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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 35  |  Issue : 2  |  Page : 660-666

Role of ultrasound assessment of parasternal intercostal muscle thickness during weaning from mechanical ventilation


1 Department of Anesthesiology, Intensive Care, and Pain Management, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Critical Care Medicine, National Heart Institute, Giza, Egypt

Date of Submission21-Sep-2021
Date of Decision03-Nov-2021
Date of Acceptance07-Nov-2021
Date of Web Publication27-Jul-2022

Correspondence Address:
Muhammad A Alghorayeb
Shanawan, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_176_21

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  Abstract 


Background
A spontaneous breathing trial (SBT) is a major diagnostic tool to predict successful extubation in patients. Several factors may lead to weaning failure, including respiratory muscle dysfunction. In cases with diaphragmatic dysfunction, there is recruitment of the extradiaphragmatic muscles, including parasternal intercostal muscles.
Objectives
To study the role of ultrasound assessment of parasternal intercostal muscle thickness during weaning from mechanical ventilation.
Patients and methods
This was a prospective observational study carried out on 40 mechanically ventilated patients, who were clinically stable to undergo a SBT. Parasternal intercostal muscle ultrasound was performed before the start of the SBT. Parasternal intercostal muscle thickness was measured at the end of inspiration (Tic-max) and at the end of expiration (Tdi-min), and then parasternal intercostal muscle thickness fraction (TFic%) was calculated.
Results
The parasternal intercostal muscle thickness fraction (TFic%) was significantly higher in patients who passed the SBT successfully (23.45 ± 7.04 vs. 7.38 ± 4.33%, P < 0.001). With a cut off value of more than 11.58%, the parasternal intercostal thickness fraction (TFic%) achieved 86.96% sensitivity and 100% specificity (area under the curve = 0.980; P < 0.001).
Conclusion
Ultrasonographic evaluation of the parasternal intercostal muscles using the thickness indices could be a good predictor of SBT outcome.

Keywords: intercostal muscles, respiratory muscles, spontaneous breathing, ultrasonography, ventilator weaning


How to cite this article:
Hassan GA, Sultan WE, Habeeb RM, Alghorayeb MA. Role of ultrasound assessment of parasternal intercostal muscle thickness during weaning from mechanical ventilation. Menoufia Med J 2022;35:660-6

How to cite this URL:
Hassan GA, Sultan WE, Habeeb RM, Alghorayeb MA. Role of ultrasound assessment of parasternal intercostal muscle thickness during weaning from mechanical ventilation. Menoufia Med J [serial online] 2022 [cited 2024 Mar 28];35:660-6. Available from: http://www.mmj.eg.net/text.asp?2022/35/2/660/352135




  Introduction Top


Critically ill patients experience atrophy of various muscles, including respiratory muscles[1]. Respiratory muscle dysfunction seems to occur much more rapidly than general limb muscles[2],[3].

Many factors contribute to this problem in the ICU. These factors include inflammation, immobilization, malnutrition, hyperglycemia, electrolyte disturbance, medication, and mechanical ventilation. Mechanical ventilation by itself may lead to sustained muscle loss, resulting in respiratory muscle dysfunction and a poor clinical outcome[4],[5].

The work of the parasternal intercostal and neck muscle is known to increase in the case of diaphragm dysfunction or increased respiratory load[6],[7].

The timing of extubation is critical. Approximately 20% of mechanically ventilated patients have difficult weaning, and weaning trials account for more than 40% of ICU stay time[8].

One of the most accurate predictors of weaning failure is the rapid shallow breathing index (RSBI). However, RSBI less than 105 had variable sensitivity and specificity[9].

Recently, monitoring of the respiratory muscle function during the weaning process gained popularity. The use of ultrasound is a simple, noninvasive, and safe bedside imaging technique that provides a direct visualization of the respiratory muscles and their function[10],[11].

The parasternal intercostal muscle ultrasound could help in the assessment of the respiratory capacity/load balance, and respiratory muscle function monitoring is therefore considered a weaning process tool[12].

The aim of this work was to study the role of ultrasound assessment of parasternal intercostal muscle thickness during weaning from mechanical ventilation.


