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Eur J Cardiothorac Surg 2003;23:833-839
© 2003 Elsevier Science NL

Long-term outcomes and risk factor analysis after pneumonectomy for active and sequela forms of pulmonary tuberculosis

Department of Thoracic and Cardiovascular Surgery (Clinical Research Institute), Seoul National University Hospital, Cancer Research Institute, Seoul National University College of Medicine, 28 Yongon-Dong, Chongro-Ku, Seoul 110-744, South Korea

Received 21 September 2002; received in revised form 11 January 2003; accepted 14 January 2003.

^* Corresponding author. Tel.: +82-2-760-3161; fax: +82-2-765-7117
e-mail: ytkim{at}plaza.snu.ac.kr

	Abstract

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion References

 
Objective: The prevalence of pulmonary tuberculosis remains high in several areas of the world, and pneumonectomy is often necessary to treat the disease. We retrospectively analyzed the morbidities, mortalities, and long-term outcomes after pneumonectomy for the treatment of active tuberculosis or its sequelae. Materials and methods: Between 1981 and 2001, 94 patients underwent either pneumonectomy or pleuropneumonectomy for the treatment of tuberculosis. The patients included 44 males and 50 females and the mean age was 40 (16–68) years. The pathology included destroyed lung in 80, main bronchus stenosis in ten, and both lesions in four. Surgical procedures performed were pneumonectomy in 47, pleuropneumonectomy in 43, and completion pneumonectomy in four. Results: One patient died postoperatively due to empyema. Twenty-three complications occurred in 20 patients: empyema in 15 (including seven bronchopleural fistulae), wound infections in five, and other complications in three. Univariate analysis revealed the presence of empyema, pleuropneumonectomy, prolonged operation time, old age, and intraoperative contamination as risk factors of postpneumonectomy empyema; it also showed that low preoperative FEV₁ and postoperative persistent positive sputum AFB were risk factors of bronchopleural fistula. In multivariate analysis, old age and low preoperative FEV₁ were risk factors of empyema while low preoperative FEV₁, positive sputum acid-fast bacilli, and the presence of aspergilloma were risk factors of bronchopleural fistula. There were 12 late deaths. Actuarial 5- and 10-year survival rates were 94±3% and 87±4%, respectively. Conclusion: Pneumonectomy could be performed with acceptable mortality and morbidity, and could achieve satisfactory long-term survival for the treatment of tuberculosis. In patients with risk factors, special care is recommended to prevent postoperative empyema or bronchopleural fistula.

Key Words: Pulmonary tuberculosis • Pneumonectomy • Empyema • Bronchopleural fistula • Survival rate

	1. Introduction

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion References

 
The development of effective anti-tuberculous bacillus medications has improved the cure rate of pulmonary tuberculosis. However, the prevalence of pulmonary tuberculosis remains high in several areas of the world, and pneumonectomy is often necessary to treat either the active disease or its sequelae such as destroyed lung, tuberculous empyema, and bronchial stenosis [1]. Performing pneumonectomy on patients afflicted with chronic infection remains a high-risk procedure and many surgeons recommend strict measures for deciding on the operation [2–4]. However, pneumonectomy or pleuropneumonectomy often remains as the only curative treatment modality for the treatment of tuberculosis when complicated with massive or recurrent hemoptysis, recurrent infection, multi-drug resistant (MDR) tuberculosis, or destroyed lung with bronchopleural fistula. We retrospectively analyzed the mortalities, morbidities, and long-term outcomes after pneumonectomy for the treatment of tuberculosis.

	2. Materials and methods

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion References

 
Between 1981 and 2001, 94 patients underwent either pneumonectomy or pleuropneumonectomy for the treatment of tuberculosis at Seoul National University Hospital. Among the 44 males and 50 females, the mean age was 40 years (range, 16–68 years). Patients complained of mild to moderate degree of exertional dyspnea, chest discomfort, recurrent cough, sputum, and hemoptysis. Fifty-nine patients (62.8%) were taking anti-tuberculous medication at the time of operation. Twenty-nine patients were taking first-line drugs such as isoniazid, rifampin, ethambutol, pyrazinamide, streptomycin, and kanamycin. Thirty were using the second-line medications such as cycloserine ethionamide, para-amino-salicylic acid, ofloxacin, etc. The median duration from the initial diagnosis of tuberculosis to surgery was 8 years (range, 0.2–40 years). Twenty patients had contralateral lung lesions at the time of surgery, among which seven patients had clinically active tuberculosis lesion including two patients with cavity. When a contralateral tuberculous lesion was present, pneumonectomy was performed when the contralateral lesion could potentially be cured by chemotherapy and when the pulmonary reserve was adequate.

