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Persistent air-leak following pulmonary resection
Chest Surg Clin N Am 12 (2002) 529 – 539
Persistent air-leak following pulmonary resection Thomas W. Rice, MD a,*, Ikenna C. Okereke, MD a, Eugene H. Blackstone, MD a,b a
Section of General Thoracic Surgery, Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland OH, 44195, USA b Section of Clinical Research, Department of Biostatistics and Epidemiology, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland OH, 44195, USA
Despite advanced technologies in thoracic surgery, persistent air leaks that occur after pulmonary resection remain a common problem. Management is relatively unchanged and solutions are no closer than they were 10 years ago. ‘‘The successful completion of a pulmonary resection requires closure of the airway. Depending upon the resection, this may include control of the bronchus, bronchioles and/or alveolar spaces. When these closures fail or are inadequate, a bronchopleural fistula or bronchoalveolar-pleural fistula develops and an air leak results. If the major airway is the site of the air leak, this catastrophic and fortunately uncommon complication is called a bronchopleural fistula. Most air leaks, however, are the result of inadequate or failed closure of distal bronchioles or alveolar spaces—bronchoalveolar-pleural fistulas. Less dramatic than an air leak from a proximal airway, an air leak from a distal airway is usually merely an annoyance but occasionally it is the source of considerable morbidity. The prevention of an air leak begins in the operating room and requires meticulous surgical technique, complete expansion of the pulmonary remnant, and, if necessary, reduction of the pleural space to ensure the remaining lung fills it. Postoperatively, maintenance of lung expansion and pleural apposition are fundamental in the avoidance of an air leak. The normal physiologic mechanisms following pulmonary resection also aid in the prevention of an air leak. The diaphragm on the side of the resection rises if not fixed by abdominal or thoracic pathology. Similarly, if not anchored, the mediastinum shifts to the side of the resection. The chest wall, if not involved with restrictive disease, compensated by contraction of the intercostals spaces. The remaining lung hyperinflates. The factors that determine the amount of pulmonary compensa-
* Corresponding author. E-mail address: [email protected] (T.W. Rice). 1052-3359/02/$ – see front matter D 2002, Elsevier Science (USA). All rights reserved. PII: S 1 0 5 2 - 3 3 5 9 ( 0 2 ) 0 0 0 2 2 - 4
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tion include the extent of resection, the volume of the pulmonary remnant, its compliance, and the presences of underlying parenchymal disease. These compensatory mechanisms of space reduction and lung hyperinflation allow approximation of the pulmonary parenchyma to the parietal pleura. The apposition of the raw operative surface of the lung to the parietal pleura assists in the closure of small bronchoalveolar pleural fistulas that have not or could not be surgically closed. The first step of healing, the inflammatory response, closes these distal fistulas if pleural-pulmonary contact is maintained postoperatively. Failure to satisfactorily close the cut surface of the pulmonary parenchyma, inadequate control of the pleural space and lack of the normal compensatory mechanisms foster a prolonged air leak’’ [1].
Definition and significance Persistent or prolonged air leak has been defined as the ‘‘leakage of air, following pulmonary resection, that persists beyond the normal hospital stay’’ [1]. Delay in hospital discharge is pivotal in characterizing this outcome. The time at which an air leak is declared persistent, however, ranges between 4 and 14 days after pulmonary resection [2]. External economic pressures to reduce the length of hospital stay result in many strategies, including discharging patients with air leaks and indwelling chest tubes, which makes hospital discharge an artificial endpoint. When, not where, an air leak stops should be the endpoint that defines persistent air leak. Thus, a new definition of persistent air leak is required. Because the precise qualification of an air leak [3] and an accurate determination of when it stops are difficult, a surrogate—typically the time of the patient’s last chest tube removal—is used. On a graph, the interval between surgery and the removal of the last chest tube after pulmonary resection has a skewed, sharply peaked distribution with a long right tail (Fig. 1).1 Whether to choose the time of chest tube removal or a percentile of patients with indwelling chest tubes to define persistent air leak is an arbitrary decision. The percentiles of days to removal of the last chest tube for 321 consecutive patients who underwent lobectomy at the authors’ institution are listed in Table 1. (The 90th percentile for chest tube removal is 7 days postoperatively.) Rather than selecting a time or percentile, reproducing this distribution for each practice and setting may be prudent. Despite its ambiguous definition, a persistent air leak that occurs after a pulmonary resection is a significant morbidity. Persistent air leaks are reported to complicate 25% of right upper lobectomies and are the sole complication in 81% of these patients [4]. Persistent air leaks and inadequate pain control are cited as the most common causes of delayed hospital discharges after lobectomy [5]. In 1 The authors note with dismay the common use of mean and standard deviation (or standard error) as summary and comparative statistics for strongly right-skewed air-leak data. The authors recommend the use of nonparametric methods, transformation of scale, or direct distributional methods for this type of data. To the extent they were documented and despite their inadequacies all standard errors have been converted to standard deviations in this chapter for uniformity of presentation.
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Fig. 1. Distribution of interval from surgery to removal of last chest tube after lobectomy in 321 patients.
1820 patients who underwent a variety of video-assisted thoracic operations, persistent air leak was the most frequent complication (4.2% of patients) [6]. Planning the prevention of this complication is more important than classifying it and requires a consideration of the factors that affect air leaks.
Preoperative factors Few studies have identified preoperative risk factors for persistent air leaks [1,3,4,6]. Male gender and chronic obstructive pulmonary disease (COPD), reflected by impaired preoperative pulmonary function, were predictive of persistent air leak (defined as chest tube removal after 7 days) after pulmonary resection [1]. Forced vital capacity (FVC) of patients with persistent air leak was significantly higher compared with patients without persistent air leak (3.92 ± 0.91 L Table 1 Duration of persistent air leak * by percentile in 321 consecutive patients Percentile
Days to chest tube removal *
0.3 5 40 60 70 87 90 93 94 95 96 97 98 99 100
1 2 3 4 5 6 7 8 9 10 11 13 21 35 65
* Air leak defined as days from lobectomy to the removal of last chest tube.
