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Ann Thorac Surg 1995;59:896-900
© 1995 The Society of Thoracic Surgeons

Results of Surgical Management of Tuberculosis: Experience in 206 Patients Undergoing Operation

Adriano Rizzi, MD, Gaetano Rocco, MD, Mario Robustellini, MD, Gerolamo Rossi, MD, Claudio Della Pona, MD, Fabio Massera, MD

Division of Thoracic Surgery, ``E. Morelli'' Regional Hospital, Sondalo, Italy

Accepted for publication December 14, 1994.


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Between January 1978 and December 1990, 206 operations for pulmonary tuberculosis were performed at our institution, a former sanatorium located in northern Italy. Patients with tuberculoma and pleural tuberculous disease were excluded from this series. Cavitary sequelae, bronchiectases, and hemoptysis were the most common indications for resection. Scar cancer and mycetoma were associated diseases in more than 60% of the patients. Healing was achieved in 90% of the patients. Operative mortality was 3%. Overall morbidity was 29.1%. Patient stratification showed that sputum-positive patients had a higher morbidity (30%) and a lower healing rate (86.2%). Before operation, an accurate assessment of both the performance status and the functional reserve of the surgical candidates is emphasized. Despite a high complication rate, aggressive surgical treatment of drug-resistant tuberculosis or its stabilized sequelae is warranted to achieve anatomobiological eradication of the disease, thus avoiding long-term troublesome complications.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The gold standard for the surgical management of pulmonary tuberculosis is controversial. The surgeon's expertise plays an important role in determining when and how to operate on an infected lung. Technical hazards can result in increased intraoperative mortality. In addition, pleural space problems can set in any time in the postoperative period, leading to serious morbidity.

This report details the experience on the surgical treatment of tuberculosis gained over a 12-year period in a former sanatorium located in northern Italy.


    Material and Methods
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Between January 1978 and December 1990, 400 patients with tuberculosis underwent surgical evaluation. Three hundred twelve patients (78%) were considered for resection. One hundred six patients with tuberculomas excised on the suspicion of cancer and tubercular pleural disease were excluded from this study. Accordingly, a total of 206 resected patients were included in this series.

More than 75% of the patients were referred to our institution from other areas of Italy or from north African countries. The mean age of the patients at the time of operation was 49 years (range, 9 to 79 years); there were 174 male and 32 female patients with a 5.4:1 male to female ratio.

In 112 patients (54.4%), recent history was positive for drug resistance (100 patients) or noncompliance (12 patients) to the medical treatment. Resistance to multiple drugs (including isoniazid and rifampin) was a common finding in the first group. Noncompliant patients had drug-susceptible tuberculosis and were all sputum pos-itive. In addition, sputum positivity was the reason for final hospitalization in all noncompliant patients.

Three patients (1.4%) were found to have atypical mycobacteriosis. Of these, 2 had infections from Mycobacterium avium, and 1 from Mycobacterium kansasii. The remaining 91 patients (44.2%) had complicated tuberculous sequelae requiring surgical treatment.

At the time of operation, 80 patients (38.8%) had positive sputum, including the 3 patients with atypical mycobacterial infections. Sputum positivity was noted in patients with chronic hemoptysis (20), lung destruction (16), tuberculous progression (21), cavity (15), and bronchiectasis (8).

Multiple-drug chemotherapy was instituted in all patients before operation. The majority of the patients included in this series were already receiving antimycobacterial drugs before surgical evaluation. Commonly used regimens included rifampin, isoniazid, and pyrazinamide, together with ethambutol or streptomycin. Quinolones, ethionamide, capreomycin, p-aminosalicylic acid, and cycloserine were added for drug-resistant disease. Patients with mycetoma superimposed on posttuberculous cavities were begun on a regimen of antimycobacterials and, more recently, azol derivatives at some time before operation (usually 2 to 3 weeks). Postoperative chemotherapy was administered for at least 3 months and included rifampin, isoniazid, quinolones, and streptomycin. Excluded from postoperative chemotherapy were patients with scar cancer. Recently, patients operated on for the association of tuberculosis and mycetoma received postoperative coverage with quinolones and azol derivatives.

