European Journal of Cardiovascular Medicine

Intensive care unit (ICU) patients who are critically ill often get mechanical ventilation using the pressure-supported approach [1]. Approximately 20% of ICU patients experience difficulty during the weaning process, with 40% of those experiencing prolonged stays during weaning trials [2]. Extended use of ventilatory assistance may result in compromised diaphragmatic function, which may complicate the process of weaning by causing atrophy and protracted dysfunction. Maintaining diaphragmatic function is essential during the weaning process, but the standard techniques for diaphragmatic assessment fluoroscopy, phrenic nerve conduction, and trans-diaphragmatic pressure measurements have drawbacks and restrictions, including the need to transport patients, exposure to ionizing radiation, and limited availability.

Lung ultrasound (LUS) is a safe, non-invasive, portable, and radiation-free tool that is useful in critical care. It provides real-time morphologic and functional information, making it a fast diagnostic tool. LUS is essential for assessing two critical factors - lung aeration status and functional status of the diaphragm, which are clues to the probability of successful extubation in mechanically ventilated patients. [3] In the ICU, rapid shallow breathing index (RSBI) and spontaneous breathing trial (SBT) are typically used to predict liberation from the mechanical ventilator (MV). Therefore, assessing patients before and during SBT is crucial in predicting extubation failure. [4] Recently, the lung ultrasound score has been introduced to assess lung abnormalities patterns. Bouhemad first proposed the lung ultrasound score for lung aeration patterns, and later, this score was also used to predict weaning outcomes. The visualization of multiple and diffuse B-lines (more than three per intercostal space) is suggestive of increased fluids in the lung. A B-line is a well-defined, laser-like, hyperechoic comet-tail artifact arising from the pleural line. [5,6] In comparison to existing weaning measures, this study attempts to evaluate the predictive power of lung ultrasonography scores as new additive parameters for weaning process results.

This study included the prospective observation of fifty mechanically ventilated and intubated patients who were admitted to the Department of Anaesthesia and Critical Care at Nalanda Medical College and Hospital in Patna, Bihar, India. To participate in this study, the patient's guardians or family members gave their written approval in accordance with the ethical committee's guidelines.

Inclusion Criteria: For this study, we selected patients who have reached the age of 18 and planned for extubation who have spent more than 48 hours in the critical care unit with intubation and mechanical ventilation.

Exclusion criteria: For this study, we excluded the following patients: those who were 18 years old or younger, patients with left or right ventricular failure, pulmonary hypertension, aortic valve disease, hyperthyroidism, any patient with a known neuromuscular disorder, any patient with primary ultrasound revealed unilateral/bilateral absent diaphragmatic mobility, and any patient who had undergone post-esophageal or thoracic surgeries due to intra-operative diaphragmatic manipulation.

Every patient involved in this study had the following procedures: a physical examination, an evaluation of their medical history, and laboratory results including arterial blood gases. Each patient's Acute Physiology and Chronic Health Evaluation (APACHE) II score was established at the time of admission [7]. Every patient's sequential organ failure assessment score (SOFA score) was calculated during their stay in the intensive care unit [8]. Following the spontaneous breathing experiment, the serum level of NT-pro BNP in each patient was measured using the electrochemiluminescence detection method [9].

The patients selected to start weaning according to the criteria shown in Table 1 were disconnected from the ventilators to allow spontaneous breath trial (SBT) either using a T tube or 8 cm H2O of pressure support for 30-120 minutes. Each diaphragm was evaluated to rule out absent diaphragmatic mobility in either side; when detected the patient was excluded from the study. This is followed by a complete diaphragmatic and lung ultrasound.

Table 1: Showing the criteria to start the weaning for the ICU patients.

After the spontaneous breath trial (SBT), a highly qualified lung ultrasound operator assessed the lung ultrasound score (LUS) using a curved array ultrasonography probe operating at a frequency of 2.5–5 MHz. The patient should be positioned supine or in lateral decubitus. To determine the degree of lung aeration, each lung was divided into three zones, each of which was analyzed anteriorly and posteriorly using B-mode. A total of 12 zones were studied. The image analysis and lung ultrasound score were calculated as per Table 2 [10].

