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Ann Thorac Surg 1998;65:319-323
© 1998 The Society of Thoracic Surgeons


Original Articles: General Thoracic

Video-Assisted Thoracoscopic Surgery for Fibrinopurulent Pleural Empyema in 67 Patients

Heinz Striffeler, MD, Matthias Gugger, MD, Vinzenz Im Hof, MD, Andreas Cerny, MD, Markus Furrer, MD, Hans-Beat Ris, MD

Department of Thoracic and Cardiovascular Surgery, University of Bern, Inselspital, Bern, Switzerland,
Department of Pulmonary Medicine, University of Bern, Inselspital, Bern, Switzerland,
Department of Internal Medicine, University of Bern, Inselspital, Bern, Switzerland

Accepted for publication August 2, 1997.

Dr Ris, Department of Thoracic and Cardiovascular Surgery, Inselspital, 3010 Bern, Switzerland.


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background. The roles of different drainage procedures in the management of empyema have to be redefined now that video-assisted thoracoscopic surgery (VATS) has been introduced. The debridement of fibrinopurulent stage II empyema with the use of VATS was assessed prospectively in regard to control of infection and restoration of pulmonary function.

Methods. Between January 1992 and May 1996, all patients at our institution with fibrinopurulent empyema that did not respond to chest tube drainage and antibiotic therapy were treated by debridement with the use of VATS. The patients were followed up prospectively by clinical and radiologic assessments 3 and 6 months after the operation and by spirometry 6 months after the operation.

Results. Video-assisted thoracoscopic surgery was initiated in 67 patients, but conversion to open decortication was required because of the finding of advanced disease in 19 patients (28%). Forty-eight patients underwent successful debridement with the use of VATS. The mean operative time was 82.1 minutes (range, 50 to 135 minutes), the mean duration of postoperative chest tube placement was 4.1 days (range, 2 to 8 days), and the mean duration of postoperative hospitalization was 12.3 days (range, 4 to 42 days). No wound infections were observed during the postoperative course. Both the 30-day mortality rate and the recurrence (ie, need for thoracotomy) rate were 4%. The mean predicted vital capacity was 84.8% ± 14.9% and the mean predicted forced expiratory volume in 1 second was 88.6% ± 19.2% 6 months after the operation.

Conclusions. Debridement with the use of VATS is safe and efficient for stage II empyema, but open decortication should be used for more advanced disease.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Pleural empyema affects a large number of patients each year and has severe and disabling sequelae when it is not recognized or is treated incorrectly. As defined by the American Thoracic Society in 1962 [1], pleural empyema may pass from its exudative form through a fibrinopurulent phase before becoming organized. As a consequence, the treatment modality used varies according to the phase of the disease [2]. Although the principles of therapy for pleural empyema have been outlined in the past [3], daily management of the disease remains controversial, often overemphasizing conservative treatment with antibiotics. Debridement with the use of video-assisted thoracoscopic surgery (VATS) recently was proposed for the treatment of the fibrinopurulent stage of empyema to increase acceptance of early surgical intervention for this disease [4] [5] [6] [7] [8] [9] [10] [11]. The results after debridement with the use of VATS suggest that appropriate control of the infection may be obtained, but long-term results in regard to the restoration of pulmonary function and the limits of this technique still need to be defined better.

Since 1992, we have adopted a standardized technique of debridement with the use of VATS for stage II empyema. All patients have been followed up prospectively in regard to control of infection and restoration of pulmonary function.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Since January 1992, a standardized approach has been used for patients with stage II pleural empyema at our institution. According to the American Thoracic Society classification [1], stage II empyema is defined by the appearance of turbid pleural fluid related to the presence of polynuclear leukocytes and fibrin deposits on the parietal and visceral pleura with encasement of the lung. In contrast to stage III empyema, no granulation tissue ingrowth into the fibrinous peel is found in stage II, or fibrinopurulent, empyema, which allows for well-defined dissection planes between the lung and the peel during operation.

