Ann Thorac Surg 1996;62:218-223
© 1996 The Society of Thoracic Surgeons
Original Articles: General Thoracic
Open Drainage of Massive Tuberculous Empyema With Progressive Reexpansion of the Lung: An Old Concept Revisited
Sohaila Mohsin Ali, MD,
Abdul Aziz Siddiqui, MD,
Joseph S. McLaughlin, MD
Department of Surgery, Aga Khan University, Karachi, Pakistan
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Abstract
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Background. This study examined the results of open drainage of massive tuberculous empyema.
Methods. During a 7-year period 47 patients with primary mixed chronic tuberculous empyema with near or total lung collapse were treated. The initial procedure was chest tube suction drainage, which permitted evaluation of the pleural cavity and the lung parenchyma despite minimal if any reexpansion of the lung. All patients were treated with antibiotics and multidrug regimens of antituberculosis agents. A pleurocutaneous window was established by removing sections of two ribs one intercostal space above the base of the pleural cavity. Irrigation was performed daily with dilute povidone iodine solution.
Results. Twenty-eight patients achieved complete reexpansion of the lung after 4 to 30 months of drainage and are cured. Eleven are in various stages of reexpansion and probably will be cured. Eight patients did not achieve reexpansion. Criteria were established retrospectively on an ongoing basis that indicate when pulmonary reexpansion is possible.
Conclusions. These totally collapsed "entrapped" lungs expanded to fill the entire pleural space despite the presence of bronchopleural fistulas and an "open" pleura. Reexpansion was progressive, gradual, and dependent on improved compliance, clearing of bronchial inflammation and obstruction, and pleural cleansing. Criteria are established that identify those patients in whom complete reexpansion may take place and the disease may be cured.
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Introduction
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See also page 223.
In 1935, Leo Eloesser [1] described an operation for drainage of tuberculous empyema in which a portion of rib was resected and a cutaneous flap was constructed. He noted that reexpansion of the lung occurred, but not in those lungs that had undergone cavitation and fibrosis. He wrongly attributed this reexpansion to the cutaneous flap, which he thought acted as a valve and produced negative pressure in the chest when the patient coughed or expired, but he noted the paradox of this concept. Subsequently there have been anecdotal reports of lung reexpansion with open drainage. This series confirms Eloesser's and later observers' findings, extends this concept to include patients with bronchopleural fistula, and provides an explanation for this phenomenon.
In December 1987 a 26-year-old mother of six presented to the Liaquat National Hospital in Karachi, Pakistan, with massive mixed tuberculous empyema (Fig 1
). She had been treated with antituberculosis therapy and multiple thoracocenteses in the tribal area of northern Pakistan for 2 years. Reportedly at least a liter of purulent material had been drained at 6-month intervals. She was acutely and chronically ill with a massive left pleural empyema, gross inflammation of the left second and third costochondral joints, and abdominal tuberculosis with ascites. The Mantoux test was positive. Cultures of the chest fluid grew Pseudomonas and ascitic fluid was culture positive for Mycobacterium tuberculosis.
A chest tube was inserted and she was treated with appropriate antibiotics and a four-drug regimen of antituberculosis agents. A chest roentgenographic examination showed the lung to be collapsed against the mediastinum. Within a month her condition improved: her fever subsided, the costochondral infection regressed, ascites and partial bowel obstruction resolved, and she began to eat and gain weight. She was considered fit for discharge; however, the lung had not expanded despite application of continuous suction to the chest tube. At 4 months the chest tube was cut off and converted to an "empyema tube" (Fig 1B
). By June 1988 the patient was markedly improved and plans were made to perform a decortication and possible lung resection, but the patient refused. Accordingly a pleurocutaneous fistula was established (Fig 1C
). The patient was instructed to irrigate the pleural space twice daily with dilute povidone iodine solution. She was seen on a monthly or bimonthly basis until June 1989, when she returned to the northern area with a mature, draining pleurocutaneous window. In October 1989 she returned to Karachi because of mild bleeding from the fistula site. A chest roentgenographic ray examination revealed complete reexpansion of the lung (Fig 1D
). The lung surface seen through the chest wall opening was covered with granulation tissue; subsequently this area epithelialized.
The foregoing experience led to the treatment by open drainage of 46 similarly affected patients who had massive mixed tuberculous empyema with collapsed and "entrapped" lung. Twenty-eight patients have experienced complete reexpansion of their lungs and are cured and 11 are in various stages of reexpansion and presumably will be cured. This experience is out of the ordinary, and the open elective treatment of mixed tuberculous empyema with total or near-total collapse and "entrapment" of the lung followed by complete reexpansion is presented together with a concept of the pathophysiology of this disorder and the response to therapy.
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Material and Methods
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Patients
During a 7-year period from December 1987 through May 1995, forty-seven patients were evaluated and treated for chronic mixed tuberculous empyema. These patients ranged in age from 9 to 68 years. Twenty-six were male and 21 were female. Thirty-eight were being treated with antituberculosis drugs. Three had not been treated previously. The current drug status of the remaining 6 was unknown, although 3 of these had received therapy in the past.
