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Ann Thorac Surg 2005;79:1851-1856
© 2005 The Society of Thoracic Surgeons

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Original article: General thoracic

Delayed Referral and Gram-Negative Organisms Increase the Conversion Thoracotomy Rate in Patients Undergoing Video-Assisted Thoracoscopic Surgery for Empyema

^a Division of Thoracic Surgery, University Hospital, Zurich, Switzerland
^b Division of Thoracic Surgery, CHUV, University Hospital, Lausanne, Switzerland
^c Department of Surgery, Kantonspital, Chur, Switzerland
^d Department of Biostatistics, University of Zurich, Zurich, Switzerland

Accepted for publication December 21, 2004.

^_* Address reprint requests to Dr Lardinois, Division of Thoracic Surgery, Raemistrasse, 100, University Hospital, CH-8091 Zurich-Switzerland (E-mail: didier.lardinois{at}usz.ch).

	Abstract

Top Abstract Introduction Patients and Methods Results Comment References

 
BACKGROUND: The role of video-assisted thoracoscopic surgery in the treatment of pleural empyema was assessed in a consecutive series of 328 patients between 1992 and 2002. An analysis of the predicting factors for conversion thoracotomy in presumed stage II empyema was performed.

METHODS: Empyema stage III with pleural thickening and signs of restriction on computer tomography imaging was treated by open decortication, whereas a thoracoscopic debridement was attempted in presumed stage II disease. Conversion thoracotomy was liberally used during thoracoscopy if stage III disease was found at surgery. Predictive factors for conversion thoracotomy were calculated in a multivariate analysis among several variables such as age, sex, time interval between onset of symptoms and surgery, involved microorganisms, and underlying cause of empyema.

RESULTS: Of the 328 patients surgically treated for stage II and III empyema, 150 underwent primary open decortication for presumed stage III disease. One hundred seventy-eight patients with presumed stage II empyema underwent a video-assisted thoracoscopic approach. Of these 178 patients, thoracoscopic debridement was successful in 99 of 178 patients (56%), and conversion thoracotomy and open decortication was judged necessary in 79 of 178 patients (44%). The conversion thoracotomy rate was higher in parapneumonic empyema (55%) as compared with posttraumatic (32%) or postoperative (29%) empyema; however, delayed referral (p < 0.0001) and gram-negative microorganisms (p < 0.01) were the only significant predictors for conversion thoracotomy in a multivariate analysis.

CONCLUSIONS: Video-assisted thoracoscopic debridement offers an elegant, minimally invasive approach in a number of patients with presumed stage II empyema. However, to achieve a high success rate with the video-assisted thoracoscopic approach, early referral of the patients to surgery is required. Conversion thoracotomy should be liberally used in case of chronicity, especially after delayed referral (>2 weeks) and in the presence of gram-negative organisms.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment References

 
Pleural empyema affects a large number of patients and may lead to severe and disabling sequelae in cases of inappropriate diagnosis or treatment [1, 2]. The choice of the appropriate treatment depends on the nature of the underlying disease, the chronicity of the empyema, and the patient’s overall condition [3]. The American Thoracic Society staging system has served as a guideline for appropriate treatment of patients with parapneumonic empyema. Stage I empyema is characterized by an exudative effusion without appearance of loculations and is usually treated by antibiotics and thoracocentesis or chest tube drainage. During the fibrinopurulent phase or stage II disease, the pleural fluid is turbid or frankly purulent and there are fibrin deposits over all pleural surfaces. Computer tomography imaging (CT scan) typically reveals pleural enhancement and loculated effusion but no signs of restriction. Treatment options consist of fibrinolytic therapy or video-assisted thoracoscopic debridement. Stage III empyema is characterized by pleural thickening and signs of restriction on CT scan. Decortication is required to free the trapped lung and to prevent recurrence and late restriction.

