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Ann Thorac Surg 2010;90:1779-1785. doi:10.1016/j.athoracsur.2010.07.033
© 2010 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Surgical Sealant for the Prevention of Prolonged Air Leak After Lung Resection: Meta-Analysis

Guislain Malapert, MD, Halim Abou Hanna, MD, Pierre Benoit Pages, MD, Alain Bernard, MD*

Department of General Thoracic Surgery, Centre Hospitalier Universitaire Dijon, Hospital du Bocage, Dijon, France

Accepted for publication July 9, 2010.

* Address correspondence to Dr Bernard, Division of Thoracic Surgery, CHU Hospital du Bocage, Blvd de Lattre de Tassigny, Dijon Cedex, 21034, France (Email: alain.bernard{at}chu-dijon.fr).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: We performed a systematic and meta-analysis of randomized controlled trials comparing a surgical sealant with buttressed staple lines using standard methods. The aim of our meta-analysis was to determine the effectiveness and safety of different techniques to reduce the proportion of patients with prolonged air leakage after pulmonary resection.

Methods: We searched the Medline, Embase, Science Direct, Food and Drug Administration, Cochrane controlled trials register, and clinical trial databases for publications between January 1995 and May 2009 that included terms related to prolonged air leak after lung resection. We included randomized controlled trials comparing glue or patch or buttressed staple line with suture or staple in patients undergoing lung resection (wedge resection or lobectomy). The prespecified primary outcome of our meta-analysis was prolonged air leak more than 7 days. Secondary outcomes were the occurrence of adverse effects.

Results: Thirteen trials were included in the meta-analysis. Overall, the trials had allocated 1,335 patients to glue or patch (1,064 patients) or buttress (271 patients) for the prevention of prolonged air leak after lung resection. The type of buttress used to reinforce the staple line was bovine pericardial strips (271 patients). In the control group of all trials for air-leakage management, single or continuous running sutures or staples were used according to the routine of the center. The use of glue or a patch or buttressing compared with control groups (1,335 patients) decreased prolonged air leak more than 7 days. Indeed, the pooled effect size odds ratio was 0.55 (95% confidence interval: 0.386 to 0.79). An I2 of 0% indicated low between-trial heterogeneity. The funnel-plot asymmetry coefficient was significantly different from zero (asymmetry coefficient –1.23 (95% confidence interval: –2.38 to –0.086; p < 0.04), indicating the presence of publication bias. Neither glue nor a patch nor buttressing influenced the occurrence of postoperative complications such as atelectasis, hemothorax, pneumonia, pneumothorax, and mortality. Eight trials (1,020 patients) showed that, compared with control groups, the use of glue or a patch or buttressing decreased postoperative arrhythmia, which yielded a pooled odds ratio of 0.44 (95% confidence interval: 0.275 to 0.72).

Conclusions: The use of surgical sealants and buttressing decreased the risk of prolonged air leakage and postoperative arrhythmia after pulmonary resection. However, given the possibility of publication bias, the conclusions should be interpreted with caution.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Prolonged air leak is defined as air leakage lasting more than 7 days after pulmonary resection. Prolonged air leak is the most common complication after lung resection and the reported incidence ranges from 15 to 18% [1, 2]. Prolonged air leak has a detrimental effect on the postoperative course as it results in a longer need for a chest tube with the associated pain, reduced mobility, and increased risk of further complications [2]. Prolonged air leak for more than 7 days is a complication that penalizes the patient by requiring a chest tube. One may question the clinical relevance of endpoints such as duration of air leak. For patients, what is the clinical impact of reducing the duration of air leakage by 1 or 2 days, as reported by some trials. Classical methods for intraoperative control of air leaks include suture and stapling, but have the disadvantage of causing further trauma to lung tissue.

Various additional techniques, including the use of a variety of sealants, such as fibrin glue, synthetic materials, and collagen patches coated with fibrinogen and thrombin, have been employed to minimize the intensity and duration of air leaks. Other techniques using staples and strips of reinforcing material to buttress the staple lines have also been tried to reduce air leaks after lung resection.