Enrollment criteria for our study included systemic signs of infection (fever, weight loss, pain), loculated pleural effusions consistent with empyema on computed tomographic (CT) scan or positive bacterial cultures at thoracentesis, and an interval of less than 3 weeks since the onset of fever or pleural effusion. All patients had been treated initially with chest tube drainage and antibiotic therapy at other institutions, and operation was considered only when there was clinical and radiologic evidence of treatment failure. A CT scan was performed in all patients before operation to confirm the diagnosis of loculated empyema and to detect additional intrathoracic abnormalities. Signs of empyema on CT scan consisted of a loculated effusion surrounded by a homogeneously thickened and contrast-enhancing pleura [12]. A VATS approach was offered to patients who fulfilled the enrollment criteria, and consent was obtained from all patients to proceed to decortication through a thoracotomy if the empyema was found to be advanced during the operation. Exclusion criteria for a VATS approach consisted of a fever of more than 3 weeks’ duration and the presence of a thickened visceral pleural peel or a shrunken hemithorax on CT scan, as well as the suspicion of a lung abscess or cancer.

After double-lumen intubation, a standard posterolateral incision was drawn on the skin of the patient, who was placed in a lateral position. An incision of 3 cm was made in the ventral aspect of this line and the operator’s index finger was introduced into the thoracic cavity (Fig 1A). This digital exploration was found to be helpful in assessing the stage of the empyema; a rigid and narrowed intercostal space as well as a thick and stiff peel between the lung and the chest wall were signs of a chronic condition that usually was not amenable to a VATS approach. Adhesions between the lung and the chest wall were broken and the pleural space was freed circumferentially by dissection using the index finger and a Senning suction device (Ulrich AG, St Gallen, Switzerland) (Fig 1B).



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Video-assisted thoracoscopic surgical debridement for stage II empyema. (A) An incision of 3 cm is made in the ventral aspect of a presumed thoracotomy line and the operator’s index finger is introduced into the chest cavity to assess the duration of the empyema and to free the underlying lung. (B) A Senning suction device (Ulrich AG, St Gallen, Switzerland) is introduced. (C) Fibrin and loculations are evacuated under endoscopic vision. (D) The fibrinous peel is dissected from the parietal and visceral surfaces.

 
The optic was inserted several centimeters away from the initial incision but within the dissected area, and fluid, loculations, and septa were removed by suction under endoscopic control (Fig 1C). The chest wall was debrided with the use of a dissector and Kaiser forceps, and special attention was paid to freeing the costodiaphragmatic sulcus completely. The instruments were inserted through the initial incision without the use of trocars. This allowed for quick and efficient removal of debris and fibrin deposits.

The lung was freed circumferentially and from the apex to the diaphragm. Visceral decortication was performed with the use of a dissector while the lung (or the peel) was held by a Duval forceps inserted through an additional port (Fig 1D). After completion of the parietal and visceral debridement, two large-bore chest tubes were inserted through the ports and placed under endoscopic vision in the costodiaphragmatic sulcus and on the pleural dome, respectively, to drain fluid and air leaks after the operation. The pleural cavity was irrigated with warm saline solution through the chest tubes and the lung was reexpanded. Finally, fiberbronchoscopic bronchial toilet of the affected lung was performed if required.

The patients then were extubated and transferred to the intermediate care unit for 24 to 48 hours. Pain relief was obtained by patient-controlled analgesia and respiratory physiotherapy was instituted. The antibiotic regimen was discontinued 14 days after the operation. The chest tubes were removed if no air leak was present and the drainage volume was less than 100 mL/day. If VATS was judged to be unrewarding during the operation, a standard posterolateral thoracotomy was performed (which included the two previously performed incisions), followed by classic decortication.

