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Ann Thorac Surg 1995;60:888-895
© 1995 The Society of Thoracic Surgeons


Original Articles: General Thoracic

Decortication Is a Valuable Option for Late Empyema After Collapse Therapy

Gilbert Massard, MD, Clotilde Rougé, MD, Jean-Marie Wihlm, MD, Soltan Ameur, MD, Ahmad Dabbagh, MD, Romain Kessler, MD, Norbert Roeslin, MD, Georges Morand, MD

Department of Thoracic Surgery, University Hospital of Strasbourg, Strasbourg, France


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background. Infection of previous collapse therapy spaces may raise challenging problems. This study evaluated a conservative surgical approach based on decortication.

Methods. Since 1979, 28 patients (mean age, 60 ± 6 years) have presented at an average of 37 ± 7 years after artificial pneumothorax for tuberculosis. Diagnosis of empyema was made on follow-up in 12 patients and on symptoms in 16 patients. Mean vital capacity was 66% ± 16% of normal. Microorganisms were isolated in 13 patients (Aspergillus fumigatus in 5, Mycobacterium tuberculosis in 4, anaerobes in 4). Decortication was made in 24 patients, associated with thoracoplasty in 4, and with partial lung resection in 2 patients. Thoracoplasty alone was performed in 2 patients, and 2 patients underwent an extrapleural pneumonectomy.

Results. Both extrapleural pneumonectomies were complicated with empyema requiring thoracoplasty, resulting in one postoperative death. Operative mortality after decortication was nil. Mean intraoperative blood loss during decortication was 1,830 ± 1,310 mL. All patients were extubated within 24 hours, except 1 patient who was ventilator-dependent preoperatively. Prolonged air leaks were common (mean duration of drainage, 16 ± 11 days), but ultimately sealed. Existence of symptoms was predictive of prolonged air leaks (p < 0.01).

Conclusions. We conclude that decortication may provide a one-stage cure avoiding the hazards of extrapleural pneumonectomy; the nonfunctioning remaining lung may resolve the space problem.


    Introduction
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 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
See also page 895.

Collapse therapy was the only resource against pulmonary tuberculosis before the advent of antituberculous chemotherapy. Various surgical methods had been designed to collapse the excavated lung; these treatments permitted a stabilization of tuberculosis in many patients, and sometimes a permanent cure.

The most current treatment was intrapleural pneumothorax. Once the pneumothorax had been created, repeated insufflations had to be performed at a 2-week interval to maintain the collapse. Pleural adhesions developed frequently, and were usually taken down by thoracoscopy [1]. When extensive adhesions precluded intrapleural pneumothorax, extrapleural pneumolysis was performed through a short posterior thoracotomy; the collapse was maintained with repeated instillations of air into the extrapleural space [2, 3]. These frequent injections of air required for any type of artificial pneumothorax represented a considerable burden to the patients, and undoubtedly predisposed to empyema. Therefore, a continuing search for substances other than air to fill the space took place over the years. Eventually, plombage procedures, designed to permanently maintain the collapse with a one-stage procedure, became popular; they were mainly used between 1948 and 1955 [4]. However, extrapleural plombage was regularly complicated by erosion of the lung, whatever the material used. Hence extraperiosteal pneumolysis was preferred, because the plomb was facing a thicker base, which became even tougher with subsequent ossification. The extraperiosteal space was created by stripping the periosteum and intercostal muscles off the ribs through a thoracoplasty incision, and the collapse was maintained by the filling material inserted within the denuded rib cage [5]. The final appearance is well described by the nickname of ``bird-cage operation.''

Extraperiosteal plombage avoided thoracoplasty and its physical sequelae. However, thoracoplasty was still required in some cases and was even combined with plombage in patients with sparse muscles, achieving the so-called mixed collapse [6].

The era of collapse therapy ended around 1960. Most surgeons and physicians familiar with its early and long-term complications have retired. Furthermore, the rare patients still living with long-term sequelae are at best in their sixties and combine at least two risk factors, namely age and poor respiratory function. Therefore, we felt that there was a need to review this very particular problem over a recent time period. The purpose of this study was to analyze late exudative complications occurring after intrapleural and extrapleural pneumothoraces, and to evaluate a therapeutic approach giving privilege to decortication whenever feasable.