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vs. 3.48 ± 0.95 L; P = 0.02); the forced expiratory volume in 1 second (FEV1) was lower (70.6% ± 22% vs. 77.1% ± 19%; P = .03); and the FEV1/FVC ratio was also lower (0.62 ± 0.13 vs. 0.68 ± 0.12; P = .008). Abolhoda et al. [4] studied 100 consecutive patients who underwent right upper lobectomy and mediastinal lymphadenectomy and found that only a FEV1/FVC ratio of less than 50% was predictive of an air leak of more than 7 days. In a prospective study of 101 patients who underwent pulmonary resection, Cerfolio et al. [3] found that only a low FEV1/FVC ratio was predictive of a persistent air leak. Older age and COPD were predictive of persistent air leaks that occurred after a video-assisted wedge resection [6]. Patients with a FEV1 of less than 1 L had more air leaks than those with higher FEV1 levels (21% vs. 2%; P .001). Thus, COPD is the critical factor that identifies patients who are at risk for persistent air leak. Identifying patients with significant COPD and preoperative treatment of reversible airway disease is a principle of pulmonary surgery. This treatment, however, may not reduce persistent air leaks. Treatment of reversible obstruction (bronchitis and asthma) targets large and medium airways, but most persistent air leaks originate from small airways and alveoli. These are the airways that are destroyed by emphysema, and because emphysema is irreversible and not affected by preoperative pulmonary preparation, persistent air leaks are unlikely to be reduced by treatment that is directed at bronchitis and asthma. Thus, in high-risk (ie, COPD) patients, the selective modification of intraoperative and postoperative management may be more likely to decrease persistent air leaks.
Intraoperative prevention Persistent air leaks are caused by either (1) a failure to control the pulmonary fissure during lobectomy or segmentectomy, or (2) a failure to seal the pulmonary parenchyma during wedge resection, or (3) damage to the remaining parenchyma by manipulation, dissection, and retraction. Surprisingly, surgical approach, resection type, fissure status, and use of staples for closing the bronchus or the fissure have not been predictive of a persistent air leak [1,4]. Two intraoperative strategies exist for preventing air leaks: improved closure of the pulmonary parenchyma in the fissure and reduction of the pleural space. Closure of the pulmonary parenchyma in the fissure Wain et al. [7] reported that, when using standard methods of closing the lung parenchyma, more than 70% of patients experienced intraoperative air leaks after lobectomy. The prevention of persistent air leaks focuses on improved control of the pulmonary parenchyma. The routine use of bovine pericardium to buttress the stapled closure of fissures during lobectomy or segmentectomy did not reduce the mean duration of air leak (2.0 ± 3.3 days in the buttressed group vs. 3 ± 2.5 days in the control group; P = .27), mean number of days to chest tube removal (5.9 ± 2.7 days vs. 6.3 ± 3.3 days; P = .62), mean length of hospital stay (8 ± 4.2 days vs. 9 ± 7 days; P = .24), or mean cost ($23,910 ± $9,943 vs. $28,678 ± $5,355;
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P = .18) [8]. In patients at high risk for persistent air leaks, those undergoing volume reduction surgery for emphysema, however, buttressing the staple lines with bovine pericardium resulted in a significant reduction (1) in the median duration of air leak in the buttressed group compared with the control group (0 days [range 0 – 28 days] vs. 4 days [range 0– 27 days], respectively; P < .0001), and (2) in the median chest tube drainage time (5.0 days [range 1– 35 days] vs. 7.5 days [range 2 – 29 days] in controls; P < .045) [9]. In the overall high-risk group, persistent air leaks were not the determining factor in prolonged hospital stays; discharge from the hospital was similar in both groups (9.5 days [range 6 – 44 days] in the buttressed group vs. 12 days [range 5 – 46 days] in the control group; P < .14). Routine buttressing of staple lines is not effective in reducing the prevalence of persistent air leaks; however, in high-risk patients with significant COPD, reinforcing parenchyma staple lines can reduce air leaks. A novel approach to the intraoperative prevention of persistent air leaks is the use of a pulmonary parenchyma sealant. Fleisher et al. [10] randomized 28 patients: 14 patients received fibrin-glue spray during lobectomy; 14 did not. Mean duration of air leak (2.3 ± 3.7 days in the fibrin-glue group vs. 3.3 ± 3.3 days in the control group; P = .94), mean chest tube drainage (6.0 ± 4.1 days vs. 5.9 ± 3.9 days; P = .95), and mean hospital stay (9.8 ± 3.1 days vs. 11.5 ± 3.9 days; P = .21) were similar between groups. In a more heterogeneous group study, patients were randomized to receive fibrin-glue application to both the bronchial stump and to the remaining pulmonary parenchyma (48% of patients had a pneumonectomy) or to serve as control subjects [11]. The prevalence of postoperative air leaks was lower in the treated group compared with the control group (39% vs. 66%, respectively; P < .02); however, the duration of air leak and hospital stay were similar between both groups. The selective use of fibrin glue in patients with intraoperative air leaks after conventional measures failed was not successful in reducing either the duration of chest tube drainage or hospital stay [12]. Fibrin glue is not an effective pulmonary sealant and does not reduce air leaks if used routinely or in high-risk patients. The use of a water-soluble, polyethylene glycol –based gel that is photopolymerized on the lung surface has been reported in three randomized clinical studies [7,13,14]. Macchiarini et al. [13] randomized 26 patients who underwent pulmonary resection: 15 patients received an application of sealant after standard closure of parenchymal sites; 11 patients became control subjects. Although the treated group was more likely to be free of air leaks at the end of operation than was the control group (10 (77%) vs. 1 (9%), respectively; P = .001), the duration of chest tube drainage, length of hospital stay, and cost were similar. In a larger, fourcenter randomized trial of patients who underwent pulmonary resection, 117 patients were randomized to treatment, with 52 becoming control subjects [7]. Although treated patients had fewer air leaks before skin closure than did control subjects (8% vs. 71%, respectively; P .001), the sealant was not durable; 61% of treated patients had an air leak during hospitalization. Mean time from skin closure to the last observed air leak was less in the treatment group than in the control group (30.9 ± 52.0 hours vs. 52.3 ± 84.0 hours, respectively; P = .006).
