Ultrasound-Based Abdominal Muscles And Diaphragm Assessment In Predicting Extubation Failure In Patients With Neurointensive Care: A Single-Center Observational Study

doi:10.21203/rs.3.rs-5312255/v1

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Ultrasound-Based Abdominal Muscles And Diaphragm Assessment In Predicting Extubation Failure In Patients With Neurointensive Care: A Single-Center Observational Study

https://doi.org/10.21203/rs.3.rs-5312255/v1

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Background: Extubation in patients with neurocritical care has high rate of failure. Ineffective cough was the variable independently associated with extubation failure, but its quantification remains challenging.

Methods: Patients with primary central nervous system injury under invasive mechanical ventilation (IMV) were included. After a successful spontaneous breathing trial (SBT), abdominal muscles and diaphragm ultrasound was performed under tidal breathing and coughing.

Results: we recruited 98 patients who were receiving IMV and 40 patients were included. Extubation failure occurred in 8 (20%) patients. Rectus abdominis (RA) and internal oblique (IO) muscle showed significantly difference regarding cough thickness (T) and cough thickening fraction (TF) between the extubation success and failure group (P<0.05). The logistic regression analysis suggested cough TFRA, cough TFIO and cough TIOwere the factors associated with extubation outcome (P<0.05). In the receiver operating characteristic analysis, cough TFIO exhibited the strongest predictive value (AUC=0.957, 95% CI:0.8979–1). A threshold of cough TFIO≥34.15% predicted extubation success with a sensitivity of 93.8% and a specificity of 75%.

Conclusion: Abdominal muscles ultrasound was a promising tool to predict extubation for neurocritical care patients.

Trial registration: The study was registered on Chinese Clinical Trial Registry:

ChiCTR2400088210, Registered 13 August 2024 - Retrospectively registered，https://www.chictr.org.cn/bin/project/edit?pid=234150

Health sciences/Risk factors

Health sciences/Medical research/Outcomes research

Neurointensive Care

Extubation prediction

Cough

abdominal muscle ultrasound

Extubation is the final step for patients in intensive care units (ICU) to wean from mechanical ventilation, which is directly related to the patients’ prognosis¹. Due to the reduced level of consciousness and the poor airway protection ability, patients in the neurointensive care units (NICUs) show higher extubation failure (ET), ranging between 20 and 40%². In NICUs, the decision regarding extubation is of critical challenging because both EF and delayed extubation can result in increasing need for tracheostomy and higher mortality^3–6. There are guidelines regarding the weaning of mechanical ventilation¹, but it is a lack of specific international extubation guidelines for the neurocritical care patients.

Extubation in patients with neurocritical care requires a combination of the patient's arousal level, airway protection ability and general clinical signs, based on the ENIO international multi-center prospective study². However, 2020 European Society of Critical Care Medicine expert consensus suggested that the state of consciousness is not a reliable indicator for predicting extubation, while ineffective cough was the variable independently associated with EF⁷. Currently, cough is assessed mainly through the scales in clinical practice, but it is subjective and has a low predictive value, with an OR value of 0.6². Cough peak flow can be used as a surrogate to judge cough strength objectively, but it requires cooperation and its predictive ability is not satisfied^8,9.

Abdominal muscles, as the main driving force for coughing, may be a valuable indicator predicting extubation. Abdominal muscle ultrasound, due to its excellent reproducibility¹⁰, has been used for evaluation before extubation. Schreiber et al. found that the thickening fraction of the transversus abdominis and rectus abdominis muscles were related to expiratory pressure, and that reduced abdominal muscle cough thickening fraction may predict the risk of extubation failure¹¹. However, the subjects in this study were the general ICU population, so the results may not be applicable to neurocritical care patients with a high risk of extubation failure. Spadaro et al proposed that whether abdominal muscle ultrasonography can be used to predict reintubation¹², which may require further research.

This study was designed to determine whether abdominal muscle and diaphragm ultrasonography can predict EF in the NICU.

This prospective observational cohort study was conducted over 8 months (December 2023 to July 2024) in Neurology ICU of a tertiary hospital and was conducted in accordance with the Declaration of Helsinki. After obtaining institutional ethics committee approval, the trial was registered in the Chinese Clinical Trial Registry (ChiCTR2400088210). Informed consent form was signed by the participant’s legal representative.

