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Ann Thorac Surg 2004;78:399-403
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Pneumonectomy for nontuberculous mycobacterial infections

Yuji Shiraishi, MDa*, Yutsuki Nakajima, MDa, Naoya Katsuragi, MDa, Makoto Kurai, MDa, Nobumasa Takahashi, MDa

a Section of Chest Surgery, Fukujuji Hospital, Tokyo, Japan

Accepted for publication February 23, 2004.

* Address reprint requests to Dr Shiraishi, Section of Chest Surgery, Fukujuji Hospital, 3-1-24 Matsuyama, Kiyose, Tokyo, 204-8522 Japan
e-mail: yujishi{at}mvb.biglobe.ne.jp

Presented at the Poster Session of the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
BACKGROUND: Pneumonectomy is considered in the treatment of nontuberculous mycobacterial infections when an entire lung is affected. However, this procedure carries high morbidity. We report on our experience in using pneumonectomy for treating patients with nontuberculous mycobacterial infections.

METHODS: Between 1983 and 2002, 53 patients infected with nontuberculous mycobacteria underwent 55 pulmonary resections. Of these patients, 11 (3 men, 8 women) underwent pneumonectomy (5 right, 6 left). Median age was 57 years (range, 43 to 69 years). Mycobacterium avium complex disease occurred in 10 patients and Mycobacterium abscessus disease in 1. Indications for pneumonectomy included multiple cavities in one lung and destruction of an entire lung. The bronchial stump was covered with a latissimus dorsi muscle flap in 7 patients and with an intercostal pedicle flap in 2.

RESULTS: Operating time ranged from 142 to 477 minutes (median, 360 minutes). The median intraoperative blood loss was 555 mL (range, 130 to 1,245 mL). There was no operative mortality. Bronchopleural fistula occurred in 3 patients. All fistulas were observed after right pneumonectomy, and were treated by reclosure of the bronchus. Empyema occurred in 1 patient, who was treated with irrigation. All patients achieved sputum-negative status after surgery. Two late deaths occurred. One patient died of respiratory failure 11 months after surgery. A second patient, the only patient who had recurrent disease, died of respiratory failure 4 years postoperatively.

CONCLUSIONS: Despite bronchial stump protection, right pneumonectomy carries a risk for bronchopleural fistula. Nonetheless, pneumonectomy can result in high cure rates in patients with nontuberculous mycobacterial infections.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
Pulmonary disease caused by nontuberculous mycobacteria has been recognized as a growing health problem [1]. Despite recent advances in the medical treatment of nontuberculous mycobacterial infections, certain organisms, including Mycobacterium avium complex and Mycobacterium abscessus, remain difficult to treat with antimicrobial treatment [2, 3]. For these organisms, the removal of heavy bacterial burdens by resecting the grossly diseased areas in the lung that contain large numbers of bacilli may enhance the efficacy of medical treatment. Resectional surgery combined with chemotherapy has, therefore, been playing an important role in the treatment of these nontuberculous mycobacterial infections [4–9]. Patients whose disease is localized to one lung and who have sufficient cardiopulmonary reserve to tolerate resection are considered for pulmonary resection. An ideal situation exists when the disease is localized to one lobe of a lung so that a lobectomy can be performed. Pneumonectomy is favored over less aggressive procedures when an entire lung is affected. However, pneumonectomy for treatment of nontuberculous mycobacterial infections has been reported to carry high morbidity, including a high incidence of bronchopleural fistula [5]. Although our team is experienced in performing surgery for mycobacterial disease and chronic empyema [9, 10], the pneumonectomy procedure has proved to be challenging. Results of pneumonectomy procedures performed on a limited number of nontuberculous mycobacterial patients have been reported [4–6]. This report reviews our experience in using pneumonectomy to treat patients with nontuberculous mycobacterial infections.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
Between 1983 and 2002, 53 patients infected with nontuberculous mycobacteria underwent 55 pulmonary resections at Fukujuji Hospital in Tokyo. The resections included pneumonectomy in 11 patients, lobectomy in 43 patients, and segmentectomy in 1 patient. Two patients had staged bilateral lobectomies. The 11 patients undergoing a pneumonectomy were enrolled in this study. Preoperative studies included chest roentgenogram, computed tomographic scan of the chest, pulmonary function tests, arterial blood gas analysis, and a quantitative perfusion scan. Smears and cultures of sputum were examined on admission. Bronchoscopy was used in some cases to rule out contralateral disease or coexisting malignancies.

