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Ann Thorac Surg 2005;79:959-963
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Current Surgical Intervention for Pulmonary Tuberculosis

Shin-ichi Takeda, MD*, Hajime Maeda, MDa, Masanobu Hayakawa, MDb, Noriyoshi Sawabata, MDa, Ryoji Maekura, MDa

a Department of Thoracic Surgery and Pulmonary Medicine, Toneyama National Hospital
b Department of Surgery, Toyonaka City Hospital, Toyonaka City, Osaka, Japan

Accepted for publication September 2, 2004.

* Address reprint requests to Dr Takeda, Toneyama National Hospital, Toneyama 5–1–1 Toyonaka 560–8552 Japan (E-mail: stakeda{at}toneyama.hosp.go.jp).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: Surgery for pulmonary tuberculosis now plays a role in facing the emergence of complicated and multidrug resistant tuberculosis (MDR-TB), and it still remains a challenge for thoracic surgeons. We report on our 16 years of experience with lung resection for pulmonary tuberculosis.

METHODS: We retrospectively reviewed the surgical results of 35 patients (23 males and 12 females: mean age, 47.8 years) who underwent therapeutic surgical resection for pulmonary tuberculosis from 1988 to 2003.

RESULTS: Indications for surgery were MDR-TB in 26 patients, hemoptysis in 7, destroyed lung in 1, and drug allergy in 1. Thirty patients (85.7%) had fibrocavitary lesions seen radiologically, and 16 (61.5%) MDR-TB patients showed sputum-positive preoperatively. Operative procedures included 22 lobectomies, 7 pneumonectomies, 5 lobectomy plus segmentectomy procedures, and 1 segmentectomy. There was one operation-related death (2.9%) and 5 major postoperative complications (14.3%). Overall, 32 of 35 (91.4%) patients including 23 of 26 (88.5%) of the MDR-TB patients remained free of TB following surgery. Preoperative comorbidity, Aspergillus coinfection, operation time, transfusion, and male were the factors shown to be predictive of an unfavorable outcome.

CONCLUSIONS: Surgery remains a crucial adjunct to medical therapy for the treatment of MDR-TB and medical failure lesions. Treatment success was obtained in cases with MDR-TB with few and incomplete sensitive drugs, and the early morbidity and mortality were acceptable in the current series. Proper selection of the patients and early decision for surgical intervention can achieve a high success rate and the salvage of lung parenchyma in this difficult group of patients.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Surgery was one of the important forms of therapy for pulmonary tuberculosis (TB) until the introduction of effective antibiotics in the 1960s. At that time, greater than 100 cases of pulmonary resection for TB, which comprised 70% of all general thoracic procedures, were conducted at Toneyama National Hospital, a former sanatorium, in Japan. By the end of the next decade, the incidence of TB in Japan had decreased along with nationwide control of the disease. However, it has recently been shown that incidence of TB is again increasing with a marked rise in the number of multidrug resistant (MDR) cases [1–4], which is defined as resistance to both isoniazid and rifampin. Incompleteness of initial anti-TB treatment, infection with human immunodeficiency virus, and intravenous drug abuse were speculated to enhance to multidrug resistant tuberculosis (MDR-TB) in the western countries [5–7]. In addition, since the MDR-TB is difficult to control by medical therapy alone, surgery has emerged as a therapeutic option [3–5].

Patients who fail to complete therapy may allow drug resistance and progressive disease to occur. As a result, surgical intervention, long neglected, has again been proposed as an effective means to treat those patients [8–10]. In order to determine the current role of surgery as well as morbidity and late outcomes after surgical intervention, we thus retrospectively analyzed our current surgical results for pulmonary tuberculosis.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
From 1988 to 2003, 199 consecutive patients received surgical treatment for TB related diseases at our hospital. There were 2,756 general thoracic procedures undertaken during the same period; of which 115 (4.2%) were cases of chronic empyema secondary to pulmonary tuberculosis (86 males, 29 females; average age of 61 ± 17 years old [range, 19 to 82 years]), 49 (1.8%) were patients with tuberculomas resected as an undiagnosed pulmonary nodule (24 males, 25 females; an average age of 53 ± 12 years old [range, 18 to 82 years]), and 35 (1.4%) were cases with known pulmonary tuberculosis (23 males, 12 females; average age of 48 ± 14 years old [range, 18 to 75 years]). In the present study, we analyzed the operative results of 35 patients who underwent therapeutic pulmonary resection for tuberculosis with 49 patients who received diagnostic surgical excision for tuberculoma and patients who underwent pleuropneumonectomy for chronic empyema secondary to tuberculosis excluded.

