Diaphragmatic ultrasound assessment of muscle recovery in patients undergoing general anesthesia: a systematic review and meta-analysis

Seung Eun Song; So Hui Yun

doi:10.22730/jmls.2025.22.1.1

Abstract

Recently, ultrasonography has been used to evaluate respiratory muscle function in intensive care units. Therefore, we aimed to determine whether this evaluation method applies even to patients recovering from general anesthesia. Randomized controlled trials on assessing diaphragmatic ultrasound undergoing general anesthesia were searched in PubMed/MEDLINE, the Cochrane Central Register of Controlled Trials, and Web of Science databases. Two reviewers will independently screen articles for eligibility and extract relevant data. The risk of bias was assessed using the Cochrane Handbook 5.1.0 for systematic reviews of interventions. Higgins' I2, the heterogeneity statistic Cochrane’s Q, and the corresponding P-values were calculated to measure the heterogeneity among the trials. We used R software (version 3.6.3; R Foundation for Statistical Computing, Vienna, Austria) for all analyses. Of the 165 studies searched, four were ultimately included. The evaluation of the diaphragm for respiratory and muscular recovery was comparable. The standardized mean difference was 1.33 (95% confidence interval, 1.11-1.56). This systematic review evaluates the effectiveness of diaphragmatic ultrasound in assessing respiratory muscle recovery in patients undergoing general anesthesia.

Key words: Diaphragm; Anesthesia, general; Neuromuscular blockade; Ultrasonography

INTRODUCTION

Many factors contribute to the impairment of respiratory function after surgery, including the extent of surgery, postoperative pain management, and diaphragmatic dysfunction [1,2]. The leading cause of postoperative respiratory complications is dysfunction of the respiratory muscles, especially the diaphragm. Muscle weakness during inspiration leads to atelectasis owing to alveolar hypoventilation, while expiration results in an inefficient cough [3,4]. Diaphragmatic movement is closely associated with postoperative vital capacity and lung compliance [2,5].

Therefore, various methods have been used to evaluate respiratory muscle function in perioperative patients. Evaluation of the movement of the diaphragm through ultrasound is in the spotlight, and valuable results are obtained when the M-mode is used [6-9].

This systematic review aimed to determine whether postoperative respiratory muscle dysfunction that may occur after general anesthesia in adults can be observed by diaphragmatic ultrasound and whether its clinical usefulness can be discussed in practice. Therefore, this study aimed to analyze the recovery of respiratory muscles before and after neuromuscular blocking agent administration based on the data that two reviewers summarized in randomized controlled trial studies and evaluated the diaphragm function in patients under general anesthesia.

METHODS

1. Study design

This meta-analysis followed the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines (Appendix 1). This study was registered with the International Prospective Register of Systematic Reviews (No. CRD42021268077).

2. Information sources and search strategy

Two authors searched the PubMed/MEDLINE, Cochrane Central Register of Controlled Trials, and Web of Science databases. The search terms included variants of terms, such as "general anesthesia," "neuromuscular block," "recovery," "diaphragm," and "ultrasound," including medical subject heading terms.

The search was restricted to studies published after 2000 and focused on randomized controlled trials conducted on humans. Additionally, only articles written in English were included.

3. Study selection and eligibility criteria

After searching for articles from the databases listed above, two authors selected the studies. The selection consisted of the following three steps: the two authors first selected the articles based on the title and then the abstract; for the remaining articles, the two authors reviewed the full text of each article for the final selection.

The inclusion criteria were as follows: patients under general anesthesia, neuromuscular blocking agent administered intravenously, and ultrasound assessment of diaphragmatic function.

Studies were excluded based on the following criteria: articles not written in English, patients not under general anesthesia, neuromuscular blocking agents not administered intravenously, did not assess diaphragmatic ultrasound, non-randomized clinical trials, non-human studies, and did not include patients aged over 18 years. Articles for which the full text was not available were also excluded.

4. Data collection process and extracted items

Two authors extracted data from the articles and crosschecked them to avoid missing or incorrect information. The extracted information included patient age, study design, publication year, author's first name, type of anesthesia, and measured outcomes. The measured outcomes were as follows: authors independently extracted data from the text, tables, and graphs. The diaphragmatic function was evaluated using ultrasound. Data from each study were analyzed to examine the correlation between muscle recovery and diaphragmatic ultrasound parameters.

5. Statistical analysis

1) Summary measures

Diaphragmatic parameters were extracted using the mean and standard deviation at specified time points. We also extracted the mean and standard deviation of the muscle recovery similarly.

2) Synthesis of results

Diaphragmatic parameters were correlated in all the included studies. Muscle relaxation correlates with diaphragmatic function. Therefore, we calculated the mean differences (MDs) for continuous outcomes. We calculated the 95% confidence interval (CI) for all estimates. A random-effects model was used for all trial results because of the possibility of different effect sizes across the studies. Higgins' I2, the heterogeneity statistic Cochrane's Q, and the corresponding P-values were calculated to measure the heterogeneity among the trials. We considered I2 >50% to indicate significant heterogeneity. Sensitivity analysis was performed by leave-one-out analysis using the meta and dmetar packages in R software (version 3.6.3; R Foundation for Statistical Computing, Vienna, Austria). Publication bias was not assessed in this meta-analysis because the number of included studies was less than 10. We used R software version 3.6.3 for all analyses.