Table 2: Showing the criteria for the lung ultrasound score for detection of the degree of lung aeration

Post-extubation failure was considered when non-invasive ventilation or reintubation was required within 48 hours following extubation. Patients' stays in hospitals, critical care units, and deaths were tracked. Based on how the patients responded to weaning trials, they were divided into two groups. After 48 hours, group B underwent machine ventilation and re-intubation due to failed weaning (FW), while group A underwent successful weaning (SW) and was moved to the ward. Weaning criteria, including PaO2, PaCO2, respiratory rate (RR), maximum inspiratory force (MiP), and rapid shallow breath index (RSBI), were correlated with the diaphragmatic excursion (E) during inspiration, lung ultrasound measurements, and diaphragmatic muscle thickening fraction (DTF). Indications for the reintubation in the patient under study were as follows:

• Hypoxemia in the form of PO₂ <50 on room air or <200 on FiO2 100%.
• Respiratory rate more than 40 or less than 6.
• Impaired conscious level, hemodynamic instability, and excessive secretions.

For quantitative parametric measurements, the data was given as mean and standard deviation (SD) [Mean ± SD]. The Statistical Package for the Social Sciences (SPSS) version 24.0 for Windows was used to undertake the statistical analysis of the study's data. The student t-test was utilized to compare two independent mean groups for parametric data. Additionally, for parametric data, the Pearson correlation test was used to investigate any potential relationships between each pair of variables within each group. The p-value less than 0.05 was considered significant.

This study was conducted on fifty patients with ages ranging from 31 to 78 years old, with a mean age of 53.80±10.94 years. Thirty-seven patients were successful in the weaning process, forming group A (SW) and representing 74% of the participants. Thirteen patients failed the weaning process and were re-intubated within 48 hours after the trial, forming group B (FW) and representing 26% of the participants. The average duration of mechanical ventilation observed in our study was 6.64±2.15 days. The demographic profiles of the patients who participated are detailed in Table 3.

Table 3: Showing the different demographic profiles and clinical data of the patients

The results of various ultrasound parameters, blood gases, and respiratory mechanics, including the mean value, t-value, and significance, are presented in Tables 4 and 5.

Table 4: Showing the comparison of different ultrasound parameters, blood gases, and respiratory mechanics results between both groups

Table 5: Showing the suggested score system for the lung US, diaphragmatic E, and DTF when used as weaning parameters.

Our results showed that a lung ultrasound score cutoff value of 13 had 94.2% sensitivity, 96% specificity, 100% negative predictive value, and 91% positive predictive value. It was also highly correlated with other parameters and had an efficacy of 97.4%, with an area under the curve (AUC) of 0.942. In terms of diaphragmatic E, we found that patients with values above 23 mm had successful weaning, while those below 12 mm had failed weaning. For values between 12 mm to 23 mm, successful weaning was seen in 7 cases from group A (SW) and 3 cases from group B (FW). The cutoff value of 11 mm had 84.5% sensitivity, 100% specificity, 95.5% negative predictive value, and 100% positive predictive value. It was also significantly correlated with other parameters, such as rapid shallow breathing index (RSBI) and maximum inspiratory pressure (MiP), and had an efficacy of 96.9%, with an AUC of 0.845. Finally, our results for DTF showed that all patients with values above 30% had successful weaning, while those with values below 28% had failed weaning. Patients with values between 28% and 30% had 5 successful and 2 failed weaning cases. The cutoff value of 27% had 89.9% sensitivity, 100% specificity, 96.1% negative predictive value, and 100% positive predictive value. It was also significantly correlated with RSBI and MiP and had an efficacy of 98.2%, with an AUC of 0.899.

