Effect of ultrasound-guided lung recruitment to reduce pulmonary atelectasis after non-cardiac surgery under general anesthesia: a systematic review and meta-analysis of randomized controlled trials

doi:10.21203/rs.3.rs-2625186/v1

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Research Article

Effect of ultrasound-guided lung recruitment to reduce pulmonary atelectasis after non-cardiac surgery under general anesthesia: a systematic review and meta-analysis of randomized controlled trials

https://doi.org/10.21203/rs.3.rs-2625186/v1

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Background

At present, the application of bedside lung ultrasound is increasing gradually, but there is no relevant expert consensus or guidance for its evaluation in the field of perioperative anesthesia. Through this meta-analysis, we tried to determine the impact of ultrasound-guided lung recruitment maneuvers (LRM) on perioperative patients.

Methods

We searched PubMed, Cochrane Library database, Embase and Clinical trials gov for the randomized controlled trials (RCTs) published up to December 31, 2022. The primary outcome was the incidence of postoperative atelectasis. Secondary outcomes included lung ultrasound score (LUS), the incidence of postoperative pulmonary complications (PPCs), the incidence of hypoxemia during resuscitation, driving pressure, lung compliance, mean arterial pressure (MAP), and heart rate (HR). A total of 443 patients were examined in nine randomized controlled trials.

Results

The incidence of atelectasis after surgery in patients with ultrasound-guided LRM was less (RR: 0.31; 95% CI: 0.25–0.40; p < 0.05), the LUS (WMD: -6.24; 95% CI: -6.90-5.59; p < 0.05) and the LUS of each part (LUS difference in front lung region (WMD: -2.00; 95% CI: -2.49 to -1.51; p < 0.05); LUS difference in lateral lung region (WMD: -2.50; 95% CI: -3.20 to -1.80; p < 0.05); The LUS of the posterior lung region was different (WMD: -3.24; 95% CI: -4.23 to -2.24; p < 0.05), and the incidence of hypoxemia during resuscitation was lower (RR: 0.33; 95% CI: 0.15 to 0.72; p < 0.05), and the lung compliance was higher (WMD: 5.30; 95% CI: 3.25 to 7.35; p < 0.05). There was no significant difference in PPCs (RR: 0.84; 95% CI: 0.41 to 1.70; p = 0.63), driving pressure (WMD: -0.24; 95% CI: -1.63 to 1.15; p > 0.05), MAP (WMD: -1.69; 95% CI: -1.69 to 2.40; p > 0.05) and HR (WMD: -2.52; 95% CI: -8.66 to 3.63; p > 0.05).

Conclusion

Ultrasound-guided lung recruitment manoeuvres can enhance perioperative lung aeration and lung compliance while reducing the development of atelectasis.Furthermore, these effects of ultrasound-guided lung recruitment manoeuvres are superior to non-ultrasound-guided ventilation strategy.

lung recruitment maneuver

ultrasound-guided

atelectasis

meta-analysis

Atelectasis is one of the most common postoperative pulmonary complications (PPCs) of general anesthesia, which can be observed in all types of surgery and patients of all ages [1, 2]. Atelectasis is a key factor in the development of most PPCs [3], which leads to a significant increase in the postoperative incidence rate and mortality of patients and consumes medical resources [4, 5]. Especially with the continuous development of minimally invasive surgery, laparoscopic surgery is increasingly carried out in hospitals. However, the development of pneumoperitoneum during laparoscopy and the change in body position (Trendelenburg position) have been shown to harm respiratory function during the procedure, which primarily aggravates atelectasis during the perioperative period [6]. These factors should be taken into consideration. Therefore, preventing atelectasis during perioperative is a huge challenge for anesthesiologists.

Current studies show that the lung recruitment maneuver (LRM) can successfully lower postoperative atelectasis in both children and adults [6, 7]. Its mechanism is to re-open collapsed lung units and increase end-expiratory lung volume by dynamically and instantaneously increasing trans-pulmonary pressure [8]. There are many methods of LRM, including sustained inflation, stepwise LRM through incremental PEEP and postural LRM, etc., but the best method and recruitment pressure are still unclear [9, 10]. The important reason is that the LRM is not monitored in real-time, online and intuitively. Additionally, the pressure carried by the lung unit will increase due to the increased airway pressure brought on by lung re-expansion, at which point the lung unit may suffer damage from excessive expansion [11]. Therefore, without any image monitoring, the value of LRM is significantly reduced. Some clinical studies failed to show the benefit of the results and even produced adverse side effects [12]. The benefits of LRM need to be balanced against the excessive expansion of lung units. Lung ultrasound is an easy-to-use, portable, non-invasive, visible and radiation-free technology widely used in clinical monitoring and diagnosis [13]. The application in the field of perioperative anesthesia can help monitor ventilation and pathological changes. Presently, the relevant research on ultrasound-guided LRM is concentrated in infants and healthy adult patients [14, 15], confirming its feasibility. However, at present, the effect of ultrasound-guided LRM is still unclear. There are differences in the occurrence of postoperative atelectasis between different studies, and there is no consensus on whether it is worth promoting.

We aim to comprehensively evaluate the effect of ultrasound-guided LRM during general anesthesia on the occurrence of postoperative atelectasis and lung ventilation during the perioperative period by comparing it with a non-ultrasound-guided ventilation strategy. Lung ventilation was evaluated by lung ultrasound score (LUS). There are three goals in this study: First, to describe the relevant literature; Second, a meta-analysis was performed to determine the association between ultrasound-guided LRM and patient-related outcomes (including postoperative atelectasis, LUS, lung compliance, driving pressure, and PPCs); Thirdly, when appropriate, we explore the heterogeneity between studies through subgroup analysis.

2.1 Agreement and registration

We report the results of this meta-analysis in compliance with the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines [16]. This study is registered in the International Prospective Register of Systematic Reviews (PROSPERO) with the registration number: CRD42023390320.

