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Ann Thorac Surg 2001;72:243-248
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Empyema and bronchopleural fistula after pneumonectomy: factors affecting incidence

Address reprint requests to Dr Deschamps, Division of General Thoracic Surgery, Mayo Clinic and Mayo Foundation, 200 First St, SW, Rochester, MN 55905
e-mail: deschamps.claude{at}mayo.edu

Presented at the Forty-seventh Annual Meeting of the Southern Thoracic Surgical Association, Marco Island, FL, Nov 9–11, 2000.

	Abstract

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Background. Factors affecting the incidence of empyema and bronchopleural fistula (BPF) after pneumonectomy were analyzed.

Methods. All patients who underwent pneumonectomy at the Mayo Clinic in Rochester, Minnesota, from January 1985 to September 1998 were reviewed. There were 713 patients (514 males and 199 females). Ages ranged from 12 to 86 years (median 64 years). Indication for resection was primary malignancy in 607 patients (85.1%), metastatic disease in 32 (4.5%), and benign disease in 74 (10.4%). One hundred fifteen patients (16.1%) underwent completion pneumonectomy. Factors affecting the incidence of postoperative empyema and BPF were analyzed using univariate and multivariate analysis.

Results. Empyema was documented in 53 patients (7.5%; 95% confidence interval [CI], 5.7% to 9.7%) and a BPF in 32 (4.5%; 95% CI, 3.1% to 6.3%). Univariate analysis demonstrated that the development of empyema was adversely affected by benign disease (p = 0.0001), lower preoperative forced expiratory volume in 1 second (FEV₁; p < 0.01) and diffusion capacity of lung to carbon monoxide (DLCO; p = 0.0001), lower preoperative serum hemoglobin (p = 0.05), right pneumonectomy (p = 0.0109), bronchial stump reinforcement (p = 0.007), completion pneumonectomy (p < 0.01), timing of chest tube removal (p = 0.01), and the amount of blood transfusions (p < 0.01). Similarly, the development of BPF was significantly associated with benign disease (p = 0.03), lower preoperative FEV₁ (p = 0.03) and DLCO (p = 0.01), right pneumonectomy (p < 0.0001), bronchial stump reinforcement (p = 0.03), timing of chest tube removal (p = 0.004), increased intravenous fluid in the first 12 hours (p = 0.04), and blood transfusions (p = 0.04). Bronchial stump closure with staples had a protective effect against BPF compared with suture closure (p = 0.009). No risk factors were identified as being jointly significant in multivariate analysis.

Conclusions. Multiple perioperative factors were associated with an increased incidence of empyema and BPF after pneumonectomy. Prophylactic reinforcement of the bronchial stump with viable tissue may be indicated in those patients suspected at higher risk for either empyema or BPF.

	Introduction

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The first successful pneumonectomy for benign disease was performed in 1931 by Rudolph Nissen and the first successful pneumonectomy for cancer was performed in 1933 by Evarts Graham [1]. Since then, empyema and bronchopleural fistula (BPF) after pneumonectomy have continued to represent a therapeutic challenge for the thoracic surgeon. Conflicting information exists regarding predisposing factors for these two conditions, and the purpose of this review was to analyze a single institution’s experience with empyema and BPF after pneumonectomy.

	Material and methods

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Between January 1, 1985, and September 30, 1998, all patients who underwent elective pneumonectomy at the Mayo Clinic in Rochester, Minnesota, were reviewed. Patients operated for malignant pleural mesothelioma were excluded. The records of these patients were analyzed for age, gender, preoperative conditions, body mass index, weight loss, preoperative serum hemoglobin, pulmonary function and gas exchange tests, indications for operation, postsurgical stage, neoadjuvant treatment, extent of operation, technique of bronchial stump closure and reinforcement, chest tube management, volume of crystalloid infusion, number of blood transfusions, and incidence of empyema and BPF. Empyema was defined as the presence of purulent material in the postpneumonectomy pleural space. Bronchopleural fistula was defined as any communication between the bronchial air space and the pleural cavity and was confirmed by bronchoscopy, thoracotomy, or both.

