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Critical care
Original research
Non-invasive ventilation versus invasive weaning in critically ill adults: a systematic review and meta-analysis
  1. Karen E A Burns1,2,3,4,5,
  2. James Stevenson6,
  3. Matthew Laird6,
  4. Neill K J Adhikari1,7,8,
  5. Yuchong Li2,5,
  6. Cong Lu2,5,
  7. Xiaolin He5,
  8. Wentao Wang9,
  9. Zhenting Liang8,
  10. Lu Chen2,5,
  11. Haibo Zhang1,2,5,10,
  12. Jan O Friedrich1,2,3,5
  1. 1 Interdepartmental Division of Critical Care Medicine, Temerty Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
  2. 2 Departments of Critical Care and Medicine, Unity Health Toronto – St. Michael’s Hospital, Toronto, Ontario, Canada
  3. 3 The Temerty Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
  4. 4 Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton, Ontario, Canada
  5. 5 Keenan Research Centre for Biomedical Science and the Li Ka Shing Knowledge Institute, St. Michael’s Hospital, Toronto, Ontario, Canada
  6. 6 The School of Medicine, Royal College of Surgeons, Dublin, Ireland
  7. 7 Department of Critical Care Medicine, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada
  8. 8 Institute of Health Policy, Management, and Evaluation, University of Toronto, Toronto, Ontario, Canada
  9. 9 The Department of Critical Care Medicine, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, China
  10. 10 Department of Anesthesia and Physiology, University of Toronto, Toronto, Ontario, Canada
  1. Correspondence to Dr Karen E A Burns, Critical Care, Unity Health Toronto, Toronto, Canada; karen.burns{at}unityhealth.to

Abstract

Background Extubation to non-invasive ventilation (NIV) has been investigated as a strategy to wean critically ill adults from invasive ventilation and reduce ventilator-related complications.

Methods We searched MEDLINE, EMBASE, the Cochrane Central Register of Controlled Trials, proceedings of four conferences and bibliographies (to June 2020) for randomised and quasi-randomised trials that compared extubation with immediate application of NIV to continued invasive weaning in intubated adults and reported mortality (primary outcome) or other outcomes. Two reviewers independently screened citations, assessed trial quality and abstracted data.

Results We identified 28 trials, of moderate-to-good quality, involving 2066 patients, 44.6% with chronic obstructive pulmonary disease (COPD). Non-invasive weaning significantly reduced mortality (risk ratio (RR) 0.57, 95% CI 0.44 to 0.74; high quality), weaning failures (RR 0.59, 95% CI 0.43 to 0.81; high quality), pneumonia (RR 0.30, 95% CI 0.22 to 0.41; high quality), intensive care unit (ICU) (mean difference (MD) −4.62 days, 95% CI −5.91 to −3.34) and hospital stay (MD −6.29 days, 95% CI −8.90 to −3.68). Non-invasive weaning also significantly reduced the total duration of ventilation, duration of invasive ventilation and duration of ventilation related to weaning (MD −0.57, 95% CI −1.08 to −0.07) and tracheostomy rate. Mortality, pneumonia, reintubation and ICU stay were significantly lower in trials enrolling COPD (vs mixed) populations.

Conclusion Non-invasive weaning significantly reduced mortality, pneumonia and the duration of ventilation related to weaning, particularly in patients with COPD. Beneficial effects are less clear (or more careful patient selection is required) in non-COPD patients.

PROSPERO registration number CRD42020201402.

  • critical care
  • COPD exacerbations
  • non invasive ventilation

Data availability statement

Data are available from KEAB. Data are available from Dr. Burns (0000-0002-9967-5424) .

http://dx.doi.org/10.1136/thoraxjnl-2021-216993

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    Key messages

    What is the key question?

    • What is the effect of non-invasive and invasive weaning in randomised or quasi-randomised trials of critically ill adults on mortality (primary outcome), pneumonia, weaning failures and other clinically important outcomes?

    What is the bottom line?

    • High-quality evidence suggests that non-invasive (vs invasive) weaning significantly reduced mortality, pneumonia and the proportion of weaning failures, and subgroup analyses found that non-invasive weaning reduced mortality, pneumonia, reintubation and intensive care unit length of stay in trials enrolling chronic obstructive pulmonary disease (COPD) (vs mixed) populations.

    Why read on?

    • Pooled data support the net clinical benefits associated with the non-invasive approach to weaning on important clinical outcomes, particularly in patients with COPD, while more careful patient selection is required in non-COPD patients.