2.2 Search Strategy

The two authors (LBC and LWH) independently searched the eligible research in PubMed, Cochrane Library database, Embase and Clinical trials gov up to December 31, 2022. We use the medical subject (MeSH) terms to search "pulmonary atelectasis" and "ultrasound", respectively, and add the search terms "ultrasound guided", "lung ultrasound", and "lung ultrasound" to make the search more comprehensive. In the absence of MeSH terms related to lung recruitment, according to previous literature, we used "lung recruitment manager", "recruitment manager", "recruitment manager" or "RM", "recruitment manager", "recruitment manager", "RM", "open lung", "protected exploitation" or "protective exploitation" to search [17, 18]. Randomized controlled trials only are allowed as the study type. There are no limitations on languages. Combine the findings discussed above to arrive at our conclusions. The search approach is displayed in Table 1.

Table 1

Search strategies.
String	Search
#1	ultrasonography[MeSH Terms]
#2	((((((((((((((((((((((((Diagnostic Ultrasound[Title/Abstract]) OR (Diagnostic Ultrasounds[Title/Abstract])) OR (Ultrasound, Diagnostic[Title/Abstract])) OR (Ultrasounds, Diagnostic[Title/Abstract])) OR (Ultrasound Imaging[Title/Abstract])) OR (Imaging, Ultrasound[Title/Abstract])) OR (Imagings, Ultrasound[Title/Abstract])) OR (Echotomography[Title/Abstract])) OR (Ultrasonic Imaging[Title/Abstract])) OR (Imaging, Ultrasonic[Title/Abstract])) OR (Sonography, Medical[Title/Abstract])) OR (Medical Sonography[Title/Abstract])) OR (Ultrasonographic Imaging[Title/Abstract])) OR (Imaging, Ultrasonographic[Title/Abstract])) OR (Imagings, Ultrasonographic[Title/Abstract])) OR (Ultrasonographic Imagings[Title/Abstract])) OR (Echography[Title/Abstract])) OR (Diagnosis, Ultrasonic[Title/Abstract])) OR (Diagnoses, Ultrasonic[Title/Abstract])) OR (Ultrasonic Diagnoses[Title/Abstract])) OR (Ultrasonic Diagnosis[Title/Abstract])) OR (Echotomography, Computer[Title/Abstract])) OR (Computer Echotomography[Title/Abstract])) OR (Tomography, Ultrasonic[Title/Abstract])) OR (Ultrasonic Tomography[Title/Abstract])
#3	((ultrasound-guided[Title/Abstract]) OR (lung ultrasound[Title/Abstract])) OR (lung ultrasonography[Title/Abstract])
#4	#1 OR #2 OR #3
#5	(((((recruitment maneuver[Title/Abstract]) OR (recruitment maneuvers[Title/Abstract])) OR (RM[Title/Abstract])) OR (open lung[Title/Abstract])) OR (protected ventilation[Title/Abstract])) OR (protective ventilation[Title/Abstract])
#6	pulmonary atelectasis[MeSH Terms]
#7	(((((((((((((((((((((((((((((((((((((((((((((((Atelectases, Pulmonary[Title/Abstract]) OR (Atelectasis, Pulmonary[Title/Abstract])) OR (Pulmonary Atelectases[Title/Abstract])) OR (Lung Collapse[Title/Abstract])) OR (Collapse, Lung[Title/Abstract])) OR (Atelectasis[Title/Abstract])) OR (Atelectases[Title/Abstract])) OR (Congestive Pulmonary Atelectasis[Title/Abstract])) OR (Atelectases, Congestive Pulmonary[Title/Abstract])) OR (Atelectasis, Congestive Pulmonary[Title/Abstract])) OR (Congestive Pulmonary Atelectases[Title/Abstract])) OR (Pulmonary Atelectases, Congestive[Title/Abstract])) OR (Pulmonary Atelectasis, Congestive[Title/Abstract])) OR (Congestive Atelectasis[Title/Abstract])) OR (Atelectases, Congestive[Title/Abstract])) OR (Congestive Atelectases[Title/Abstract])) OR (Atelectasis, Congestive[Title/Abstract])) OR (Resorption Pulmonary Atelectasis[Title/Abstract])) OR (Atelectases, Resorption Pulmonary[Title/Abstract])) OR (Atelectasis, Resorption Pulmonary[Title/Abstract])) OR (Pulmonary Atelectases, Resorption[Title/Abstract])) OR (Pulmonary Atelectasis, Resorption[Title/Abstract])) OR (Resorption Pulmonary Atelectases[Title/Abstract])) OR (Resorption Atelectasis[Title/Abstract])) OR (Atelectases, Resorption[Title/Abstract])) OR (Atelectasis, Resorption[Title/Abstract])) OR (Resorption Atelectases[Title/Abstract])) OR (Contraction Pulmonary Atelectasis[Title/Abstract])) OR (Atelectases, Contraction Pulmonary[Title/Abstract])) OR (Atelectasis, Contraction Pulmonary[Title/Abstract])) OR (Contraction Pulmonary Atelectases[Title/Abstract])) OR (Pulmonary Atelectases, Contraction[Title/Abstract])) OR (Pulmonary Atelectasis, Contraction[Title/Abstract])) OR (Postoperative Pulmonary Atelectasis[Title/Abstract])) OR (Atelectases, Postoperative Pulmonary[Title/Abstract])) OR (Atelectasis, Postoperative Pulmonary[Title/Abstract])) OR (Postoperative Pulmonary Atelectases[Title/Abstract])) OR (Pulmonary Atelectasis, Postoperative[Title/Abstract])) OR (Compression Pulmonary Atelectasis[Title/Abstract])) OR (Atelectases, Compression Pulmonary[Title/Abstract])) OR (Atelectasis, Compression Pulmonary[Title/Abstract])) OR (Compression Pulmonary Atelectases[Title/Abstract])) OR (Pulmonary Atelectases, Compression[Title/Abstract])) OR (Pulmonary Atelectasis, Compression[Title/Abstract])) OR (Compression Atelectasis[Title/Abstract])) OR (Atelectases, Compression[Title/Abstract])) OR (Atelectasis, Compression[Title/Abstract])) OR (Compression Atelectases[Title/Abstract])
#8	#6 OR #7
#9	((randomized controlled trial[Publication Type] OR randomized[Title/Abstract] OR placebo[Title/Abstract] ) OR (RCT[Title/Abstract]))
#10	#4 AND #5 AND #8 AND #9

Mesh: Medical Subject Headings; [Title/Abstract]: search field; [Publication Type]: search field; OR: Boolean logic operator; AND: Boolean logic operator.

