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Ann Thorac Surg 2003;76:225-230
© 2003 The Society of Thoracic Surgeons

Original article: general thoracic

Minimally invasive surgery in the treatment of empyema: intraoperative decision making

John R. Roberts, MDa*

a Division of General Thoracic Surgery, Vanderbilt University Hospital, Nashville, Tennessee, USA

* Address reprint requests to Dr Roberts, 5181 Remington Drive, Brentwood, TN, USA 37027.
e-mail: robertshane{at}comcast.net

Presented at the Forty-eighth Annual Meeting of the Southern Thoracic Surgical Association, San Antonio, TX, Nov 8–10, 2001.


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 
BACKGROUND: Pneumonia, parapneumonic effusions, and empyema continue to be significant health problems, especially in elderly individuals. Minimally invasive thoracic surgery in the treatment of empyema has been demonstrated but has not been well defined. Furthermore, it has not been determined how to choose patients who can be treated with thoracoscopy versus thoracotomy. We report the results of a strategy in which all patients were initially approached with thoracoscopy and converted to open decortication only if the lung could not be inflated to fill the chest.

METHODS: A total of 172 patients underwent decortication for empyema over a 5-year period. Thoracoscopic decortication was attempted in all patients; patients were converted to open decortication if access to the pleural space was not possible, or if the lung could not be mobilized sufficiently to reach both the chest wall and the diaphragm. Proportions were compared using the {chi}2 test.

RESULTS: Of the 172 patients, 66 successfully underwent decortication with thoracoscopic techniques only. The remaining 106 patients required complete thoracotomy. No difference was found in the reoperation rate; 3 of 106 open thoracotomy patients underwent reexploration for recurrent empyema, whereas two of 66 thoracoscopy patients required reoperation for hemothorax (p = 0.347). There was a tendency for thoracoscopic patients to require reoperation for bleeding (p = 0.08); both patients taken back to the operation room for bleeding had undergone thoracoscopic pleurectomy. Eleven of 166 patients (all explored with open thoracotomy) died after decortication, for a mortality rate of 6.6%. All of these patients had gone to surgery from the intensive care unit.

CONCLUSIONS: Using the criteria of complete expansion of the lung surface to the chest wall and diaphragm allowed accurate selection of patients who could undergo complete thoracoscopic decortication without risk of recurrent empyema. Computed tomographic scans did not help to predict which patients would require open procedures. Thoracoscopic patients were more likely to require reoperation for bleeding if thoracoscopic pleurectomy was performed.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Discussion
 References
 
Thirty years ago the American Thoracic Society described three phases (exudative, fibrinopurulent, and organizing) in the natural course of empyema [1]. In the exudative (or parapneumonic effusion) phase the fluid is free flowing; it can often be treated with the combination of antibiotics and some sort of minimally invasive drainage (thoracentesis or tube thoracostomy). During the fibrinopurulent phase adhesions, loculations, and thick pus formed that make simple drainage ineffective [2]. These patients may occasionally be drained with tube thoracostomy, but many will require surgical drainage, either thoracoscopic or open. In the organizing phase, thick peels form that are more difficult to remove and may require formal thoracotomy.

For the purposes of preoperative and intraoperative surgical decision making, differentiating between acute and chronic empyema is not important; both require drainage. Furthermore, the difference between acute and chronic empyema is a clinicopathologic difference, not a preoperative diagnosis. Finally, it usually cannot be determined before surgery and sometimes not until pathologic analysis. At presentation one must determine whether the patient has empyema; at surgery one must determine whether the patient receives adequate drainage. Not until surgery (and sometimes not until pathologic analysis) can one be sure whether the patient has acute or chronic empyema. In either diagnosis, the surgical goal is the same—to completely drain the infected space, and to do it with few complications and without reoperation.

Formal decortication of organized empyema with thoracoscopy has been demonstrated [3] but not incorporated into a rationale. Because tube thoracostomy (chest tube) drainage is considered adequate if the lung is completely expanded, we hypothesized that thoracoscopic drainage would be adequate if the lung completely filled the chest at the completion of the procedure, even if a thin pleural peel were left behind. Because the lung seldom fills the chest unless mobilized from the diaphragm, mobilizing the lower lobe away from the diaphragm became a routine part of our thoracoscopic decortication.

