Diaphragmatic Ultrasound Parameters as Predictors of Weaning Success in Cervical Spinal Cord Injury

Introduction

Cervical spinal cord injury refers to cervical spinal cord damage caused by displacement of the cervical vertebrae or the intrusion of foreign bodies such as bone fragments into the spinal canal. It is primarily attributed to trauma, including traffic accidents, falls, and sports injuries [1]. It can lead to partial or complete loss of sensory and motor function below the injury site, causing tetraplegia and serious complications like respiratory failure and infections [2]. Damage to intercostal and phrenic nerves weakens respiratory muscles, leading to dyspnea and dependence on ventilator support. Weaning from mechanical ventilation, the process of restoring spontaneous breathing, is critical for recovery. However, premature weaning increases complications and mortality, while prolonged ventilation raises the risk of ventilator-associated pneumonia [3]. Therefore, accurately predicting the optimal weaning time is vital for CSCI patients. The diaphragm is the main respiratory muscle, and its dysfunction is a key factor in weaning failure. Bedside ultrasound, with its advantages of safety, mobility, and non-radiation, enables real-time assessment of diaphragmatic function by measuring changes in thickness and movement amplitude [4].

Recent studies have demonstrated that bedside ultrasound parameters, such as diaphragm excursion (DE), diaphragm thickening fraction (DTF), and diaphragm contraction velocity (DCV), can reflect diaphragmatic function and are associated with ventilator weaning outcomes in critically ill patients; however, most previous research has focused on patients with chronic obstructive pulmonary disease (COPD) or general intensive care unit (ICU) populations, and evidence specifically targeting cervical spinal cord injury patients remains limited [5–7]. In addition, knowledge gaps persist regarding the comparative predictive value of different ultrasonographic indices in this unique clinical context.

Given the specific pathophysiological features of cervical spinal cord injury, particularly phrenic nerve involvement and diaphragmatic dysfunction, more targeted research is warranted. Therefore, bedside ultrasound, with its advantages of flexible mobility, non-radiation, and harmlessness, can be applied to assess the diaphragmatic function through direct observation and measurement of thickness variation and motion amplitude of the diaphragm [8]. This study aimed to expand on existing research by focusing exclusively on cervical spinal cord injury patients and comprehensively evaluating multiple ultrasound parameters for their predictive efficacy. Our study focused on analyzing the utility of bedside ultrasound monitoring of diaphragmatic function in predicting the ventilator weaning outcomes of patients with cervical spinal cord injury.

Material and Methods

SUBJECTS:

A prospective study was designed to incorporate 136 patients with cervical spinal cord injury admitted to and treated in the hospital between December 2021 and December 2023 as the subjects. The study was approved by the Ethics Committee of the 901st Hospital of PLA Joint Logistics Support Force (Approval No. IACUC-20211123), and was conducted in accordance with the principles of the Declaration of Helsinki and relevant national guidelines. The family members of the patients signed the informed consent form. The sample size was determined based on the available eligible patients during the study period; a formal sample size calculation was not performed. Inclusion criteria were: 1) patients definitely diagnosed by relevant guidelines and imaging examination, 2) those aged ≥18 years old, 3) those with cervical spinal cord injury of American Spinal Injury Association (ASIA) grade A–D, 4) those treated with invasive mechanical ventilation for >48 h [9,10], and 5) those meeting the ventilator weaning criteria for spontaneous breathing trial (SBT) and recommended to remove the ventilator [11]. The exclusion criteria were: 1) patients with respiratory tract malformation or obstruction, 2) those with intra-abdominal hypertension, 3) those complicated with malignant tumors, 4) those with a history of chronic pulmonary diseases including chronic obstructive pulmonary disease, bronchiectasis, and asthma, 5) those complicated with severe cardiac, hepatic or renal dysfunction, and 6) those with severe coagulation disorders. The detailed participant flow is illustrated in Figure 1.

COLLECTION OF GENERAL DATA:

The age, sex, body mass index (BMI), Acute Physiology and Chronic Health Evaluation II (APACHE II) score (it involved 3 aspects of age, acute physiology [12], and long-term health, with a total score of 0–71 points, with a higher score indicated greater severity), coronary heart disease, hypertension, diabetes mellitus, ventilator-assisted ventilation time, heart rate (HR), respiratory rate, arterial partial pressure of carbon dioxide (PaCO2), partial pressure of oxygen (PaO2), and oxygenation index [oxygenation index=PaO2/fraction of inspired oxygen (FiO2)] were collected.

BEDSIDE ULTRASOUND MONITORING OF DIAPHRAGMATIC FUNCTION:

Bedside ultrasound monitoring of diaphragmatic function was carried out before weaning. All patients underwent diaphragmatic ultrasound evaluation at a standardized time point, within 30 min before the initiation of SBT. Patients with cervical spinal cord injury received ultrasonography in the supine position using the EX20 color Doppler ultrasonic diagnostic system (Shenzhen Lanmage Medical Technology Co., Ltd., China), with the head of the bed elevated by 30°. Using M-mode ultrasound, the probe (frequency: 1.2–5.0 MHz) was placed at the intersection point between the midclavicular line and the inferior margin of costal arch to measure the diaphragmatic motion, during which the liver or spleen was set as the acoustic window, the acoustic beam was pointed to the diaphragmatic dome, and the sample line was perpendicular to the diaphragmatic dome (Figure 2). The vertical distance of the diaphragm between the end of maximal inspiration and the end of calm expiration was calculated as the diaphragm excursion (DE). Next, the probe (3.0–12.0 MHz in frequency) in M mode was placed on the anterior axillary line between the 8th and 9th ribs, and the sample line was perpendicular to the diaphragm, to determine the diaphragmatic thickness at the end of expiration (DTee) and diaphragmatic thickness at the end of inspiration (DTei). Finally, we computed the following parameters: diaphragm thickening fraction (DTF)=(DTei-DTee)/DTee×100%, diaphragm contraction velocity (DCV)=DE/contraction time, and diaphragmatic-shallow rapid breathing index (D-RSBI)=respiratory rate/right DE. All the above ultrasound parameters were measured 3 times to obtain the average values.

