Abstract
Background
This study explored the performance of bedside ultrasound monitoring of diaphragmatic function in predicting the ventilator weaning outcomes of patients with cervical spinal cord injury.
Material/Methods
The clinical data of 136 eligible patients hospitalized from December 2021 to December 2023 were obtained for this prospective study, and they were assigned into weaning failure and weaning success groups. Intergroup comparisons were conducted on the general data and diaphragmatic function parameters: diaphragm excursion (DE), diaphragm thickening fraction (DTF), diaphragm contraction velocity (DCV), diaphragmatic-shallow rapid breathing index (D-RSBI), diaphragmatic thickness at the end of expiration (DTee), and diaphragmatic thickness at the end of inspiration (DTei).
Results
Among the diaphragmatic function parameters, decreases in DE and DTF but increases in DCV and D-RSBI were observed in the weaning failure group compared with those in the weaning success group (P<0.05). There were no significant differences in DTei and DTee between the 2 groups (P>0.05). The areas under the receiver operating characteristics (ROC) curves of DE, DTF, DCV, and D-RSBI alone and their combination for predicting ventilator weaning outcomes were all >0.70, and the combination had the highest predictive value. The combination of DE, DTF, DCV, and D-RSBI was superior to the 4 parameters alone in terms of the net benefit for predicting ventilator weaning outcomes in the threshold ranges of 0–0.842, 0.843–0.878, and 0.907–1.000.
Conclusions
Bedside ultrasound monitoring of diaphragmatic function parameters DE, DTF, DCV, and D-RSBI has good predictive value for the ventilator weaning outcomes of patients with cervical spinal cord injury.
Keywords: Diaphragm; Monitoring, Ambulatory; Ultrasound, High-Intensity Focused, Transrectal
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.
Figure 1.
The flowchart shows the processes of patient recruitment, exclusion, and grouping. IAH – intra-abdominal hypertension; SBT – spontaneous breathing trial; MV – mechanical ventilation.
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.
Figure 2.
Illustration of probe positioning and ultrasound views in patients with cervical spinal cord injury.
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).
Table 1.
General data (χ̄±s)/[n (%)].
| Variable | Weaning failure group (n=42) | Weaning success group (n=94) | t/χ2 | P | |
|---|---|---|---|---|---|
| Age (year) | 46.35±2.53 | 47.21±2.28 | 1.964 | 0.052 | |
| Sex | Male | 24 (57.14) | 55 (58.51) | 0.022 | 0.881 |
| Female | 18 (42.86) | 39 (41.49) | |||
| BMI (kg/m2) | 23.14±2.21 | 23.89±2.13 | 1.875 | 0.063 | |
| APACHE II score (point) | 23.26±2.54 | 21.45±2.88 | 3.522 | 0.001 | |
| Coronary heart disease | Yes | 7 (16.67) | 15 (15.96) | 0.011 | 0.917 |
| No | 35 (83.33) | 79 (84.04) | |||
| Hypertension | Yes | 13 (30.95) | 30 (31.91) | 0.012 | 0.911 |
| No | 29 (69.05) | 64 (68.08) | |||
| Diabetes mellitus | Yes | 5 (11.90) | 11 (11.70) | 0.646 | 0.799 |
| No | 37 (88.10) | 83 (88.30) | |||
| Ventilator-assisted ventilation time (days) | 5.26±1.45 | 4.41±1.34 | 3.322 | 0.001 | |
| HR (beats/min) | 80.39±7.23 | 80.58±7.69 | 0.143 | 0.886 | |
| Respiratory rate (breaths/min) | 20.33±3.83 | 18.29±3.20 | 3.239 | 0.002 | |
| PaCO2 (mmHg) | 38.56±6.54 | 36.15±6.74 | 1.944 | 0.054 | |
| PaO2 (mmHg) | 89.52±8.69 | 90.12±8.75 | 0.370 | 0.712 | |
| Oxygenation index | 228.65±12.45 | 231.55±12.58 | 1.246 | 0.215 | |
BMI – body mass index; APACHE II – Acute Physiology and Chronic Health Evaluation II; HR – heart rate; PaCO2 – arterial partial pressure of carbon dioxide; PaO2 – partial pressure of oxygen.
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.
Table 2.