  Patients and methods Top


This was a prospective observational study that was carried out on 40 mechanically ventilated patients, who were recruited from the ICUs of Menoufia University Hospital from July 2020 to April 2021 and after approval of the medical ethics committee. All patients who were invasively mechanically ventilated for up to 24 h and were ready to undergo a spontaneous breathing trial (SBT) were included. Patients were recruited 6–24 h before the first weaning trial. Informed consent was obtained from the patients' health-care proxy.

Patients were ready for SBT if they were alert, afebrile, had a fraction of inspired oxygen (FiO2) of less than 50%, positive end-expiratory pressure level (PEEP) less than or equal to 8 cmH2O, PaO2/FiO2 more than 200, pH more than or equal to 7.35 and less than or equal to 7.45, respiratory rate (RR) less than or equal to 35 breaths/min, and were hemodynamically stable in the absence of vasopressors.

The exclusion criteria were as follows: pregnancy, age less than 18 years, surgical dressings near or over the sternum which would preclude the ultrasound examination, underweight patients (BMI <18.5 kg/m2), morbidly obese patients (BMI ≥40 kg/m2), and primary neuromuscular diseases.

All enrolled patients were ventilated under pressure support ventilation with a PEEP of 5 cmH2O, and pressure support was set to reach a tidal volume of 6–8 ml/kg of predicted body weight. Then, a 30-min SBT was performed under a pressure support of 7 cmH2O and PEEP set to zero was performed. The SBT was defined as successful if patients could clinically tolerate the 30-min period[12].

SBT was considered failed if the patients experience any of the following: tachypnea (RR >35 breaths/min or increased by ≥50% from baseline), hemodynamic instability (heart rate >140, systolic blood pressure >180 or increased by 20%, or systolic blood pressure <90 mmHg), hypoxemia (PaO2 ≤50–60 mmHg on FiO2 ≥0.5 or SaO2 <90%) or acidosis (pH < 7.32 or a decrease in pH ≥0.07 pH units), change in mental status (agitation, anxiety, or depressed mental status), discomfort, diaphoresis, or cyanosis, and signs of increased work of breathing[13].

Parasternal intercostal ultrasound was performed while patients were ventilated under pressure support ventilation before the start of the SBT.

Ultrasound was performed using SonoScape E1Exp Portable Color Doppler Ultrasound System, Sonoscape Medical Corp., Shenzhen, China.

A 10–15 MHz linear array probe was applied perpendicular to the anterior surface of the chest at the level of the second intercostal, cutting the ribs longitudinally, ∼6–8 cm from the lateral sternal edge with a window visualizing the second and third ribs. The second parasternal intercostal muscle was identified as a biconcave three-layered structure: The muscle echotexture is located between two linear hyperechoic membranes that run from adjacent ribs [Figure 1][12].
Figure 1: M-mode of intercostal muscle thickness (Tic) at end inspiration and end expiration using SonoScape E1Exp portable ultrasound.

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By using M-mode, the ultrasound beam cut perpendicularly through the muscle's midsection [Figure 1]. On frozen M-mode images, the thickness of the parasternal intercostal muscle was measured at the end of expiration and the end of inspiration. The fractional increase in thickness at the end of inspiration was used to calculate the parasternal intercostal muscle thickening fraction (parasternal intercostal muscle thickening = end-inspiration thickness − end-expiration thickness/end-expiration thickness)[12]. All measurements were repeated on at least three separate breaths and their average was reported. Ultrasound was performed mostly on the right parasternal intercostal muscle as it is more feasible.

Statistical analysis

Data were collected, tabulated, and then analyzed using IBM SPSS Statistics, version 22 (IBM Corp., Armonk, New York, USA). Normally distributed numerical data was presented as mean and SD, and skewed data as median and interquartile range (IQR). Qualitative data was presented as numbers and percentages. Comparison of normally distributed numerical data was done using the unpaired t test. Skewed data was compared using the Mann–Whitney test. Categorical data was compared using the χ2 test. Receiver-operating characteristic (ROC) curve analysis was used to examine the predictive value of the diaphragmatic ultrasound. A two-sided P value less than 0.05 was considered statistically significant.