Among the 24 patients with empyema, six were managed with a chest tube placement and two were controlled with open window drainage preoperatively. No specific surgical treatment was performed in the remaining 16 patients. Twelve patients had other medical diseases, such as diabetes mellitus, hypertension, myasthenia gravis, and gout. The tuberculosis was confined to the pulmonary system, except for a patient who had suffered from spinal tuberculosis as well as pulmonary tuberculosis.

2.1. Preoperative assessment
Preoperative evaluations included chest roentgenogram, computed tomography, sputum smear and culture test for acid-fast bacilli (AFB), fiberoptic bronchoscopy, pulmonary function tests, and a quantitative pulmonary perfusion scan for patients whose pulmonary function was reduced. The indications for surgery included destroyed lung in 80 (85.1%), main bronchus stenosis in ten (10.6%), and both lesions in four (4.3%). Preoperative empyema was complicated in 24 patients who had a destroyed lung (28.6%). There was no empyema among the patients whose pathology was bronchial stricture. When empyema was complicated preoperatively, the patients were treated with systemic antibiotics and/or chest tube placement. The patients were operated on when active systemic bacterial infection was controlled. Pulmonary aspergilloma was complicated in four patients (4.3%). Sputum AFB was documented preoperatively in 29 patients (30.1%), and MDR strains were detected in 26 (27.7%). In eight patients (8.5%), sputum AFB was detected despite operation. Preoperative mean FEV₁ was 1.51±0.04 (range, 0.73–2.98) L/s and mean FVC was 2.03±0.05 (range, 1.14–3.50) L.

2.2. Operative technique
All patients, except for a case where we performed video-assistant pneumonectomy, underwent posterolateral thoracotomy. Since 1990, we have been using the double-lumen endotracheal tube routinely to prevent the risk of spillage of infected materials into the contralateral bronchus. Surgical procedures performed were pneumonectomy in 47, pleuropneumonectomy in 43, and completion pneumonectomy in four. Thirty-two patients underwent right side operation, and 62 underwent left side resection. A bronchial stump was either stapled or over-sawn with Vicryl^® suture and was reinforced with a pericardial fat pad or parietal pleura, or not reinforced based on the surgeon's decision. Pleuropneumonectomy was performed when the pleural space was completely obliterated due to previous inflammation or when preoperative empyema was complicated. Despite careful dissection, some extent of intraoperative contamination took place in 26 patients during operation and copious saline or antiseptic solution irrigation was performed at that time. Postoperatively fluid restriction and prophylactic antibiotics therapy was initiated. Patients were not routinely put on the ventilator postoperatively. However, when the operation time was long or when the patient's vital signs were unstable, overnight ventilator supports were performed in seven patients. Once the patient's bowel sound returned, anti-tuberculous chemotherapy was resumed as instructed by pulmonary physicians. Mean operation time was 325±14 (range, 115–760) minutes and the mean hospital stay was 27±6 (range, 6–378) days.

2.3. Follow-up
Follow-up data was obtained from the outpatient clinic chart reviews or by telephone calls to patients or families. The follow-up process ended on June 2002, and the mean follow-up duration was 114±7 months (range, 9 months–21 years) (Fig. 1 ).

View larger version (112K): [in this window] [in a new window]   Fig. 1. A 24-year old female suffered from multi-drug-resistant tuberculosis with a destroyed left lung. Preoperative chest roentgenography (a) and chest computed tomography (b) show destruction and collapse of the left lung as well as thin-walled cavities in the right upper and lower lobes. The patient underwent left pleuropneumonectomy. Chest roentgenography of postoperative day (c) and recent follow-up (d) show left pleuropneumonectomy status with decreased right upper lobe cavity.

	3. Results

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion References

 
There was one operative death (1.1%), where the patient had undergone right pneumonectomy for a tuberculous destroyed lung. The postoperative course was complicated with the development of bronchopleural fistula and empyema; as a result, the patient died of aspiration pneumonia of the remaining left lung. A total of 23 complications developed in 20 patients (21.3%); postpneumonectomy empyema in 15 (15.9%), wound infections in five (5.3%), postoperative bleeding in two (2.1%), and postpneumonectomy syndrome in one patient (1.1%) (Table 1). Bronchopleural fistula was documented in seven patients (7.5%).

