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Anesthesiology and Perioperative Science

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Open Access 01.06.2024 | Review Article

Effect of ultrasound-guided recruitment maneuver on atelectasis: a systematic review and meta-analysis of randomized controlled trials

verfasst von: Yi Xu, Yang Han, Huijia Zhuang, Fei Fei, Tingting Zheng, Hai Yu

Erschienen in: Anesthesiology and Perioperative Science | Ausgabe 2/2024

Abstract

To summarize the existing evidence on the effects of ultrasound-guided recruitment maneuver (RM) during perioperative period on atelectasis, oxygenation and other clinical outcomes in adult patients undergoing abdominal surgery. In this systematic review and meta-analysis, PubMed, Embase, Cochrane Library, Web of Science, China National Knowledge Infrastructure, and WanFang databases were searched from inception to May 2023 for relevant randomized controlled trials (RCTs) comparing the perioperative use of ultrasound-guided RM with a control group in adult patients undergoing abdominal surgery. The primary outcome was the incidence of early postoperative atelectasis (within 24 h after surgery). A total of 12 RCTs with 895 patients were included. The ultrasound-guided RM significantly reduced the incidence of postoperative atelectasis (RR [risk ratio]: 0.44, 95% CI [confidence interval]: 0.34 to 0.57, P < 0.001), with a median fragility index of 4. Prespecified subgroup analyses demonstrated the consistent findings. Additionally, ultrasound-guided RM could decrease postoperative lung ultrasound score (MD [mean difference]: − 3.02, 95% CI: − 3.98 to − 2.06, P < 0.001), reduce the incidence of postoperative hypoxemia (RR: 0.32, 95% CI: 0.18 to 0.56, P < 0.001), improve postoperative oxygenation index (MD: 45.23 mmHg, 95% CI: 26.54 to 63.92 mmHg, P < 0.001), and shorten post-anesthesia care unit (MD: − 1.89 min, 95% CI: − 3.14 to − 0.63 min, P = 0.003) and hospital length of stay (MD: − 0.17 days, 95% CI: − 0.30 to − 0.03 days, P = 0.02). However, there was no significant difference in the incidence of atelectasis at the end of surgery between two groups (RR: 0.99, 95% CI: 0.86 to 1.14, P = 0.89). The use of ultrasound-guided RM perioperatively reduced the risk of atelectasis and improve oxygenation after abdominal surgery. Strategies to reduce the development of perioperative atelectasis are presented to highlight areas for future research.

Supplementary Material 1.

Supplementary Information

The online version contains supplementary material available at https://doi.org/10.1007/s44254-024-00056-4.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Confidence interval

Fragility index

GRADE

Grading of Recommendations, Assessment, Development and Evaluations

LUS

Lung ultrasound

Mean difference

PACU

Post-anesthesia care unit

PRISMA

Preferred reporting items for systematic reviews and meta-analyses

RCTs

Randomized controlled trials

Recruitment maneuver

Risk ratio

Standard deviation

1 Introduction

Pulmonary atelectasis is pervasive in the perioperative period, and its prevalence has been estimated to be as high as 90% among a broad population of patients undergoing mechanical ventilation with general anesthesia [1, 2]. Atelectasis negatively impacts respiratory mechanics, induce inflammatory responses, and impairs oxygenation, which is associated with increased morbidity and mortality, prolonged hospital stays, and increased healthcare costs [3‐5].

Recruitment maneuver (RM), which constitute part of the lung-protective ventilation strategy and ‘open lung ventilation’ concept, are beneficial in reopening collapsed alveoli and improving lung mechanics, thereby reducing the risk of perioperative atelectasis [6‐10]. However, conventional RM can cause alveolar overdistention or incomplete recruitment. Moreover, because of its potential side-effects, such as hemodynamic instability and hypoxemia, high-quality supportive evidence is lacking to recommend a routine [3]; and the safe and effective recruitment strategy is far from being established.

Lung ultrasound (LUS) has emerged as a useful bedside tool to accurately diagnose atelectasis and quantitatively evaluate aeration loss during perioperative period [11‐13]. In recent years, LUS has been used for guiding safe and effective RM to optimize the recruitment strategy and reduce the risk of perioperative atelectasis [14]. However, there is a sparsity of high-quality data regarding the efficacy of ultrasound-guided RM on clinical outcomes. Also, given that most RCTs are single-center small-sampled studies, the conclusions are yet to be confirmed.