Preoperative work-up included conventional radiologic studies, chest computed tomography, bronchoscopy, and bronchography, the last being used in selected cases. In addition, performance status and respiratory function also were studied carefully. In this setting, quantitative ventilation-perfusion scans were obtained to predict postoperative function in those patients with major contralateral disease.

Median preoperative forced expiratory volume in 1 second was 1,660 mL (range, 1,120 to 2,430 mL). A predicted postoperative less than 800 mL contraindicated surgical treatment.

Preoperatively, care also was taken in improving the nutritional status of the consumptive patients scheduled for operation.

In all patients presenting with posttuberculous bronchiectases, preoperative bronchography was performed routinely, especially before the computed tomography era.

Operative Indications
Operative indications are summarized in Table 1Go. Elective indications accounted for 91% of all operations. Concomitant medical disorders, occurring alone or in combination, were common among the patients undergoing operation (Table 2Go). The presence of tuberculous sequelae in the contralateral lung could lead to a major reduction in pulmonary function. As a contributing factor to the progression of tuberculosis to a stage not amenable to medical treatment, immunodepression was diagnosed by skin test negativity in patients who had recurrent infections despite normal blood panels. Diabetes, malnutrition, and psychiatric conditions were concomitant disorders in more than 50% of the patients. Liver function often was impaired by long-standing therapies with antimycobacterial drugs or alcoholism.


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Table 1. . Indications for the Surgical Treatment of Tuberculosis (January 1978--December 1990)
 

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Table 2. . Concomitant Medical Disorders
 
Operative Procedures and Pathologic Findings
The distribution of involvement was as follows:

An almost even distribution was noted as to right-sided versus left-sided tubercular involvement (54.7% versus 45.3%). Upper lobes predominantly were involved by the disease.

Lobectomy was by far the most frequent procedure, often via an extrapleural approach (Table 3Go). Extrapleural dissection was indicated when intrapleural pneumolysis could not be achieved due to dense and vascularized adhesions.


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Table 3. . Operations for Tuberculosis (January 1978-- December 1990)
 
The bronchial closure was done using a stapling device in 123 patients (61.9%), whereas hand-sewn interrupted sutures were used in 76 (38.1%). The choice of bronchial closure was made according to the intraoperative evalu- ation of bronchial wall features (ie, malacia, calcifications) as well as to the bronchographic findings, when available. After major resections, especially upper lobectomies, the bronchial stump was covered with pleural (75%) or intercostal muscle flaps.

Whenever pleural space problems were anticipated, an attempt at pleural space obliteration was made through tailored thoracoplasty (6 patients) or muscle transposition (11 patients). Both thoracoplasty and muscle transposition were concomitant with resection. In the remaining patients, routine decortication was performed.

At operation, we found unexpected additional lesions in 67 patients, incomplete fissures in 56, silicotic adenopathy in 34, bronchial malacia in 12, lack of cleavage from the chest wall in 47, and hilar sclerosis in 46. Moreover, 21 patients had a destroyed left lung requiring an extrapleural pneumonectomy. Additional technical hazards, such as dense pleural adhesions due to reintervention (21 patients), vascularized apical adhesions (42), and pachypleuritis (36), also were encountered.

Intraoperative complications included chest wall bleeding in 12 patients, bronchial hemorrhage in 6, cavitation rupture in 12, bronchial rupture in 7, tear of diaphragm in 2, and tear of pulmonary artery in 1. Intraoperative median blood loss was 950 mL (range, 400 to 2,500 mL), whereas median total blood loss, inclusive of the early postoperative period, was 1,800 mL (range, 1,000 to 4,000 mL).

Surgically treated tuberculosis was associated with mycetomas or lung cancer in more than 60% of the patients (Table 4Go). In 9 patients with suspected lung cancer, histologic examination showed the association of silicosis and tuberculous sequelae. A scar cancer was found in 54 patients with suspected lesions who had been treated previously by our phthisiologists for a tuberculous lesion in the same area of the lung. On follow-up radiographs, there was evidence of (1) nodular conglomeration in the same area of previous tuberculous involvement, (2) recently developed satellite lesions surrounding tuberculous sequelae, or (3) parenchymal cavitations in areas where only nodular lesions were previously noted. All patients presented aspecific symptoms (ie, weight loss, low-grade fever, or hemoptysis). The need for surgical exploration was indicated by no symptomatic or radiologic improvement after 8 weeks of multidrug chemotherapy. At operation, in all instances parenchymal scarring was evident in conjunction with a neoplastic nodule. A complete locoregional lymph node dissection was performed after positive frozen section of the parenchymal lesion. An adenocarcinoma was found in 50 patients (93%).