The variables used for the analysis of risk factors for developing complications include: gender, old age (>50 years), the presence of parenchymal destruction of the affected lung, the presence of preoperative empyema, pleuropneumonectomy (vs. pneumonectomy), a longer operation time (>300 min), low preoperative FEV₁, right side procedure (vs. left side), the presence of diabetes mellitus, MDR tuberculosis, the presence of preoperative hemoptysis, the presence of aspergilloma, a positive preoperative/postoperative sputum AFB smear, preoperative/postoperative anti-tuberculous medication, presence of tuberculous lesion on the contralateral side, and intraoperative contamination of the pleural cavity.

Univariate analysis showed that old age (P=0.029), the presence of preoperative empyema (P=0.007), pleuropneumonectomy (P=0.019), a longer operation time (>300 min; P=0.016), and intraoperative contamination of the pleural cavity (P=0.002) were risk factors for the development of postpneumonectomy empyema. Multivariate analysis, however, revealed that old age (P=0.007) and low preoperative FEV₁ (<1.6 L/min) (P=0.016) were significant risk factors of empyema (Table 2).

View larger version (14K): [in this window] [in a new window]   Fig. 2. Long-term survival curve of patients after pneumonectomy for tuberculous sequelae. (a) Overall survival; (b) survival according to the operation time; and (c) survival according to the presence of multi-drug-resistant (MDR) tuberculosis.

	4. Discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion References

 
Pneumonectomy for a benign inflammatory lung disease has been considered a high-risk procedure and several authors have concluded that the procedure should be avoided whenever possible [2]. However, there are situations when pneumonectomy or pleuropneumonectomy remains the only curative treatment modality for the treatment of tuberculosis. Those include a destroyed lung, significant hemoptysis, main bronchial stenosis, MDR strain, or significant symptoms such as a productive cough. Twenty-three patients (24.5%) complained various amount of recurrent hemoptysis in our cases. Other symptoms included chest discomfort, productive cough, and dyspnea.

Several authors report 4–8.5% operative mortality of pneumonectomy for inflammatory lung disease [2,5]. On the other hand, others report relatively low (0–2.4%) operative mortality [6–9]. We experienced 1.1% early mortality, which was lower than the mortality of pneumonectomy for the lung cancer during the same period in our institution.

Although there is a discrepancy regarding operative mortality, almost every author agrees that morbidity remains high and the major problem is postpneumonectomy empyema. Fifteen patients (15.9%) developed empyema after pneumonectomy in our series. The reported incidence of empyema ranges from 5 to 32% [2,6–8]. Several studies have tried to find risk factors for developing empyema after pneumonectomy for a benign inflammatory lung disease. The risk factors reported to be significant for this cumbersome complication were the presence of preoperative empyema, aspergilloma, violation of parenchymal cavity during pneumonectomy, excessive blood loss, right pneumonectomy, and re-exploration for hemorrhage [2,5,9]. Our study revealed that old age, the presence of preoperative empyema, pleuropneumonectomy, a longer operation time, and intraoperative contamination of the pleural cavity were risk factors for the development of postpneumonectomy empyema in univariate analysis. Multivariate analysis, however, revealed that old age and low preoperative FEV₁ were significant. The presence of aspergilloma was not a significant factor in univariate study and had borderline significance (P=0.094) in multivariate analysis.

The presence of preoperative empyema has been advocated to be an important risk factor for developing postoperative empyema [9]. Shiraishi et al. recommended pleuropneumonectomy for the treatment of empyema with a destroyed lung and reported rates of 8.5% operative mortality and 9.6% postoperative empyema with the procedure. Among the 24 patients who had preoperative empyema in our series, we performed 22 pleuropneumonectomies and two conventional pneumonectomies. There was no operative mortality in those patients. Postoperative empyema developed in eight out of 24 patients (33%) who had empyema preoperatively, whereas it developed in only seven out of 70 (10%) who did not have preoperative empyema. We performed 43 pleuropneumonectomies and in 22 cases, empyema was present preoperatively. In the remaining 21 cases, pleuropneumonectomy was employed due to the presence of dense adhesion in the pleural space. Other alternative procedures, such as pneumonectomy through empyema [10], decortication [11], and thoracomyoplasty [12], have been advocated. Pneumonectomy through empyema was complicated, however, with frequent occurrence of postoperative empyema [10]. Although decortication or thoracomyoplasty may be adequate to obliterate the pleural space, the remaining destroyed lungs usually keep the respiratory symptoms. Indeed, there are many cases where the lungs never expand in spite of meticulous decortication. Therefore, we do not think it is an appropriate approach to attempt decortication for patients whose diseased lungs are completely destroyed and whose pleural space is infected, especially if the bronchopleural fistula is present. In this situation, we would elect to perform pleuropneumonectomy because attempting decortication would definitely result in major pleural space contamination and patients would end up with postoperative empyema. Myocutaneous flap might be used to fill the empyema space. However, if there are active ongoing infections in the remaining destroyed lung, the lungs will not work as a gas exchange organ or as a natural prosthesis. Instead, it will work as a source of future infection of the contralateral lungs or of the pleural space.