    Patients and Methods
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Patients
From January 1, 1979, to July 1, 1994, we dealt with 28 consecutive patients presenting with a presumed late empyema after collapse therapy for tuberculosis. These were 24 men and 4 women, with a mean age of 60 ± 6 years (range, 49 to 71 years; median, 61 years). Intrapleural pneumothorax had been performed in 23 patients, and extrapleural pneumothorax in 5 patients; 12 were right-sided and 16 left-sided. The mean anteriority of collapsotherapy was 36.8 ± 7.8 years (range, 26 to 57 years; median, 34 years) (Table 1Go).


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Table 1. . Patient Characteristics
 
Methods
Patient charts were reviewed for operative report, intraoperative and postoperative bleeding, duration of suction drainage, and duration of hospital stay. Any postoperative complication was taken into account. Microbiology studies screened routinely for aerobes, anaerobes, mycobacteria, and fungi.

In patients having undergone a single decortication, intraoperative bleeding and duration of postoperative drainage were compared between subgroups: symptomatic versus asymptomatic patients; microbiologically positive versus negative patients.

Statistics
The {chi}2 test, Student's t test, and correlation analysis were used when appropriate. Statistical significance was admitted for any value of p less than 5%.


    Results
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 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Clinical Presentation
A diagnosis of late empyema was made on follow-up in 13 asymptomatic patients, who showed a recent change of their pleural sequelae on chest roentgenograms. Another 15 patients complained of single or combined symptoms including fever (n = 7), increasing shortness of breath (n = 5), pain (n = 2), hemoptysis (n = 3), and relentless cough (n = 1). A single patient presented with a spontaneous fistulization to the skin. Chest roentgenograms disclosed a more or less pronounced swelling of the pleural pocket in 22 patients (Figs 1 and 2GoGo), and an air-fluid level suggestive of a bronchopleural fistula in 6 patients.




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Fig 1. . Exudative complication 37 years after artificial intrapleural pneumothorax. (A) Preoperatively, the chest roentgenogram showed a large pleural opacity with mediastinal compression. (B) Result 6 months after decortication is satisfactory.

 



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Fig 2. . Exudative complication arising 32 years after creation of an extrapleural pneumothorax. (A) Preoperative chest roentgenogram discloses an exudative complication in a former extrapleural collapse space, typically presenting as a protruding apical pleural mass. (B) Follow-up chest film 6 months after decortication.

 
Preoperative respiratory function studies showed a global restrictive insufficiency, with a mean vital capacity at 66% ± 16% of normal (range, 36% to 103%; median, 67%). Seven patients had a normal vital capacity, more than 80% of predicted; restriction was mild in 11 patients (60% to 80% of predicted) and severe in 10 patients (less than 60% of predicted). Expiratory flow was satisfactory in most patients; the mean ratio of forced expiratory volume in 1 second to vital capacity was 66.9% ± 9.2% (range, 45% to 85%); obstruction with a ratio of less than 60% was present in 5 patients. Lung perfusion scan was available in 24 patients and showed a mean perfusion rate of 23.7% ± 15.3% on the injured side (range, 0% to 56%; median, 26%) (Table 1Go).

Operative Procedure
Tube thoracostomy and preoperative pleural lavages were made in 15 patients; in 10 patients, the lavages were made deliberately during 1 to 4 weeks in expectance of a decortication. In the remaining 5 patients, operation was indicated mainly because of a failure of conservative management with lavages.

An attempt at decortication was made in every patient. Isolated decortication was the only treatment in 18 patients. In 4 patients, the underlying lung appeared too stiff to reexpand satisfactorily, and a four- to six-rib thoracoplasty was added. In 2 patients, simultaneous partial lung resection was performed: 1 patient underwent right lower lobe resection for bronchial fibrostenosis and 1 patient underwent resection of the apical segment of the left lower lobe for bronchopleural fistula. Extrapleural pneumonectomy was made on two occasions for completely destroyed and inexpandable lungs. Two patients, in whom decortication was technically impossible because of extensive calcifications, underwent a seven-rib thoracoplasty (Table 2Go).