Eligibility criteria

Subjects included in the study should meet the following criteria: (1) Patients aged 18–80 years admitted to the NICU with planned elective extubation after 48 h of mechanical ventilation. (2) Patients with primary central nervous system injury, including stroke, status epilepticus, infectious and infectious encephalopathy, etc. The exclusion criteria are defined: (1) severe brain stem injury resulting in inability to breathe spontaneously. (2) history of abdominal surgery. (3) uncontrolled respiratory and circulatory diseases, including heart failure, pneumothorax, severe emphysema, pulmonary hypertension, uncontrolled asthma, etc.

Extubation Protocol

Physicians, who were not involved in the study and blinded to the study findings, took the decision for extubation. All patients should meet the following criteria before extubation: hemodynamic stability without vasoactive drug, a successful spontaneous breathing trial (SBT) for at least 30 minutes, a successful cuff leak test, fraction of inspired oxygen (FiO2) < 40%, positive end-expiratory pressure (PEEP) < 5 cmH2O. Patients were followed up for 48 hours after extubation.

Data Collection

The demographic and clinical characteristics (age, sex, diagnosis, intubation method, intubation diameter, duration of mechanical ventilation, weaning and ICU stay) were collected. Ultrasound examination was performed before extubation. All variables were measured three times, and the average was included in the analysis. EF is defined as reintubation or initiation of unplanned non-invasive ventilation within 48h after extubation¹³.

Measurements

The ultrasonography device used in this study was GE LOGIQ E10s with a 10–15 MHz linear probe and a 3.5–5 MHz phased array probe. Ultrasound examination was performed by an experienced and qualified physiotherapist. All measurements were taken with patients in the supine position. To reduce variability, all measurements were taken three consecutive times at the same location and the average was calculated.

Abdominal muscle Ultrasound

A high-frequency (10–15 MHz probe) linear array transducer was placed midway between the 12th rib and the iliac crest along the anterior axillary line for the measurement of external oblique muscle (EO), internal oblique muscle (IO) and transversus abdominis (TrA). Rectus abdominis (RA) was measured with the probe placing 2 to 3 cm above the umbilicus, 2 to 3 cm to the right of the midline¹⁴. Pressure applied to the probe should be kept to a minimum to prevent compression of the abdominal wall, as this may change the thickness of the underlying muscles¹⁴.

Each muscle was first found in B mode, then the thickness is measured in M mode. Abdominal muscle thickness was measured under tidal breathing and coughing. For patients who can cooperate, Patients were asked to cough three times actively as much as possible. For patients who were not cooperative, cough was stimulated by pinching the suprasternal trachea or by inserting a sputum suction tube into airway. Thickness of each muscle was measured at end-inspiratory (Tei) and maximum cough (Tcough), as shown in Fig. 1 and Fig. 2. Muscle thickness is defined as the distance between the inner layers of each muscle, excluding surrounding aponeurosis. Cough Thickening fraction of abdominal muscle (cough TFabd) was computed as the percent change in thickness between end-inspiration and maximum cough (cough TFadb = (Tcough-Tei)/ Tei)×100%).

Diaphragm Ultrasound

Diaphragm excursion is performed using a 3.5–5 MHz phased array probe. The probe is placed below the right costal arch at the midclavicular line, with the direction as perpendicular to the movement direction of the dome roof. The M-mode is then used to display the motion of the anatomical structures along the selected line. Diaphragm excursion (DE) is the vertical distance between the starting point (beginning of inhalation) and the peak point (end of inhalation) and DE-Inspiratory time (s) is the horizontal distance between these two points. DE- contraction speed (cm/s) is the slope of DE and DE-Inspiratory time ¹⁵

Diaphragm thickness measurement is measured with a high-frequency (10-15MHZ) linear array probe, and the probe is placed perpendicular to the long axis of the ribs or parallel to the intercostal space at the 8th to 11th intercostal space in the front or midaxillary line. The diaphragm thickness is recorded at the end of inspiration (Tei) and end of expiration (Tee). The thickening fraction (TF) can be calculated using the M mode (TF = (Tei- Tee) / Tee).

