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Ann Thorac Surg 2008;86:1640-1645. doi:10.1016/j.athoracsur.2008.07.056
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Pulmonary Resection in the Treatment of Multidrug-Resistant Tuberculosis: A Retrospective Study of 56 Cases

Haifeng Wang, MM, Hongsheng Lin, MM, Gening Jiang, MD*

Department of Thoracic Surgery, Shanghai Pulmonary Hospital, Tongji University, Shanghai, China

Accepted for publication July 10, 2008.

* Address correspondence to Dr Jiang, Department of Thoracic Surgery, Shanghai Pulmonary Hospital, Tongji University, 507 Zhengmin Rd, Shanghai, 200433, China (Email: jgnwp{at}yahoo.com.cn).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Multidrug-resistant tuberculosis (MDR-TB) has become a challenge to TB control, and surgical resection is regaining its status as an integral component of multimodal treatment. We evaluated the efficacy and risks of pulmonary resection in the treatment of MDR-TB.

Methods: A retrospective review was performed of 56 patients who had undergone pulmonary resection for MDR-TB from January 1995 to July 2006. Preoperative diagnoses included cavitation in 25 patients, lung destruction in 17, endobronchial TBs in 10, and tuberculoma in 4.

Results: Mycobacterium tuberculosis resistant to both isoniazid and rifampin was isolated from the sputum of all patients preoperatively but in only 5 patients postoperatively. Pneumonectomy was performed on 25 patients and lobectomy on 31. No patients died perioperatively, but major complications occurred in 14 patients, with a morbidity of 25%. Complications included reoperation due to uncontrollable postoperative bleeding in 1 patient, chylothorax in 1, wound infection in 1, bronchopleural fistula in 9, and chronic tuberculous empyema in 2. Analysis of variance showed that lung function was significantly correlated with the type of preoperative diagnosis. Univariate and multivariate logistic regression analyses revealed that endobronchial TB significantly contributed to the development of bronchopleural fistula, and bronchial stump reinforcement could prevent its occurrence.

Conclusions: Pulmonary resection plays an important role in the treatment of MDR-TB. Endobronchial TB is a significant risk factor for developing bronchopleural fistula, but bronchial stump reinforcement can effectively prevent its occurrence.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Multidrug-resistant tuberculosis (MDR-TB) refers to Mycobacterium tuberculosis resistant to at least both isoniazid and rifampin. Although pulmonary TB has been largely controlled in the West, with the exception of immunodeficient patients, it is not rare in developing countries. The situation in China is quite critical, too. According to the World Health Organization, in 2005 there were 8.8 million new cases of TB globally, an incidence of 136/100,000 [1].

Worldwide, the prevalence of primary and acquired MDR-TB among all cases of TB is 7.6% and 17.1%, respectively [2]. The main cause of MDR-TB is inadequate chemotherapy. The treatment for MDR-TB is a prolonged and expensive course of medication, with a low cure rate and high rates of relapse, toxicity, morbidity, and mortality [3]. Previous studies showed that chemotherapy combined with surgical resection was an effective way of controlling MDR-TB. For patients with indications for an operation, timely intervention should be considered [4]. Surgical resection can remove irreversibly damaged lung parenchyma that will not respond to chemotherapy. This in turn leads to reduced rates of recurrence and mortality, resulting in cure in 88.5% to 95.6% of patients [4–7].


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
We retrospectively reviewed the records of 56 consecutive patients undergoing pulmonary resection for the treatment of MDR-TB in the Department of Thoracic Surgery, Shanghai Pulmonary Hospital, Tongji University, from January 1995 to July 2006. The Institutional Review Board of Shanghai Pulmonary Hospital, Tongji University approved the protocol of the current study.

By the time of operation, the mean duration of anti-TB chemotherapy was 43.5 months (range, 3 to 240 months). Before operation, each patient had been treated with a mean of 5.4 (range, 3 to 11) different anti-TB agents: 18 patients had used 3 to 4 anti-TB agents, 22 patients had used 5 to 6, and 16 patients had used at 7 or more. Isoniazid had been used in 56 patients, rifampin in 56, ethambutol in 45, streptomycin in 43, pyrazinamide in 40, ofloxacin in 17, protionamide in 14, paraaminosalicylate in 11, levofloxacin in 9, rifapentine in 9, amikacin in 5, capreomycin in 2, and ciprofloxacin in 2.