Culture Status
Positive cultures for M tuberculosis were forthcoming in 24 patients. The 23 remaining patients had strong presumptive evidence of tuberculosis including at least three of the following: strong family history of tuberculosis, chronic low-grade fever, positive Mantoux test, high erythrocyte sedimentation rate, "typical" appearance of endobronchial tuberculosis on bronchoscopy, and radiologic evidence of tuberculosis in the contralateral lung. In addition 28 had positive cultures of nontubercular organisms, most commonly Pseudomonas aeruginosa, Klebsiella species, Enterobacter species, and combinations of Pseudomonas and Staphylococcus and Enterococcus species. All patients with negative cultures had received or were receiving antibiotics at the time the cultures were obtained.
Treatment
After initial evaluation patients were placed on a four-drug regimen of antituberculosis therapy. Four drugs were used routinely because of the significant incidence of resistance to INH and rifampicin in Pakistan. Chest tube drainage was carried out in those patients in whom this procedure had not been performed previously. Subsequently a modified Eloesser procedure was performed by removing 7.5-cm segments of two ribs anterior to the midaxillary line, one intercostal space above the most dependent part of the empyema cavity [1]. The skin was affixed to the thickened parietal pleura with interrupted absorbable sutures. These openings initially measured 5 x 5 cm but contracted to half of the original size as maturation took place. No window required revision. Irrigation was performed with 300 to 500 mL of dilute povidone iodine solution (5 mL of povidone iodine solution to 500 mL of normal saline solution or boiled water) twice daily. The patients were instructed to lie on their sides during this lavage unless a bronchopleural fistula was present, in which case the irrigation with a 50-mL syringe was performed sitting or standing up. Bronchopleural fistulas often were identified by the patient because of coughing and an iodine taste during the irrigation. Antituberculosis drug therapy was continued for a minimum of 9 months and for at least a month after complete reexpansion of the lung. Antibiotics were administered until drainage became minimal. It should be noted that none of these patients became completely sterile for nontuberculosis bacteria. If drainage increased cultures were again obtained and antibiotic administration reinstituted.
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Results
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Group I
Twenty-eight patients experienced complete reexpansion of the lung from 4 to 30 months after open drainage. The majority of these patients presented with complete collapse of the lung against the mediastinum, in many despite the presence of functioning chest tube suction. The others had minimal reexpansion from previously placed chest tube suction. In those patients who were treated for the first time by closed suction drainage minimal if any reexpansion occurred. Recollapse of minimally reexpanded lungs was common when closed tube drainage was converted to open drainage.
Group II
Eleven patients are responding to therapy and their lungs are in varying stages of reexpansion after 3 to 30 months of open drainage. A 14-year-old girl with nearly complete reexpansion and resolved contralateral pulmonary infiltrates is awaiting epithelialization of the exposed lung at 20 months.
Group III
Eight patients did not achieve reexpansion of the lung. These patients were generally older, had had tuberculosis for longer periods, and had organisms that were resistant to drug therapy; lung destruction with fibrosis, bronchiectasis, and pleural adhesions was the rule.
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Comment
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Current therapy of chronic mixed tuberculous empyema includes pleural drainage and appropriate drug therapy, including antituberculous drugs and antibacterial agents. When total or near-total collapse is present and expansion does not take place definitive operation is indicated. Because these lungs usually defy decortication in the traditional manner, lung resection, often pneumonectomy, is carried out. Thoracoplasty and myoplasty may be required. The morbidity and mortality in these circumstances is high [26].
The reasons for this lack of reexpansion of the lung once the purulent material is evacuated probably relate to multiple factors. We believe the most important of these are tuberculous pneumonia and endobronchial disease and obstruction. Thickened pleura may play a role as may frank fibrosis and cavitation, but these factors, although important, were present in a relatively smaller number of patients. Commonly at operation decortication is not feasible. A traditional peel is not present, the lung surface is inflamed and friable, bronchopleural fistulas often are present, and positive pressure is not successful in reexpanding the lung. Operative maneuvers result in pulmonary laceration, the production of additional fistulas and failure. Pneumonectomy often becomes the only option [7].
The presented treatment scheme addresses both the bronchial and parenchymal disease and the secondary pleural involvement. Key is the eradication of active tuberculosis and secondary bacterial infection by appropriate drug therapy and open pleural drainage. The resolution of parenchymal and bronchial disease allows the lung to reexpand, but this is a gradual process that may take many months (Table 1
). Pleural drainage and irrigation promotes elimination of the pleural infection and may prevent the formation of a thickened visceral pleura, which results in true entrapment.