2.3 Selection Criteria

Two authors (LBC and LWH) independently assessed the eligibility of studies by reading the titles, abstracts, and full texts. The chief investigator (WXH) arbitrated the disagreements and made final decisions. We included the study according to the following criteria:

Design: Only randomized controlled trials (RCTs) were included, and the study was a human trial.

Age and surgery: The patients included all age groups and underwent non-cardiac surgery.

Intervention measures: In the test group, the lung recruitment strategy was carried out after the ultrasound evaluation or under the guidance of ultrasound, while in the control group, the lung recruitment strategy was not carried out or under the guidance of ultrasound.

(4) Eligible studies must report postoperative atelectasis and at least one of the following results: LUS, LUS of each part, the incidence of PPCs, the incidence of hypoxemia during resuscitation, driving pressure, lung compliance, mean arterial pressure (MAP), and heart rate (HR).

2.4 Results

The primary outcome was the incidence of postoperative atelectasis. Secondary outcomes were LUS, LUS of each part, the incidence of PPCs, the incidence of hypoxemia during resuscitation, driving pressure, lung compliance, MAP, and HR.

We conducted a subgroup analysis based on whether the control group used LRM, the type of LRM used, and whether the test object was adult or child for the classification variable: the incidence of postoperative atelectasis.

2.5 Data Extraction

The two authors (LBC and LWH) extracted the following data from the original full text: the first author, year of publication, study design, surgical type, patient characteristics [age, sex, body mass index (BMI), surgical type, sample size, ASA classification, and whether the control group uses LRM, ventilation settings (FiO₂, VT, PEEP and LRM), postoperative atelectasis, LUS, driving pressure, lung compliance, MAP, HR, pulse oxygen saturation during resuscitation and PPCs. Due to the difference in assessment caused by different examinations, the incidence of postoperative atelectasis here is only determined by lung ultrasound. Each hemithorax was divided into six quadrants. The intercostal space of each of the sections was scanned. Each of the 12 quadrants was assigned a score of 0 to 3 based on the following scoring system: 0, 0 to 2 B lines; 1, at least three B lines or one or more small subpleural consolidations separated by a normal pleural line; 2, multiple coalescent B lines or multiple small subpleural consolidations separated by a thickened or irregular pleural line; 3, consolidation or subpleural consolidation of more than 1 cm × 2cm. The LUS (0 to 36) was calculated by adding the scores for the 12 quadrants, with higher scores indicating more severe aeration loss. The purpose of recording pulse oxygen saturation during resuscitation is to observe the lowest pulse oxygen saturation during resuscitation and to evaluate whether there is hypoxemia. Hypoxemia is defined as pulse oxygen saturation ≤ 95%. Any dispute shall be reviewed and decided by LS and WX.

The continuous data are extracted in the form of means ± standard deviations. According to the suggestion of Cochrane Collaboration, the continuous data expressed in terms of median, interquartile range and range are converted into mean and standard deviation [19]. If the data is only provided in graphic format, GetData Graph Digitizer 2.25(http://getdata-graph-digitizer.com/) is adopted to quantify it.

2.6 Statistical analysis

We used Review Manager 5.3 (Cochrane Collaboration, Oxford, UK) and Stata 17.0 (StataCorp, College Station, Texas, USA) to summarize data according to PRISMA standards. The coefficient I² is calculated to evaluate heterogeneity, which is defined as low (25% -49%), medium (50%-74%) and high (> 75%) levels [20]. Whenever there is significant heterogeneity, we will conduct a meta-analysis by eliminating one study to find the potential source of heterogeneity. P < 0.05 was considered statistically significant. Egger's test was applied to evaluate the publication bias.

2.7 Quality Assessment

We used the Cochrane Collaboration technique to evaluate methodological quality, including random sequence generation, random assignment concealment, blinding of researchers and subjects, blinding of outcome evaluators, and completeness of outcome data, selective reporting of research results, and other biases. Each project contains three levels of bias risk: low bias risk, unclear bias risk and high bias risk. We also use GRADEpro [21] (McMaster University, Hamilton, Ontario, 2014), a method to evaluate the quality of evidence and the degree of strategic recommendations for assessing the quality of evidence.

3.1. Study Characteristics

The research screening process is shown in Fig. 1. At first, we searched 139 potentially relevant studies (Pubmed, 21; Web of Science, 31; Embase, 27; Cochrane Library database, 46; Clinical trials gov.14). Then, 67 duplicates were deleted. The titles and abstracts of the remaining documents were thoroughly reviewed, and 48 unrelated studies such as non-RCT, review, animal experiments or inconsistent research purposes were excluded. Finally, 24 full texts were selected, and only 9 met the inclusion requirements. The reasons for the 15 exclusions were as follows: 4 were clinical registration trials, 2 were cardiac surgery, 5 did not report the results of postoperative atelectasis, 1 reported atelectasis was diagnosed by chest radiograph instead of lung ultrasound, and 3 performed ultrasound-guided or ultrasound-assessed LRM on both the experimental group and the control group. Finally, 9 randomized controlled trials were included in 443 patients [6, 14, 15, 22, 23, 24, 25, 26, 27]. The detailed information of the included study is shown in Table 2.