    Introduction

    Mechanical ventilation is often required to support critically ill patients with acute respiratory failure (ARF). Although life-saving, invasive ventilation is associated with ventilator-related complications, such as ventilator-associated pneumonia (VAP). VAP, in turn, is associated with attributable mortality of approximately 13%.1 Cumulative exposure to invasive mechanical ventilation is associated with long-term sequelae including muscle weakness,2 3 reduced health-related quality of life,4 5 post-traumatic stress disorder,6 7 depression,8 delirium9 and cognitive impairment.10 Consequently, minimising patients’ exposure to invasive mechanical ventilation has been identified as a key research priority by critical care societies.11

    Non-invasive ventilation (NIV), administered with a patient–ventilator interface, can provide partial ventilator support to patients with ARF without the need for an artificial airway. Interfaces include nasal mask, oronasal mask, full face masks, mouthpiece, nasal pillows and helmets.12 NIV does not provide airway protection. Similar to invasive ventilation, NIV can augment tidal volumes, reduces respiratory rates, apply positive end-expiratory pressure and improve gas exchange.12 13 Unlike invasive mechanical ventilation, NIV preserves patient’s ability to cough, swallow and speak.14 Patients who are treated with NIV may receive less invasive monitoring and sedation15 and experience less psychological distress.16 For these reasons, investigators have studied NIV as a method to reduce patient’s exposure to invasive mechanical ventilation during weaning. With this technique, patients who do not meet conventional criteria for extubation (ie, fail a spontaneous breathing trial (SBT) or are not ready to undergo an SBT) are extubated directly to NIV. Non-invasive support is then reduced over time, minimising patients’ exposure to invasive ventilation and related complications.

    To better understand the net clinical benefits associated with non-invasive weaning, we sought to critically appraise, summarise and update a prior systematic review and meta-analysis17 of the effect of non-invasive weaning compared with invasive weaning on important outcomes in light of new evidence.

    Methods

    Data sources and searches

    We updated a previously conducted search of MEDLINE (January 1966 to July 2021), EMBASE (January 1980 to July 2021) via Ovid SP and the Cochrane Central Register of Controlled Trials (CENTRAL) (the Cochrane Library 2012, July 2021) without language restrictions. Details of the search strategies used are provided in online supplemental appendix 1. Two reviewers (JS, ML) independently screened citation titles and abstracts. One reviewer (JOF) updated manual searches of abstracts from conference proceedings published in the American Journal of Respiratory and Critical Care Medicine, Intensive Care Medicine, Critical Care Medicine and Chest from June 2013 to August 2020. We reviewed bibliographies of retrieved articles to identify potentially relevant trials, contacted authors to obtain additional information regarding study methods where needed and searched for ongoing trials on www.isrctn.com and www.clinicaltrials.gov.

    Supplemental material

    Study selection

    We included randomised and quasi-randomised trials that (1) enrolled adults with respiratory failure who required invasive mechanical ventilation for at least 24 hours but before they met conventional criteria for extubation, (2) compared extubation with immediate application of NIV to continue the ventilation weaning process with continued invasive weaning and (3) reported at least one of mortality (primary outcome), VAP, weaning failure (using authors’ definitions), intensive care unit (ICU) or hospital length of stay, total duration of ventilation, duration of ventilation related to weaning, duration of invasive ventilation, adverse events or quality of life. We excluded trials that compared non-invasive with invasive weaning in the immediate postoperative setting (typically with less than 24 hours of invasive ventilation), compared NIV with unassisted oxygen supplementation and investigated NIV after unplanned extubation.

    Data abstraction and risk of bias assessment

    Two unblinded authors (JS, ML) abstracted data regarding risk of bias (randomisation, allocation concealment, completeness of follow-up, selective outcomes reporting) using a standardised data abstraction form. We did not formally assess blinding in these necessarily unblinded trials. Disagreements regarding study selection and data abstraction were resolved by consensus and arbitration with a third author (KEAB).

    Data synthesis and statistical analysis

    We pooled data across studies using random effects models. We derived summary estimates of risk ratio (RR) and mean difference (MD) with 95% CIs for binary and continuous outcomes, respectively, using Review Manager V.5.4 (Cochrane Collaboration, Oxford).18 If an outcome was reported at two different times, we included the more protracted measure in pooled analyses (eg, mortality).

