Research ArticleOriginal Research

Extubation Failure Prediction by Echography of the Diaphragm After Cardiothoracic Surgery: The EXPEDIA Study

Thibaut Genty, Florent Laverdure, Olivier Peyrouset, Saïda Rezaiguia-Delclaux, Jacques Thès and François Stéphan
Respiratory Care March 2022, 67 (3) 308-315; DOI: https://doi.org/10.4187/respcare.09476

Abstract

BACKGROUND: Successful extubation is difficult to predict. Ultrasound measurement of the diaphragm thickening fraction (DTF) might help predict weaning failure after cardiothoracic surgery.

METHODS: We assessed the predictive performance of diaphragm ultrasound in a derivation cohort of 50 prospectively included cardiothoracic surgery subjects ready for a weaning trial and in a validation cohort of 39 subjects ventilated for ≥ 48 h. DTF was assessed by ultrasound during pressure support ventilation (PSV) then during a T-piece spontaneous breathing trial (SBT). DTF was the percentage change in diaphragm thickness between expiration and inspiration and DTFmax, the higher DTF value of the 2 hemidiaphragms. DTFmax during SBT (static study) and the difference in DTFmax between PSV and SBT (dynamic study) were analyzed.

RESULTS: In the derivation cohort, DTFmax during SBT was 25.6 ± 17.3% in subjects with successful extubation and 65.2 ± 17.3% in those with weaning failure (difference 39.7 [95% CI 27.4–51.9], P < .01). During SBT, DTFmax ≥ 50% was associated with weaning failure (area under the receiver operating characteristic curve [AUC] 0.94 ± 0.05). In the dynamic study, a ≥ 40% DTFmax increase was associated with weaning failure (AUC 0.91 ± 0.06). In the validation cohort, DTFmax during SBT was 20.3 ± 17.1% in subjects with successful extubation and 82.0 ± 51.6% in those with weaning failure (difference 61.8 [95% CI 41.6–82.0], P < .01). During SBT, DTFmax ≥ 50% predicted weaning failure (AUC 0.99 ± 0.02). In the dynamic study, a ≥ 40% increase in DTFmax predicted weaning failure (AUC 0.81 ± 0.09).

CONCLUSIONS: Measuring DTFmax during SBT and the DTFmax change when switching from PSV to SBT may help predict weaning failure after cardiothoracic surgery. The study was registered on ANZCTR. Clinical trial registration number: U1111-1180-1999.

Introduction

Of the total duration of invasive mechanical ventilation, 40% is spent on weaning.1 Weaning and extubation is a critical period about which knowledge has improved over the last 2 decades.2,3 Weaning readiness can be assessed by either a trial of pressure support ventilation (PSV) or a spontaneous breathing trial (SBT) on a T-piece.4 Weaning failure is often due to a combination of respiratory failure, heart failure, ineffective cough, neurologic disorders, and/or upper-airway obstruction. Factors that add to the difficulty of weaning after surgery include pain, atelectasis, and diaphragm dysfunction. Diaphragm dysfunction can result from reflex inhibition of diaphragm contractions due to muscle injury, presence of a chest tube, and/or phrenic nerve injury.5 In studies of heart surgery, 7% of subjects needed re-intubation and 5% tracheostomy for prolonged ventilation.6,7

Ultrasound assessment of diaphragm thickening during contractions has been described as a noninvasive and reproducible method available at the bedside8-10 and capable of providing information on muscle strength,11 diaphragm dysfunction or diaphragm palsy,12 work of breathing (WOB) in ventilated patients,13,14 and progression of ventilator-induced diaphragm atrophy.15,16 Moreover, the diaphragm thickening fraction (DTF) measured at the apposition zone during the respiratory cycle estimates the WOB.17,18

In patients with nonsurgical conditions, DTF measurement may help to predict weaning failure.19-21 Little information is available about DTF after heart surgery, however. In a recent study, a decrease in diaphragm thickening was often found after heart surgery but was not associated with the respiratory outcome.22 The potential usefulness of DTF measurement for predicting weaning failure after heart surgery has not been evaluated.

Here, our primary objective was to determine whether DTF values measured during the SBT predicted weaning failure after cardiothoracic surgery. The secondary objectives were to assess DTF changes during the transition from PSV to SBT and to determine whether these changes predicted weaning failure.

QUICK LOOK

Current Knowledge

In nonsurgical patients, the diaphragm thickening fraction (DTF) measured by ultrasound may help to predict ventilator liberation. Little information is available about DTF after heart surgery. The potential usefulness of DTF measurement for predicting weaning failure after heart surgery has not been evaluated.

