Management of postpneumonic empyemas in children

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1 European Journal of Cardio-thoracic Surgery 25 (2004) Management of postpneumonic empyemas in children Cemal Ozcelik a, *, Refik Ülkü a, Serdar Onat a, Zerrin Ozcelik b, Ilhan Inci c, Omer Satici d a Department of Thoracic Surgery, Dicle University School of Medicine, Diyarbakir, Turkey b Department of Pharmacology, Dicle University School of Medicine, Diyarbakir, Turkey c Department of Thoracic Surgery, Adnan Menderes University School of Medicine, Diyarbakir, Turkey d Department of Biostatistics, Dicle University School Of Medicine, Diyarbakir, Turkey Received 29 June 2003; received in revised form 9 December 2003; accepted 18 December 2003 Abstract Objectives: Despite continued improvement in medical therapy, pediatric empyema remains a challenging problem for the surgeon. Multiple treatment options are available; however, the optimal therapeutic management has not been elucidated. The aim of this study is to assess different treatment options in the management of postpneumonic pediatric empyemas. Methods: A retrospective review was performed of pediatric patients admitted to Dicle University School of Medicine Thoracic and Cardiovascular Surgery Department between 1990 and 2002, with the diagnosis of empyema. Data tabulated included patient demographics, presentation, treatment and outcome. Results: There were 515 children (289 boys and 226 girls) with a mean age of 4.7 ranging from 18 days to 15 years. Empyema was secondary to pneumonia in all children. The most common radiologic finding was pleural effusion in 285 patients (55.32%). Staphylococcus aureus was the most frequently encountered organism and found in 105 patients (20.38%). Pleural fluid cultures were negative in 195 patients (37.86%). In addition to antibiotic therapy, initial treatment included serial thoracenthesis ðn ¼ 29Þ; chest tube drainage alone ðn ¼ 214Þ; chest tube drainage with intrapleural fibrinolytic therapy ðn ¼ 72Þ; chest tube drainage with primary operation ðn ¼ 191Þ; and primary operation without chest tube drainage ðn ¼ 9Þ: Overall response rate with fibrinolytic treatment (complete and partial response) was obtained in 58 patients. In addition to decortication pulmonary resections were performed in 12 patients. Overall mortality rate was 1.55%. There was no operative mortality. Postoperative morbidity included wound infection in 21, delayed expansion in 8, and atelectasis in 35 patients. Conclusions: Multiple therapeutic options are available for the management of pediatric empyema. Depending on stages, every option has a role in the treatment of postpneumonic pediatric empyema. In the absence of bronchopleural fistula, intrapleural fibrinolytic treatment should be tried in all patients with multiloculations in stage II empyema. In the absence of pneumonia, decortication for empyema is a safe approach with low mortality and morbidity rates. q 2003 Elsevier B.V. All rights reserved. Keywords: Empyema; Fibrinolytic treatment; Decortication; Postpneumonic 1. Introduction Low socioeconomic status, inappropriate antibiotic use, malnutrition, and delay in seeking treatment are contributing factors to the development of empyema in patients with pneumonia [1]. In cases of bacterial pneumonia, pleural effusion can be frequently seen with an incidence of 40% [2]. Although most of parapneumonic effusions can be treated with only the administration of the appropriate antibiotics for the underlying pneumonia, some of them will progress into a complicated parapneumonic effusion or into * Corresponding author. Tel.: þ ; fax: þ address: cozcelik@dicle.edu.tr (C. Ozcelik). a frank empyema [2,3]. When a parapneumonic effusion reaches a complicated one or a frank empyema, controversies begin about the treatment modalities [4,5]. Treatment of empyema is based on early diagnosis, appropriate antibiotic treatment, and prompt drainage of the pleural space [6]. Complete drainage is crucial to controlling pleural sepsis, restoring pulmonary function, and preventing pulmonary fibrosis with entrapment. Available treatment options include tube thoracostomy, image-directed pleural catheters, intrapleural fibrinolytics, thoracoscopic drainage, and thoracotomy with decortication. Success rates with these treatment regimens have been highly variable, most likely related to the stage of empyema at presentation [6 8]. Multiloculated empyemas in the fibrinopurulent stage may /$ - see front matter q 2003 Elsevier B.V. All rights reserved. doi: /j.ejcts

2 C. Ozcelik et al. / European Journal of Cardio-thoracic Surgery 25 (2004) be resistant to catheter or tube drainage and represent difficult management problems [8]. Delays in accurate diagnosis and, thus, effective management, can prolong the patient s illness and result in the need for extensive surgical interventions [9]. 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 [10]. The aim of this study is to assess different treatment options in the management of postpneumonic pediatric empyemas. 