Operative mortality included all deaths clearly related to the operation, regardless of the postoperative interval. Because bronchopleural fistula and empyema might have the potential to occur as late as 1 month after surgery, all bronchopleural fistulas or empyemas occurring during the surgical follow-up period were considered postoperative complications.

Patients were 8 women (73%) and 3 men (27%). Age at the time of surgery ranged from 43 to 69 years (median, 57 years). Mycobacterium avium complex disease occurred in 10 patients, and Mycobacterium abscessus disease occurred in 1 patient. Body mass index ranged from 15.5 to 22.2 kg/m2 (median, 16.6 kg/m2; Table 1). None of the patients were immunocompromised. All patients met the diagnostic criteria recommended by the American Thoracic Society for disease caused by nontuberculous mycobacteria [11]. At our institution, multidrug regimens containing clarithromycin (600 to 800 mg daily) were initiated as preoperative chemotherapy for 9 patients who underwent surgery after 1992 [9]. Two patients, who underwent a pneumonectomy before that date, received antituberculous drugs, such as ethambutol, isoniazid, kanamycin, and rifampin. For 1 patient, chemotherapy was discontinued before surgery because of anorexia. Duration of illness before surgery ranged from 13 to 109 months (median, 57 months).


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  		Table 1. Patient Characteristics

 
The indications for pulmonary resection were (1) medical treatment failure in 10 patients and (2) superimposed infection with Pseudomonas aeruginosa in 1 patient. None of the patients were operated on for treatment of massive hemoptysis. The indications for pneumonectomy were (1) presence of multiple cavitary lesions in one lung (Fig 1) in 6 patients and (2) destruction of an entire lung in 5 patients. Four patients had scattered nodular lesions on the opposite side. All 6 patients with multiple cavities and 3 of the 5 patients with a destroyed lung presented with positive sputum at the time of surgery. Perfusion scans revealed that the lungs that were removed had received from 0.7% to 33.4% (median, 18.6%) of the total lung perfusion (Table 1).



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  		Fig 1. Chest computed tomographic scan of patient 10 showing cavitary lesions in the left upper lobe (A) as well as in the left lower lobe (B).

 
The surgery was performed under general anesthesia with the use of a double-lumen endobronchial tube. A posterolateral thoracotomy was made, and the sixth or seventh rib was removed. Pneumonectomy was performed either intrapleurally or extrapleurally, depending on the degree of pleural adhesions. When doing extrapleural dissection, we liberally used electrocautery or bipolar scissors (PowerStar Bipolar Scissors; Ethicon Inc, Somerville, NJ) to reduce blood loss [10]. Great care was taken to keep the cavities intact. The bronchus was divided and closed with sutures or staples. Stapled bronchial closure, our preferred method of closing the bronchus, was used in the surgeries of 6 of the 7 patients who underwent surgery after 1999. No lymphadenectomy was performed. The bronchial stump was covered with a latissimus dorsi muscle flap in 7 patients and with an intercostal pedicle flap in 2 patients. In the remaining 2 patients, there was no bronchial stump coverage. The technique of constructing a latissimus dorsi muscle flap was the same as the technique described by Pairolero and associates [12]. Meticulous hemostasis was again achieved using electrocautery and an argon beam coagulator. The pleural cavity was irrigated with at least 10 L of saline solution and povidone iodine, and then the chest was drained. All patients were extubated before leaving the operating room.

After the surgery, 7 patients were kept on chemotherapy regimens for at least 6 months, with the duration of most of the regimens spanning 2 years. Postoperative regimens were generally the same as preoperative ones, and usually included clarithromycin, rifampin, ethambutol, and streptomycin. The remaining 4 patients did not receive postoperative chemotherapy for various reasons, which included side effects in 2 patients, respiratory failure in 1 patient, and for an unknown reason in 1 patient. Postsurgical follow-up was completed on June 30, 2003. The duration of follow-up ranged from 0.6 to 16.9 years (median, 2.0 years).


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
The right side was operated on in 5 patients, and the left side was operated on in 6 patients. Operating time ranged from 142 to 477 minutes (median, 360 minutes). The median intraoperative blood loss was 555 mL (range, 130 to 1,245 mL; Table 2). No spillage of the contents of cavities into the operative field occurred in any patient.


