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Ann Thorac Surg 2005;79:1167-1173
© 2005 The Society of Thoracic Surgeons

Original articles: General thoracic

Characterization and Importance of Air Leak After Lobectomy

Ikenna Okereke, MDa, Sudish C. Murthy, MD, PhDa,*, Joan M. Alster, MSb, Eugene H. Blackstone, MDa,b, Thomas W. Rice, MDa

a Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio
b Department of Quantitative Health Sciences, The Cleveland Clinic Foundation, Cleveland, Ohio

Accepted for publication August 30, 2004.

* Address reprint requests to Dr Murthy, Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, 9500 Euclid Ave/Desk F24, Cleveland, OH 44195 (E-mail: murthys1{at}ccf.org).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Appendix 1
 Appendix 2
 References
 
BACKGROUND: Air leak after pulmonary resection is a common occurrence that is incompletely characterized. Our objectives were to determine prevalence of air leak and identify its risk factors, characterize its duration and discover its correlates, and evaluate its clinical importance.

METHODS: Air leak was studied in 319 patients undergoing isolated anatomic lobectomy between January 1998 and July 2001. Risk factors for air leak were identified by logistic regression of patient characteristics, indications for lobectomy, lobe resected, and fissure management. Factors associated with air leak duration were sought by time-related analysis. Association of complications with air leak was evaluated by propensity-matched pairs analysis.

RESULTS: Prevalence: Air leak prevalence was 58% (186 patients). It occurred less frequently after left lower lobectomy (p < 0.0001) and later in the series (p = 0.008). It was surgeon dependent (p = 0.007) but not associated with forced expiratory volume in 1 second. Duration: The 10th, 50th, and 90th percentiles of air leak duration were 1.6, 3, and 7 days, respectively. No factors, including fissure management, were reliably associated with air leak duration. Importance: Air leak was associated with more complications (30% vs 18%, p = 0.07) and protracted hospital course (p = 0.02).

CONCLUSIONS: Postoperative air leak is a common occurrence after lobectomy, but fortunately it is self-limiting in most patients. Air leak is independently associated with longer hospital stay and other postoperative complications. Surgical technique is important and may be the only modifiable factor.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Appendix 1
 Appendix 2
 References
 
Air leak frequently occurs after pulmonary resection and can complicate hospital stay [1–4]. Although there are randomized trials of its treatment [5, 6], those studies have included heterogeneous types of operation and indications. Thus, there is no consensus on the most effective method for its prevention [1, 4, 7–9] and little information regarding risk factors [10–12]. Understanding the importance of air leak could lead to strategies to prevent it and justify additional cost incurred by these strategies [4, 9, 13]. Therefore, purposes of this study were to (1) determine prevalence of air leak and identify its risk factors, (2) characterize duration of air leak and discover its correlates, and (3) evaluate importance of air leak to patient recovery. This study represents an important departure from prior ones in that the study population is homogeneous with respect to type of operation and indication for operation.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Appendix 1
 Appendix 2
 References
 
Patients
Of 441 patients undergoing lobectomy between January 1998 and July 2001, air leak was studied in 319 consecutive patients who had lobectomy only. Patients undergoing lobectomy with chest wall resection, sleeve lobectomy, or bilobectomy were excluded. Thus, the study cohort represented a homogeneous population with respect to era of operation, indication for operation (> 90% for cancer; Table 1), operative approach (98% thoracotomy), and surgery type (lobectomy only). Upper lobectomy predominated (see Table 1), and three surgeons performed 56%, 32%, and 11% of the operations. Fissures were most frequently stapled. Chemical sealants and parenchymal staple line buttressing materials were not used during this study. Mean age of study patients was 65 ± 11 years.


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  		Table 1. Operative Characteristics Overall and According to Absence or Presence of Air Leak
 
Demography, clinical factors and functional status, and lung pathology (Tables 2 and 3) were reviewed and abstracted, as were length of postoperative stay and complications. These data were recorded in a thoracic surgery registry that was approved for research by the institutional review board.