2. Materials and methods Hospital records of 515 patients who were treated for postpneumonic empyema were retrospectively reviewed at Dicle University Research Hospital Thoracic Surgery Department between January 1990 and December Children who had an empyema that was associated with trauma, tuberculous empyema, hydatid disease, or foreign body retention were excluded from the study. Videoassisted thoracoscopic surgery (VATS) was not used in any of the patients. Diagnosis of pneumonia and empyema was established based on a combination of physical examination, chest X-rays, and pleural fluid chemical and culture analysis. The diagnosis of empyema required one of the following criteria: (1) grossly purulent pleural fluid documented by thoracentesis, (2) positive Gram stain, (3) pleural fluid glucose level less than 50 mg/dl, (4) pleural fluid level ph below 7.00, (5) pleural fluid lactic dehydrogenase (LDH) level above 1000 IU/l [2]. An ultrasonography or computed tomography of the chest was obtained both to differentiate pleural complications from an intraparenchymal process, to determine the best site for thoracentesis or the insertion of a thoracostomy tube when pleural effusions were difficult to access, and to detect loculations. Initially all patients were treated with broadspectrum antibiotics and later with more sensitive drugs. In uncomplicated parapneumonic effusions, intermittent therapeutic thoracentesis combined with the use of appropriate antibiotic therapy was used (Fig. 1) Tube thoracostomy indications In complicated parapneumonic effusions and in grossly purulent pleural fluid, closed-tube thoracostomy was performed immediately. In patients without bronchopleural fistula, pleural lavage with povidone-iodinated serum physiologic fluid via the chest tube was carried out immediately. In patients with inadequate drainage thoracic ultrasonograms and/or CT were obtained for the presence and sites of the loculations. In these patients, second chest tube, whenever necessary, was inserted to obtain an adequate drainage before When a complete drainage was obtained, the chest tube was removed and the patient was discharged from the hospital after a control chest X-ray obtained the following day Intrapleural fibrinolytic treatment (IPFT) Since 1994, we started using intrapleural streptokinase in patients with an inadequate drainage following chest tube insertion. The criteria we use is as follows: (1) poor drainage despite an appropriately positioned, patent chest tube; (2) multiple loculi as depicted by septations on CT scan, or ultrasonography; or (3) presumed multiloculations as indicated by the initial drainage of a volume of fluid less than expected by imaging studies. The chest tube was clamped and streptokinase 2500 units/ml, or urokinase 1000 units/ml was instilled into the tube of the patients. Tubes remained clamped for a period of 4 h. After unclamping, tubes were placed back on suction and drainage was recorded daily. During this period, clinical course was evaluated by monitoring for fever, chest tube drainage, WBC counts, erythrocyte sedimentation rate (ESR) and daily chest radiograms. Coagulation parameters and hematocrit levels were routinely monitored. Patients were also observed for signs of anaphylaxis, respiratory decompensation, chest pain and bleeding. In patients without clinical and radiological improvement, or no increase in pleural fluid drainage, or in whom allergic reaction developed, fibrinolytic treatment was discontinued. In those patients clinical judgment was made according to CT 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 clinical symptoms and signs with minimal residual space radiographically. Failure was defined as incomplete drainage of fluid or no decrease in cavity size despite complete drainage. Thoracoscopic debridement was not performed due to lack of technical facilities Timing and indication of decortication Patients whose conditions did not improve clinically with i.v. antibiotics and closed-tube thoracostomy drainage or intrapleural fibrinolytic therapy were considered for decortication. In those in whom initial thoracentesis was negative or minimal on admission, primary decortication without trying chest tube drainage was carried out if radiological investigation revealed solidified pleural material and significant compression of the lung. In all cases, decortication was performed via lateral thoracotomy incision with sparing of both the latissimus dorsi and serratus anterior muscles. The pleural space was entered through the fifth intercostal space. Rib resection was not performed to gain exposure. The intrapleural gelatinous debris and fibrin mass were evacuated. There was inclination for the lung to

3 1074 C. Ozcelik et al. / European Journal of Cardio-thoracic Surgery 25 (2004) Fig. 1. Management of childhood empyema. reexpand without formal decortication. Therefore, the fibrinous peel on the surface of the visceral and parietal pleura was carefully removed. After mobilizing the lung, a plane of cleavage between the visceral pleura and the peel could usually be initially started on the surface of the lobes avoiding the interlobar fissure. Patients could be categorized into five initial treatment groups: Group I: thoracentesis alone, Group II: chest tube drainage alone Group III: chest tube drainage with intrapleural fibrinolytic therapy Group IV: chest tube drainage with primary operative management Group V: primary operative management without chest tube drainage. Student s t-test was used for statistical evaluation. P-value less than 0.05 was accepted as significant statistically. Patients were regularly seen in the policlinic 10 days, 1 and 3 months after discharge. Mean long-term follow-up was 3.8 years (6 months to 13 years).