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Intervals from skin closure to the removal of the last chest tube and from skin closure to discharge were similar. No complications were associated with the use of the sealant. Two percent of treatment patients had a residual space on follow-up chest radiograph; the control group did not (P = .6). Porte et al. [14] studied this sealant during lobectomy in patients with moderate to severe air leaks. In the randomized treatment group (62 patients), mean air leak was less than that in the control group (38 ± 43 mL vs. 60 ± 53 mL, respectively; P = .04). Mean time to last observable air leak was less (34 hours vs. 63 hours; P = .01), and the mean percentage of patients free of air leak at 3 and 4 days was greater (87% vs. 59%; P = .002). The occurrence of incomplete lung expansion after chest tube removal, and the length of hospital stay were similar between groups. Four patients (6%) in the treatment group developed localized empyema and incomplete lung reexpansion that required chest tube insertion to drain the infected sealant. The authors concluded that ‘‘this sealant may be a useful adjuvant to conventional techniques for reducing moderate to severe air leaks after lobectomy, but its use seemed to increase the risk of postoperative empyema’’ [14]. Using this sealant at the authors’ institution doubles the material cost of lobectomy. Routine use of this sealant is not beneficial in the prevention of air leaks and, in high-risk situations, may complicate further the management of persistent air leaks. Pleural space reduction Creating a pleural tent during upper lobectomy permits the apical parietal pleura to fall onto the superior parenchymal surfaces of the lower and middle lobes and has the potential to allow the residual space to become extrapleural (Fig. 2). In 48 consecutive patients who underwent upper lobectomy, 28 had a pleural tent created and 20 did not [15]. In the tented group, mean air leak time was less than that observed in the control group (1.6 ± 1.6 days vs. 3.9 ± 5.4
Fig. 2. Posteroanterior chest radiograph 3 months after left upper lobectomy and pleural tent in a man 62 years of age who has severe COPD (preoperative FEV1 36% of predicted value; FVC 80% of predicted value; FEV1/FVC ratio 0.45). The apical opacity is fluid outside of the pleural tent.
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days, respectively; P = .04). Similarly, mean total chest tube drainage was less (1600 ± 510 mL vs. 2500 ± 1500 mL; P = .009), mean chest tube duration was less (4.0 ± 1.1 days vs. 6.6 ± 4.5; P = .004), and mean total hospital stay was less (6.4 ± 2.1 days vs. 8.6 ± 4.5 days; P = .02). In a prospective randomized study of 40 patients who underwent upper lobectomy, the use of a pleural tent resulted in a shorter duration of chest tube drainage (4.3 ± 0.9 days vs. 7.4 ± 3.6 days in the non-tented group; P < .0001) and in a shorter hospital stay (7.6 ± 0.4 days vs. 9.4 ± 2.7 days; P = .02) [16]. Although three patients (15%) in each group had apical spaces, only those without a pleural tent required additional postoperative chest tube placement. Brunelli et al. [17] randomized 50 patients to receive a pleural tent during upper lobectomy or to become control subjects. In the tented group, mean days of postoperative air leak was less than that in the control group (1.2 ± 2.0 vs. 5.8 ± 7.9, respectively; P = .01). Similarly, mean days to chest tube removal was less (5.4 ± 1.7 vs. 10.4 ± 7.5; P = .01) and mean hospital stay was less (6.9 ± 2.0 days vs. 10.8 ± 6.0 days; P = .01). Although these authors suggested that a pleural tent should be created routinely at the time of upper lobectomy, the inadequacy of the comparison methods and the potential for complications, both early (eg, hemorrhage, empyema) and late (eg, restrictive pulmonary disease, difficult reoperations), should limit its routine use. Pleural tenting should be reserved for high-risk patients with severe COPD. During lower lobectomy or bilobectomy (right middle and lower lobes), the creation of a pneumoperitoneum by transdiaphragmatic injection of air can be used to reduce air leaks (Fig. 3). Of 16 patients who underwent bilobectomy, 8 were randomized to receive a 1200-mL pneumoperitoneum [18]. On postoperative day 1, one patient in the pneumoperitoneum group and four in the control group had a basilar pneumothorax (P < .0001). By postoperative day 3, no air leaks occurred in the pneumoperitoneum group, and four control patients had sustained air leaks (P < .001). Three control patients were discharged home with a Heimlich valve and a persistent air leak. Median hospital stay was significantly shorter in patients who received a pneumoperitoneum compared with those who did not (4 days [range 3 –6 days] vs. 6 days [range 4 – 8 days], respectively; P < .001). Pneumoperitoneum is a useful adjunct in patients with severe COPD and in those with significant intraoperative air leaks after undergoing lower lobectomy or bilobectomy.
Postoperative management Most patients with air leaks experience a speedy resolution with aggressive chest tube management. Although 89% of patients who are treated with standard intraoperative lobectomy techniques develop air leaks [7], they quickly resolve, with only 20% to 25% of patients reported to have an air leak on the second postoperative day [3,19]. The presence of a pneumothorax on the first postoperative chest radiograph (P = .05) and the insertion of a chest tube in the
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Fig. 3. (A) A postoperative pneumoperitoneum was administered to a man 68 years of age after left upper lobectomy. The patient had COPD (preoperative FEV1 47% of predicted value; FVC 91% of predicted value; FEV1/FVC ratio 0.52). At the time, there was a persistent air leak. There is subcutaneous emphysema but no pneumothorax. (B) Posteroanterior chest radiograph after permissive chest tube removal (a small expiratory air leak is present). There is a residual pneumothorax (arrows) and significant subcutaneous emphysema. (C) Posteroanterior chest radiograph at 2-month follow-up. The left lower lobe fills the pleural space and there is no pneumonia or empyema in the left chest. The patient has developed a cavitating right pneumonia.
