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Ann Thorac Surg 1996;62:1026-1029
© 1996 The Society of Thoracic Surgeons


Original Articles: General Thoracic

Pleural Empyema: 24-Year Experience

Dov Weissberg, MD, Yael Refaely, MD

Department of Thoracic Surgery, Tel Aviv University Sackler School of Medicine, Tel Aviv, and E. Wolfson Medical Center, Holon, Israel

Accepted for publication May 20, 1996.


    Abstract
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 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background. Despite the widespread use of antibiotics, empyema remains a common and serious problem, and its treatment is controversial.

Methods. Our experience in 380 patients with empyema was retrospectively reviewed.

Results. The causes of empyema were as follows: pneumonia (n = 308), late complication of tuberculosis (n = 24), trauma (n = 15), pulmonary gangrene (n = 3), retained foreign body (n = 1), and undetermined (n = 29). An exudative state was diagnosed in 273 patients, a fibrinopurulent state in 55, and an organizing state in 52. Pleuroscopy was performed in 107 patients resistant to treatment, and this revealed an expansible lung in 49 patients, a nonexpansible lung in 51, and exceptional findings (foreign body, necrotizing pneumonitis, and perforated esophageal cancer) in 7. Treatment was modified accordingly. Five patients died (mortality, 1.3%).

Conclusions. Pleuroscopy is very helpful in disclosing factors responsible for resistance to treatment and in carrying out thorough pleural toilet. The use of talc in selected patients causes pleurodesis and prevents the reaccumulation of pus. Decortication is the ideal treatment in the organizing stage, enabling complete lung expansion. Fenestration is lifesaving in moribund patients who cannot tolerate decortication.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Despite the widespread use of antibiotics in the treatment of pulmonary infections and in patients who undergo operations involving the chest, empyema remains a serious problem. Its management is often controversial and varies depending on the stage of empyema, the duration of the process, the thickness of the exudate, the presence of loculations, the condition of the patient, and the personal experience of the surgeon. This retrospective review of our experience reflects the changing trend in the management of bacterial nontuberculous empyema over the past 24 years.


    Patients and Methods
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Between August 1971 and December 1994, 380 patients (235 male, 145 female) with bacterial nontuberculous empyema were admitted to our department. The age ranged from 16 to 84 years (median, 58 years). The empyema in 24 patients occurred as a late complication of previous intrapleural procedures performed for the management of pulmonary tuberculosis (oleothorax, paraffin or lucite ball plombage, therapeutic pneumothorax), but Mycobacterium tuberculous was not found to be a culprit pathogen in any of the present infections. Patients with postresectional empyema were not included. The causes of empyema are summarized in Table 1Go.


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Table 1. . Causes of Empyema
 
The disease was divided into three stages according to the classification of the American Thoracic Society [1]: exudative, with thin liquid, a low cellular content, and an easily expansible lung (273 patients); fibrinopurulent, with accumulations of pus, large numbers of polymorphonuclear leukocytes, fibrin and a tendency to form loculations and a membrane limiting lung expansion (55 patients); and organizing, with a thick fluid content and a well-formed fibrinous or fibrous membrane encasing the lung and preventing its expansion (52 patients). The predominant infecting organisms were Staphylococcus aureus, Staphylococcus epidermidis, Pseudomonas sp, pneumococcus, Klebsiella pneumoniae, Escherichia coli, Aerobacter aerogenes, Proteus sp, and various anaerobic organisms. Frequently, multiple microorganisms were present. No pathogenic organisms were identified in 27 patients.


    Results
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 Introduction
 Patients and Methods
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All patients were treated initially with tube thoracostomy drainage of the pleura and with antibiotics, chosen on the basis of the results of sensitivity studies, except in those patients in whom no pathogens were identified. This treatment was successful in 265 patients. No positive response was observed in the other 115. Early in the series, before the use of pleuroscopy was instituted, 2 patients in this group had undergone a seven-rib thoracoplasty; 6 others had undergone fenestration. As of 1975, the remaining 107 patients who had not shown a satisfactory response to treatment had undergone pleuroscopy for toilet, with the aspiration of all pus, and for identification of the causes of failure. All pleuroscopies were direct and involved the use of a mediastinoscope, as described in our earlier publications [2, 3]. The patients were divided into three groups on the basis of the findings noted at pleuroscopy (Fig 1Go).



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Fig 1. . Treatment algorithm for empyema. (CT = computed tomography.)

 
In the first group (n = 49) the empyema was in the exudative or early fibrinopurulent stage and the lung was fully expansible. Treatment with closed-tube thoracostomy and antibiotics was continued, with resolution of the empyema in 30 patients within the subsequent 2 to 3 weeks. All pathogenic organisms were eliminated in the remaining 19 patients, as the result of prolonged treatment with antibiotics. However, liquid continued to accumulate, even though consecutive cultures remained sterile. Talc was therefore insufflated, resulting in pleurodesis in all instances [4, 5].

