [19 (13–23 mm) vs. 28 (24.25–30.25 mm), P=0.005]. Decrease in tdi was observed in previous studies. It was demonstrated that more than 18 h of full-support MV was associated with marked reduction of muscle fibers of the costal diaphragm [16]. Moreover, diaphragmatic fiber atrophy showed significant correlation with duration of MV [33]. Applying serial ultrasound measurements, diaphragm thinning occurs within 48 h even with partial support MV with continuous decrease by ∼6% per day of MV [34]. Another study observed 15% decrease in diaphragm force within 72 h of assist-control mechanical ventilation [35]. Diaphragmatic oxidative stress is induced by partial support ventilation as much as controlled ventilation [36].

Trying to find the effect of MV on diaphragm activity, we applied tdi at end inspiration as an ultrasound parameter of diaphragm activity. As was observed in diaphragmatic thickness at resting state, we observed significant decrease in tdi at end inspiration by approximately 17% on the third day of MV. On the fifth day of MV, that decrease continued by approximately 18.5% in patients. In the 10 patients who were still on ventilator till the seventh day, tdi at end inspiration was also significantly less compared with baseline recordings [36 (25.7–35.3 mm) vs. 38 (33.75–44.75 mm), P=0.012]. Using twitch transdiaphragmatic pressure generation recordings to assess diaphragm function, Jaber et al. [37] found that twitch transdiaphragmatic pressure decreased progressively during the period of MV. Similarly, Hermans et al. [38] observed positive correlation between duration of MV and diaphragmatic weakness. Moreover, decrease of percentage of contractile activity (as quantified by the diaphragmatic thickness fraction) by more than 10% was varied from 44 to 77% of mechanically ventilated patients [39],[40].

Diaphragm weakness contributes to weaning failure and can predict extubation difficulties [29],[41]. In the current study, we demonstrated that patients who experienced difficult or prolonged weaning were associated with more % of decline of tdi at end inspiration (recorded at time of initiation of weaning process from baseline recordings) than in those with simple weaning [37.3 (17.5–41.1) vs. 5.8 (0–7.9), P=0.003]. Furthermore, % of decline of tdi at end inspiration showed significant negative correlations with serum electrolytes including potassium, calcium, and magnesium. Alterations in intracellular electrolytes as well as mineral disturbances might account for the decreased diaphragm contractility. Hypocalcemia and hypomagnesemia could lead to decreased diaphragm function and respiratory muscle strength [42],[43]. It was also documented that hypophosphatemia reduced diaphragm contractile strength in mechanically ventilated patients presented with respiratory failure [44].

The main risk factors for ventilator-induced diaphragmatic dysfunction are duration of MV [38] and sepsis [45],[46]. However, we did not find any correlations between this degree of decline of diaphragmatic activity and duration of MV, age, and disease severity assessment scores (APACHE, SAPS II, M SOFA, and CCI). Similarly, Medrinal et al. [47] did not find a link between maximum inspiratory pressure (as an index of respiratory muscle function) and sepsis and the duration of MV evaluated at time of extubation. Although Dres et al. [48] showed that age at admission and duration of MV were associated with diaphragmatic dysfunction; however, neither of these factors were significant in the multivariate analysis. The difference in timing of evaluation of diaphragm weakness and the timing of included risk factors could affect the results. We evaluated the risk factors at the time of admission suggesting that the risk factors related to diaphragmatic dysfunction at admission could improve with time.


  Conclusion Top


MV is associated with gradual diaphragmatic atrophy which can be detected by transthoracic ultrasound and could predict weaning outcome in mechanically ventilated patients with COPD.

Limitation of the study

This study did not consider assessment of other muscles, such as intercostal muscles, pectoralis muscles, or leg muscles as that atrophy of diaphragm may be a part of disuse atrophy. In addition, this study lacked points about systemic inflammation that might cause muscle atrophy. Moreover, it missed evaluation of patients’ baseline nutritional status.

Acknowledgements

The authors thank the residents and the nurses for their help during the study.

Professor Hoda A Makhlouf contributed to concepts, design of the study, and statistical analysis. Professor Ali A. Hasan contributed to definition of intellectual content and manuscript review and takes responsibility of the integrity of the work as a whole from inception to published article. Shereen Farghaly contributed to literature search, clinical studies, data analysis, statistical analysis, manuscript preparation and manuscript review.