Several reports have demonstrated that video-assisted thoracoscopic surgery (VATS) is a valid treatment option for stage II empyema and allows appropriate control of infection and restoration of pulmonary function in early stage empyema [1, 2, 4–6]. Video-assisted thoracoscopic surgery is an attractive minimally invasive approach and has made surgical intervention a more acceptable early treatment option in this respect [7, 8]. Stage II empyema is a transitory stage between the exudative (stage I) and chronic (stage III) forms of empyema and represents only a short time frame in the evolution toward chronicity. Unfortunately, there is actually no single valid test available to distinguish stage II and III empyema on clinical signs and laboratory measurements. As a consequence, it became apparent that VATS has its limitations in the treatment of empyema, especially for the treatment of chronic empyema, which is still best treated with open decortication.

In this study, the role of VATS was critically evaluated in a consecutive series of 328 patients with surgically treated empyema, and a multivariate analysis was performed to determine the predicting factors associated with a conversion thoracotomy in patients undergoing VATS for presumed stage II disease.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment References

 
Since 1992, a standardized approach has been used for the surgical treatment of patients with pleural empyema [1, 2]. All patients with stage II or III disease were operated on according to this initially described approach and were followed in a consecutive manner.

Patient Selection
Enrollment criteria for surgery in patients with suspected American Thoracic Society stage II and III empyema consisted of loculated pleural effusion and pleural enhancement on CT scan associated with signs of infection (fever, leukocytosis, elevation of C-reactive protein), weight loss, chest pain, and a positive bacterial culture or a pH less than 7.1 of the pleural liquid assessed by thoracocentesis or chest tube drainage. Stage III empyema was suspected in the presence of pleural thickening and signs of restriction on CT scan. All patients had been treated initially with antibiotics, and 74.7% (245 of 328 patients) had thoracocentesis or chest tube drainage before admission in our institution.

A VATS approach was offered to all patients with suspected stage II empyema, ie, loculated pleural effusion and pleural enhancement without pleural thickening or signs of restriction at CT scan associated with signs of infection. Informed consent was obtained from all patients to proceed to conversion thoracotomy and open decortication if a stage III empyema was found at surgery. Exclusion criteria for a primary VATS approach consisted of the presence of a presumed stage III empyema with pleural thickening and signs of restriction on CT scan or the suspicion of abscess, bronchopleural fistula, or tumor at initial workup.

Technique of Video-Assisted Thoracoscopic Surgery Debridement
After double-lumen intubation, the patient was placed in a lateral position. A standard posterolateral thoracotomy incision was drawn on the skin of the patient, and a 3-cm incision was performed in the ventral aspect of this line. The operator’s index finger was introduced into the chest cavity. This digital exploration was found to be helpful to assess the chronicity of empyema; a rigid and narrowed intercostal space and palpable peel on the lung surface correlated with stage III empyema, which was unlikely to be successfully treated by VATS [1].

The pleural space was freed circumferentially by finger dissection and by use of a Senning suction device (Ulrich AG, St. Gallen, Switzerland). The optic was inserted through an additional 7-mm thoracic port placed one intercostal space above the initial incision but within the dissected area, and fluid, loculations, and septa were removed under endoscopic vision by use of the suction device and endoscopic Kaiser forceps (OP-Medical AG, Oberägeri, Switzerland). Material for microbiologic analysis was collected in all patients. The chest cavity was debrided, and the lung was freed circumferentially and from the apex to the diaphragm. An endoscopic lung forceps was inserted through a third thoracic port in the posterior aspect of the sixth intercostal space, which allowed the exposure of the lung surfaces and the fissures. Debridement of the visceral pleura and the fissures was performed by use of an Ulrich endoscopic dissector device (Ulrich AG, St. Gallen, Switzerland) [1].

Conversion thoracotomy and open decortication was considered in the presence of incapability to dissect the peel from the underlying lung surfaces.