4 C. Ozcelik et al. / European Journal of Cardio-thoracic Surgery 25 (2004) Table 1 Chest X-ray findings on admission Tension pneumothorax 35 (6.79) Total opacification 118 (22.91) Pleural effusion 285 (55.33) Hydropneumothorax 51 (9.90) Bilateral pleural effusion þ pneumonia 26 (5.04) Total 515 (100) 3. Results There were 515 children (289 boys and 226 girls) with a mean age of 4.7 ranging from 18 days to 15 years. All patients underwent plain chest radiography and 87 had computed chest tomography, and 40 had chest ultrasonography before initial thoracentesis. Radiological findings at the time of admission are shown in Table 1. Pleural fluid culture results are shown in Table 2. Staphylococcus aureus was the most common causative microorganism (20.38%), whereas pleural fluid culture was negative in 195 cases (37.86%). Of 61 patients with bronchopleural fistula, 48 underwent thoracotomy (78.68%) Treatment of empyema Group I This group was consistent with stage I empyema. All 29 patients were treated with appropriate intravenous antibiotics and serial thoracentesis Group II This group was consistent with stage II empyema. Two hundred and fourteen patients were treated with closed chest tube drainage and pleural irrigation. Before fibrinolytic use, there were 155 children with empyema. Seventy-one (45%) were treated with closed-tube thoracostomy, 84 (55%) underwent decortication. The use of intrapleural fibrinolytic treatment (IPFT) decreased decortication rates in patients with stage II multiloculations. Table 2 Pleural fluid cultures of the patients Pseudomonas 59 (11.45) Staphylococcus aureus 105 (20.38) Escherichia coli 53 (10.29) Proteus 29 (5.63) Streptococcus pneumonia 26 (5.04) Pneumococcus 48 (9.32) No growth 195 (37.86) Total 515 (100) (%) (%) Group III This group was consistent with stage II empyema. Urokinase treatment was received by 13 patients because it was not always available although we preferred it as the fibrinolytic agent. Fifty-nine patients received streptokinase. All patients, excluding eight, had an increase in chest tube drainage within 24 h following instillation of fibrinolytic agent, with volume of drainage considerably greater than instilled. Most of the improved drainage was within 48 h. Total drainage prior to fibrinolytic treatment was ^ 478 ml. Total net drainage after fibrinolytic treatment was ^ ml. The rate of drainage after fibrinolytic treatment was 73.77%. Length of fibrinolytic treatment was 4.73 days (range 2 10). Two patients reported transient pain during streptokinase therapy that was easily controlled with oral acetaminophen. None of the other patients developed fever, bleeding or any allergic reactions. The coagulation parameters of all our patients remained within normal limits before and after fibrinolytic therapy. Complete response was obtained in 43. Partial response was obtained in 15. In these patients, weekly follow-up was done and follow-up showed that pleural pouch disappeared and the lungs were reexpanded at the end of the second week. There were 14 failures (19.44%). In one patient treated with streptokinase, 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 one day after cessation of IPFT. Another child died because of food aspiration during IPFT. In one patient, a bronchopleural fistula developed on the eighth day of IPFT and treatment was stopped. Large pleural pouch was present in seven patients and incomplete drainage remained in five patients and they underwent decortication Group IV This group was consistent with stage III empyema. After chest tube drainage, 191 patients underwent decortication. All had either incomplete drainage or trapped lung on computed chest tomography. In addition to decortication, we performed bilobectomy superior in one, lobectomy in five, wedge resection in five, and segmentectomy in one patient. In one of the patients who underwent lobectomy, the lack of expansion continued and on the 17th postoperative day she underwent Sawamura thoracoplasty [11]. In a patient in whom we performed decortication although the lung was fully hepatized we avoided pneumonectomy. In the postoperative period, antibiotic treatment and repeated bronchoscopic aspirations were of no benefit. Pulmonary perfusion scintigram showed no perfusion in the left lung and he underwent left pneumonectomy on the 84th postoperative day, and was discharged from the hospital 10 days later. He was admitted to the hospital again because of his septic clinical picture due to right-sided pneumonia on the eighth day of his

