Risk factors for ICU-acquired weakness in patients undergoing mechanical ventilation: a systematic review and meta-analysis

Introduction

Mechanical ventilation (MV) serves as a vital therapeutic intervention in the intensive care unit (ICU), facilitating the maintenance of airway patency and delivering essential respiratory support through invasive ventilators (1). Patients are often under prolonged sedation and analgesia while undergoing MV therapy, which can cause diaphragmatic atrophy, thereby increasing the risk of death and poor long-term functional outcomes. Therefore, patients undergoing MV often require pharmacological intervention to sustain life (2).

Corticosteroids (CSs) are widely used in MV patients due to their potent anti-inflammatory and immunomodulatory effects (3). They can improve hypoxemia and reduce the duration of MV and shock (4). However, prolonged use of CSs may lead to decreased muscle protein synthesis and increased protein breakdown, thereby elevating the risk of intensive care unit-acquired weakness (ICU-AW) (5). Although several studies have explored the association between CS use and ICU-AW, the results remain inconsistent.

This meta-analysis intends to comprehensively delve into the connection of ICU-AW risks with CS use in ICU patients, providing an evidence-based foundation for clinical practice. We present this article in accordance with the PRISMA reporting checklist (6) (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1155/rc).

Methods

Data sources

This study was registered with PROSPERO (CRD42024558263).

Search strategy

A systematic search in various databases, involving PubMed, Web of Science, Embase, Cochrane Library, China National Knowledge Infrastructure (CNKI), Wanfang Data, VIP Database, and the Chinese Biomedical Literature Database (CBM) was conducted up to December 2024. The strategy was formulated by combining subject terms with free-text keywords, including “Respiration, Artificial”, “Muscle Weakness”, “Intensive Care Units”, “intensive care unit acquired weakness*”, “critical illness polyneuropathy”, “critical illness myopathy”, and “Adrenal Cortex Hormones”. The English search expression is available in Appendix 1. To ensure a comprehensive literature search, citation indexing may be employed to trace the references of included documents when necessary.

Inclusion criteria

We screened titles and abstracts, evaluated full texts, and independently identified articles that fulfilled the criteria. The following epidemiological studies were incorporated: (I) patients undergoing MV in the ICU, aged 18 years or older; (II) randomized controlled trials (RCTs) or cohort studies; (III) the outcome measure was the number of cases of ICU-AW.

Exclusion criteria

The following articles were discarded: (I) reviews, meta-analyses, and case reports; (II) conference abstracts and registration program; (III) research that cannot be obtained in full text; (IV) animal experiments; (V) articles failing to report the required outcome measure; (VI) non-English articles; (VII) studies where the corresponding data could not be extracted.

Article screening and data extraction

Two investigators (M.Z. and Y.F.) independently searched and reviewed articles per the inclusion and exclusion criteria, as well as collected relevant data. When different opinions arose, discussions or consultations with a third investigator might be conducted to reach a consensus. The data extracted primarily included first author, publication date, country, research type, age, MV duration, details in the experimental group (number of participants and number of ICU-AW cases), details in the control group (number of participants and number of ICU-AW cases), types and dosages of CS used, days on analgesics or sedatives, lactate levels, average blood glucose levels, the Acute Physiology and Chronic Health Evaluation II (APACHE II) scores, the Sequential Organ Failure Assessment (SOFA) scores, average body mass index (BMI), and days on neuromuscular blockers.

Quality evaluation

The quality of the included RCTs was independently appraised by two investigators (M.Z. and Y.F.) by means of the Revised Cochrane Risk-of-Bias Tool for Randomized Trials (ROB2) tool (7). This evaluation assessed various biases, including those linked to randomization, deviations from intended interventions, missing outcome data, outcome measurement, and result reporting.

The risk of bias in cohort studies was appraised by means of the Newcastle-Ottawa Scale (NOS) (7), which focuses on three aspects: study population selection, inter-group comparability, and outcome measurement. Studies scoring ≥7 were categorized as high-quality research, studies with scores between 4 and 6 were deemed moderate quality, and those with a score of ≤3 were classified as low-quality research.