Several trials have compared these different techniques to reduce air leakage with classical methods. We performed a systematic and meta-analysis of randomized controlled trials that compared the use of surgical sealants or buttressed staple lines with the use standard methods. The aim of our meta-analysis was to determine the effectiveness and safety of different techniques to reduce the percentage of patients with a prolonged air leak after pulmonary resection.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Literature Search
We searched the Medline, Embase, Science Direct, Food and Drug Administration, Cochrane controlled trials register, and clinical trial databases for publications between January 1995 and May 2009 that included terms related to prolonged air leak after lung resection. We entered the relevant articles into a science citation index to retrieve reports that cited these articles, manually searched for conference proceedings and thoracic congresses, screened reference lists of all the articles obtained, and checked the proceedings of the US Food and Drug Administration advisory and health technology assessment agencies.

Trial Selection
We included randomized controlled trials comparing glue or patch or buttressed staple line with suture or staple in patients undergoing a lung resection (wedge resection or lobectomy). We included every randomized controlled trial that reported on the primary or secondary outcome of prolonged air leak for more than 7 days. Two reviewers (G.M. and H.A.) independently evaluated the reports for their eligibility. Disagreements were resolved by consensus.

Quality Assessment
Two reviewers (G.M. and H.A.) independently assessed concealment of treatment allocation, blinding (masking) and analyses. Concealment of allocation was considered adequate if the investigators responsible for patient selection were unable to determine before allocation which treatment was next in line (central randomization, sealed, opaque, sequentially numbered assignment envelopes). Patient blinding was considered adequate if it was stated that patients were blind to the assigned treatment. Therapist blinding was considered adequate if participants assessing the outcomes were blinded to group assignment. The number of patients randomized per group and the number of patients analyzed per group were extracted to distinguish between trials that had included all randomized patients in the analysis (considered as an intent-to-treat analysis and therefore adequate) and trials that had not. Disagreements were resolved by consensus.

Outcome measures
The prespecified primary outcome of our meta-analysis was prolonged air leak longer than 7 days. Secondary outcomes were the occurrence of adverse effects.

Data collection
Data on publication status, trial design, patient characteristics (age, pulmonary pathology, type of procedure) treatment regimens, prolonged air leak more than 7 days, adverse effects, quality assessment and funding were extracted in duplicate (by G.M. and H.A.) using a standardized form. Any disagreements were resolved by discussion.

Statistical Analysis
For prolonged air leak more than 7 days considered as dichotomous outcomes, effect sizes were estimated by odds ratio (OR). An effect size less than 1 indicates the superiority of sealant treatment compared with suture or staple. We used a random-effects meta-analysis to pool effect sizes and calculated the I2 statistic for each meta-analysis. This statistic describes the percentage of total variation across a trial that is attributable to statistical heterogeneity rather than chance [3]. The I2 values of 25%, 50%, and 75% correspond to low, moderate, and high between-trial heterogeneity, respectively. We performed stratified meta-analyses to investigate potential sources of statistical heterogeneity. The following trial characteristics were considered for stratification: adequacy of concealment of allocation, blinding of patients, adequacy of the analysis, trial size, type of pathology, type of procedure, and type of sealant. We used prespecified cutoffs of 100 randomized patients to distinguish between small- and large-scale trials. Univariable random-effects meta-regression analysis was used to examine whether effect sizes were affected by these factors.

We performed post hoc sensitivity analyses excluding outlier studies from the main meta-analysis. Studies were considered outliers if the confidence interval of the estimated effect size from these studies did not overlap with pooled overall effect size. Sensitivity analyses also focused on the buttressed staple line and surgery for emphysema when studies were excluded from the main meta-analysis.

Asymmetry of the funnel-plot was assessed by the asymmetry coefficient to search for likely effects of publication bias [4]. The Egger test detects funnel plot asymmetry by determining whether the intercept deviates significantly from zero in a regression of standardized effect estimates against their precision [4].

For these trials, we determined the contribution to Cochran's heterogeneity Q statistic in the overall analysis [5]. An approach developed by the DerSimonian and Laird methods was used to perform random-effects meta-analysis for overall effect measures [6]. All confidence intervals (CI) relate to the 95% limit, and p values were two-sided. Analyses were performed using STATA 11 statistical software (StataCorp, College Station, TX).

In addition, we conducted a Bayesian approach to random-effects meta-analysis [7]. We performed a sensitivity analysis to prior distributions. The three Bayesian models differ only with respect to the prior placed on the between-study variance {sigma}2: (1) a noninformative inverse gamma (IG [0.0001, 0.0001]); (2) a half-normal (0, 1,000); and (3) a Dumouchel prior [8]. Bayesian analysis was performed using WinBugs software [9].