5 1076 C. Ozcelik et al. / European Journal of Cardio-thoracic Surgery 25 (2004) discharge from the hospital. He was connected to the mechanical ventilation. On the seventh day he died of sepsis Group V This group was consistent with stage III empyema. In nine patients initial thoracentesis was negative or minimal. In these patients we performed decortication as the initial treatment without performing closed-tube thoracostomy after radiological investigation. Treatment groups were classified according to duration of symptoms, duration of chest tube, and length of hospital stay (Table 3). Patients successfully treated with antibiotic and serial thoracentesis alone had a shorter duration of symptoms prior to treatment (10.4 versus 14.4 days in group II, 16.8 days in group III, 19.4 days in group IV, and 19.6 days in group V, P, 0:05; P, 0:003; P, 0:0001; and P, 0:002; respectively, Student s t-test). Also, the comparison of group II and group IV was significant statistically, in favor of group II ðp, 0:0001Þ: According to the duration of chest tube, the comparison of group II and group IV, and the comparison of group III and group IV were significant statistically, in favor of group IV ðp, 0:000Þ: According to the length of hospital stay, comparison of groups I and II, I and III, and I and IV were significant in favor of group I, respectively (P, 0:001; P, 0:007; and P, 0:000). In addition, comparison of group IV and group V was significant in favor of group V ðp, 0:001Þ: 3.2. Morbidity and mortality Eight patients (1.55%) died during the treatment. In five of these patients, there was congestive heart failure and pneumonia at the time of admittance. One patient died because of congestive heart failure and bilateral bronchopneumonia on the fifth and the other died because of congestive heart failure and pneumonia on the seventh day of hospitalization. In one patient with fibrinopurulent phase empyema, intrapleural streptokinase treatment was discontinued because of hemorrhagic drainage. This patient died 1 day later in septic condition. Another patient in chronic Table 3 Comparison of treatment modalities according to duration of symptoms, duration of chest tube, and length of hospital stays Groups Duration of symptoms (day) Duration of chest tube (day) Length of hospital stay (day) Group I ðn ¼ 29Þ 10.4 ^ ^ 6.57 Group II ðn ¼ 214Þ ^ ^ ^ Group III ðn ¼ 72Þ ^ ^ ^ Group IV ðn ¼ 191Þ ^ ^ ^ 5.67 Group V ðn ¼ 9Þ ^ ^ 1.50 phase with fibrinolytic treatment failure died because of food aspiration prior to decortication. Postoperative complications consisted of incisional infection in 21 patients, atelectasis in 35. Wound infection was manifested by seropurulent fluid. Complete resolution was achieved by antibiotics according to culture (Staphylococcus aureus) and dressing twice a day. Atelectasis was treated with respiratory exercise, nasotracheal aspiration, and bronchoscopic aspiration (27 patients). Delayed expansion lasting more than 10 days occurred in eight patients. All required an additional closed-tube thoracostomy. One of these underwent modified Sawamura thoracoplasty and one underwent pneumonectomy. In the group IV only one patient who underwent late left pneumonectomy had been admitted with septic clinical picture due to right-sided pneumonia and died as he did not respond to the intensive treatment. 4. Discussion Bacterial pneumonia is the most common cause of thoracic empyema in the pediatric age group. Pleural effusion during the course of nonspecific bacterial pneumonia progresses to empyema for several reasons including malnutrition, immunodeficiency, irregular antibiotic treatment, delay in diagnosis of pneumonia, contamination during thoracentesis, the tendency for antibiotic treatment in the acute phase in pediatric clinics, and disappearance of the signs and symptoms of pneumonia [1]. The high incidence in 0 3 year age group might be explained by low standards of childcare in overcrowded families. The incidence in this age group correlated with published data [12]. The finding that Staphylococcus aureus was the most common infective agent agrees with other reports [1,13]. As outlined by Mayo [14], the goals of treatment in patients with pediatric empyema are to (1) save life, (2) eliminate the empyema, (3) reexpand the trapped lung, (4) restore mobility of the chest wall and diaphragm, (5) return respiratory function to normal, (6) eliminate complications or chronicity, and (7) reduce the duration of hospital stay. The pursuit of these goals has led to the development of multiple therapeutic options in addition to potent antibiotics for these challenging problems. These options include repeated thoracentesis, closed-tube thoracostomy, image-directed intrapleural catheter drainage, intrapleural fibrinolytic therapy, VATS decortication and thoracotomy with decortication. Unfortunately, results with these treatment regimens have been highly variable. As a result, the optimum therapeutic strategy for empyema has yet to be elucidated. Moreover, the availability of nonoperative alternatives frequently results in delayed surgical consultation, and ultimately, increased patient morbidity and mortality [1,9,15]. In large part, the variable success observed with different therapeutic strategies is related to the stage of the empyema

