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Original Research: INTERVENTIONAL PULMONOLOGY |

Treatment of Persistent Pulmonary Air Leaks Using Endobronchial Valves FREE TO VIEW

John M. Travaline, MD, FCCP; Robert J. McKenna, Jr, MD, FCCP; Tiziano De Giacomo, MD; Federico Venuta, MD, FCCP; Steven R. Hazelrigg, MD, FCCP; Mark Boomer, MD; Gerard J. Criner, MD, FCCP; for the Endobronchial Valve for Persistent Air Leak Group*
Author and Funding Information

From the Temple University School of Medicine (Drs. Travaline and Criner), Philadelphia, PA; Cedars-Sinai Medical Center (Dr. McKenna), Los Angeles, CA; the University of Rome (Drs. De Giacomo and Venuta), Rome, Italy; Southern Illinois University School of Medicine (Dr. Hazelrigg), Springfield, IL; and Saint Francis Hospital (Dr. Boomer), Tulsa, OK.

John M. Travaline, MD, FCCP, Professor of Medicine, Temple Lung Center, 3401 North Broad St, Philadelphia, PA 19140; e-mail: trav@temple.edu

*Members and affiliations for the Endobronchial Valve for Persistent Air Leak Group are listed in the Appendix.


Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (www.chestjournal.org/site/misc/reprints.xhtml).


© 2009 American College of Chest Physicians


Chest. 2009;136(2):355-360. doi:10.1378/chest.08-2389
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Published online

Background:  Prolonged pulmonary air leaks are a significant source of frustration for patients and physicians. When conventional therapy fails, an alternative to prolonged chest tube drainage or surgery is needed. Bronchoscopic blockage of a bronchus can be performed with the hope of accelerating closure of the air leak by reducing the flow of air through the leak. To our knowledge, this article presents the largest series of patients with prolonged air leaks treated with an endobronchial valve.

Methods:  With Internal Review Board approval, endobronchial valves were compassionately placed using flexible bronchoscopy in patients with prolonged air leaks at 17 international sites.

Results:  Between December 2002 and January 2007, 40 patients (15 women; mean age ± SD, 60 ± 14 years) were treated with one to nine endobronchial valves per patient. The air leaks had recurrent spontaneous pneumothorax (n = 21), postoperative (n = 7), iatrogenic (n = 6), first-time spontaneous pneumothorax (n = 4), bronchoscopic lung volume reduction (n = 1), and trauma (n = 1) etiologies. Nineteen patients (47.5%) had a complete resolution of the air leak, 18 (45%) had a reduction, 2 had no change, and 1 had no reported outcome. The mean time from valve insertion to chest tube removal was 21 days (median, 7.5 days; interquartile range [IQR], 3 to 29 days) and from valve procedure to hospital discharge was 19 ± 28 days (median, 11 days; IQR, 4 to 27 days).

Conclusions:  Use of endobronchial valves is an effective, nonsurgical, minimally invasive intervention for patients with prolonged pulmonary air leaks.

Figures in this Article

Prolonged pulmonary air leaks are common and may cause considerable morbidity, prolonged hospital stay, and increased health-care costs. When an air leak is present on the fourth postoperative day, the chance of air leak on postoperative day 7 is 83%.1 In addition to occurring after 15% of thoracic operations,2 other causes of prolonged air leaks may include the following underlying pulmonary diseases: bullous emphysema, advanced pulmonary sarcoidosis, radiation fibrosis, and interstitial lung disease. The treatment of patients with air leaks due to underlying pulmonary disease is often very challenging due to the poor ability of the diseased lung to heal.

Because the poor performance status caused by pulmonary disease may increase the risk for surgical intervention, alternative therapies are needed. Treatment of prolonged air leaks by sclerosing agents3 has shown little efficacy and variable patient tolerance. Various endobronchial approaches include the application of gelfoam, the use of fibrin glue in conjunction with endovascular metallic ring-shaped coil placement,4 tracheobronchial stent deployment,5 and endobronchial valves.613 The results of these nonsurgical approaches appear promising and, for some patients, may be the only treatment option after all conventional treatments have failed or are associated with high risk. To our knowledge, this article reports the largest series of patients with prolonged pulmonary air leaks, mostly related to secondary pneumothoraces, treated with an endobronchial valve (Zephyr EBV; Emphasys Medical; Redwood City, CA) in order to assess the results of this bronchoscopic approach for the treatment of prolonged air leak.