  Results Top


During the study period, we evaluated 54 patients eligible for weaning. Ten patients were excluded from the study, three of which had hemodynamic instability, four cases had previously failed SBT, and three had a decreased level of consciousness, one case had brain stem hemorrhage, one case was diagnosed as Guillain Barre syndrome and two cases with morbid obesity. Forty mechanically ventilated patients were enrolled during the study period.

Forty patients underwent their first SBT. The mean age of the study group was 56.43 ± 17.42 years, 29 of them were males and 11 were females. The mean BMI was 29.68 ± 5.98. The mean duration of mechanical ventilation before the first SBT was 6.90 ± 5.20 days. The acute physiology and chronic health evaluation II (APACHE II) score on admission to the ICU (mean = 19.70 ± 9.59) was used to assess the severity of the disease process. The causes of ICU admission were coma, sepsis, shock, acute respiratory failure, postoperative, road traffic accident, acute kidney injury, intracerebral hemorrhage, postictal, and organophosphate poisoning.

The mean parasternal intercostal muscle thickness at the end of expiration (Tic-min) was 3.43 ± 1.40 mm and the mean parasternal intercostal muscle thickness at the end of inspiration (Tic-max) was 3.86 ± 1.45 mm. The parasternal intercostal muscle thickness fraction (TFic%) had a mean of 14.21 ± 9.78%.

According to the SBT outcome, the patients were classified into two groups [Table 1]: the successful SBT group (23 patients) and the failed SBT group (17 patients). The duration of mechanical ventilation was significantly longer in those with failed SBT than those with successful SBT (10.88 ± 5.48 vs. 3.96 ± 2.2 days, P < 0.001, respectively). Also, patients with failed SBT had significantly higher APACHE II score (23.71 ± 10.14 vs. 16.74 ± 8.18, P = 0.021, respectively). All other demographic data did not differ considerably between the patients with successful and failed SBT. According to sex, there was no considerable difference between patients with successful and failed SBT (P = 0.816) [Table 1]. The traditional weaning parameters (RR, tidal volume, RSBI, PaO2/FiO2, and arterial blood gases) did not change considerably according to the SBT outcome [Table 1].
Table 1: Patient characteristics according to the spontaneous breathing trial outcome

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The parasternal intercostal muscle thickness at the end of expiration (Tic-min) was significantly lower in patients with failed SBT (2.64 ± 1 vs. 4.01 ± 1.38 mm, P = 0.001, respectively). Also, the parasternal intercostal muscle thickness at the end of inspiration (Tic-max) was significantly lower in patients with failed SBT (3.26 ± 1.3 vs. 4.29 ± 1.43 mm, P = 0.024, respectively) [Table 2]. To assess the changes in thickness, the parasternal intercostal muscle thickness fraction (TFic%) was calculated, and accordingly, it was significantly higher in patients who failed to pass SBT (23.45 ± 7.04 vs. 7.38 ± 4.33%, P < 0.001, respectively) [Figure 2].
Figure 2: Parasternal intercostal muscle thickness fraction (TFic%) according to the spontaneous breathing trial outcome.

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Table 2: Parasternal intercostal muscle ultrasound indices according to spontaneous breathing trial outcome

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To assess the accuracy and best cutoffs of the ultrasound parameters in the prediction of weaning outcome, ROC curves were done [Figure 3].
Figure 3: ROC curves of parasternal intercostal muscle thickness fraction (TFic%), parasternal intercostal muscle thickness at end of inspiration (Tic-max), and parasternal intercostal muscle thickness at end of expiration (Tic-min). ROC, receiver-operating characteristic.

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TFic% with a cutoff value of less than or equal to 11.58% was associated with successful SBT with the best sensitivity and negative predictive value (86.96, 85%, respectively) and high specificity and positive predictive value (100, 100%, respectively) [Table 3].
Table 3: Diagnostic tests of parasternal intercostal muscles ultrasound indices

Click here to view



  Discussion Top


The main finding of this study is that the parasternal intercostal muscle thickness fraction (TFic%) could be used as a predictor of SBT outcome in an opposite way to that of the diaphragmatic thickness fraction.

