Journal of Evidence-Based Medicine ISSN 1756-5391 REVIEW Cuff-leak test for predicting postextubation airway complications: a systematic review Ting Zhou 1 , Hong-Ping Zhang 1 , Wei-Wei Chen 1 , Ze-Yu Xiong 2 , Tao Fan 3 , Juan-Juan Fu 4 , Lei Wang 1 and Gang Wang 1 1 Pneumology Group, Department of Integrated Traditional Chinese and Western Medicine, West China Hospital, Sichuan University, Chengdu, P.R. China 2 Division of Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, University of Pittsburgh Medical Center, Pittsburgh, PA, USA 3 Department of Respiratory and Critical Care Medicine, West China Hospital, Sichuan University, Chengdu, P.R. China 4 Department of Respiratory and Sleep Medicine, John Hunter Hospital, Hunter Medical Research Institute, Newcastle University, NSW, Australia Keywords cuff-leak test; postextubation airway complications; accuracy; GRADE; systematic review Correspondence Dr. G. Wang, MD & PhD, Pneumology Group, Department of Integrated Traditional Chinese and Western Medicine, West China Hospital, Sichuan University, Chengdu 610041, P.R. China Tel: 0086-8542-3546 E-mail: [email protected]Received 29 August 2011; accepted for publication 17 October 2011. doi: 10.1111/j.1756-5391.2011.01160.x Abstract Background and objective: Postextubation problems such as laryngeal edema and reintubation are common complications after tracheal intubation. The cuff-leak test has been proposed as a method of identifying those patients at high risk in clinical practice, but its efficacy remains controversial. Methods: We searched electronic databases including PubMed, the Cochrane Con- trolled Trials Register, Web of Science, Ovid, and Embase. Studies were included if they were concerned with accuracy of the cuff-leak test and the effect of cuff- leak test screening on patient-important outcomes. Two reviewers independently assessed study quality with the QUADAS tool and extracted data. We compiled diagnostic two by two tables and pooled estimates of sensitivity and specificity, but refrained from pooling when there was considerable clinical or statistical hetero- geneity. Results: Sixteen diagnostic tests with 3172 participants and six clinical trials with 2500 patients were identified. The median diagnostic odds ratios for predicting postextubation laryngeal edema and reintubation were 18.16 (range, 3.54 to 356.00) and 10.80 (2.74 to 1665.00), respectively. The accuracy of the cuff-leak test varied with different methods, duration of intubation, and study population. An indirect comparison found significant differences in post-extubation incidence of laryngeal edema (OR = 2.09, 95% CI, 1.28 to 2.89) but not reintubation (OR = 0.94, 95% CI, 0.32 to 1.57) if using cuff-leak test screening. Conclusions: Our results suggest the cuff-leak test accurately predicts which adult patients are at high risk of postextubation airway complications, but randomized controlled trials are needed to further assess this diagnostic strategy. Introduction Translaryngeal intubation is a potentially life-saving proce- dure for patients in respiratory distress, but it sometimes generates local complications (1). Our recent study showed that prophylactic administration of steroids in multidose regimens before planned extubation reduces the incidence of laryngeal edema after extubation and consequent rein- tubation for adults (2), but Young et al. suggest that cor- ticosteroids should be given only to patients at high risk (3). However, pretreating patients with corticosteroids as- sumes postextubation airway complications are predictable events (4). As the presence of an endotracheal tube precludes direct visualization of the upper airway prior to extubation, a cuff- leak test, which shows whether there is a leak around the 242 JEBM 4 (2011) 242–254 c 2011 Blackwell Publishing Asia Pty Ltd and Chinese Cochrane Center, West China Hospital of Sichuan University
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Journal of Evidence-Based Medicine ISSN 1756-5391
REVIEW
Cuff-leak test for predicting postextubation airwaycomplications: a systematic reviewTing Zhou1, Hong-Ping Zhang1, Wei-Wei Chen1, Ze-Yu Xiong2, Tao Fan3, Juan-Juan Fu4,Lei Wang1 and Gang Wang1
1 Pneumology Group, Department of Integrated Traditional Chinese and Western Medicine, West China Hospital, Sichuan University,Chengdu, P.R. China2 Division of Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, University of Pittsburgh Medical Center, Pittsburgh,PA, USA3 Department of Respiratory and Critical Care Medicine, West China Hospital, Sichuan University, Chengdu, P.R. China4 Department of Respiratory and Sleep Medicine, John Hunter Hospital, Hunter Medical Research Institute, Newcastle University, NSW,Australia
Dr. G. Wang, MD & PhD, PneumologyGroup, Department of Integrated TraditionalChinese and Western Medicine, West ChinaHospital, Sichuan University, Chengdu610041, P.R. ChinaTel: 0086-8542-3546E-mail: [email protected]
Received 29 August 2011; accepted forpublication 17 October 2011.