In the United States, patients were treated under compassionate- use regulatory provisions in which individual Food and Drug Administration and Internal Review Board approvals were obtained for each patient. Outside the United States, the device was commercially available, with an approved indication for treatment of air leak. Individual case studies for six patients have been previously reported712 in the medical literature.

The endobronchial valve system used in this series (Fig 1) consists of a silicone-based, one-way valve mounted in a self-expanding nitinol retainer. The self-expanding retainer stabilizes the device in the airway and provides an airtight seal against the bronchial wall. The one-way valve is positioned in the center of the device to allow it to function independently of the anchoring portion of the valve. The valve is intended to block air from flowing through the air leak while allowing distal secretions to drain normally. The device is designed to function as a permanent implant but can, at physician discretion, be removed with graspers subsequent to resolution of the air leak. Figure 2 shows a transcopic valve in the right middle lobe bronchus.

Figure Jump LinkFigure 1 Transcopic endobronchial valve (Zephyr EBV; Emphasys Medical, Redwood City, CA).Grahic Jump Location
Figure Jump LinkFigure 2 Bronchoscopic view of valve following deployment in right middle lobe bronchus.Grahic Jump Location

Anesthesia and access approaches varied across centers, depending on patient status and physician preference. The procedure was performed with IV sedation, spontaneous breathing, and flexible bronchoscopy. Alternative approaches involved general anesthesia, rigid bronchoscopy, and mechanical ventilation.

Prior to valve implantation, the chest drainage system was observed to assess the air leak. A balloon-tipped catheter was inserted into the lobar airway suspected of supplying the air leak. To provide selective bronchial occlusion, the balloon was inflated to block the airflow to that region of the lung. The air leak rate through the chest tube was then assessed qualitatively for reduction. If the leak rate was reduced, the balloon catheter was deflated and repositioned into a more distal airway. The process was repeated to identify the segmental or subsegmental airway or airways that, when occluded, offered the greatest reduction in air leak rate. These airways then were targeted for valve placement.

The endobronchial valves were delivered to the target airway using a flexible catheter. The valves were compressed into the distal tip of the delivery catheter using a valve loader supplied with the system. The delivery catheter was then passed through the working channel of a standard adult bronchoscope (≥ 2.8 mm inner diameter) and guided to the target airway. Once in place, the valve was deployed.

Following valve implantation, patients were allowed to recover from anesthesia according to standard hospital practice. Vital signs and arterial blood gas levels were closely monitored. Chest radiography often was used to assess target lung inflation status. Between December 2002 and January 2007, 15 centers used the endobronchial valves to treat patients with prolonged pulmonary air leaks.

The following data were retrospectively abstracted from patients' medical records: demographic information, the cause of the air leak, associated diseases, and whether hospitalization was medical or surgical. In addition, several end points were chosen to assess endobronchial valve efficacy in treating the underlying bronchopleural fistula, including the lung involved, the number and duration of chest tubes used, the need for other interventions to treat the air leak, and length of hospital stay. These variables were analyzed using simple descriptive statistics.

Fifteen women and 25 men (mean age ± SD, 60 ± 14 years) had at least one endobronchial valve (range, one to nine valves) placed for the management of prolonged pulmonary air leak. Primary comorbidities in these patients were cancer (30%); COPD (30%); pneumonia (7.5%); and other (22.5%), which were rheumatoid arthritis (n = 2), tuberculosis (n = 1), trauma (n = 1), aspergilloma (n = 1), bronchiectasis (n = 1), cor pulmonale (n = 1), lung transplantation (n = 1), and multiple comorbidities (n = 1).

Table 1 shows the etiology and classification of the air leaks prior to the endobronchial valve procedure. Prior to the procedure, 39 patients had at least one chest tube (range, one to five tubes per patient). One patient had an Eloesser flap. The mean duration of air leak prior to valve treatment was 119 days (median, 20 days; interquartile range [IQR], 15 to 45 days). Thirty-five patients were treated with an endobronchial valve only. Prior to placement of an endobronchial valve, five patients had other treatments, which included blood patch (n = 3), wedge resection (n = 1), and pleurodesis (n = 1).

