ABDULHAMEED AZIZ, 1 JEFFREY M. HEALEY, 1 FAISAL QURESHI, 1 TIMOTHY D. KANE, 1 GEOFFREY KURLAND, 2 MICHAEL GREEN, 3 and DAVID J.

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1 SURGICAL INFECTIONS Volume 9, Number 3, 2008 Mary Ann Liebert, Inc. DOI: /sur Comparative Analysis of Chest Tube Thoracostomy and Video-Assisted Thoracoscopic Surgery in Empyema and Parapneumonic Effusion Associated with Pneumonia in Children ABDULHAMEED AZIZ, 1 JEFFREY M. HEALEY, 1 FAISAL QURESHI, 1 TIMOTHY D. KANE, 1 GEOFFREY KURLAND, 2 MICHAEL GREEN, 3 and DAVID J. HACKAM 1 ABSTRACT Background: Controversy exists regarding the optimal management strategy for children having empyema or parapneumonic effusion as a complication of pneumonia. We hypothesized that video-assisted thoracoscopic surgery (VATS)-assisted drainage of pleural fluid and debridement of the pleural space is superior to a chest tube alone in the management of these patients. We further identified predictive factors namely, presentation, radiographic findings, antibiotic usage, and pleural fluid features that could predict the need for VATS rather than primary chest tube drainage. Methods: Forty-nine pediatric patients with pneumonia complicated by parapneumonic effusion or empyema treated at the Children s Hospital of Pittsburgh ( ) were divided into three groups according to the therapy instituted: Primary chest tube, chest tube followed by VATS, or primary VATS. The groups were analyzed in terms of demographics and outcome, as judged by pleural fluid analysis and hospital resource utilization. Demographic and outcome data were compared among groups using one-way analysis of variance and the Student t-test. Results: All groups were similar with respect to demographics and initial antibiotic usage. Patients undergoing primary VATS had a higher initial temperature, whereas radiographic findings of mediastinal shift and air bronchograms were more likely to be found in patients who underwent primary chest tube placement. Patients undergoing primary VATS demonstrated a significantly shorter total stay and lower hospital charges than the other groups. Forty percent of children started on chest tube therapy failed even with subsequent VATS, necessitating a significantly longer hospital course (18 3 vs days; p 0.05) and higher hospital charges ($50,000 7,000 vs. $29, ) than those having primary VATS. Conclusions: Patients treated by primary VATS had a shorter stay and lower hospital charges than patients treated by chest tube and antibiotic therapy alone. There were no demographic, physiologic, laboratory, or chest radiographic data that predicted the selection of VATS as an initial treatment. These data suggest a strategy of primary VATS as first-line treatment in the management of empyema or parapneumonic effusion as a complication of pneumonia in pediatric patients. 1 Divisions of Pediatric Surgery, 2 Pediatric Pulmonology, and 3 Pediatric Infectious Disease, Children s Hospital of Pittsburgh and the University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania. 317

2 318 ACCUMULATION OF FLUID in the pleural space may follow the development of pneumonia in as many as 28% of children [1 3]. The successful management of such fluid which may either represent a parapneumonic effusion or be contaminated with micro-organisms, leukocytes, and fibrin to form an empyema is a crucial component of the overall care of these patients. Controversy exists regarding the appropriate management strategy for empyema or complicated parapneumonic effusion in children. Current options include primary chest tube placement (either open or with radiologic guidance) or video-assisted thoracoscopic surgery (VATS) with removal of pleural fluid and exudate. Primary chest tube drainage may be favored by some clinicians because of the perceived advantages of radiographic drainage for localized fluid collections, avoidance of general anesthesia, and the smaller thoracostomy tubes used. However, the fibrinous pleural fluid in the setting of empyema often clogs these small drains, resulting in inadequate drainage [7]. Intrapleural administration of fibrinolytics may augment drainage, although this measure is not helpful in all cases [4 6]. Open placement may lead to suboptimal placement of the tip of the tube. These shortcomings have led to the use of primary VATS-assisted drainage of the pleural space in pediatric patients with empyema and parapneumonic effusion [6,8 19]. A VATS-based approach offers the potential for better lung expansion after removal of pleural debris and exudate, excellent magnified vision, optimization of the location of the chest tube, and reduced chest wall and muscle trauma compared with traditional thoracotomy [20]. We therefore hypothesized that primary VATS would be superior to delayed VATS in patients with loculated empyema or complicated parapneumonic effusions. To address this hypothesis, we evaluated primary chest tube therapy, failed chest tube therapy with secondary VATS, and primary VATS in relation to patient outcome. We further categorized the presentation, radiographic findings, and pleural fluid findings in this pediatric cohort. Lastly, we evaluated the role of initial antibiotic treatment within the surgically treated AZIZ ET AL. groups to help guide concomitant pharmacotherapy. Patient selection PATIENTS AND METHODS The Institutional Review Board for Human Subject Research approved the methodology and scope of this retrospective review. The medical records of all non-smoking, previously healthy children up to age 18 years, with no surgical history or history of empyema or parapneumonic effusion, and with a documented pneumonia and empyema/effusion by chest radiograph, who were treated at the Children s Hospital of Pittsburgh from January 1997 through July 2003 were evaluated. The following data were obtained from the chart review: Sex, age, presenting symptoms (cough, fever [temperature 38 C], anorexia, nausea, vomiting, chills, shortness of breath, dehydration, myalgia), duration of symptoms, co-morbidities (asthma, neoplasia, transplant history), and history of empyema. Details of the hospital admission included vital signs on presentation (ventilation rate, heart rate, fever), chest radiographic findings (mediastinal shift, consolidation, effusion, collapse, air bronchogram), antibiotic treatment (drug, duration), surgical procedure (chest tube, chest tube followed by VATS, primary VATS), and pleural fluid content (glucose, lactate dehydrogenase [LDH], protein, white cell count, ph). Final outcome parameters were intensive care unit (ICU) stay, total days in hospital, and total hospital charges. Procedures The patients were divided into three groups according to the therapy instituted: Primary chest tube, initial chest tube placement followed by VATS, or primary VATS. Video-assisted thoracoscopic surgery was performed with the patient under general anesthesia. In certain cases, selective lung ventilation was achieved using either selective mainstem intubation or a bronchial blocker as indicated, although in most cases, lung isolation was not required. With the patient in the lateral decubitus