For all patients, the duration of fever, chest tube drainage, and hospitalization was recorded during the postoperative period, as was the reoperation rate in case of failure to control the empyema. All patients were followed up prospectively by clinical and radiologic assessments 3 and 6 months after the operation and by pulmonary function tests 6 months after the operation. Patients who required sternotomy for cardiac procedures or a thoracotomy with lung resection for lung cancer before or after debridement with the use of VATS were excluded from postoperative pulmonary function assessments. Pulmonary function was not assessed before the operation because all patients had large-bore chest tubes in place that would have influenced the results. In addition, no ventilation-perfusion lung scans were performed [13] because the preoperative extent of ventilation-perfusion mismatch was considered to be related to the presence of large loculations compressing the lung and not to lung encasement itself.


    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Between January 1992 and May 1996, 88 patients with pleural empyema were treated at our institution after failing to respond to large-bore chest tube drainage and an antibiotic regimen. In 21 patients, the history and radiologic findings suggested chronic disease, and open decortication was performed without attempted VATS. In 67 patients with presumed stage II empyema, VATS was initiated. However, in 19 of these patients (28%), VATS had to be abandoned and open decortication performed because the disease was found to be too far advanced. The outcomes of these patients were not included in the study analysis.

Forty-eight patients (39 men and 9 women with a mean age of 51.4 years [range, 20 to 86 years]) were treated by debridement with the use of VATS. The underlying cause of empyema was pneumonia in 65% of the patients, previous thoracic or abdominal operation in 12%, intrathoracic malignancy in 8%, pulmonary embolism in 7%, and trauma in 7%. Bacteriologic examination of the specimens collected at the beginning of the operation revealed negative cultures in 44% of the patients, Streptococcus pneumoniae in 23%, Staphylococcus aureus in 14%, group A streptococcus in 8%, Mycobacterium tuberculosis in 8%, and Haemophilus influenzae and Pseudomonas aeruginosa in 1 patient each. No mixed cultures and no anaerobic microorganisms were identified.

The mean operative time was 82 minutes (range, 50 to 135 minutes). No intraoperative complication requiring emergency thoracotomy occurred in any of the patients. Forty-seven patients (98%) were extubated at the end of the procedure and 1 required prolonged mechanical ventilation because of respiratory failure. The latter patient died 14 days after operation of multiorgan failure resulting from an abscess of the ipsilateral lower lobe that was not detected on the initial CT scan but was recognized at autopsy. Another patient with metastatic cervical cancer died 16 days after the operation of cerebral metastases without evidence of empyema, yielding a 30-day mortality rate of 4%.

Fever exceeding 37°C was observed after the operation for a mean of 2.4 days (range, 1 to 5 days). The mean duration of chest tube drainage was 4.1 days (range, 2 to 8 days). Air leaks were seen in 15% of the patients at the end of the operation and were managed by chest tube drainage. No air leak persisted for more than 3 days. The mean duration of postoperative hospitalization was 12.3 days (range, 4 to 42 days). Hospitalization for more than 14 days was related to the underlying disease (pancreatitis, cancer, acquired immunodeficiency syndrome, and cardiovascular disorders) rather than to the sequelae of the operation. No wound infections occurred during the postoperative course.

Five patients died during follow-up 2 to 6 months after the operation without evidence of persistent or recurrent empyema: 1 of acute pancreatitis, 2 of acquired immunodeficiency syndrome, and 2 of metastatic cancer. Two patients required reoperation for recurrent empyema 5 days and 6 weeks, respectively, after debridement with the use of VATS, for a recurrence rate of 4%.

Radiologic assessment by chest roentgenograms 3 months after the operation usually revealed a well-expanded lung without obvious pleural thickening but a partially obliterated costodiaphragmatic sulcus.