The manuscript has been read and approved by all the authors; the requirements for authorship as stated earlier in this document have been met; and each author believes that the manuscript represents honest work, if that information is not provided in another form.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Dreyfuss D, Saumon G. Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 1998; 157:294–323.  Back to cited text no. 1
    
2.
Tobin MJ. Advances in mechanical ventilation. N Engl J Med 2001; 344:1986–1996.  Back to cited text no. 2
    
3.
Watson AC, Hughes PD, Louise HM, 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; 29:1325–1331.  Back to cited text no. 3
    
4.
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; 167:120–127.  Back to cited text no. 4
    
5.
Chang AT, Boots RJ, Brown MG, Paratz J, Hodges PW. Reduced inspiratory muscle endurance following successful weaning from prolonged mechanical ventilation. Chest 2005; 128:553–559.  Back to cited text no. 5
    
6.
Vassilakopoulos T, Petrof BJ, Paratz J, Hodges PW. Ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 2004; 169:336–341.  Back to cited text no. 6
    
7.
Powers SK, Kavazis AN, Levine S. Prolonged mechanical ventilation alters diaphragmatic structure and function. Crit Care Med 2009; 37:S347–S353.  Back to cited text no. 7
    
8.
Shanely RA, Van Gammeren D, Deruisseau KC, Zergeroglu AM, McKenzie MJ, Yarasheski KE, Powers SK. Mechanical ventilation depresses protein synthesis in the rat diaphragm. Am J Respir Crit Care Med 2004; 170:994–999.  Back to cited text no. 8
    
9.
Mead J. Functional significance of the area of apposition of diaphragm to rib cage. Am Rev Respir Dis 1979; 119:31–32.  Back to cited text no. 9
    
10.
Ambrosino N, Gabbrielli L. The difficult-to-wean patient. Expert Rev Respir Med 2010; 4:685–692.  Back to cited text no. 10
    
11.
Eskandar N, Apostolakos MJ. Weaning from mechanical ventilation. Crit Care Clin 2007; 23:263–274.  Back to cited text no. 11
    
12.
Matamis D, Soilemezi E, Tsagourias M, Akoumianaki E, Dimassi S. Sonographic evaluation of the diaphragm in critically ill patients. Technique and clinical applications. Intensive Care Med 2013; 39:801–810.  Back to cited text no. 12
    
13.
Wait JL, Nahormek PA, Yost WT, Rochester DP. Diaphragmatic thickness-lung volume relationship in vivo. J Appl Physiol 1989; 67:1560–1568.  Back to cited text no. 13
    
14.
DiNino E, Gartman EJ, Sethi JM, McCool FD. Diaphragm ultrasound as a predictor of successful extubation from mechanical ventilation. Thorax 2014; 69:423–427.  Back to cited text no. 14
    
15.
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.  Back to cited text no. 15
    
16.
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; 358:1327–1335.  Back to cited text no. 16
    
17.
Barr J, Fraser GL, Puntillo K, Ely EW, Gélinas C, Dasta JF 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; 41:263–306  Back to cited text no. 17
    
18.
García VE, Sandoval AJC, Díaz CLA, Salgado CJC. Invasive mechanical ventilation in COPD and asthma. Med Intensiva 2011; 35:288–298.  Back to cited text no. 18
    
19.
Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Critical Care Medicine 1985; 13:818–829.  Back to cited text no. 19
    
20.
Vincent JL, Moreno R, Takala J, Willatts S, De Mendonca A, Bruining H et al. The SOFA (Sepsis-related Organ Failure Assessment) score to de-scribe organ dysfunction/failure. On behalf of the Working group on Sepsis-Related Problems of the European Society of Intensive Care Medicine. Intensive Care Med 1996; 22:707–710.  Back to cited text no. 20
    
21.
Le Gall JR, Lemeshow S, Saulnier F. A new Simplified Acute Physiology Score (SAPS II) based on a European/North American multicenter study. JAMA 1993; 270:2957–2963.  Back to cited text no. 21
    
22.
Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987; 40:373–383.  Back to cited text no. 22
    
23.
Ueki J, de Bruin PF, Pride NB. In vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax 1995; 50:1157–1161.  Back to cited text no. 23
    
24.
Shen HN, Lin LY, Chen KY, Kuo PH, Yu CJ, Wu HD et al. Changes of heart rate variability during ventilator weaning. Chest 2003; 123:1222–1228.  Back to cited text no. 24
    
