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Ann Thorac Surg 2003;76:1849-1853
© 2003 The Society of Thoracic Surgeons

Original article: general thoracic

Intrapleural fibrinolytic treatment of multiloculated postpneumonic pediatric empyemas

Cemal Ozcelik, MDa*, Ilhan Inci, MDb, Ozgur Nizam, MDc, Serdar Onat, MDa

a Thoracic Surgery Department, Dicle University School of Medicine, Diyarbakir, Turkey
b Thoracic Surgery Department, Adnan Menderes University School of Medicine, Diyarbakir, Turkey
c Thoracic and Cardiovascular Surgery Department, Zonguldak State Hospital, Turkey, Diyarbakir, Turkey

Accepted for publication June 5, 2003.

* Address reprint requests to Dr Ozcelik, Thoracic Surgery Department, Dicle University School of Medicine, Diyarbakir, Turkey.
e-mail: cozcelik{at}dicle.edu.tr


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
BACKGROUND: Progression of empyema, with the development of fibrinous adhesions and loculations, makes simple drainage difficult or impossible. The appropriate management remains controversial. Intrapleural fibrinolytic treatment to facilitate drainage of loculated empyema instead of open thoracotomy has been advocated since the 1950s. The aim of this study was to assess the effectiveness of intrapleural fibrinolytic treatment in postpneumonic pediatric empyemas.

METHODS: In our clinic, we used intrapleural fibrinolytic agents in 72 pediatric patients with multiloculated empyema between 1994 and 2002. Streptokinase, 250,000 U in 100 mL of 0.9% saline solution (59 patients), and urokinase, 100,000 U in 100 mL of 0.9% saline solution (13 patients), were instilled daily into the chest tube, and the tube was clamped for 4 hours followed by suction. This treatment was continued daily for 2 to 10 days until resolution was demonstrated by chest radiograms or computed chest tomography.

RESULTS: The rate of drainage after fibrinolytic treatment was increased 73.77%. Treatment was ineffective in 14 (19.44%) of 72 patients who underwent fibrinolytic instillation. Treatment was discontinued because of allergic reaction and pleural hemorrhage in 1 patient, and because of development of bronchopleural fistula in another one. The regimen was completely successful in 43 (59.72%) patients, and partially successful in another 15 (20.83%). Twelve of those patients who had failure eventually required decortication and recovered completely. One patient died of sepsis and pleural hemorrhage; another patient died because of food aspiration.

CONCLUSIONS: In all patients with loculations except those with a bronchopleural fistula, intrapleural fibrinolytic treatment should be tried. Thus, the majority of children with loculated empyemas can be treated successfully without invasive interventions, such as thoracoscopic debridements or open surgery.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
The use of intrapleural fibrinolytic agents for empyema thoracis was first described by Tillet and Sherry in 1949 [1]. Since that time, reports have been sporadic about intrapleural fibrinolytic therapy [2–8]. In the fibrinopurulent phase of empyema, multiloculations may develop, and this condition may be resistant to catheter or tube drainage and represent difficult management problems. Therefore, to obtain an adequate drainage, use of intrapleural fibrinolytic agents and thoracoscopic debridement are alternative modalities at this phase [9]. Delays in accurate diagnosis and, thus, effective management can prolong the patient's illness and result in the need for extensive surgical interventions [10–12]. As a result, the optimal therapeutic approach to complicated empyema has yet to be defined, and most likely depends on accurate staging of the pleural disease. As reported by numerous investigators, decortication may be the most effective way to evacuate the pleural debris, reexpand the trapped lung, and shorten the hospital stay. However, it is an invasive intervention, and this invasive approach must be questioned. We think that intrapleural fibrinolytic instillation is an alternative approach both to thoracoscopic debridement and to surgery in loculated postpneumonic empyema in children.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Between 1990 and 2002, 501 children were hospitalized with parapneumonic empyema at the Department of Thoracic Surgery, Dicle University Research Hospital. Since December 1994, we began using intrapleural fibrinolytic agent to manage multiloculated empyema thoracis in addition to conventional treatment. After the findings from physical examinations and roentgenologic studies, we made a more precise diagnosis of pleural effusion in suspected cases with pleural aspiration. The fluid was sent for culture, Gram staining, and biochemical analysis. After the diagnosis of empyema was made, a chest tube was inserted in patients who had either grossly purulent pleural fluid aspirated or one of the following biochemical measurements in their effusion: (1) glucose level less than 40 mg/dL, (2) lactate dehydrogenase level greater than 1,000 IU/L, (3) positive pleural fluid microbiology culture or Gram stain revealing organism, or (4) white blood cell count greater than 1,000/mL.