Postoperative spirometry 6 months after the operation was obtained in 29 patients. In addition to the 7 patients who died, 5 patients were lost to follow-up after 3 months and 7 patients required cardiac operation or lung resection for lung cancer and were not considered for follow-up pulmonary function testing. The mean postoperative vital capacity of the 29 patients tested was 84.8% ± 14.9% predicted (range, 37% to 112%). In 52% of the patients, the vital capacity was greater than 90% predicted. The mean forced expiratory volume in 1 second (FEV1) was 88.6% ± 19.2% predicted (range, 36% to 113%). In 69% of the patients, the FEV1 was greater than 90% predicted. The worst results were obtained in the 2 patients who underwent reoperation for recurrent empyema, in whom the FEV1 after the second operation was 34% and 45% predicted, respectively.


    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
The mainstays of therapy for pleural empyema remain control of infection, prevention of persistent and recurrent disease of the pleural space, and restoration of pulmonary function by obviating restrictive lung disease [2]. Different treatment options are available according to the stage and duration of the empyema, its underlying cause, and the general condition of the patient. Stage I parapneumonic empyema is treated concurrently by the administration of appropriate antibiotics and the early and proper institution of large-bore chest tube drainage. Stage III empyema is considered for decortication through an open thoracotomy. However, the treatment of transitional or fibrinopurulent stage II empyema remains controversial.

Stage II empyema is characterized by the presence of turbid fluid with increased pleural leukocyte and lactate dehydrogenase levels, and decreased glucose and pH levels. The deposition of intrapleural fibrin leads to the development of loculations and a fibrinous pleural peel, limiting lung expansion. These alterations may occur as early as several days after bacterial invasion of the pleural cavity, depending on the underlying cause of the empyema as well as on the microorganisms involved.

This stage usually cannot be managed by chest tube drainage alone and several treatment options have been described, ranging from enzymatic debridement [12] [14] to tube thoracostomy to open thoracotomy and early decortication [2] [11]. Enzymatic drainage through CT-guided insertion of chest tubes has shown promising results; however, a prolonged treatment period of 2 to 3 weeks often is required to resolve the empyema [14]. Early open decortication offers excellent results in regard to infection control and restoration of lung function, but it has a low acceptance rate among both patients and physicians because of pain-related morbidity in the early postoperative period. Reluctance to use an early surgical approach in patients with empyema eventually leads to late referral of the patients in a more advanced stage of empyema and a lower chance of restoring pulmonary function through decortication.

Recently, debridement with the use of VATS has been proposed for the treatment of stage II fibrinopurulent loculated empyema. The major advantages of VATS over open thoracotomy are reduced postoperative pain and dysfunction. These advantages result in greater acceptance by patients and the avoidance of lengthy hospitalizations with prolonged use of chest tubes and antibiotics before operation is considered. However, the safety and efficacy of VATS in the treatment of pleural empyema require confirmation and the limits of this technique need to be defined.

Our results indicate that VATS is a safe and useful tool in the treatment of fibrinopurulent empyema with loculations that fail to respond to closed chest tube drainage and antibiotic therapy. The operative time averaged 80 minutes and 98% of all patients were extubated at the end of the procedure. Postoperative chest tube drainage averaged 4.1 days. The mean duration of hospitalization was 12.3 days and was related more to the underlying disease than to the procedure itself. Postoperative air leaks were seen in the minority of patients and did not persist for longer than 3 days. These results are in accordance with those reported by other investigators who have performed debridement with the use of VATS for patients with fibrinopurulent empyema [4] [11].

Successful treatment of empyema depends in part on the technical aspects of the operation [2], but primarily on the duration of the inflammatory process being treated. If operation is performed early after the onset of empyema, complete evacuation of fibrin layers from the parietal and visceral pleura is likely to be achieved either by VATS or by open decortication. However, in patients with more advanced and chronic disease, it is less likely that VATS will be successful. Failure to recognize the limits of VATS in the treatment of empyema might result in recurrence and poor outcome with respect to pulmonary function.