Statistical Analysis

Descriptive statistics include frequency (percentages) for categorical variables and median and interquartile ranges (IQRs) for continuous variables. Chi-squared tests and Mann–Whitney U tests were used to compare categorical variables and continuous variables, respectively. The association between abdominal muscle and diaphragm function and the risk of extubation failure was assessed by using logistic regression. Indicators that are significantly related to extubation failure were assessed by using receiver operating characteristic (ROC) curve analysis to discriminate between extubation success/failure. The indicators which have the largest the area under the curve (AUC) was set the cutoff point based on The Youden Index. All tests were two-sided, and P values less than 0.05 were considered statistically significant. All statistical analyses were performed by using SPSS Statistics 26.0.

According to the extubation failure rate in patients with neurointensive care is around 20%², A sample of 8 from the positive group and 32 from the negative group achieves 81% power to detect a difference of 0.3000 between the area under the ROC curve (AUC) under the null hypothesis of 0.8000 and an AUC under the alternative hypothesis of 0.5000 using a two-sided z-test at a significance level of 0.050.

Of the 98 patients who were mechanically ventilated during the study period, 76 were extubated after 48 h of ventilation. Among them, 36 patients were excluded for reasons given in Fig. 3. Of the 40 patients included in the analysis, eight (20%) patients failed extubation. The demographic variables were similar between patients who failed extubation and those who did not, as depicted in Table 1. The intubation method (oral or nasal) and the intubation diameter were not the factors influencing extubation outcome. The predominant neurological illnesses in the cohort were Storke (N = 31). The duration of mechanical ventilation, weaning and ICU stay was significantly higher in the extubation failure group (P < 0.05).

Table 1

Demographic and clinical characteristics
Parameters	Extubation success (n = 32)	Extubation failure (n = 8)	P value
Age in years, median (IQR)	61.7 (51.21-75)	67.5 (54–82)	0.54
Sex (male/female), n (%)	21/11 (65.6/34.4)	3/5 (37.5/62.5)	0.294
Intubation method (Oral/nasal), n (%)	30/2 (93.8/6.2)	7/1 (87.5/12.5)	0.548
Intubation diameter	7.28 (7-7.5)	7.25 (7-7.5)	0.754
Diagnosis, n (%)			0.13
Storke	27 (84.37)	4 (50)
Status epilepticus	2 (6.25)	1 (12.5)
Intracranial infection	2 (6.25)	3 (37.5)
Mitochondrial encephalomyopathy	1 (3.13)	0(0)
Duration of mechanical ventilation in hours, median (IQR)	84.7 (42.75)	248.25 (94.25-375.25)	0.011
Duration of weaning in hours, median (IQR)	101 (47-143.5)	315.5 (222.75-399.75)	< 0.001
Duration of ICU stay in hours, median (IQR)	224.75 (111.75-307.75)	533.63 (471.25-627.75)	< 0.001
IQR interquartile range

Based on the diaphragm and abdominal muscle ultrasound evaluation before extubation, RA and IO muscle showed significantly difference between the groups regarding cough thickness and cough thickening fraction, as depicted in Table 2 and Fig. 4. The logistic regression analysis for all variables suggested cough TFRA, cough TFIO and cough TIO were the factors associated with extubation outcome (P < 0.05), as shown in Table 3. In the receiver operating characteristic analysis, cough TFIO exhibited the strongest predictive discrimination for extubation failure (AUC = 0.957, 95% CI:0.8979–1). Cough TFRA and cough TIO also showed favorable predictive ability (AUC = 0.8945, 95% CI: 0.797–0.9921; AUC = 0.7617, 95% CI:0.5936–0.9298, respectively), as shown in Fig. 5.

