Intrapleural fibrinolytic treatment of multiloculated postpneumonic pediatric empyemas Cemal Ozcelik, Ilhan Inci, Ozgur Nizam and Serdar

Onat Ann Thorac Surg 2003;76:1849-1853

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Intrapleural Fibrinolytic Treatment of Multiloculated Postpneumonic Pediatric Empyemas

Cemal Ozcelik, MD, Ilhan Inci, MD, Ozgur Nizam, MD, and Serdar Onat, MD
Thoracic Surgery Department, Dicle University School of Medicine, Diyarbakir, Thoracic Surgery Department, Adnan Menderes University School of Medicine, and Thoracic and Cardiovascular Surgery Department, Zonguldak State Hospital, Turkey

Background. Progression of empyema, with the development of brinous adhesions and loculations, makes simple drainage difcult or impossible. The appropriate management remains controversial. Intrapleural brinolytic 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 brinolytic treatment in postpneumonic pediatric empyemas. Methods. In our clinic, we used intrapleural brinolytic 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 brinolytic treat-

ment was increased 73.77%. Treatment was ineffective in 14 (19.44%) of 72 patients who underwent brinolytic instillation. Treatment was discontinued because of allergic reaction and pleural hemorrhage in 1 patient, and because of development of bronchopleural stula 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 stula, intrapleural brinolytic 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. (Ann Thorac Surg 2003;76:1849 53) 2003 by The Society of Thoracic Surgeons

he use of intrapleural brinolytic agents for empyema thoracis was rst described by Tillet and Sherry in 1949 [1]. Since that time, reports have been sporadic about intrapleural brinolytic therapy [2 8]. In the brinopurulent phase of empyema, multiloculations may develop, and this condition may be resistant to catheter or tube drainage and represent difcult management problems. Therefore, to obtain an adequate drainage, use of intrapleural brinolytic agents and thoracoscopic debridement are alternative modalities at this phase [9]. Delays in accurate diagnosis and, thus, effective management can prolong the patients 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 dened, 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
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@dicle.edu.tr.

must be questioned. We think that intrapleural brinolytic instillation is an alternative approach both to thoracoscopic debridement and to surgery in loculated postpneumonic empyema in children.

Material and Methods

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 brinolytic agent to manage multiloculated empyema thoracis in addition to conventional treatment. After the ndings from physical examinations and roentgenologic studies, we made a more precise diagnosis of pleural effusion in suspected cases with pleural aspiration. The uid 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 uid 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 uid microbiology culture or Gram stain revealing organism, or (4) white blood cell count greater than 1,000/mL.
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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.

Table 1. Characteristics of 72 Patients With Intrapleural Fibrinolytic Treatment

Variable Age (y) Sex (female/male) Involved side (right/left) Mean time before drainage (d) Mean length of hospitalization (d) Mean drainage before IPFT (mL) Mean length of IPFT (d) Mean drainage with IPFT (mL) Radiogram Total opacication Mediastinal shift Pleural opacication Pleural opacication scoliosis Response rate Complete responsea Partial response Failureb
a

Mean (range) 5 (0.4115) 72 (29/43) 72 (42/30) 16.80 (230) 20.84 (8 44) 495.57 (30 2,400) 4.73 (210) 365.19 (100 1,600) 38 29 20 12 43 (59.7%) 15 (20.8%) 14 (19.4%)

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 brinolytic 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 uid less than expected by imaging studies. Patients were excluded from the study if they had a bronchopleural stula.

Fibrinolytic Agent Instillation

For intrapleural brinolytic 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 brinolytic 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 brinolytic treatment. In patients without clinical and radiologic improvement, no change in pleural uid drainage, occurrence of bronchopleural stula, or in whom allergic reaction developed, brinolytic treatment was discontinued. In those patients clinical judgment was made according to computed tomographic scan of the chest. In patients successfully treated with brinolytic agents, chest tubes were removed. Complete response was dened as resolution of symptoms and signs of infection with complete drainage of uid 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 dened as incomplete drainage of uid 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.

In all of these patients, a minimal pleural pouch remained enzymatic b debridement of pleural debris. None of them required operation. A large pleural pouch remained in 7 patients, and there was incomplete drainage in 5 patients. All required decortication. IPFT intrapleural brinolytic treatment.

Results
Seventy-two of 346 patients (20.8%) since 1994 with multiloculated empyemas were treated with brinolytic agents. Patients demographics and radiographic ndings are shown in Table 1. Pleural uid analysis was made in all patients. Glucose and lactate dehydrogenase levels could only be obtained in pleural uid analysis. We had no opportunity to assess pleural uid 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 uid culture. Pathogenic Staphylococcus aureus grew in 32 (44.44%) pleural uid cultures, and Pseudomonas species in 9 pleural uid cultures. There was no growth in 23 (31.94%) pleural uid 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 brinolytic 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 brinolytic agent, with volume of drainage

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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 stula 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 opacication 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
The treatment options in pediatric empyemas include repeated thoracentesis, closed-tube thoracostomy, image-directed intrapleural catheter drainage, intrapleural brinolytic 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 brinopurulent stage, the previously sterile pleural effusion becomes infected, with accumulation of polymorphonuclear cells and debris. The uid is more viscous, and brin 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, 1719]. 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 brinolytic agents is another option to facilitate drainage and lung expansion in stage 1 and 2 empyemas inadequately treated by a chest tube. Intrapleural brinolytic 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 brinolytic 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, 2123]. In recent reported series on IPFT, the success rates average 44% to 100% [4, 6, 7, 2328]. Temes and associates [24] performed IPFT in all 26 patients who had been sent for decortication. There was a trend toward signicance 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 rst 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 uid 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 brinolytic agents are infrequent. Berglin and colleagues [30] reported that the use of intrapleural SK has caused

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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 40C 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 puried 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 brinolysis on the pulmonary circulation. Thoracoscopic debridement and irrigation is reported to be used as a rst-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 brinopurulent 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 brinolytic therapy [2, 21, 22]. In conclusion, the optimal management of multiloculated empyema remains to be claried. 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 rst-line option before proceeding with VATS or open surgical techniques.