In our first 13 patients treated by VATS since 1992, no recurrences or deaths were observed during the first 30 days of follow-up [7]. Subsequently, the indications for debridement with the use of VATS were extended and patients with more advanced stages of empyema were treated. The results of this series include a 30-day mortality rate of 4% and a recurrence (ie, need for reoperation and open decortication) rate of 4%. Spirometry performed 6 months after the operation revealed normal FEV1 values in 69% of the assessed patients and reduced values in 31%. Among those patients who had reduced FEV1 values, the worst results were obtained in the 2 patients who required reoperation and open decortication at a later date. These results support the need for early surgical intervention after the onset of empyema, which can include debridement with the use of VATS. However, they also suggest that open decortication should be performed when the disease is judged to be too far advanced.

Unfortunately, there currently is no ideal investigation available that enables accurate preoperative determination of the duration of an empyema. An interval of no more than 2 to 3 weeks after the onset of pleural effusion is indicative of an early stage of fibrinopurulent empyema [1], but it failed to identify the ultimate need for open decortication in 28% of our patients. Other investigators have reported a conversion rate of 10% when they used similar indications for debridement with the use of VATS, without late recurrence, but the results of pulmonary function tests were not provided [10]. Several authors have suggested that a low pH level in the pleural effusion (<6.8) is related to the duration of the empyema. Because all our patients were referred after chest tube drainage and antibiotics had failed to resolve an established empyema, pH measurements were not available to determine which surgical procedure was needed.

No microorganisms could be identified in 44% of the intraoperative fibrin deposits harvested for Gram stain and cultures. This observation also was made in previous reports [9] [10]. It may be related to the autolysis of bacteria such as S pneumoniae and possibly other microorganisms in purulent empyema fluid [15], or to previously administered antibiotics. Of note is the lack of anaerobic bacteria recovered in our series, which is in contrast to data reported previously and compiled recently [16]. This may be related to extensive handling and prolonged transportation to the microbiology laboratory where standard anaerobic cultures were performed.

A preoperative CT scan is mandatory and should be performed in every patient scheduled for operation. It should not be replaced by ultrasonography in adults because it allows for the detection of underlying lung diseases such as tumors or abscesses, confirms the diagnosis of empyema, and assesses, to some degree, the duration of the empyema [12]. Previously unknown intrathoracic malignant tumors were found by CT scan in 8% of our patients and pulmonary embolism was suggested in 7%. However, in our experience, a CT scan does not enable the selection of those patients with fibrinopurulent empyema who can be treated successfully by VATS. Appropriate preoperative determination of the stage of empyema thus remains unresolved.

Since 1992, the introduction of VATS debridement for the treatment of pleural empyema at our institution, this technique has been offered to all patients with presumed fibrinopurulent empyema that does not resolve with chest tube drainage and antibiotic therapy. However, the patients are prepared for open decortication during the same operation if required. We have not had any problems with patient acceptance of this approach. Initially, a 3-cm incision is made in the ventral aspect of a presumed thoracotomy line and finger palpation is used to assess the narrowing and rigidity of the intercostal space, the thickness of the underlying pleural peel, and the degree of adherence of the lung to the chest wall. This maneuver determines quickly and efficiently the duration of the empyema and whether debridement with the use of VATS may be successful, avoiding a lengthy and fruitless procedure.