postoperative period (P < .001) are the only postoperative predictors of a persistent air leak [1]. Chest tube management The first step in the treatment of an air leak is to ensure that the drainage system is functioning. Although the use of chest tube suction has not been substantiated by clinical studies, it is used early in the postoperative period to facilitate the complete reexpansion of the remaining lung so that it fills the pleural
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space. Suction should not exceed 20 cm H2O. Ceasing suction early and placing chest tubes to an underwater seal is more effective than continued suction to stop air leaks [19]. After suction cessation, a pneumothorax most likely will complicate large expiratory leaks, and patients may require the reinstitution of suction at lower levels ( 10 cm H2O). Persistent air leaks that are not controlled with chest tubes inserted operatively may require a repositioning of these tubes or the insertion of additional ones. The slight withdrawal of the chest tube (1 –2 cm) may stop air leaks by removing the tube from the site of the air leak and allowing apposition of the parenchyma to the parietal pleura. At this point, a persistent large air leak requires bronchoscopy to rule out disruption of the bronchial closure and a bronchopleural fistula. In patients who have ‘‘small’’ air leaks on forced expiration and no air leaks with normal breathing, a trial of ‘‘provocative clamping’’ and ‘‘permissive chest tube removal’’ (ie, a small expiratory air leak and a small pneumothorax are tolerated) may be considered [20]. In six patients who underwent this treatment, complete expansion of the lung was seen during 5 months of follow-up and no sequelae were reported [21]. Studies have reported that 4.2% of patients discharged with indwelling chest tubes and a Heimlich valve required readmission, with a 0.5% incidence of pleural complications; pneumonia was also reported [22,23]. Chest tubes were removed a mean of 7.9 ± 3.5 days (range 2– 24 days) after discharge [22]. Pleurodesis Although comforting for the surgeon, proving that postoperative pleurodesis is beneficial for the patient is difficult. There have been incidental case reports of retrograde or thoracoscopic instillation of a variety of sclerosing agents, including fibrin glue, autologous blood, and tetracycline [24 –31]. Because patients with persistent air leak are treated with pleurodesis and because pleurodesis is a marker for persistent air leak, assessment of its efficacy is difficult. Reoperation Excluding surgery for disrupted bronchial stump closure and bronchopleural fistula, reoperation for persistent air leak is uncommon. In patients who have undergone pulmonary resection, 0.05% required reoperation for persistent air leak [1]. This may be accomplished by thoracoscopy [26,29].
Summary Air leaks are an unavoidable complication of pulmonary resection. The definition of a persistent air leak is arbitrary and may even be irrelevant in solving the problem. Persistent air leaks are more common in patients with severe COPD, and preoperative interventions are ineffective in reducing their prevalence. Meticulous surgical technique and care in handling and resection of the pulmonary
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parenchyma are essential in preventing persistent air leaks. Buttressing parenchymal staple lines and creating a pleural tent or pneumoperitoneum should be reserved for patients at risk for persistent air leaks. The use of currently available sealants is ineffective for the treatment of this complication. To stop persistent air leaks, early cessation of suction and placing chest tubes to an underwater seal is more effective than continuous suction. The management of persistent air leaks may require provocative chest tube clamping and permissive chest tube removal or patient discharge from the hospital with a chest tube and a Heimlich valve.
References [1] Rice TW, Kirby TJ. Prolonged air leak. Chest Surg Clin N Am 1992;2:803 – 11. [2] Adebonojo SA. How prolonged is ‘‘prolonged air leak’’? Ann Thorac Surg 1995;59:549 – 50. [3] 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 – 31. [4] Abolhoda A, Liu D, Brooks A, et al. Prolonged air leak following radical right upper lobectomy: an analysis of incidence and possible risk factors. Chest 1998;113:1507 – 10. [5] Wright CD, Wain JC, Grillo HC, et al. Pulmonary lobectomy patient care pathway: a model to control cost and maintain quality. Ann Thorac Surg 1997;64:299 – 302. [6] Hazelrigg SR, Nunchuck SK, LoCicero III J, et al. Video-assisted thoracic surgery study group data. Ann Thorac Surg 1993;56:1039 – 43. [7] Wain JC, Kaiser LR, Johnstone DW, et al. Trial of a novel synthetic sealant in preventing air leaks after lung resection. Ann Thorac Surg 2001;71:1623 – 9. [8] Miller Jr JI, Landreneau RJ, Wright CE, et al. A comparative study of buttressed versus nonbuttressed staple line in pulmonary resections. Ann Thorac Surg 2001;71:319 – 23. [9] Stammberger U, 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 – 5. [10] Fleisher AG, Evans KG, Nelems B, et al. Effect of routine fibrin glue use on the duration of air leaks after lobectomy. Ann Thorac Surg 1990;49:133 – 4. [11] Mouritzen C, Dromer M, Keinecke HO. The effect of fibrin glueing to seal bronchial and alveolar leakages after pulmonary resections and decortications. Eur J Cardiothorac Surg 1993;7:75 – 80. [12] Wong K, Goldstraw P. Effect of fibrin glue in the reduction of postthoracotomy alveolar air leak. Ann Thor Surg 1997;64:979 – 81. [13] Macchiarini P, Wain J, Almy S, et al. Experimental and clinical evaluation of a new synthetic, absorbable sealant to reduce air leaks in thoracic operations. J Thorac Cardiovasc Surg 1999; 117:751 – 8. [14] 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 – 22. [15] Robinson LA, Preksto D. Pleural tenting during upper lobectomy decreases chest tube time and total hospitalization days. J Thorac Cardiovasc Surg 1998;115:319 – 27. [16] Okur E, Kir A, Halezeroglu S, et al. A. Pleural tenting following upper lobectomies or bilobectomies of the lung to prevent residual space and prolonged air leak. Eur J Cardiothorac Surg 2001;20:1012 – 5. [17] Brunelli A, Al Refai M, Muti M, et al. Pleural tent after upper lobectomy: a prospective randomized study. Ann Thorac Surg 2000;69:1722 – 4. [18] Cerfolio RJ, Holman WL, Katholi CR. Pneumoperitoneum after concomitant resection of the right middle and lower lobes (bilobectomy). Ann Thorac Surg 2000;70:942 – 7. [19] Cerfolio RJ, Bass C, Katholi C. Prospective randomized trial compares suction versus water seal for air leaks. Ann Thorac Surg 2001;71:1613 – 7.
