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Ann Thorac Surg 2001;71:443-447
© 2001 The Society of Thoracic Surgeons


Original article: general thoracic

Surgical treatment of active and sequelar forms of pulmonary tuberculosis

Redha Souilamas, MDa, Marc Riquet, MDa, Françoise Le Pimpec Barthes, MDa, Antoine Chehab, MDa, Athos Capuani, MDa, Eric Faure, MDa

a Department of Thoracic Surgery, Hôpital Laennec, Paris, France

Accepted for publication July 17, 2000.

Address reprint requests to Dr Riquet, Département de Chirurgie Thoracique, Hôpital Laennec, 42 rue de Sèvres 75007 Paris, France
e-mail: marc.riquet{at}lnc.ap-hop-paris.fr


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. The incidence of tuberculosis has risen since 1990, and in some countries, the resistant forms are becoming more and more frequent. Surgical treatment is once again needed to manage these problems. The purpose of this study was to analyze the indications and results of resection, which we performed for pulmonary tuberculosis.

Methods. From 1980 to 1997, 477 patients were operated on for thoracic or intrathoracic tuberculosis in Laennec Hospital, Paris (259 suffered lung diseases). There were 165 women and 94 men, aged 25 to 86 years (mean 46 years), from Europe (n = 148), North Africa (n = 65), Subsaharian Africa (n = 34), Asia (n = 7), and the West Indies (n = 5). This population was reviewed concerning the lung tuberculosis (sequelae or active lesions), the indications of lung resection, the type of resections performed, and the results at 1, 6, and 12 months.

Results. Active lesions were present in 97 cases and sequelae in 162. Surgery was performed for a therapeutic purpose in 104 patients with sequelae, and in 10 patients with active tuberculosis (pneumonectomy, n = 19; pleuropneumonectomy, n = 19; lobectomy, n = 54; and segmentectomy, n = 22). Surgery was performed for a diagnostic purpose in 54 patients with sequelae, and in 87 patients with active lesions (lobectomy, n = 32; segmentectomy, n = 19; wedge resection, n = 94, of which 11 performed by video-assisted thoracoscopy since 1991). One patient died after pleuropneumonectomy. We observed 25 complications: empyema, n = 7; hemothorax, n = 2; prolonged air leaks, n = 14; and pneumopathy, n = 2. All patients with active lesions subsequently were given antitubercular drugs. Follow-up was 100% at 1 month, 57% (n = 92) and 77% (n = 75) at 6 months for patients with sequelae and for patients with active lesions, respectively. All were asymptomatic with a normal chest roentgenogram. The number of operations for active lesions is increasing over the years, while it is decreasing for sequelar lesions.

Conclusions. In our department, surgery is being performed more frequently to make a diagnosis in cases of active tuberculosis, and to treat complicated lesions in case of sequelae. Lung resection for active tuberculosis evolving under treatment or for drug resistance was rare. However, our study confirms the good results commonly obtained by surgery and supports the idea that surgery may help eradicate tuberculosis when social and economic circumstances render its medical management difficult or hazardous.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
With medical therapy, the incidence of tuberculosis in France decreased 7% each year starting in 1974 until 1985. Since 1990, this trend progressively inverted [1, 2]. Such incidence of pulmonary disease has increased worldwide due to poor social situations and poverty, immigration, homelessness, intravenous drug abuse, increase of patients with acquired immunodeficiency syndrome, inadequate first-course therapy, poor patient compliance, and inadequate follow-up, thus allowing drug resistance and progressive disease to occur [2]. With the increasing number of new cases of tuberculosis, especially in Paris district [1], we wondered whether surgery had to play a more important role in the treatment of lung tuberculosis, and therefore, we reviewed all the patients who underwent lung resection for tuberculosis in our general thoracic surgery department since 1980.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Between January 1980 and December 1997, 477 patients underwent a surgical procedure for thoracic tuberculosis. In 46% of the patients, the procedure was performed for extrapulmonary diseases: mediastinal lymph nodes tuberculosis (n = 100), pleural (n = 83) and pericardial (n = 6) involvement, and chest wall or thoracic vertebra cold abscesses (n = 29). In 54% (259 patients), surgery was performed for pulmonary disease; these 259 patients constitute the basis of the study. There were 165 men and 94 women with a mean age of 46 years (range 21 to 86 years). Thirty-six were native of France (13.9%); the others originated from the rest of Europe, n = 112; North Africa, n = 65; Subsaharian Africa, n = 34; Asia, n = 7, and the West Indies, n = 5. The tuberculous lesions of the lung parenchyma were either active foci or sequelae of previously treated tuberculosis. The diagnostic criteria for sequelae have been: a previous history of tuberculosis, pathology (caseofibrous lesions, empty cavern [3]) and absence of acid-fast bacilli in resected lung tissue samples neither by direct examination nor by culture. The diagnostic criteria for active tubercular lung lesions have been bacteriologic (presence of mycobacterium tuberculosis in the resected specimens either by direct examination or by cultures) and histologic (specific tubercular lesions of caseous follicular type [3]). Only patients with lesions caused by Mycobacterium tuberculosis were included. Patients were classified in two groups: group A (n = 162) consisted of patients undergoing surgery for sequelae and group B consisted of patients with active tuberculosis (Tb).