doi: 10.1111/j.1756-5391.2011.01160.x
Abstract
Background and objective: Postextubation problems such as laryngeal edema andreintubation are common complications after tracheal intubation. The cuff-leak testhas been proposed as a method of identifying those patients at high risk in clinicalpractice, but its efficacy remains controversial.Methods: We searched electronic databases including PubMed, the Cochrane Con-trolled Trials Register, Web of Science, Ovid, and Embase. Studies were includedif they were concerned with accuracy of the cuff-leak test and the effect of cuff-leak test screening on patient-important outcomes. Two reviewers independentlyassessed study quality with the QUADAS tool and extracted data. We compileddiagnostic two by two tables and pooled estimates of sensitivity and specificity, butrefrained from pooling when there was considerable clinical or statistical hetero-geneity.Results: Sixteen diagnostic tests with 3172 participants and six clinical trials with2500 patients were identified. The median diagnostic odds ratios for predictingpostextubation laryngeal edema and reintubation were 18.16 (range, 3.54 to 356.00)and 10.80 (2.74 to 1665.00), respectively. The accuracy of the cuff-leak test variedwith different methods, duration of intubation, and study population. An indirectcomparison found significant differences in post-extubation incidence of laryngealedema (OR = 2.09, 95% CI, 1.28 to 2.89) but not reintubation (OR = 0.94, 95%CI, 0.32 to 1.57) if using cuff-leak test screening.Conclusions: Our results suggest the cuff-leak test accurately predicts which adultpatients are at high risk of postextubation airway complications, but randomizedcontrolled trials are needed to further assess this diagnostic strategy.
Introduction
Translaryngeal intubation is a potentially life-saving proce-dure for patients in respiratory distress, but it sometimesgenerates local complications (1). Our recent study showedthat prophylactic administration of steroids in multidoseregimens before planned extubation reduces the incidenceof laryngeal edema after extubation and consequent rein-
tubation for adults (2), but Young et al. suggest that cor-ticosteroids should be given only to patients at high risk(3). However, pretreating patients with corticosteroids as-sumes postextubation airway complications are predictableevents (4).
As the presence of an endotracheal tube precludes directvisualization of the upper airway prior to extubation, a cuff-leak test, which shows whether there is a leak around the
endotracheal tube with the cuff deflated, was first proposedin 1988 as a simple method of predicting the occurrence ofpostextubation airway complications (5). This test consists ofdeflating the balloon cuff of the endotracheal tube in order toassess the air leak around the tube, which permits an indirectevaluation of upper airway patency (6).