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  		Table 2. Patient Characteristics Overall and According to Presence of Air Leak (Categorical Variables)
 

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  		Table 3. Patient Characteristics Overall and According to Absence and Presence of Air Leak (Continuous Variables, Mean ± Standard Deviation)
 
Air Leak
Occurrence and duration of air leak were abstracted by detailed medical record review. Air leak was characterized beginning with initial postoperative assessment in the recovery room after lobectomy. We did not use intraoperative presence of air leak as a surrogate for postoperative air leak, because of the known poor correlation between the two [9]. It was documented by a dedicated thoracic surgical team at least twice daily and confirmed by surgeon. If air leak occurred, day of resolution was documented and confirmed in the same fashion. Unexpectedly, no latent air leaks were observed; therefore, duration of air leak was calculated as the interval from initial observation in the recovery room to confirmed cessation. It was not possible from medical record review to characterize air leak in terms of quantitative volume, effort dependency, or association with respiratory cycle, although these often unrecorded variables were clinically important for chest tube management. Time of conversion of chest tube from suction to water seal was not consistently documented.

Chest Tube Management
Chest tube management was by clinical protocol, uniform across the study time frame and surgical services. It consisted of an early period (at least 1 day) of suction (–20 cm H2O) with conversion to water seal when air leak qualitatively diminished and chest radiograph demonstrated lung expansion.

Air leak (186 patients) was treated in three ways, used alone or in combination.

• Chest tubes were left in place without chemical pleurodesis until cessation of the leak or decrease in pleural drainage to less than 200 mL/day (74 patients [40%] managed with this alone).
• Chemical pleurodesis was performed by instilling a solution of 200 mg doxycycline and 300 mg lidocaine through existing chest tubes (112 patients, 60%). The chest tube system was suspended above the patient for 8 hours, during which the position of the patient was changed every half hour.
• Patients were discharged with Heimlich valves (7 patients, 4%, all had chemical pleurodesis).

Clinical End Points
Respiratory complications included atelectasis, pneumonia, and pleural effusion. Atelectasis was defined by chest radiogram and required bronchoscopy for management. Pneumonia was defined by occurrence of at least two of the following three criteria: chest infiltrate on radiography, positive sputum culture, and antibiotic administration. Pleural effusion was defined by chest radiogram and required intervention (thoracentesis, thoracostomy, thoracoscopy, or reoperation); it did not include chylothorax or empyema. Cardiac complications were new-onset atrial arrhythmia or perioperative myocardial infarction [14].

Data Analysis
AIR LEAK OCCURRENCE
Factors associated with occurrence of air leak were identified by multivariable logistic regression (see Appendix 1 for risk factors considered) using bootstrap bagging and a p value for variable retention of 0.05 [15, 16]. Following determination of a main effects model, all possible two-way interactions between these effects were evaluated. During model building, noninformative means imputation was employed for sporadic missing values; final models were confirmed without imputation.

AIR LEAK DURATION
Among patients with air leak, a parametric method was used to characterize the distribution of intervals from operation to cessation of air leak [17]. (For additional details, see http://www.clevelandclinic.org/heartcenter/hazard.) With this method, multivariable analysis was performed using the same variables and variable selection techniques described under "Air Leak Occurrence."

AIR LEAK IMPORTANCE
Additional nonsignificant variables were added to the parsimonious model for air leak occurrence (see "Air Leak Occurrence") to create for each patient a propensity score that expressed the probability of developing air leak after surgery [18, 19]. Variables included the following: age, body mass index, smoking history, cardiac disease, forced expiratory volume in 1 second (FEV1), Eastern Cooperative Oncology Group (ECOG) score, diabetes, preoperative creatinine, preoperative hemoglobin, disease status (malignant vs benign), pleural adhesions, surgery for mass, left lower lobectomy, well-differentiated tumor, induction therapy, use of epidural analgesia indicator, perioperative mediastinoscopy, mediastinal lymph node dissection, fissure management, bronchial closure, date of operation, and surgeon. This propensity score was used to create a propensity-matched data set of equal numbers of patients with and without air leak using greedy matching. This data set was used to assess whether air leak was associated with postoperative complications, hospital death, or length of hospital stay. Savage scores were used to assess length of stay because discharge policy dictates similar median lengths of stay, but Savage scores compare the right tails of the distribution of discharge day.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Appendix 1
 Appendix 2
 References
 
Air Leak Occurrence
Prevalence of air leak was 58% (186 of 319 patients; Tables 1–3). Patients less likely to experience air leak were those undergoing left lower lobectomy, those operated on more recently, and those operated on by one surgeon (Table 4 and Fig 1). Importantly, gender, patient size, FEV1, FEV1/forced vital capacity (FVC), smoking history, induction therapy, and fissure management did not emerge as risk factors for occurrence of air leak. Suppression of surgeon and date of operation in the multivariable analysis did not reveal additional and more informative correlates of air leak.