After completion of the debridement of the parietal and visceral pleura, two 28F chest tubes were inserted through the ventral ports and placed under endoscopic vision in the costodiaphragmatic sulcus and the pleural dome, respectively. The pleural cavity was rinsed with several liters of warm saline solution through the chest tubes, and the lung was reexpanded. The patients were extubated as soon as they fulfilled the criteria for extubation, and respiratory physiotherapy was instituted. The antibiotic regimen was discontinued 14 days after the operation except in the presence of a lung abscess. The chest tubes were removed in the absence of air leaks and when the drainage volume was less than 100 mL/day.

Data Collection
Demographic data, time interval between onset of symptoms and surgery, underlying cause of empyema, microbiologic findings, postoperative morbidity, and the presence or absence of recurrent empyema up to 6 months after surgery were recorded in every patient.

Statistical Analysis
Summaries of continuous variables were given as mean ± standard deviation, whereas summaries of binary variables were given as counts and proportions. To determine predictive factors for conversion thoracotomy in presumed stage II empyema accessed by VATS for the factors age, sex, presence of bacteria, presence of gram-positive and gram-negative organisms, and time interval between onset of symptoms and surgery, as well as for the different etiologic groups (postpneumonic, postoperative, posttraumatic, postembolic, tuberculosis), univariate logistic regression and then multivariate analysis with a multiple logistic regression model was used. Significance was accepted at p less than 0.05.

	Results

Top Abstract Introduction Patients and Methods Results Comment References

 
Between 1992 and 2002, 328 patients underwent surgery for stage II or III pleural empyema; there were 227 men and 101 women, with a mean age of 55 years (range, 18 to 90 years).

Underlying Cause of Empyema
The underlying cause of empyema (Table 1) was pneumonia in 200 patients (61%), previous thoracic or abdominal operations in 52 (16%), chest trauma in 32 (10%), tuberculosis in 20 (6%), pulmonary embolism in 13 (4%), intrathoracic malignancy in 5 (2%), pleural aspergillosis in 5 (2%), and pleural actinomycosis in 1 (0.3%).

One hundred seventy-eight patients (54%) with presumed stage II disease underwent a VATS approach, which had to be converted to open decortication in 79 of these patients (44%) because of chronicity of disease; VATS debridement without the need for thoracotomy was performed in 99 patients (56%). In patients with presumed stage II empyema, VATS debridement without thoracotomy was achieved in 68% (17 of 25) of patients with posttraumatic, in 71% (25 of 35) with postoperative, in 75% (9 of 12) with tuberculous, and in 60% (6 of 10) with postembolic empyema, but only in 45% (42 of 93) of patients with parapneumonic empyema (Table 1). As a consequence, the conversion rate for thoracotomy and open decortication was higher in patients with parapneumonic empyema (55%) as compared with those with posttraumatic (32%) or postoperative empyema (29%; Table 1).

In patients undergoing surgery for parapneumonic empyema, a trend toward increased chronicity of the disease requiring a primary open decortication was observed since 1997. Primary thoracotomy was performed in 45% and 56% of patients with parapneumonic empyema between 1992 and 1996, and 1997 and 2002, respectively.

Microbiologic Assessment
Bacteriologic examination of the collected material during surgery revealed negative cultures in 40% of the patients. Streptococcus pneumoniae was found in 25%, Staphylococcus aureus in 15%, and other streptococci in 10% of the patients. Infections caused by gram-negative germs (Haemophilus influenzae, Pseudomonas aeruginosa, Escherichia coli, Proteus mirabilis, Enterobacter cloacae) were found in 6% of the patients between 1992 and 1996, and in 28% between 1997 and 2002 (p < 0.0001). Anaerobic microorganisms were not found between 1992 and 1996, but in 5% of the patients since 1997.