Diaphragmatic function parameters (x±s).
| Group | DE (mm) | DTF (%) | DCV (cm/s) | D-RSBI[breaths/(min·mm)] | DTei (mm) | DTee (mm) |
|---|---|---|---|---|---|---|
| Weaning failure (n=42) | 12.55±3.60 | 33.45±7.81 | 1.91±0.70 | 1.76±0.53 | 2.54±0.96 | 2.13±0.74 |
| Weaning success (n=94) | 14.64±3.16 | 38.29±7.27 | 1.51±0.63 | 1.40±0.57 | 2.61±0.87 | 1.96±0.68 |
| t | 3.414 | 3.501 | 3.319 | 3.431 | 0.420 | 1.311 |
| P | 0.001 | 0.001 | 0.001 | 0.001 | 0.675 | 0.192 |
DE – diaphragm excursion; DTF – diaphragm thickening fraction; DCV – diaphragm contraction velocity; DRSBI – diaphragmatic-shallow rapid breathing index; DTei – diaphragmatic thickness at the end of inspiration; DTee – diaphragmatic thickness at the end of expiration.
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.
Table 3.
Predictive values of DE, DTF, DCV, and D-RSBI for ventilator weaning outcomes of patients with cervical spinal cord injury.
| Item | AUC | Cut-off value | 95% CI of AUC | P | Specificity | Sensitivity | Youden index |
|---|---|---|---|---|---|---|---|
| DE | 0.732 | 14.25 mm | 0.638–0.826 | <0.001 | 0.713 | 0.690 | 0.403 |
| DTF | 0.741 | 34.5% | 0.649–0.832 | <0.001 | 0.755 | 0.643 | 0.398 |
| DCV | 0.706 | 2.05 cm/s | 0.612–0.800 | <0.001 | 0.798 | 0.500 | 0.298 |
| D-RSBI | 0.708 | 1.5 breaths/ (min·mm) | 0.615–0.801 | <0.001 | 0.638 | 0.786 | 0.424 |
| Combination | 0.896 | – | 0.839–0.953 | <0.001 | 0.883 | 0.786 | 0.669 |
DE – diaphragm excursion; DTF – diaphragm thickening fraction; DCV – diaphragm contraction velocity; D-RSBI – diaphragmatic-shallow rapid breathing index; AUC – areas under the curve.
Figure 3.
ROC curves shoed the predictive values of DE, DTF, DCV, and D-RSBI for ventilator weaning outcomes of patients with cervical spinal cord injury. ROC – receiver operating characteristics; DE – diaphragm excursion; DTF – diaphragm thickening fraction; DCV – diaphragm contraction velocity, D-RSBI – diaphragmatic-shallow rapid breathing index.
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).
Figure 4.
Decision curves of DE, DTF, DCV, and D-RSBI for predicting ventilator weaning outcomes of patients with cervical spinal cord injury. DE – diaphragm excursion; DTF – diaphragm thickening fraction; DCV – diaphragm contraction velocity; D-RSBI – diaphragmatic-shallow rapid breathing index.
Discussion
Classified as a serious nervous system injury, cervical spinal cord injury can cause motor, sensory, and autonomic nervous dysfunction in patients [14]. The high plane of cervical spinal cord injury also leads to diaphragmatic and intercostal muscle paralysis, inhibits the movement of respiratory muscle, and induces respiratory dysfunction, so patients need to maintain their respiratory function through a ventilator to prevent death from respiratory failure [15]. The timing of ventilator weaning is critical for mechanically ventilated patients. Premature weaning can lead to weaning failure and raise the reintubation and death rates, and delayed weaning can increase the complication rate and the length of ICU stay [16]. Successful weaning signifies a trend of improved condition in patients, which is a basic requirement for transfer out of the ICU or discharge from the hospital [17]. Therefore, how to accurately predict the weaning outcomes of patients with cervical spinal cord injury is a major concern in the field of critical care medicine.
The diaphragm is the most important respiratory muscle executing autonomous respiration. Diaphragmatic dysfunction is a major reason for weaning failure, and the probability of poor diaphragmatic function is substantially increased in patients receiving ventilator therapy [18]. The results of the present study indicated that DTF was lower in the weaning failure group than in the weaning success group, mainly because DTF reflects the contraction efficiency and atrophy degree of the diaphragm, and a lower DTF value means weaker diaphragm contraction and higher atrophy degree. Moreover, the imbalance between mechanical load and actual load of the diaphragm can induce diaphragmatic fatigue and increase the risk of weaning failure [19]. Defined as the vertical distance of the diaphragm from the end of maximal inspiration to the end of calm expiration, DE is associated with the expansion of the thoracic cage and the contribution of the diaphragm to respiration [20]. Our study shows that DE declined in the weaning failure group compared to that in the weaning success group, suggesting that the diaphragmatic fatigue or dysfunction during the spontaneous respiration of patients can increase the risk of weaning failure. In the case of a low DE value, the small motion amplitude as well as the poor strength and endurance of the diaphragm leads to insufficient respiratory drive and reduced ventilatory capacity in patients [21]. Such a low DE value indicates a small tidal volume, low respiratory system compliance, and high resistance of the respiratory system, which decrease the lung expansion and retraction capacity in the respiratory system [22].