A considerable number of studies on the cuff-leak test havebeen published, but their results remain controversial (7–9),leaving physicians to make difficult decisions regarding ex-tubation. The GRADE (Grades of Recommendation, As-sessment, Development, and Evaluation) approach providesguidance on grading the quality of underlying evidence andthe strength of recommendations in health care. Accordingto the GRADE system, the best way to assess any diagnosticstrategy is a randomized controlled trial in which investi-gators randomize patients to experimental or control diag-nostic approaches and measure mortality, morbidity, symp-toms, and quality of life (10). Although a meta-analysis onthe cuff-leak test’s accuracy was undertaken recently (11),the test accuracy is at best a surrogate for patient-importantoutcomes. Furthermore, that study lacked subgroup or com-parative analyses, and did not link evidence on diagnosistest accuracy to clinical practice. We performed the presentsystematic review to establish the overall accuracy of thecuff-leak test for predicting postextubation airway compli-cations, which should trigger a clinical decision to initiatetreatment.
MethodsEthical review
This study was designed as a systematic review, so it did notrequire ethical approval, but we extracted any ethical reviewinformation from included studies.
Search strategy and selection criteria
We searched electronic databases including PubMed (1980to Jan 2011), CENTRAL (Cochrane Controlled Trials Regis-ter, issue 1, 2011), Web of Science (1994 to Jan 2011), Ovid(1994 to Jan 2011), and Embase (1984 to Jan 2011). Using“cuff leak test”(13) as our only search term, we searched forall clinical trials on the cuff-leak test, and scanned the refer-ence lists of review articles and included studies to identifyother potentially eligible studies. There was no limitation onlanguage, year of publication, or publication status. Trialswere included if they involved diagnostic tests in adults andhad adequately reported data for calculating sensitivity andspecificity. After excluding duplicates, two reviewers (T.Z.and W.W.C.) reviewed the full text of all pieces with titlesand abstracts that seemed to fit the criteria for inclusion.
Data extraction
From each included article we extracted details on authors,year of publication, study population, gender of subjects,sample size, duration of intubation, test methods, diagnosticcutoff points, true and false positive (TP and FP) and falseand true negative (FN and TN) subjects, and methodologicalquality.
The two reviewers independently assessed the quality ofeach study and extracted data. Disagreements were resolvedby consensus or by consulting a third reviewer (G.W.). If in-formation was not reported adequately, we requested detailsfrom the authors. If the authors did not respond to our letters,the “unknown” items were treated as “no.” Each reviewerextracted the data to construct a 2 × 2 table for every cutoffpoint that was published in each study.
Reference standards and patient-importantoutcomes
After extubation, stridor or dyspnea, an audible high pitchedinspiratory wheeze caused by turbulent airflow through nar-rowed airways, is generally accepted as a clinical indicationof laryngeal edema (2). Major laryngeal edema necessitatespostextubation reintubation. Therefore, reference standardsfor postextubation airway complications included laryngealedema and reintubation secondary to upper airway obstruc-tion. In this study, our primary patient-important outcomewas laryngeal edema after extubation, with subsequent rein-tubation necessitated by laryngeal edema as the secondarypatient-important outcome.
Quality assessment
We assessed the methodological quality of studies usingguidelines in the quality assessment for studies of diagnosticaccuracy (QUADAS) tool (maximum score, 14) (14). Qual-ity scoring in QUADAS was undertaken, in which a scoreof 1 was given when a criterion was fulfilled, 0 if a crite-rion was unclear, and −1 if the criterion was not achieved.Test accuracy studies with design deficiencies can producebiased results (15). Accordingly, the following characteris-tics in study design, which encompass some of the moreimportant forms of bias, were evaluated (13, 16): (1) cross-sectional design; (2) sample size calculation; (3) consecutiveor random sampling subjects; (4) blinding; (5) prospectivedata collection.
Effect of cuff-leak test screeningon patient-important outcomes
According to the GRADE system and using methods de-tailed in a previous review (2), we evaluated whether there
was an effect of cuff-leak test screening—followed, whenindicated, by prophylactic administration of steroids—on in-cidence of postextubation airway complications such as la-ryngeal edema and reintubation secondary to upper airwayobstruction.