Table Graphic Jump Location
Table 1 Etiology of Air Leak Grouped by Classification (n = 40)

Figure 3 shows representative chest radiographs of a 66-year-old woman with a history of COPD and coronary artery disease who had a loculated right pneumothorax and bronchopleural fistula following video-assisted thoracoscopy and talc pleurodesis. A bronchopleural fistula remained despite chest tubes (Fig 3A) but was reduced following the placement of four endobronchial valves (Fig 3B).

Figure Jump LinkFigure 3 A: Representative chest radiograph showing patient with right-loculated basilar pneumothorax and extensive soft-tissue air (lower arrow and upper arrow, respectively). B: One week following an endobronchial valve placement procedure (four valves) [valves encircled; arrows noting absence of abnormalities noted in A], showing lessened pneumothorax and soft-tissue air.Grahic Jump Location

Valve procedures were performed in one session in 37 patients, two sessions in 2 patients, and four sessions in 1 patient, for a total of 116 valves inserted. The classic-type valve was used in 5 patients, and transcopic valves were used in 35 patients. The mean number of valves placed per patient was 2.9 ± 1.9 overall, 3.19 ± 2.2 for secondary pneumothorax, 2.83 ± 2.3 for iatrogenesis, and 2.75 ± 1.5 for primary and 2.28 ± 1.1 for postsurgical air leak. The valves were placed in the right upper lobe (n = 11), right middle lobe (n = 3), right lower lobe (n = 3), left upper lobe (n = 11), left lower lobe (n = 5), right upper and right lower (n = 1), right lower and middle lobe (n = 1), and right upper and left upper lobe (n = 1). In four patients, the target lobe was not reported. The valve procedures were performed using conscious sedation in 16 patients, general anesthesia in 16 patients, and deep sedation in 8 patients.

Following valve placement, the air leaks resolved or decreased in 37 patients (92.5%); 19 patients (47.5%) had complete resolution of acute air leak, 18 patients (45.0%) had reduction, and 2 patients (5.0%) had no change in air leak status. For one patient (2.5%), the immediate change in air leak was not reported. No relationship was found between the resolution or reduction in air leak and the location of the valve or the etiology of the air leak (data not shown). Overall, the mean time from valve placement to chest tube removal for the 28 patients with complete information was 21 days (median, 7.5 days; IQR, 3 to 29 days). The time from insertion of the valve to hospital discharge (35 patients were discharged alive; 1 patient had missing information) was 19 ± 28 days (median, 11 days; IQR, 4 to 27 days). Thirty-four patients had no adverse event related to the valve placement; adverse events for the remaining six patients were valve expectoration, moderate oxygen desaturation; initial malpositioning of the valve that required redeployment, pneumonia, methicillin-resistant Staphylococcus aureus colonization following a second valve procedure, and an unspecified event.

Of the 40 patients, 8 had the valves removed after cessation of the air leak. In two of the eight patients, the valves were removed over two sessions. Overall, the valves were in place for an average of 66 ± 53 days (range, 7 to 143 days) prior to removal. In 32 patients, the clinician elected to leave the valves in place.

Follow-up ranged from 5 to 1,109 days after valve implantation. At last follow-up, 24 patients were reported to be alive. The causes of death for the remaining 16 patients were underlying disease (n = 8), cancer (n = 4), bronchiectasis (n = 1), emphysema (n = 1), respiratory failure (n = 1), and sepsis (n = 1). No deaths were attributed to the valve or implantation of the valve.

We show that the implantation of endobronchial valves is effective for a large number of patients with prolonged air leaks following primary and secondary causes of pneumothorax. Complete cessation of air leak following endobronchial valve implantation was achieved in 48% of patients. An additional 45% experienced diminution in the magnitude of air leak. Combined, 93% of patients had improvement in air leak status following valve treatment. The valve implantation procedure and the valve itself also were well tolerated, with few adverse events.

Prolonged pulmonary air leak leads to considerable morbidity for patients, and complications have prompted the need for a nonsurgical, minimally invasive approach to treat patients with this condition. One such approach is an endobronchial valve system (Zephyr EBV), a device initially developed as a nonsurgical method of lung volume reduction for emphysema. This bronchoscopically deployed, one-way device blocks airflow into targeted areas of the lung that are the origin of prolonged air leaks. The valves are placed in the segmental or subsegmental airways proximal to the area of the air leak. The air is prevented from entering the pleural space, thereby enabling the lung to possibly reexpand and heal.