In the second group (n = 51) the empyema was in the late fibrinopurulent or organizing stage. The lung was not expansible. Thirteen patients in this group had undergone decortication, resulting in complete expansion of the lung and recovery within 4 to 15 days (median, 8.3 days). The other 38 patients were septic and unable to tolerate a major operation. Twenty-six of these patients had a bronchopleural fistula; 20 patients were moribund. Fenestration of the pleura was performed in these 38 patients by resecting segments of two ribs together with intercostal muscles and suturing the skin to the parietal pleura. The infection was thus controlled in 36 of these patients, and the space became obliterated by granulation tissue [6]. The remaining 2 patients died.

The third group (n = 7) was a heterogeneous group of patients who had special problems. Three patients had necrotizing pneumonitis with secondary empyema. Their empyema was treated initially with antibiotics and pleural drainage, but eventually they underwent pleuroscopy, which disclosed pulmonary gangrene. There was also vascular thrombosis. Pneumonectomy was indicated in 2 patients and lobectomy in 1 but was postponed because of fulminating infection and the hazard of its causing mediastinitis. Fenestration was therefore performed as a preliminary to resection, followed after 7 days by resection and closure of the chest. All patients recovered without complications. Two patients had perforation of esophageal cancer. Treatment with antibiotics and closed-tube thoracostomy therefore had no effect, and several days elapsed before the esophageal perforation was diagnosed at pleuroscopy. Both patients died from sepsis and multiple-organ failure. Two patients had foreign bodies in the pleural cavity. One had undergone aortocoronary bypass 2 years earlier. His empyema did not resolve in response to treatment with antibiotics and pleural drainage. Pleuroscopy revealed a forgotten 30 x 30–cm laparotomy sponge. Removal of the foreign body resulted in prompt recovery. The other patient had accidentally swallowed a peach pit but remained unaware of the accident; several days later she was admitted to the hospital for evaluation of chest pain and fever. After 5 days, perforation of the esophagus was diagnosed and pleuroscopy disclosed the peach pit in the pleura. The patient was moribund, and despite vigorous treatment with antibiotics and tube thoracostomy drainage, she died as a result of sepsis and multiple-organ failure.

Altogether 5 patients died, all as a result of sepsis, for a mortality of 1.3%.


    Comment
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 Abstract
 Introduction
 Patients and Methods
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 Comment
 References
 
Empyema usually occurs as an extension of an infectious process, most commonly originating from the lung [7]. It can also occur as the result of complications of thoracic operations; bronchopleural fistula; infections in the mediastinum, under the diaphragm and in the spine; and penetrating trauma of the chest. Once fully developed, the original source of infection may be impossible to determine [8]. We could not determine the source of infection in 29 patients, constituting 7.6% of our study group. The bacterial flora in our series was similar to that reported for other series and did not influence the nature of management.

There are three strategies in the treatment of empyema. The first is to control the offending organism, which is usually identified by culture of the pus obtained by needle aspiration. Treatment with appropriate antibiotics can then be started. The second is to evacuate the contents of empyema. Initially this can be achieved by tube drainage. When empyema begins to organize, however, drainage alone becomes ineffective and toilet pleuroscopy may be necessary to aid in evacuation. Once the organizing stage becomes advanced, effective evacuation becomes impossible. The third strategy is to restore normal respiratory function by complete reexpansion of the lung. This is possible without operative intervention, as long as the organizing process has not started. Decortication is necessary once fibrosis has set in and the lung is encased in an armor of scar tissue. This involves the dissection and removal of the fibrous tissue that encases the lung, enabling the normal underlying lung tissue to expand. However, after a prolonged debilitating infection, many patients cannot tolerate such major intervention. Fenestration of the pleura can then be done to help to get rid of the infection and save the patient's life, but only with permanent loss of pulmonary function. Accordingly, the most important factor in the management of empyema is the stage of its development: it is relatively easy in the beginning but becomes more difficult with each advancing stage.