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  		Table 4. Risk Factors for Air Leak
 


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  		Fig 1. Decrease in percentage of patients experiencing air leaks across experience. Graph is a nomogram of the multivariable logistic equation of Table 4, with the equation solved for surgeon C = "no." Dashed lines enclose 68% confidence limits of the estimates, equivalent to 1 standard error. and {circ} = raw data frequencies by year. (LLL = left lower lobectomy.)

 
Air Leak Duration
Among patients with air leak, 10th, 50th (median), and 90th percentiles of air leak duration were 1.6, 3, and 7 days, respectively (Fig 2). Bootstrap bagging techniques failed to identify any risk factor reliably associated with duration of air leak, including FEV1, FEV1/FVC, smoking history, type of lobectomy, induction therapy, and fissure management. Efficacy of chemical pleurodesis was not demonstrable (see Appendix 2).



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  		Fig 2. Duration of air leak among 186 patients. (A) Percentage of patients with air leak. Circles represent nonparametric (Kaplan-Meier) estimates, and vertical bars are 68% confidence limits, equivalent to one standard error. Numbers in parentheses represent patients with air leak. Solid line is parametric estimate enclosed within 68% confidence limits. (B) Probability density function, showing percentage of patients whose air leak had ceased.

 
Air Leak Importance
Propensity matching produced 82 well-matched pairs of patients with and without air leak. Postoperative in-hospital complications were higher (30%) among patients who experienced air leak than in those who did not (18%, possibly higher than expected by chance) (p = 0.07; Table 5). Distribution of length of postoperative stay was not different for the first 5 days (the median time to discharge in both groups); thereafter, hospital stay was longer in patients who experienced air leak (p [Savage scores] = 0.02; Fig 3).


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  		Table 5. Comparison of Postoperative Events Between Propensity-Matched Pairs
 


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  		Fig 3. Duration of postoperative stay in propensity-matched patients with (- - -) and without (—) air leak. Graph is a cumulative distribution function.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Appendix 1
 Appendix 2
 References
 
Air leak is a common and potentially preventable problem that may be best considered in the same context as intraoperative blood loss; that is, there is no amount of air leak that is ever good, and no substitute for none. Until now, air leak has been considered a complication only when it persists beyond the normal hospital stay [20]. This arbitrary definition has rendered it difficult to compare multicenter data and ignores the potential impact of the vast majority of air leaks. This large study was devised to characterize air leak after lobectomy in a rigorous fashion, documenting its prevalence, duration, and clinical importance without arbitrarily classifying (dichotomizing) its duration as persistent or not. We hoped to generate new insight and clarify a very old problem. We chose to study a homogeneous group of patients (isolated lobectomy) in whom fissure management is critical, staple line length is less random, and type of surgery and indications for operation do not confound outcome.

Prevalence
Postoperative air leak was a frequent but not inevitable occurrence. It was least common after left lower lobectomy. Potential explanations for this are (1) a single left-sided fissure to control (vs two on the right side), (2) superior mobility of the left hemidiaphragm that is space obliterating and in direct apposition to the staple line, and (3) shifting of the pericardium and mediastinum to the left, allowing the left upper lobe to fill the remaining space.

Overall, our surgical technique appeared to improve during the study period, with occurrence of air leak declining substantially. This improvement was independent of adding a young surgeon whose patients experienced the lowest prevalence of air leak. The influx of new surgeons during the course of the study fostered dialogue that heightened awareness and resulted in subtle practice changes. This was fueled in part by efforts to shorten hospital stay. Interestingly, when air leak prevalence for each surgeon was examined, it did not correlate with years in practice. We were also unable to explain this difference by type of stapler used, management of the fissure, or surgical volume. Lower FEV1, lower FEV1/FVC ratio, diabetes mellitus, advanced age, male gender, and pleural adhesions were not found to be risk factors for air leak, as variably suggested by others [10, 12, 21–24]. We suspect that the reason FEV1 and FEV1/FVC ratio were not implicated as risks for air leak in this study was that all cases were lobectomies. Consequently, stapled margins were likely under less tension than might be expected for wedge resection and more pneumostatic. Pleural adhesions have recently been identified as a risk factor for prolonged air leak [24]. We did not find this in our study, despite grading pleural adhesions. Differences in perioperative mechanical ventilation are difficult to account for. We minimize barotrauma during reexpansion of the operated lung, and our patients are routinely extubated in the operating room. Differences in other technical details, such as lysis of pleural adhesions, could also account for differences in findings. In addition, reliability statistics have not been used in any previous study, and we suspect that some risk factors previously identified might be less important than reported.