The management of persistent air leaks remains a challenge for pulmonologists and thoracic surgeons. Whether they arise from primary or secondary pneumothoraces or complicate lung resection surgery, they are associated with increased morbidity and frustrate patients who want to be free of chest tubes and not undergo additional surgical procedures. In many patients, surgical options for the treatment of air leaks do not exist, and effective alternative interventions are necessary.

Predictors of persistent air leaks in patients include poor wound-healing characteristics, such as preoperative use of steroids, a low FEV1 percentage, and low maximum voluntary ventilation percentage.14 Intraoperative techniques for surgeons to decrease the likelihood of persistent air leak following lung resection include bovine pericardium buttressing of staple lines,15 use of pleural tents for upper lobectomies,16 use of pneumoperitoneum after lower lobectomies,17 and the use of fibrin glue.18 When persistent air leaks develop despite these measures, they are associated with prolonged hospitalization and increased cost. Patients with prolonged air leak also have an increased risk for postoperative morbidities, such as empyema, fever, and pneumonia.19

Several investigators713 have reported the use of endobronchial valves in the management of persistent air leaks, and in all the cases, the patient's underlying condition made the choice of a nonsurgical intervention most appropriate. For example, Toma and colleagues13 reported the use of endobronchial valves in two complex medical conditions. One woman with lymphangioleiomyomatosis shortly following single-lung transplantation required a modified Monaldi decompressing procedure on her native lung complicated by a persistent air leak. The other patient had bilateral pneumothoraces and a persistent air leak following a complicated course of severe pneumonia and ARDS. Similarly, the patients reported here all had significant comorbidities, limiting the safe application of surgical intervention and necessitating the use of less-invasive therapy.

The major limitation of this report is its retrospective, nonrandomized, and uncontrolled methodology. This case series, however, contributes additional information to support the application of this nonsurgical approach to the management of persistent pulmonary air leaks. Further, it serves as a basis to study endobronchial valves in a controlled, randomized, and prospective fashion.

In summary, this report on a large series of patients confirms what has been previously demonstrated in case reports about the use of an endobronchial valve for the treatment of prolonged pulmonary air leak. Further, based on the efficacy of this valve in the treatment of prolonged air leak, it extends the indication for the use of the valve in patients with this condition. It is a reasonable, nonsurgical, minimally invasive intervention that may be appropriate for the treatment of prolonged air leaks in patients who are either operable or inoperable. Prospective trials are needed, however, to further characterize the clinical circumstances in which this intervention may be most appropriate.

Dr. Travaline contributed to the concept and organization for the manuscript, data collection and organization, statistical analysis, and the primary preparation and writing of the manuscript. Dr. Criner contributed to the concept and organization of the manuscript. Dr. McKenna contributed to the primary preparation and writing of the manuscript. All authors contributed to data collection and additional review, writing, and editing of the manuscript.

Dr. Travaline was a coinvestigator for the VENT Study-Endobronchial Valve for Emphysema Palliation Trial Emphasys Medical, Inc, from 2003 to 2008. Dr. Boomer is a consultant for Pneum Rx. The remaining authors have reported to the ACCP that no significant conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Appendix

Members of the Endobronchial Valve for Persistent Air Leak Group (alphabetically arranged by their institutional affiliations) are as follows: The Alfred Hospital and Monash University, Melbourne, Australia: Gregory I. Snell and Trevor J. Williams; Cedars-Sinai Medical Center, Los Angeles, CA: Robert J. McKenna, Jr.; Cleveland Clinic, Cleveland, OH: Atul C. Mehta, Thomas R. Gildea, and Michael S. Machuzak; Henry Ford Hospital, Detroit, MI: Michael J. Simoff; Medical University of South Carolina, Charleston, SC: Charlie Strange; New York Presbyterian Medical Center, New York, NY: Roger A. Maxfield; Remington Davis Clinical Research Group, Columbus, OH: Edward M. Cordasco, Jr.; Saint Francis Hospital, Tulsa, OK: Mark Boomer; Southern Illinois University School of Medicine, Springfield, IL: Steven R. Hazelrigg; Temple University, Philadelphia, PA: John M. Travaline and Gerard J. Criner; University of California Davis Medical Center, Sacramento, CA: Andrew Chan; University of Iowa, Iowa City, IA: J. Scott Ferguson; University of Kentucky, Lexington, KY: Rolando Berger; University of Rome “La Sapienza,” Rome, Italy: Tiziano De Giacomo and Federico Venuta; and University of Tennessee Medical Center, Knoxville, TN: Thomas E. Gaines.