To ensure reproducibility, the measurements were independently performed by 2 experienced sonographers, who were blinded to the patient outcome groups throughout the study. Interobserver variability was assessed, and the intraclass correlation coefficient (ICC) was calculated to evaluate measurement consistency, with ICC >0.75 considered indicative of good reliability.

EVALUATION OF VENTILATOR WEANING OUTCOMES AND GROUPING METHODS:

According to relevant weaning criteria [13], weaning success was defined as patients having spontaneous respiration for more than 48 h after tracheal extubation, stable vital signs, and required no mechanical ventilation again, and weaning failure was defined as patients needing mechanical ventilation support again due to SBT failure or inability to maintain spontaneous respiration within 48 h after extubation or died within 48 h after weaning. Finally, the patients were divided into a weaning failure group [42 (30.88%)] and a weaning success group [94 (69.12%)] based on the ventilator weaning outcomes.

STATISTICAL ANALYSIS:

We used SPSS 25.0 software for statistical analysis. The format of mean±standard deviation (χ̄± s) was selected to express the measurement data, and the independent-samples t test was performed for comparison between groups. The count data are represented as percentages [n (%)] and examined by the χ² test. ROC curves were plotted, and the areas under the curve (AUCs) were calculated to explore the predictive values of DE, DTF, DCV, and D-RSBI for the ventilator weaning outcomes of patients with cervical spinal cord injury, with AUC <0.5, 0.5≤ AUC <0.7, 0.7≤ AUC <0.9, and AUC ≥0.9 indicating no value, low value, moderate value, and high value, respectively. R4.1.0 statistical software was applied to plot the decision curves of DE, DTF, DCV, and D-RSBI for predicting ventilator weaning outcomes, with the high-risk threshold as the abscissa and the net benefit as the ordinate. To assess reproducibility, interobserver variability of ultrasound parameters was quantified by calculating the ICC using a 2-way random-effects model. An ICC value greater than 0.75 was interpreted as good agreement, and values above 0.90 as excellent agreement. The threshold of significance was determined as α=0.05.

Results

GENERAL DATA:

The APACHE II score and respiratory rate were higher, and the ventilator-assisted ventilation time was longer in the weaning failure group than those in the weaning success group (P<0.05), but there were no statistically significant differences in other data between the 2 groups (P>0.05) (Table 1).

DIAPHRAGMATIC FUNCTION PARAMETERS:

By contrast to the weaning success group, the weaning failure group presented decreases in DE and DTF as well as increases in DCV and D-RSBI (P<0.05), but DTei and DTee were not statistically significantly different between the 2 groups (P>0.05) (Table 2). All 4 indicators demonstrated moderate effect sizes (d=0.61–0.65), supporting their clinical relevance and discriminative value.

PREDICTIVE VALUE OF DE, DTF, DCV, AND D-RSBI FOR VENTILATOR WEANING OUTCOMES OF PATIENTS WITH CERVICAL SPINAL CORD INJURY:

The plotted ROC curves showed that DE, DTF, DCV, and D-RSBI alone and their combination had an AUC >0.70 for predicting the ventilator weaning outcomes of patients with cervical spinal cord injury, suggesting high predictive values (Table 3, Figure 3). The combined predictive model was constructed using a multivariate logistic regression framework. DE, DTF, DCV, and D-RSBI were simultaneously entered as covariates, and the predicted probabilities from the model were used to generate the combination ROC curve. This approach yielded the highest AUC (0.896), confirming the best predictive performance. The optimal cut-off values for each parameter were determined using the Youden index (sensitivity+specificity-1), which identifies the point that maximizes the overall diagnostic effectiveness.

DECISION CURVES OF DE, DTF, DCV, AND D-RSBI FOR PREDICTING VENTILATOR WEANING OUTCOMES OF PATIENTS WITH CERVICAL SPINAL CORD INJURY:

According to the decision curves constructed, the combination of DE, DTF, DCV, and D-RSBI was superior to the 4 parameters alone in terms of the net benefit for predicting the ventilator weaning outcomes of patients with cervical spinal cord injury in the threshold ranges of 0–0.842, 0.843–0.878, and 0.907–1.000 (Figure 4).

Discussion

CLINICAL IMPLICATIONS:

The findings of this study highlight important clinical applications. Bedside ultrasound monitoring of diaphragmatic function provides a non-invasive, real-time, and repeatable method for assessing weaning readiness in patients with cervical spinal cord injury. Incorporating indices such as DE, DTF, DCV, and D-RSBI into routine evaluation may help identify patients at higher risk of weaning failure, enabling timely interventions such as respiratory muscle training, secretion management, and optimization of ventilatory support. When combined with conventional clinical parameters, these ultrasound indices have the potential to enhance the accuracy of weaning decisions, reduce reintubation rates, shorten ICU stays, and ultimately improve patient outcomes. Integrating these measures into standardized weaning protocols could further strengthen evidence-based practice, providing clinicians with objective markers of diaphragmatic function that support safer and more effective weaning strategies.

Conclusions

Bedside ultrasound monitoring of the diaphragmatic function parameters DE, DTF, DCV, and D-RSBI has good potential to predict ventilator weaning outcomes of patients with cervical spinal cord injury. These findings should be considered preliminary and associative, and further validation in larger, multicenter cohorts is warranted.