Preoperative work-up included chest roentgenogram, bronchoscopy, respiratory function tests, as well as isotopic quantitative perfusion scans to predict postoperative respiratory function. Before 1985, bronchography was routinely performed and was thereafter progressively abandoned. Since 1985, chest computed tomography (CT) has been routinely performed. Since 1990, CT-guided needle biopsy has been occasionally performed for diagnosis purpose if necessary. Preoperative care in improving the nutritional status and "respiratory physiotherapy" was always undertaken in order to clear out bronchial secretions and enhance respiratory performances.

All operations were performed under general anesthesia and selective intubation of bronchi. The standard operative approach was posterolateral thoracotomy with the patient lying on the healthy side. Nineteen pneumonectomies, 19 pleuropneumonectomies, 86 lobectomies, 39 segmentectomies, and 96 wedges resections were performed. Recently, a few wedge resections were performed by video-assisted thoracoscopy, but nothing was modified in the general principles of patient setup. The patients were extubated as soon as possible at the end of the procedure and everything was performed to mobilize the patients as early as possible, including intensive respiratory physiotherapy.

Records were retrospectively reviewed for tubercular lesions and surgical indications, surgical procedures, and postoperative events. Follow-up was obtained through review of clinic consultations, written correspondence, telephone calls, or data provided by the patients’ private physicians. Median follow-up period was 6.9 months (range 1 to 34 months) but results were more particularly focused on the 1-, 6-, and 12-month follow-up periods.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The number of operations for active tuberculosis (group B) has increased over time. From 1980 to 1990, 28% of the patients underwent surgery for active tuberculosis (45 vs 113) compared with 51% since 1990 (52 vs 49) (p < 0.001). Whatever the group, there was two types of indications: surgery for diagnostic purpose (n = 145 [56%]) and operations for therapeutic purpose (n = 114 [44%]).

The types of surgical resection for group A, indications (therapeutic vs diagnostic), and the main clinical pathologies are listed in Table 1. The types of surgical resection for group B and indications (therapeutic vs diagnostic) are listed in Table 2.


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Table 1. Surgical Resection for Group A, Indication (Therapeutic vs Diagnostic), and Main Clinical Pathology When Therapeutic

 

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Table 2. Surgical Resection for Group B, Indication (Therapeutic vs Diagnostic), and Main Clinical Pathology When Therapeutic

 
Operations for therapeutic purpose were more frequent in group A ((104 of 162 [64%]) than in group B (10 of 97 [10%]), whereas operations for diagnostic purpose were more frequent in group B (87 of 97 [90%]) than in group A (58 of 162 [36%]).