Duration
Regardless of any specific intervention, more than 50% of air leaks ceased by postoperative day 3. By the 7th postoperative day (see Fig 2), only 10% of air leaks remained, representing 6% of all patients undergoing lobectomy over the course of the study.

We could not identify any predictors of air leak duration, although many preoperative and intraoperative factors were examined. Clearly, early identification of patients with the longest duration air leaks is central to specific therapies (Heimlich valve, talcum pleurodesis, reoperation, etc.) being promptly instituted in this small subset of patients. To this end, the air leak grading system described by Cerfolio and colleagues [5, 23] may be useful.

As best we can tell, chemical pleurodesis with doxycycline, although safe, did not demonstrably reduce air leak duration. There are at least two possible explanations. Most air leaks resolve quickly with or without treatment, reducing the study's power to identify a subtle effect of indiscriminate use of doxycycline sclerosis. Second, doxycycline at the concentration used was inadequate.

Clinical Importance and Recommendations
We have demonstrated that presence of air leak (regardless of duration) predicts a worse outcome (longer hospital stay and more complicated postoperative course). Thus, we now consider any air leak as a surgical complication, not simply those lasting 7 days or more. This emphasizes the importance of preventing air leak at the time of operation. A comprehensive strategy for air leak must include both prevention and effective management.

Prevention
Because preoperative identification of patients at high risk for air leak may not be possible, we recommend concentrating on intraoperative prevention. Technical factors of the operation are important, although unfortunately, specific details of resection influencing air leak did not emerge from this study. Every attempt should be made to leave the operating room with pneumostasis. Unfortunately, intraoperative assessment of air leak is an inadequate surrogate for postoperative air leak [9].

Pneumostasis can be achieved by careful handling of the lung, meticulous dissection of the fissure, and avoidance of exposed raw surface of the lung. Several operative techniques have been recommended to achieve this [7]. Others have advocated tissue sealants and staple line buttressing [4, 7–9, 13, 25]. Although multiple feasibility studies exist, we are awaiting positive randomized efficacy studies before recommending any specific sealant or buttress. However, cost-benefit issues are important because our experience suggests that tissue sealants can increase operating room supply costs by as much as 50%.

Pleural space reduction is also important for pneumostasis. Pleural tenting, transient diaphragm paralysis, and pneumoperitoneum are useful techniques for large space problems and may reduce the prevalence of air leak through mechanisms similar to those that occur after left lower lobectomy [4, 26–29]. The role of intraoperative ventilator management, though difficult to quantify, is likely important. The operated lung must be carefully reinflated, and spikes in airway pressure must be avoided to prevent staple line disruption.

Management
Practical guidelines for postoperative management of air leak when it occurs have been proposed by others [5, 6, 23, 30]. Indiscriminant chemical pleurodesis with doxycycline was ineffective, and we are now adopting an early water seal policy for chest tube management. Postoperative pneumoperitoneum may be useful for space problems [26]. Refractory air leaks may best be handled with talcum slurry instillation, although problems with this approach have been detailed previously [31, 32]. Use of Heimlich valves should be restricted to responsible patients and situations in which minimal drainage is present. Close follow-up of these patients is imperative. We reserve reoperation for the rare air leak that fails more conservative therapies.

Limitations
This is a single-center clinical study that relies on retrospective review of data. In addition, time-related magnitude of air leak was not quantified in all patients, precluding its use in analysis. Moreover, factors such as intraoperative anesthetic management, maneuvers used to demonstrate intraoperative air leak, and individual surgeon tolerance to air leak were not quantified.

Conclusions
Postoperative air leak is a common occurrence after lobectomy, but fortunately it is self-limiting in most patients. Air leak is independently associated with longer hospital stay and other postoperative complications. Surgical technique is important and may be the only modifiable factor.


   Appendix 1
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Appendix 1
Appendix 2
 References
 
Variables Considered in Analyses
DEMOGRAPHY
Age (years), gender, height (cm), weight (kg), body surface area (m2), body mass index (kg · m–2), weight to height ratio.

CLINICAL CONDITION AND PRERESECTION TREATMENTS
American Society of Anesthesiologists score, Eastern Cooperative Oncology Group score, induction chemoradiotherapy, mediastinoscopy, radiation, chemotherapy (the latter two were considered induction therapy whether combined or used separately).