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[20] Kirschner PA. Provocative clamping and removal of chest tubes despite persistent air leaks. Ann Thorac Surg 1992;53:740 – 1. [21] Kato R, Kobayashi T, Watanabe M, et al. Can the chest tube draining the pleural cavity with persistent air leakage be removed? Thorac Cardiovasc Surg 1992;40:292 – 6. [22] McKenna Jr. RJ, Fischel RJ, Brenner M, et al. Use of the Heimlich valve to shorten hospital stay after lung reduction surgery for emphysema. Ann Thorac Surg 1996;61:1115 – 7. [23] Ponn RB, Silverman HJ, Federico JA. Outpatient chest tube management. Ann Thorac Surg 1997;64:1437 – 40. [24] Kinoshita T, Miyoshi S, Katoh M, et al. Intrapleural administration of a large amount of diluted fibrin glue for intractable pneumothorax. Chest 2000;117:790 – 5. [25] Matar AF, Hill JG, Duncan W, et al. Use of biological glue to control pulmonary air leaks. Thorax 1990;45:670 – 4. [26] O’Neill PJ, Flanagan HL, Mauney MC, et al. Intrathoracic fibrin sealant application using computed tomography fluoroscopy. Ann Thorac Surg 2000;70:301 – 2. [27] Rivas de Andres JJ, Blanco S, de la Torre M. Postsurgical pleurodesis with autologous blood in patients with persistent air leak. Ann Thorac Surg 2000;70:270 – 2. [28] Samuels LE, Shaw PM, Blaum LC. Percutaneous technique for management of persistent airspace with prolonged air leak using fibrin glue. Chest 1996;109:1653 – 5. [29] Suter M, Bettschart V, Vandoni RE, et al. Thoracoscopic pleurodesis for prolonged (or intractable) air leak after lung resection. Eur J Cardiothorac Surg 1997;12:160 – 1. [30] Thistlewaite PA, Luketich JD, Ferson PF, et al. Ablation of persistent air leaks after thoracic procedures with fibrin sealant. Ann Thorac Surg 1999;67:575 – 7. [31] Yokomise H, Satoh K, Ohno N, et al. Autoblood plus OK432 pleurodesis with open drainage for persistent air leak after lobectomy. Ann Thorac Surg 1998;65:563 – 5.
Persistent air-leak following pulmonary resection Thomas W. Rice, MD a,*, Ikenna C. Okereke, MD a, Eugene H. Blackstone, MD a,b a
Section of General Thoracic Surgery, Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland OH, 44195, USA b Section of Clinical Research, Department of Biostatistics and Epidemiology, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland OH, 44195, USA
Despite advanced technologies in thoracic surgery, persistent air leaks that occur after pulmonary resection remain a common problem. Management is relatively unchanged and solutions are no closer than they were 10 years ago. ‘‘The successful completion of a pulmonary resection requires closure of the airway. Depending upon the resection, this may include control of the bronchus, bronchioles and/or alveolar spaces. When these closures fail or are inadequate, a bronchopleural fistula or bronchoalveolar-pleural fistula develops and an air leak results. If the major airway is the site of the air leak, this catastrophic and fortunately uncommon complication is called a bronchopleural fistula. Most air leaks, however, are the result of inadequate or failed closure of distal bronchioles or alveolar spaces—bronchoalveolar-pleural fistulas. Less dramatic than an air leak from a proximal airway, an air leak from a distal airway is usually merely an annoyance but occasionally it is the source of considerable morbidity. The prevention of an air leak begins in the operating room and requires meticulous surgical technique, complete expansion of the pulmonary remnant, and, if necessary, reduction of the pleural space to ensure the remaining lung fills it. Postoperatively, maintenance of lung expansion and pleural apposition are fundamental in the avoidance of an air leak. The normal physiologic mechanisms following pulmonary resection also aid in the prevention of an air leak. The diaphragm on the side of the resection rises if not fixed by abdominal or thoracic pathology. Similarly, if not anchored, the mediastinum shifts to the side of the resection. The chest wall, if not involved with restrictive disease, compensated by contraction of the intercostals spaces. The remaining lung hyperinflates. The factors that determine the amount of pulmonary compensa-
* Corresponding author. E-mail address: [email protected] (T.W. Rice). 1052-3359/02/$ – see front matter D 2002, Elsevier Science (USA). All rights reserved. PII: S 1 0 5 2 - 3 3 5 9 ( 0 2 ) 0 0 0 2 2 - 4
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tion include the extent of resection, the volume of the pulmonary remnant, its compliance, and the presences of underlying parenchymal disease. These compensatory mechanisms of space reduction and lung hyperinflation allow approximation of the pulmonary parenchyma to the parietal pleura. The apposition of the raw operative surface of the lung to the parietal pleura assists in the closure of small bronchoalveolar pleural fistulas that have not or could not be surgically closed. The first step of healing, the inflammatory response, closes these distal fistulas if pleural-pulmonary contact is maintained postoperatively. Failure to satisfactorily close the cut surface of the pulmonary parenchyma, inadequate control of the pleural space and lack of the normal compensatory mechanisms foster a prolonged air leak’’ [1].