Group A consisted of patients predominantly needing therapeutic operations. These patients (n = 104) were all symptomatic and presented with chronic or relapsing lung infection and had hemoptysis in one-third of cases; 95% (n = 91) had a previous history of documented and treated tuberculosis that occurred 4 to 15 years before the lung resection. Most of the operations performed were major resections, and all the pneumonectomies and pleuro-pneumonectomies (n = 38) took place in that subgroup. Diagnostic intervention in group A was for suspected malignancy. All patients were smokers and only 6 had a previous history of pulmonary tuberculosis. Among the 41 wedge resections performed, 11 have been performed by video-assisted thoracoscopy (since 1991). Morbidity was 14% and mortality was only 1% (one death). Complications after resection for group A patients are listed in Table 3. Major complications were observed after pneumonectomies and pleuropneumonectomies: seven empyemas, all cured by drainage and irrigation with antibiotics. The complications observed in other procedures were essentially prolonged air leaks, cured by chest tubes drainage. One hundred sixty-two patients in group A have been followed up at 1 month (100%), 92 at 6 months (56.8%), and 29 at 12 months (18%). All were asymptomatic and the chest roentgenogram did not show any particular anomaly.


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Table 3. Complications After Resection for Group A Patients

 
In group B, only 10 patients underwent resection for therapeutic reasons: 3 for resistance and 7 for increasing lesions while under treatment. Resistance to antitubercular drugs was a primary resistance to Isoniazid and to Streptomycine in the first patient, a secondary resistance to Isoniazid and Streptomycine with a progressing destruction of the infected lobe in the second patient, and a secondary resistance to Isoniazid alone in the third patient. The remaining 87 patients underwent resection for diagnostic purpose. All patients presented with a lesion suggestive of lung cancer after thorough workup: four of them had a previous history of tuberculosis; 2 had positive tuberculin skin test that had led to an antitubercular treatment for 6 months without any improvement; one patient had positive serology for human immunodeficiency virus HIV (he was the only one of the whole series). The postoperative period was uneventful in this group except in three cases: two prolonged air leaks and one reoperation for bleeding. The diagnosis was histologically established in all the cases. Specimens of resected lung cultures grew positive in 14 cases. All patients were discharged after operation with an adapted or standard antitubercular drugs regimen. Ninety-seven patients (100%) have been followed up at 1 month, 75 (77%) at 6 months, and 32 (33%) at 12 months. All were asymptomatic, chest roentgenogram did not disclose any anomaly and sputum bacteriological investigations proved negative. More particularly, the patients having demonstrated resistance to treatment were cured of their infection at 12 months.


    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Lung resections were performed for both active tuberculosis and sequelae. Resections for sequelae seemed to become less frequent whereas resections for active lesion were increasing. Most of the indications were for therapeutic purpose in case of sequelae because of complicated lesions (infection and hemoptysis). In patients with active disease, establishing a diagnosis was the major indication, and surgery allowed achieving this aim, and indications for therapeutic purpose were few (10%), aimed mainly at drug-resistant cases, or disease evolving despite antitubercular drug therapy. Postoperative complications were of moderate grade, with only one death, and most morbidity was successfully managed with few reinterventions. Long-term results seem to be good but several patients were lost to follow-up.

Lung resections represented 54% of all the cases we have treated surgically over the same period (259 of 477). This is an intermediate rate when compared with other similar series that report frequencies ranging from 45% [4] to 63% [5]. However, surgery for active tuberculosis (n = 97) was indicated in only 20.3% of the whole group (97 of 477), whereas in France, 64.6% of the officially registered new cases of tuberculosis (extrathoracic included) concern the lung [1].