Statistical analysis

All statistical analyses were conducted using Stata software (version 16.0). The heterogeneity between the results was assessed using the Q-test (α=0.10) and I² index. If the heterogeneity was low (P>0.10 and I²<50%), a fixed-effects model was applied; otherwise, a random-effects model was used. The results are presented using the risk ratio (RR) and 95% confidence interval (CI). The number of cases of ICU-acquired weakness related to steroid use was extracted, and the risk of ICU-acquired weakness due to steroid use was calculated (RR). Subgroup analyses were performed based on factors such as MV time, age, type of CS, duration of CS use, dosage of CSs, blood glucose levels, lactate, BMI, SOFA score, APACHE II score, and ICU length of stay (LOS). The odds ratios (ORs) and 95% CIs of risk factors were extracted from the original studies. Meta-analysis was conducted if a risk factor was reported in two or more studies. Egger’s test was used to assess the symmetry of the funnel plot. If the funnel plot was significantly asymmetrical or if Egger’s test yielded P<0.05, there was publication bias.

Results

Literature search results

Initially, a preliminary search yielded 150 articles in Chinese and 1,021 articles in English. Additionally, four more articles were identified through other sources. After importing these references into EndNote X9 for both automatic and manual deduplication, 768 articles remained. Following an initial review based on titles and abstracts, we narrowed the selection down to 346 articles. A total of 325 articles were excluded due to the absence of ICU-AW data, involvement in animal experiments, publication in non-Chinese or non-English languages, classification as case reports, or other criteria that rendered them ineligible for inclusion. Ultimately, we obtained 21 relevant publications. The flowchart of the selection process is displayed in Figure 1.

Figure 1 Literature screening flowchart. CBM, Chinese Biomedical Literature Database; CNKI, China National Knowledge Infrastructure; ICU-AW, intensive care unit-acquired weakness.

Basic characteristics of the included articles

This study included 21 articles involving 6,894 ICU patients for MV treatment. Among them, 9 papers were in Chinese and 12 papers in English. The types of studies included 19 cohort studies (8-26) and 2 RCTs (27,28). Of the studies, 18 evaluated ICU-AW with the Medical Research Council scale (8-11,13,14,17,18,20,21,23,26-28), while one each used the peroneal nerve test (12), deep tendon reflexes (25), and electrophysiology (19) (Table 1).

Quality evaluation

The NOS scale was leveraged to appraise the quality of 19 included cohort studies. The scores for all studies ranged from 6 to 8 points. Among these, 5 studies reported independent blinding assessments by physical therapists or clinicians. Of the 19 studies, 17 were rated as high quality and 2 as moderate quality (Table 2).

Figure 2 presents the quality assessment results for the two RCTs included in the meta-analysis, using the ROB2 tool to evaluate the risk of bias across five domains: (D1) bias arising from the randomization process; (D2) bias due to deviations from intended interventions; (D3) bias due to missing outcome data; (D4) bias in measurement of the outcome; and (D5) bias in selection of the reported result.

Figure 2 Risk of bias assessment for the two included RCTs using the ROB2 tool. RCTs, randomized controlled trials; ROB2, Revised Cochrane Risk-of-Bias Tool for Randomized Trials.

As shown in Figure 2, Wolfe et al. (2018) (28) had a high risk of bias in randomization (D1) and selection of the reported result (D5), while Patel et al. (2014) (27) exhibited a low risk in most domains but raised concerns in the measurement of the outcome (D4).

Meta-analysis results

This study included 21 articles, all of which appraised the association of CS on ICU-AW risks in ICU patients undergoing MV. Slight heterogeneity was shown between the included studies (I²=47.5%), so a random-effects model (REM) was employed for meta-analysis. The results pointed out that CS use was significantly associated with ICU-AW risks (RR =1.52, 95% CI: 1.31–1.76). The pooled overall effect is shown in Figure 3.

Figure 3 Forest plot of the effect of corticosteroids on the risk of ICU-AW in patients undergoing MV. CI, confidence interval; ICU-AW, intensive care unit-acquired weakness; MV, mechanical ventilation; RR, risk ratio.

Risk factor analysis

Further analysis of risk factors was executed based on MV duration, age, CS type, duration of CS usage, CS dosage, blood glucose levels, lactate levels, BMI, SOFA score, APACHE II score, and LOS in the ICU. The results are listed in Table 3, and subgroup analyses are summarized in Table 4.