RESULTS

1. Study selection and characteristics

We obtained 165 articles after an initial database search in PubMed (n=77), Cochrane Library (n=52), and Web of Science (n=33). A total of 68 duplicate articles were excluded. Two authors independently reviewed the articles. Subsequently, 49 reports were excluded based on a review of the abstract or title. Final full-text reviews were performed on the remaining 48 articles. Of the 13 articles, nine were excluded based on the exclusion criteria, and four were included in our study [10-13]. The reasons for the exclusion are described in Fig. 1.

The details of the selected four studies are summarized in Table 1. In the included studies, changes in diaphragmatic function after surgery were compared with baseline values using ultrasonography. The trial sizes ranged from 58 to 120 patients. The selected studies generally included patients with an American Society of Anesthesiology (ASA) physical status classification of I to IV. In one study, different drugs were administered to compare the effects of reversal agents [13]. Diaphragmatic ultrasound was performed during breathing with a convex transducer positioned below the right costal arch at the midclavicular line by angling the ultrasound beam cranially and perpendicular to the diaphragmatic dome. The M-mode was used on the vertical axis to measure the diaphragm thickness.

2. Results of individual studies

In the heterogeneity test, the P-value was 0.407, and I2 was <5%, indicating low heterogeneity (Fig. 2). Lang's study [10] showed a significant decrease in diaphragm function in the postoperative residual curarization group compared to the control group. Furthermore, Huang's study [11] demonstrated a significant reduction in diaphragmatic thickening fraction during deep breathing among patients who experienced adverse events after extubation.

3. Synthesis of results

The evaluation of the diaphragm for respiratory and muscular recovery was comparable. The standardized MD (SMD) was 1.33 (95% CI, 1.11-1.56). This result showed a low heterogeneity. After performing a meta-analysis, we conducted a subgroup analysis of the effective index, although the number of studies was small. The subgroup analyses did not show a significant difference in the effective index (Fig. 3). The number of studies included was small, so it did not significantly affect the bias. However, no studies were outside the CI of the average effect size in the funnel plot (Fig. 4). A sensitivity analysis for diaphragmatic dysfunction after surgery was performed according to the study design (Table 2).

DISCUSSION

The evaluation of diaphragm function through ultrasound is used as a helpful indicator when determining ventilator weaning by assessing whether the respiratory muscle is recovered in critically ill patients [14-17]. Ultrasound has several advantages, such as being able to be performed directly on the bedside, reducing the risk of radiation, and even in patients who have difficulty in cooperation. Moreover, as ultrasound imaging has become clearer and easier to use in recent years, various studies have attempted to evaluate its efficacy in surgical patients.

In this study, we compared and analyzed the degree of recovery of the respiratory muscles after surgery in patients under general anesthesia using ultrasound. Each of the four studies included in this analysis showed significant results, and it can be interpreted that it is helpful to use ultrasound because the SMD is substantial (>0.8).

However, this study had some limitations. First, the number of studies and the number of people participating was small. Therefore, the CI was long. This is because evaluating patients after surgery is more complex than assessing patients in intensive care units. Surgery patients move more depending on the degree of pain and arousal, and it is difficult to quickly estimate these using ultrasound because they do not observe long-term changes. Moreover, even if clinical trials or study protocols (three cases) [18-20] are registered, there will be many cases where research cannot be sufficiently conducted to obtain clinically significant results. Another limitation is that individual studies' indicators for evaluating diaphragmatic function were slightly different.

Although it takes time to become skilled, real-time monitoring is possible using a non-invasive method, and the clinical usefulness of ultrasound can be evaluated positively concerning the safety of patient management during the perioperative period. In the future, it is expected that more diverse and highly utilized studies will be conducted, and significant results will be obtained based on a lot of studies.

Notes

CONFLICT OF INTEREST

The author reports no conflict of interest.

FUNDING

This work was supported by a research grant from Jeju National University Hospital 2019.

Figure 1.

PRISMA flow diagram. PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-analyses.

Figure 2.

Forest plot for diaphragmatic function and respiratory recovery. SD: standard deviation, SMD: standardized mean difference, CI: confidence interval.

Figure 3.

Forest plot for subgroup analysis. SD: standard deviation, SMD: standardized mean difference, CI: confidence interval, EV: effect variable, DED: diaphragm excursion difference, DTF_DB: deep breathing diaphragmatic thickening fraction during extubation, DIA: diaphragm inspiratory amplitude.

Figure 4.

Funnel plot for publication bias.

Table 1.

Study characteristics

Study	Duration (months)	Effective index	Target (ASA)	Sample size
Lang et al. [10] (2021)	4	DED	I-II	75
Huang et al. [11] (2023)	13	DTF_DB	II-III	120
Rustagi et al. [12] (2023)	24	DIA	I-II	90
Huang et al. [13] (2023)	6	DIA	III-IV	58

ASA: American Society of Anesthesiology classification, DED: diaphragm excursion difference, DTF_DB: deep breathing diaphragmatic thickening fraction during extubation, DIA: diaphragm inspiratory amplitude

Table 2.

Sensitivity analysis

Study	SMD	95% CI	P-value	tau²	tau	I² (%)
Lang et al. [10] (2021)	1.36	1.11-1.61	<0.0001	0.017	0.129	23.1
Huang et al. [11] (2023)	1.37	1.13-1.62	<0.0001	0.007	0.086	12.1
Rustagi et al. [12] (2023)	1.16	0.86-1.46	<0.0001	0.000	0.000	0.0
Huang et al. [13] (2023)	1.37	1.13-1.62	<0.0001	0.005	0.071	9.0
Fixed effect model	1.33	1.11-1.56	<0.0001	0.000	0.000	0.0

SMD: standardized mean difference, CI: confidence interval.

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