We retrospectively analyzed the results of the surgical treatment of patients undergoing therapy for empyema to determine whether this thoracoscopic protocol/algorithm was appropriate. In all patients, the approach was first attempted with thoracoscopy. If access to the chest could not be gained, or the lung could not be freed from the diaphragm or the expanded lung could not fill the chest, the patients were then opened for open thoracotomy. The goal was to confirm whether this protocol allows accurate selection of patients that can be treated with thoracoscopy alone.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Discussion
 References
 
All patients undergoing surgical treatment for empyema under 1 surgeon’s care for the last 5 years were analyzed. Patients were considered to have empyema if they had fever, leukocytosis, pleural fluid with a pH less than 7.2, and a pulmonary infiltrate, with no other source of fever identified before or after the surgery. Positive cultures of neither fluid nor blood were required to make the diagnosis.

All patients were brought to the operating room, underwent general anesthesia, and then underwent a diagnostic bronchoscopy to identify any endobronchial lesions and to culture sputum. Double-lumen endotracheal tubes were then placed and patients positioned in the lateral decubitus position. Thoracoscopic evaluation was attempted through three ports: the seventh intercostal space in the anterior axillary line, the second intercostal space in the midaxillary line, and the fifth intercostal space in the auscultatory triangle. If access could not be obtained, the patient then underwent either a vertical thoracotomy (sparing the latissimus and serratus muscles) or a posterolateral thoracotomy (dividing the latissimus and sparing the serratus).

If thoracoscopic debridement was possible, suctioning and decortication were done until the lung was freed from the diaphragm and either no peel or a thin peel remained on the surface of the lung. Several thoracoscopic techniques were used to accomplish this, including complete decortication under direct visualization, incision making through the peel to partition it, and suctioning. The fissures were always opened completely, and the lung was mobilized from the mediastinum anteriorly and posteriorly and from the diaphragm.

The lung was then inflated. If the lateral surfaces of the lung could reach the chest wall and the inferior surface reach the diaphragm, the decortication was considered complete. If not, a thoracotomy was performed, and the decortication and pleurectomy (if necessary) was done in the usual open fashion.

Demographic data collected were age, sex, and etiology of the empyema (Table 1). Hospital data collected included length of stay, chest tube duration, intensive care unit duration, days intubated, days hospitalized before surgical drainage, complications, and mortality (Fig 1). Computed tomographic (CT) reports of those patients who had had scans within 3 days of their surgery were reviewed to determine whether any CT finding would reliably predict the need for open drainage or the ability to successfully undergo thoracoscopic drainage. Scans were separated into those that revealed pleural thickening or rind, empyema, enhancing fluid collection, organized fluid/loculated fluid, or fluid with or without air/fluid levels, from high to low probability of pleural rind that would prevent thoracoscopy. Data are reported as means ± standard deviation, where appropriate. Averages were compared using Student’s t test and proportions were compared using the {chi}2 test. Values of p less than or equal to 0.05 were accepted as significant.


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  		Table 1. Etiology of Empyema

 


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  		Fig 1. Results of analysis of hospital data for patients who underwent thoracoscopic decortication (grey bars) and those who underwent open thoracotomy (black bars). The y-coordinate indicates numbers of days for length of stay (LOS), use of chest tube days, preoperative period (Preop days), intensive care unit (ICU days), and intubation (Days Intub). The difference in preoperative days was highly significant (p = 0.015).

 

   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Discussion
 References
 
Demographic results are summarized in Table 2. A total of 172 patients underwent surgical treatment for empyema, 106 by open thoracotomy, and 66 by thoracoscopic drainage. Of the patients, 73% were men, of whom two thirds required open drainage. The remaining 27% of the patients were women, almost half of whom were treated thoracoscopically. Patients ranged in age from 3 to 92 years; there was no significant difference between the two groups. Most of the empyemas resulted from either primary or secondary pneumonia. Patients with secondary pneumonia developed pneumonia from several causes, including transplantation (bone marrow, liver, or lung), cardiac surgery, and esophageal perforation. A minority of patients developed empyema after local causes (7% esophageal perforations and 2% subphrenic infection). The greatest number of deaths occurred among patients with pneumonia; however, empyema in postsurgical patients (ie, those who had undergone cardiac surgery or lung cancer resection) resulted in the highest perioperative mortality (percent).