Predictive Factors for Conversion Thoracotomy in the 178 Patients With Presumed Stage II Empyema
Univariate analysis showed that postpneumonic empyema (p = 0.003), male sex (p = 0.013), prolonged time between onset of symptoms and surgery (p < 0.0001), and gram-negative organisms (p = 0.0001) were significantly associated with conversion thoracotomy (Table 2). In this group of 178 patients, the time between onset of symptoms and surgery was 9.8 ± 3.2 days for the patients who underwent thoracoscopic debridement in comparison with 17.3 ± 3.8 days in the patients with conversion thoracotomy. The patients with postpneumonic empyema were referred to surgery later than the patients with empyema of other causes, with a time between onset of symptoms and surgery of 14.9 ± 4.8 days versus 11.2 ± 4.6 days. Multivariate analysis using a stepwise logistic regression model identified the time interval between onset of symptoms and surgery (p < 0.0001) and gram-negative microorganisms (p < 0.01) as significant predictive factors for conversion thoracotomy in presumed stage II empyema accessed by VATS, whereas age of the patient, sex, and underlying cause of empyema (parapneumonic, postoperative, posttraumatic, postembolic, tuberculosis) were not (Table 2). The probability for conversion thoracotomy in presumed stage II empyema accessed by VATS strongly increased after a time interval between onset of symptoms and surgery greater than 14 days (Fig 1).

View larger version (26K): [in this window] [in a new window]   Fig 1. Probability of conversion thoracotomy in 178 patients undergoing video-assisted thoracoscopic surgery for presumed stage II empyema according to the time interval between onset of symptoms and surgery.

Recurrent empyema was found in 2.4% (8 of 328), 2% after VATS debridement and 2.6% after open decortication. All 8 patients had initially a parapneumonic empyema, and recurrence was diagnosed after an average time of 25 days (range, 10 to 42 days) after the initial operation. All patients underwent reoperation by thoracotomy, and all had an uneventful recovery.

	Comment

Top Abstract Introduction Patients and Methods Results Comment References

 
The mainstay of treatment of pleural empyema is control of ongoing infection and the prevention of recurrent infection and late restriction. Incomplete drainage of the pleural space with persistent signs of infection should prompt surgical intervention. Delaying surgical treatment in these situations is responsible for functional impairment and is associated with substantial morbidity and mortality [9, 10]. However, the decision making for appropriate treatment (surgical and nonsurgical) is a vexing clinical problem owing to the absence of specific clinical, radiologic, and laboratory characteristics for appropriate preoperative staging of empyema [8].

The advent of VATS for the management of fibrinopurulent stage II empyema has shown rewarding results in several reports [2, 11–13]. Video-assisted thoracoscopic surgery has the advantage of being less invasive than open decortication and having a better acceptance by the referring physician and the patient [6, 7, 14]. However, it is obvious that VATS has its limitations for the treatment of stage III disease [1, 3]. To overcome these limitations of VATS in the treatment of empyema and the problem of inability to accurately predict the stage of empyema in the preoperative phase, we have adapted a simple and pragmatic approach in patients with empyema referred for surgery since 1992. Patients with a long-lasting history, a thickened pleural peel, and signs of restriction on CT scan and those with an additional pathologic finding on CT scan such as an abscess or a tumor underwent decortication by primary thoracotomy. In all other situations, the patients were informed that a VATS approach would be attempted, and informed consent was obtained to proceed to thoracotomy if VATS was likely to be unrewarding. A 3-cm-long incision was made in the ventral aspect of a presumed thoracotomy line, and intraoperative evaluation of the pleural space was made by finger palpation and endoscopic exploration. In case of an organizing stage III empyema, the incision was enlarged to a standard thoracotomy. This pragmatic approach allowed a rapid distinction between patients who were likely to profit from a VATS debridement and those who required formal decortication. The current study summarizes our experience in this respect on a consecutive series of 328 patients referred for surgery of stage II and III empyema between 1992 and 2002.