25.
Esteban A, Frutos F, Tobin MJ, Alía I, Solsona JF, Valverdu V et al. Spanish Lung Failure Collaborative Group A comparison of four methods of weaning patients from mechanical ventilation. N Engl J Med 1995; 332:345–350.  Back to cited text no. 25
    
26.
Esteban A, Alia I, Tobin M, Gil A, Gordo F, Vallverdu I et al. Effect of spontaneous breathing trial duration on outcome of attempts to discontinue mechanical ventilation. Am J Respir Crit Care Med 1999; 159:512–518.  Back to cited text no. 26
    
27.
Boles JM, Bion J, Connors A, Herridge M, Marsh B, Melot C et al. Weaning from mechanical ventilation. Eur Respir J 2007; 29:1033–1056.  Back to cited text no. 27
    
28.
Vassilakopoulos T, Zakynthinos S, Roussos C. The tension-time index and the frequency/tidal volume ratio are the major pathophysiologic determinants of weaning failure and success. Am J Respir Crit Care Med 1998; 158:378–385.  Back to cited text no. 28
    
29.
Purro A, Appendini L, De Gaetano A, Gudjonsdottir M, Donner CF, Rossi A. Physiologic determinants of ventilator dependence in long-term mechanically ventilated patients. Am J Respir Crit Care Med 2000; 161:1115–1123.  Back to cited text no. 29
    
30.
Fauroux B, Isabey D, Desmarais G, Brochard L, Harf A, Lofaso F. Nonchemical influence of inspiratory pressure support on inspiratory activity in humans. J Appl Physiol 1998; 85:2169–2175.  Back to cited text no. 30
    
31.
Arora NS, Rochester DF. COPD and human diaphragm muscle dimensions. Chest 1987; 91:719–724.  Back to cited text no. 31
    
32.
Ishikawa S, Hayes JA. Functional morphometry of the diaphragm in patients with chronic obstructive lung disease. Am Rev Respir Dis 1973; 108:135.  Back to cited text no. 32
    
33.
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; 183:364–371.  Back to cited text no. 33
    
34.
Grosu HB, Lee YI, Lee J, Eden E, Eikermann M, Rose KM. Diaphragm muscle thinning in patients who are mechanically ventilated. Chest 2012; 142:1455–1460.  Back to cited text no. 34
    
35.
Sassoon CS, Zhu E, Caiozzo VJ. Assist-control mechanical ventilation attenuates ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 2004; 170:626–632.  Back to cited text no. 35
    
36.
Futier E, Constantin JM, 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:R116.  Back to cited text no. 36
    
37.
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 2010; 183:364–371.  Back to cited text no. 37
    
38.
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:R127.  Back to cited text no. 38
    
39.
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; 41:642–649.  Back to cited text no. 39
    
40.
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. Critical Care 2015; 19:422.  Back to cited text no. 40
    
41.
Farghaly S, Hasan AA. Diaphragm ultrasound as a new method to predict extubation outcome in mechanically ventilated patients. Aust Crit Care 2016; 30:37–43.  Back to cited text no. 41
    
42.
Aubier M, Viires N, Piquet J, Murciano D, Blanchet F, Marty C et al. Effects of hypocalcemia on diaphragmatic strength generation, J Appl Physiol 1985; 58:2054–20611.  Back to cited text no. 42
    
43.
Molloy DW, Dhingra S, Solven F, Wilson A, Mc Carthy DS. Hypomagnesia and respiratory muscle power. Am Rev Resp Dis 1984; 129:497–498.  Back to cited text no. 43
    
44.
Aubier JM, Murciano D, Lecoguic Y, Viires N, Squara P, Pariente R. Effects of hypophosphatemia on diaphragmatic contractility in patients with acute respiratory failure. N Engl J Med 1985; 313:420–424.  Back to cited text no. 44
    
45.
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; 188:213–219.  Back to cited text no. 45
    
46.
Supinski GS, Callahan LA. Diaphragm weakness in mechanically ventilated critically ill patients. Crit Care 2013; 17:R120.  Back to cited text no. 46
    
47.
Medrinal C, Prieur G, Frenoy E, Quesada AR, Poncet A, Bonnevie T et al. Respiratory weakness after mechanical ventilation is associated with one-year mortality − a prospective study. Critical Care 2016; 20:231.  Back to cited text no. 47
    
48.
Dres M, Dubé BP, 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 ICU patients. Am J Respir Crit Care Med 2017; 195:57–66.  Back to cited text no. 48
    


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