Table 2

Characteristic of Diaphragm and abdominal muscle ultrasound evaluation
Parameters	Extubation success (n = 32)	Extubation failure (n = 8)	P value
DE-Tidal (cm), median (IQR)	1.32 (0.96–1.63)	1.24 (0.99–1.5)	0.839
DE-Inspiratory time (s), median (IQR)	1.14 (0.93–1.29)	1.00 (0.91–1.16)	0.398
DE-Contraction speed (cm/s), median (IQR)	1.20 (0.80–1.48)	1.15 (0.95–1.37)	0.933
DTF (%), median (IQR)	29.31 (19.41–42.23)	38.51 (19.29–60.38)	0.636
TeiRA (mm), median (IQR)	7.01 (5.6–8.68)	6.33 (4.69-8.00)	0.437
Cough TRA (mm), median (IQR)	10.18 (8.23–12.54)	8.08 (6.20–9.70)	0.044
Cough TFRA (%), median (IQR)	49.15 (38.67–56.05)	29.40 (23.97–34.37)	0.001
TeiEO (mm), median (IQR)	3.33 (2.68–4.14)	2.72 (2.14–3.25)	0.081
Cough TEO (mm), median (IQR)	5.29 (3.71–5.95)	4.10 (3.15–4.94)	0.101
Cough TFEO (%), median (IQR)	63.24 (22.92–89.20)	48.85 (33.06–61.24)	0.565
TeiIO (mm), median (IQR)	5.00 (3.83–6.21)	4.72 (2.60–6.63)	0.660
Cough TIO (mm), median (IQR)	8.61 (6.95–10.09)	6.04 (3.62–8.35)	0.023
Cough TFIO (%), median (IQR)	82.04 (50.91-111.12)	29.37 (22.93–37.50)	< 0.001
TeiTrA (mm), median (IQR)	2.16 (1.89–2.47)	2.21 (1.34–2.76)	0.648
Cough TTrA (mm), median (IQR)	4.90 (3.57–5.63)	4.95 (2.70–7.37)	0.946
Cough TFTrA (%), median (IQR)	130.05 (68.17-172.24)	126.97 (92.81-169.42)	0.973
IQR interquartile range; DE diaphragm excursion; DTF diaphragm thickening fraction; T thickness; TF thickening fraction; ei end-inspiratory; RA rectus abdominis; EO external oblique muscle; IO internal oblique muscle; TrA transversus abdominis

Table 3

logistic regression analysis to predict extubation failure
Parameters	OR (95% CI)	P value
DE-Tidal (cm)	0.759 (0.176–3.267)	0.712
DE-Inspiratory time (s),	0.267 (0.013–5.588)	0.394
DE- Contraction speed (cm/s),	0.820 (0.182–3.698)	0.797
DTF(%),	1.026 (0.985–1.068)	0.221
TeiRA (mm),	0.823 (0.537–1.262)	0.371
Cough TRA (mm),	0.675 (0.450–1.010)	0.056
Cough TFRA (%),	0.859 (0.768–0.961)	0.008
TeiEO (mm),	0.451 (0.174–1.171)	0.102
Cough TEO (mm),	0.665 (0.388–1.140)	0.138
Cough TFEO (%),	0.990 (0.968–1.013)	0.388
TeiIO (mm),	0.929 (0.618–1.395)	0.722
Cough TIO (mm),	0.692 (0.494–0.969)	0.032
Cough TFIO (%),	0.847(0.742–0.968)	0.015
TeiTrA (mm),	1.153 (0.318–4.179)	0.829
Cough TTrA (mm),	1.010 (0.700-1.457)	0.958
Cough TFTrA (%),	0.999 (0.988–1.011)	0.911
DE diaphragm excursion; DTF diaphragm thickening fraction; TeiRA rectus abdominis thickness at end-inspiratory; T thickness; TF thickening fraction; ei end-inspiratory; RA rectus abdominis; EO external oblique muscle; IO internal oblique muscle; TrA transversus abdominis

According to the Youden Index, the cutoff point of cough TFIO that resulted in the highest discriminative capacity was ≥ 41.52%, yielding a sensitivity of 90.6% and a specificity of 100%. However, in the clinical practice of intensive care medicine, an indicator with higher sensitivity—that can better detect those patients with a greater chance of extubation success—may be more useful. Therefore, we adjusted the cutoff point to ≥ 34.15%, and the resultant sensitivity was 93.8%, specificity was 75%.

In a monocentric prospective cohort including neurologically critical patients under IMV, we found that quantitative assessment of cough using ultrasound was a promising tool to predict extubation in NICU.