Indications for resection were:

1 infection with M tuberculosis resistant to at least isoniazid and rifampin as revealed by drug sensitivity testing;
2 progression of disease despite second-line therapy;
3 repeated hemoptysis or secondary infection;
4 localized disease amenable to resection; and
5 adequate cardiopulmonary reserve for lung resection.

Major preoperative clinical manifestations included cough in 32 patients, hemoptysis in 21, expectoration in 19, low-grade fever in 11, chest distress in 5, dyspnea in 4, night sweats in 3, fatigue in 2, chest pain in 2, and emaciation in 1.

Preoperative examinations included full blood analysis, biochemistry, arterial blood gas analysis, electrocardiogram, spirometry, acid-fast sputum smear, culture and drug sensitivity testing, chest roentgenogram and computed tomography (CT), and fiberoptic bronchoscopy.

We divided these patients into four groups according to disease characteristics shown on chest roentgenogram, CT, and bronchoscopy: Group 1, tuberculous cavity, 25 (44.7%); group 2, lung destruction, 17 (30.4%); group 3, endobronchial TB, 10 (17.9%), including 6 with main bronchial and 4 with lobar bronchial TB; and group 4, tuberculoma in 4 (7%).

The diagnosis of endobronchial TB was primarily made at bronchoscopy and was confirmed by pathology postoperatively. Endoscopic findings included erythema, edema, ulceration, granulation, and stenosis or occlusion of the affected bronchus. Because microbiologic diagnosis had already been made, biopsy during bronchoscopy was not routine, and frozen section analysis was not done intraoperatively.

The operations included 25 pneumonectomies (44.6%), including 19 left and six right pneumonectomies; 31 lobectomies (55.4%), including eight left upper, 16 right upper, one right middle, three right lower, one right upper and middle, and two right middle and lower lobectomies.

Double-lumen endobronchial intubation was routinely used to facilitate single-lung ventilation as well as to prevent soiling of the contralateral lung. All operations were undertaken through a posterolateral thoracotomy, and care was taken not to contaminate the pleural cavity. Extrapleural dissection was performed whenever there were firm adhesions. If pleural contamination did occur, the chest cavity was thoroughly washed with 0.25% neomycin solution plus 1:20 iodophor solution and saline. The bronchial stump was managed with an automatic stapler was in 20 patients and interrupted 4-0 absorbable Vicryl suture (Ethicon, Somerville, NJ) in 36. Forty-two of the bronchial stumps were reinforced, among which 30 were wrapped by pedicled parietal pleura and the other 12 by pedicled pericardium.

The operations lasted a mean of 195 minutes (range, 90 to 450 minutes). One or 2 intercostal tubes were used on every patient postoperatively. For pneumonectomy, 1 clamped tube was left in situ for 48 hours and unclamped intermittently to check hemostasis and maintain mediastinal position. For lobectomy, 2 tubes were used until there was no air-leak and drainage was below 200 mL in 24 hours.

Patients were followed up postoperatively at the outpatient department of Shanghai Pulmonary Hospital. Patients underwent sputum examination monthly until 2 consecutive negative smears were obtained, then every other month for 6 months, and every 6 months thereafter. Patients underwent chest roentgenogram each month for 3 consecutive months, once at 6 months and every 6 months thereafter. As of April 2007, follow-up ranged from 9 to 137 months, and no patient has been lost to follow-up.