D-RSBI can directly measure the diaphragmatic motion, serving as an indicator of respiratory load and respiratory efficiency [23]. In the present study, D-RSBI was higher in the weaning failure group than in the weaning success group, and a higher D-RSBI suggests a greater respiratory load, lower respiratory efficiency, and a higher probability of weaning failure of the patients. DCV is the ratio of DE to the inspiratory time capable of reflecting the contraction rate and fatigue degree of the diaphragm, which is in relation to the muscle strength of the diaphragm [24]. The higher DCV in patients with weaning failure is attributable to the increased respiratory rate, which gives rise to the contraction rate. Additionally, the patients’ spontaneous respiration is not fully recovered, so the weaning failure rate is fairly high. Both DTei and DTee represent the changes in diaphragmatic thickness [25]. No statistically significant differences in DTei and DTee were observed between the 2 groups in the present study, which may be affected by individual differences such as height and weight of the patients, so they cannot be used as indicators for evaluating diaphragmatic function.
As shown in the ROC curves plotted, AUC >0.70 for predicting the ventilator weaning outcomes of patients with cervical spinal cord injury was obtained for DE, DTF, DCV, and D-RSBI alone as well as in combination, which had some predictive value, and the combination had the highest predictive value. Based on the decision curves, the net benefit of the combination of DE, DTF, DCV, and D-RSBI for the prediction of ventilator weaning outcomes of patients with cervical spinal cord injury was greater than that of the 4 parameters alone in the threshold ranges of 0–0.842, 0.843–0.878, and 0.907–1.000, suggesting that bedside ultrasound monitoring of DE, DTF, DCV, and D-RSBI can predict the ventilator weaning outcomes of such patients. Our ROC/AUC values were comparable to or slightly higher than in previous studies. Earlier investigations reported that DE and DTF generally showed AUCs ranging from 0.70 to 0.75 [26,27], while our study demonstrated AUCs of 0.732 for DE and 0.741 for DTF. Notably, the combination of multiple ultrasound-derived indices achieved an AUC of 0.896, higher than single-parameter assessments, underscoring the incremental predictive value of multimodal ultrasound evaluation. Therefore, the risk of ventilator weaning failure can be predicted by monitoring DE, DTF, DCV, and D-RSBI in patients with cervical spinal cord injury in clinical settings. The reduction in DE and DTF and the rise in DCV and D-RSBI suggest a high ventilator weaning probability. However, the ventilator weaning success rate can be improved by targeted treatments, including sputum drainage, stimulated passive exercise of the diaphragm muscle, and respiratory muscle endurance training.
This study has several limitations. First, the single-center design and relatively small sample size limit the generalizability of the findings, and no formal sample size calculation was performed. Multivariate regression to adjust for confounders was also not conducted, which weakens the robustness of the conclusions. Second, ultrasound assessment of the diaphragm is operator-dependent, and image quality can be influenced by factors such as subcutaneous adiposity or abdominal distension. Third, we did not fully standardize confounding factors, such as ventilator settings, sedation, intra-abdominal pressure, which could have affected diaphragmatic excursion and thickening. Fourth, only single-timepoint and unilateral measurements were performed, and no comparison with invasive or electrophysiological reference standards was included. Finally, long-term outcomes, such as reintubation rates and mortality, were not systematically assessed.
Future studies should adopt multicenter designs with larger cohorts, predefined sample size calculations, and multivariate regression models to control for confounders. Standardized protocols, repeated bilateral measurements, integration with respiratory mechanics, and external validation may enhance predictive accuracy. Comparative studies using standard techniques and interventional trials are also warranted.
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.
Footnotes
Financial support: This study was financially supported by the Project of 901th Hospital of PLA Joint Logistics Support Force (No. 2024YGYB07)
Conflict of interest: None declared
Publisher’s note: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher
Declaration of Figures’ Authenticity: All figures submitted have been created by the authors who confirm that the images are original with no duplication and have not been previously published in whole or in part.
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