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Table 4. . Diseases Associated With Tuberculosis
 
Pathologic staging was T1 N0 in 36 patients, T2 N0 in 12, T1 N1 in 4, and T1 N2 in 2 patients. Not surprisingly, postoperative evolution was related to the stage of the tumor rather than to the tuberculous disease. Survival rates for stages I and II are comparable with the ones reported in the literature (77% and about 48%, respectively). The 2 patients with N2 disease are still alive and free from disease at 18 and 14 months of operation. They have not been subjected to adjuvant therapy.

Tuberculosis was the most common predisposing factor in the majority of patients with symptomatic mycetomas. Aspergillomas developed in posttuberculous sputum-negative cavitations and bronchiectases, often resulting in life-threatening hemoptysis.

In 52 patients (25.2%) with tuberculous sequelae mycobacteria were found in the pathologic specimen.


    Results
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
As of December 1993, minimum follow-up is 3 years (range, 3 to 12 years).

Healing was defined as no clinical or radiologic signs of disease 3 years after operation. Postoperative healing was obtained in 90% of the treated patients (Table 5Go). Sputum-positive patients showed a lower healing rate (86.25%) (see Table 5Go).


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Table 5. . Results of Surgical Treatment of Tuberculosis (206 Patients)
 
Operative mortality, defined as deaths occurring within 30 days of operation, was 3% (Table 6Go). Three late deaths, occurring more than 2 years after operation, were related to the progression of the tuberculous disease (1.4%). Overall morbidity was 29.1%, whereas for sputum-positive patients it was 30% (Table 7Go). Moreover, sputum-positive patients had a slightly higher major complication rate than sputum-negative patients (10% versus 7.9%), whereas the minor complication rate was the same (20% versus 21%).


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Table 6. . Operative Mortality (206 Patients)
 

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Table 7. . Postoperative Complications (206 Patients)
 
Early postoperative morbidity was defined as occurring within 30 days of operation. The causes of early postoperative morbidity included fever (16 patients), hemoptysis (6 patients), wound breakdown (8 patients), and residual space (10 patients).

Late postoperative morbidity comprised wound breakdown (2 patients), tuberculous empyema (3 patients), and aspecific empyema (5 patients). This group also includes 4 patients who had recurrent tuberculosis after operation and persistent sputum positivity. Accordingly, 4 of 80 patients (5%) had persistent sputum positivity after operation. Air space problems and residual hemoptysis were seen in patients who had undergone operation for posttuberculous bronchiectases and cavities. As a rule, residual hemoptysis was unremarkable and resolved with little or no additional treatment.

A bronchopleural fistula complicated the postoperative course of 4 patients (1.9%) who had been operated on for lung destruction (1) or multiple cavities (3). Three bronchopleural fistulas developed after pneumonectomy and one after bilobectomy. Three patients had the bronchus closed with the stapling device (2 after completion pneumonectomy and 1 after bilobectomy), and 1 with interrupted sutures (after pneumonectomy). In no instances was endoscopic closure of the fistula attempted due to the underlying empyema. The bronchopleural fistula occurring after bilobectomy healed spontaneously after adequate pleural chest tube drainage. After pneumonectomy, a complicating empyema developed in 1 patient who had the bronchus stapled. Successful management of this last complication included a tailored thoracoplasty with intrathoracic muscle transposition.

In the remaining 2 patients, chronic respiratory insufficiency made surgical repair unfeasible, leading to well-tolerated continued chest tube drainage. At a later time, both patients refused an open-window procedure.

Postoperatively, 4 additional patients had development of an aspecific (1) and a tuberculous empyema (3). They had been operated on for chronically bleeding apical cavities. Successful long-term results were obtained with chest tube drainage converted to open pleural window, and tailored thoracoplasty or muscle transposition, as indicated.