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  		Table 2. Demographic Characteristics of Study Patients

 
Figure 2 summarizes a breakdown of the hospital data. Although all of the differences were highly significant, the p values are not included because the populations were different. The average length of stay for all patients (VATS and OPEN together) was 22.0 days, of which 6.7 days were before surgery and 15.3 after surgery. The mean patient retained a chest tube for 10.5 days after surgery, spent 3.2 days in the intensive care unit, and was intubated for 2.5 days. The difference between the two groups in preoperative days was significant (p = 0.015) and may have contributed to the need for open surgery.



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  		Fig 2. Breakdown of computed tomographic (CT) scoring for patients who underwent open thoracotomy (grey bars) and those who underwent thoracoscopic surgery (black bars). Data from 84 patients who had CT scans within 3 days of surgery were analyzed to determine whether the CT findings could predict the surgery that would be necessary to effect drainage. Readings of frank radiologic empyema indicated that patients were more likely to require open rather than thoracoscopic drainage.

 
Bronchoscopy was performed preoperatively to obtain sputum culture, and was done postoperatively to remove any bloody secretions and to assist in lung expansion. Only 17 of 172 patients had culture results from sputum and pleura that were identical; the majority had been treated with antibiotics preoperatively and, despite having purulent sputum or pleural fluid (or both), did not culture any organisms.

Complications were classified as major or life threatening. Major complications prolonged hospital stay but were not fatal; they included atrial fibrillation, pneumonia not requiring intubation, and nonemergent reoperation. Life-threatening complications required transfer to an ICU or emergency surgery; these included aspiration or pneumonia requiring intubation, cardiac arrest, acute respiratory distress syndrome, or emergency surgery. No complications were seen for any of the thoracoscopy sites, including the axillary site.

The patients who underwent open thoracotomy were sicker both before and after surgery. The incidence of complications—both major and life-threatening–were greater among patients who underwent open decortications than for those with thoracoscopic procedures, both pre- and postoperatively (Table 3). Patients undergoing open procedures were more likely to require postoperative reintubation and ultimately tracheostomy. Four of 106 open thoracotomy patients required reoperation, 3 for recurrent empyema and 1 for bleeding. Two of 66 thoracoscopic patients required reoperation for bleeding. Both of these patients had also undergone pleurectomy in addition to decortication. There were no reoperations for recurrent empyema in the thoracoscopy group, supporting our hypothesis that this algorithm (complete expansion of the lung to the chest wall and diaphragm) allows complete drainage and prevents recurrence of infection. The 30-day mortality in the entire group was 1.8% (three deaths among 166 patients). Hospital mortality was 7.43% (11 deaths among 166 patients).


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  		Table 3. Complications in Study Patients

 
Computed tomographic scans were performed on 84 patients within 3 days of surgery. The scan reports were reviewed to determine whether the scans could predict the ability to drain the chest completely using thoracoscopy alone. Scans were classified according to terms used by the radiologists; these included "pleural rind or thickening," "empyema," "enhancing fluid," "organized fluid," and "air/fluid levels." This would seem to progress from most likely case to require thoracotomy to most likely to be drainable with thoracoscopy.

Figure 2 shows the results of this analysis. No particular CT finding accurately predicted the type of surgery that would be necessary. Those patients in whom the radiologist diagnosed empyema were more likely to require thoracotomy.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Discussion
 References
 
Although the principles of drainage for empyema have not changed in the past 30 years, the acceptance by pulmonologists of the importance of early surgical drainage of empyema and of parapneumonic effusions has changed [4]. Drainage of parapneumonic fluid is recommended when patients have pus in the pleural space, pleural fluid with a positive Gram stain or culture, or pH less than 7.2 (Table 4) [5, 6]. Typical management of a patient with parapneumonic effusions or empyema might include multiple thoracentenses followed by chest tube placement, interventional radiologic drains, and finally surgical drainage, all spread over a 3-week period and requiring several CT scans. Although some investigators still advocate intrapleural fibrinolytics [7], most studies in the past decade have demonstrated that thoracoscopy is more effective than tube thoracostomy and streptokinase [8] as well as more cost-effective [9].