References
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trapleural streptokinase as adjunctive treatment for persistent empyema in pediatric patients. Chest 1993;103:1190 3. Moulton JS, Moore PT, Mencini RA. Treatment of loculated pleural effusions with transcatheter intracavitary urokinase. AJR Am J Roentgenol 1989;153:9415. Berglin E, Ekroth R, Teger-Nilsson AC, William-Olsson G. Intrapleural instillation of streptokinase. Effects on systemic brinolysis. Thorac Cardiovasc Surg 1981;29:124 6. Hubbard WN. The systemic toxic responses of patients to treatment with streptokinase-streptodornase. J Clin Invest 1951;30:11714. Goehring WO, Grant JJ. Allergic reaction to streptokinase-

streptodornase solution given intrapleurally. JAMA 1953; 152:1429 30. 33. Frye MD, Jarratt M, Sahn SA. Acute hypoxemic respiratory failure following intrapleural thrombolytic therapy for hemothorax. Chest 1994;105:15956. 34. Ridley PD, Braimbridge MV. Thoracoscopic debridement and pleural irrigation in the management of empyema thoracis. Ann Thorac Surg 1991;51:4614. 35. Mackinlay TAA, Lyons GA, Chimondeguy DJ, Piedras MAB, Angaramo G, Emery J. VATS debridement versus thoracotomy in the treatment of loculated postpneumonia empyema. Ann Thorac Surg 1996;61:1626 30.

INVITED COMMENTARY
Over two millennia have passed since the rst clinical description of pleural empyema by Hippocrates who recommended open incision and drainage. It was not until 1918 that Evarts Graham and the World War I Empyema Commission changed routine therapy to closed intercostal drainage resulting in a dramatic fall in mortality from 75% to 15% in streptococcal empyemas. But despite prompt intercostal tube insertion, some empyemas have already progressed to the multiloculated brinopurulent stage that precludes adequate treatment by simple drainage alone. For these patients, open surgical or thoracoscopic decortication, with its attendant mortality and morbidity, has been traditionally advocated. However, it was in 1949 that Sol Sherry described the rst clinical use of intrapleural streptokinase to facilitate drainage of infected hemothoraces without surgery. Initially, this approach was successful but it soon lost favor because of the toxic side effects of this crude preparation of streptokinase. In subsequent years, a variety of successful clinical series have been published using this conservative, nonsurgical approach using more puried intrapleural brinolytic agents to treat multiloculated pleural empyemas (MPE) in patients that traditionally would have been treated with aggressive thoracotomy and decortication. Almost all published clinical reports of intrapleural brinolysis for MPE involved a predominate adult population with a complete nonsurgical success rate averaging 80% in most series, and with a considerably lower actual hospital cost compared to the surgical approach. The authors of the current report address this problem in the pediatric population in a large single institution, welldocumented series of 72 children who were treated for post-pneumonic MPE with the intrapleural brinolytic agents streptokinase or urokinase. Their results are remarkably similar to the prior adult series with an overall 81% complete recovery rate with minimal morbidity using the nonsurgical intrapleural brinolysis approach. These excellent results now extend the potential indications for this conservative approach to all patient age groups. The key factor in predicting a successful outcome with any intervention, including intrapleural brinolyis for MPE, is appropriate patient selection, as advocated by the authors. In 1962, the American Thoracic Society described the current staging of empyemas into three phases: stage I Exudative stage with thin, free uid which is readily drained by chest tube alone; stage II Fibrinopulent stage where there is early organization with thicker pus, brin and multiloculation, usually requiring more aggressive intervention; and stage III Organizing stage with broblast ingrowth and a thick inelastic pleural peel preventing lung expansion. Fortunately most empyemas are either stage I or II and are amenable to conservative chest tube drainage alone (stage I), with the needed addition of intrapleural brinolysis in stage II. Proper staging of the empyema, as described by the authors, generally predicts who will benet from the nonsurgical approach with brinolytic therapy, and which of the much smaller patient population likely has a stage III empyema requiring open surgical decortication. The authors, as well as most prior series, recommend an initial trial of drainage and possible intrapleural brinolysis in almost all patients with MPE, since computed tomography was not uniformly accurate in predicting which patients would fail brinolyic therapy and require surgery. Since urokinase is no longer available, streptokinase is once again the only practical agent for intrapleural brinolysis, although it has some possible febrile and allergic reactions. As an aside, in my own thoracic surgical practice I continue to successfully treat MPE nonsurgically as described herein, currently using intrapleural streptokinase, but have effectively prevented toxic side effects of this agent by administering a small intravenous dose of methylprednisolone 30 minutes prior to each daily instillation. Doctor Ozcelik and associates are to be commended not only for their excellent results in this difcult patient population, but also for sending the thoracic surgical community a clear message reiterating the effectiveness of this conservative, low morbidity, and low-cost approach to an old but controversial pleural problem. Lary A. Robinson, MD Division of Cardiovascular and Thoracic Surgery Department of Interdisciplinary Oncology H. Lee Moftt Cancer Center and Research Institute 12902 Magnolia Dr Tampa, FL 33612-9497 e-mail: robinson@moftt.usf.edu

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Intrapleural fibrinolytic treatment of multiloculated postpneumonic pediatric empyemas Cemal Ozcelik, Ilhan Inci, Ozgur Nizam and Serdar Onat Ann Thorac Surg 2003;76:1849-1853
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