MV duration

Fifteen articles mentioned the effect of MV duration, with obvious heterogeneity (I²=56.8%, P=0.004). A REM was employed. The results uncovered that among ICU patients undergoing MV with CS, in patients with an MV duration ≥8 days (RR =1.71, 95% CI: 1.23–2.37) and <8 days (RR =1.54, 95% CI: 1.17–2.02), CS use was associated with the risk of ICU-AW (95% CIs overlapped by 65%). This result suggested that the duration of MV may contribute to ICU-AW through mechanisms such as muscle disuse and diaphragm dysfunction, but did not confirm the decisive impact of MV duration thresholds on the risk.

Age

21 articles reported the impact of age, and an REM was leveraged (I²=47.5%, P=0.009). According to the meta-analysis, among ICU patients undergoing MV treatment using CS, the risk of ICU-AW was notably increased in patients aged 60 or older (RR =1.71, 95% CI: 1.36–2.23, P<0.001) and those aged <60 years (RR =1.35, 95% CI: 1.16–1.58, P<0.001). 95% CIs overlapped by 47%, suggesting that while older patients may experience muscle mass loss and reduced metabolic function, the age difference could be confounded by other factors, such as comorbidities.

Duration of CS usage

Five articles examined the influence of the duration of CS usage, and an FEM was utilized (I²=39.7%, P=0.16). The results uncovered that the use of CSs for both ≥7 days (RR =2.27, 95% CI: 1.37–3.36, P=0.001) and <7 days (RR =1.76, 95% CI: 1.13–2.73, P=0.01) was strongly associated with an increased risk of ICU-AW. 95% CIs overlapped by 38%, suggesting that while the duration of CS use may influence the risk, given differences in treatment regimen (e.g., bolus therapy vs. gradual tapering) and the overlapping confidence intervals, it was impossible to draw definitive conclusions regarding the effect of CS usage duration on the risk levels.

CS dosage

Six articles reported CS dosage, with low heterogeneity (I²=23.3%, P=0.26), and an FEM was adopted. The meta-analysis showed that, in ICU patients undergoing MV with CS treatment, those receiving a dosage of ≥1 g/day were associated with an increased risk of ICU-AW (RR =2.39, 95% CI: 1.64–3.49, P=0.001). In contrast, a CS dosage of <1 g/day showed no significant association with the risk of ICU-AW (RR =1.95, 95% CI: 0.77–4.90, P=0.16). It should be noted that there were differences in the potency of different CSs (e.g., 1 g of hydrocortisone was roughly equivalent to 250 mg of methylprednisolone). Furthermore, the broad CI in the low-dose group reflected the limited data available for this subgroup.

Blood glucose levels

Nine studies examined the effect of blood glucose levels, with minimal heterogeneity (I²=34.4%, P=0.14), and an FEM was employed. Based on the meta-analysis, the risk of ICU-AW was significantly associated with blood glucose levels >13 mmol/L (RR =1.83, 95% CI: 1.38–2.42, P<0.001) compared to blood glucose levels ≤13 mmol/L (RR =1.42, 95% CI: 1.22–1.66, P<0.001). Both groups demonstrated an increased risk of ICU-AW, with 95% CIs overlapping by 55%. This suggests that hyperglycemia may exacerbate muscle damage through insulin resistance and advanced glycation end-products, but strict blood glucose control targets should be individually assessed.

Lactate levels

Four articles on lactate levels were incorporated, exhibiting no heterogeneity (I²=0.0%, P=0.91). Hence, an FEM was employed. The results showed that patients with lactate levels ≥4 mmol/L (RR =1.62, 95% CI: 1.27–2.07, P<0.001) and <4 mmol/L (RR =1.51, 95% CI: 1.21–1.87, P<0.001) both were associated with an increased risk of ICU-AW, with 95% CIs overlapping by 58%. This result supported the hypothesis that acidosis may contribute to the development of ICU-AW by affecting neuromuscular excitability, but did not confirm that lactate levels were an independent modifier.

BMI

A total of 11 studies were included, with mild heterogeneity (I²=53.3%, P=0.02). A REM was employed. The results showed that both patients with BMI ≥24 kg/m² (RR =1.72, 95% CI: 1.14–2.61) and BMI <24 kg/m² (RR =1.51, 95% CI: 1.21–1.80) were associated with an increased risk of ICU-AW (with 95% CIs overlapping by 42%). While obesity may exacerbate muscle damage through a chronic inflammatory state, the current data were insufficient to support a significant difference in risk across different BMI levels.