All patients received individualized multituberculosis drugs for a mean duration of 3.9 years before the operation. Indications for surgery: MDR-TB (n = 26), hemoptysis (n = 7), symptomatic destroyed lung (n = 1), and severe allergy to an antituberculosis drugs [isoniazid (INH), rifampin (RFP)] (n = 1) (Table 1). Six patients with hemoptysis first received bronchial artery embolization; however, surgery was indicated because of the recurrent hemoptysis. One patient who had positive smear and destroyed left lung was regarded as a surgical candidate. Each patient was shown to have localized disease with adequate pulmonary functional reserve before being considered as a surgical candidate in general. Considerable bilateral disease was not seen in this series, however, 14 (40.0%) patients had bilateral lesions on radiologic images. Further cavity and fibrocavitary lesions were found in 30 patients (85.7%), and 16 of 26 (61.5%) MDR-TB patients were sputum smear positive preoperatively. In particular MDR-TB patients, 4 were new cases, and 22 were retreatment cases. All MDR-TB patients showed sputum smear positive at first presentation; however, with vigorous second line individualized chemotherapy with cycloserine, ethionamide, and floroquinolones (levofloxacin, ofloxacin, and sparfloxiacin), 10 patients become smear negative. Even in the sputum smear negative MRD-TB patients, a radiologically persistent fibrous cavitation, suggesting no improvements, were regarded as indications for surgery. The operative procedures included 22 lobectomies, 7 pneumonectomies including 1 completion pneumonectomy, 5 lobectomy plus segmentectomies, and one segmentectomy. One patient, who received a left upper segmentectomy, had a history of right upper lobectomy 20 years previously and a left upper segmentectomy indicated for a new contralateral lesion.


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  		Table 1. Clinical Profiles of 35 Patients
 
Surgical resection was performed by a posterolateral or axillary thoracotomy under general anesthesia according to the severity of the intrapleural adhesion, with a double-lumen endotracheal tube or single-lumen endotracheal tube with a bronchial blocker. We did not use a stapler for closure of the bronchus for patients with TB. The initial 22 patients did not receive reinforcement with muscle, omentum, or fat pad flap on the bronchial stump, whereas 5 of the most recent 13 patients were treated with a pericardial fat pad to the bronchial stump. Each patient received preoperative epidurals for pain management, and aggressive pulmonary toilet, including bronchoscopy, performed during anesthesia and just before extubation. Postoperatively the patients were scheduled to have an intensive antituberculosis chemotherapy regimen for at least 6 months. Postoperative medical therapy was performed for a mean duration of 1.8 years (range, 6 months to 7 years) in all patients. In particular, MDR-TB patients were scheduled to be treated for 18 to 24 months using second line chemotherapy, which was determined by the resected lesion smear or sputum culture. The mean follow-up period was 5.2 years (range, 2 to 14 years).

To identify the risk factors for an unfavorable outcome after surgery we divided the 35 patients into two groups. The success group (n = 27) were those patients who showed negative sputum smear and culture without further therapy after surgery. The unfavorable group (n = 8) included those who showed positive sputum smear results postoperatively, operation related death, or reoperation for TB related sequelae. Various factors affecting surgical outcome between success and unfavorable groups were compared.

Complete records during hospitalization, including perioperative problems, were available for all patients and were reviewed for patient demographic data, clinical presentation, causative organisms, patient treatment, and outcome. Results are given as the mean ± standard deviation. Comparisons of the two groups were made by unpaired t test or Fisher’s exact test (StatView 5.0; Abacus Concepts, Berkeley, CA). Stratified logistic regression analyses were used to explore the risk factors for development of unfavorable outcomes. Variables significantly related to the unfavorable outcomes in univariate analysis were considered in multivariate analysis. Probability values of less than 0.05 were considered significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
There were 23 men and 12 women with a mean age of 47.8 years in the TB group, with an average % vital capacity (VC) of 93.3% and forced expiratory volume in 1 second (FEV1) of 2.54 L, respectively, in the TB group. Six patients had diabetes mellitus (DM) requiring medication, 5 liver cirrhosis, 5 mixed Aspergillus infection and 1 methicillin resistant staphylococcus aureus (MRSA) pneumonia. Three of the 35 patients had a parent or brother who died of pulmonary tuberculosis, and another 2 patients underwent lobectomy, and 1 an artificial pneumothorax procedure listed in Table 1.