We found pleuroscopy an excellent aid in the evacuation of an empyema cavity. In addition, it is very helpful in determining the stage of empyema and the causes of resistance to treatment. Toilet pleuroscopy is, in essence, an extension of the basic treatment of empyema: evacuation of pus. It is particularly useful during the fibrinopurulent stage, when the organizing process begins and the pus is thick and mixed with semiorganized fibrin. This semisolid material resembling scrambled egg tends to plug the pleural tubes, interfering with drainage. However, at pleuroscopy, it can be fragmented and removed, together with pus, using a suction device and various types of forceps. When the empyema is multiloculated, the septa composed of fibrin also can be broken and removed in pieces. Tube drains are then inserted and left in place until all drainage ceases. Using this simple approach, thoracotomy can be avoided in the great majority of patients. However, there has been surprisingly little use of pleuroscopy in the evacuation of empyema contents. Ridley and Braimbridge [9] reported on 30 patients treated by pleuroscopic debridement followed by irrigation of the empyema cavity, with complete resolution in 18 (60%). More recently, O'Brien and associates [10] described their experience in 8 patients whose pleural empyema developed after penetrating chest trauma. These authors used video-assisted thoracoscopy for drainage and decortication and achieved complete resolution of empyema in all patients. The experience of both these groups lends strong support to the use of pleuroscopy (direct or video assisted) in the management of this problem.

Pleuroscopy aimed at determining the causes of resistance may reveal factors that were not suspected before the procedure. It has revealed some unusual causes of empyema in our patients, such as perforation of an esophageal tumor; foreign bodies in the pleural cavity, one left after an earlier operation and the other gaining entry as the result of a traumatic injury; and gangrene of the lung caused by a fulminant inflammatory process (see Table 1Go). In each instance, the findings influenced our therapeutic approach.

The ability of the lung to expand is the main factor in determining whether treatment of an empyema by drainage or pleuroscopy will suffice. Much of this information can be obtained from chest radiograms and computed tomographic scans [11, 12], but this is not always sufficient. A direct look at the pleura with simultaneous inflation of the lung in an effort to promote its expansion is much more informative.

If the diagnostic workup shows entrapment of the lung in an armor of fibrous tissue, decortication should be done to free the lung and bring about healing of the empyema. In this operation, we carry out the dissection in the extrapleural plane, between the parietal pleura and the endothoracic fascia. The entire parietal pleura is thus resected. The visceral pleura is not removed, only freed from the inflammatory peel adherent to it. Such dissection may cause tears in the lung, with some bleeding and air leaks, which, however, can be minimized by a combination of blunt and sharp dissection, using scalpel, scissors, and gauze pledgets. We personally dislike using electrocautery in this setting. The lung, released from its encasement, expands well upon inflation. Although one would logically expect an improvement in pulmonary function after this procedure, this has not been uniformly observed [13, 14].

The magnitude of decortication requires careful selection of patients. Ill, toxic patients are not suitable candidates [8, 15]. Of the 51 patients with a nonexpansible lung identified at pleuroscopy, only 13 could tolerate this procedure and the results were uniformly excellent. The remaining 38 patients with a nonexpansible lung were septic and debilitated and unable to tolerate decortication: 20 were moribund and 26 had a bronchopleural fistula. Fenestration was therefore selected as a less extensive operation, eradicating the sepsis in 36 of the 38 patients. It was also performed as a palliative measure in 2 patients with esophageal cancer. Although it eradicates sepsis, fenestration does not allow complete expansion of the lung, resulting in a restriction of respiratory function. This, however, must be accepted as a compromise for survival [6, 16, 17].

Pulmonary gangrene, an uncommon cause of empyema, occurs most often as a result of vascular thrombosis induced by the infecting organism [18] or aspiration [19]. Once established, the infectious process extends directly from the lung to the pleura, with fulminant empyema evolving rapidly. No treatment of empyema can succeed as long as the gangrenous lung remains in the pleural cavity. In fulminant empyema, however, the diagnosis of pulmonary gangrene can be missed easily, precluding effective treatment. This problem was clearly demonstrated in the 3 patients described here whose empyema did not respond to treatment, until pulmonary gangrene was diagnosed at pleuroscopy and effective therapy could be initiated. Empyema resulting from pulmonary gangrene must be treated aggressively. Anything less than thorough debridement of all necrotic tissue does not suffice [20]. Pulmonary resection was mandatory in our patients, but the dissection of hilar structures in the presence of pus could lead to mediastinitis. Fenestration was therefore performed as a preliminary measure, followed by thorough mechanical cleansing and packing with a bactericidal acid solution of sodium hypochlorite (Edinborough University Solution) every 12 hours for 7 days. Resection was then carried out in a clean field with immediate closure of the "window." Prompt recovery followed in all patients, demonstrating the value of aggressive therapy, as well as the occasional need for treatment in stages.

The mortality rate associated with streptococcal empyema during World War I ranged from 30% to 70% [21]. Many of the deaths were caused by pneumothorax and mediastinal instability, rather than by primary infection [15]. When this fact was recognized and prevented, and once antibiotics became available, the mortality associated with empyema declined sharply [22, 23]. In this series, 5 patients died, for a mortality rate of 1.3%. All deaths occurred as a direct result of sepsis and multiple-organ failure, and none could be prevented. Two of the deaths occurred in patients with perforated esophageal cancer. Metastatic spread had occurred in both, which undoubtedly contributed to the depression of their immunologic response.