Therefore, we conducted a systematic review and meta-analysis to determine the effects of ultrasound-guided RM on perioperative atelectasis, blood oxygenation, and other related clinical outcomes in adult patients undergoing abdominal surgery.

2 Materials and methods

This systematic review and meta-analysis followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2020 guidelines (see Supplementary 1) [15], and the protocol was registered in the PROSPERO database (registration number CRD42023463305).

2.1 Search strategy

We performed a comprehensive search in the following databases: PubMed, Embase, Cochrane library, Web of Science, China National Knowledge Infrastructure, Wanfang data, and the China Science and Technology Journal Database (VIP, http://qikan.cqvip.com) from inception to May 2023, using the combination of keywords and database-specific subjects to describe “ultrasound”, “recruitment maneuver” and “pulmonary atelectasis”. The reference lists of relevant sources were also checked to identify additional studies missed from the original electronic search. No restriction was applied to language or publication status. The detailed search strategy can be found in Supplementary material 2.

2.2 Eligibility criteria

Study inclusion criteria were as follows: (1) design: randomized controlled trials (RCTs); (2) population: adult patients aged 18 yr or older undergoing elective abdominal surgery; (3) intervention: perioperative use of ultrasound-guided RM, and no restriction on the timing or type of RM; (4) comparison: conventional RM or no treatment; (5) outcomes: eligible studies must report at least one of predefined outcomes. The primary outcome was early postoperative atelectasis (within 24 h after surgery). Secondary outcomes were postoperative LUS scores, atelectasis at the end of surgery, postoperative hypoxemia, postoperative oxygenation index (i.e., PaO₂/FiO₂ ratio), duration of post-anesthesia care unit (PACU) stay, and length of hospital stay. No language, sample size or date of publication restrictions were applied. Exclusion criteria were as follows: (1) ultrasounds only be used to diagnose atelectasis or the details are unknown; (2) nonhuman studies; (3) unextrable data.

2.3 Data extraction

Two reviewers (Author Y.X. and Y.H.) independently assessed trial eligibility based on titles, abstracts, full-text reports, and further information from the investigators as needed. Relevant data were extracted using prespecified extraction sheets. We used a standardized data collection form to record following study characteristics: study design (first author and year of publication), study population (sample size, type of surgery, setting of mechanical ventilation), interventions (method and timing), and outcome measures of interest. Any disagreements were resolved by discussion or mediated by a third reviewer (Author H.Z.).

2.4 Risk of bias and certainty of evidence

Two reviewers (Author Y.X. and Y.H.) independently assessed the risk of bias of each study in duplicate using the Cochrane risk of bias tool for randomized trials (RoB-2) [16]. The certainty of evidence for each outcome was determined using the Grading of Recommendations, Assessment, Development and Evaluations (GRADE) system. All disagreements were resolved by discussion with an arbiter (Author H.Z.).

2.5 Statistical analysis

We calculated the risk ratio (RR) with corresponding 95% confidence interval (CI) for dichotomous variables, and mean difference (MD) with corresponding 95% CI for continuous variables. If the outcome data reported median and inter-quartile ranges, the data were converted to estimate mean and standard deviation (SD) using the method described by Weir et al. [17]. A random-effects model was used to account for potential clinical and methodologic diversity between studies; the inverse-variance and Mantel-Haenszel methods were used for estimating the study weight of continuous and dichotomous variables, respectively. Heterogeneity across studies was assessed and further quantified using the I² statistic, with an I² < 25% interpreted as low, I² of 25–75% as moderate, and I² > 75% as high. Prespecified subgroup analyses for the primary outcome were performed as follows: (1) patient population (elderly vs non-elderly); (2) type of comparisons (no RM vs conventional RM); (3) type of interventions (sustained RM vs stepwise RM); (4) timing of interventions (single RM vs repeated RM); and (5) fraction of inspired oxygen (low FiO₂ < 0.6 vs high FiO₂ ≥ 0.6). After an overall evaluation, we conducted a sensitivity analysis of the exclusion of studies with high or some concerns in the overall assessment of the risk of bias. Funnel plots were used to assess publication bias. All statistical analyses were performed using Review Manager 5.3 software (Cochrane Collaboration; Oxford, UK), and a two-sided P-value of < 0.05 was considered statistically significant. Additionally, we calculated the fragility index (FI) [18, 19] using the calculator tool ClinCalc: Fragility Index Calculator to assess the robustness of each trial; furthermore, we reported the median and the range of the fragility indices of the enrolled studies.