Initially all patients were treated with broad-spectrum antibiotics and later with sensitive drugs. After chest tube insertion, drainage from the chest tube was recorded every day, and standard posteroanterior and lateral chest radiograms were taken daily.

Inclusion criteria
During the treatment course, computed thorax tomography or ultrasonography was obtained according to the patients' clinical response and improvement of radiograms. Basic indication for the use of intrapleural fibrinolytic treatment (IPFT) in pleural empyema is the presence or expectation of inadequate drainage. The criteria we used were as follows: (1) poor drainage despite an appropriately positioned, patent chest tube; (2) multiple loculi as depicted by septations on computed tomographic scan or ultrasonography; or (3) presumed multiloculation as indicated by the initial drainage of a volume of fluid less than expected by imaging studies. Patients were excluded from the study if they had a bronchopleural fistula.

Fibrinolytic agent instillation
For intrapleural fibrinolytic instillation, the method described by Robinson and colleagues was used [2]. The chest tube was clamped and streptokinase (SK, 250,000 U; Streptase; Hoechst, Istanbul, Turkey) or urokinase (UK, 100,000 U; Abbott, Istanbul, Turkey) in 100 mL of saline solution, was instilled by means of the thoracostomy tube. Tubes remained clamped for a period of 4 hours. After unclamping, tubes were placed back on suction, and drainage was recorded daily. During fibrinolytic treatment, patients were assessed for resolution of clinical symptoms, increased chest tube drainage, and evidence of radiologic improvement. Patients were also observed for signs of anaphylaxis, respiratory decompensation, chest pain, and bleeding. Coagulation factors were routinely assessed before and after instillation of the fibrinolytic treatment. In patients without clinical and radiologic improvement, no change in pleural fluid drainage, occurrence of bronchopleural fistula, or in whom allergic reaction developed, fibrinolytic treatment was discontinued. In those patients clinical judgment was made according to computed tomographic scan of the chest. In patients successfully treated with fibrinolytic agents, chest tubes were removed.

Complete response was defined as resolution of symptoms and signs of infection with complete drainage of fluid and no residual space radiographically. Partial responders had resolution of clinical symptoms and signs with minimal residual space, less than one quarter of the involved hemithorax, radiographically. Failure was defined as incomplete drainage of fluid or residual space more than one quarter of the involved hemithorax. If patients had incomplete drainage, or had no decrease in cavity size despite complete drainage, they were offered decortication.


   Results
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 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Seventy-two of 346 patients (20.8%) since 1994 with multiloculated empyemas were treated with fibrinolytic agents. Patients' demographics and radiographic findings are shown in Table 1.


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  		Table 1. Characteristics of 72 Patients With Intrapleural Fibrinolytic Treatment

 
Pleural fluid analysis was made in all patients. Glucose and lactate dehydrogenase levels could only be obtained in pleural fluid analysis. We had no opportunity to assess pleural fluid pH levels. In 3 of the patients, glucose level was above 40 mg/dL and in 2 patients lactate dehydrogenase level was less than 1,000 U/L. All patients had 2 to 45 days of antibiotic therapy before thoracentesis. Thus, only 49 patients (68.05%) had bacteria in the pleural fluid culture. Pathogenic Staphylococcus aureus grew in 32 (44.44%) pleural fluid cultures, and Pseudomonas species in 9 pleural fluid cultures. There was no growth in 23 (31.94%) pleural fluid cultures.

Response rates are shown in Table 1. Total drainage before IPFT was 495.57 ± 478 mL. Total net drainage after IPFT was 365.19 ± 352.36 mL. The rate of drainage after fibrinolytic treatment was increased 73.77%.