Table 2

Study characteristics.
Study	Surgery	Age (years)	No.of patients (Male/Female)	ASA	FiO₂(%)	VT (ml/kg)	PEEP (cmH₂O)	LRM (Ultrasound-guided)	LRM (Control)
Ji-Hyun Lee 2020	simple, superficial surgerys	≤ 6years	86 (34/52)	N	0.4	8	5	The recruitment manoeuvre was performed under ultrasound guidance,a steady airway pressure of 15cmH₂O, with 5cmH₂O increments in PEEP until a peak pressure of 30cmH₂O was achieved.	The recruitment manoeuvre was performed by maintaining a steady airway pressure of 15cmH₂O, with 5cmH₂O increments in PEEP until a peak pressure of 30cmH₂O was achieved.
I.-K. Song 2017	elective minor surgery	≤ 1years	40 (25/15)	I-II	0.4	8	5	The recruitment manoeuvre was performed after each lung ultrasound examination; a stepwise increase in airway pressure from 10 cmH₂O by 5 cmH₂O increments was applied manually.	None
Sun-Kyung 2021	laparoscopic gynaecological surgery	N	40 (0/40)	I-II	0.4	8	5	Manual inflation was applied until no collapsed areas were visible on the ultrasound.	The recruitment manoeuvre was performed by manual inflation with a pressure of 30cmH₂O for 10s.
Yi Liu 2022	laparoscopic gynecologic surgery	18–65 years	41 (0/41)	I-II	0.4	6–8	6	The maximum airway pressure was set to start at 10 cmH₂O and gradually increased by 5 cmH₂O until the collapsed lung area was not visible on ultrasound.	None
Young-Eun Jang 2020	elective noncardiac surgery in the prone position	༜3 years	40 (20/20)	N	0.4	6	7	Alveolar recruitment to restore FRC with 30–40 cmH₂O of continuous positive airway pressure via a closed system for approximately 5-10s.	None
Yang, Y 2021	Laparoscopic Surgery for Colorectal Carcinoma	≥ 60 years	40 (30/10)	I-III	0.4	6–8	4	The recruitment manoeuvre were performed with a gradual rise in airway pressure from 10 cmH₂O by 5cmH₂O increments and it was applied manually until no collapsed lung areas were visible on the sonogram.	None
Acosta,C.M. 2018	Non-emergency and non-thoracic surgery	6 months-7 years	42 (36/6)	I-II	0.5	6	5	The recruitment manoeuvre was performed after lung ultrasound examination.PEEP was increased in steps of 5cmH₂O, from 5 to 15cmH₂O, every three breaths. The target recruitment pressure of 30cmH₂O was maintained for 10 breaths.	None
Acosta,C.M. 2021	Non-emergency and non-thoracic surgery	6 months-7 years	41 (26/15)	I	0.4	7	5	The recruitment manoeuvre was performed after lung ultrasound examination.PEEP was increased in steps of 5cmH₂O, from 5 to 15cmH₂O, every three breaths. The target recruitment pressure of 30cmH₂O was maintained for 10 breaths.	None
Acosta, C. M. 2020	Non-emergency and non-thoracic surgery	6 months-5 years	40 (27/13)	I-II	0.5	6	5	Ventilation was turned to pressure control ventilation using a driving pressure of 12 cmH₂O and PEEP of 10 cmH₂O, but they were immediately and sequentially placed: (1) in the left lateral position (90s), (2) in the right lateral position (other 90s), (3) back to the supine position.	None

SD: standard deviation; ASA: American Society of Anesthesiologists; BMI: body mass index; PEEP: positive end-expiratory pressure; C: control;LRM: lung recruitment maneuver;VT:tidal volume; FiO₂: fraction of inspired oxygen ;FRC:functional residual capacity; CPAP: continuous positive airway pressure; N: not reported.

Table 2 shows the basic characteristics of the included study. We included RCTs with ultrasound-guided LRM. These investigations need to use lung ultrasonography to evaluate atelectasis, count the number of cases in the experimental and control groups, and determine whether the difference is statistically significant. Our study defined the experimental group of these studies as the ultrasound-guided LRM group.

Figure 2 shows the results of quality evaluation using Review Manager 5.3. The integrity of outcome data and the risk of selective reporting of research results were rated as low risk in all investigations, indicating low risk in random sequence generation. Three trials [6, 25, 27] did not provide information about random assignment concealment. Two studies [23, 27] did not blind the researcher or the subject, four studies [6, 22, 25, 26] did not describe whether to blind the researcher or the subject, five studies [6, 22, 25, 26, 27] did not describe whether to blind the outcome evaluator, and nine studies [6, 14, 15, 22, 23, 24, 25, 26, 27] have a low risk of other biases.

3.2. Grading Evidence Quality

The results of using GRADEpro to evaluate the quality of evidence are listed in Table 3. We categorize the quality of the evidence into four categories: high, medium, low, and extremely low, based on the risks of bias, inconsistency, indirection, imprecision, and publication bias. Regarding the risk of bias, we listed the risk of all 18 indicators as not serious. Due to I², the inconsistency of LUS, LUS of each part and driving pressure are rated as serious > 50%, indicating unacceptable heterogeneity. Because all studies directly compared the ultrasound-guided LRM with a certain sample size and the control group, the indirectness and imprecision of all indicators were classified as non-serious. Finally, according to the type of LRM, we have moderate confidence in the incidence of hypoxemia during resuscitation, driving pressure, PPCs, and postural LRM. In contrast, we have high confidence in the rest of the results.