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
From 1995 to 2009, we identified 811 references and considered 60 to be potentially eligible for the meta-analysis (Fig 1). Thirteen trials [10–22] were included in the meta-analysis (Fig 1). Forty-seven articles were excluded for the following reasons: no randomized trials (n = 37), no surgical sealant (n = 4), pleural tenting (n = 2), outcome after prolonged air leak more than 7 days not reported (n = 4; Fig 1). In the sealant group, glue or patch was used in nine trials [11, 14–18, 20–22] and buttress in four trials [10, 12, 13, 19] (Table 1). Overall, the trials had allocated 1,335 patients to glue or patch (1,064 patients) or buttress (271 patients) for the prevention of prolonged air leak after lung resection. Fibrin glue was used in three trials (210 patients) [11, 16, 22], and four trials used synthetic sealants (500 patients) [14, 15, 17, 20]. Two trials used a collagen patch (354) coated with fibrinogen and thrombin [18, 21]. The type of buttress used to reinforce the staple line was bovine pericardial strips (271 patients) [10, 12, 13, 19]. In the control group of all trials [10–22], single or continuous running sutures or staples were used for air leakage management according to the routine of the centre. The average age of patients ranged from 55 to 68 years, and in two trials [10, 13], the lung resection was used to treat emphysema (Table 1). The type of lung resection was lobectomy in four trials [12, 15, 18, 19], wedge resection in three trials [10, 13, 22], and lobectomy or wedge in six trials [11, 13, 16, 17, 20, 21] (Table 1).


Figure 1
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  		Fig 1. Flow diagram of articles evaluated for inclusion or exclusion.

 

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  		Table 1 Characteristics of Identified Randomized Controlled Trials
 
Assessment of Quality
Concealment of allocation was judged to be adequate in seven trials [11, 14, 16, 19–22] (Table 1). For all other trials, concealment of allocation remained unclear. The therapist who assessed the outcomes was blinded to the assigned intervention in five trials [13, 14, 16, 21, 22]. Seven trials [10, 12, 14, 16, 19–21] were considered to have performed an intent-to-treat analysis.

Pooled Effect Sizes
A total of 13 trials contributed to the meta-analysis of the prevention of prolonged air leak more than 7 days. The glue or patch or buttress compared with control groups (1,335 patients) decreased prolonged air leak of more than 7 days. Indeed, the pooled effect size was 0.55 (95% CI: 0.386 to 0.79; Fig 2). An I2 of 0% indicated low between-trial heterogeneity (p < 0.5 for heterogeneity). The results from stratified analyses are presented in Table 2. Concealment of allocation, blinding, intent-to-treat, trial size, emphysema, procedure, and type of sealant had no influence on between-trial heterogeneity and p values for interactions between trial characteristics (Table 2).


Figure 2
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  		Fig 2. Forest plot of the meta-analysis of outcomes of air leak more than 7 days. (CI = confidence interval; OR = odds ratio.)

 

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  		Table 2 Results of Stratified Meta-Analyses Related to Methodologic Characteristics of Trials With Glue or Patch or Buttress Compared With Control Groups a
 
Sensitivity Analysis
One trial [16[was found to be an outlier. When the study of Fabien and coworkers [16] was excluded from the analysis, the pooled effect size decreased to 0.58 (95% CI: 0.403 to 0.833) with an I2 of 0%. When four trials [10, 12, 13, 19] with a buttressed staple line were excluded from the analysis, the pooled effect size was 0.58 (95% CI: 0.37 to 0.89) with an I2 of 9.6%. When three trials [10, 13, 22] including surgery for emphysema were excluded from the analysis, the pooled effect size was 0.58 (95% CI: 0.39 to 0.86) with I2 of 1.6%.

Bayesian approaches with a sensitivity analysis to prior distributions demonstrated that glue, sealant, patch, or buttress decreased prolonged air leak of more than 7 days compared with control groups (Table 3). The effect size was comparable to that estimated by the frequentist method.