Analysis of variance was used to compare the difference in lung function among patients with different types of MDR-TB. Univariate and multivariate logistic regression analyses were used to assess risk factors for bronchopleural fistula (BPF). We defined BPF, persistent or recurrent smear positivity, and chronic tuberculous empyema as disease recurrence and calculated disease-free survival using the Kaplan-Meier method. All statistical analyses were done using SPSS 12.0 software (SPSS Inc, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
We identified 56 consecutive patients (33 men, 23 women) undergoing pulmonary resection for the treatment of MDR-TB. Their mean age was of 39.1 years (range, 21 to 71 years). Forty-five patients were tested for human immunodeficiency virus (HIV), and all results were negative. (HIV antibody testing was performed selectively before 2000, since that time it has become a routine preoperative investigation.)

All 56 patients had a positive sputum smear at the time of operation. Preoperative drug-sensitivity testing of M tuberculosis cultured from sputum revealed that all samples from the 56 patients were resistant to at least both isoniazid and rifampin, in accordance with the diagnostic criteria for MDR-TB. Among the 56 patients, 2 were resistant to only isoniazid and rifampin, 16 were resistant to streptomycin, isoniazid, and rifampin, 9 were resistant to isoniazid, rifampin, and ethambutol, and 29 were resistant to streptomycin, isoniazid, rifampin, and ethambutol. Because of technical limitations, we could only perform drug-sensitivity testing for these 4 drugs.

We compared spirometry and arterial blood gas tests among the four different manifestations of disease. Patients with lung destruction and endobronchial TB a significantly lower forced expiratory volume in 1 second (FEV1) and PaO 2 than those with tuberculoma and tuberculous cavity (p < 0.05). Values for PaCO 2 did not differ significantly between the four groups of patients (Table 1).


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  		Table 1 Lung Function Among Different Disease Manifestations
 
There was no in-hospital perioperative death. Major postoperative complications occurred in 14 patients, including 9 patients with BPFs (16.1%), 2 (3.6%) with chronic tuberculous empyema without fistula, and 1 patient (1.8%) each with hemothorax requiring reoperation, chylothorax managed with total parenteral nutrition, and wound infection successfully treated with drainage and antibiotic therapy.

There were altogether nine cases of BPF. Two BPFs were treated by closed drainage combined with careful irrigation using 0.25% neomycin solution and metronidazole solution alternatively twice a day when the patients were stable. Three BPFs underwent delayed reoperation and closure through a thoracotomy when there was no ongoing evidence of sepsis, and the other four were treated by closed intercostal drainage alone.

The 2 patients with chronic tuberculous empyema were diagnosed 18 months and 30 months after operation without obvious evidence of a BPF. The diagnosis of tuberculous empyema was established by positive culture of M tuberculosis from pleural fluid. These were treated by open window drainage, followed by a second-stage pedicled muscle flap plombage once sepsis had been controlled.

Among the 56 patients, 51 had negative sputum cultures immediately after the operation, with an operational conversion rate of 91.1%. They received postoperative anti-TB therapy for a mean of 12 months (range, 6 to 18 months). During the follow-up, 49 remained sputum-negative, and 2 relapsed to sputum-positive when complicated with chronic tuberculous empyema 18 months and 30 months postoperatively. Two patients remained sputum-positive postoperatively and throughout follow-up. Three patients remained sputum-positive immediately after their operation but became sputum-negative during postoperative medical therapy.

Univariate logistic analysis showed that only endobronchial TB and bronchial stump reinforcement were significantly related to the incidence of BPF (p < 0.05; Table 2). None of the remaining factors, such as duration of disease, number of preoperative relapses, number of drugs resistant to, sex, age, FEV1, operation type, side of operation, operation time, and method of bronchial stump closure had any significant relationship to the incidence of BPF (p > 0.05).


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  		Table 2 Univariate Logistic Analysis for Risk Factors of Postoperative Bronchopleural Fistula
 
The two significant factors, endobronchial TB and bronchial stump reinforcement, were further investigated using multivariate logistic regression analysis. The results showed that endobronchial TB was a more powerful predictor of postoperative BPF (odds ratio, 18.839; p < 0.05), whereas bronchial stump reinforcement remained inversely related to the rate of BPF (odds ratio, 0.061; p < 0.05; Table 3).