    We evaluated the impact of statistical heterogeneity among pooled studies for each outcome using the Cochran Q statistic (threshold p<0.10)19 20 and the I2 statistic21 22 with threshold values of 0%–40%, 30%–60%, 50%–90% and >75% representing heterogeneity that might not be important or represent moderate, substantial or considerable heterogeneity, respectively.22 If a heterogeneity value overlapped two categories, we assigned it the higher heterogeneity rating. In sensitivity analyses, we assessed the impact of excluding quasi-randomised trials on estimates of mortality and VAP. We planned subgroup analyses to compare the effects of non-invasive weaning on mortality and weaning failures in studies of patients with chronic obstructive pulmonary disease (COPD) only compared with mixed populations (any non-COPD) and in studies that enrolled >50% versus <50% patients with COPD. We assessed for differences between subgroup summary estimates using the χ2 test.23 We examined funnel plots visually for evidence of publication bias. We used the principles of grades of recommendation, assessment, development, and evaluation (GRADE)24 to assess the quality of the body of evidence associated with specific outcomes (mortality, weaning failure, VAP, duration of ventilation related to weaning and reintubation).

    Results

    Trial identification

    We previously identified 16 trials25–40 meeting our eligibility criteria. In updated searches of 971 records (online supplemental appendix 1), we assessed 20 new articles for eligibility (figure 1). Of these, we included 12 new trials41–52 that evaluated NIV as a weaning strategy. One trial28 was previously assessed to be quasi-randomised. We were unable to clarify whether another trial42 reported as ‘randomised’ was truly randomised or quasi-randomised. One trial did not include outcomes data by group and only contributed data to the quality assessment.41 In summary, we included 28 trials reporting on 2066 patients in our updated review.

    Figure 1
    Figure 1

    Trial selection process. This review represents an update of a previously conducted systematic review and meta-analysis.16

    Of the 28 included trials, 4 trials were published only in abstract form,27 30 41 43 8 trials were published in Chinese,28 31 33 34 42 48 49 52 1 trial was a dissertation subsequently published in full36 and another was a pilot randomised controlled trial (RCT).40 We excluded 19 studies53–71 including 8 newly excluded publications (figure 1).72–79 The two reviewers (JS, ML) achieved complete agreement on study selection.

    Fourteen trials included exclusively COPD (n=922) patients (table 1).25 28 30–34 36 38 42 43 45 47 52 Of non-COPD trials, COPD was diagnosed in approximately 75% of patients in three trials,26 29 37 approximately one-third of patients in two trials,27 35 over 20% of patients in another trial39 46 and unspecified in a final trial.41 Three trials excluded patients with COPD40 49 51 and one trial each focused exclusively on specific patient populations including after cardiac surgery,44 elderly patients with severe community-acquired pneumonia49 and adults with acute respiratory distress syndrome48 or hypoxemic respiratory failure.51 The largest trial stratified on the presence of COPD but included less than 4% of patients with COPD.50

    View this table:
    Table 1

    Populations and interventions in studies of non-invasive ventilation (NIV) in critically ill adults

    Patients were considered difficult to wean in two trials26 37 and persistent weaning failures in another trial.29 Five trials31–34 43 included COPD patients with respiratory failure due to pulmonary infection. No included trials evaluated high-flow nasal cannulae in the intervention group.

    Quality assessment

    Overall, the quality of the included trials was moderate-to-good (figure 2). In most trials, allocation to treatment group was by random assignment with one quasi-randomised confirmed to allocate patients according to hospital admission order.28 We judged allocation concealment to be adequate in 13 trials,25 27 29 30 37–40 44 47 50–52 unclear in 14 trials26 31–36 41–43 45 46 48 49 and inadequate in a quasi-randomised trial.28 In three trials,33 34 41 denominators were not provided in binary outcomes to ensure complete outcomes reporting. One trial49 was deemed to be at high risk of bias due to incomplete outcomes reporting as >5% of the patients (4 NIV arm, 1 control arm) were excluded post randomisation. With regard to selective outcomes reporting two trials were deemed to be at high risk of bias29 41 and three trials were deemed to be at unclear risk of bias28 44 45 (online supplemental appendix 2). On inspection of a funnel plot for the primary outcome, we noted the potential absence of small negative trials (online supplemental appendix 3).

    Supplemental material

    Supplemental material

    Supplemental material

    Figure 2
    Figure 2

    Risk of bias of the included trials. Green, yellow and red circles represent low, unclear and high risk of bias, respectively.