There was one 30-day mortality in a 75-year-old patient who underwent completion pneumonectomy (mortality 2.9%). This patient previously underwent a left upper lobectomy for lung cancer, and a completion pneumonectomy was attempted for a lesion in the left lower lobe with MDR-TB, MRSA, and Aspergillus superinfection. Because of the severe adhesion due to the recurrent infection and previous surgery, the patient was reexplored for hemothorax, followed by empyema and sepsis. As for postoperative complications, there were 2 patients with MRSA empyema without a bronchopleural fistula, 2 with postoperative clotted hemothorax necessitating reexploration, 2 prolonged air leakage, 1 with a sepsis and DIC, and one lung abscess (morbidity = 22.9% and major complication = 14.3%). There were no patients with bronchopleural fistulas or respiratory failure requiring mechanical ventilation, except for the previously mentioned operation death case.

In the comparison between the success and unfavorable groups, there were significant differences in gender, the presence of comorbidity, operative time, and bleeding. Preoperative duration of medical therapy, MDR, bilateral lesion, VC, and Aspergillus superinfection did not statistically affect the intermediate postoperative unfavorable outcome (Table 2). In the univariate analyses in the logistic regression tests, statistical differences were found in gender (p = 0.0049), Aspergillus superinfection (p = 0.0026), transfusion (p = 0.0213), comorbidity (p = 0.0065), and operating time (p = 0.0179); however, no independent factors were discovered by multivariate analysis.


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  		Table 2. Various Factors Affecting Surgical Outcome: Success Versus Unfavorable
 
Follow-up examinations were conducted for 33 patients at our hospital. In the late period, 2 patients died of cancer (1 lung cancer, 1 hepatoma) and 30 are alive and free from TB. Three patients required surgical intervention in the late period, in 2 of whom MRSA empyema required radical operation using omentum flap for this complication, and 1 who developed Aspergillus infection in the residual lobe, which eventually necessitated reoperation. Further, 2 MDR-TB patients, who once showed negative conversion, again showed positive sputum, and 1 had a positive MRD-TB from the chest wall after surgery. The MDR-TB patients had initial bilateral pulmonary lesions preoperatively, and in 1 relapse may still develop in the ipsilateral residual lingual segment because a segmentectomy was employed to preserve the pulmonary parenchyma. Overall, 32 (91.4%) of the patients including 23 (88.5%) of the MDR-TB patients have been free from TB after surgery. The number of sensitive drugs used and success rate (Table 3) revealed overall favorable results even in patients with few sensitivity drugs. There was no late mortality due to respiratory failure; however, 1 death occurred due to a tuberculosis related complication in a previously mentioned MDR-TB patient.


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  		Table 3. Number of Sensitive Drugs and Sputum Negative Ratio in Multidrug Resistant Tuberculosis: INH, RFP, EB, SM, and KM
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Historically, surgery has played a major role in the treatment of pulmonary tuberculosis, while the introduction of multidrug therapy based on streptomycin (SM), aminosalicylic acid (PAS), INH, and RFP in the 1970s significantly reduced its prominence. However, drug resistance is becoming an important problem in the management of the disease throughout the world, largely due to the complacency of physicians and patients as well as the high rate of infection in the developing countries [3, 11–14]. In addition, the retreatment cases had higher prevalence of MDR-TB than those in initial treatment cases [2, 8, 12]. Current indication of lung resection for pulmonary tuberculosis includes MDR-TB with a poor response to medical therapy, hemoptysis due to bronchiectasis or Aspergillus superinfection, and destroyed lung as previously reported [2, 3, 7, 14–19], which are consistent with our indications.

In the current series we assessed the surgical results of 35 patients known to have tuberculosis, and who were included in the current surgical indications. Results of medical therapy alone for MDR-TB are not satisfactory, and 40% of treatment failure patients have a dismal prognosis [1, 2, 4]. In the early series, the long duration was considered due to the fact that the pulmonary physicians were reluctant to advise surgery, partly because of the unpredictable outcome. In addition, the patients who benefited by surgery seemed to belong to a selected and minority group (26 [13.8%] of a total of 189 MDR-TB patients during the same period). Surgery for a destroyed lung is indicated when the related complications that are potentially lethal because of serious inflammatory phenomena or secondary superinfection have been detected [18–21]. However, the timing and decision for surgery have changed historically over the past decades. Preoperative comorbidity, operation time, gender, and bleeding were the factors for prediction of unfavorable outcome in the current series. In contrast, the number of sensitive drugs did not affect the postoperative outcome in patients with MDR-TB.