3 Results

3.1 Study search and selection

One thousand six hundred thirty-five articles were identified from the initial search, and 63 potentially eligible studies were retrieved for full-text review. After duplicate and ineligible studies were removed, 12 RCTs with a total of 895 participants were finally included in our qualitative and quantitative analyses [14, 20‐30]. The study selection flow chart is shown in Fig. 1.

3.2 Characteristics of included studies

The characteristics of the included studies are summarized in Table 1. All eligible trials were published between 2019 and 2023 with sample size from 40 to 122 patients. Five trials were published in English and seven were in Chinese. Of the 12 trials, a half recruited elderly patients aged ≥ 65 yr [23‐25, 27, 28, 30]. Most of the trials (9/12, 75%) were conducted in the context of lung-protective ventilation strategy [14, 20‐26, 29]. The study intervention (i.e., ultrasound-guided RM) was performed by incremental positive end-expiratory pressure (PEEP) in eight trials [20‐26, 28] and by sustained inflation in four trials [14, 27, 29, 30]. The ultrasound-guided RM was compared with conventional RM and with no RM in four [14, 25, 27, 29] and six trials [20, 21, 23, 24, 28, 29], respectively; ultrasound-guided RM, conventional RM and no RM were all compared in two trials [22, 26]. Six trials [21, 23, 25, 27, 28, 30] received a single RM at the end of surgery, and the remaining six received the repeated RM (both after tracheal intubation and at the end of surgery) [14, 20, 22, 24, 26, 29]. The vast majority enrolled patients undergoing laparoscopic surgeries; and type of surgeries included one mix upper abdominal surgery [21], two gastric surgeries [27, 29], three colorectal surgeries [23, 25, 28], two gallbladder surgeries [26, 30], three gynecological surgeries [14, 20, 22], and one urinary surgery [24].

Table 1

Characteristics of included studies

Reference	No. of patients n (I/C)	Age	Type of surgery	Ultrasound-guided group	Control group	LPV^a	Timing of intervention	FiO₂
Chen 2023 [24]	76 (38/38)	I: 72.8 ± 4.8 C: 72.3 ± 4.0	Laparoscopic radical prostatectomy	Incremental PEEP	No RM	Y	T1: 5 min after induction T2: At the end of surgery	0.5
Chen' 2023 [25]	94 (49/45)	I: 69 (65–79) C: 68 (65–86)	Laparoscopic radical resection of colorectal cancer	Incremental PEEP	Conventional RM	Y	At the end of surgery	0.4
Dong 2020 [26]	90 (30/60)	I: 51.70 ± 10.31 C: 51.45 ± 12.66	Laparoscopic cholecystectomy	Incremental PEEP	1: No RM 2: Conventional RM	Y	T1: 10 min after induction T2: At the end of surgery	0.6
Fan 2023 [27]	120 (60/60)	I: 65.17 ± 12.33 C: 65.43 ± 12.21	laparoscopic radical gastrectomy	SI	Conventional RM	N	At the end of surgery	0.6
Geng 2021 [28]	42 (21/21)	I: 66.4 ± 4.6 C: 69.5 ± 6.2	Laparoscopic colorectal cancer surgery	Incremental PEEP	No RM	N	At the end of surgery	1.0
La 2023 [29]	80 (40/40)	I: 70 ± 5 C: 71 ± 4	laparoscopic radical gastrectomy	SI	Conventional RM	Y	At 15-min intervals	0.5
Liu 2022 [20]	41 (20/21)	I: 37.2 ± 9.7 C: 38.1 ± 10.9	Laparoscopic gynaecological surgery	Incremental PEEP	No RM	Y	T1: Immediately after induction T2: At the end of surgery	0.4
Liu 2023 [21]	122 (40/82)	I: 50.7 ± 4.2 C: 55.1 ± 4.8	Major open upper abdominal surgery	Incremental PEEP	No RM	Y	At the end of surgery	0.5
Park 2021 [14]	40 (20/20)	I: 46.2 ± 9.6 C: 49.4 ± 14.8	Laparoscopic gynaecological surgery	SI	Conventional RM	Y	T1:5 min after induction T2: At the end of surgery	0.4
Wu 2022 [22]	90 (30/60)	I: 47.20 ± 9.27 C: 50.24 ± 8.73	Laparoscopic gynaecological surgery	Incremental PEEP	1: No RM 2: Conventional RM	Y	T1: Immediately after induction T2: At the end of surgery	0.4
Yang 2021 [23]	40 (20/20)	I: 66.4 ± 4.6 C: 69.5 ± 6.2	Laparoscopic surgery for colorectal carcinoma	Incremental PEEP	No RM	Y	At the end of surgery	0.4
Zhang 2023 [30]	60 (30/30)	I: 55.30 ± 8.31 C: 54.87 ± 10.27	Laparoscopic cholecystectomy	SI	No RM	N	Before tracheal extubation	1.0