    Primary outcome: mortality

    Twenty-seven trials involving 2042 patients (increase of 1048) provided mortality data. Mortality was reported at 30 days,36 39 45 50 60 days,25 49 90 days,26 29 50 180 days,50 ICU37 40 46 47 50–52 and hospital discharge26 30 32–35 38 40–44 46 50 51 and at undefined times.27 28 31 48 There was strong evidence that non-invasive weaning reduced mortality (RR 0.57, 95% CI 0.44 to 0.74; p≤0.0001; high quality) with moderate heterogeneity (I2=27%) (figure 3).

    Figure 3
    Figure 3

    Effect of non-invasive weaning on mortality. COPD, chronic obstructive pulmonary disease; M-H, Mantel-Haenszel.

    Secondary outcomes

    Eleven trials involving 829 patients, using variable definitions, reported the proportion of patients successfully weaned.25–27 30 37–40 43 46 51 The pooled data demonstrated a significant reduction in the proportion of weaning failures using non-invasive weaning (RR 0.59, 95% CI 0.43 to 0.81; p=0.001; high quality) with low heterogeneity (I2=22%).

    Pooled data from 23 trials involving 1581 (increase of 628) patients25 26 28–39 42 43 45–49 51 52 that reported VAP for which criteria for the diagnosis were provided in 10 trials25 28 29 31–36 39 42 45–48 50 51 showed that non-invasive weaning was associated with decreased VAP (RR 0.30, 95% CI 0.22 to 0.41; p<0.00001; high quality) with low heterogeneity (I2=24%) (figure 4).

    Figure 4
    Figure 4

    Effect of non-invasive weaning on ventilator-associated pneumonia. COPD, chronic obstructive pulmonary disease; M-H, Mantel-Haenszel.

    Meta-analysis also supported that non-invasive weaning significantly reduced ICU (MD −4.62 days, 95% CI −5.91 to −3.34; p<0.00001, I2=80%) and hospital (MD −6.29 days, 95% CI −8.90 to −3.68; p<0.00001, I2=75%) stay, total duration of mechanical ventilation (MD −5.26 days, 95% CI −7.86 to −2.67; p<0.0001, I2=83%) and duration of invasive ventilation (MD −7.75 days, 95% CI −9.86 to −5.64; p<0 00 001, I2=94%), all with considerable heterogeneity. Non-invasive weaning significantly reduced the duration of mechanical ventilation related to weaning (MD −0.57 days, 95% CI −1.08 to −0.07; p=0.03; moderate quality due to inconsistency with I2=88%) favouring non-invasive weaning (figure 5). No study reported quality of life (table 2).

    Figure 5
    Figure 5

    Effect of non-invasive weaning on duration of ventilation related to weaning. COPD, chronic obstructive pulmonary disease; IV, intravenous.

    View this table:
    Table 2

    Summary estimates of effect of non-invasive ventilation in critically ill adults

    Adverse events

    The pooled result showed no difference in arrhythmias (RR 0.70, 95% CI 0.41, 1.20; four trials, 565 patients),26 36 37 50 non-significantly lower reintubation (RR 0.69, 95% CI 0.47 to 1.01; 14 trials, moderate quality due to inconsistency, 1336 patients)26–29 32 34 35 37–40 46 48 50 and tracheostomy rates (RR 0.25, 95% CI 0.10 to 0.61; 10 trials, 1130 patients)26 29 35 37–40 46 50 51 with variable heterogeneity (table 2).

    Sensitivity and subgroup analyses

    Exclusion of two potentially quasi-randomised trials28 42 maintained significant reductions in mortality (RR 0.62, 95% CI 0.47 to 0.80) and VAP (RR 0.30, 95% CI 0.22 to 0.43) both favouring non-invasive weaning.

    We noted a significant difference in RR between subgroups (p=0.0003) evaluating non-invasive weaning on mortality in COPD (RR 0.36, 95% CI 0.25 to 0.51; 14 trials, 922 patients; p<0.00001, I2=0%) versus mixed population (RR 0.81, 95% CI 0.62 to 1.05; 13 trials, 1120 patients; p=0.11, I2=7%). A subgroup analysis that compared trials enrolling at least 50% (RR 0.44, 95% CI 0.31 to 0.63; 18 trials, 1200 patients) versus less than 50% patients with COPD (RR 0.80, 95% CI 0.61 to 1.06; nine trials, 842 patients) also showed a larger and statistically significant (p=0.009) mortality reduction in subgroup analysis favouring COPD trials. The effect of non-invasive weaning on weaning failures did not differ significantly between COPD and mixed populations and trials enrolling at least 50% versus less than 50% patients with COPD. Similarly, we found significant differences between subgroups evaluating non-invasive weaning on VAP and ICU length of stay in COPD versus mixed populations. A post hoc subgroup analysis demonstrated significantly lower reintubation rate (p=0.02) in COPD trials (RR 0.48, 95% CI 0.34 to 0.67) versus mixed patient populations (RR 0.89. 95% CI 0.59 to 1.35) (table 3).