Statistical analysis
For each study, the sensitivity, specificity, positive and nega-tive likelihood ratios (PLR and NLR), and diagnostic odds ra-tio (DOR) were calculated. The DerSimonian Laird method(random effects model) was used to incorporate variationamong studies when pooling sensitivity, specificity, PLR,NLR, and DOR. Furthermore, a summary receiver operatorcharacteristic (sROC) curve of all the studies was created, asthis is a better summary of the study results than is a sin-gle jointed summary estimate of sensitivity and specificity.The area under the sROC curve (AUC) was used to judgethe degree of accuracy of the tests according to publishedguidelines (excellent: ≥0.97; very good: 0.93–0.96; good:0.75–0.92; poor: 0.50–0.75) (17).
I2 or Q tests, though commonly used in meta-analysis,are not recommended for assessing statistical homogeneityin diagnostic reviews because they do not take into accountthe association between sensitivity and specificity. Statisticalheterogeneity was defined as an overlapping 95% confidenceinterval (CI) of both sensitivity and specificity and differ-ences in point estimates among the studies of less than 20%(18, 19). In cases of statistical or clinical heterogeneity (interms of characteristics of populations and test characteris-tics), we refrained from pooling and presented median valuesand ranges instead. We carried out subgroup and compara-tive analyses to assess the effects of different methods of thecuff-leak test, as well as the effects of risk factors for postex-tubation airway complications (e.g., duration of intubation,gender, and reason for admission) (20) on the accuracy ofthe cuff-leak test, when each subgroup included data of atleast four diagnostic studies. Furthermore, to assess the ef-fects of QUADAS scores and other covariates (i.e., importantstudy design characteristics) on the diagnostic ability of thecuff-leak test, we included them as covariates in univariatemeta-regression analysis.
Investigating publication bias for diagnostic tests is prob-lematic (21). Funnel plot-based tests used to detect pub-lication bias in reviews of randomized controlled trialshave proven misleading for diagnostic studies (22). There-fore, we did not assess publication bias in this systematicreview.
The threshold of significance was set at P < 0.05. Allstatistical analyses were performed using Stata version 8.0(Stata Corp LP, College Station, Texas) and MetaDiSc ver-sion 1.1.1 (Zamora J, Muriel A, Abraira V, Madrid, Spain).
Citations screened for titles and abstracts (n=118)
Duplicates excluded (n=38)
Unique abstracts identified (n=80)
Detailed information evaluated (n=38)
Irrelevant trials excluded
(n=42)
Not diagnostic tests (n=17)
Letters (n=1)
Comments (n=5)
Reviews (n=6)
Others (n=5)
Diagnostic tests included (n=21)
Studies on children or infants
(n=3)
Eligible trials identified (n=16)
Potentially relevant trials (n=18)
In adequately reported
information (n=2)
Incomplete data (n=1)
Abstract only (n=1)
Figure 1 Flow chart of study identification, inclusion, and exclusion
ResultsStudies included
Our search strategy initially yielded 118 citations (Figure 1).Of these, 16 unique studies on predicting postextubationairway complications were included in our review; the in-cluded studies involved a total of 3172 participants (3218extubations) (1, 7, 8, 23–35). In addition, six clinical tri-als (2500 total patients) on prophylactic administration ofsteroids (with or without cuff-leak test screening) for pre-venting postextubation airway complications were identified(20, 24, 25, 36–38), as described in our previous review (2).
The adult subjects of the included studies varied from themedical care population to trauma or surgical patients, andwere thus somewhat heterogenous (Table 1). The aver-age sample size of the included studies was 201, with arange of 49–543. We found that the sample size was notconsistent with the number of extubations in four studies(27, 28, 32, 33), suggesting that at least two cuff-leak testswere performed in the same subject. Participants were tra-cheally intubated via the oral or nasal route for a length oftime ranging from less than 24 hours to several days, andwere monitored for about 24 or 48 hours after extubation.