PREOPERATIVE PULMONARY COMORBIDITIES
Smoking history and pack years, previous cancer surgery, forced expiratory volume in 1 second (FEV1, L · s–1), FEV1 expressed as percent of predicted normal, forced vital capacity (FVC, L), FVC expressed as percent of predicted normal, FEV1/FVC ratio, pleural adhesions.

PREOPERATIVE NONPULMONARY COMORBIDITIES
Diabetes, creatinine, hemoglobin, weight loss, cardiac diseases, previous cardiac surgery.

TUMOR CHARACTERISTICS—CLINICAL STAGING
Benign versus malignant disease, preoperative tumor, node, and metastasis (TNM) classifications.

TUMOR CHARACTERISTICS—PATHOLOGY
Pathologic stage, pathologic T, N, and M classifications, number of malignant pulmonary nodules, histopathology including degree of differentiation (well, moderate, poor, undifferentiated) and type (adenocarcinoma, squamous cell, bronchoalveolar, large cell, other).

INDICATION FOR OPERATION
Infection, mass, cancer.

PROCEDURAL VARIABLES
Surgeon, approach (thoracotomy, video-assisted), fissure management (blunt dissection, electrocautery, gastrointestinal anastomosing stapler [Endo GIA, United States Surgical Corp, Auto Suture Company Division, Norwalk, CN); multi-fire]), lobectomy type (left lower, left upper, right lower, right middle, right upper), bronchial closure (buttressed, stapled, sutured), mediastinal lymph node dissection, date of operation (years since January 1, 1998).

POSTOPERATIVE MANAGEMENT
Epidural analgesia, volume (L) of crystalloid infused during surgery, use of intraoperative blood transfusion.


   Appendix 2
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Appendix 1
 Appendix 2
References
 
Assessment of Air Leak Management by Pleurodesis
DATA ANALYSIS
Among patients with air leak, logistic regression with bootstrap bagging (Breiman L. Bagging predictors. Machine Learning 1996;24:123–40; Blackstone EH. Breaking down barriers: helpful breakthrough statistical methods you need to understand better. J Thorac Cardiovasc Surg 2001;122:430–9) was employed to identify variables associated with chemical pleurodesis and to develop a propensity score (Rosenbaum PR, Rubin DB. The central role of the propensity score in observational studies for causal effects. Biometrika 1983;70:41–55; Blackstone EH. Comparing apples and oranges. J Thorac Cardiovasc Surg 2002;123:8–15) using patient, tumor, and operative variables (see "Air Leak Importance" under Patients and Methods). Effect of chemical pleurodesis on air leak duration was then assessed in four ways: (1) The propensity score and chemical pleurodesis were added to the multivariable analysis of air leak duration. (2) Chemical pleurodesis was treated as a time-varying covariable. (3) Interaction of surgeon and chemical pleurodesis was studied by multivariable analysis. (4) A nonparsimonious model containing many explanatory variables considered to be potential predictors of air leak duration as well as the time-varying chemical pleurodesis variable and propensity score was developed.

RESULTS
Of the 186 patients with air leak, 112 (60%) received at least one attempt at chemical pleurodesis. Chemical pleurodesis was strongly dependent on surgeon and was used more frequently earlier in the experience (Appendix 2, Table 1) . It was repeated in 54 patients—twice in 30 and three or more times in 24. Sixty-two of the 112 patients (55%) had chemical pleurodesis on postoperative day 1, 21 (19%) on day 2, 18 (16%) on day 3, 5 (4%) on day 4, 4 (4%), on day 5, and 2 (2%) on day 7. Effectiveness of chemical pleurodesis was not demonstrable (p > 0.9) by any of the four assessments, because use of chemical pleurodesis was highly confounded with surgeon.


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  		Appendix Table 1. Patient and Operative Characteristics According to Chemical Pleurodesis Treatment Among 186 Patients With Air Leak
 


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Appendix 1
 Appendix 2
 References
 

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 Ann. Thorac. Surg.Home page
M. H. Cho, A. Malhotra, D. M. Donahue, J. C. Wain, R. S. Harris, D. Karmpaliotis, and S. R. Patel
Mechanical ventilation and air leaks after lung biopsy for acute respiratory distress syndrome.
Ann. Thorac. Surg., July 1, 2006; 82(1): 261 - 266.
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E. E. Roselli, S. C. Murthy, T. W. Rice, P. L. Houghtaling, C. D. Pierce, D. P. Karchmer, and E. H. Blackstone
Atrial fibrillation complicating lung cancer resection
J. Thorac. Cardiovasc. Surg., August 1, 2005; 130(2): 438 - 444.
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