Disseminated intravascular coagulation developed after inadequate drainage of pleural cavity in 2 patients who had undergone resection for complex mycetoma and chest wall tuberculous involvement requiring technically demanding pneumolysis. They underwent successful treatment by immediate reoperation with removal of large intrapleural blood clots and proper chest tube placement.

Mean postoperative hospital stay was 13.1 days (range, 9 to 25 days).


    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The indications for the surgical management of tuberculosis already have been outlined [1, 2]. Essential to the success of the procedure is the timing of operation. In our practice resection was scheduled (1) after 6 to 8 months of multiple-drug antitubercular treatment, (2) when smears and cultures were negative, (3) in the presence of stable functional and biological condition, (4) when prevalent monolateral involvement was anticipated, (5) when tubercular bronchitis was excluded, (6) in the absence of radiologic improvement of parenchymal sequelae or for drug resistance (sputum-positive patients), and (7) to correct complications of pulmonary tuberculosis (such as hemoptysis or superimposed infections). Operation for tuberculosis has to be performed according to the general principles of radicality and functional tolerance. Furthermore, essential to long-term results are adequate preoperative and postoperative medical treatments aimed at reducing the mycobacterial burden and protecting the patient against the risks of reactivation of the disease due to postoperative immunosuppression. Other authors [3] recommend earlier operation (after a 3-month regimen of chemotherapy) in patients with resistant mycobacterial infections or mycobacterial infections other than tuberculosis due to the attendant possibility of lung destruction. In this setting, crucial to decreasing postoperative complication rate is an adequate nutritional status to be obtained through individualized dietetic regimens [4].

After partial lung resection, the use of muscle flaps to cover the bronchial stump or when residual space is anticipated is advocated [3]. This is especially true when, as in our series, the upper lobes are involved most frequently. Muscle flaps were used when pleural flaps failed to ensure adequate protection of the bronchial stump. Obliteration of pleural space was obtained with tailored thoracoplasties or with costal resection ``a la demande'', and decortication according to the Fowler-Delorme technique [5].

Essential to the optimal use of stapling devices is the resection line, which has to fall on healthy tissue. Accordingly, an obvious contraindication to operation is the endoscopic finding of tuberculous bronchitis, in that endobronchial granulation tissue, erosion, and ulceration of the mucosa may predispose to the development of bronchopleural fistula [4, 6].

Preoperative identification of the exact amount of diseased parenchyma becomes of paramount importance. Conventional radiographs and chest computed tomography may be of some help. The latter is reported to have lower sensitivity for bronchiectases localized in the middle lobe or the lingula [7]. Accordingly, we add bronchography in bronchiectatic patients to obtain information about bronchial wall dynamics and to identify irreversible anatomofunctional alterations, such as adenolectasis (or false diverticulae), filling defect images, parietal atrophy, and accordionlike appearance [8]. These bronchographic findings, together with an accurate intraoperative evaluation of the diseased bronchus, may help the surgeon select the appropriate technique for bronchial closure. Intraoperatively, excessive skeletization and massive bleeding from hypertrophic bronchial vessels are potential complications of bronchial dissection. In addition, tedious oozing can result from pneumolysis. Intrapleural clotting due to ineffective drainage of the chest cavity may in turn lead to disseminated intravascular coagulation [9].

Pomerantz and associates [3] reported an overall 45% complication rate in the postoperative period of patients undergoing operation for either resistant tuberculosis or mycobacteriosis other than tuberculosis. Similarly, Reed and colleagues [2] had a total complication rate of 46%. The different morbidity in our series (29.1%) presumably could be explained by a lower incidence of both sputum-positive patients and atypical infections.

The association of tuberculosis and cancer in our patients deserves further consideration. Scar cancers may be found in patients who had medically treated tuberculosis and in whom apparent recurrences develop in the same areas of the lung. Often, these patients present with an aspecific clinical and radiologic picture. A common finding is lack of improvement despite adequate medical treatment, which results in surgical evaluation [4]. In our experience, the observation of an abnormal desmoplastic reaction surrounding the tumor supports the view according to which a scar cancer results from chronic stimulation of lung parenchyma [1]. In addition, the inclusion of scar cancer among adenocarcinomas is justified by the overlapping clinical behavior [1]. Surprisingly, 48 patients (88.9%) with scar cancer had stage I disease. This could be explained only in part by the possibility of an earlier detection of lung cancer in patients subjected to radiologic surveillance for their underlying tubercular disease.