All included diagnostic tests were cross-sectional stud-ies (Table 2). Four of 16 trials were approved by Institu-tional Review Board (IRB), and only one study was reg-istered in public service platform of trial registration (24).No sample size calculations were applied in any includedstudy. Subjects who participated in the cuff-leak test werechosen consecutively or at random in 14 of the includedstudies. Blinding was used in 12 studies. The averageQUADAS score of the methodological quality of studieswas 8.2 whose QUADAS assessment was presented inFigure 2.
The cuff-leak test and the threshold effect
The included studies used two kinds of methods for the cuff-leak test, qualitative (presence or absence of leak aroundthe tube) and quantitative. The quantitative method, Miller’stest, was proposed by Miller et al. in 1996 (33), and canbe further subdivided into an absolute measure (measuredin milliliter volume) and a relative measure (quantified aspercent volume). The cutoff value of the cuff-leak test inthe quantitative method varied from 88–283 ml or 10–57%in included studies. Regression analysis of the diagnos-tic threshold found no threshold effect in this systematicreview (all P > 0.05 for both Spearman correlation co-efficient and beta coefficient in Moses’ model) (Data notshown).
Outcomes for systematic reviewand subgroup analyses
The total incidence of postextubation laryngeal edema was6.79% (95% CI 5.94–7.73%) with a range of 0.60–36.8%,while the incidence for reintubation secondary to laryngealedema was 3.52% (95% CI 2.79–4.36%) with a range of0.0–10.53% (Table 3). The incidence of postextubation la-ryngeal edema was 0.57% for less than 24 hours of intuba-tion, 4.61% for between 24 hours and 5 days, and 16.70%for more than 5 days. T
Figure 2 Quality assessment in 16diagnostic tests according to QUADASitems, presented as the proportion ofincluded studies
The subgroup and comparative analyses were based on thedifferent methods of the cuff-leak test, durations of intuba-tion, and study populations (Table 4). The heterogeneity wasacross Se, Sp, PLR NLR, and DOR. There were increasedmedians of specificity, DOR, and AUC for identifying pa-tients at high risk of postextubation laryngeal edema in thequalitative method and the absolute volume compared withthe relative volume cuff-leak test, but the sensitivity of thequalitative method, at 1.00, had a broader range (Figure 3A).All three methods of the cuff-leak test had similar specifici-ties for predicting postextubation reintubation, about 0.85(Figure 3B).
The accuracy of the cuff-leak test varied with differentdurations of intubation. There was a higher median speci-ficity of 0.90, DOR of 69.75, and AUC of 0.92 in predictingpostextubation laryngeal edema in subjects with more than5 days mean duration of intubation compared with those withless than 5 days. Furthermore, there was a higher medianspecificity of 0.92 and DOR of 37.76 for predicting postex-tubation reintubation in patients with more than 5 days ofmean duration of intubation.
Multiple regression analysis
QUADAS scores, other quality factors of diagnostic tests,duration of intubation, and study populations were im-ported into a meta-regression analysis to assess the ef-fect of study quality on the DOR of the cuff-leak testfor identifying high-risk patients. The analysis found thatvariations of QUADAS, cross-sectional design, consecu-
tive or random, blinding, prospective design, duration ofintubation, and study population did not contribute to theheterogeneity of ratio of DOR (rDOR) (all P > 0.05)(Table 5).