SOFA score

Six studies reported SOFA scores, with noticeable heterogeneity (I²=52.0%, P=0.06). Thus, an REM was utilized. The results showed that patients with a SOFA score ≥8 (RR =1.63, 95% CI: 0.82–3.23, P=0.16) and those with a SOFA score <8 (RR =1.29, 95% CI: 0.76–2.20, P=0.35) both showed an increased risk of ICU-AW, with 95% CIs overlapping by 100%. However, no statistically significant difference was observed between the two groups, as their 95% CIs fully overlapped. It should be noted that the dynamic nature of SOFA scores may affect the accuracy of grouping. Furthermore, only six studies in the analysis reported SOFA data.

APACHE II score

11 articles investigated the APACHE II score, and minimal heterogeneity was observed among these articles (I²=37.2%, P=0.10). Therefore, effect sizes were pooled using an FEM. The results showed that patients with an APACHE II score ≥19 (RR =1.49, 95% CI: 1.22–1.82) and <19 (RR =1.48, 95% CI: 1.21–1.81) both demonstrated an increased risk of ICU-AW (95% CIs overlap by 89%). This suggested that disease severity was a general risk factor for ICU-AW, rather than a specific modifier.

LOS in the ICU

13 articles examined the LOS in the ICU, showing a low level of heterogeneity (I²=30.9%, P=0.14). Hence, an FEM was employed. The results showed that ICU LOS >14 days (RR =1.91, 95% CI: 1.42–2.58) and ≤14 days (RR =1.46, 95% CI: 1.27–1.69) both demonstrated an association with increased risk of ICU-AW (confidence intervals overlap by 31%). While the point estimates suggested that longer ICU stays may be associated with a higher risk, confounding factors (such as the underlying disease course) may influence this association.

Publication bias and sensitivity analysis

Publication bias between studies was assessed by means of Begg’s test and Egger’s funnel plot. By analyzing the 21 papers included, the shape of the funnel plot was essentially symmetrical (Figure 4). The P value for Begg’s test was 0.415 and for Egger’s test was 0.527. The results indicated no apparent publication bias in this study. To further appraise the stability of the findings, a sensitivity analysis was executed (Figure S1). The findings of the sensitivity analysis demonstrated that none of the studies had a noticeable influence on the meta-analysis results. Excluding any single study exhibited a minimal influence on the combined RR, with the overall effect size consistently approaching 1.52. This implied the robustness and consistency of the meta-analysis results.

Figure 4 Funnel plot for publication bias. RR, risk ratio.

Discussion

This study conducts a meta-analysis to appraise the association of CS on ICU-AW risks in ICU patients undergoing MV. The results uncover that the use of CS is significantly associated with ICU-AW risks (RR =1.52, 95% CI: 1.31–1.76), particularly among patients with an MV duration of ≥8 days, older individuals (≥ 60 years), those receiving high CS doses (≥1 g) or long-term CS treatment ≥7 days), as well as patients exhibiting hyperglycemia (>13 mmol/L), elevated lactate levels (≥4 mmol/L), an APACHE II score of ≥19, a BMI of ≥24 kg/m², and a LOS in the ICU exceeding 14 days. This finding suggests that clinicians should carefully weigh the anti-inflammatory effects of CSs against the potential risk of neuromuscular damage when applying these treatments. Furthermore, early intervention measures should be implemented for high-risk patients.

Our findings both agree with and differ from prior research. In accordance with the findings of Sharshar et al. (8), our study reveals a noticeable link between CS use and an increased risk of ICU-AW, particularly pronounced with high doses and prolonged usage. However, this finding diverges from the perspective proposed by Hermans et al. (29) that CS may have a protective effect. These discrepancies may stem from differences in the study populations and treatment regimens. Although a strong association between CS use and ICU-AW was observed, it must be emphasized that 19 of the 21 studies included in this meta-analysis were observational in design. Unmeasured confounders, such as disease severity and polypharmacy, may influence this association. Therefore, these findings should be interpreted as evidence of correlation rather than causation.