We experienced pleuropneumonectomy and prolonged operative times as risk factors for developing postoperative empyema. Intraoperative contamination of the pleural cavity, which can occur when the preoperative empyema is ruptured during the procedure [5] or when the perforation of the destroyed lung parenchyme occurs during the dissection [2], was a risk factor for postoperative empyema. We elected to perform pleuropneumonectomy when empyema or extensive pleural symphysis was present in order to decrease such a situation as other authors had recommended [13].

It was an interesting observation that preoperative lower FEV₁ was a risk factor predicting postoperative empyema. There was no reasonable explanation for this finding. However, considering low FEV₁ was a risk factor of bronchopleural fistula in our study, it might be related to frequent development of bronchopleural fistula. It has been well documented that the left side is predominant in inflammatory lung diseases. Sixty-two cases were left side, compared to 32 on the right side, in our study. Several papers reported that right pneumonectomy is more apt to develop empyema postoperatively; however, we were not able to find any significant correlation with these reports.

The presence of postoperative sputum AFB and the presence of aspergilloma were risk factors for the development of postoperative bronchopleural fistula, along with low preoperative FEV₁. Despite perioperative anti-tuberculous medication, eight patients remained positive for sputum AFB and two of them developed fistula. The presence of aspergilloma was also a risk factor. Complex aspergilloma is defined when aspergilloma is present in the destroyed lung [14]. All four patients with aspergilloma in our series were considered as complex form. Daly et al. [15] reported as high as 34% operative mortality and 78% postoperative complications after the operation of complex aspergilloma. Pneumonectomy was performed in seven out of 32 (22%) complex aspergilloma in their study. In our experience between 1981 and 1999, we operated on 73 complex aspergilloma and pneumonectomy was performed in three patients (4%) (unpublished data). In our study, the presence of aspergilloma was a risk factor of postoperative bronchopleural fistula in multivariate analysis. Preoperative FEV₁ seemed to be a significant risk factor of bronchopleural fistula and none of the patients with [15] a good preoperative FEV₁ higher than 1.6 liters/min developed bronchopleural fistula in our study.

There are only a few papers showing long-term survival after pneumonectomy for tuberculosis. Ashour and associates reported no long-term death during 12–124 months of follow-up periods after 24 pneumonectomies for tuberculosis [6]. For high-risk patients with preoperative empyema, Shiraishi et al. reported a 5-year survival rate of 83% during 0–18.8 year follow-up periods [5]. Our study showed 5- and 10-year survival rates were 94±3%, 88±4%, respectively. Compared to the high complication rate, the long-term survival rate seems to be good. Old age, MDR-tuberculosis, and prolonged operative time were risk factors of poor long-term survival. Among these three factors, multivariate analysis revealed that patients with MDR-tuberculosis and patients whose operations took longer were at high risk. The longer operation time will represent the presence of severe diseases, such as lung parenchymal destruction, pleural symphysis, as well as the presence of preoperative empyema. It is reasonable that MDR-tuberculosis patients will have poor long-term survival. More rigorous perioperative and long-term anti-tuberculous medication is mandatory for those patients.

In conclusion, we have demonstrated in this paper that pneumonectomy could be performed with acceptable mortality and morbidity, and could achieve satisfactory long-term survival for the treatment of tuberculosis. However, in patients with risk factors, special care is recommended to prevent postoperative empyema or bronchopleural fistula.

	Footnotes

 
Presented at the 16th Annual Meeting of the European Association for Cardio-thoracic Surgery, Monte Carlo, Monaco, September 22–25, 2002.

	References

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion References

 

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