Effect of cuff-leak test screening withprophylactic administration of steroidson postextubation airway complications
We found no clinical trials in which investigators random-ized subjects to either take or not take the cuff-leak test. Insix of the studies, patients were divided into three groupswho were treated with either the cuff-leak test screening fol-lowing by prophylactic administration of steroids in the caseof positive results (the CLT group, n = 686), or steroids orplacebo without cuff-leak test screening (the steroids group,n = 905 and the placebo group, n = 909). In the CLT group,only 208 patients (30.3%) had positive cuff-leak test results[the CLT (positive) group)] and received prophylactic ad-ministration of steroids. There was no significant differencein the incidence of postextubation laryngeal edema betweenthe CLT group and the steroids group (OR = 1.39, 95%CI 0.79–2.24, P = 0.070). However, the incidence of pos-textubation reintubation in the CLT group was similar tothat in the placebo group (OR = 0.94, 95% CI 0.32 to1.57, P = 0.860) (Table 6). According to inference analy-sis, the mean dose of equivalent methylprednisolone in theCLT group was much more decreased than that with thesteroids group (34.23 ± 2.20 mg vs 74.23 ± 1.38 mg, P <
Postextubation problems such as laryngeal edema and rein-tubation prolong the need for mechanical ventilation and in-crease morbidity in intensive care unit patients. In our study,the incidence of laryngeal edema varied from 0.6–36.8%, andthe reintubation rates secondary to laryngeal edema from0–80.0%, possibly because of different study populations,severity of diseases, and durations of intubation. We foundthat the cuff-leak test accurately identifies adult patients athigh risk of postextubation airway complications, and cuff-leak test screening reduces the incidence of postextubationlaryngeal edema but not of reintubation in indirect com-parison analysis. We also found that the incidence of pos-textubation laryngeal edema increased when intubation wasprolonged.
Systematic reviews of interventions sometimes find verysimilar estimates of the effects of competing interventionsin different studies, with differences in effects small enoughto be explicable by chance. However, in test accuracy re-views large differences are commonly noted among studies,differences too large to be explained by chance, indicatingthat actual test accuracy varies among studies, or that there isheterogeneity in test accuracy. Substantial heterogeneity wasfound to be present in our study, so we refrained from pool-ing and presented median values and ranges instead (37). Wethen explored the reasons for the heterogeneity with meta-regression techniques, but found no clinical heterogeneity.This indicates that the study design, duration of intubation,and study population did not substantially affect the diagnos-tic accuracy.
The cuff-leak test, a simple method for predicting postex-tubation airway complications, includes three methods, onequalitative and two quantitative. Pettignano et al. (40) demon-strated that the qualitative cuff-leak test is reproducible andreliable. We posited that the cuff-leak test quantified in per-cent volume would have the highest accuracy among the threeapproaches because height, weight, gender, and other factorswould be adjusted for by this method. However, there were noreasonable explanations for this finding. The accuracy of thecuff-leak test for predicting postextubation airway compli-cations varied among the three different methods. Therefore,the qualitative method should be used in combination withthe quantitative method in clinical practice.
The best way to evaluate a diagnostic test is to under-stand the expected clinical benefits and harms attributableto its use. Integration of systematic reviews of diagnostictest accuracy and decision making is an emerging area ofactive research (12, 41). We need to consider the range ofpotential “threshold probabilities” that should trigger a clin-ical decision to initiate treatment (42). Ideally, patients athigh risk of developing postextubation airway complicationsshould be identified as early as possible. Treatments such as
Figure 3 Symmetric ROC curves for the cuff-leak test in predictingpostextubation laryngeal edema (A) and reintubation (B). = eachstudy in the meta-analysis (the size of each study is indicated by thesize of the solid circle); SROC curves summarize the overall diagnosticaccuracy
prophylactic administration of steroids to reduce postextu-bation airway complications should then be started (3). Thebest way to assess any diagnostic strategy is a randomizedcontrolled trial in which investigators randomize patients toexperimental or control diagnostic approaches and measurepatient-important outcomes (43). There are no trials usingrandom allocation of the cuff-leak test, but six trials wereidentified in which the diagnostic strategies of the cuff-leaktest with prophylactic administration of steroids were com-pared indirectly. Our previous study suggests that patients
Table 5 Weighted meta-regression of the effects of methodological
quality, duration of intubation, and study population on diagnostic
ReintubationQUADAS −0.204 0.82 (0.51, 1.31) 0.336Cross-sectional design – – –Consecutive or random −5.239 0.01 (0.00, 0.98) 0.057Blinding −0.833 0.43 (0.06, 3.08) 0.338Prospective – – –Duration of intubation 0.017 1.02 (0.76, 1.35) 0.892Study population 0.526 1.69 (0.40, 7.16) 0.406
with positive cuff-leak test results, or at high risk, wouldrealize much more benefit from prophylactic steroid admin-istration (2). Furthermore, a recently published study (44)and another abstract (45) show that the efficacy of steroidsin preventing stridor and reintubation was only observed in ahigh-risk population as identified by the cuff-leak test, whichstrengthens the effect of the cuff-leak test on predicting pos-textubation airway complications. Using the GRADE sys-tem, we found evidence that cuff-leak test screening wouldreduce the incidence of postextubation laryngeal edema butnot reintubation. However, this pattern was weaker for trialsin which the comparisons were indirect (46).