ICU patients have to go through a challenging weaning procedure with a 20% failure rate, according to studies [11]. The choice to begin the weaning process is based on several indicators and parameters, primarily the respiratory mechanics and arterial blood gases, with all of these factors indirectly reflecting the diaphragmatic function. A poor weaning choice might result in increased death rates, longer ICU stays, and cardio-respiratory discomfort due to a high failure rate. Furthermore, delaying weaning decisions raises the risk of diaphragmatic atrophy and infections linked to ventilator use [12,13]. The diaphragmatic muscle, the primary breathing muscle, can be directly visualized and assessed at the bedside with ultrasound, which is routinely available in the intensive care unit. This information can be used to predict the success of the weaning process. In our investigation, 13 patients (representing 26 percent of the study group) had a failed weaning experiment and were re-intubated and mechanically ventilated within 48 hours. This nearly aligns with the findings of Esteban et al. Failure rates were found to be roughly 20%, 26.7%, and 23.3%, respectively, by Saeed et al. and Baess et al. [2,14,15]. Ferrari et al.'s 63% failure rate [16] raises doubts about this. This is explained by a nonuniform rule in the research population selection, which may have an impact on the weaning process's outcome. There are several reasons for mechanical ventilation in addition to varying ventilation periods prior to the process's start. While M-mode was easier to utilize than B-mode when dealing with noncooperative ICU patients, we used it to measure the diaphragmatic E and to estimate the degree of movement. Several authors, including Umbrello et al., also employed M-mode. In their respective studies, Baess et al. and Boussuges et al. examine how M-mode is used to assess diaphragmatic mobility in 210 healthy people [1,15,17].

However, other authors have examined mobility using B mode, such as Saeed et al. [14], whose study showed that non-ICU patients could easily use B mode to assess diaphragmatic movement. Table 4 shows the correlation between our results and a variety of weaning characteristics, such as blood gases and respiratory mechanics, with RSBI being one of the metrics that the other authors used the most frequently for comparison [1,14,15].  The RSBI in the current study varied from 51 to 98 breaths/min/L between group A (SW) with an average value of 71.97, and from 104 to 124 breaths/min/L between group B (FW) with an average value of 113.5. According to Saeed et al., patients who successfully weaned had an average RSBI of 91, but patients who failed to wean had an average RSBI of 123.6 [14]. Similar to several earlier trials [16,14,15], DTF, E, and lung US demonstrated significant to high significant connection with the other parameters, including the arterial blood gases and the respiratory mechanics, primarily the RSBI and MiP. With 84.5% sensitivity and 100% specificity, the cut-off value in the current investigation was 11 mm Diaphragmatic E. This is in line with numerous writers who, with varying degrees of sensitivity and specificity, reported using 10–11 mm Diaphragmatic E as a cut-off value in the assessment of the weaning outcome. In contrast to Baess et al., who discovered 69.5% sensitivity and 71.4% specificity, Saeed et al. revealed 86.4% sensitivity and 87.5% specificity. Additionally, Jiang et al. found sensitivity and specificity of 84% and 83%, respectively [14,15,18,19]. 

In our investigation, the DTF cut-off value of 27% demonstrated 89.9% sensitivity and 100% specificity. This is comparable to the 30% DTF cut-off value published by Baess et al. and Di Nino et al., respectively, with a sensitivity of roughly 69.57% and 88% and specificity of roughly 71.43% and 71% [15,20]. Ferrari et al. [16] found a higher cut-off value of 36% with 82% sensitivity and 88% specificity, which raises questions about this. A lower cut-off value of 20% was also discovered by Umbrello et al. [1].  All agree that E and DTF are reliable predictors of weaning outcomes, notwithstanding some slight variations in the diagnostic validity results when compared to earlier experiments. With greater sensitivity, effectiveness, and an improved AUC score in line with Umbrello et al. and Baess et al., the DTF outperformed E in terms of reliability [1,15]. Additionally, the results of the lung ultrasound were in line with the findings of Caltabeloti and Rouby and Soummer et al. [21, 22]. Ultimately, a high sensitivity and specificity ultrasonography score was produced, which is comparable to the other weaning characteristics and can be useful during the weaning trials. Ultrasonography is a quick, non-invasive, and extensively accessible diagnostic tool. The primary constraints, however, were the operator-dependent technique and the limits of the ultrasound technology, which included the existence of pneumothorax and the inability to use the optimal window for diaphragm visualization due to morbid obesity.