Effective cough is a prerequisite for successful extubation¹⁶ and Ineffective cough was the variable independently associated with extubation failure¹⁷. In our study, we used abdominal muscle ultrasound to measure its thickness and thickening fraction under coughing to compare the differences between patients with successful and failed extubation. The result showed that Cough TFIO, Cough TFRA and Cough TIO have high predictive value for extubation. Cough TFIO has the largest AUC value among all variables, and its value ≥ 34.15% predicts successful extubation. Schreiber et al. found that the thickening fraction of IO and RA were related to expiratory pressure, and reduced abdominal muscle thickening scores during coughing were associated with a higher risk of weaning failure¹¹. This may explain the high predictive value of the internal oblique and rectus abdominis muscles. Abdominal muscles are the final critical step in cough reflex and determine whether secretions can be effectively removed¹⁸, which directly affects patient's ability to protect airway and extubation outcome¹⁹. Despite the importance of abdominal muscles, clinical research evidence is sparse. Some scholars urge not to ignore the role of expiratory muscles anymore²⁰. Therefore, further research is worth exploring whether early intervention on abdominal muscles can reduce the extubation failure rate in neurocritical care patients.

Diaphragm ultrasound can reflect diaphragm function but cannot predict extubation¹⁷. In our study, we found that diaphragm excursions and contraction speed measured during tidal breaths were lower in EF patients, compared with patients who were successfully extubated. However, the difference is not significant and cannot be used as an indicator to predict extubation. This result was also confirmed in a study on prediction of extubation in patients with neurocritical care⁸ and a multicenter study¹⁷. Diaphragm ultrasound may be more valuable before SBT and it can reflect whether the patient has the ability to breathe spontaneously^21,22. However, for patients who have passed the SBT, diaphragm function is no longer the determining factor for extubation. Instead, patient's adequate expectoration ability should be considered¹⁷.

Our research has several limitations. The sample size is limited and it is a single-center study, so the findings need to be confirmed in a large cohort. This experiment did not compare cough peak flow, and this work needs to be completed in the future.

In a monocentric prospective cohort, we found that abdominal muscles ultrasound was a promising tool to predict extubation for neurocritical care patients, especially for rectus abdominis and internal oblique muscles. Those results should be validated in a larger cohort.

Ethics approval and consent to participate

This study got the approval of the local ethics committee of The First Affiliated Hospital of Fujian Medical University, Fuzhou, China (MRCTA, ECFAH of FMU [2024] 380). The contacts of the ethics committee are: 0086–0591-87,981,028, [email protected], and No.20, Chazhong Road, Fuzhou, Fujian Province, China. Participants’ legal representative sign an informed consent form before this study.

Consent for publication

All results are reported as group-level statistics (e.g., means, standard deviations) and tracing to the person level is not possible. The manuscript does not contain any person’s individual data in any form.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors have no competing interests as defined by BMC, or other interests that might be perceived to influence the results and/or discussion reported in this paper.

Funding

The study is funded by the Startup Fund for Scientific Research of Fujian Medical University (2021QH1099) and Rehabilitation Medicine Center Open research fund(2023YKFKF-04). The funding body has no influence on the design of the study, data collection, analysis of data, interpretation of data, or writing the manuscript.

Author’s contribution

XQ designed the study and drafted the manuscript. CJC and BHY collected the clinical data. LL analyzed data. ZQW and JN critically revised the manuscript and contributed in experimental design. All authors read and approved the final manuscript.

Acknowledgements

Not applicable.

Conflict of Interest

The authors declare that they have no competing interests.

AUC Area under the curve

DE diaphragm excursion

DTF diaphragm thickening fraction

ei end-inspiratory

RA rectus abdominis

EO external oblique muscle

IO internal oblique muscle

TrA transversus abdominis

IMV Invasive mechanical ventilation

IQR Inter‑quartile range

ICU Intensive care unit

EF Extubation failure

SBT Spontaneous breathing trial

NIV Non‑invasive ventilation

T thickness

TF thickening fraction

ROC Receiver operating characteristic

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Ultrasound-Based Abdominal Muscles And Diaphragm Assessment In Predicting Extubation Failure In Patients With Neurointensive Care: A Single-Center Observational Study

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Abstract

Figures

Introduction

Methods

Eligibility criteria

Extubation Protocol

Data Collection

Measurements

Abdominal muscle Ultrasound

Diaphragm Ultrasound

Statistical Analysis

Results

Discussions

Conclusion

Declarations

Abbreviations

References

Additional Declarations

Status:

Version 1