Table 3

Quality of evidence by GRADE.
Certainty assessment							№ of patients		Effect		Certainty	Importance
№ of studies	Study design	Risk of bias	Inconsistency	Indirectness	Imprecision	Other considerations	Ultrasound-guided	Control	Relative (95% CI)	Absolute (95% CI)	Certainty	Importance
Incidence of atelectasis
9	randomised trials	not serious	not serious	not serious	not serious	none	52/222 (23.4%)	169/221 (76.5%)	RR 0.31 (0.25 to 0.40)	528 fewer per 1,000 (from 574 fewer to 459 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by Age
9	randomised trials	not serious	not serious	not serious	not serious	none	52/222 (23.4%)	169/221 (76.5%)	RR 0.31 (0.25 to 0.40)	528 fewer per 1,000 (from 574 fewer to 459 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by Age—age ≥ 18(Adult)
3	randomised trials	not serious	not serious	not serious	not serious	none	25/60 (41.7%)	52/61 (85.2%)	RR 0.49 (0.36 to 0.67)	435 fewer per 1,000 (from 546 fewer to 281 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by Age—age༜18(Children)
6	randomised trials	not serious	not serious	not serious	not serious	none	27/162 (16.7%)	117/160 (73.1%)	RR 0.23 (0.17 to 0.33)	563 fewer per 1,000 (from 607 fewer to 490 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by the Type of LRM
9	randomised trials	not serious	not serious	not serious	not serious	none	52/222 (23.4%)	169/221 (76.5%)	RR 0.31 (0.25 to 0.40)	528 fewer per 1,000 (from 574 fewer to 459 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by the Type of LRM - Sustained Inflation
5	randomised trials	not serious	not serious	not serious	not serious	none	33/117 (28.2%)	85/117 (72.6%)	RR 0.39 (0.29 to 0.53)	443 fewer per 1,000 (from 516 fewer to 341 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by the Type of LRM - Stepwise LRM through Incremental PEEP
3	randomised trials	not serious	not serious	not serious	not serious	none	15/85 (17.6%)	64/84 (76.2%)	RR 0.24 (0.15 to 0.37)	579 fewer per 1,000 (from 648 fewer to 480 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by the Type of LRM - Postural LRM
1	randomised trials	not serious	not serious	not serious	serious	none	4/20 (20.0%)	20/20 (100.0%)	RR 0.22 (0.10 to 0.50)	780 fewer per 1,000 (from 900 fewer to 500 fewer)	⨁⨁⨁◯ Moderate	CRITICAL
Subgroup Analysis of Atelectasis by LRM or Non-LRM Used in Control Group
9	randomised trials	not serious	not serious	not serious	not serious	none	52/222 (23.4%)	169/221 (76.5%)	RR 0.31 (0.25 to 0.40)	528 fewer per 1,000 (from 574 fewer to 459 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by LRM or Non-LRM Used in Control Group -Compare to LRM in Control Group
3	randomised trials	not serious	not serious	not serious	not serious	none	14/100 (14.0%)	59/99 (59.6%)	RR 0.24 (0.14 to 0.39)	453 fewer per 1,000 (from 513 fewer to 364 fewer)	⨁⨁⨁⨁ High	CRITICAL
Subgroup Analysis of Atelectasis by LRM or Non-LRM Used in Control Group -Compare to Non-LRM in Control Group
6	randomised trials	not serious	not serious	not serious	not serious	none	38/122 (31.1%)	110/122 (90.2%)	RR 0.35 (0.27 to 0.46)	586 fewer per 1,000 (from 658 fewer to 487 fewer)	⨁⨁⨁⨁ High	CRITICAL
LUS after LRM
6	randomised trials	not serious	not serious	not serious	not serious	none	122	122	-	MD 6.24 lower (6.9 lower to 5.59 lower)	⨁⨁⨁⨁ High	CRITICAL
Driving Pressure
2	randomised trials	not serious	not serious	not serious	serious	none	41	41	-	MD 0.24 lower (1.63 lower to 1.15 higher)	⨁⨁⨁◯ Moderate	CRITICAL
Mean Arterial Pressure
3	randomised trials	not serious	not serious	not serious	not serious	none	62	62	-	MD 0.35 higher (1.69 lower to 2.4 higher)	⨁⨁⨁⨁ High	CRITICAL
Heart Rate
3	randomised trials	not serious	not serious	not serious	not serious	none	62	62	-	MD 2.52 lower (8.66 lower to 3.63 higher)	⨁⨁⨁⨁ High	CRITICAL
Lung Compliance
4	randomised trials	not serious	not serious	not serious	not serious	none	82	82	-	MD 5.3 higher (3.25 higher to 7.35 higher)	⨁⨁⨁⨁ High	CRITICAL
LUS of Each Part of the Lung after LRM
2	randomised trials	not serious	not serious	not serious	not serious	none	120	123	-	MD 2.31 lower (2.69 lower to 1.94 lower)	⨁⨁⨁⨁ High	CRITICAL
LUS of Each Part of the Lung after LRM - Anterior
2	randomised trials	not serious	not serious	not serious	not serious	none	40	41	-	MD 2 lower (2.49 lower to 1.51 lower)	⨁⨁⨁⨁ High	CRITICAL
LUS of Each Part of the Lung after LRM - Lateral
2	randomised trials	not serious	not serious	not serious	not serious	none	40	41	-	MD 2.5 lower (3.2 lower to 1.8 lower)	⨁⨁⨁⨁ High	CRITICAL
LUS of Each Part of the Lung after LRM - Posterior
2	randomised trials	not serious	not serious	not serious	not serious	none	40	41	-	MD 3.24 lower (4.23 lower to 2.24 lower)	⨁⨁⨁⨁ High	CRITICAL
Hypoxemia during Resuscitation
2	randomised trials	not serious	not serious	not serious	serious	none	7/80 (8.8%)	21/79 (26.6%)	RR 0.33 (0.15 to 0.72)	178 fewer per 1,000 (from 226 fewer to 74 fewer)	⨁⨁⨁◯ Moderate	CRITICAL
PPCs
3	randomised trials	not serious	not serious	not serious	serious	none	10/100 (10.0%)	12/100 (12.0%)	RR 0.84 (0.41 to 1.70)	19 fewer per 1,000 (from 71 fewer to 84 more)	⨁⨁⨁◯ Moderate	CRITICAL

CI: confidence interval; MD: mean difference; RR: risk ratio.

3.3. Primary Outcomes

3.3.1 Incidence of postoperative atelectasis: The incidence of postoperative atelectasis was reported in nine studies with 443 patients[6, 14, 15, 22, 23, 24, 25, 26, 27]. Among them, there were 222 cases in the ultrasound-guided LRM group and 221 cases in the control group(Fig. 3). The incidence of postoperative atelectasis in the ultrasound-guided LRM group was lower than in the control group. Low heterogeneity was observed in the results (RR: 0.31; 95% CI: 0.25 to 0.40; p < 0.05; heterogeneity P > 0.10; I² = 37%).

3.3.2 Subgroup analysis of postoperative atelectasis by LRM or non-LRM used in the control group: Whether the control group used LRM or not was reported in the nine studies with 443 patients[6, 14, 15, 22, 23, 24, 25, 26, 27], of which 126 patients in the control group used LRM in two studies[14, 15], and 317 patients in five studies did not use LRM[6, 22, 23, 24, 25, 26, 27]. The findings demonstrated that whether the control group did not employ LRM or did so with non-ultrasound-guided LRM, the incidence of postoperative atelectasis was reduced in patients with ultrasound-guided LRM (compared to non-LRM in the control group: RR = 0.33; 95% CI: 0.25–0.43; P < 0.05; heterogeneity p > 0.10; I² = 30%; compared to LRM in the control group: RR = 0.26; 95% CI: 0.15–0.46; P < 0.05; heterogeneity P < 0.10; I ²=73%)(Fig. 4).