Comparing diaphragmatic and lung ultrasonography to other conventional indices like blood gases and respiratory mechanics, these methods offer fast, non-invasive indicators for the weaning process with highly accurate results. As a result, they might be employed as predictive parameters to evaluate the outcome of the weaning process.

1. Umbrello M, Formenti P, Longhi D, 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.
2. Esteban A, Frutos F, Tobin MJ, et al. Comparison of four methods of weaning patients from mechanical ventilation. Spanish Lung Failure Collaborative Group. N Engl J Med 1995;332:345-50.
3. Llamas-Alvarez AM, Tenza-Lozano EM, Latour-Perez J. Diaphragm and Lung Ultrasound to Predict Weaning Outcome: Systematic Review and Meta-Analysis. Chest. Dec 2017;152(6):1140-1150.
4. Antonio ACP, Teixeira C, Castro PS, et al. Behavior of lung ultrasound findings during spontaneous breathing trial. Revista Brasileira de terapia intensiva. Jul-Sep 2017;29(3):279-286.
5. Bouhemad B, Mongodi S, Via G, Rouquette I. Ultrasound for “lung monitoring” of ventilated patients. Anesthesiology. Feb 2015;122(2):437-447.
6. Tenza-Lozano E, Llamas-Alvarez A, Jaimez-Navarro E, Fernandez-Sanchez J. Lung and diaphragm ultrasound as predictors of success in weaning from mechanical ventilation. Critical ultrasound journal. Jun 18 2018;10(1):12.
7. Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med 1985;13(10):818-829.
8. Ferreira FL, Bota DP, Bross A, M´elot C, Vincent JL Serial evaluation of the SOFA score to predict outcome in critically ill patients. Jama 2001;286(14):1754-1758.
9. Saenger AK, Rodriguez-Fraga O, Ler R, et al. Specificity of B-type natriuretic peptide assays: cross-reactivity with different BNP, NTproBNP, and proBNP peptides. Clin Chem 2017;63(1):351–358.
10. Soummer A, Perbet S, Brisson H, et al. The lung ultrasound study group: ultrasound assessment of lung aeration loss during a successful weaning trial predicts post-extubation distress. Crit Care Med 2012;40:2064–72.
11. Epstein SK. Extubation. Respir Care 2002;47(4):483–92.
12. Funk GC, Anders S, Breyer MK, et al. Incidence and outcome of weaning from mechanical ventilation according to new categories. Eur Respir J 2010;35 (1):88–94.
13. Hudson MB, Smuder AJ, Nelson WB, et al. Both high level pressure support ventilation and controlled mechanical ventilation induce diaphragm dysfunction and atrophy. Crit Care Med 2012;40(4):1254–60.
14. Saeed A, El Assal G, Ali TM, et al. Role of ultrasound in assessment of diaphragmatic function in chronic obstructive pulmonary disease patients during weaning from mechanical ventilation. Egypt J Bronchol 2016;10:167–72.
15. Baess A, Abdallah TH, Emara DM, et al. Diaphragmatic ultrasound as a predictor of successful extubation from mechanical ventilation: thickness, displacement, or both? Egypt J Bronchol 2016;10:162–6.
16. Ferrari G, De Filippi G, Elia F, et al. Diaphragm ultrasound as a new index of discontinuation from mechanical ventilation. Crit Ultrasound J 2014;6:8.
17. Boussuges A, Gole Y, Blanc P. Diaphragmatic motion studied by m-mode ultrasonography: methods, reproducibility, and normal values. Chest 2009;135(2):391-400.
18. Jiang JR, Tsai TH, Jerng JS, et al. Ultrasonographic evaluation of liver/spleen movement and extubation outcome. Chest 2004;126(1):179-85.