Ventrally, the external intercostal muscle fibers are replaced by a fibrous aponeurosis, conventionally known as parasternal intercostal muscles. It lies in between the chondrocostal junctions and the sternum. It has an inspiratory action that gradually decreases from the second intercostal space to the fifth one[14],[15].

Inappropriate ventilator assist plays an important role in the development of respiratory muscle injury or even atrophy[7]. This provides a good rationale for monitoring respiratory drive during mechanical ventilation. The gold standard method of respiratory drive monitoring uses a nasogastric catheter to determine the muscular pressure. Also, it can be monitored using electrodes to measure electrical activity of the diaphragm[16],[17]. However, both techniques are invasive. Therefore, it is interesting to investigate the role of extradiaphragmatic inspiratory muscle activity. They are responsive to respiratory load and their electromyogram activity increases in response to lower inspiratory support levels and can be used as a surrogate of respiratory drive[7],[18].

Roesthuis et al.[7] used surface electrodes to record the surface electromyography activity from the extradiaphragmatic inspiratory muscles including the alae nasi, genioglossus, scalene, sternocleidomastoid, and parasternal intercostals. However, the parasternal surface electromyography correlates poorly with the change in diaphragm activity, limiting its use as a surrogate for electrical activity of the diaphragm[7],[19].

Ultrasonography of respiratory muscles was introduced as a new technique for the assessment of respiratory drive. It is a noninvasive bedside tool that is widely available and provides a real-time assessment of muscle contraction. Also, it is feasible, reproducible, and can reliably be used[11].

Dres et al.[12] in their substudy (B) on 16 mechanically ventilated patients used ultrasound to assess the diaphragmatic thickness fraction and parasternal intercostal muscle thickness fraction by applying different pressure support levels. Their results showed a direct relationship between parasternal intercostal muscle thickening fraction and respiratory load. There was a strong correlation between pressure support level and parasternal intercostal muscle thickening (r=−0.61), and this relationship shows that the thickening fraction can assess the load capacity balance in mechanically ventilated patients[12].

This study was carried out to evaluate the role of ultrasound assessment of parasternal intercostal muscle thickness during weaning from mechanical ventilation. We hypothesize that measuring the parasternal intercostal muscle thickening could be helpful during the weaning process.

It was a prospective observational study, carried out on 40 mechanically ventilated patients recruited from the ICUs.

The results of this study showed that 23 (57.5%) patients had successful first SBT and 17 (42.5%) patients failed to pass their first SBT.

Also, the results of this study showed a relatively long period of mechanical ventilation in patients who failed to pass their SBT (10.88 ± 5.48 vs. 3.96 ± 2.2 days), with a strong inverse correlation between the duration of mechanical ventilation and SBT outcome (r=−0.666).

These findings go hand in hand with the results of Liang et al.[20] on 352 mechanically ventilated patients. They assessed the characteristics of patients who fail to pass their first 30-min SBT. They found that patients with weaning failure had a significantly longer duration of mechanical ventilation before the first SBT attempt (5.1 ± 1.8 vs. 4.4 ± 1.8 days)[20].

This is because prolonged mechanical ventilation is one of the outcomes of diaphragm dysfunction, which leads to additional diaphragmatic injury and atrophy. This is known as ventilator-induced diaphragm dysfunction, and it is one of the most common causes of weaning failure[21].

In this study, APACHE II was applied within 24 h of admission of the patient to the ICU as a classification system of the severity of disease. It was found that the APACHE II score was significantly higher in patients who failed to pass SBT (23.71 ± 10.14 vs. 16.74 ± 8.18).

The traditional weaning parameters (arterial blood gases, hemodynamic parameters, PaO2/FiO2%, and RSBI) did not differ considerably regardless of the SBT outcome, as all patients were assessed for readiness for the weaning process before the start of SBT.

The data of this study showed that the mean parasternal intercostal muscle thickness at end expiration (Tic-min) was 3.43 ± 1.40 mm, and the mean parasternal intercostal muscle thickness at end inspiration (Tic-max) was 3.86 ± 1.45 mm. Remarkably, as per this study results, the parasternal intercostal muscle in critically ill patients was thicker than in healthy participants, as reported by Yoshida et al.[22] and Dres et al.[12].