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Table 2. . Operative Procedures and Results
 
Microbiology and Pathology
Microbiologic expertise of pleural tap or intraoperative specimens was negative in 15 patients. Four patients were positive for Mycobacterium tuberculosis, 5 for Aspergillus fumigatus, and 4 for pyogenes (anaerobes in 3 and gram-negative bacteria in 1 patient). Further, microbiology was negative in 3 of 7 patients with fever, and in 4 of 6 patients with an air-fluid level on chest roentgenogram (Table 2Go).

Pleural tap disclosed a sterile hemorragic effusion in 2 patients on coumadin presenting with an acute swelling of their pleural pocket. One of them was operated on immediately. The second patient had a chronic respiratory failure and was on ventilator; operation was not considered a reasonable option and a chest tube was inserted. However, a secondary infection of the pleural effusion led to an operative intervention 18 months later.

Two incidental carcinomas were discovered during decortication. The first patient had disseminated pleural lesions, corresponding to an indifferentiated carcinoma. Another patient had a peripheral upper lobar mass believed to be scar tissue, which was wedged out by staple resection. However, at pathologic examination this lesion was shown to be an adenocarcinoma, and a regular lobectomy was performed 2 months later.

Postoperative Complications
Although there was no operative death according to the generally accepted definition (30 days or initial hospital stay), 1 death is related to treatment. This patient underwent an extrapleural pneumonectomy complicated with empyema. Management with ambulatory lavages failed and an eight-rib thoracoplasty was done 10 weeks later. Peridural analgesia made for intractable pain was complicated with acute urine retention requiring a suprapubic catheter insertion. This final procedure led to an ileal injury, treated with emergency laparotomy and ileal resection. The patient succumbed eventually to a respiratory distress syndrome 17 days after laparotomy and 113 days after extrapleural pneumonectomy.

The severity of operation in these patients is suggested by a prolonged mean hospital stay of 28 ± 19 days (range, 12 to 110 days), exceeding 30 days for 8 patients. Most procedures were technically difficult, because large calcifications had occurred (Fig 3Go). Mean intraoperative blood loss was 1,830 ± 1,310 mL (range, 300 to 5,000 mL). Postoperative bleeding during the first 24 hours averaged 1,150 ± 396 mL (range, 360 to 2,000 mL). However, no patient required reexploration for persistent bleeding.




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Fig 3. . Pleural calcifications. (A) Computed tomographic scan shows a bulky and calcified pleural pocket. (B) Roentgenographic analysis of the decortication specimen shows several layers of calcified material.

 
Respiratory failure with need for permanent mechanical respiratory support persisted in a single patient, who was ventilator-dependent preoperatively. Twenty-one patients were extubated within 6 hours after the procedure, and the remaining 6 patients were extubated during the initial 24-hour period.

Prolonged air leaks were a common problem. Mean duration of drainage was 16 ± 11 days (range, 2 to 54 days); 15 patients were still drained 2 weeks postoperatively. Basically, chest tubes were left in until air leaks were completely sealed, and were withdrawn when no pleural space reappeared after 1 to 2 days of clamping. Two patients required pneumoperitoneum to seal their air leaks. Two patients had a residual pleural space, which resolved with tube thoracostomy in 1 patient, and required thoracoplasty in 1 patient.

Complications With Reference to the Surgical Procedure
Isolated decortication was well tolerated. One patient had pleural space disease postoperatively requiring thoracoplasty (5.5%); 1 patient had acute bleeding of a duodenal ulcer requiring emergency operation. Because in 17 patients the pleural space was sealed at removal of chest tubes, the result of the operation was satisfactory in 94.5% of cases.

Partial lung resection combined with decortication, performed in 2 patients, was well tolerated. However, 1 patient had prolonged air leaks with drainage until postoperative day 22.

Three patients suffered complications after decortication with immediate thoracoplasty: parietal sepsis, space disease treated with tube thoracostomy, and gastric ulcer bleeding in 1 patient each.

Both patients undergoing isolated thoracoplasties did well. One of these patients was ventilator-dependent preoperatively, and still required mechanical respiratory supply postoperatively.