    View this table:
    Table 3

    Secondary analysis of summary estimates of effect of non-invasive ventilation by subgroup

    Discussion

    In this updated systematic review, we identified 28 trials (2066 patients) enrolling mechanically ventilated patients that compared weaning with extubation to non-invasive ventilation to ongoing weaning on mechanical ventilation. Compared with invasive weaning, non-invasive weaning reduced mortality (high quality), VAP (high quality), weaning failures (high quality), length of stay in the ICU and hospital and tracheostomy. Moreover, non-invasive (vs invasive weaning) significantly reduced the duration of invasive ventilation, total duration of ventilation and the duration of ventilation related to weaning. The effects on mortality and VAP remained significant after exclusion of quasi-randomised trials. Subgroup analysis suggested that the benefits of non-invasive weaning were higher in COPD versus mixed patient populations, with significant between-group differences in mortality, ICU length of stay and reintubation favouring patients with COPD.

    Compared with our previous review, this update includes data from 12 additional trials and 1072 additional patients.17 Patients with COPD accounted for half the trials and 44.6% of the patients overall. Overall trials included in the current review were of moderate-to-good quality. Lack of blinding and the inconsistent use of standardised weaning protocols in both arms and absence of a sedation protocol in the invasive weaning arm raise the possibility that control patients in some trials may not have received optimal care, biasing in favour of non-invasive weaning. The largest trial included patients with variable reasons for ARF and carefully protocolised weaning in both groups.50 Similar to our systematic review, Perkins et al found significant differences in the duration of invasive ventilation and total duration of ventilation. Unlike our review, this study did not find differences in rates of mortality or tracheostomy.50 The low proportion of patients with COPD included in their trial (4% COPD) versus the larger number of patients with COPD included in our review (44.6%) may, at least in part, explain the discordant findings. In general, results of large trials have been found to agree with meta-analyses to which they contribute,80 but differences between large trials and meta-analyses of smaller trials addressing the same question have been demonstrated in some fields81 and may depend on the selection of included trials, methods used to summarise data and outcomes reported.82

    Non-invasive weaning may be particularly suitable for patients with COPD, whose failure to wean is characterised by respiratory muscle weakness and gas trapping leading to intrinsic positive end-expiratory pressure, both of which are assisted by non-invasive ventilation. In contrast, patients with non-hypercapneic respiratory failure may fail a SBT for other reasons (eg, excess sputum) or may have other reasons why extubation should be deferred (eg, low level of consciousness). A survey of self-reported practices found that intensivists commonly reported using non-invasive weaning in patients with COPD (>50% of respondents in most regions) but were less likely to do so (<30% in most regions) for other indications such cardiogenic pulmonary oedema or postoperatively.83 Two large-scale observational studies of weaning practices83 84 should provide more data on the real-world use of non-invasive weaning. Clinicians weighing the trade-off between the risks associated with failed extubation versus prolonged invasive ventilation can be reassured that non-invasive weaning is superior to invasive weaning, for patients with COPD. However, enthusiasm should be tempered by considerations of experience required among physicians, nurses and respiratory therapists to safely implement non-invasive weaning, reintubation if required, and the need for standalone non-invasive ventilators or ventilators capable of both forms of ventilation. This is particularly important in non-COPD patients where benefits are less clear based on our subgroup analyses.