Yoshida et al.[22] used ultrasound to assess the thickness of the intercostal muscles in 12 healthy males. They found that the mean parasternal intercostal muscle thickness at the second intercostal space was 2.17 ± 0.83 mm at rest and 2.62 ± 0.96 mm at maximal inspiration. They concluded that human intercostal muscle thickness can be measured with ultrasound and their thickness increases only in the anterior portions during maximal breathing.

Dres et al.[12] in their substudy (A) performed parasternal intercostal muscle ultrasound on 23 healthy individuals. They found that the mean parasternal intercostal muscle thickness at end expiration was 2.8 (IQR 2.1–3.3 mm) and the mean parasternal intercostal muscle thickness at end inspiration was 2.8 (IQR 2.2–3.4 mm).

However, the parasternal intercostal muscle thickness in this study was close enough to the finding of Wallbridge et al.[23]. They compared the assessment of the parasternal intercostal muscles by ultrasound and computed tomography in 20 stable chronic obstructive pulmonary disease patients. They found that the parasternal intercostal muscle thickness at end inspiration measured by ultrasound was 4.2 mm (IQR 3.3–5.4).

That increase in the parasternal intercostal muscle thickness in critically ill patients may be a result of edema, inflammation, injury, or over-recruitment[12],[24].

In the present study, when comparing patients according to the SBT outcome, we found that parasternal intercostal muscle thickness indices were significantly different between patients according to the success or failure of SBT.

The parasternal intercostal muscle thickness at end expiration (Tic-min) and the parasternal intercostal muscle thickness at end inspiration (Tic-max) were significantly lower in patients with failed SBT (2.64 ± 1 vs. 4.01 ± 1.38 mm; 3.26 ± 1.3 vs. 4.29 ± 1.43 mm, respectively). However, the patients with failed SBT had a significantly higher thickness fraction (TFic%) (23.45 ± 7.04 vs. 7.38 ± 4.33%).

Despite the atrophy of the parasternal intercostal muscles seen in patients who failed to pass SBT, there was a significant increase in their TFic%. Critically ill patients have a high incidence of diaphragmatic dysfunction, causing respiratory failure and prolonged weaning from mechanical ventilation[25]. As a compensatory mechanism, there is recruitment of extradiaphragmatic muscles, including the parasternal intercostal muscles[7].

Umbrello et al[26] in their study on 21 mechanically ventilated patients used esophageal transdiaphragmatic pressure, diaphragm, and parasternal intercostal ultrasonography to estimate the respiratory effort. They found that patients with diaphragm dysfunction had significantly higher parasternal intercostal muscle thickness fraction (TFic%) in comparison to patients without diaphragmatic dysfunction (13.2 ± 9.2 vs. 2.1 ± 1.7%). They concluded that measurement of parasternal intercostal muscle thickening may discriminate between low inspiratory effort and high effort in the presence of a dysfunctional diaphragm.

These data are consistent with the results of Dres et al.[12] substudy (C) on 52 mechanically ventilated patients. They found a significant increase in TFic% in patients with failed SBT [18% (IQR 10–33) vs. 7% (IQR 4–10)].

In this study, ROC curves were done to validate the accuracy of the parasternal intercostal muscle ultrasound parameters. The area under the curve of parasternal intercostal muscle thickness fraction (TFic%) was 0.980, so it has good discriminating capacity, and we can assume that it is a good predictive marker for SBT outcome in critical patients.

The TFic% cutoff value less than or equal to 11.58% was associated with the best sensitivity (86.93%) and specificity (100%) compared with other parasternal intercostal muscle ultrasound parameters.

These findings are consistent with results of Dres et al.[12] in their substudy (C) on 52 mechanically ventilated patients as they found that the best cutoff value of TFic% less than or equal to 9.5% can discriminate the SBT outcome with 91% sensitivity and 72% specificity (area under the curve = 0.88).


  Conclusion Top


Parasternal intercostal muscle ultrasound seems feasible, reproducible, and easily employed. The parasternal intercostal muscle thickness fraction (TFic%) with a cutoff value of more than 11.58% achieved 86.96% sensitivity and 100% specificity. So, assessment of the parasternal intercostal muscle thickness can be a good predictor of the weaning outcome of mechanically ventilated patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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