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  		Table 2. Intraoperative Variables and Postoperative Complications

 
There was no operative mortality. One patient (9%) experienced acute respiratory failure on postoperative day 3 and required prolonged mechanical ventilation. Bronchopleural fistula occurred in 3 patients (27%). All fistulas were observed on the right side and were not associated with empyema. Of the 3 patients, 2 patients with a latissimus dorsi muscle flap had a fistula at 2 weeks and 2.3 months after surgery, and the remaining patient, who had an intercostal muscle flap, exhibited a fistula 3 months postoperatively. The patient who had a fistula at 2 weeks was the patient who was on a ventilator owing to acute respiratory failure. Routine bronchoscopy demonstrated minor disruption of the bronchial stump, although no increase in air was seen in the pneumonectomy space on a chest radiograph. The patient was returned to the operating room for reclosure of the bronchus, for the stump was expected to sustain positive pressure produced by mechanical ventilation for a long time. In the remaining 2 patients, a fall in the fluid level on a chest radiograph aroused the suspicions, although they were asymptomatic. When reopening the thoracotomy incision, in all 3 patients, we noticed that the stump was covered with the muscle flap and the pleural fluid was not purulent. After isolation of the stump, a fistula approximately 1 mm was identified. The stump was debrided back to healthy tissue and reclosed with sutures. Treatment was successful in all 3 patients without occurrence of postoperative empyema. Empyema without bronchopleural fistula occurred in 1 patient (9%) 1.4 months after surgery. The responsible organism was Serratia marcescens. The empyema was eventually cured after 2 months of irrigation of the pneumonectomy space with antibiotic solutions and povidone iodine.

All patients achieved sputum-negative status after the surgery. Relapse occurred in 1 patient. This patient had had scattered nodular lesions on the left lung before undergoing a right pneumonectomy. The contralateral lesions gradually progressed, and the patient finally had a relapse 2 years after surgery. This patient was one of the 3 patients who had recurrent disease after pulmonary resection in our entire series of 53 patients. Two late deaths occurred. One patient, who required prolonged mechanical ventilation, died of respiratory failure 11 months postoperatively. A second patient, the patient who had recurrent disease, died of respiratory failure 4 years postoperatively.


   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
Nontuberculous mycobacterial lung disease has become a significant health problem. Mycobacterium avium complex is the most common nontuberculous mycobacteria that has been shown to cause pulmonary disease. Other, rapidly growing mycobacteria and Mycobacterium kansasii follow [1]. Among the rapidly growing mycobacteria, Mycobacterium abscessus is the most common [7]. Although the advent of newer macrolides (eg, clarithromycin and azithromycin) has dramatically improved the results of chemotherapy for treatment of nontuberculous mycobacteria, medical therapy for Mycobacterium avium complex and Mycobacterium abscessus remains complicated [2, 3]. Therefore, in case of medical treatment failure, resectional surgery has been advocated for patients who have the disease localized to one lung and who are able to tolerate resection [11]. The purpose of surgery is to remove all gross lesions that contain a large number of bacilli. Lobectomy is considered in cases in which the disease is localized to one lobe. Pneumonectomy is considered over less aggressive procedures when patients have multiple cavities in one lung or if a lung is entirely destroyed.

Compared with lobectomy, pneumonectomy has been performed less frequently. Corpe [4] reported the results of 124 patients, who had excisional surgery for pulmonary infections caused by Mycobacterium avium-intracellulare. Of these patients, 9 underwent a pneumonectomy. In the report of Pomerantz and associates [5], 38 patients with mycobacterial infections other than tuberculosis underwent 41 pulmonary resections. Of these, 17 patients underwent a pneumonectomy. Their report is the largest study to use pneumonectomy for treatment of nontuberculous mycobacteria. Nelson and colleagues [6] studied 28 patients with Mycobacterium avium-intracellulare lung disease who underwent pulmonary resection. Of these patients, 8 underwent a pneumonectomy. In the present report, of the 53 patients undergoing pulmonary resection for nontuberculous mycobacterial infection during the past 20 years, 11 underwent a pneumonectomy.

This report reflects the fact that we have recently encountered an increasing number of nontuberculous mycobacterial patients who require a pneumonectomy. The patients in this report, who were referred to our hospital, were in such an advanced stage of the disease that pneumonectomy was the procedure of choice. In an earlier report that covered a time span ranging from April 1993 through January 2001, we described a situation in which only three pneumonectomies were performed on patients with Mycobacterium avium complex infection [9]. In this report, 6 of the 11 pneumonectomies were performed after January 2001. Although early surgical treatment has been advocated [5, 8], there are still patients who, because of a long history of medical treatment, have had to delay surgical treatment. Patients with some contralateral lesions may be eligible for pneumonectomy. In this report, 4 patients had scattered nodular lesions on the side opposite the affected side. On the basis of our experience, we believe that the tiny nodular lesions can be treated with aggressive postoperative chemotherapy, because removing a diseased lung prevents further spread to the contralateral lung.