Cerfolio RJ, Tummala RP, Holman WL, et al. A prospective algorithm for the management of air leaks after pulmonary resection. Ann Thorac Surg. 1998;66:1726-1730. [PubMed] [CrossRef]
 
Abolhoda A, Liu D, Brooks A, et al. Prolonged air leak following radical upper lobectomy: an analysis of incidence and possible risk factors. Chest. 1998;113:1507-1510. [PubMed]
 
West D, Togo A, Kirk AJB. Are bronchoscopic approaches to post-pneumonectomy bronchopleural fistula an effective alternative to repeat thoracotomy? Interact Cardiovasc Thorac Surg. 2007;6:547-550. [PubMed]
 
Sivrikoz CM, Kaya T, Tulay CM, et al. Effective approach for the treatment of bronchopleural fistula: application of endovascular metallic ring-shaped coil in combination with fibrin glue. Ann Thorac Surg. 2007;83:2199-2201. [PubMed]
 
Singh SS, Pyragius MD, Shah PJ, et al. Management of a large bronchopleural fistula using a tracheobronchial stent. Heart Lung Circ. 2007;16:57-59. [PubMed]
 
Fann JI, Berry GJ, Burdon TA. The use of endobronchial valve device to eliminate air leak. Respir Med. 2006;100:1402-1406. [PubMed]
 
Mitchell KM, Boley TM, Hazelrigg SR. Endobronchial valves for treatment of bronchopleural fistula. Ann Thorac Surg. 2006;81:1129-1131. [PubMed]
 
Ferguson JS, Sprenger K, Van Natta T. Closure of a bronchopleural fistula using bronchoscopic placement of an endobronchial valve designed for the treatment of emphysema. Chest. 2006;129:479-481. [PubMed]
 
Feller-Kopman D, Bechara R, Garland R, et al. Use of a removable endobronchial valve for the treatment of bronchopleural fistula. Chest. 2006;130:273-275. [PubMed]
 
De Giacomo T, Venuta F, Diso D, et al. Successful treatment with one-way endobronchial valve of large air-leakage complicating narrow-bore enteral feeding tube malposition. Eur J Cardiothorac Surg. 2006;30:811-812. [PubMed]
 
Snell GI, Holsworth L, Fowler S, et al. Occlusion of a broncho-cutaneous fistula with endobronchial one-way valves. Ann Thorac Surg. 2005;80:1930-1932. [PubMed]
 
Anile M, Venuta F, De Giacomo T, et al. Treatment of persistent air leakage with endobronchial one-way valves. J Thorac Cardiovasc Surg. 2006;132:711-712. [PubMed]
 
Toma TP, Kon OM, Oldfield W, et al. Reduction of persistent air leak with endoscopic valve implants. Thorax. 2007;62:830-833. [PubMed]
 
Cerfolio RJ, Bass CS, Pask AH, et al. Predictors and treatment of persistent air leaks. Ann Thorac Surg. 2002;73:1727-1731. [PubMed]
 
Hazelrigg SR, 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. [PubMed]
 
Robinson LA, Preksto D. Pleural tenting during upper lobectomy decreases chest tube time and total hospitalization days. J Thorac Cardiovasc Surg. 1998;115:319-326. [PubMed]
 
Toker A, Dilege S, Tanju S, et al. Perioperative pneumoperitoneum after lobectomy-bilobectomy operations for lung cancer: a prospective study. Thorac Cardiovasc Surg. 2003;51:93-96. [PubMed]
 
Fabian T, Federico JA, Ponn RB. Fibrin glue in pulmonary resection: a prospective, randomized, blinded study. Ann Thorac Surg. 2003;75:1587-1592. [PubMed]
 
Brunelli A, Monteverde M, Borri A, et al. Predictors of prolonged air leak after pulmonary lobectomy. Ann Thorac Surg. 2004;77:1205-1210. [PubMed]
 

