Ultrasound shear wave elastography for assessing diaphragm function in mechanically ventilated patients: a breath-by-breath analysis

Quentin Fossé, Thomas Poulard, Marie-Cécile Niérat, Sara Virolle, Elise Morawiec, Jean-Yves Hogrel, Thomas Similowski, Alexandre Demoule, Jean-Luc Gennisson, Damien Bachasson, Martin Dres, Quentin Fossé, Thomas Poulard, Marie-Cécile Niérat, Sara Virolle, Elise Morawiec, Jean-Yves Hogrel, Thomas Similowski, Alexandre Demoule, Jean-Luc Gennisson, Damien Bachasson, Martin Dres

Abstract

Background: Diaphragm dysfunction is highly prevalent in mechanically ventilated patients. Recent work showed that changes in diaphragm shear modulus (ΔSMdi) assessed using ultrasound shear wave elastography (SWE) are strongly related to changes in Pdi (ΔPdi) in healthy subjects. The aims of this study were to investigate the relationship between ΔSMdi and ΔPdi in mechanically ventilated patients, and whether ΔSMdi is responsive to change in respiratory load when varying the ventilator settings.

Methods: A prospective, monocentric study was conducted in a 15-bed ICU. Patients were included if they met the readiness-to-wean criteria. Pdi was continuously monitored using a double-balloon feeding catheter orally introduced. The zone of apposition of the right hemidiaphragm was imaged using a linear transducer (SL10-2, Aixplorer, Supersonic Imagine, France). Ultrasound recordings were performed under various pressure support settings and during a spontaneous breathing trial (SBT). A breath-by-breath analysis was performed, allowing the direct comparison between ΔPdi and ΔSMdi. Pearson's correlation coefficients (r) were used to investigate within-individual relationships between variables, and repeated measure correlations (R) were used for determining overall relationships between variables. Linear mixed models were used to compare breathing indices across the conditions of ventilation.

Results: Thirty patients were included and 930 respiratory cycles were analyzed. Twenty-five were considered for the analysis. A significant correlation was found between ΔPdi and ΔSMdi (R = 0.45, 95% CIs [0.35 0.54], p < 0.001). Individual correlation displays a significant correlation in 8 patients out of 25 (r = 0.55-0.86, all p < 0.05, versus r = - 0.43-0.52, all p > 0.06). Changing the condition of ventilation similarly affected ΔPdi and ΔSMdi. Patients in which ΔPdi-ΔSMdi correlation was non-significant had a faster respiratory rate as compared to that of patient with a significant ΔPdi-ΔSMdi relationship (median (Q1-Q3), 25 (18-33) vs. 21 (15-26) breaths.min-1, respectively).

Conclusions: We demonstrate that ultrasound SWE may be a promising surrogate to Pdi in mechanically ventilated patients. Respiratory rate appears to negatively impact SMdi measurement. Technological developments are needed to generalize this method in tachypneic patients.

Trial registration: NCT03832231 .

Keywords: Diaphragm; Diaphragm dysfunction; Intensive care unit; Mechanical ventilation; Shear wave elastography; Transdiaphragmatic pressure; Ultrasound imaging.

Conflict of interest statement

JLG is a scientific consultant for Supersonic Imagine, Aix-en-Provence, France. MD received personal fees from Lungpacer Medical Inc., Vancouver, Canada. AD reports personal fees from Medtronic, grants, personal fees and non-financial support from Philips, personal fees from Baxter, personal fees from Hamilton, personal fees and non-financial support from Fisher & Paykel, grants from French Ministry of Health, personal fees from Getinge, grants, personal fees and non-financial support from Respinor, grants, personal fees and non-financial support from Lungpacer, personal fees from Lowenstein, outside the submitted work. The remaining authors do not declare any competing interest.

Figures

Fig. 1
Fig. 1
Typical ultrasound image obtained during shear wave elastography imaging of the diaphragm. Shear modulus map obtained from ultrasound shear wave elastography overlaid with standard ultrasound B-Mode during intercostal scanning of the diaphragm at the right zone of apposition
Fig. 2
Fig. 2
Flowchart of the study
Fig. 3
Fig. 3
Diaphragm shear modulus and transdiaphragmatic pressure across different breathing conditions. PTPdi, pressure–time product of transdiaphragmatic pressure (Panel a); ΔPdi, inspiratory change in transdiaphragmatic pressure (Panel b); ΔSMdi, inspiratory change in diaphragm shear modulus assessed using ultrasound shear wave elastography (Panel c). The error bars correspond to 25th and 75th percentile. PS, pressure support ventilation with baseline inspiratory support and positive end-expiratory pressure; PS+25%, PS with inspiratory pressure support increased by 25%; PS-25%, PS with inspiratory pressure support decreased by 25%; PSZEEP, PS with baseline inspiratory support and positive end-expiratory pressure set at 0; SBT, spontaneous breathing trial; SBT Start, start of the SBT; SBT End, end of the SBT. a Significantly different from PS+25%; b Significantly different from PS; c significantly different from PS−25%; d Significantly different from PSZEEP (all p < 0.05)
Fig. 4
Fig. 4
Relationship between changes in diaphragm shear modulus and changes in transdiaphragmatic pressure. Averaged data (panel a, data are shown as median (Q1–Q3)) and all data points with individual and overall linear regression lines (panel b). Panel c displays the individual linear regressions in patients with a significant ΔPdi-ΔSMdi correlation (p < 0.05). Panel d displays the individual linear regressions in patients with no significant ΔPdi-ΔSMdi correlation (p > 0.05). ΔPdi, inspiratory change in transdiaphragmatic pressure; ΔSMdi, inspiratory change in diaphragm shear modulus assessed using ultrasound shear wave elastography; PS, pressure support ventilation with baseline inspiratory support and positive end-expiratory pressure; PS+25%, PS with inspiratory pressure support increased by 25%; PS−25%, PS with inspiratory pressure support decreased by 25%; PSZEEP, PS with baseline inspiratory support and positive end-expiratory pressure set at 0; SBT Start, start of the spontaneous breathing trial. In panel a., only cycles gathered at the end of each condition and at the start of SBT were used. In panel b, cycles gathered at all time-points were used
Fig. 5
Fig. 5
Physiological variables and diaphragm shear modulus over time in two patients. Temporal evolution of airway flow, esophageal (Pes), gastric (Pga) and transdiaphragmatic (Pdi) pressures, and diaphragm shear modulus (SMdi) in a patient with a significant ΔPdi–ΔSMdi relationship (r = 0.81, p = 0.002, panel a) and in a patient with a non-significant ΔPdi–ΔSMdi relationship (r = 0.14, p = 0.643, panel b). Respiratory rates were of 12 and 33 breaths.min−1 for panel a and b, respectively

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