The primary end points of analysis were empyema and BPF. The effects of various risk factors on these end points were evaluated with both univariate and multivariate analysis. The effects of categorical variable risk factors were evaluated using ² tests [2] and Fisher’s exact tests [3]. Risk factors represented by continuous variables were assessed using two-sample t tests [4] when the data were approximately normal and by rank sum tests [5] when the data were found to be insufficiently Gaussian. Multiple logistic regression [6] was used during multivariate analysis to simultaneously evaluate the effects of risk factors. Specifically, stepwise selection was used to identify significant predictors. All statistical tests were two-sided with the threshold of significance set at p less than 0.05. All analyses were conducted using SAS (SAS Institute Inc, Cary, NC).

	Clinical findings

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There were 713 patients (514 men and 199 women). Median age was 64 years and ranged from 12 to 86 years. Indication for pneumonectomy was primary lung cancer in 607 patients (85.1%), benign disease in 74 (10.4%), and metastatic cancer in 32 (4.5%). Primary lung cancers were classified as stage IA in 51 patients, IB in 72, IIA in 135, IIB in 6, IIIA in 302, and stage IIIB in 41. Squamous cell carcinoma occurred in 354 patients, adenocarcinoma in 169, large cell carcinoma in 44, bronchoalveolar cell carcinoma in 16, carcinoid tumor in 11, and other in 13. Benign diseases included destructive lung disease in 25 patients, BPF in 20, bronchiectasis in 13, aspergillosis in 12, and lobar torsion in 4. The original site of metastatic cancer was a soft tissue sarcoma in 13 patients, osteogenic sarcoma in 5, melanoma in 3, lymphoma in 3, breast carcinoma in 2, and other in 6.

Associated conditions were present in 360 patients (50.5%) and included chronic obstructive pulmonary disease (Table 1) in 213 (30.0%), coronary artery disease in 92 (12.9%), cardiac arrhythmia in 66 (9.3%), diabetes mellitus in 58 (8.1%), alcoholism in 42 (5.9%), corticosteroid use in 33 (4.6%), asthma in 32 (4.5%), valvular heart disease in 25 (3.5%), hematologic disease in 15 (2.1%), congestive heart failure in 12 (1.7%), chronic renal failure in 8 (1.1%), and other in 95 (13.3%). No patient had isolated empyema at the time of pneumonectomy. Median preoperative serum hemoglobin was 13.3 g/dL (range 7.4 to 18.9 g/dL).

One hundred nineteen patients (16.7%) had a prior lung resection; 109 had one previous resection, 6 patients had 2, and 4 patients had 3. Previous pulmonary resections included lobectomy in 75 patients, segmentectomy or wedge in 34, and bilobectomy in 10. One hundred four patients (14.6%) had preoperative chemotherapy or radiation therapy: 55 had radiation alone, 25 had chemotherapy alone, and 24 had a combination of both. Mediastinoscopy was performed in 285 patients (40.0%).

Pneumonectomy was on the left in 362 patients (50.8%) and on the right in 351 (49.2%). Completion pneumonectomy was performed in 115 patients (16.1%). An extended resection was performed in 246 patients (34.5%) and in addition to pneumonectomy included en bloc resection of parietal pleura in 87 (12.2%), en bloc chest wall in 74 (10.4%), left atrium in 20 (2.8%), carina in 20 (2.8%), diaphragm in 13 (1.8%), superior vena cava in 12 (1.7%), esophageal muscle in 8 (1.1%), thoracic aortic adventitia in 7 (7.3%), and right atrium, vertebral fascia, first thoracic nerve, spine and main pulmonary artery in 1 patient each (0.2%). Intrapericardial dissection was performed in 242 patients (33.9%), and extracorporeal circulation was used in 2 (0.3%). A total of 622 patients (87.2%) underwent mediastinal lymphadenectomy.