Figures

Figure Jump LinkFigure 1 Transcopic endobronchial valve (Zephyr EBV; Emphasys Medical, Redwood City, CA).Grahic Jump Location
Figure Jump LinkFigure 2 Bronchoscopic view of valve following deployment in right middle lobe bronchus.Grahic Jump Location
Figure Jump LinkFigure 3 A: Representative chest radiograph showing patient with right-loculated basilar pneumothorax and extensive soft-tissue air (lower arrow and upper arrow, respectively). B: One week following an endobronchial valve placement procedure (four valves) [valves encircled; arrows noting absence of abnormalities noted in A], showing lessened pneumothorax and soft-tissue air.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1 Etiology of Air Leak Grouped by Classification (n = 40)

References

Cerfolio RJ, Tummala RP, Holman WL, et al. A prospective algorithm for the management of air leaks after pulmonary resection. Ann Thorac Surg. 1998;66:1726-1730. [PubMed] [CrossRef]
 
Abolhoda A, Liu D, Brooks A, et al. Prolonged air leak following radical upper lobectomy: an analysis of incidence and possible risk factors. Chest. 1998;113:1507-1510. [PubMed]
 
West D, Togo A, Kirk AJB. Are bronchoscopic approaches to post-pneumonectomy bronchopleural fistula an effective alternative to repeat thoracotomy? Interact Cardiovasc Thorac Surg. 2007;6:547-550. [PubMed]
 
Sivrikoz CM, Kaya T, Tulay CM, et al. Effective approach for the treatment of bronchopleural fistula: application of endovascular metallic ring-shaped coil in combination with fibrin glue. Ann Thorac Surg. 2007;83:2199-2201. [PubMed]
 
Singh SS, Pyragius MD, Shah PJ, et al. Management of a large bronchopleural fistula using a tracheobronchial stent. Heart Lung Circ. 2007;16:57-59. [PubMed]
 
Fann JI, Berry GJ, Burdon TA. The use of endobronchial valve device to eliminate air leak. Respir Med. 2006;100:1402-1406. [PubMed]
 
Mitchell KM, Boley TM, Hazelrigg SR. Endobronchial valves for treatment of bronchopleural fistula. Ann Thorac Surg. 2006;81:1129-1131. [PubMed]
 
Ferguson JS, Sprenger K, Van Natta T. Closure of a bronchopleural fistula using bronchoscopic placement of an endobronchial valve designed for the treatment of emphysema. Chest. 2006;129:479-481. [PubMed]
 
Feller-Kopman D, Bechara R, Garland R, et al. Use of a removable endobronchial valve for the treatment of bronchopleural fistula. Chest. 2006;130:273-275. [PubMed]
 
De Giacomo T, Venuta F, Diso D, et al. Successful treatment with one-way endobronchial valve of large air-leakage complicating narrow-bore enteral feeding tube malposition. Eur J Cardiothorac Surg. 2006;30:811-812. [PubMed]
 
Snell GI, Holsworth L, Fowler S, et al. Occlusion of a broncho-cutaneous fistula with endobronchial one-way valves. Ann Thorac Surg. 2005;80:1930-1932. [PubMed]
 
Anile M, Venuta F, De Giacomo T, et al. Treatment of persistent air leakage with endobronchial one-way valves. J Thorac Cardiovasc Surg. 2006;132:711-712. [PubMed]
 
Toma TP, Kon OM, Oldfield W, et al. Reduction of persistent air leak with endoscopic valve implants. Thorax. 2007;62:830-833. [PubMed]
 
Cerfolio RJ, Bass CS, Pask AH, et al. Predictors and treatment of persistent air leaks. Ann Thorac Surg. 2002;73:1727-1731. [PubMed]
 
Hazelrigg SR, 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. [PubMed]
 
Robinson LA, Preksto D. Pleural tenting during upper lobectomy decreases chest tube time and total hospitalization days. J Thorac Cardiovasc Surg. 1998;115:319-326. [PubMed]
 
Toker A, Dilege S, Tanju S, et al. Perioperative pneumoperitoneum after lobectomy-bilobectomy operations for lung cancer: a prospective study. Thorac Cardiovasc Surg. 2003;51:93-96. [PubMed]
 
Fabian T, Federico JA, Ponn RB. Fibrin glue in pulmonary resection: a prospective, randomized, blinded study. Ann Thorac Surg. 2003;75:1587-1592. [PubMed]
 
Brunelli A, Monteverde M, Borri A, et al. Predictors of prolonged air leak after pulmonary lobectomy. Ann Thorac Surg. 2004;77:1205-1210. [PubMed]
 
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