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  		Table 3 Results of Pooling Trials With Glue or Patch and Buttress Compared With Control Groups Using Bayesian Model With Sensitivity Prior a
 
Publication Bias
The funnel-plot asymmetry coefficient was significantly different from zero (asymmetry coefficient –1.23 (95% CI: –2.38 to –0.086; p < 0.04), indicating the presence of publication bias (Fig 3). Figure 3 suggests that publication bias may be present, as the "funnel" appears to be skewed with a scarcity of small studies (a high standard error) in the bottom left-hand corner of the plot. Probable, missing studies were in the bottom right-hand corner of the plot.


Figure 3
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  		Fig 3. Funnel plot to detect publication bias. Odds ratios (OR) are plotted on a logarithmic scale.

 
Adverse Events
The principal adverse events reported in the trials were atelectasis, arrhythmia, hemothorax, pneumonia, pneumothorax, empyema, and postoperative death (Table 4). Neither glue nor patch nor buttress influenced the occurrence of postoperative complications such as atelectasis, hemothorax, pneumonia, pneumothorax, and death (Table 4). Seven trials (817 patients) with glue or patch or buttress showed a decreased risk of postoperative arrhythmia compared with control groups (Table 4) [12, 14, 17–21], which yielded a pooled odds ratio of 0.48 (95% CI: 0.28 to 0.81) and no between-trial heterogeneity (I2 = 0%). Five trials with glue or patch or buttress compared with control groups contributed to the meta-analysis of empyema [11, 14, 15, 18, 19], which showed a pooled odds ratio of 2.2 (95% CI: 0.57 to 8.5; p < 0.25) and no between-trial heterogeneity (I2 = 0%; Table 4).


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  		Table 4 Meta-Analysis of Adverse Effects of Glue or Patch or Buttress Compared With Control Groups
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The various methods such as glue or patch or buttress can reduce the occurrence of prolonged air leak for more than 7 days compared with the conventional methods of suturing or stapling alone. The Cochrane review for the same endpoint selected eight studies [23]. The authors [23] concluded that using a surgical sealant could reduce the incidence of prolonged air leak after pulmonary resection, but the duration of hospitalization was not influenced. They did not recommend this practice routinely, but advised that other trials be conducted [23]. The prolonged air leak endpoint is nevertheless relevant because it indicates that patients are obliged to keep their chest tube, which causes pain and sometimes infectious complications. Secondly, the duration of the chest tube is not the only factor that explains the duration of hospitalization.

Presumably, a publication bias was identified as shown in the funnel plot (Fig 3). The distribution of studies is asymmetrical around zero because smaller studies, which showed no statistically significant effects, remain unpublished [24]. Small studies are often more significant than studies involving larger cohorts. Because of the risk of publication bias, the findings of our meta-analysis must be interpreted with caution.

Our meta-analysis did not reveal heterogeneity between studies for this endpoint. All authors had probably applied the same definition for this endpoint, thus reinforcing its clinical relevance. However, the quality of the studies included in this meta-analysis is intermediate. Indeed, for six of the 13 trials [10, 12, 13, 15, 17, 18], no information on the randomization method was provided. These studies generate a potential selection bias. In only five of the 13 studies [13, 14, 16, 21, 22] were outcomes evaluated without knowledge of the assigned treatment. However, it is unlikely that there is a measurement bias. Indeed, patients with a prolonged air leak for more than 7 days are obliged to keep their chest tube. Consequently, this outcome is objective enough to prevent a systematic error in measurement. The homogeneity between studies argues in favor of this hypothesis. The sensitivity analysis excluding trials with a buttressed staple line, and the surgical treatment of emphysema did not change the pooled effect of the meta-analysis.

For most adverse events, no excess risk was reported. Surprisingly, the surgical sealants and buttress significantly reduced the occurrence of postoperative arrhythmia. The prevalence of arrhythmia after lung surgery [25] is between 8% and 42%. Factors influencing postoperative arrhythmia were age, a history of cardiac disease and the type of pulmonary resection including pneumonectomy [25]. In a randomized controlled trial, these factors are distributed equally in each group and are therefore unlikely to influence the occurrence of arrhythmia. The only factor that may differ in the two treatment groups is a persistent chest tube in patients with prolonged air leak. The chest tube could favor the occurrence of arrhythmia.

The effect size of the four methods is in the same direction, as indicated by the absence of significant interaction. This "naive" indirect comparison does not show whether one method is superior to the others in its ability to reduce prolonged air leak after lung resection. The systematic search of the literature did not identify trials that made a direct comparison between different products. To answer this question, indirect comparisons may help to classify these different methods, depending on the effect sizes. The use of a surgical sealant to prevent prolonged air leak increases costs. But only medicoeconomic studies may show that the cost of these methods are offset by the reduction in the length of hospital stay [26].