Video-assisted thoracoscopic surgery usually is believed to be associated with a lower postoperative morbidity than thoracotomy. However, in a prospective study comparing VATS and posterolateral thoracotomy for lung resection, there was no significant difference in regard to pulmonary function, shoulder girdle function, postthoracotomy pain, or patient acceptance between the two approaches 3 months after the operation [17]. Similar results were obtained by other investigators [18] [19]. These results do not support the universal use of VATS in the treatment of pleural empyema, especially in its more chronic organizing phase, which we believe is not well suited to this technique. Video-assisted thoracic surgery is a safe and efficient treatment option for fibrinopurulent empyema, but thoracotomy should be used if necessary during the same procedure when the empyema is found to be at a more advanced stage.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Andrews NC, Parker EF, Shaw RP, et al. Management of non-tuberculous empyema. Am Rev Respir Dis 1962;85:935-936.
  2. Thurer RJ Decortication in thoracic empyema: indications and surgical technique. Chest Surg Clin N Am 1996;6:461-490.[Medline]
  3. Graham EA Some fundamental considerations in the treatment of empyema thoracis. St Louis: Mosby, 1925:7-110.
  4. Hutter JA, Harari D, Braimbridge MV The management of empyema thoracic by thoracoscopy and irrigation. Ann Thorac Surg 1985;39:517-520.[Abstract]
  5. Kerr JA, Rodgers BM Thoracoscopy in the management of empyema in children. J Pediatr Surg 1993;28:1128-1132.[Medline]
  6. Ferguson MK Thoracoscopy for empyema, bronchopleural fistula and chylothorax. Ann Thorac Surg 1993;56:644-645.[Abstract]
  7. Striffeler H, Ris HB, Würsten HU, Im Hof V, Stirnemann P, Althaus U Videoassisted thoracoscopic treatment of pleural empyema. A new therapeutic approach. Eur J Cardiothorac Surg 1994;8:585-588.[Abstract]
  8. Hurley JP, McCarthy J, Wood AE Retrospective analysis of the utility of videoassisted thoracic surgery in 100 consecutive procedures. Eur J Cardiothorac Surg 1994;8:589-592.[Abstract]
  9. Liu HP, Chang CH, Lin PJ, Hsieh HC, Chang JP, Hsieh MJ Videoassisted thoracic surgery. The Chang Gung experience. J Thorac Cardiovasc Surg 1994;108:834-840.[Abstract/Free Full Text]
  10. Mackinlay TA, Lyons GA, Chimondeguy DJ, Piedras MA, Angamaro G, Emery J VATS debridement versus thoracotomy in the treatment of loculated postpneumonia empyema. Ann Thorac Surg 1996;61:1626-1630.[Abstract/Free Full Text]
  11. Weissberg D, Refaely Y Pleural empyema: 24-year experience. Ann Thorac Surg 1996;62:1026-1029.[Abstract/Free Full Text]
  12. Lee-Chiong TL, Matthay RA Current diagnostic methods and medical management of thoracic empyemas. Chest Surg Clin N Am 1996;6:419-438.[Medline]
  13. Swoboda L, Laule K, Blattmann H, Hasse J Decortication in chronic empyema: investigation of lung function based on perfusion scintigraphy. Thorac Cardiovasc Surg 1990;38:359-361.[Medline]
  14. Debesse B, Bellamy J, Dumouchel A, et al. Drainage pleural et éradication du foyer pulmonaire. Traitment standard des pleurésies purulentes aigues à germes banales. Rev Mal Respir 1983:1245-1246.
  15. Cottagnoud P, Tomasz A Triggering of pneumococcal autolysis by lysozyme. J Infect Dis 1993;167:684-690.[Medline]
  16. Bryant RE, Salmon CJ Pleural empyema. Clin Infect Dis 1996;22:47-64.
  17. Furrer M, Rechsteiner R, Eigenmann V, Signer Ch, Althaus U, Ris HB Thoracotomy and thoracoscopy: postoperative pulmonary function, pain and chest wall complaints. Eur J Cardiothorac Surg 1997;12:82-87.[Abstract]
  18. Landreneau RJ, Hazzelrigg SR, Mack MJ, et al. Postoperative pain-related morbidity: video-assisted thoracic surgery versus thoracotomy. Ann Thorac Surg 1993;56:1285-1289.[Abstract]
  19. Giudicelli R, Thomas P, Lonjon T, et al. Video-assisted minithoracotomy versus muscle-sparing thoracotomy for performing lobectomy. Ann Thorac Surg 1994;58:712-718.[Abstract]



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