In terms of risk factors, patients of advanced age exhibit higher susceptibility due to the natural decline of muscle mass and metabolic functions (30). Long-term MV increases risk through mechanisms like activity restriction and diaphragm disuse (31). Metabolic disorders such as hyperglycemia and hyperlactate are involved in the pathogenesis of ICU-AW by affecting neuromuscular function and protein metabolism. Patients with high BMI may be more prone to muscle weakness due to a chronic inflammatory state and muscle fat infiltration. It is noteworthy that indicators of disease severity, such as the APACHE II score, exhibit a positive correlation with the risk, reflecting the damage to the neuromuscular system caused by critical illness itself (32). In alignment with the findings of Hogue et al. (33), our findings reveal that obesity serves as an independent risk factor, and prolonged LOS in the ICU exacerbates the onset of weakness through a multitude of intricate mechanisms. Compared to previous studies that focused on single factors, this research offers the advantage of a comprehensive assessment of the synergistic effects among various factors, thereby providing a more complete basis for clinical risk warning. However, due to the heterogeneity in the methodologies employed in the included studies, caution is warranted when interpreting the impact of specific factors.

CS may increase the risk of ICU-AW through various pathways: (I) imbalance in protein metabolism, where the activation of the ubiquitin-proteasome system promotes muscle protein degradation while inhibiting synthesis; (II) hyperglycemia and insulin resistance, as elevated blood glucose can lead to neuronal damage and exacerbate muscle atrophy (29); (III) inflammation and oxidative stress, where high doses of CS may aggravate mitochondrial dysfunction in muscles (34), and high lactate levels (≥4 mmol/L) could affect neuromuscular excitability through acidosis (26); (IV) immobilization and disuse atrophy, where prolonged MV duration and increased LOS in the ICU lead to reduced muscle activity, further worsening muscle weakness (35). These mechanisms interact synergistically, rendering high-risk patients (like older individuals and those with elevated APACHE II scores) more susceptible to developing ICU-AW. Future research should investigate how to mitigate these mechanisms, particularly focusing on targeting metabolic disorders, inflammation, and early rehabilitation, to improve patient outcomes in ICU settings.

This study has a few limitations. First, the included studies are primarily observational studies (19 cohort studies and only 2 RCTs), which may affect causal inference. Second, the impact of different types of CSs (e.g., hydrocortisone vs. methylprednisolone) and sex differences was not analyzed. Third, the sample size of some subgroup analyses is small (for instance, only 4 studies related to lactate levels), and thus the results need to be interpreted cautiously. However, this research provides important insights into clinical practice. For patients undergoing MV who require CSs, it is advisable to minimize the duration of treatment, avoid high doses, and closely monitor indicators like blood glucose and lactate levels. Future studies could further explore the effects of early rehabilitation training and nutritional support interventions on reducing the risk of ICU-AW. The subgroup analyses in this study have important limitations. First, the 95% CIs for all subgroup comparisons overlap, indicating that the evidence for these factors (such as age, duration of MV, etc.) as effect modifiers is limited. Second, most of the subgroup analyses had insufficient sample sizes, particularly in the CS dose and duration subgroups. Therefore, these results should be interpreted as exploratory findings rather than definitive conclusions. This study is primarily based on observational data. Despite the use of strict inclusion criteria and statistical adjustments, residual confounding may still affect the interpretation of the results. Future RCTs are needed to validate the causality of these associations.

Conclusions

This meta-analysis shows that CS use is significantly associated with the risk of ICU-AW in MV ICU patients, particularly with high doses and prolonged use. Given that the primary evidence comes from observational studies, this association needs to be further validated in prospective research. Furthermore, among patients in the ICU receiving MV with CSs, those who are older (≥60 years), have prolonged MV duration (≥8 days), exhibit hyperglycemia, possess a BMI ≥24 kg/m², present elevated lactate levels (≥4 mmol/L), demonstrate high APACHE II scores, and experience extended LOS in the ICU are at greater risk of ICU-AW. Caution should be exercised in clinical practice with patients using CSs, especially with high doses and prolonged use of treatment. Early and timely assessment of ICU-AW risks should be conducted in these patients, along with the development of a personalized early rehabilitation plan aimed at reducing the incidence of ICU-AW.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1155/rc

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1155/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1155/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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