In conclusion, this meta-analysis showed that the use of glues, patches, or buttressing reduces the occurrence of prolonged air leak after pulmonary resection. However, publication bias should temper the conclusions of this meta-analysis. Further trials will confirm the effectiveness of these methods on the prevention of postoperative prolonged air leak.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Rice TW, Kirby TJ. Prolonged air leak Chest Surg Clin North Am 1992;2:802-811.
  2. Abolhoda A, Liu D, Brooks A, Burt M. Prolonged air leak following radical upper lobectomy: an analysis of incidence and possible risk factors Chest 1998;113:1507-1510.[Medline]
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  8. Sutton AJ, Abrams K. Bayesian methods in meta-analysis and evidence synthesis Stat Meth Med Res 2001;10:277-303.[Abstract/Free Full Text]
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  10. Hazelrigg S, Boley TM, Naunheim KS, et al. Effect of bovine pericardial strips on air leak after stapled pulmonary resection Ann Thorac Surg 1997;63:1573-1575.[Abstract/Free Full Text]
  11. Wong K, Goldstraw P. Effect of fibrin glue in the reduction of postthoracotomy alveolar air leak Ann Thorac Surg 1997;64:979-981.[Abstract/Free Full Text]
  12. Venuta F, Rendina EA, De Giacomo T, et al. Technique to reduce air leaks after pulmonary lobectomy Eur J Cardiothorac Surg 1998;13:361-364.[Abstract/Free Full Text]
  13. Stammberger UZ, Klepetko W, Stamatis G, et al. Buttressing the staple line in lung volume reduction surgery: a randomized three-center study Ann Thorac Surg 2000;70:1820-1825.[Abstract/Free Full Text]
  14. Wain JC, Kaiser LR, Johnstone JW, et al. Trial of a novel synthetic sealant in preventing air leaks after lung resection Ann Thorac Surg 2001;71:1623-1629.[Abstract/Free Full Text]
  15. Porte HL, Jany T, Akkad R, et al. Randomized controlled trial of a synthetic sealant for preventing alveolar air leaks after lobectomy Ann Thorac Surg 2001;71:1618-1622.[Abstract/Free Full Text]
  16. Fabian T, Federico JA, Ponn RB. Fibrin glue in pulmonary resection: a prospective, randomized, blinded study Ann Thorac Surg 2003;75:1587-1592.[Abstract/Free Full Text]
  17. Allen MS, Wood DE, Hawkinson RW, et al. Prospective randomized study evaluating a biodegradable polymeric sealant for sealing intraoperative air leaks that occur during pulmonary resection Ann Thorac Surg 2004;77:1792-1801.[Abstract/Free Full Text]
  18. Lang G, Csekeo A, Stamatis G, et al. Efficacy and safety of tropical application of human fibrinogen/thrombin-coated collagen patch (TachoComb) for treatment of air leakage after standard lobectomy Eur J Cardiothorac Surg 2004;25:160-166.[Abstract/Free Full Text]
  19. Gomez-Caro A, Roca Calvo MJ, Lanzas JT, et al. The approach of fused fissures with fissureless technique decreases the incidence of persistent air leak after lobectomy Eur J Cardiothorac Surg 2007;31:203-208.[Abstract/Free Full Text]
  20. Tansley P, Al-Mulhm F, Lim E, Ladas G, Goldstraw P. A prospective, randomized, controlled trial of the effectiveness of Bioglue in treating alveolar air leaks J Thorac Cardiovasc Surg 2006;132:105-112.[Abstract/Free Full Text]
  21. Anegg U, Lindenmann J, Matzi V, et al. Efficiency of fleece-bound sealing (Tachosil) of air leaks in lung surgery: a prospective randomized trial Eur J Cardiothorac Surg 2007;31:198-202.[Abstract/Free Full Text]
  22. Moser C, Opitz I, Zhai W, et al. Autologous fibrin sealant reduces the incidence of prolonged air leak and duration of chest tube drainage after lung volume reduction: a prospective randomized blinded study J Thorac Cardiovasc Surg 2008;136:843-849.[Abstract/Free Full Text]
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