3.3.3 Subgroup analysis of the effect of adults and children on postoperative atelectasis: The incidence of postoperative atelectasis in adults and children were reported in the nine studies with 443 patients[6, 14, 15, 22, 23, 24, 25, 26, 27]. The results showed that ultrasound-guided LRM reduced the incidence of postoperative atelectasis in adults (RR = 0.49; 95% CI: 0.36 to 0.67; p < 0.05; heterogeneity p > 0.10; I² = 0%)(Fig. 5). Using ultrasound-guided LRM also reduces the incidence of postoperative atelectasis in children (RR = 0.23; 95% CI: 0.17 to 0.33; p < 0.05; heterogeneity p > 0.10; I² = 0%). It may be more effective in children than adults (heterogeneity p < 0.05; I² = 89.6%;P for subgroup differences < 0.01).

3.3.4 Subgroup analysis of the effect of LRM type on postoperative atelectasis: 5 studies used sustained inflation[14, 22, 23, 24, 25], 3 studies used stepwise LRM through incremental PEEP[6, 15, 26], and 1 study used postural LRM[27]. The results showed that sustained inflation reduced the incidence of postoperative atelectasis, and stepwise LRM through incremental PEEP and postural LRM achieved this effect more significantly(Fig. 6). However, due to insufficient studies, we should be cautious about the effect of posture LRM on postoperative atelectasis. There is only one study of postural LRM, which is not applicable to heterogeneity analysis. The other two studies are low heterogeneity (sustained inflation: RR = 0.39; 95% CI: 0.29 to 0.53; p < 0.05; heterogeneity p > 0.10; I² = 16%; stepwise LRM through incremental PEEP: RR = 0.24; 95% CI: 0.15 to 0.37; p < 0.05; heterogeneity p > 0.10; I² = 0%; postural LRM: RR = 0.22; 95% CI: 0.10 to 0.50; p < 0.05).

3.4. Secondary Outcomes

3.4.1 LUS: The LUS after surgery was reported in six studies with 244 patients[6, 14, 23, 25, 26, 27], and the other three reported consolidation and B-line scores[15, 22, 24]. The LUS after surgery was statistically different between the ultrasound-guided LRM and the control group(Fig. 7). The LUS after surgery in the ultrasound-guided LRM group was lower. High heterogeneity was observed in the results (WMD: -6.24; 95% CI: -6.90 to -5.59; p < 0.05; heterogeneity p < 0.10; I² = 87%).

3.4.2 LUS of each part: Two studies, including 81 patients, reported LUS of each part after surgery[22, 23]. After the surgery, the LUS of each part is as follows: LUS in anterior lung region (WMD: -2.00; 95% CI: -2.49 to -1.51; p < 0.05); LUS in lateral lung region (WMD: -2.50; 95% CI: -3.20 to -1.80; p < 0.05); LUS in the posterior lung region (WMD: -3.24; 95% CI: -4.23 to -2.24; p < 0.05; heterogeneity p > 0.10; I² = 59%)(Fig. 8). The results showed that compared with the control group, the ultrasound-guided group could reduce the LUS of the anterior, lateral and posterior parts, and the results were statistically significant.

3.4.3 PPCs: PPCs were reported in three studies with 200 patients[14, 15, 25]. There was no significant difference in PPCs between the ultrasound-guided LRM and the control group(Fig. 9). The results observed no heterogeneity (RR: 0.84; 95% CI: 0.41 to 1.70; p = 0.63; heterogeneity p > 0.10; I² = 0%).

3.4.4 Hypoxemia during resuscitation: Hypoxemia during resuscitation was reported in two studies with 159 patients[15, 24]. The results showed that ultrasound-guided LRM helped reduce the incidence of hypoxemia during resuscitation(Fig. 10). The results observed no heterogeneity (RR: 0.33; 95% CI: 0.15 to 0.72; p < 0.05; heterogeneity p > 0.10; I² = 0%).

3.4.5 Driving pressure: Driving pressure was reported in two studies with 82 patients[6, 14]. There was no significant difference in driving pressure between the two groups(Fig. 11). High heterogeneity was observed in the results (WMD: -0.24; 95% CI: -1.63 to 1.15; p > 0.05; heterogeneity p < 0.10; I² = 92%).

3.4.6 Lung compliance: Lung compliance was reported in four studies involving 164 patients[6, 14, 26, 27]. Compared with the control group, lung compliance in the ultrasound-guided LRM group is helpful in improving lung compliance(Fig. 12). Low heterogeneity was observed in the results (WMD: 5.30; 95% CI: 3.25–7.35; p < 0.05; heterogeneity p > 0.10; I² = 39%).

3.4.7 MAP: Three studies examined the MAP differences in 124 patients[6, 14, 26]. There was no statistical difference in MAP between the two groups, and low heterogeneity was observed in the results (WMD: -1.69; 95% CI: -1.69 to 2.40; p > 0.05; heterogeneity p > 0.10; I² = 36%)(Fig. 13).

3.4.8 HR: Three studies examined the HR differences in 124 patients[6, 14, 26]. There was no statistical difference in HR between the two groups, and no heterogeneity was observed in the results (WMD: -2.52; 95% CI: -8.66 to 3.63; p > 0.05; heterogeneity p > 0.10; I² = 0%)(Fig. 14).

3.5 Publication bias

The funnel plot of primary outcomes is presented in Fig. 15 (Incidence of postoperative atelectasis). The funnel plot was used to evaluate the publication bias of the included study. Visual inspection of the funnel plot found no evidence of publication bias in the primary outcome. Combined with the funnel plot results, the results of the Egger test showed that the Egger test t = 0.16, P>| t |=0.874 (P > 0.05) suggested there was little possibility of publication bias in the nine articles included.

This meta-analysis included 9 randomized controlled trials to compare the ultrasound-guided LRM strategy with the non-ultrasound-guided ventilation strategy in patients undergoing non-cardiac surgery. LRM is an effective method to reduce postoperative atelectasis. However, few systematic evaluations or meta-analyses report the impact of ultrasound-guided LRM on patients. Therefore, it is necessary to comprehensively analyze the previous randomized controlled trials. Our results show that for the patients undergoing non-cardiac surgery, compared with the non-ultrasound-guided ventilation strategy, ultrasound-guided RM can reduce the incidence of atelectasis after surgery, the LUS and the incidence of hypoxemia during resuscitation, and improve lung compliance while there is no significant difference in driving pressure, PPCs, MAP and HR. The heterogeneity of LUS is high, while the incidence of atelectasis, PPCs, hypoxemia during resuscitation, MAP and HR is low. The heterogeneity of LUS may come from several sources. First, the enrolled patients have a wide range of ages and different operations. Secondly, the intraoperative ventilation strategy is highly variable. Tidal volume, LRM and PEEP can affect oxygenation and respiratory mechanics, resulting in differences in LUS changes after LRM.