What This Paper Contributes to Our Knowledge

In subjects after cardiothoracic surgery, we found that 2 ultrasound indices based on DTF performed well in predicting ventilator liberation, namely DTF ≥ 50% for at least one hemidiaphragm during a T-piece spontaneous breathing trial (SBT) and a ≥ 40% increase in DTF during the switch from pressure support ventilation to the SBT.

Methods

Study Design and Subjects

The derivation cohort was recruited prospectively in a single 23-bed cardiothoracic ICU. The protocol was approved by the appropriate ethics committee (Comité de protection des personnes d’Ile de France [#2013-A01552]) and was registered on ANZCTR (U1111-1180-1999). Informed consent was obtained from all subjects or next of kin. Patients who were receiving mechanical ventilation, admitted to the ICU after cardiothoracic surgery between May 2016–November 2016, and ready to undergo a first SBT were eligible. Weaning readiness was defined as effective cough; absence of excessive tracheobronchial secretions; stable cardiovascular and metabolic status; and adequate oxygenation, pulmonary function, and mentation.23 We excluded patients with a history of stroke or diaphragmatic surgery as well as tracheostomized patients. Subjects were included only for the first SBT. Patients in whom diaphragmatic palsy was diagnosed during the ultrasonography were also excluded. The derivation cohort served to define the diaphragmatic ultrasound index that best predicted weaning failure. The same operator made all measurements (TG). No minimum duration of previous ventilation was required.

The validation cohort consisted of subjects who received invasive mechanical ventilation for at least 48 h after cardiothoracic surgery during the 12-month period from October 2016–September 2017 and who met the above-listed weaning-readiness criteria. All ultrasound measurements were performed by the same operator (FL).

Study Protocol

All subjects in both cohorts initially received PSV adjusted to provide a tidal volume of 8 mL/kg of ideal body weight and to eliminate signs of acute respiratory failure. PEEP was 5–10 cm H2O.

Two diaphragm ultrasound assessments were performed in each subject, the first during PSV and the second within the next hour, during the SBT, after at least 5 min of stable continuous breathing. We were thus able to evaluate changes in diaphragm thickness between 2 different work load conditions. The SBT lasted 30–60 min, during which subjects received an oxygen (O2) flow of 6–12 L/min to maintain peripheral SpO2 ≥ 92%. Forced inspiration was not used for the measurements.

Successful extubation was defined as extubation without re-intubation within the following 48 h.23 Weaning failure was defined as SBT failure or extubation followed by re-intubation within 48 h. SBT failure was defined as any of breathing frequency > 35 breaths/min, SpO2 < 90% with 12 L/min O2, signs of respiratory distress (use of accessory muscles, intercostal recession, nasal flaring), heart rate > 140 beats/min, systolic arterial pressure increase > 20%, arrhythmia, or altered consciousness.23 After SBT failure, subjects received PSV at a level that kept them comfortable. Requiring bi-level positive airway pressure (BPAP) or high-flow nasal cannula (HFNC) oxygen after extubation was not classified as extubation failure. The use of these oxygenation methods in cardiothoracic surgery subjects has been reported previously.24

We collected the following data: age, sex, body mass index, history of COPD, diabetes, heart failure (left-ventricular ejection fraction < 40%), Simplified Acute Physiology Score II, surgical procedure, duration of ventilation, duration of PSV, ICU length of stay, tracheostomy, and death.

Diaphragm Ultrasound

The diaphragm ultrasound examinations were performed by 2 experienced operators (TG and FL) who were blinded to extubation decisions. They used a 3.5-MHz Vivid 6 ultrasound probe (GE Healthcare, Chicago, Illinois) to measure diaphragm excursion along the midaxillary line on the left and right sides, with the goal of identifying subjects with diaphragm palsy.12 The diaphragm was identified as an echogenic curved structure located between the abdominal organs (liver or spleen) and the lungs. Diaphragm palsy was defined as the absence of movement or as paradoxical motion during the breathing cycles.10

Diaphragm thickness was measured using a 7–10-MHz linear Vivid 6 ultrasound probe (GE Healthcare). Measurements were performed as previously described8,11,25,26 using the leading-edge method to minimize thickness overestimation due to inclusion of the peritoneal membrane. The breathing frequency curve was connected to the ultrasound device to locate end expiration and end inspiration on the ultrasound images. Diaphragm end-expiratory thickness (eET) was measured just before thickening started and end-inspiratory thickness (eIT) at the inspiratory peak. The DTF was computed as follows: DTF=(eIT-eET)/eET. For this study, we computed DTF as the mean of measurements during 3 consecutive breaths. DTF was measured separately for each hemidiaphragm in each subject; the higher of the 2 values was defined as DTFmax. ΔDTFmax was defined as the change in DTFmax when switching from PSV to the SBT: ΔDTF (%) = (DTFmax SBT-DTFmax PSV)/DTFmax PSV.