Definition and significance Persistent or prolonged air leak has been defined as the ‘‘leakage of air, following pulmonary resection, that persists beyond the normal hospital stay’’ [1]. Delay in hospital discharge is pivotal in characterizing this outcome. The time at which an air leak is declared persistent, however, ranges between 4 and 14 days after pulmonary resection [2]. External economic pressures to reduce the length of hospital stay result in many strategies, including discharging patients with air leaks and indwelling chest tubes, which makes hospital discharge an artificial endpoint. When, not where, an air leak stops should be the endpoint that defines persistent air leak. Thus, a new definition of persistent air leak is required. Because the precise qualification of an air leak [3] and an accurate determination of when it stops are difficult, a surrogate—typically the time of the patient’s last chest tube removal—is used. On a graph, the interval between surgery and the removal of the last chest tube after pulmonary resection has a skewed, sharply peaked distribution with a long right tail (Fig. 1).1 Whether to choose the time of chest tube removal or a percentile of patients with indwelling chest tubes to define persistent air leak is an arbitrary decision. The percentiles of days to removal of the last chest tube for 321 consecutive patients who underwent lobectomy at the authors’ institution are listed in Table 1. (The 90th percentile for chest tube removal is 7 days postoperatively.) Rather than selecting a time or percentile, reproducing this distribution for each practice and setting may be prudent. Despite its ambiguous definition, a persistent air leak that occurs after a pulmonary resection is a significant morbidity. Persistent air leaks are reported to complicate 25% of right upper lobectomies and are the sole complication in 81% of these patients [4]. Persistent air leaks and inadequate pain control are cited as the most common causes of delayed hospital discharges after lobectomy [5]. In 1 The authors note with dismay the common use of mean and standard deviation (or standard error) as summary and comparative statistics for strongly right-skewed air-leak data. The authors recommend the use of nonparametric methods, transformation of scale, or direct distributional methods for this type of data. To the extent they were documented and despite their inadequacies all standard errors have been converted to standard deviations in this chapter for uniformity of presentation.
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Fig. 1. Distribution of interval from surgery to removal of last chest tube after lobectomy in 321 patients.
1820 patients who underwent a variety of video-assisted thoracic operations, persistent air leak was the most frequent complication (4.2% of patients) [6]. Planning the prevention of this complication is more important than classifying it and requires a consideration of the factors that affect air leaks.
Preoperative factors Few studies have identified preoperative risk factors for persistent air leaks [1,3,4,6]. Male gender and chronic obstructive pulmonary disease (COPD), reflected by impaired preoperative pulmonary function, were predictive of persistent air leak (defined as chest tube removal after 7 days) after pulmonary resection [1]. Forced vital capacity (FVC) of patients with persistent air leak was significantly higher compared with patients without persistent air leak (3.92 ± 0.91 L Table 1 Duration of persistent air leak * by percentile in 321 consecutive patients Percentile
Days to chest tube removal *
0.3 5 40 60 70 87 90 93 94 95 96 97 98 99 100
1 2 3 4 5 6 7 8 9 10 11 13 21 35 65
* Air leak defined as days from lobectomy to the removal of last chest tube.
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vs. 3.48 ± 0.95 L; P = 0.02); the forced expiratory volume in 1 second (FEV1) was lower (70.6% ± 22% vs. 77.1% ± 19%; P = .03); and the FEV1/FVC ratio was also lower (0.62 ± 0.13 vs. 0.68 ± 0.12; P = .008). Abolhoda et al. [4] studied 100 consecutive patients who underwent right upper lobectomy and mediastinal lymphadenectomy and found that only a FEV1/FVC ratio of less than 50% was predictive of an air leak of more than 7 days. In a prospective study of 101 patients who underwent pulmonary resection, Cerfolio et al. [3] found that only a low FEV1/FVC ratio was predictive of a persistent air leak. Older age and COPD were predictive of persistent air leaks that occurred after a video-assisted wedge resection [6]. Patients with a FEV1 of less than 1 L had more air leaks than those with higher FEV1 levels (21% vs. 2%; P .001). Thus, COPD is the critical factor that identifies patients who are at risk for persistent air leak. Identifying patients with significant COPD and preoperative treatment of reversible airway disease is a principle of pulmonary surgery. This treatment, however, may not reduce persistent air leaks. Treatment of reversible obstruction (bronchitis and asthma) targets large and medium airways, but most persistent air leaks originate from small airways and alveoli. These are the airways that are destroyed by emphysema, and because emphysema is irreversible and not affected by preoperative pulmonary preparation, persistent air leaks are unlikely to be reduced by treatment that is directed at bronchitis and asthma. Thus, in high-risk (ie, COPD) patients, the selective modification of intraoperative and postoperative management may be more likely to decrease persistent air leaks.