Both patients undergoing extrapleural pneumonectomies suffered postoperative empyema; control of infection required a large thoracoplasty in both patients.

Potential Risk Factors for Isolated Decortication
Existence of symptoms and positivity for microorganisms were presumed to be an indicator of both operative difficulties and postoperative complications. The 18 patients who underwent isolated decortications were assigned to subgroups according to these criteria and compared. Operative bleeding was taken in account as an indicator of technical difficulty, and duration of postoperative drainage time was considered as indicator of postoperative complications.

In symptomatic patients, bleeding was not a significant factor when compared to asymptomatic patients; on the other hand, duration of postoperative drainage was twice as long as in asymptomatic patients (Table 3Go).


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Table 3. . Postoperative Prognosis: Comparison of Symptomatic Versus Asymptomatic Patients
 
Patients from whom cultures grew microorganisms did not bleed significantly more than the others; there was a trend toward prolonged air leaks, which was not statistically relevant (Table 4Go).


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Table 4. . Postoperative Prognosis: Comparison of Microbiologically Positive Versus Negative Patients
 
Neither vital capacity nor percentage of perfusion on nuclear scan were related to intraoperative or postoperative problems (Table 5Go).


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Table 5. . Postoperative Prognosis: Correlation Analysis
 
Long-term Results
All 27 operative survivors have been seen at our outpatient clinic at 3 months after discharge. The final result was satisfactory in all patients in that there were neither residual pleural space disease nor signs of sepsis in any patient. Twenty-six patients have been seen at 6 months and were stable; the final patient had died at 5 months with metastatic bronchial carcinoma incidentally discovered during decortication. A complete follow-up, ranging from 6 to 180 months, is available for 11 patients. Two patients died, one at 9 months of pleural cancer and one at 52 months of congestive heart failure; and 9 patients are still doing well. A further 7 patients were followed up for 12 to 44 months, and follow-up was discontinued for various reasons independent from their original illness; all 7 were stable at the latest checkup. The remaining 8 patients have been followed-up by their referring pulmonologist; no case of infectious relapse were found.


    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
A recent increase of pleural sequelae in a patient previously treated with artificial pneumothorax is generally attributed to an infected pleural effusion. Although infection has been hypothesized in all 28 patients of this series, only 13 proved to be infected by microbiologicals. In particular, 3 patients with fever and 4 patients with radiologic evidence of bronchopleural fistula had negative samples. This surprising observation has been made previously by other researchers [7]. Two explanations are possible: either the infective agent does not grow at culture or the radiologic modification is related to an exudative reaction to a parenchymal infection, which may have resolved at the time of diagnosis [7]. One might anticipate that most late infections should be correlated to relapsing tuberculosis in these patients, who had never received major antituberculous drugs. However, the incidence of tuberculous empyema is surprisingly low: 4 of 28 patients in this experience, and 1 of 15 patients reported by Schmid and De Haller [7]. In fact, previous series demonstrated that tuberculous empyema was a rather usual early complication of collapse therapy, but did not contribute significantly to the late morbidity [8]. Bronchopleural fistulas resulting from pleural perforation of a caseous lesion or erosion by a common infection create the ideal microclimate for colonization with Aspergillus fumigatus [9, 10]. However, the risk for aspergillisation has probably been overestimated. In this report, the incidence was as low as for tuberculous empyema; furthermore, only 2 of 6 patients with obvious bronchopleural fistula did grow Aspergillus on cultures. Pleural infection with common pyogenes may result either from contamination with a bronchopleural fistula or from bacterial seeding during intrapleural manipulations such as repeated thoracenteses.

Empyema is not the only possible diagnosis, and infection may be discarded when pleural tap is frankly hemorragic. Hemorragic effusions have been described with pleural or pulmonary malignancies arising in collapse therapy spaces [11, 12]. In this series, we observed 2 patients with malignant change (7%). The incidence is sufficiently high to be kept in mind intraoperatively; any suspect lesion should be sent for frozen section analysis intraoperatively. Spontaneous pleural bleeding had occurred in 2 more patients who were receiving warfarin; to our knowledge, this type of complication has rarely been reported [13].