Lung resection for diagnostic purpose was performed in 35.8% of cases with tuberculosis sequelae and in up to 89.7% of cases that proved to be active lesions. Such an indication, 56% of the whole series, was due to the fearful idea of letting a cancer evolve. The possibility of neoplasia was outlined as a major indication as early as 1974 by McLaughlin and Hanking [6]; the frequency of such an indication may be as high as 77% [7]. Furthermore, cancer may be associated with lung tuberculosis as scar cancer in as much as 33% of cases, as reported by Rizzi and associates [8], who paradoxically excluded resections performed for tuberculoma. Most authors [4, 5, 7, 9], including us, did not report on scar cancers; however, we agree that the risk of scar cancer is an additional reason to resort to surgery for diagnostic and therapeutic purpose. Indeed, most diagnostic difficulties are encountered in case of peripheral nodular forms such as tuberculomas. Reviewing 36 cases of resected tuberculomas, Ishida and associates found 24 of them (66%) to have radiographic criteria of malignancy [10]. Percutaneous needle aspiration appears to be of limited value in these cases [4, 7], and most of the procedures were failures. Video-assisted thoracoscopy wedge resection appears to be the first-choice technique for diagnosing these nodular forms, and tubercular nodules represent 10% of video-assisted thorascopy resected coin lesions [11]. This more recent approach permits, like thoracotomy, the excision of the whole tubercular lesion and, thus, plays a major role in its treatment. It is the reason why we thought it necessary to include it in our study, contrary to Rizzi and associates [8]. Explanation of that point of view is stressed by Perelman and Strelzov [5]: "the capabilities of antibacterial therapy are limited for patients in whom tuberculosis is detected for the first time and who have tuberculomas without overt signs of exacerbation. The characteristics of the blood supply to such pathologic entities make it difficult for the drugs to act on mycobacteria efficiently. Conditions are then created for the development of secondary drug resistance by mycobacteria; there also remains the probability of exacerbation or recurrence of tuberculosis."

In our experience, surgery was rarely performed for drug-resistant tuberculosis (3 patients). Two recent French papers did not mention any patient operated on for this indication [4, 12]. Moreover, our patients did not have true multidrug-resistant disease, which is defined as having organisms resistant to at least Isoniazid and Rifampicin [13]. Yet, according to the literature, the major indication for surgical treatment of pulmonary tuberculosis is becoming true multidrug resistance [8, 1316]. This difference between countries is partly explained by a spontaneous low multiresistance rate, which is around 0.5% in France, whereas, for instance, it is 3.5% in the US [2]. However, primary resistance was observed in 6% of patients suffering lung tuberculosis in one pneumology department in Paris, 2.9% being primary resistance to Isoniazid, but no resistance to Rifampicin or Ethambutol was observed [17]. Whereas some authors have in mind the resistance of isolated tuberculous mycobacteria to several basic antituberculous drugs, others use the term to mean the absence of well-defined positive clinical and radiologic effects in response to antitubercular therapy [5]. These cases, seldom mentioned in the literature, represent 7 of 10 patients we operated on, 10 out of 12 patients operated on by Mouroux and associates [4], and as many as 129 of 347 patients operated on by Ribet [12]. The lack of efficiency of the medical treatment in such cases is not explained, but surgery proved helpful in curing them.

In our series, resection for sequelae was performed in 104 patients presenting with complicated disease, mainly infections and/or hemoptysis, sometimes life threatening. Aspergilloma was present in 36 out of these 104 patients (Table 2). Aspergilloma is not reported in some series [7, 9, 13]; sometimes its frequency is rare (one case for Mouroux and associates [4]), but it may be present in as much as 45% of patients [8].

The major operations we had to perform (pneumonectomies and pleuropneumonectomies) took place in this subgroup of patients, who presented with complicated sequelae, and we never had to perform such operations for active tuberculosis. This could be explained by the rare indications of surgery for drug-resistant tuberculosis present in our series; Pomerantz and Brown [14] performed 62 pneumonectomies in 111 patients operated on for drug-resistant tuberculosis. In a series of 20 pneumonectomies for tuberculosis [18], lung destruction was due to drug-resistant tuberculosis in 20% of the patients (4 of 20). The overall mortality and morbidity in our series was low: 0.4% (1 of 259) and 9.6% (25 of 259), respectively.

Complications occurred essentially after surgery for sequelae with therapeutic purpose, and in that subgroup, the corrected rates, 1% and 20%, respectively, are high but they remain among the low rates of the literature we have referred to. The most frequent complication we observed was prolonged postoperative air leak (n = 17) after partial lung resections. Such prolonged air leaks may be the cause of residual pleural spaces that are classically treated by secondary tailored thoracoplasty. As the risk of such spaces to occur may be great in case of upper lobe destruction, some authors even advocate pleural space obliteration through tailored thoracoplasty while performing lobectomy or pleurolobectomy when pleural space problems are anticipated [10]. We never had to perform thoracoplasty for residual pleural space and always obtained space obliteration using a chest tube inserted by posterior approach [19].