Statistical Analysis

To have 80% power for evidencing a 30% increase in DTF during the SBT compared to PSV (as observed in a test sample), with the alpha risk set at 5%, 48 subjects were needed in the derivation cohort.

The normality of data distribution was assessed by the Kolmogorov-Smirnov test. Quantitative variables were described as mean (± SD) and compared using Student t test if normally distributed and were described as median (interquartile range [IQR]) otherwise. We described qualitative variables as number (%). The best DTFmax cutoff value was determined during the SBT (static cutoff) and after the switch from PSV to the SBT (dynamic cutoff) using receiver operating characteristic (ROC) curves. ROC curves were compared according to Hanley et al.27 The significance threshold was set at P < .05.

As previously reported,9 we assessed measurement reproducibility between the 2 observers (TG and FL) in 17 subjects during spontaneous breathing or PSV by computing the intraclass correlation coefficient.

Sensitivity was the ability of DTFmax during SBT or of ΔDTFmax during the PSV-to-SBT switch to correctly identify subjects who would experience weaning failure. Specificity was the ability of DTFmax during SBT or of ΔDTFmax during the PSV-to-SBT switch to correctly identify subjects who would be successfully extubated. Statistical analyses were performed with Statview 5.0 statistical packages (SAS Institute, Cary, North Carolina).

Results

Study Population and Outcomes

Figure 1 is the subject flow chart. Of 70 patients screened for the derivation cohort, 20 were excluded for the following reasons: history of stroke, n = 10; tracheotomy, n = 6; and diaphragmatic palsy diagnosed by ultrasonography, n = 4. The remaining 50 subjects were included. Among them, 10 (20%) failed weaning and 40 (80%) were successfully extubated. Of the 10 subjects with weaning failure, 7 failed during the SBT, and 3 were re-intubated due to respiratory insufficiency. In this cohort, none of the successfully extubated subjects required re-intubation beyond 48 h.

Fig. 1.
Fig. 1.

Flow charts of the derivation (A) and validation (B) cohorts.

In the validation cohort, of 66 screened patients, 27 were excluded for the following reasons: tracheotomy, n = 15; history of stroke, n = 8; and diaphragmatic palsy diagnosed by ultrasonography, n = 4. Of the remaining 39 subjects, 11 (28%) failed weaning and 28 (72%) were successfully extubated. Of the 11 subjects with weaning failure, 7 failed during the SBT, and 4 were re-intubated within 48 h for respiratory insufficiency. Of the 28 successfully extubated subjects, 4 required re-intubation beyond 48 h (pneumonia, n = 2; surgical complication, n = 1; and heart failure, n = 1). Table 1 reports the main subject characteristics and Table 2 the ventilation parameters.

View this table:
Table 1.

Main Baseline Characteristics of the Subjects in the Derivation and Validation Cohorts

View this table:
Table 2.

Respiratory Parameters and Blood Gas Values in Subjects Receiving Pressure Support Ventilation and During the Spontaneous Breathing Trial

DTFmax Values during the SBT

The interobserver intraclass correlation coefficient for DTF measurements was 0.86 (95% CI 0.65–0.95), indicating good reliability. Table 3 shows that the DTFmax during the SBT differed significantly between the groups with failed versus successful weaning in both the derivation and the validation cohorts. The AUC for DTFmax during the SBT was 0.94 (0.05) in the derivation cohort and 0.99 (0.02) in the validation cohort (see related supplemental material at http://rc.rcjournal.com).

View this table:
Table 3.

Maximum Diaphragmatic Thickening Fraction in the 2 Cohorts According to Weaning Outcome

Figure 2 depicts the DTFmax values during the SBT in the groups with failed and successful weaning in both cohorts. The 2 ROC curves are comparable (P = .13). A DTFmax cutoff of ≥ 50% during the SBT predicted weaning failure with 90.0% (95% CI 0.54–0.99) sensitivity and 92.5% (95% CI 0.78–0.98) specificity in the derivation cohort. Corresponding values in the validation cohort were 90.9% (95% CI 0.57–0.99) and 100% (95% CI 0.85–1.00).