The characteristics of patients in this report were similar to the characteristics of patients described in other studies. As reported previously [5, 6], most of our patients were middle-aged. The majority were slender females as were the patients in the report by Pomerantz and associates [5]. The number of right-sided and left-sided operations was equal. Even though the number of patients was small, distribution of destroyed lungs on the right and left sides was even. These findings were consistent with the findings of the previous report [5]. With regard to the technical aspects of pneumonectomy, we prefer extrapleural dissection for performing pneumolysis whenever dense pleural adhesions exist, as per the advocacy of Brown and Pomerantz [13]. Although extrapleural dissection may be associated with bleeding, the amount of intraoperative blood loss in this report was acceptable [14]. In addition, no contamination of the pleural space was encountered. Meticulous dissection using electrocautery and bipolar scissors is thought to have helped to reduce intraoperative blood loss and to avoid perforation of infected cavities.

We experienced no operative mortality on patients whose disease was so advanced as to require a pneumonectomy. Only 1 patient infected with Mycobacterium abscessus experienced acute respiratory failure, a condition that resulted in late death. It is crucial to select patients on the basis of indications for pneumonectomy, pulmonary function, and perfusion to the operated lung. Taking out one lung does not affect the respiratory function of patients with a destroyed lung, as pulmonary blood flow to the operated side is scant. Pneumonectomy, therefore, can be considered even for patients with relatively marginal pulmonary function. For patients with multiple cavities, the lungs on the operated side still receive approximately 20% to 30% of total lung perfusion. For these patients, pneumonectomy can be considered only when the patients have sufficient pulmonary reserve and lesser procedures, such as lobectomy with segmentectomy and bilobectomy, are not feasible. Preoperative pulmonary rehabilitation is also important to improve respiratory function in those patients who are not robust.

Pneumonectomy for nontuberculous mycobacterial infections has been reported to be associated with a high incidence of bronchopleural fistula [15]. An especially high morbidity rate after right pneumonectomy for nontuberculous mycobacterial lung diseases was pointed out by Pomerantz and associates [5]. In their study, of the eight bronchopleural fistulas occurring in 38 patients with mycobacterial infections other than tuberculosis, seven fistulas occurred after right pneumonectomy. Moreover, five of the fistulas occurred despite the use of muscle flaps. Since 1999, we have used a latissimus dorsi muscle flap to buttress the bronchial stump on all patients undergoing a pneumonectomy for nontuberculous mycobacterial infections, as per the advocacy of Pomerantz and associates [5]. We have, however, continued to encounter the problem of development of bronchopleural fistula on the right side. An incidence of bronchopleural fistula in this report was unexpectedly higher compared with that in our previous report, which demonstrated that five bronchopleural fistulas occurred after 50 right extrapleural pneumonectomies for empyema [10]. Positive airway pressure produced by prolonged mechanical ventilation could be considered a possible contributing factor to the occurrence of fistula at 2 weeks, as pointed out by Wright and associates [16]. Additionally, delayed wound healing of the bronchial stump could be responsible for the remaining fistulas. The fact that the bronchial stump after right pneumonectomy remains at risk for bronchopleural fistula despite the use of muscle flaps raises a question of whether bronchial stump reinforcement with muscle flaps can be advocated to prevent bronchopleural fistula. Based on our limited experience, we conjecture that the merit of using the muscle flap is to lessen the chance of harmful consequences of bronchopleural fistula, such as contamination of the pleural space and life-threatening aspiration of the pleural fluid, rather than to prevent bronchopleural fistula. In this report, all bronchopleural fistulas were detected before symptoms appeared. The fistulas were small and were not associated with empyema. It was possible to treat the fistulas with reclosure of the bronchus without consequence.