The bronchus was closed with a stapling device in 656 patients (92.0%) and hand-sutured in 57 (8.0%). The bronchial stump was reinforced with viable tissue in 175 patients (24.5%) and included muscle in 111, parietal pleura in 46, and pericardium in 18. The serratus anterior muscle was used in 93 patients, latissimus dorsi in 14, and a combination of both in 4. Tube thoracostomy to balance the mediastinum was done in 654 patients (91.7%) and the chest tube was removed in the operating room in 517, during the first postoperative day in 125, the second postoperative day in 8 and the third postoperative day in 4.

Overall, 124 patients had at least one blood transfusion (median 3 U, range 1 to 39 U); 108 of these patients (15.1%) had at least one intraoperative transfusion (median 2 U, range, 1 to 37 U) and 46 (6.5%) had at least one transfusion within the first 24 postoperative hours (median 2 U, range 1 to 18 U). The median volume of crystalloid infused in the first 12 hours, including the intraoperative period, was 23.8 mL/kg (range 0.96 to 201.1 mL/kg).

	Results

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Five patients (0.07%) died within 24 hours after pneumonectomy and were excluded from further analysis. Empyema occurred in 53 of the surviving 708 patients (7.5%; 95% confidence interval [CI], 5.7% to 9.7%) and BPF in 32 (4.5%; 95% CI, 3.1% to 6.3%). The median time interval between pneumonectomy and diagnosis of empyema was 24 days (range 1 day to 5.8 years) and the median interval between pneumonectomy and diagnosis of BPF was 20.5 days (range 1 to 344 days). The incidence of empyema for primary lung cancer, metastatic disease, and benign disease was 5.8%, 3.1%, and 24%, respectively, and the incidence of BPF was 4.1%, 0%, and 9.9%, respectively.

Univariate analysis demonstrated that benign disease (p = 0.0001), lower preoperative forced expiratory volume in 1 second (FEV₁; p < 0.01) and diffusion capacity of lung to carbon monoxide (DLCO; p = 0.0001), lower preoperative serum hemoglobin (p = 0.05), right pneumonectomy (p = 0.0109), bronchial stump reinforcement (p = 0.008), completion pneumonectomy (p < 0.01), timing of chest tube removal (p = 0.01), and intraoperative and overall amount of blood transfused (p < 0.01), adversely affected incidence of empyema (Tables 2 and 3). Similarly, the development of BPF was significantly associated with benign disease (p = 0.03), lower preoperative FEV₁ (p = 0.03) and DLCO (p = 0.01), right pneumonectomy (p < 0.0001), bronchial stump reinforcement (p = 0.03), timing of chest tube removal (p = 0.0043), increased intravenous fluid in the first 12 hours (p = 0.04), and overall amount of blood transfused (p = 0.04). Bronchial stump closure with staples had a protective effect against BPF compared with suture closure (p = 0.009) (Tables 4 and 5). No risk factors were identified as being jointly significant in multivariate analysis.

	Comment

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Empyema after pneumonectomy can be life threatening and occurs in 2% to 16% of patients (Table 6). This complication is often associated with a BPF, leading to a further increase in morbidity and mortality [7, 8]. The incidence of BPF after pneumonectomy is greater than that after lobectomy or segmentectomy [9]. Both local and systemic factors have been implicated in the development of BPF [9, 10]. Local factors include carcinoma at the bronchial margin, a long bronchial stump, disrupted bronchial blood supply, technique of stump closure, presence of empyema, extended resection, and preoperative radiation [11–22]. Systemic factors include the patient’s nutritional status, diabetes, presence of sepsis, preoperative chemotherapy, and the underlying lung disease that requires pneumonectomy to manage [13, 22–25]. Extended resection, mechanical ventilation, right versus left pneumonectomy, and surgeon level of experience have also been identified as possible contributing factors [11, 26].

Like others, we have demonstrated that benign disease [21, 24, 25, 27], completion pneumonectomy [27, 28], right pneumonectomy [29, 30], and suture closure of the bronchial stump [15] are risk factors for the development of postoperative empyema and BPF. Although only a minority of our patients underwent hand-sutured bronchial stump closure, there was no specific indication for either stump closure technique other than surgeon preference. We have also demonstrated that the timing of chest tube removal correlated with an increased incidence of empyema and BPF. One possible explanation is that the prolonged duration of chest thoracostomy increased the potential of retrograde contamination.