SI Sustained inflation, RM Recruitment maneuvers, PEEP Positive end-expiratory pressure, LPV lung-protective ventilation, FiO₂ Fraction of inspiratory oxygen

^alow tidal volume (6–8 ml/kg) and appropriate positive end-expiratory pressure

3.3 Risk of bias and certainty assessment

Figure 2 reports the risk of bias assessment. Six studies had a low overall risk of bias; four studies were globally evaluated with some concerns on the basis of an unclear randomization process, measurement of the outcome and deviations from the intended interventions; two studies were classified as having a high overall risk of bias mainly because of deviations from intended interventions and missing outcome data. The certainty of evidence ranged from high to very low. Details regarding our GRADE assessment of pooled effect estimates (including summary of findings and evidence profile) can be found in Supplementary material 3.

3.4 Primary outcome: incidence of early postoperative atelectasis (within 24 h after surgery)

Based on the pooling of data from ten RCTs (n = 723 patients) [14, 20‐25, 27, 28, 30], the use of ultrasound-guided RM demonstrated a significant reduction in the incidence of early postoperative atelectasis (RR: 0.44, 95% CI: 0.34 to 0.57, P < 0.001), with moderate heterogeneity (I² = 27%; P = 0.19; Fig. 3). The certainty of evidence for this outcome was high. There was no subgroup difference related to the patient population (P = 0.41), type of comparisons (P = 0.83), type of study interventions (P = 0.77), timing of study interventions (P = 0.85), and level of FiO₂ (P = 0.68) (Supplementary Table 1). The FI values of each study were reported in Table 1, and their median and range was 4 (0 to 16). In addition, 80% of included RCTs had an FI value of ≤ 4.

3.5 Secondary outcomes

3.5.1 Early postoperative LUS score

Nine trials (n = 577) [14, 20, 22, 23, 25, 26, 28‐30] demonstrated that ultrasound-guided RM might reduce LUS score in early postoperative period (MD: − 3.02, 95% CI: − 3.98 to − 2.06, P < 0.001; low certainty) with high heterogeneity (I² = 89%; P < 0.001) (Supplementary Fig. 1).

3.5.2 Incidence of atelectasis at the end of surgery

Eight trials (n = 513) [14, 20, 21, 23, 25, 26, 28, 30] demonstrated that the incidence of atelectasis at the end of surgery did not differ between the two groups (RR: 0.99, 95% CI: 0.86 to 1.14, P = 0.89; low certainty). Significant statistical heterogeneity was detected (I² = 60%; P = 0.01) (Supplementary Fig. 2).

3.5.3 Incidence of postoperative hypoxemia

The data from eight trials (n = 692) [14, 21, 22, 24‐26, 29, 30] indicated that ultrasound-guided RM reduced the incidence of postoperative hypoxemia (RR: 0.32, 95% CI: 0.18 to 0.56, P < 0.001; moderate quality) with no heterogeneity (I² = 0%; P = 0.91) (Supplementary Fig. 3).