Fig. 2.
Fig. 2.

Values of DTFmax (%) according to weaning outcome in the derivation (A) and validation (B) cohorts. DTFmax: the best diaphragmatic thickening fraction value of one of the 2 hemidiaphragms. The gray lines represent the DTFmax value of 50%, beyond which subjects were at risk for weaning failure. In the derivation cohort, the outlying circle represents a subject with successful extubation despite a major increase in DTFmax to 90% after switching from pressure support ventilation to the spontaneous breathing trial; during extubation, the physician in charge observed that the endotracheal tube was obstructed by a solid mucous plug. DTFmax measured after extubation decreased to 25%.

DTFmax Values during PSV

Table 3 shows that DTFmax values in subjects receiving PSV differed significantly between subjects with failed versus successful weaning in both cohorts.

Change in DTFmax Values: (ΔDTFmax)

In successfully extubated subjects, DTFmax values were similar during PSV and during the SBT (Fig. 3). In contrast, in subjects who failed weaning, DTFmax increased significantly after switching from PSV to the SBT (Fig. 3). The median ΔDTFmax was small in successfully extubated subjects in both cohorts (−1.5% [IQR −24.3 to 22.2] in the derivation cohort and 7.1% [IQR −27.0 to 37.4] in the validation cohort) and large in subjects with weaning failure (130.0% [IQR 48.0–148.0] in the derivation cohort and 80% [IQR 57.0–142.0] in the validation cohort).

Fig. 3.
Fig. 3.

ΔDTFmax (%) after switching from pressure support ventilation (PSV) to the spontaneous breathing trial (SBT) in the derivation (A) and the validation (B) cohort. Gray represents subjects with successful weaning and black those with weaning failure. DTFmax: the best DTF value of one of the 2 hemidiaphragms; SBT: spontaneous breathing trial on a T-piece. * Difference between DTFmax during PSV and SBT in the group with weaning failure in the derivation cohort: (32.7 [95% CI 19.2–41.6], P < .001). † Difference between DTFmax values during the SBT in the groups with successful and failed weaning in the derivation cohort: (39.7 [95% CI 27.4–51.9], P < .001). ‡ Difference between DTFmax values during PSV and SBT in the group with failed weaning in the validation cohort: (43.2 [95% CI 9.8–76.5], P = .02). § Difference between DTFmax values during the SBT in the groups with successful and failed weaning in the validation cohort: (61.8 [95% CI 41.6–81.9], P < .001).

The AUC for ΔDTFmax was 0.91 (0.06) in the derivation cohort and 0.81 (0.09) in the validation cohort (see related supplemental material at http://rc.rcjournal.com). ΔDTFmax ≥ 40% predicted weaning failure with 90.0% (95% CI 0.54–0.99) sensitivity and 90.0% (95% CI 0.75–0.97) specificity in the derivation cohort. Corresponding values in the validation cohort were 90.9% (95% CI 0.57–0.99) and 100% (95% CI 0.85–1.00), respectively.

Discussion

In our study, both DTFmax ≥ 50% during the first SBT (static assessment) and ΔDTFmax ≥ 40% after switching from PSV to the first SBT (dynamic assessment) total performed well for predicting weaning failure in subjects admitted to the ICU after cardiothoracic surgery. In the 89 total subjects, the re-intubation rate (7.8%) and SBT failure rate (16%) are consistent with previous reports.6,28

Diaphragm ultrasonography with DTF measurement is a noninvasive tool that accurately assesses WOB.9,13,14 DTF correlates significantly with diaphragm electrical activity and transdiaphragmatic pressure.14,18 In healthy individuals, the mean DTF value during quiet inspiration is about 20%,29 and the highest DTF values can reach 200% during maximal inspiration.30 Thus, marked diaphragmatic thickening during forced breathing reflects the diaphragmatic reserve.31

DTF is a good marker for estimating changes in WOB.13,17,18 In patients receiving various levels of pressure support (PS) (PSV, BPAP, or HFNC oxygen), DTF decreases in proportion to the increase in PS,13,17,18 with higher PS levels being associated with weaker diaphragm contractions. Thus, DTF might serve as a subclinical marker for detecting an increase in WOB.13