We conclude that pleuroscopy should be used liberally in the management of empyema. It is helpful in disclosing factors responsible for resistance to treatment and in carrying out thorough pleural toilet. Persistent accumulations of liquid after its sterility has been proved by repeat cultures should be considered an indication for talc pleurodesis. Decortication is the ideal treatment in the organizing stage, enabling complete lung expansion. Fenestration is lifesaving in moribund patients who cannot tolerate decortication.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Address reprint requests to Dr Weissberg, E. Wolfson Medical Center, Holon 58100, Israel.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. American Thoracic Society. Management of nontuberculous empyema. Am Rev Respir Dis 1962;85:935–6.
  2. Weissberg D, Kaufman M, Zurkowski Z. Pleuroscopy in patients with pleural effusion and pleural masses. Ann Thorac Surg 1980;29:205–8.[Abstract]
  3. Weissberg D, Kaufman M. Diagnostic and therapeutic pleuroscopy. Experience with 127 patients. Chest 1980;78:732–5.[Abstract/Free Full Text]
  4. Weissberg D, Kaufman M. The use of talc for pleurodesis in the treatment of resistant empyema. Ann Thorac Surg 1986;41:143–5.[Abstract]
  5. Weissberg D, Ben-Zeev I. Talc pleurodesis. Experience with 360 patients. J Thorac Cardiovasc Surg 1993;106:689–95.[Abstract]
  6. Weissberg D. Empyema and bronchopleural fistula. Experience with open window thoracostomy. Chest 1982;82:447–50.[Abstract/Free Full Text]
  7. Pothula V, Krellenstein DJ. Early aggressive surgical management of parapneumonic empyemas. Chest 1994;105:832–6.[Abstract/Free Full Text]
  8. Takaro T, Scott SM, Bridgman AH, Sethi GK. Suppurative diseases of the lungs, pleurae and pericardium. Curr Probl Surg 1977;14(11):1–62.
  9. Ridley PD, Braimbridge MV. Thoracoscopic debridement and pleural irrigation in the management of empyema thoracis. Ann Thorac Surg 1991;51:461–4.[Abstract]
  10. O'Brien J, Cohen M, Solit R, et al. Thoracoscopic drainage and decortication as definitive treatment for empyema thoracis following penetrating chest injury. J Trauma 1994;36:536–40.[Medline]
  11. Pugatch RD, Faling LJ. Computed tomography of the thorax: a status report. Chest 1981;80:618–26.[Abstract/Free Full Text]
  12. Brown LR, Muhm JR. Computed tomography of the thorax. Current perspectives. Chest 1983;83:806–13.[Abstract/Free Full Text]
  13. Carroll DJ, McClement J, Himmelstein A, et al. Pulmonary function following decortication. Am Rev Tuberc 1951;63:231–41.[Medline]
  14. Toomes H, Vogt-Moykopf I, Ahrendt J. Decortication of the lung. Thorac Cardiovasc Surg 1983;31:338–41.[Medline]
  15. LeRoux BT, Mohlala ML, Odell JA, Whitton ID. Suppurative diseases of the lung and pleural space. Part I: Empyema thoracis and lung abscess. Curr Probl Surg 1986;23(1):1–89.
  16. Shamji FM, Ginsberg RJ, Cooper JD, et al. Open window thoracostomy in the management of postpneumonectomy empyema with or without bronchopleural fistula. J Thorac Cardiovasc Surg 1983;86:818–22.[Abstract]
  17. Eerola S, Virkkula L, Varstela E. Treatment of postpneumonectomy empyema and associated bronchopleural fistula. Scand J Thorac Cardiovasc Surg 1988;22:235–9.[Medline]
  18. Reich JM. Pulmonary gangrene and the air crescent sign. Thorax 1993;48:70–4.[Abstract/Free Full Text]
  19. Hammond JMJ, Lyddell C, Potgieter PD, Odell J. Severe pneumococcal pneumonia complicated by massive pulmonary gangrene. Chest 1993;104:1610–2.[Abstract/Free Full Text]
  20. Young JN, Samson PC. Pseudomonas aeruginosa septicemia with gangrene of the lung and empyema. Ann Thorac Surg 1980;29:254–7.[Abstract]
  21. Graham EA, Bell RD. Open pneumothorax: its relation to the treatment of acute empyema. Am J Med Sci 1918;156:839–71.
  22. Lindskog GE, Hubbel DS. An analysis of 215 cases of bronchiectasis. Surg Gynecol Obstet 1955;100:643–50.[Medline]
  23. Snider GL, Saleh SS. Empyema in the thorax in adults: review of 105 cases. Dis Chest 1968;54:410–5.[Medline]



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