The reexpansion of these lungs initially was a fortuitous finding and was unexpected with an open pleural space. Once recognized the treatment plan became formalized on an ongoing basis. Presently, initial treatment consists of chest tube drainage and appropriate antibiotic therapy. Clinically most patients will be relieved of shortness of breath with chest tube drainage. Radiographic and clinical appraisal of the affected lung for potential reexpansion is performed at this time. Paradoxically the most common finding indicating potential reexpansion is total collapse of the lung against the mediastinum (Figs 2, 3
). This indicates that the lung and pleura have not undergone fibrosis. Chest tube drainage may produce minimal reexpansion, in which case the lung parenchyma may be evaluated. A clear rim of parenchyma showing no cavitation or bronchiectasis implies the potential for reexpansion. Cavitation and fibrosis, often with pleural adhesions, bode poorly for reexpansion. A fibrotic lung that does not totally collapse and on which thickened pleura can be identified probably will not respond. Those patients in whom a nonproductive cough persists on the basis of bronchial involvement will usually have reexpansion. In contrast, those patients in whom a productive cough persists on the basis of cavitary disease usually will not have reexpansion of their lung.
In the earlier stages of this series, chest tube drainage was continued for several months. Presently open drainage is instituted at a much earlier stage, often within the first month after establishing the lack of expansion on suction drainage and assuring that mediastinal shift will not take place. Chest tube drainage is bothersome, is often painful, does not provide efficient drainage, and does not conveniently allow mechanical cleansing of the pleural space. Open drainage is well tolerated. Patients rapidly learn to irrigate their pleural cavity, and both the patient and the family feel they are important participants in the management of this condition. Although the treatment process is prolonged, the patient experiences progressive well being.
This treatment scheme has been successful in 28 patients and probably will be successful in the 11 others who have demonstrated partial reexpansion as early as 3 months after open drainage. Eight patients did not achieve expansion of their lungs despite open drainage. Infection was controlled in all but 1, who died of uncontrolled drug-resistent tuberculosis within 1 month. Five of these patients were treated successfully by pneumonectomy and 1 awaits pneumonectomy. The last patient died of a brain tumor after 5 years of satisfactory palliation with open drainage.
Evarts Graham described the mechanism of lung reexpansion in patients with open drainage for bacterial empyema treated during the influenza pandemic of 1918. They attributed this reexpansion to the "gradual pull of adhesions between the lung and the chest wall" [8]. Such has not been the experience with tuberculous empyema, where lack of expansion has led to decortication, lung resection, and thoracoplasty. With modern antituberculous drug therapy the pulmonary and bronchial components are controlled and the lung becomes capable of reexpansion.
The pathophysiology of this process is unusual. The exact mechanism is speculative, but certain factors seem clear. As the antituberculosis therapy eradicates the parenchymal disease, lung compliance is improved. Parenthetically, with the clearing of bronchial infection and obstruction, aeration becomes possible. The granulating lung surface adheres to the parietal pleura and gradually pulls the lung outward in a progressive manner. This continues until complete reexpansion of the lung takes place. This process occurs in the face of continued atmospheric pressure and has occurred in patients in whom unclosed bronchopleural fistulas persist, which close as they are sealed by granulation tissue against the chest wall. The final phase is epithelialization of the exposed lung and contraction of the chest wall defect. Of interest is the fact that these skin-lined fistulas heal completely. No patient has required revision of the skin-lined defect, which remains as a large epithelialized dimple.
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Footnotes
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Presented at the Thirty-second Annual Meeting of The Society of Thoracic Surgeons, Orlando, FL, Jan 29-31, 1996.
Address reprints requests to Dr Ali, Division of Thoracic and Cardiovascular Surgery, University of Maryland Medical Center, 22 S Greene St, Baltimore, MD 21201.
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References
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- Eloesser L. An operation for tuberculous empyema. Surg Gynecol Obstet 1935;60:10967.
- Langston HT, Barker WL, Graham AA. Pleural tuberculosis. J Thorac Cardiovasc Surg 1967;54:5119.[Medline]
- Samson PC. Empyema thoracis: essentials of present day management. Ann Thorac Surg 1971;11:21021.[Medline]
- Hankins JR, Miller JE, McLaughlin JS. The use of chest wall muscle flaps to close bronchopleural fistulas: experience with twenty-one cases. Ann Thorac Surg 1978;25:4919.[Abstract]
- Ninvivo J, Brandolino M. Rare infections in thoracic surgery. In: Pearson FG, Deslauriers J, Ginsberg RJ, et al, eds. Thoracic surgery. New York: Churchill Livingston, 1995:1062-4.
- Hood RM, Antmank Boyd A, et al. Pleural infection in surgical disease of the pleura and chest wall. Philadelphia: Saunders, 1986:78-181.
- Odell JA. Pleural tuberculosis. In: Deslauriers J, Lacquet LK, eds. International trends in general thoracic surgery. Vol 6. Surgical management of pleural disease. St Louis: Mosby, 1990:459-68.
- Graham E, Singer J, Ballon H. Surgical diseases of the chest. Philadelphia: Lea & Febiger, 1935:118-81.
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Discussion
Ann. Thorac. Surg. 1996 62: 223-224.
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