The main problem with late complications of artificial pneumothorax is to define an appropriate treatment plan. Whereas Schmid and De Haller [7] recommend conservative management, we perform decortication liberally. Our postoperative results show that it is a reasonable option. Prolonged postoperative drainage should not be an argument against a one-stage cure with excellent long-term results. We believe that Schmid and De Haller's criteria for decortication are too restrictive, as this procedure has been demonstrated to be feasable even in poor risk patients. In 1976, Personne and colleagues [14] reported on a series of 53 patients with a preoperative forced expiratory volume in 1 second of less than 1,000 mL. Only two operative deaths occurred, and an easy outcome was observed in 84%. Although treatment is mandatory in symptomatic patients by any means, our results demonstrate that the operative risk is lowest, in terms of bleeding and air leaks, in asymptomatic patients and in patients with sterile cultures. Therefore, we recommend to proceed with decortication in the latter patients as a first choice option, rather than wait for symptoms to appear and operate with an increased risk. There is an analogy to the treatment plan we proposed for aspergilloma [10].

The operative technique of decortication does not need to be extensively described. Anesthesia with a double lumen catheter is mandatory to prevent intraoperative flooding of the opposite lung when a bronchopleural fistula is suspected. A large posterolateral thoracotomy with resection of the fifth or sixth rib is necessary for adequate access. Parietal decortication has to progress up to the pleural reflexions close to the spinal gutter, the anterior mediastinal recess, and the costodiaphragmatic junction. At times considerable strength has to be developed to mobilize calcified peels. Bleeding must be anticipated; intraoperative use of aprotinin might be beneficial. When the cleavage with the lung is not easily found, the pocket should be entered to discover the convexity of the lung; the pleural peel may then be excised in several steps. Pleural reflexions may be left behind. Two to three chest tubes are inserted at the end of the operation and put to vigorous suction as air leaks seal when the apposition of pleural surfaces is restored. Adjuvant therapy should include antituberculous drugs when Mycobacterium tuberculosis has been evidenced, or itraconazole when Aspergillus superinfection occurs. Antibiotics are given either as perioperative prophylaxis or according to sensitivity studies when cultures are positive. Aggressive physiotherapy is of paramount importance.

Reexpansion does not rely on the duration of collapse therapy, but on the state of the underlying lung [8, 15]. However, there is a lack of criteria to estimate the potential of reexpansion preoperatively. Absence of perfusion on lung scan may be an indicator of a completely destroyed lung. Computed tomographic scan may help to analyze the remaining parenchyma, but our experience is very limited in this domain.

Functional improvement after decortication is debated, and previous studies are controversial [14, 16]. We do not believe in restoring any function. The main aim of decortication is to reexpand the lung and completely fill the pleural space to cure the empyema; the native lung acts merely as a natural prosthesis.

Some alternatives to decortication should be discussed. Conservative management relies either on repeated thoracenteses or on external drainage. Repeated thoracenteses are a burden and may be technically hazardous in thickened and calcified pleurae. Drainage with tube thoracostomy is pure palliation, reexpansion of the lung is impossible because of a stiffened pleura, lavages may lead to troublesome bleeding, and suction may be painful. Open window thoracostomy cleans out a sepsis, but is not a satisfactory long-term solution as it leads to prolonged treatments and repeated hospital stays. A final step with thoracoplasty or muscle plombage is often asked for by the patient.

Really curative alternatives are thoracoplasty and extrapleural pneumonectomy. Extrapleural pneumonectomy might be the choice of an inexperienced surgeon who is unaware of the possibilities of a careful decortication. Excision of both the infected cavity and the underlying lung is an ideal plan theoretically, but this major procedure carries a high complication rate [10]. Therefore, we recommend that extrapleural pneumonectomy be avoided by any means. Thoracoplasty without any attempt at decortication requires an extensive procedure, removing seven to nine ribs to completely collapse the cavity. This aggressive procedure is certainly superior to the harm of a decortication. Hence, thoracoplasty alone should be precluded, except when parietal decortication is technically impossible through extensive ossifications, as we encountered twice. On the other hand, thoracoplasty is a most valuable adjuvant to decortication when reexpansion of the lung is incomplete. However, the final result is difficult to anticipate, as the mediastinum and diaphragm may shift generously and contribute to a complete filling of a hemithorax with a small native lung. Therefore, it is advisable to give a try to decortication alone, and to defer a limited thoracoplasty to a second stage whenever really necessary.