It is unclear why excess perioperative crystalloid and blood transfusions had an adverse effect on these two complications. Perhaps these findings reflect the technical challenges of surgical dissection when significant adhesions from previous lung operations or radiation therapy are present [12, 27, 28].

Similarly, the adverse effects of decreased FEV₁ and DLCO could reflect the extent of lung destruction and secondary pulmonary infection. Others have reported comparable findings [29]. Although none of our patients had isolated empyema before pneumonectomy, it is likely that our 20 patients with BPF before pneumonectomy had significant pleural space contamination. This may suggest that whereas prophylactic antibiotic administration has been shown to be of benefit in other types of general thoracic surgical procedures [31], those patients with significant lung destruction might benefit from more type-specific perioperative antibiotic regimens.

Meticulous attention to details is key to prevention of complications at the time of pneumonectomy. Knowledge of the bronchial blood supply is critical as overzealous dissection can devascularize the stump. Excessive length should also be avoided to prevent pooling of contaminated secretions and subsequent stump breakdown. Finally, ample evidence exists demonstrating that the risk of empyema and BPF is increased after radiation therapy [12] or when preexisting empyema is present [21].

Our preference is to reinforce the bronchial stump with viable tissue, primarily with extrathoracic skeletal muscle if the hilum has been previously irradiated or resection is performed in the presence of empyema [7, 32–37]. Although the present study did not demonstrate a reduced incidence of BPF with tissue reinforcement, we believe that this unexpected finding is secondary to patient selection, because our practice has been to reinforce those patients most likely to develop either of these complications. Lastly, if chest thoracostomy is performed at the time of pneumonectomy, we remove the chest tube immediately while the patient is still in the operating room [36].

Postpneumonectomy empyema probably occurs more commonly than is generally appreciated, possibly because the condition can occur at any time after pneumonectomy, including decades later [38, 39]. Consequently, a criticism of our study is that because it is retrospective and nonrandomized, the possibility exists that not all patients have been captured, thereby underestimating the true incidence of empyema.

In conclusion, our analysis suggests that multiple perioperative factors are associated with an increased incidence of empyema and BPF after pneumonectomy. The bronchus should be handled with meticulous care, and we favor prophylactic reinforcement of the bronchial stump with viable tissue in those patients who have undergone previous irradiation or for whom resection is performed in the presence of empyema.

	Discussion

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DR PETER M. SIDELL (Fort Myers, FL): You imply that reinforcing the stump increased the risk but here you are recommending that we reinforce it. Can you clarify that point?

DR DESCHAMPS: This was not unexpected because we do reinforce the stump in every patient at risk. Those patients with necrotic lung or infected pleural cavity or irradiated bronchus are the ones who are likely to benefit from prophylactic muscle transposition.

We had an overall incidence of BPF of 4.5% in this group of patients, which is a little below the average of the last 10 years’ series in the literature. If we did not put a muscle on the bronchus, we think probably this average would be much higher. This study is not prospective or randomized, so there is some limitation to this study, but because of the nature of the practice and those patients are targeted to have a higher incidence of BPF, we think that our rate would be higher without the muscle.

DR CAROLYN E. REED (Charleston, SC): As usual from the Mayo Clinic a beautiful presentation and beautiful slides. Doctor Deschamps, do you think the reason you found that there was no association with induction therapy, particularly chemoradiation, was the fact that you did not have many patients who underwent induction treatment, and would you cover the stump for those patients who undergo induction therapy?

DR DESCHAMPS: Yes. The first half of that period we did not use chemoradiation preoperatively very often. And, yes, we would favor using the muscle in all those patients. We would like to think that our rate, as I said, would be higher without the muscle, and for that reason we favor using muscle transposition on the bronchus.

DR JAMES C. JONES (Clarks Summit, PA): I see that you listed corticosteroids as a possible risk factor for bronchial fistula. Did your data demonstrate or suggest a causal relationship between steroid use and bronchopleural fistula?

DR DESCHAMPS: Yes, we did, and we did not find a significant effect by the steroids.

	References

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