Limitations
Our study has some limitations. First, three different meth-ods of the cuff-leak test, and prophylactic administrationof steroids with or without the cuff-leak test screening,were compared indirectly but not head-to-head, which woulddecrease the reliability and generalizability of the results.Second, substantial heterogeneity was found in our study,so we did not conduct pooled estimates. Third, only onetherapeutic strategy (prophylactic administration of steroids)was used following a positive cuff-leak test in the includedstudies. Fourth, postextubation airway complications such aslaryngeal edema and reintubation secondary to upper airwayobstruction, which were taken as reference standards, werealso patient-important outcomes. What’s more, there is a timeinterval between cuff-leak test screening and the occurrenceof patient-important outcomes or reference standards.
In conclusion, our systematic review suggests that thecuff-leak test accurately identifies patients at high risk of
CLT = cuff-leak test; NNT = number needed to treat; CI = confidence interval. avs Steroids; bvs Placebo; cvs CLT.
postextubation airway complications, and treating patientswith positive test results with prophylactic steroids seemsto reduce the incidence of postextubation laryngeal edemabut not postextubation reintubation. Further randomized con-trolled trials, in which investigators randomize patients to thecuff-leak test or a sham test with prophylactic administrationof steroids and measure postextubation airway complica-tions, are needed to assess this diagnostic strategy.
Funding:
This research was supported by the National Natural ScienceFoundation of China (No. 30971326), the Sichuan YouthScience and Technology Foundation (No. 2010JQ0008), andthe Funding Doctoral Fund of the Ministry of Education ofChina (No. 20070610155).
Conflicts of Interest:
Dr. Gang Wang is supported by the National Natural ScienceFoundation of China (No. 30971326), the Sichuan Youth Sci-ence and Technology Foundation (No. 2010JQ0008), YouthScience Funding of Sichuan University (2011SCU04B17)and the Funding Doctoral Fund of the Ministry of Edu-cation of China (No. 20070610155). Dr. Lei Wang is sup-ported by the National Natural Science Foundation of China(No. 30901907).
Authorship:
Dr. Gang Wang contributed substantially to the conceptionand design of the study; collection, extraction and interpre-tation of the data; drafting of the manuscript; and statisticalanalysis. Drs. Ting Zhou, Hong-ping Zhang, Tao Fan, Juan-juan Fu, and Wei-wei Chen were responsible for collection,extraction, and interpretation of the data. Dr. Ze-yu Xiongwas responsible for interpretation of the data and critical re-vision of the manuscript. Dr. Lei Wang provided insight intothe statistical methods.
Ethics:
This study was designed as a systematic review, so it did notrequire ethical approval, but we extracted any ethical reviewinformation from included studies.
Acknowledgments
We are grateful to Ding LW and De Bast Y who sent addi-tional information on their original studies. We also thankProfs. Gibson PG. (University of Newcastle, Australia), Vander Windt DA (Keele University, UK), de Vet HC (VUUniversity, Amsterdam). Liu GJ (Chinese Cochrane Cen-ter, China) for their statistics suggestions, and Ms. Ruan Rfor her help in preparing this manuscript.
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