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  		Table 3 Multivariate Logistic Analysis for Risk Factors of Postoperative Bronchopleural Fistula
 
The overall disease-free survival was 75% (42 of 56). Disease-free survival among different groups of patients was 40.0% for endobronchial TB (4 of 10), 70.6% for lung destruction (12 of 17), 88.0% for cavitation (22 of 25), and 100% for tuberculoma (4 of 4; p < 0.05; Fig 1). Disease-free survival for lung destruction, cavitation, and tuberculoma combined was 82.6% (38 of 46). Mean disease-free survival was 45.125 months (95% confidence interval [CI], 11.151 to 79.099 months) for endobronchial TB, and 109.924 months (95% CI, 95.397 to 124.450 months) for the other types of diseases (p < 0.01; Fig 2). Disease-free survival for pneumonectomy was 60% (15 of 25) and for lobectomy was 87.1% (27 of 31). Mean disease-free survival was 63.228 months (95% CI, 43.710 to 82.745 months) for pneumonectomy and 116.000 months (95% CI, 100.452 to 131.548 months) for lobectomy (p < 0.05; Fig 3).


Figure 1
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  		Fig 1. Kaplan-Meier estimates of disease free-survival among patients with the four different types of disease. Survivals compared with number of patients in each group are given in parentheses (p = 0.013). (TB = tuberculosis.)

 

Figure 2
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  		Fig 2. Kaplan-Meier estimates of disease-free survival between patients with endobronchial tuberculosis (TB) and other types of disease (p = 0.003).

 

Figure 3
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  		Fig 3. Kaplan-Meier estimates of disease-free survival between patients with pneumonectomy and lobectomy (p = 0.021).

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Although HIV-related MDR-TB is uncommon in China, the new wave of inner migration has caused serious problems in China's control of TB, including MDR-TB. Just as in other parts of the world, MDR-TB in China is mainly the result of inadequate anti-TB therapy, including poor prescription, interrupted drug supply, and patient noncompliance. At least 5 drugs are needed for the treatment of MDR-TB, and the duration of drug therapy may need to be as long as 18 to 24 months [8–10]. Patients must also take expensive and poorly tolerated second-line drugs whose high prices and toxicity do not guarantee efficacy. On the contrary, medical treatment of MDR-TB is often unsuccessful, and surgical resection has therefore reemerged as a powerful weapon in the fight against TB.

MDR-TB often manifests as cavitation, lung destruction, endobronchial TB, and tuberculoma. In this study, by comparing long-term outcomes among patients with these clinical presentations of MDR-TB, we found that lung destruction and endobronchial TB were more detrimental than tuberculous cavitation and tuberculoma.

In fact, the development of MDR-TB is a progressive process. Destruction of lung parenchyma can progress from 1 segment to 1 lobe, to multiple lobes, to the whole lung, and finally to both lungs, accompanied by progressive deterioration of lung function. Lalloo and colleagues [11] thus recommended timely surgical intervention to prevent the spread of MDR-TB and protect the remaining normal lung. For the same reason, we advocate that if a diagnosis of MDR-TB is established, no highly effective anti-TB agents are available, and symptoms are progressive, that lung resection should be considered to prevent further damage to the lungs [12].

Surgical resection can decrease the load of resistant bacilli and therefore shorten and simplify anti-TB therapy and, consequently, relieve patients from excessive economic and psychologic burdens. Furthermore, because MDR-TB is most often smear-positive, definitive surgical resection will in most patients promptly eliminate the source of and, therefore, the spread of MDR M tuberculosis.

As a result of careful patient selection, and improvements in thoracic anesthesia and anti-TB agents, postoperative morbidity and mortality have dropped dramatically after lung resection for MDR-TB. At the present time, according to most reports, postoperative mortality after lung resection for MDR-TB varies from 0% to 3.3% and the incidence of complication from 12% to 30%, mainly BPF, empyema, postoperative bleeding, respiratory failure, and infection. BPF is perhaps the most morbid complication associated with the treatment of MDR-TB. In-hospital perioperative mortality in our study was 0% and morbidity was 25%, including a 16% incidence of BPF, similar to rates previously reported by others [4–7, 13–15].