3.5.4 Postoperative oxygenation index

Seven RCTs (n = 618) [14, 21, 22, 24, 26, 27, 29] suggested that postoperative oxygenation index was significant improved in the ultrasound-guided RM group (MD: 45.23 mmHg, 95% CI: 26.54 to 63.92 mmHg, P < 0.001; moderate quality) but with high heterogeneity (I² = 84%; P < 0.001) (Supplementary Fig. 4).

3.5.5 Length of PACU stay

Among seven RCTs involving 467 patients [14, 20, 21, 23, 25, 26, 28], the use of ultrasound-guided RM was associated with a significant reduction in length of PACU stay when compared with the control group (MD: − 1.89 min, 95% CI: − 3.14 to − 0.63 min, P = 0.003; low certainty) with no heterogeneity (I² = 0; P = 0.44) (Supplementary Fig. 5).

3.5.6 Length of hospital stay

Based on the pooling of data from ten trials (n = 723) [14, 20‐25, 27, 28, 30], the length of hospital stay was significantly shorter in the ultrasound-guided RM group compared with the control group (MD: − 0.17 days, 95% CI: − 0.30 to − 0.03 days, P = 0.02; low certainty) with no heterogeneity (I² = 0; P = 0.48) (Supplementary Fig. 6).

3.6 Publication bias

Publication bias was assessed visually using a funnel plot (Supplementary Fig. 7). The symmetry of such funnel plots was assessed visually, and no obvious asymmetry was detected for the primary outcome.

3.7 Sensitivity analyses

After excluding studies with some concerns or high risk of bias [23, 25‐27, 30], the sensitivity analysis demonstrated a consistent reduction with regard to the incidence of early postoperative atelectasis in the ultrasound-guided group (RR: 0.46, 95% CI: 0.33 to 0.66, P < 0.001).

4 Discussion

This is a systematic review and meta-analysis of 12 RCTs with 895 patients to evaluate the effects of perioperative ultrasound-guided RM on postoperative atelectasis and other clinical outcomes in adult patients undergoing abdominal surgery. Our meta-analysis demonstrated that perioperative use of ultrasound-guided RM could significantly reduce the risk of postoperative atelectasis, with high quality of evidence. Additionally, ultrasound-guided RM can decrease postoperative LUS score, reduce incidence of postoperative hypoxemia, improve oxygenation index, as well as shorten PACU and hospital length of stay. However, there was no difference in the incidence of atelectasis at the end of surgery between the two groups.

To the best of our knowledge, this is the first systematic review and meta-analysis to determine the efficacy of perioperative ultrasound-guided RM in adult surgical patients, and represents the most up-to-date assessment of the issue. The increase in the risk of compression and absorption atelectasis is explained by impairments of respiratory physiology during general anesthesia [31‐33]. Development of atelectasis is associated with a series of pathophysiological mechanisms including decreased functional residual capacity and lung compliance, impairment of gas exchange and blood oxygenation, and development of lung injury [33]. Given that atelectasis is the most common type of pulmonary complications and a significant contributing factor to the development of lung injury, our study has focused on early detection and prevention of atelectasis to improve patient outcomes. To date, there are inconsistencies in the literature regarding the utility of RM in perioperative period. A previous meta-analysis showed that RM could reduce postoperative pulmonary complications and improve oxygenation and respiratory mechanics, but its safety remained to be further clarified [8]. Furthermore, the safety and effectiveness of RM strategy has been greatly enhanced by direct real-time guidance of LUS, but its efficacy is not fully elucidated.

The results of our study suggested that the use of ultrasound-guided RM was associated with a large reduction (more than 50%) in the incidence of atelectasis after abdominal surgery. The findings were consistent with prespecified subgroup analyses for the primary outcome. Depending on the fluctuation of airway pressure, the method for achieving an RM tends to divided into sustained RM and stepwise RM, which is optimal still remains unclear. Our subgroup analyses suggested that both sustained and stepwise RM under ultrasound-guidance represent effective measures for prevention of atelectasis with a non-significant difference. Moreover, perioperative ultrasound-guided RM reduced the incidence of atelectasis in both elderly and non-elderly patients, with no significant difference between the two subgroups. Our subgroup analyses also revealed that the incidence of postoperative atelectasis was significantly lower in the ultrasound-guided RM group, regardless of whether conventional RM was performed in the control group. The results of subgroup analyses confirmed the efficacy of ultrasound-guided RM.