    Comparison with other studies

    A clinical practice guideline that cited our previous review85 gave a conditional recommendation in favour of non-invasive weaning for patients with hypercapneic respiratory failure but made no recommendation for patients with hypoxemic respiratory failure. Compared with the 2018 review by Yeung et al,86 we included five additional trials.27 30 38 51 52 Similar to their study, we documented beneficial effects of NIV on mortality, VAP, duration of invasive ventilation and ICU stay.86 In a sensitivity analysis of nine trials (n=788 patients who failed an initial SBT), they reported beneficial effects of non-invasive weaning on hospital mortality but wide ‘highest posterior density intervals’, from Bayesian estimates, precluded a definitive statement of the effect of NIV on this outcome. Unlike their study, we also identified beneficial effects of non-invasive (vs invasive) weaning in reducing the proportion of weaning failures and tracheostomies, as well as, hospital length of stay and the duration of ventilation related to weaning with considerable heterogeneity. Moreover, we found significant effects of non-invasive weaning, compared with invasive weaning on mortality, VAP, ICU stay and reintubation in COPD versus mixed populations. Similar to our previous meta-analysis,17 we found that non-invasive weaning significantly reduced mortality, weaning failure, VAP, ICU and hospital lengths of stay, total duration of ventilation and reintubation compared with invasive weaning. In this updated review, we also found that non-invasive (vs invasive) weaning significantly reduced the duration of ventilation related to weaning but did not significantly reduce the rate of reintubation. Although our prior review noted a significant difference in mortality between COPD versus mixed populations overall, it did not find significant differences comparing trials in which at least 50% of enrolled patients had COPD with trials in which less than 50% of patients had COPD. By contrast, in our updated review, we found significant differences between COPD versus mixed populations in four outcomes (mortality, VAP, ICU stay and reintubation) and in mortality in a subgroup analysis that compared trials enrolling at least 50% versus less than 50% patients with COPD. These findings underscore the greater net clinical benefits associated with the non-invasive approach to weaning for patients with COPD. The findings of our updated review extend the findings of our previous review by identifying beneficial effects of non-invasive (vs invasive) weaning in reducing the duration of ventilation related to weaning, hospital length of stay and the proportions of weaning failures and tracheostomies. Moreover, they highlight the robustness and stability of the evidence favouring non-invasive weaning for patients with COPD as new trials were added to the prior pool of trials. At present, however, our analyses do not support the use of non-invasive weaning in mixed populations. Aligned with our findings, a recent systematic review and individual patient meta-analysis in six trials highlighted the potential beneficial effect of non-invasive ventilation after early extubation in reducing total days spent on invasive mechanical ventilation, though this was not associated with a significant reduction in ICU mortality.87

    Strengths and limitations

    This review was strengthened by a comprehensive trial search and standard systematic review methods to reduce risk of bias. Limitations of this work include this risk of bias in primary trials, primarily driven by potential publication bias, specifically the absence of small negative trials and imprecision. Overall, the quality of the evidence was graded as high for key outcomes in our review including mortality, weaning failure and VAP. Notwithstanding, some outcomes, in particular VAP, were subject to ascertainment bias, since microbiological confirmation via sputum culture is easier in intubated patients. Highly variable control group event rates for mortality and VAP may reflect heterogeneity in the patient populations included and selection criteria used between studies or different usual care practices and contribute to indirectness of evidence.

    Conclusion

    Pooled data support the net clinical benefits associated with the non-invasive approach to weaning on a wide range of clinical outcomes. In subgroup analysis, we found significant benefit of non-invasive weaning in trials enrolling COPD versus mixed populations on mortality and other important outcomes including pneumonia, reintubation and ICU length of stay.

    Data availability statement

    Data are available from KEAB. Data are available from Dr. Burns (0000-0002-9967-5424) .

    Ethics statements

    Patient consent for publication

    Ethics approval

    Not required.

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    Supplementary materials

    Footnotes

    • Twitter @karenburnsk

    • Correction notice This article has been corrected since it was published Online First. Some affiliations were listed incorrectly and a minor error was noted in Table 3.

    • Collaborators Not applicable.

    • Contributors KEAB conducted the literature searches, resolved discrepancies between citation reviewers, selected studies meeting inclusion criteria, assessed study quality, conducted risk of bias assessments, double checked data entry, prepared initial and subsequent drafts of the manuscript and integrated comments into revised versions of the manuscript. JS and ML screened abstracts, selected studies meeting inclusion criteria, abstracted data, assessed study quality, conducted risk of bias assessments and integrated comments into revised versions of the manuscript. YL, CL, ZL and LC assisted with screening articles for inclusion. YL, CL, XH, ZL, WW, LC and HZ translated articles, abstracted data, assessed study quality and conducted risk of bias assessments. NKJA provided methodologic guidance, aided with drafting the manuscript and integrated comments into revised versions of the manuscript. JOF provided methodologic guidance, assessed study quality and conducted risk of bias assessments, hand searched conference proceedings and integrated comments into revised versions of the manuscript. All authors revised and approved the final version of the manuscript.

    • Funding KEAB holds a career award from the Physician Services Incorporated Foundation.

    • Competing interests None declared.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.