Intraoperative prevention Persistent air leaks are caused by either (1) a failure to control the pulmonary fissure during lobectomy or segmentectomy, or (2) a failure to seal the pulmonary parenchyma during wedge resection, or (3) damage to the remaining parenchyma by manipulation, dissection, and retraction. Surprisingly, surgical approach, resection type, fissure status, and use of staples for closing the bronchus or the fissure have not been predictive of a persistent air leak [1,4]. Two intraoperative strategies exist for preventing air leaks: improved closure of the pulmonary parenchyma in the fissure and reduction of the pleural space. Closure of the pulmonary parenchyma in the fissure Wain et al. [7] reported that, when using standard methods of closing the lung parenchyma, more than 70% of patients experienced intraoperative air leaks after lobectomy. The prevention of persistent air leaks focuses on improved control of the pulmonary parenchyma. The routine use of bovine pericardium to buttress the stapled closure of fissures during lobectomy or segmentectomy did not reduce the mean duration of air leak (2.0 ± 3.3 days in the buttressed group vs. 3 ± 2.5 days in the control group; P = .27), mean number of days to chest tube removal (5.9 ± 2.7 days vs. 6.3 ± 3.3 days; P = .62), mean length of hospital stay (8 ± 4.2 days vs. 9 ± 7 days; P = .24), or mean cost ($23,910 ± $9,943 vs. $28,678 ± $5,355;
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P = .18) [8]. In patients at high risk for persistent air leaks, those undergoing volume reduction surgery for emphysema, however, buttressing the staple lines with bovine pericardium resulted in a significant reduction (1) in the median duration of air leak in the buttressed group compared with the control group (0 days [range 0 – 28 days] vs. 4 days [range 0– 27 days], respectively; P < .0001), and (2) in the median chest tube drainage time (5.0 days [range 1– 35 days] vs. 7.5 days [range 2 – 29 days] in controls; P < .045) [9]. In the overall high-risk group, persistent air leaks were not the determining factor in prolonged hospital stays; discharge from the hospital was similar in both groups (9.5 days [range 6 – 44 days] in the buttressed group vs. 12 days [range 5 – 46 days] in the control group; P < .14). Routine buttressing of staple lines is not effective in reducing the prevalence of persistent air leaks; however, in high-risk patients with significant COPD, reinforcing parenchyma staple lines can reduce air leaks. A novel approach to the intraoperative prevention of persistent air leaks is the use of a pulmonary parenchyma sealant. Fleisher et al. [10] randomized 28 patients: 14 patients received fibrin-glue spray during lobectomy; 14 did not. Mean duration of air leak (2.3 ± 3.7 days in the fibrin-glue group vs. 3.3 ± 3.3 days in the control group; P = .94), mean chest tube drainage (6.0 ± 4.1 days vs. 5.9 ± 3.9 days; P = .95), and mean hospital stay (9.8 ± 3.1 days vs. 11.5 ± 3.9 days; P = .21) were similar between groups. In a more heterogeneous group study, patients were randomized to receive fibrin-glue application to both the bronchial stump and to the remaining pulmonary parenchyma (48% of patients had a pneumonectomy) or to serve as control subjects [11]. The prevalence of postoperative air leaks was lower in the treated group compared with the control group (39% vs. 66%, respectively; P < .02); however, the duration of air leak and hospital stay were similar between both groups. The selective use of fibrin glue in patients with intraoperative air leaks after conventional measures failed was not successful in reducing either the duration of chest tube drainage or hospital stay [12]. Fibrin glue is not an effective pulmonary sealant and does not reduce air leaks if used routinely or in high-risk patients. The use of a water-soluble, polyethylene glycol –based gel that is photopolymerized on the lung surface has been reported in three randomized clinical studies [7,13,14]. Macchiarini et al. [13] randomized 26 patients who underwent pulmonary resection: 15 patients received an application of sealant after standard closure of parenchymal sites; 11 patients became control subjects. Although the treated group was more likely to be free of air leaks at the end of operation than was the control group (10 (77%) vs. 1 (9%), respectively; P = .001), the duration of chest tube drainage, length of hospital stay, and cost were similar. In a larger, fourcenter randomized trial of patients who underwent pulmonary resection, 117 patients were randomized to treatment, with 52 becoming control subjects [7]. Although treated patients had fewer air leaks before skin closure than did control subjects (8% vs. 71%, respectively; P .001), the sealant was not durable; 61% of treated patients had an air leak during hospitalization. Mean time from skin closure to the last observed air leak was less in the treatment group than in the control group (30.9 ± 52.0 hours vs. 52.3 ± 84.0 hours, respectively; P = .006).
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Intervals from skin closure to the removal of the last chest tube and from skin closure to discharge were similar. No complications were associated with the use of the sealant. Two percent of treatment patients had a residual space on follow-up chest radiograph; the control group did not (P = .6). Porte et al. [14] studied this sealant during lobectomy in patients with moderate to severe air leaks. In the randomized treatment group (62 patients), mean air leak was less than that in the control group (38 ± 43 mL vs. 60 ± 53 mL, respectively; P = .04). Mean time to last observable air leak was less (34 hours vs. 63 hours; P = .01), and the mean percentage of patients free of air leak at 3 and 4 days was greater (87% vs. 59%; P = .002). The occurrence of incomplete lung expansion after chest tube removal, and the length of hospital stay were similar between groups. Four patients (6%) in the treatment group developed localized empyema and incomplete lung reexpansion that required chest tube insertion to drain the infected sealant. The authors concluded that ‘‘this sealant may be a useful adjuvant to conventional techniques for reducing moderate to severe air leaks after lobectomy, but its use seemed to increase the risk of postoperative empyema’’ [14]. Using this sealant at the authors’ institution doubles the material cost of lobectomy. Routine use of this sealant is not beneficial in the prevention of air leaks and, in high-risk situations, may complicate further the management of persistent air leaks. Pleural space reduction Creating a pleural tent during upper lobectomy permits the apical parietal pleura to fall onto the superior parenchymal surfaces of the lower and middle lobes and has the potential to allow the residual space to become extrapleural (Fig. 2). In 48 consecutive patients who underwent upper lobectomy, 28 had a pleural tent created and 20 did not [15]. In the tented group, mean air leak time was less than that observed in the control group (1.6 ± 1.6 days vs. 3.9 ± 5.4
Fig. 2. Posteroanterior chest radiograph 3 months after left upper lobectomy and pleural tent in a man 62 years of age who has severe COPD (preoperative FEV1 36% of predicted value; FVC 80% of predicted value; FEV1/FVC ratio 0.45). The apical opacity is fluid outside of the pleural tent.