The most clinically evident pathophysiological effect of atelectasis is hypoxemia, and impaired oxygenation during routine general anesthesia was correlated with the degree of atelectasis [34, 35]. The primary mechanisms are the reduced ventilation-to-perfusion ratio and intrapulmonary shunt [36]. Additionally, inflammatory and mechanical factors associated with atelectasis could impair hypoxic pulmonary vasoconstriction [35, 37], thereby leading to hypoxemia; and effective RMs could promptly reverse gas exchange dysfunction. Our findings showed that perioperative use of ultrasound-guided RM was beneficial in improving oxygenation, manifested in the reduced incidence of hypoxemia and increased oxygenation index. We also found that ultrasound-guided RM could shorten PACU and hospital length of stay; of note, the differences, although statistically significant, did not indicate a clinical relevance. Moreover, data regarding PACU and hospital length of stay were transformed from median to mean (SD) in several trials, which may limit the precision of the effect estimate. Thus, the clinical relevance of above endpoints should be explored by further large and definitive RCTs.

The strengths of this review included an exhaustive literature search including major databases and grey literature. From the perspective of evidence-based medicine, it is necessary to collected current evidence on this topic, which included non-SCI or non-English literature. In addition, our methodology followed a rigorous guidance set forth by the Cochrane Collaboration, which included study selection, data extraction, risk-of-bias and certainty assessment. Random-effects models were chosen to reflect the potential clinical heterogeneity of the included studies. Our protocol also featured prespecified subgroup analyses and sensitivity analyses to mitigate the risk of spurious finding; and these analyses demonstrated that ultrasound-guided RM consistently decreased postoperative atelectasis. Finally, there were high certainty of evidence, little between-study heterogeneity and publication bias for the primary outcome.

This study also has several limitations. First, the majority of studies were small single-center RCTs so there is the risk of a ‘small study’ effect, namely a bias raising from the tendency by small studies to publish and report larger and more advantageous effect size than studies with larger sample size. Second, it is important to underline the potential low robustness of arising from the relatively low FI of most included RCTs, thus our results should be interpreted with caution. Third, as elective abdominal surgery encompasses a broad range of surgical procedures, there is inherent heterogeneity of underlying conditions and patient characteristics. A certain variation in intraoperative ventilation strategies amongst the included studies also existed. Fourth, we have focused on investigating the association between ultrasound-guided RM and early postoperative outcomes because of the absence of long-term data in the included RCTs, and further studies are needed to evaluate its consequences on long-term outcomes and patient-centered outcomes, which are fundamental outcomes in anesthesia and perioperative care research. Last, we included only articles in English and Chinese in our study owing to the restriction, and the enrolled studies had not inadequately reported safety outcomes.

In conclusion, our meta-analysis suggests that perioperative ultrasound-guided RM strategy could help reduce the incidence of postoperative atelectasis and improve oxygenation, as well as shorten PACU and hospital length of stay. The optimal strategy including timing and method is not fully elucidated, and further studies are warranted in this area. Additionally, future studies should consider extend follow-up periods and evaluate long-term outcomes, thereby offering insights into the sustained impact of ultrasound-guided RM.

Acknowledgements

Not applicable.

Declarations

Not applicable.

All authors listed above approved the submission of final manuscript.

Competing interests

Professor Hai Yu is a member of the Editorial Board in Anesthesiology and Perioperative Science and recuses himself from every editorial procedure of this submission including peer-review and academic decisions. All authors declare that they have no conflict of interests.

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Titel: Effect of ultrasound-guided recruitment maneuver on atelectasis: a systematic review and meta-analysis of randomized controlled trials
verfasst von: Yi Xu
Yang Han
Huijia Zhuang
Fei Fei
Tingting Zheng
Hai Yu
Publikationsdatum: 01.06.2024
Verlag: Springer Nature Singapore
Erschienen in: Anesthesiology and Perioperative Science / Ausgabe 2/2024
Elektronische ISSN: 2731-8389
DOI: https://doi.org/10.1007/s44254-024-00056-4

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Effect of ultrasound-guided recruitment maneuver on atelectasis: a systematic review and meta-analysis of randomized controlled trials

Abstract

Supplementary Information

Publisher’s Note

1 Introduction