Of the 72 patients, 59 were treated with SK. Urokinase solution was not available most of the time during this study. Four patients reported transient pain during streptokinase therapy that was easily controlled with oral acetaminophen. None of the other patients, excluding one with streptokinase therapy, experienced fever, bleeding, or any allergic reactions. The coagulation factors of all our patients remained within normal limits before and after IPFT. All patients, excluding 8, had an increase in chest tube drainage within 24 hours after instillation of fibrinolytic agent, with volume of drainage considerably greater than instilled. Most of the improved drainage was within 48 hours.

Complete response was obtained in 43 (59.72%) patients. Partial response was obtained in 15 (20.83%) patients. In none of these patients was surgery indicated because of a pleural pouch. These patients were discharged from the hospital in an asymptomatic status on oral antibiotic treatment. In these patients, weekly follow-up was performed; this showed that the pleural pouch disappeared and the lungs were reexpanded at the end of the second week.

There were 14 failures (19.44%). In 1 patient treated with SK, IPFT was discontinued because of hemorrhage. Drainage was hemorrhagic on the third day of treatment. That case was in septic condition, and pneumonia was persisting. He died 1 day after cessation of IPFT. Another child died because of food aspiration during IPFT. In 1 patient, a bronchopleural fistula developed on the eighth day of IPFT and treatment was stopped. A large pleural pouch was present in 7 patients, and incomplete drainage remained in 5 patients; they underwent decortication. In 7 of these patients there was pleural opacification on their radiograms before IPFT. Although 5 patients were suitable candidates for thoracoscopic debridement, thoracoscopy could not be performed because of lack of technical facilities.

No postoperative complications occurred in the patients who underwent thoracotomy, and they were discharged after a mean hospital stay of 10 days. They completely recovered after thoracotomy.


   Comment
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 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
The treatment options in pediatric empyemas include repeated thoracentesis, closed-tube thoracostomy, image-directed intrapleural catheter drainage, intrapleural fibrinolytic therapy, video-assisted thoracic surgical (VATS) decortication, and thoracotomy with decortication. Unfortunately, results with these treatment regimens have been highly variable [13].

In large part, the variable success observed with different therapeutic strategies is related to the stage of the empyema at the time of treatment [14]. There are generally accepted to be three stages of empyema [10, 15, 16]. Stage 1, also called the exudative phase, usually responds well to antibiotics and thoracentesis or chest tube drainage. In stage 2, the fibrinopurulent stage, the previously sterile pleural effusion becomes infected, with accumulation of polymorphonuclear cells and debris. The fluid is more viscous, and fibrin deposition may lead to multiple loculations. In this stage antibiotics with a properly positioned chest tube may result in cure. Failures are the result of improperly positioned chest tubes, loculations, or early peels trapping the lung. The transition from stage 1 to 2 may occur quickly, often within 24 to 48 hours. Stage 3 empyema (organizing empyema) is chronic and characterized by a thick, inelastic pleural peel that traps and compresses the lung. This phase requires antibiotics and decortication to obtain expansion of the underlying lung.

Determination of the stage of the empyema has been reported to be crucial in choosing an appropriate therapeutic option [12, 17–19]. Duration of symptoms has been suggested as one means of estimating the stage of the empyema [12]. However, an empyema can progress to organization within 1 week of onset. In our patients the mean time before tube thoracostomy was 16.80 days (range, 2 to 30 days). Staging that is performed according to the duration of symptoms could have classed stage 3 patients as stage 2 patients. Thus, we think that staging on the basis of duration of symptoms cannot give the most accurate result.

The use of intrapleural fibrinolytic agents is another option to facilitate drainage and lung expansion in stage 1 and 2 empyemas inadequately treated by a chest tube. Intrapleural fibrinolytic agents have been used in the treatment of thoracic empyema since the 1950s [20]. This type of treatment has been largely overlooked by thoracic surgeons in the last several decades [2]. One reason for this lack of enthusiasm is reported to be the variable results and side effects of the fibrinolytic agent SK used exclusively in the earlier studies.