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  		Table 4. Indications for Drainage of Pleural Fluid

 
Choosing the approach to drain patients is less straightforward. Thoracoscopic drainage is accepted for drainage of hemothorax [10]. Scherer and colleagues [11] reported that video-assisted thoracic surgery was replacing open thoracotomy for treatment of posttraumatic thoracic complications. Thoracoscopic drainage of clotted blood is usually simpler than for the complete evacuation of infection found in the fibrinopurulent stage of empyema (Fig 3). Thoracoscopic decortication, with or without parietal pleurectomy, is much more difficult.



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  		Fig 3. Operative data for patients who underwent open thoracotomy (grey bars) and those who underwent video-assisted thoracoscopic surgery (black bars). There was greater estimated blood loss in the open thoracotomy group but no significant difference in operative time between the two groups. (EBL = estimated blood loss; OR = operating room.)

 
Recently, thoracoscopic techniques have been applied to a greater percentage of patients with parapneumonic effusions and empyema. At least two reports demonstrate that thoracoscopic techniques can be used to treat even patients with chronic empyema and trapped lung [12, 13]. Most practitioners use open procedures to treat their patients with chronic empyema, and reserve minimally invasive techniques for early empyema.

Many reports support the use of thoracoscopy for treatment of empyema, and several groups of investigators describe it as the preferred procedure [14–17]. It is clear that these patients are sick and are at risk for both morbidity and mortality. Table 5 summarizes the studies published in the last 20 years in which thoracoscopy was one of the modalities used to treat empyema. The perioperative mortality rate ranges widely, depending on whether 30-day mortality or in-hospital mortality is used. Furthermore, selection of patients may seriously affect the statistics. Chen and colleagues [20] reported 0% mortality in those 30 patients on whom surgery was done, but the overall mortality rate of the 171 patients treated for empyema was 13.5%.


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  		Table 5. Review of Morbidity and Mortality

 
Thoracoscopy appears to be an appropriate method to treat empyema in selected patients, as it permits evacuation of most of the infected material, allowing the remaining infection to be cleared by the body’s immune defenses and the drains that are placed. Our approach was successful in that no patients undergoing thoracoscopic drainage required reoperation for infection. Thus complete expansion of the lung to the chest wall and freedom from the diaphragm allows eradication of the remaining infection. No CT findings could predict which procedure would be necessary; the decision had to be made at surgery.

Although pneumonia was the most common cause of empyema, other causes (empyema after heart surgery, esophageal perforations, and transplantation) were relatively more lethal. Our data suggests that patients referred for surgery earlier may be less likely to require open thoracotomy, and that CT scans do not reliably predict whether open or thoracoscopic techniques will be adequate.


   Discussion
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
References
 
DR DARRYL S. WEIMAN (Memphis, TN): This really wasn’t a prospective randomized trial, so is it really fair to be comparing these two groups? The patients undergoing open thoracotomy were really failures of the thoracoscopic techniques to begin with.

DR ROBERTS: Right, and that is why I said I was not comparing them per se so much as giving the data for purposes of illustration. They really were very different groups.

DR WEIMAN: I have to apologize because the slide went by so fast and I am so old I didn’t get to figure it out. On the slide on operative time, it seemed that the opens took longer, or did I miss that?

DR ROBERTS: Yes.

DR WEIMAN: I missed it?

DR ROBERTS: No, the open procedures did take longer.

DR WEIMAN: That seems to go against everything else in the literature.

DR ROBERTS: In our hands perhaps the reason that may be is that we pretty quickly made a decision as to whether or not we could do a complete procedure thoracoscopically using the criteria that I described, and if not, then made the decision to open. So in essence we try to select those patients that have relatively minimal infection that can be can be completely cleared thoracoscopically.