In the present study, both univariate and multivariate logistic regression analysis demonstrated that endobronchial TB was an important risk factor for the development of postoperative BPF (OR, 18.839). The reason, we suppose, is that on occasion, surgical resection of the whole length of diseased bronchus is incomplete, such that the bronchial stump may be colonized by residual M tuberculosis, leaving a potential origin of relapse. Besides this, endobronchial TB itself may impair the healing of the bronchial stump. Park and colleagues [5] retrospectively studied lung resection for MDR-TB and found that endobronchial TB was a risk factor for developing postpneumonectomy BPF. To prevent postpneumonectomy BPF, it is reasonable, on the basis of the above hypothesis, to perform frozen section pathology on the resected bronchial stump to make sure that no M tuberculosis remains in the bronchial stump.

Postoperative BPF is a cause of significant morbidity and potential mortality in patients with TB. The incidence of this complication ranges from 0% to 16.7% [4–7]. To prevent BPF, a vascularized pedicled muscle, pleura, or pericardial flap is most frequently used for bronchial stump reinforcement. By multivariate analysis we found that wrapping the bronchial stump with pedicled pleura or pericardium could significantly reduce the incidence of postoperative BPF (OR, 0.061, p < 0.05). Our finding is consistent with Shiraishi and colleagues [6]. Van Leuven and colleagues [13] did not advocate routine bronchial stump reinforcement except for sputum-positive patients. They also believed that preserving blood supply to the bronchus was crucial to the healing of the bronchial stump, and as such warned against dissection to the point of devascularization of the bronchus and specifically against using electric coagulation around the bronchus.

We did not find a relationship between FEV1 and postoperative BPF; however, some authors have reported that FEV1 is intimately related to the development of BPF. Specifically, a vital capacity of less than 50% and a low FEV1 preoperatively have been implicated as important risk factor for BPF [16].

With regard to the management of the bronchial stump, Deschamp and colleagues [17] found that automatic stapling was more helpful in decreasing BPF than absorbable sutures. We found no significant relationship between method of bronchial stump closure and postoperative BPF.

Two cases of chronic tuberculous empyema occurred in our study. No evidence of BPF was found in these 2 patients. We presume that this complication may have been caused by residual M tuberculosis in the regional lymph nodes or at the bronchial margin. Even with standard anti-TB chemotherapy, M tuberculosis inside diseased lymph nodes may retain some activity. The potential for the subsequent development of resistance in this population of organisms to anti-TB agents implicates these lymph nodes as insidious elements that could cause relapse of disease when conditions are favorable. We contend that regional tuberculous lymph nodes may break up or perforate into the bronchus; therefore, we recommend removal of apparently affected peribronchial lymph nodes to reduce the chance of empyema and BPF. Unlike lymph node dissection during operations for cancer, we do not disrupt seemingly normal lymph nodes because we want to preserve the vasculature around the bronchial stump.

In our study, 2 patients with a diagnosis of endobronchial TB remained sputum-positive postoperatively and were unresponsive to anti-TB chemotherapy. This implies that patient selection is very important in treating this subgroup of MDR-TB patients. Endobronchial lavage and endobronchial stenting are feasible choices as well.

The Kaplan-Meier survival analyses revealed that endobronchial TB and pneumonectomy both reduced disease-free survival. The explanation is that although pneumonectomy did not correlate with the development of a BPF in our study, 4 of 5 patients with persistent or recurrent positive smears (without BPF) had undergone pneumonectomy.

For refractory MDR-TB that is localized, a timely pulmonary resection maybe the only way to prevent further pulmonary deterioration and preserve lung function. According to previous reports, more than 90% of MDR-TB patients may be converted to sputum-negative with surgical resection [4–7]. Lung resection for MDR-TB is currently a relatively safe procedure. The pivotal issue is how to reduce postoperative morbidity.

Unfortunately, resection is not the panacea for all MDR-TB. If the disease has progressed to the point where there is extensive parenchymal damage and the lung function is critically impaired, resection is no longer possible. Therefore, the ideal management and prevention of MDR-TB is standard anti-TB chemotherapy, followed when the disease is no longer responsive to chemotherapy by consideration of lung resection before destruction of parenchyma and associated decline in pulmonary function make surgical resection impossible.