After heart surgery, mechanical ventilation is briefer and diaphragm muscle wasting less likely to develop than in patients with ARDS,32 in whom the main mechanisms of diaphragmatic damage are ventilator-induced diaphragmatic dysfunction and sepsis-related diaphragmatic muscle damage.33 After heart surgery, diaphragmatic dysfunction is the rule, even in patients who are successfully extubated.22 The multiple underlying mechanisms include phrenic nerve control inhibition by a reflex mechanism independent of pain, phrenic nerve stretching or injury during surgery, ventilator-induced diaphragmatic dysfunction, and neuromyopathy.34-37 A role for atelectasis and chest drains is suspected but has not been proven.38

A recent study showed that a low DTFmax before heart surgery helped to identify subjects at increased risk for postoperative pulmonary complications.39 Surgery is followed by a decrease in inspiratory muscle strength40 and by diaphragmatic dysfunction with reductions in diaphragm excursion and thickening.22,34 This dysfunction is transient.34 DTF values may reflect the balance between the work of the diaphragm and the respiratory needs.9,17,18,41 We performed the ultrasound during the period of maximum diaphragmatic dysfunction,34 when a small WOB increase may disrupt this balance. Subjects with high DTFmax values during the SBT already had a high WOB and were consequently at greater risk for SBT failure or re-intubation due to diaphragmatic fatigue. Subjects with COPD were recently shown to have an increased diaphragmatic work load and a reduction in diaphragmatic force reserve compared to healthy volunteers.31

However, DTF measurement is still a matter of controversy. In several studies of nonsurgical subjects, a higher DTF value was associated with better weaning outcomes.19-21,42-45 The diaphragm was evaluated during PSV,45 during an SBT, or after an SBT.19 Diaphragm dysfunction was defined as < 30% of thickening of a least one hemidiaphragm.19,46 An increase in DTF at total lung capacity indicates that diaphragmatic function is preserved and that a diaphragmatic force reserve is available to tackle an increase in WOB.31 In contrast, a DTF increase during breathing at rest probably indicates that no further reserve is available.47 A recent multi-center study suggests that a low DTF may not be a good marker of diaphragmatic dysfunction.46 We agree that a low DTF is not a major factor in determining weaning failure. On the contrary, our results suggest that a high DTF value may be the most useful indicator.

In all studies of diaphragmatic ultrasound during weaning, DTF was viewed as a static predictor of extubation.46,48 This may explain the discrepancies with our study. We used DTF as not only a static but also a dynamic index that allowed us to observe diaphragmatic function under 2 different WOB conditions (PSV and SBT). A DTF increase after switching from PSV to the first SBT indicated an increase in respiratory load and a higher risk of weaning failure.

In a population at low risk for weaning failure, diaphragm ultrasound to guide weaning of the ventilator may be seen as excessive monitoring associated with unnecessary costs. Diaphragm ultrasound may be most beneficial in the event of SBT failure to provide information on the diaphragmatic work load.

There are several limitations to our work. First, this is a single-center study whose results require confirmation at other centers. Second, the PS level was not standardized. However, in the dynamic study, this level was not a major factor since diaphragmatic contraction was assessed under the same work load conditions during the SBT in all subjects. Third, there is a risk of measurement bias, as the diaphragm is not very thick. Nonetheless, the intraclass correlation coefficient indicated good interobserver reliability in our study. Fourth, we did not add a DTF measurement during maximal inspiration, which would have allowed us to evaluate the diaphragmatic force reserve. It is difficult for patients to perform a maximal inspiration in the early postoperative period. Finally, we defined weaning failure as clinical SBT failure or as re-intubation within 48 h after the initial extubation. A more recent definition of weaning failure includes re-intubation up to 7 d after the initial extubation.49 However, it seems unlikely that diaphragm fatigue can result in re-intubation after more than 48 h of spontaneous breathing.

Conclusions

Our results suggest that the DTFmax value measured by ultrasound during the SBT and the DTFmax change after switching from PSV to SBT may help to predict weaning failure after cardiothoracic surgery.

Footnotes

  • Correspondence: Thibaut Genty MD, Department of Anesthesiology and Intensive Care, Marie Lannelongue Hospital, 133 avenue de la Résistance, 92350 Le Plessis Robinson, Groupe Hospitalier Paris Saint Joseph, Paris, France. E-mail: t.genty{at}ghpsj.fr

  • The authors have disclosed no conflicts of interest.

  • The study was supported solely by institutional sources.

  • Supplemental material related to this paper is available at http://rc.rcjournal.com.

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