Despite the extensive disease of the patients in our report, we achieved a favorable outcome after pneumonectomy. All patients were in sputum-negative status after the operation. Relapse occurred in only 1 patient. This patient had had scattered nodular lesions on the left lung before undergoing a right pneumonectomy, and relapse could have resulted from the fact that no chemotherapeutic drugs were used before or after surgery because of adverse effects of the drugs in this patient. Because patients have only one lung after pneumonectomy, relapse on the remaining lung can be lethal. Therefore, adequate, long-term chemotherapy is mandatory after surgery. We recommend 2 years of multidrug chemotherapy regimens that contain clarithromycin after pneumonectomy.

It has been our experience that despite the bronchial stump protection with muscle flap, patients treated with right pneumonectomy for nontuberculous mycobacterial infections remain at risk for bronchopleural fistula. However, the use of a muscle flap may be helpful in minimizing the risk of detrimental consequences of bronchopleural fistula. The pneumonectomy procedure can result in high cure rates for patients with extensive nontuberculous mycobacterial infections when those patients are prescribed adequate preoperative and postoperative multidrug coverage.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Marras T.K., Daley C.L. Epidemiology of human pulmonary infection with nontuberculous mycobacteria. Clin Chest Med 2002;23:553-567.[Medline]
  2. Field S.K., Cowie R.L. Treatment of Mycobacterium avium-intracellulare complex lung disease with a macrolide, ethambutol, and clofazimine. Chest 2003;124:1482-1486.[Medline]
  3. Daley C.L., Griffith D.E. Pulmonary disease caused by rapidly growing mycobacteria. Clin Chest Med 2002;23:623-632.[Medline]
  4. Corpe R.F. Surgical management of pulmonary disease due to Mycobacterium avium-intracellulare. Rev Infect Dis 1981;3:1064-1067.[Medline]
  5. Pomerantz M., Madsen L., Goble M., Iseman M. Surgical management of resistant mycobacterial tuberculosis and other mycobacterial pulmonary infections. Ann Thorac Surg 1991;52:1108-1112.[Abstract/Free Full Text]
  6. Nelson K.G., Griffith D.E., Brown B.A., Wallace R.J., Jr Results of operation in Mycobacterium avium-intracellulare lung disease. Ann Thorac Surg 1998;66:325-330.[Abstract/Free Full Text]
  7. Griffith D.E., Girard W.M., Wallace R.J., Jr Clinical features of pulmonary disease caused by rapidly growing mycobacteria: an analysis of 154 patients. Am Rev Respir Dis 1993;147:1271-1278.[Medline]
  8. Shiraishi Y., Fukushima K., Komatsu H., Kurashima A. Early pulmonary resection for localized Mycobacterium avium complex disease. Ann Thorac Surg 1998;66:183-186.[Abstract/Free Full Text]
  9. Shiraishi Y., Nakajima Y., Takasuna K., Hanaoka T., Katsuragi N., Konno H. Surgery for Mycobacterium avium complex lung disease in the clarithromycin era. Eur J Cardiothorac Surg 2002;21:314-318.[Abstract/Free Full Text]
  10. Shiraishi Y., Nakajima Y., Koyama A., Takasuna K., Katsuragi N., Yoshida S. Morbidity and mortality after 94 extrapleural pneumonectomies for empyema. Ann Thorac Surg 2000;70:1202-1206.[Abstract/Free Full Text]
  11. American Thoracic Society. Diagnosis and treatment of disease caused by nontuberculous mycobacteria. Am J Respir Crit Care Med 1997;156(Suppl):S1-25.[Medline]
  12. Pairolero P.C., Arnold P.G., Piehler J.M. Intrathoracic transposition of extrathoracic skeletal muscle. J Thorac Cardiovasc Surg 1983;86:809-817.[Abstract]
  13. Brown J., Pomerantz M. Extrapleural pneumonectomy for tuberculosis. Chest Surg Clin N Am 1995;5:289-296.[Medline]
  14. Connery C.P., Knoetgen J., III, Anagnostopoulos C.E., Svitak M.V. Median sternotomy for pneumonectomy in patients with pulmonary complications of tuberculosis. Ann Thorac Surg 2003;75:1613-1617.[Abstract/Free Full Text]
  15. Conlan A.A., Kopec S.E. Indications for pneumonectomy. Pneumonectomy for benign disease. Chest Surg Clin N Am 1999;9:311-326.[Medline]
  16. Wright C.D., Wain J.C., Mathisen D.J., Grillo H.C. Postpneumonectomy bronchopleural fistula after sutured bronchial closure. Incidence, risk factors, and management. J Thorac Cardiovasc Surg 1996;112:1367-1371.[Abstract/Free Full Text]



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