Several reports have documented successful drainage of multiloculated empyema using SK and UK administrated through a single chest tube [2, 21–23]. In recent reported series on IPFT, the success rates average 44% to 100% [4, 6, 7, 23–28]. Temes and associates [24] performed IPFT in all 26 patients who had been sent for decortication. There was a trend toward significance in the duration of empyema before treatment, with nonresponders having longer durations (mean, 4.50 ± 3.25 versus 2.15 ± 1.86 weeks; p = 0.088). In his study, the complete recovery rate was 62%, the partial recovery was 8%, and the no recovery rate was 31%. Thus more than two thirds of patients with traditional indication for decortication for empyema thoracis were treated successfully with IPFT and without thoracotomy. Robinson and coworkers [2] described 13 patients treated with intrapleural SK or UK instillations. They reported 77% success rate and no treatment-related morbidity or mortality.

Instillation of UK to loculated pleural effusions was first reported in 1989 by Moulton and colleagues [29]. They treated 5 patients with infected hemothoraces and 8 patients with empyema. They reported 92% success rate without any complications. Jerges-Sanchez and associates [23], in a multicenter trial, reported 48 cases treated with intrapleural SK instillation with a 92% success rate. Only 4 patients required surgical treatment. Moulton and coworkers [26] reported 118 patients with complicated pleural fluid collection treated with intracavitary UK. Decortication was performed in only one of these patients, who had a chronic sterile hemothorax. Their overall success rate was 94% (111 of 118 patients) without any complication. Bergh and associates [7] reported 38 cases treated with SK. Radiologic improvement was observed in 30 patients without any serious complications, and there was no need for decortication.

Complications of the therapeutic use of intrapleural fibrinolytic agents are infrequent. Berglin and colleagues [30] reported that the use of intrapleural SK has caused no evidence of coagulation effects. However, Rosen and associates [28] reported a single case of a major hemorrhage after intrapleural SK instillation. This has been attributed to systemic absorption of the agent. We also observed the same side effect in one of our cases. Other systemic side effects with intrapleural SK are fever as high as 40°C and pleural pain [28]. Toxic responses such as arthralgias, nausea, malaise, and headache were also reported earlier with this agent [31], although they appear to be less frequent with the purified form of SK [4]. Anaphylaxis and acute hypoxemic respiratory failure, although very uncommon, have also been reported [32, 33]. Urokinase has the major advantage of being nonantigenic and nonpyrogenic. On the other hand, Frye and coworkers [33] reported a patient who exhibited acute hypoxemic respiratory failure after the intrapleural instillation of both SK and UK 24 hours apart. Hypoxemia is thought to result most likely from a direct effect of the products of fibrinolysis on the pulmonary circulation.

Thoracoscopic debridement and irrigation is reported to be used as a first-line treatment in empyema thoracis, and is thought to be safe and atraumatic [34]. These authors advocate that this technique is well tolerated and produces rapid drainage of pus with resolution of pyrexia and associated toxemia. They also add that if the operation fails it does not exclude the use of further surgical measures. Mackinlay and associates [35] reported 31 patients in the fibrinopurulent phase treated with VATS and compared this group with 33 patients treated by formal thoracotomy. They stated that VATS treatment had the same success rate as open thoracotomy but offered substantial advantages over thoracotomy in terms of resolution of the disease, hospital stay, and cosmesis. In our center VATS is not available for pediatric patients; however, we think that loculated pediatric pleural empyemas may be treated by VATS, but it requires general anesthesia, which may be a major drawback of the procedure.

No consensus exists regarding the optimal agent, dose, and treatment interval. Although success rates of up to 92% with loculated empyema have been reported, accurate staging of empyema is critical for choosing the appropriate patient to undergo fibrinolytic therapy [2, 21, 22].

In conclusion, the optimal management of multiloculated empyema remains to be clarified. Multiloculated empyema does not appear to preclude an initial trial of chest tube drainage or IPFT. Our 80% success rate indicates that IPFT in pediatric multiloculated empyema is a safe procedure and should be considered as a first-line option before proceeding with VATS or open surgical techniques.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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