We conclude that decortication is safe in terms of mortality and morbidity, and may be performed in patients with a poor functional reserve. Excellent results on pleural space disease may be anticipated. However, prolonged air leaks are likely, especially in symptomatic and obviously infected patients. The functional value of the reexpanded lung is debatable, but one should keep in mind that the main purpose of decortication in this indication is to use the native lung as a ``natural prosthe-sis'' to fill the pleural space and thus to avoid extrapleural pneumonectomy.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Presented at the Poster Session of the Thirty-first Annual Meeting of The Society of Thoracic Surgeons, Palm Springs, CA, Jan 30-Feb 1, 1995.

Address reprint requests to Dr Massard, Department of Thoracic Surgery, University Hospital of Strasbourg, 1 place de l'Hopital, F-67091 Strasbourg, France.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Dumarest J, Mollard H, Lefevre P, Germain J. La pratique du pneumothorax thérapeutique. Paris: Masson, 1945.
  2. Le Foyer P, Delbecq E. Principes et mode d'action du pneumothorax extra-pleural. Traité du pneumothorax extra-pleural. Paris: G. Doin, 1950:3-33.
  3. Roberts ATM. Extrapleural pneumothorax: a review of 128 cases. Thorax 1948;3:166–73.
  4. Shepherd MP. Plombage in the 1980s. Thorax 1985;40:328–40.[Medline]
  5. Wilson NJ, Armada O, Vindzberg WV, O'Brien WB. Extraperiosteal plombage thoracoplasty: operative technique and results with 161 cases with unilateral surgical problems. J Thorac Surg 1956;32:797–819.
  6. Lucas BGB, Cleland WP. Thoracoplasty with plombage: a review of the early results in 125 cases. Thorax 1950;5:248–56.[Medline]
  7. Schmid FG, De Haller R. Late exudative complications of collapse therapy for pulmonary tuberculosis. Chest 1986;89:822–7.[Abstract/Free Full Text]
  8. Neff TA, Buchanan BD. Tension pleural effusion: a delayed complication of pneumothorax therapy in tuberculosis. Am Rev Respir Dis 1975;111:543–8.[Medline]
  9. Krakowka P, Rowinska E, Halweg H. Infection of the pleura by Aspergillus fumigatus. Thorax 1970;25:245–53.[Medline]
  10. Massard G, Roeslin N, Wihlm JM, Dumont P, Witz JP, Morand G. Pleuro-pulmonary aspergilloma: clinical spectrum and results of surgical treatment. Ann Thorac Surg 1992;54:1159–64.[Abstract]
  11. Harland RW, Sharma M, Rosenzweig DY. Lung carcinoma in a patient with lucite sphere plombage thoracoplasty. Chest 1993;103:1295–7.[Abstract/Free Full Text]
  12. Willen R, Bruce T, Dahlstrom G, Dubiel WT. Squamous epithelial cancer in metaplastic pleura following extrapleural pneumothorax for pulmonary tuberculosis. Virchows Arch [A]1976;370:225-31.
  13. Massard G, Wihlm JM, Roeslin N, Morand G. Extrapleural hematoma as a late complication of collapse therapy. Chest 1992;101:473–4.
  14. Personne C, Maurette M, Seigneur F, Toty L, Hertzog P. Décortications à haut risque fonctionnel. Rev Fr Mal Resp 1976;4:389–98.
  15. Petty TL, Filley GF, Mitchell RS. Objective functional improvement by decortication after 20 years of artificial pneumothorax for pulmonary tuberculosis. Am Rev Respir Dis 1961;84:572–8.[Medline]
  16. Patton WE, Watson TR, Gaensler EA. Pulmonary function before and at intervals after surgical decortication of the lung. Surg Gynecol Obstet 1952;95:477–96.[Medline]



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