We thank Prof Peter Clarke and Dr Stephen Barnett from the Department of Thoracic Surgery, Austin Hospital, Melbourne, Australia, for their contributions in the rhetoric and structural organization to this article.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. World Health Organization Global tuberculosis control: Surveillance, planning, financingGeneva, Switzerland: World Health Organization; 2007.
  2. World Health Organization, International Union Against Tuberculosis and Lung Disease The WHO/IUATLD Global Project on Anti-Tuberculosis Drug Resistance Surveillance 1999–2002: anti-tuberculosis drug resistance in the world; third global reportGeneva, Switzerland: World Health Organization; 2004.
  3. Törün T, Güngör G, Ozmen I, et al. Side effects associated with the treatment of multidrug-resistant tuberculosis Int J Tuberc Lung Dis 2005;9:1373-1377.[Medline]
  4. Takeda S, Maeda H, Hayakawa M, et al. Current surgical intervention for pulmonary tuberculosis Ann Thorac Surg 2005;79:959-963.[Abstract/Free Full Text]
  5. Park SK, Lee CM, Heu JP, et al. A retrospective study for the outcome of pulmonary resection in 49 patients with multidrug-resistant tuberculosis Int J Tuberc Lung Dis 2002;6:143-149.[Medline]
  6. Shiraishi Y, Nakajima Y, Katsuragi N, et al. Resectional surgery combined with chemotherapy remains the treatment of choice for multidrug-resistant tuberculosis J Thorac Cardiovasc Surg 2004;128:523-528.[Abstract/Free Full Text]
  7. Naidoo R, Reddi A. Lung resection for multidrug resistant tuberculosis Asian Ann Thorac Cardiovasc Surg 2005;13:172-174.
  8. Farmer P, Kim JY. Community based approaches to the control of multidrug resistant tuberculosis: introducing "DOTS-plus" BMJ 1998;317:671-674.[Free Full Text]
  9. Tahaoglu K, Törün T, Sevim T, et al. The treatment of multidrug-resistant tuberculosis in Turkey N Engl J Med 2001;345:170-174.[Medline]
  10. Chakrabarti B, Davies PD. Key issues in multidrug-resistant tuberculosis Future Microbiol 2007;2:51-61.[Medline]
  11. Lalloo UG, Naidoo R, Ambaram A. Recent advances in the medical and surgical treatment of multi-drug resistant tuberculosis Curr Opin Pulm Med 2006;12:179-185.[Medline]
  12. Crofton J, Chaulet P, Maher D, et al. Guidelines for the management of drug-resistant tuberculosisWHO/TB/96.210Geneva, Switzerland: WHO; 1997.
  13. Van Leuven M, De Groot M, Shean KP, et al. Pulmonary resection as an adjunct in the treatment of multiple drug-resistant tuberculosis Ann Thorac Surg 1997;63:1368-1372.[Abstract/Free Full Text]
  14. Pomerantz BJ, Cleveland Jr JC, Olson HK, et al. Pulmonary resection for multi-drug resistant tuberculosis J Thorac Cardiovasc Surg 2001;121:448-453.[Abstract/Free Full Text]
  15. Connery CP, Knoetgen 3rd J, Anagnostopoulos CE, et al. Median sternotomy for pneumonectomy in patients with pulmonary complications of tuberculosis Ann Thorac Surg 2003;75:1613-1617.[Abstract/Free Full Text]
  16. Somocurcio JG, Sotomayor A, Shin S, et al. Surgery for patients with drug-resistant tuberculosis: report of 121 cases receiving community-based treatment in Lima, Peru Thorax 2007;62:416-421.[Abstract/Free Full Text]
  17. Deschamps C, Bernard A, Nichols III FC, et al. Empyema and bronchopleural fistula after pneumonectomy: Factors affecting incidence Ann Thorac Surg 2001;72:243-248.[Abstract/Free Full Text]



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