Of the 328 patients, 150 underwent primary open decortication owing to chronic stage III empyema or the underlying cause of empyema requiring thoracotomy and resection such as abscessing lung tumors, bronchopleural fistula, or abscessing lung infarctions after pulmonary embolism. Computed tomographic scan may not only help to estimate the chronicity of an empyema but also help to determine its underlying cause, which is important to define treatment strategy and the surgical approach [3].

One hundred seventy-eight patients underwent a VATS attempt for presumed stage II disease, but conversion thoracotomy was judged necessary in another 79 patients because of chronicity of the disease. In fact, a VATS debridement seemed feasible and rewarding in 56% of the referred patients with suspected stage II empyema. These findings are similar to those from a recently published report in which 38% of the patients with empyema were managed by VATS and 62% by open decortication [14].

Our results confirm the importance of the interval between onset of symptoms or pleural effusion and surgery on the chronicity of empyema and the accessibility to a VATS treatment [5, 6, 15, 16]. Patients with presumed stage III disease had a long-lasting (>3 weeks) history and presented with a thickened enhanced pleura and signs of restriction on CT scan. A chronic stage III empyema inaccessible to a VATS approach was confirmed in all these patients during surgery. The interval between onset of symptoms and surgery was also crucial for the accessibility of VATS in patients with presumed stage II empyema. Our results emerging from a multivariate analysis demonstrated that it was the most important predictor for conversion thoracotomy in this respect. The probability of conversion thoracotomy rose from 22% to 86% between an interval of 12 and 16 days, respectively. The importance of early referral of patients with suspected empyema to surgery cannot be overemphasized if a minimal invasive approach is considered.

In patients with clinical stage II empyema, the conversion thoracotomy rate was higher in the patients with postpneumonic empyema (55%) as compared with those with posttraumatic (32%) and postoperative (29%) empyema. We speculate that this was related to a longer period of unsuccessful medial treatment before referral to surgery in patients with parapneumonic empyema. The conversion thoracotomy rate in patients undergoing a VATS approach for parapneumonic empyema has been analyzed in several reports and ranged from 18% to 59% [3, 6, 7, 17, 18]. Again, this discrepancy may be explained by a difference in referral pattern for surgery between the reported series and a stage migration phenomenon related to the policy of medical treatment before surgery. Indeed, the underlying cause of empyema was not a significant predictor for conversion thoracotomy in our patients as assessed by multivariate analysis in a stepwise multiple logistic regression model. In contrast, this analysis revealed that VATS debridement could even be more successful in that group of patients than in the patients with other causes of empyema if the patients with postpneumonic empyema had been referred to surgery earlier.

The second predictor for conversion thoracotomy in patients with presumed stage II was the presence of gram-negative microorganisms in the collected pleural fluid. The presence of E coli and E cloacae was always associated with conversion thoracotomy in our series. Furthermore, we observed an increased incidence of conversion thoracotomy in the second part of our study period, which paralleled an increased incidence of gram-negative and anaerobic microorganisms found at operation. It has been suggested that the rapidity of progression and stage transition of empyema are affected by the type and virulence of the involved organisms [8].

The 30-day postoperative mortality was 4% for all patients, which is in accordance with the results of other reports ranging from 1.3% to 6.6% [3, 7, 14, 15]. In our series, postoperative complications were observed in 9% and a reoperation rate for recurrent empyema in 2.4%, which is also comparable to other studies [7].

Although the results of our study and other series suggest that appropriate control of infection may be obtained by VATS debridement for stage II pleural empyema, the results regarding prevention of late restriction and restoration of pulmonary function still await further confirmation. In an earlier report, we have shown some degree of restriction in about 30% of the patients undergoing VATS debridement for empyema at pulmonary function testing 6 months after the operation [1].

In conclusion, VATS debridement offers an elegant minimal invasive approach in a number of patients with presumed stage II empyema. However, conversion thoracotomy should be liberally used in case of chronicity, especially after delayed referral (>2 weeks) and in the presence of gram-negative organisms.

	References

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