In terms of the effectiveness of ultrasound-guided LRM, according to the study of Monassese et al. [28], the LUS in the lung ultrasound image is significantly related to the degree of ventilation function damage and the number of atelectasis areas. According to the results of this study, the LUS of the ultrasound-guided LRM group decreased by 6.24 points on average compared with the non-ultrasound control group after the surgery, and the number of atelectasis in the ultrasound-guided LRM group (23.4%) after the surgery was significantly lower than that in the non-ultrasound control group (76.5%). The above results also help to confirm the good consistency between LUS and the diagnosis of atelectasis. Among the LUS of atelectasis sites, the LUS of the posterior lung region is the highest, and the effect of LRM is the most significant. The findings support the idea that atelectasis occurs in gravity-dependent regions [29], and ultrasound-guided LRM lowers the LUS of the posterior lung area by an average of 3.24 points, which is significantly better than that of the non-ultrasound control group. This finding supports the idea that lung ultrasound has some advantages in visualizing and purposefully guiding lung recruitment strategy. The technique of ultrasound-guided LRM can dramatically lower the frequency of postoperative atelectasis during surgery and lessen the severity of atelectasis, according to the aforementioned findings.

We classified the methods of LRM used in the included studies, including sustained inflation, stepwise LRM through incremental PEEP and postural LRM. Sustained inflation sets the airway pressure to a high value and continuously ventilates for a period of time. This is usually achieved by adjusting the airway pressure limit valve on the ventilator and squeezing the airbag. The stepwise LRM through incremental PEEP is to gradually increase the airway pressure by increasing PEEP. The postural LRM uses the mechanical ventilation strategy of changing the posture under the condition of conventional ventilation and re-expanding the atelected alveoli into an oxygenated state. After subgroup analysis of three types of methods, the results showed that using sustained inflation, stepwise LRM through incremental PEEP and postural LRM in the ultrasound-guided group could reduce the incidence of postoperative atelectasis. The RR value of stepwise LRM through incremental PEEP and postural LRM is lower than that of sustained inflation. The incidence of atelectasis in patients with stepwise LRM through incremental PEEP is 17.6%, while in patients with sustained inflation is 28.2%. This also shows that although sustained inflation is easy to implement and widely used in the clinical environment when switching back to machine control mode, there is a risk of alveolar collapse again. Relevant animal studies have found that [30, 31, 32] the high inspiratory flow rate caused by sustained inflation can cause damage to the alveolar-capillary membrane and the translocation of bacteria and cytokines into the systemic circulation. The clinical study [33] found that the benefits of sustained inflation were limited due to unstable circulatory dynamics, increased barotrauma and volume injury, increased intracranial pressure [34] and decreased alveolar fluid clearance, leading to poor oxygenation and other serious clinical adverse reaction [35]. Therefore, although the stepwise LRM through incremental PEEP takes longer, it is also considered more physiological. It simulates the sigh movement of healthy people during normal breathing and can offset the tendency of alveolar collapse during low tidal volume ventilation [36]. In addition, although the risk ratio of postural LRM in this study was the lowest, it is still advised that more studies be conducted to fully understand the effect because postural LRM was only included in one study, and the sample size was small.

Although ultrasound-guided LRM significantly reduced the incidence of postoperative atelectasis in both the children and adults subgroups, the overall risk of postoperative atelectasis after ultrasound-guided LRM in the children subgroup was 23%, significantly lower than 49% in the adult subgroup. The following two factors should be considered: Firstly, Yang Y et al. [25] in the adult subgroup are laparoscopic surgery for the elderly, and Yi Liu et al.[23] are also included in laparoscopic surgery for some elderly patients; Secondly, in the adult subgroup, the operation is more complicated, resulting in longer mechanical ventilation time. "Lung-protective ventilation for the surgical patient: international expert panel-based consensus recommendations" [37] published in 2019 indicates that age > 50 years old and mechanical ventilation time > 2 h are risk factors for atelectasis. Hence, the adult subgroup in the study has a higher risk of postoperative atelectasis. It also shows the necessity of LRM in such operations. It is also anticipated that future pertinent studies will provide more conclusive results to confirm the viability of ultrasound-guided surgery in the elderly population because most current studies concentrate on ultrasound-guided LRM in children, while very few studies are conducted on the elderly population at high risk of postoperative atelectasis.

Whether the control group uses LRM is also worth further discussion. Although the control group in some studies using low tidal volume and PEEP, they did not undergo lung re-expansion during operation [6, 22, 23, 24, 25, 26, 27], while the control group in the remaining studies used non-ultrasound-guided RM during operation [14, 15]. Whether or not the control group had experienced postoperative atelectasis, the data demonstrated that the incidence of the condition was decreased in the ultrasound-guided group. Surprisingly, compared with the subgroup of the control group who underwent LRM, the patients who did not undergo LRM had a lower risk of postoperative atelectasis. Ji-Hyun Lee et al.[15] found in their study that although the patients underwent LRM, the control of the airway pressure of 30 cm H₂O could not ensure the regression of alveolar atelectasis. Most patients in the ultrasound-guided group needed more than 30 cm H₂O pressure to make the alveolar re-expansion. Therefore, the two studies, including LRM in the control group, limited the airway pressure below 30 cm H₂O, which also limited the advantages of LRM, and verified that ultrasound-guided high-quality LRM is an important means to ensure the effectiveness of LRM. In the past, there was no high-quality evidence to recommend routine LRM after tracheal intubation for patients undergoing general anesthesia. Anesthesiologists need to evaluate the risk-benefit ratio of patients in order to develop treatment plans. Blind lung recruitment may benefit patients less and have adverse effects. What helps to eliminate such concerns is the significance of ultrasound-guided lung recruitment.