DR DANIEL L. MILLER (Rochester, MN): Doctor Roberts, was there any correlation in regard to the time of onset of the empyema to the time of surgical intervention that you could predict if you could do it thoracoscopically? We all know that if you can get in there earlier, maybe within 2 to 3 weeks of the initial event, that you might be able to do it via VATS. Did you analysis your data to see if there was a difference between the patients that had an open procedure and ones that were treated thoracoscopically only?

Also, did any of these patients have intrapleural streptokinase or TPA infusion? I know that some institutions favor this approach. If any of your patients had intrapleural infusion, did that correlate if you could do it thoracoscopically compared to the open approach if the empyema had been

One final comment: usually you can drain the empyema without difficulty, but the problem is when you try to reinflate the lung the lung is trapped. It is very difficult and tedious to do a nice decortication thoracoscopically. I wonder if you could comment on your technique for this portion of the procedure. Thank you.

DR ROBERTS: I did have some data in there as to the preoperative days in hospital. The open patients were hospitalized almost 10 days prior to surgery, and for the video-assisted patients it was just under 5.

Streptokinase is not used often at Vanderbilt, either by medical or surgical groups. We did have a few patients early in the series that received streptokinase, but there were so few of them that I didn’t analyze that separately.

DR ALAA Y. AFIFI (Albany, NY): I enjoyed your presentation also. Just a few questions; perhaps you could enlighten us. The first question is in reference to the issue of reoperation on patients that underwent thoracoscopy or open procedures. Two of the open thoracotomy patients required reoperation for empyema, and my question is, why? If it is an open procedure, could you not drain it completely?

Certainly the other issue is there was a significant increased incidence of reoperation for bleeding postoperatively in the thoracoscopy patients. In other words, 3 of the 57 patients that underwent the video-assisted thoracoscopy approach required reoperation for bleeding. Would you explain the significant difference between these patients and the open thoracotomy patients?

And finally, there was a very significant difference in mortality, with the thoracoscopic approach being essentially zero and the open approach being almost double-digit percentages. What were the significant risk factors, or comorbidity, between both groups?

DR ROBERTS: Thank you for your questions. The reoperations for the open patients were unusual patients who presented essentially with complete opacification of their chest and had empyemas. They underwent decortication and pleurectomy, had multiple chest tubes, and then had need for recurrent procedures for limited collections. For instance, two of the patients had HIV disease. So it is possible that that is the explanation for the three reoperations for empyema in the open group.

In the thoracoscopic groups, we did pleurectomies on 45% of the patients. Three of those thoracoscopic pleurectomy patients required reoperation. I have learned that when I do pleurectomies thoracoscopically I am very cautious as to whether or not we have completely controlled the bleeding.

And then, finally there is no question that the groups are different and that is why the mortality was very different. Most of the patients who had open procedures were in the intensive care unit intubated, sick, and on pressors. All of the patients that were done completely thoracoscopically were not intubated, and were not ICU patients. So, again, I included those data for purposes of illustration more than anything else. I don’t think the groups can really be compared, because they were very different.

DR RUSSELL R. KRAEGER (St. Louis, MO): I enjoyed the paper very much and I have one question and then a comment. I was wondering what percentage of your patients had preoperative thoracentesis, and if they did, were there any characteristics that you could predict from the thoracentesis data as to who would require open versus VATS?

And my comment is, I thought that one slide said that 20% of your VATS patients required reintubation, or was that a misprint? I just don’t understand where that would come from.

DR ROBERTS: No, that was a misprint. I don’t have data, at least I did not analyze the data with respect to findings from preoperative thoracenteses might predict thoracotomy as opposed to thoracoscopy. One group of the patients were patients who had malignant empyemas, that is, patients who had had multiple thoracenteses for malignant effusions and then developed empyemas afterwards apparently as a complication from their thoracenteses. But that is all the data that I have about thoracentesis as it relates to this presentation.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 

  1. Andrews N.C., Parker E.F., Shaw R.P., et al. Management of non-tuberculous empyema. Am Rev Respir Dis 1962;85:935-936.
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