The significant incidence of superimposed mycetomas and the observation of predominant left lung destruction after tuberculous infection represent a challenge to the surgeon [2, 10, 11]. Resection of asymptomatic mycetomas is advocated to avoid catastrophic complications [10]. We, unlike others [4], believe that inactive, long-standing cavitations (so-called open negative state) are to be resected in the presence of adequate pulmonary function to avoid a likely fungal superinfection [2]. The physiopathologic features of the destroyed lung, causing large intrapulmonary shunting, have to be kept in mind when interpreting preoperative function tests of patients who otherwise might be denied a curative resection [11].

In conclusion, the surgical management of tuberculosis is focused on the biological and anatomic eradication of the disease [12]. Proper patient selection and timing of operation are crucial to avoid relapses and provide definitive cure [12]. Adequate courses of antimycobacterial drugs and careful evaluation of the nutritional status and the pulmonary reserve are critical to optimal operation. This is especially true for consumptive patients with drug-resistant or atypical tuberculosis. Conversely, patients with tuberculous sequelae may face operation with acceptable performance status. Hemoptysis is a common presenting symptom, often being associated with radiologic evidence of parenchymal damage involving the upper lobes. Lung destruction, predominantly involving the left side, appears to be related to a combination of altered anatomic and hemodynamic factors [11]. Whether it is planned for resistant or atypical mycobacterial infections or for tuberculous sequelae, operation for tuberculosis implies substantial morbidity. Both patient condition and surgical hazards contribute to the high complication rate. However, an aggressive policy toward parenchymal tuberculosis can result in a successful outcome in more than 90% of the treated patients [4].


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    Acknowledgments
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
We thank Dr Thomas W. Shields for his continuous support and constructive criticism.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Rocco, Via Agricoltura, 20, 23037 Tirano, Italy


    References
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Shields TW. Pulmonary tuberculosis and other mycobacterial infections of the lung. In: Shields TW, ed. General thoracic surgery. Philadelphia: Lea & Febiger, 1989:792--8.
  2. Reed CE, Parker EF, Crawford FA. Surgical resection for complications of pulmonary tuberculosis. Ann Thorac Surg 1989;48:165–7.[Abstract]
  3. Pomerantz M, Madsen L, Goble M, Iseman M. Surgical management of resistant mycobacterial tuberculosis and other mycobacterial pulmonary infections. Ann Thorac Surg 1991;52:1108–12.[Abstract]
  4. Pomerantz M. Surgery for tuberculosis. Chest Surg Clin North Am 1993;4:723–7.
  5. Pairolero PC, Trastek VF. Surgical management of chronic empyema; the role of thoracoplasty. Ann Thorac Surg 1990;50:689–90.[Medline]
  6. Donath J, Khan FA. Tuberculous and posttuberculous bronchopleural fistula. Chest 1984;86:697–703.[Abstract/Free Full Text]
  7. Giron J, Skaff F, Maubon A, et al. L'apport de la TDM en coupes millimetriques dans le diagnostic et le bilan des bronchiectases. Comparison avec la broncographie a propos de cinquante-quatre patients. Ann Radiol 1988;31:25–33.
  8. Pinet F, Amiel M, Rubet A, Froment JC, eds. Selective bronchography and bronchial brushing. New York: Springer-Verlag, 1979:99--105.
  9. Rocco G, Rizzi A, Robustellini M, Rossi G, Della Pona C, Massera F. About the surgical treatment of pulmonary mycetoma. Ann Thorac Surg 1994;57:260–2.[Medline]
  10. Massard G, Roeslin N, Wihlm JM, Dumont P, Witz JP, Morand G. Pleuropulmonary aspergilloma: clinical spectrum and results of surgical treatment. Ann Thorac Surg 1992;54:1159–64.[Abstract]
  11. Ashour M, Pandya L, Mezraqji A, et al. Unilateral post-tuberculous lung destruction: the left bronchus syndrome. Thorax 1990;45:210–2.[Abstract/Free Full Text]
  12. Klingensmith WE, Beckley W. Resectional surgery in pulmonary tuberculosis: its bacteriologic basis. J Thorac Cardiovasc Surg 1963;45:146–51.[Medline]



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