The three studies [14, 15, 25 ] included in this meta-analysis mentioned PPCs. It can be seen that there is no significant difference in PPCs between the two groups, indicating that although ultrasound-guided LRM is guided accurately by the advantage of visualization, it does not reduce the incidence of PPCs. According to previous studies [38, 39], it is still controversial whether intraoperative LRM can reduce the incidence of PPCs in patients. Some studies have shown that it can reduce the incidence of PPCs and improve the prognosis of patients. Still, there are also large sample studies [40] that the intraoperative LRM in patients undergoing major abdominal surgery does not reduce the risk of PPCs. Based on the results of previous studies and this study, it can be considered that the ultrasound-guided LRM during operation will not increase or aggravate the incidence of PPCs, but it is not certain to reduce the incidence of PPCs and improve the prognosis of patients with PPCs. This has a certain relationship with the risk factors that produce PPCs [41], including patient-related risk factors (such as chronic obstructive pulmonary disease(COPD), aging, smoking, pulmonary hypertension and malnutrition) and perioperative risk factors (such as surgical site, anesthesia mode, emergency surgery and long mechanical ventilation time). Therefore, there are differences in the occurrence of PPCs in complex clinical environments. The incidence of hypoxemia during resuscitation was also reported in two studies [15, 24], and it was discovered that the ultrasound-guided LRM group could lessen the incidence of hypoxemia. Therefore, according to the above conclusions, ultrasound-guided LRM has certain advantages over a non-ultrasound-guided ventilation strategy. Although it has no obvious effect on PPCs, its advantages in improving short-term oxygenation are still worthy of attention.

We analyzed two indicators related to pulmonary function: lung compliance and driving pressure. The results showed that ultrasound-guided LRM improved lung compliance, but there was no significant difference in driving pressure. Christopher et al. [42] showed that in patients who received mechanical ventilation during general anesthesia, the increased driving pressure was related to an increased incidence of PPCs, and lower driving pressure might have lung protection. Another meta-analysis [43] showed that driving pressure was a significant factor affecting the incidence of PPCs in the lung protective ventilation strategy. There was no statistical difference in the driving pressure in this study, which to some extent, explained that there was no significant difference in PPCs.

The effect on hemodynamics during LRM is noteworthy. We evaluated two hemodynamic parameters: MAP and HR. There was no significant difference between the non-ultrasound-guided group and the ultrasound-guided group. However, we cannot show that RM has no impact on the circulation system on this basis. The time point of multiple data records is after the end of LRM, and the hemodynamic parameters during the implementation of LRM are not recorded. In fact, the increase of trans-pulmonary pressure (TP) during LRM will lead to the increase of central venous pressure (CVP), pulmonary vascular resistance index (PVRI) and pulmonary artery pressure (PAP), which will increase the preload and afterload of the right ventricle, and lead to the temporary decrease of left and right ventricular ejection fraction (R/LVEF) during LRM. Cherabi et al. [44] showed that the effect of LRM on the right ventricle was temporary. The hemodynamics also returned to normal with the decrease in high airway pressure.

There are some limitations of this meta-analysis that need to be taken into account. ① The included studies have significant clinical differences in surgical type, anesthesia induction, mechanical ventilation time and LRM. Ideally, data such as PEEP level, type of LRM, specific operation or population, duration of mechanical ventilation and other data are analyzed one by one to determine the best lung protective ventilation strategy for different populations in a specific operation. However, there is still a dearth of high-quality studies to help select the most personalized lung protective ventilation approach for various individuals and operations. Lung ultrasound has not yet found widespread use in the field of perioperative use; ② Low-risk patients recover from atelectasis quickly after short surgery, and it is uncertain whether the patients receiving short-term mechanical ventilation benefit from lung protective ventilation, including the use of low tidal volume, high level of PEEP and/or various LRM during surgery; ③ Lung ultrasound has not been widely used in clinical practice. Anesthesiologists, rather than professional ultrasound doctors, evaluate some studies. At this time, the anesthesiologists' techniques and experience may cause some errors in the evaluation results; ④ The results of this meta-analysis are only limited to patients without lung disease, patients with high-risk and complicated lung disease or emergency surgery, and further research is needed; ⑤ The RCTs included in this study are single-center and small-sample trials, which may have bias risk. In the future, multi-center and large-sample trials are needed to improve the analysis results.

LRM:Lung recruitment maneuvers;RCTs:Randomized controlled trials;LUS:Lung ultrasound score;PPCs:Postoperative pulmonary complications;MAP:Mean arterial pressure;HR:Heart rate; MeSH: Medical Subject Headings; RR: Relative risk;PRISMA: Preferred Reporting Items for the Systematic Reviews and Meta-Analyses;MD:Mean diferences;WMD:Weighted mean difference;SD:Standard deviation; ASA:American Society of Anesthesiologists;BMI:Body mass index; PEEP:Positive end-expiratory pressure;C:Control;VT:Tidal volume;FiO2:Fraction of inspired oxygen;FRC:Functional residual capacity;N:Not reported;CI:Confidence interval;COPD:Chronic obstructive pulmonary disease;TP:Trans-pulmonary pressure;CVP:Central venous pressure;PVRI:Pulmonary vascular resistance index;PAP:Pulmonary artery pressure.

Acknowledgements

We acknowledge all staf who helped perform this study.

Author Contributions

LBC designed the study, searched the scientific literature, collected the data and drafted the manuscript. LWH searched the scientific literature, collected the data and performed statistical analyses. WXH conducted quality assessment, resolved differences, helped to revise the manuscript, provided administrative and technical support. LSJ contributed to the conception of the study, searched the scientific literature, collected the data and revised the manuscript. All authors read and approved the final manuscript and take public responsibility for it.

Funding Statement

This work was supported by General Program for Clinical Research at Peking University Shenzhen Hospital(Grant No.LCYJ2020016).

Availability of data and materials

All data generated or analysed during this study are included in this published article [and its supplementary information files].

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

There were no conficts of interest.

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No competing interests reported.

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Effect of ultrasound-guided lung recruitment to reduce pulmonary atelectasis after non-cardiac surgery under general anesthesia: a systematic review and meta-analysis of randomized controlled trials

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1. Introduction

2. Materials And Methods

2.1 Agreement and registration

2.2 Search Strategy

2.3 Selection Criteria

2.4 Results

2.5 Data Extraction

2.6 Statistical analysis

2.7 Quality Assessment

3. Results

3.1. Study Characteristics

3.2. Grading Evidence Quality

3.3. Primary Outcomes

3.4. Secondary Outcomes

3.5 Publication bias

4. Discussion

5. Conclusion

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