Surgery is efficient and reliable in curing tuberculosis, both sequelar and active forms. In active forms evolving under antitubercular drugs, cure is obtained in 64.8% of patients [12], and in drug-resistant active forms, cure is obtained in 80% or more [14, 16]. All patients we followed up were cured, but one has to take into consideration the high number of patients who were lost to follow-up at 6 and 12 months. Patients lost to follow-up had left their home without having given new addresses, and even their private physicians had no news concerning them. Such defection is linked to the marginal social conditions of a mainly immigrant population (86%) that make the life of the concerned patients difficult and unstable. In an other Parisian study of Brechot and associates [17], 22% of the patients were lost to follow-up 3 months after establishing the diagnosis of tuberculosis and initiating treatment; and in one medical unit of our hospital, the same rate of defection (26%) was observed [20]. Our results stress that the difficulties encountered in managing tuberculosis, which are due to the socioeconomic context surrounding a noncompliant and socially unstable population, also exist after surgery.

To conclude, in our department, surgery was more frequently performed to make a diagnosis in cases of active tuberculosis. Lung resections for tuberculosis evolving under treatment or for drug resistance were rare. However, our study confirms the good results obtained by lung resection for tuberculosis that are reported by all the authors publishing at the present time. It adds further support to the idea that surgery may be a valuable tool for eradicating residual active foci, in cases where socio-economic conditions render medical management difficult or hazardous.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Tchakamian S., Haury B. Les cas déclarés de tuberculose en 1994. Bull Epidemiol Hebdo 1995;52:225-227.
  2. Hubert B., Desenclos J.C., Schwoebel V. Epidemiologie actuelle de la tuberculose. Med Ther 1995;1:7-17.
  3. Hruban R.H., Hutchins G.M. Mycobacterial infections. In: Dail D.H., Hammar S.P., eds. Pulmonary Pathology. New York: Springer Verlag, 1994:331-350.
  4. Mouroux J., Maalouf J., Padovani B., Rotomondo C., Richelme H. Surgical management of pleuropulmonary tuberculosis. J Thorac Cardiovasc Surg 1995;110:1-9.
  5. Perelman M.I., Strelzov V.P. Surgery for pulmonary tuberculosis. World J Surg 1997;21:457-467.[Medline]
  6. McLaughlin J.S., Hanking J.R. Current aspects of surgery for pulmonary tuberculosis. Ann Thorac Surg 1974;17:513-525.
  7. Whyte R.I., Deegan S.P., Kaplan D.K., Evans C.C., Donnely R.J. Recent surgical experience for pulmonary tuberculosis. Resp Med 1989;83:357-362.[Medline]
  8. Rizzi A., Rocco G., Robustellini M., Rossi G., Della Pona C., Massera F. Results of surgical management of tuberculosis: experience in 206 patients undergoing operation. Ann Thorac Surg 1995;59:896-900.[Abstract/Free Full Text]
  9. Reed C.E., Parker E.F., Crawford F.A. Surgical resection for complications of pulmonary tuberculosis. Ann Thorac Surg 1989;48:165-167.[Abstract]
  10. Ishida T., Yokuyama H., Kaneko S., Surgi K., Sugimachi K., Hara N. Pulmonary tuberculoma and indications for sur-gery: radiographic and clinicopathological analysis. Resp Med 1992;86:431-436.[Medline]
  11. Debrosse D., Riquet M., Deslandes P., et al. Videothoracoscopie des nodules pulmonaires. Peut-on se passer d’un repérage préopératoire. Rev Mal Resp 1995;12:459-464.
  12. Ribet M. L’incidence véritable de la tuberculose pulmonaire. Rev Mal Resp 1994;11:437.
  13. Treasure R.L., Seaworth B.J. Current role of surgery in Mycobacterium tuberculosis. Ann Thorac Surg 1995;59:1405-1409.[Abstract/Free Full Text]
  14. Pomerantz M., Brown J. The surgical management of tuberculosis. Sem Thorac Cardiovasc Surg 1995;7:108-111.[Medline]
  15. Kir A., Tahaoglu H., Okur E., Hatipoglu T. Role of surgery in multidrug resistant tuberculosis: results of 27 cases. Eur J Cardiothoracic Surg 1997;12:531-534.[Abstract]
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