Overall, 32 (91.4%) of the present patients including 23 (88.5%) of 26 MTR-TB patients were free from TB after surgery. In terms of negative sputum conversion, 92.3% of the MTR-TB patients have benefited by surgical resection. However, Sung and colleagues [12] analyzed risk factors of relapse and found longer duration of medical therapy and advanced parenchymal lesions had an impact on postoperative results, which was similar to the present study. We consider that the postoperative individualized chemotherapy is mandatory for MDR-TB patients even after removal of the most grossly involved lesions, to ensure long-term cure [8]. Nakajima [21] emphasized a high prevalence of smear-positive in the resected lung in patients with MDR-TB having fibrocavitary lesions, even sputum smear negative preoperatively, of which evidence can strongly support our aggressive policy for this disease.

Other important aspects of TB surgery are assessments of operative risk and pulmonary functional reserve. Pulmonary resections for TB comprised only 1.4% of all general thoracic procedures at our institution. A lobectomy or pneumonectomy for TB is considered to be a high-risk procedure and technically hazardous because the thorax is filled with adhesions, scarring, and an area of chronic sepsis [22]. Even for the experienced surgeons, hilar dissection may pose significant problems. The violation of diseased parenchymal cavity during surgery, cavity lesion eroding to the pleura, excessive bleeding, and other medical problems including poor nutrition may affect the risks of surgery. In reviewing the comparison between TB patients and lung cancer patients, it is obvious that a pulmonary resection for TB is a high-risk procedure because of its difficulty. Rizzi and colleagues [17] reported that mean blood loss was 950 mL and Reed and colleagues [18] reported blood loss of 1,050 mL. In the current selective series for TB, blood loss for TB surgery was 3 times larger than that during lung cancer surgery (557 mL vs 164 mL). Despite the relative rarity of pulmonary resection procedure for TB, the general thoracic surgeon should keep in mind the impact of technical difficulties and higher complication rate. In early 1980, we treated a patient who had a bronchial fistula, one year after left pneumonectomy for MDR-TB, which was treated by reclosure by transsternal approach [14] followed by extraperiosteal air plombage [23]. We paid particular attention to bronchial stump complication, resulting in no events of this complication in the present patients. As for the morbidity, major complications developed in 14.7% of the present patients, which was similar to the report by Reed and colleagues [18] and a higher incidence of total complications ranging from 20% to 46% were reported [7, 17, 18, 24]. Regarding the pulmonary functional reserve in the present series, our patients had fairly tolerable VC (mean %VC, 96%) as compared with that of 49% in chronic empyema secondary to tuberculosis seen at our institution. Surgical complications for TB patients will continue to represent a challenge to the practicing thoracic surgeons, as well as control of the comorbidity including poor nutrition, DM, and compromised lung function.

Based on our limited experience, an early decision for operation and salvage of lung parenchyma in MTR-TB may have an impact on the surgical results. Further, proper patient selection and timing of operation are crucial to avoid relapse and offer an opportunity for an excellent outcome. In addition, expanding the indication for surgery for bilateral cavity should be considered in terms of pulmonary functional reserve. The significant incidence of superimposed Aspergillomas and lung destruction after surgery for TB still remain as serious problems [18]. Massard and colleagues [22] advocated resection of asymptomatic mycetomas to avoid potential catastrophic complications as well as preventive resection of long-standing cavitation to avoid fungal superinfection. We agree with their aggressive attitude to control TB and its complication TB, though universally accepted indications for these lesions remain to be established.

Conclusions
Our results suggest that pulmonary resection can be successful for patients with MDR-TB who have few or incomplete sensitive drugs; however, vigorous individualized perioperative chemotherapy should be done. In the present cases, early morbidity and mortality were acceptable and the role of surgery was justified in terms of operative outcome in spite of a high complication rate due to the inherent technical difficulties. Further, we recommend that an early decision for surgical intervention and aggressive policy for operations for patients with pulmonary TB may lead to an acceptable salvage of lung parenchyma tissue as well as a high success rate.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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