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days, respectively; P = .04). Similarly, mean total chest tube drainage was less (1600 ± 510 mL vs. 2500 ± 1500 mL; P = .009), mean chest tube duration was less (4.0 ± 1.1 days vs. 6.6 ± 4.5; P = .004), and mean total hospital stay was less (6.4 ± 2.1 days vs. 8.6 ± 4.5 days; P = .02). In a prospective randomized study of 40 patients who underwent upper lobectomy, the use of a pleural tent resulted in a shorter duration of chest tube drainage (4.3 ± 0.9 days vs. 7.4 ± 3.6 days in the non-tented group; P < .0001) and in a shorter hospital stay (7.6 ± 0.4 days vs. 9.4 ± 2.7 days; P = .02) [16]. Although three patients (15%) in each group had apical spaces, only those without a pleural tent required additional postoperative chest tube placement. Brunelli et al. [17] randomized 50 patients to receive a pleural tent during upper lobectomy or to become control subjects. In the tented group, mean days of postoperative air leak was less than that in the control group (1.2 ± 2.0 vs. 5.8 ± 7.9, respectively; P = .01). Similarly, mean days to chest tube removal was less (5.4 ± 1.7 vs. 10.4 ± 7.5; P = .01) and mean hospital stay was less (6.9 ± 2.0 days vs. 10.8 ± 6.0 days; P = .01). Although these authors suggested that a pleural tent should be created routinely at the time of upper lobectomy, the inadequacy of the comparison methods and the potential for complications, both early (eg, hemorrhage, empyema) and late (eg, restrictive pulmonary disease, difficult reoperations), should limit its routine use. Pleural tenting should be reserved for high-risk patients with severe COPD. During lower lobectomy or bilobectomy (right middle and lower lobes), the creation of a pneumoperitoneum by transdiaphragmatic injection of air can be used to reduce air leaks (Fig. 3). Of 16 patients who underwent bilobectomy, 8 were randomized to receive a 1200-mL pneumoperitoneum [18]. On postoperative day 1, one patient in the pneumoperitoneum group and four in the control group had a basilar pneumothorax (P < .0001). By postoperative day 3, no air leaks occurred in the pneumoperitoneum group, and four control patients had sustained air leaks (P < .001). Three control patients were discharged home with a Heimlich valve and a persistent air leak. Median hospital stay was significantly shorter in patients who received a pneumoperitoneum compared with those who did not (4 days [range 3 –6 days] vs. 6 days [range 4 – 8 days], respectively; P < .001). Pneumoperitoneum is a useful adjunct in patients with severe COPD and in those with significant intraoperative air leaks after undergoing lower lobectomy or bilobectomy.
Postoperative management Most patients with air leaks experience a speedy resolution with aggressive chest tube management. Although 89% of patients who are treated with standard intraoperative lobectomy techniques develop air leaks [7], they quickly resolve, with only 20% to 25% of patients reported to have an air leak on the second postoperative day [3,19]. The presence of a pneumothorax on the first postoperative chest radiograph (P = .05) and the insertion of a chest tube in the
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Fig. 3. (A) A postoperative pneumoperitoneum was administered to a man 68 years of age after left upper lobectomy. The patient had COPD (preoperative FEV1 47% of predicted value; FVC 91% of predicted value; FEV1/FVC ratio 0.52). At the time, there was a persistent air leak. There is subcutaneous emphysema but no pneumothorax. (B) Posteroanterior chest radiograph after permissive chest tube removal (a small expiratory air leak is present). There is a residual pneumothorax (arrows) and significant subcutaneous emphysema. (C) Posteroanterior chest radiograph at 2-month follow-up. The left lower lobe fills the pleural space and there is no pneumonia or empyema in the left chest. The patient has developed a cavitating right pneumonia.
postoperative period (P < .001) are the only postoperative predictors of a persistent air leak [1]. Chest tube management The first step in the treatment of an air leak is to ensure that the drainage system is functioning. Although the use of chest tube suction has not been substantiated by clinical studies, it is used early in the postoperative period to facilitate the complete reexpansion of the remaining lung so that it fills the pleural
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space. Suction should not exceed 20 cm H2O. Ceasing suction early and placing chest tubes to an underwater seal is more effective than continued suction to stop air leaks [19]. After suction cessation, a pneumothorax most likely will complicate large expiratory leaks, and patients may require the reinstitution of suction at lower levels ( 10 cm H2O). Persistent air leaks that are not controlled with chest tubes inserted operatively may require a repositioning of these tubes or the insertion of additional ones. The slight withdrawal of the chest tube (1 –2 cm) may stop air leaks by removing the tube from the site of the air leak and allowing apposition of the parenchyma to the parietal pleura. At this point, a persistent large air leak requires bronchoscopy to rule out disruption of the bronchial closure and a bronchopleural fistula. In patients who have ‘‘small’’ air leaks on forced expiration and no air leaks with normal breathing, a trial of ‘‘provocative clamping’’ and ‘‘permissive chest tube removal’’ (ie, a small expiratory air leak and a small pneumothorax are tolerated) may be considered [20]. In six patients who underwent this treatment, complete expansion of the lung was seen during 5 months of follow-up and no sequelae were reported [21]. Studies have reported that 4.2% of patients discharged with indwelling chest tubes and a Heimlich valve required readmission, with a 0.5% incidence of pleural complications; pneumonia was also reported [22,23]. Chest tubes were removed a mean of 7.9 ± 3.5 days (range 2– 24 days) after discharge [22]. Pleurodesis Although comforting for the surgeon, proving that postoperative pleurodesis is beneficial for the patient is difficult. There have been incidental case reports of retrograde or thoracoscopic instillation of a variety of sclerosing agents, including fibrin glue, autologous blood, and tetracycline [24 –31]. Because patients with persistent air leak are treated with pleurodesis and because pleurodesis is a marker for persistent air leak, assessment of its efficacy is difficult. Reoperation Excluding surgery for disrupted bronchial stump closure and bronchopleural fistula, reoperation for persistent air leak is uncommon. In patients who have undergone pulmonary resection, 0.05% required reoperation for persistent air leak [1]. This may be accomplished by thoracoscopy [26,29].
Summary Air leaks are an unavoidable complication of pulmonary resection. The definition of a persistent air leak is arbitrary and may even be irrelevant in solving the problem. Persistent air leaks are more common in patients with severe COPD, and preoperative interventions are ineffective in reducing their prevalence. Meticulous surgical technique and care in handling and resection of the pulmonary
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parenchyma are essential in preventing persistent air leaks. Buttressing parenchymal staple lines and creating a pleural tent or pneumoperitoneum should be reserved for patients at risk for persistent air leaks. The use of currently available sealants is ineffective for the treatment of this complication. To stop persistent air leaks, early cessation of suction and placing chest tubes to an underwater seal is more effective than continuous suction. The management of persistent air leaks may require provocative chest tube clamping and permissive chest tube removal or patient discharge from the hospital with a chest tube and a Heimlich valve.
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