6 C. Ozcelik et al. / European Journal of Cardio-thoracic Surgery 25 (2004) at the time of treatment [6]. There are generally accepted to be three stages of empyema [16]. Stage I, also called the exudative phase, represents the fluid stage of empyema that usually responds nicely to thoracentesis or chest tube drainage alone. In stage II, 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. The net effect is to make drainage more difficult; however, empyema in the fibrinopurulent stage may still be amenable to chest tube drainage. The transition from stage I to II may occur quickly, often within h. Stage III empyema (organizing empyema) is chronic and characterized by a thick, inelastic pleural peel that traps and compresses the lung. Determination of the stage of the empyema has been reported to be crucial in choosing an appropriate therapeutic option [9]. Duration of symptoms has been suggested as one means of estimating the stage of the empyema [9]. However, an empyema can progress to organization within 1 week of onset. Moreover, not all patients progress through these stages in sequential fashion [17]. In complicated parapneumonic effusion, both serial thoracentesis and chest tube drainage can be advocated as a first-line therapy. There have been some reports of the effectiveness of this procedure after early diagnosis [5,18]. Tube drainage is recommended in children because of its reliability, rather than multiple thoracentesis [7]. Pleural lavage via the chest tube is useful for augmenting drainage and mechanical clearance and various antimicrobial agents can be added to the washing fluid [1,5]. We use pleural lavage via the chest tube in the absence of bronchopleural fistula. LeMense et al. [6] have suggested that this decreases the severity of pleural sepsis while instituting further therapy. It is possible that multiple loculations are actually communicating and can be drained with a single chest tube. Because of the low reported success rate of tube thoracostomy for loculated empyema, alternative approaches have been developed. Intrapleural fibrinolytic agents have been used in the treatment of thoracic empyema since the 1950s [19]. Several reports have documented successful drainage of multiloculated empyema using SK and UK administrated through a single chest tube [7,20]. In the recent reported series on IPFT, the success rates average % [20 22]. Temes [21] performed IPFT in all 26 patients who had been sent for decortication. There was a trend toward significance in the duration of empyema prior to treatment, with nonresponders having longer durations (mean 4.50 ^ 3.25 versus 2.15 ^ 1.86 weeks; P ¼ 0:088). In his study, the CR rate was 62%, the PR 8%, and the NR 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 et al. described 13 patients treated with intrapleural streptokinase or urokinase instillations [7]. They reported 77% success rate and no treatment-related morbidity or mortality. Thompson et al. reported 60 children either receiving intrapleural urokinase or saline. In this randomized study, the primary outcome measure was length of hospital stay. They stated that treatment with urokinase resulted in a significantly shorter hospital stay [23]. In the present study, response rates with fibrinolytic agent was concordant with those rates reported in literature. Thoracoscopic debridement of empyema is advocated in the management of empyema, especially in the presence of loculations [8,24,25]. Thoracoscopic debridement and irrigation is reported to be used as a first-line treatment in empyema thoracis which is thought to be safe and atraumatic [24]. The 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 et al. reported 31 patients in fibrinopurulent phase treated with VATS and compared this group with 33 patients treated by formal thoracotomy [25]. 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. Tonz et al. reported with their limited experience that VATS adds little benefit to the treatment of childhood empyema [26]. In our center VATS is not available for pediatric patients but 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. We do not have any experience about it. The presence of a thick rind with trapped lung is an indication for operation and decortication [1,5,6]. The inability to evacuate fibrinous debris via chest tube is also an indication for decortication. Decortication should be performed as soon as possible if drainage is not effective. It may be an initial treatment instead of wasting time by performing tube thoracostomy and all our patients in group V were benefited from surgical intervention. When the patient s status is suitable for surgery, we recommend this approach because of the decrease in mortality and morbidity, reduction of hospital stay, and discharge of the patient without an open wound. Decortication has few morbidity and mortality rates. Postoperative complications such as atelectasis and delayed expansion are mainly from parenchymal disease. In conclusion, the optimum management of complicated thoracic empyema remains to be clarified. Multiloculated empyema does not appear to preclude an initial trial of chest tube drainage or intrapleural fibrinolytic therapy. In the absence of bronchopleural fistula, IPFT should be tried in all cases of fibrinopurulent phase empyema not responding to closed chest tube drainage. This type of treatment increases the success of conservative treatment. In the absence of pneumonia, decortication for empyema is a safe approach with low mortality and morbidity.

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