3 CHEST TUBE VS. VATS IN PEDIATRIC EMPYEMA 319 position, a 5-mm bladeless trocar (Ethicon, Cincinnati, OH) was placed approximately 2 cm inferior to the spine of the scapula. A 5-mm, 30 angled videoscope was then passed into the pleural cavity, and the degree of pleural inflammation and amount of pleural fluid was assessed. The pleural cavity was then gently insufflated to a pressure of 6 10 mm Hg to allow better viewing and to facilitate placement of additional ports. Typically, one additional 5 mm port was placed anterior to the first port, in the mid-axillary line, under direct vision. Through these two ports, pleural fluid was aspirated, and the pleural peel was removed using grasping forceps. If the peel was particularly thick and friable, these ports were increased to 10 mm 12 mm, allowing placement of the 10- mm 45 endoscope if desired and permitting removal of larger pieces of debris. In such cases, a third port (either 5 or 10 mm) was placed to allow combined aspiration and grasping. The procedure was terminated when the lung was maximally freed, and all pockets of fluid were removed, even if some pleural exudate remained. A chest tube was then placed under direct vision, typically through the anterior-most port, and directed toward the apex. The tube was maintained on suction for 48 h. Post-operative pain control typically was achieved with either an epidural catheter or intravenously administered long-acting narcotic agents. The chest tube typically was removed when the drainage was slight ( 50 ml/day) and a chest radiograph showed lung expansion without air leakage. Primary chest tube placement was performed either over a guidewire using ultrasound or computed tomography guidance or through a 1 cm open incision. The presence of a pulmonary peel in the setting of a pleuralbased fluid collection was required to establish the diagnosis of empyema in all cases. Age-appropriate sedation was used in all cases. Patients were managed on either the pediatric surgery service or the general pediatrics service of the Children s Hospital of Pittsburgh. Improvement in clinical course was determined by the combined association of reduced fever, greater appetite and energy, and improvement of the chest radiograph appearance. Failure to improve substantially after 48 to 72 h from initial chest tube placement (continued chest tube drainage 150 ml/24 h, continued fever, no change in chest radiograph infiltrate) led to a decision to perform a VATS pleural debridement. The ultimate decision as to whether an individual child was improving was made by the treating physician using one or a combination of these criteria, along with findings on physical examination as to how ill the child was. After performance of VATS drainage, no patient required re-operation. Statistical analysis Comparisons were made using the Student t-test, one-way analysis of variance (ANOVA) with Tukey-Kramer post-test analysis, or nonparametric ANOVA, as appropriate. Statistical significance was determined at p 0.05 in all cases. RESULTS Patient demographics and clinical features at presentation Forty-nine children with a mean age of 5.8 years had empyema or parapneumonic effusion as a complication of community-acquired pneumonia. These patients were treated with either primary chest tube alone (n 21), chest tube followed by VATS (n 15), or primary VATS (n 13). Four of the children had a history significant for asthma. No patients had a history of neoplasia or organ transplantation. Patient demographics are listed in Table 1. As can be seen, patients did not differ significantly among treatment groups. Antibiotic usage did not differ among groups, and there was no effect of antibiotic usage on total days spent in the hospital or total hospital charges. As shown in Figure 1, the three most commonly used antibiotics were third- and second-generation cephalosporins and vancomycin. Thirdgeneration cephalosporins (cefotaxime, ceftriaxone) were chosen most often. All antibiotics were given intravenously. Vital signs at presentation are shown in Table 2. Patients between one and six years of age who underwent primary chest tube placement followed by VATS had a significantly lower

4 320 AZIZ ET AL. TABLE 1. PATIENT DEMOGRAPHICS BY TREATMENT GROUP Primary Chest tube, Primary All chest tube then VATS VATS patients (n 21) (n 15) (n 13) P value a (n 49) Average age (years) b Duration of symptoms (days) b Presenting symptoms (%) Fever ( 38 C) Cough Shortness of breath Myalgia Vomiting Nausea Dehydration a Calculated using nonparametric ANOVA among primary chest tube, then video-assisted thoracoscopic surgery (VATS), and primary VATS. b Mean standard deviation. temperature before treatment than did the other two groups (p 0.05; ANOVA). The chest radiographic findings are listed in Table 3. Patients who underwent primary chest tube treatment and later required VATS were more likely to exhibit mediastinal shift and air bronchograms than the other groups (p 0.05; ANOVA). Pleural fluid characteristics are shown in Table 4. Patients undergoing primary VATS FIG. 1. Effect of initial antibiotic on outcome of pediatric patients with pneumonia and parapneumonic effusion/empyema according to remaining treatment. (A) Total days spent in hospital. (B) Total hospital cost. CT chest tube; CT/VATS chest tube placement followed by video-assisted thoracoscopic surgical pleural debridement; VATS primary video-assisted thoracoscopic surgical debridement of pleural space.

5 CHEST TUBE VS. VATS IN PEDIATRIC EMPYEMA 321 TABLE 2. VITAL SIGNS AT PRESENTATION BY TREATMENT GROUP a Chest tube, Primary chest tube then VATS Primary VATS All patients Birth to 1 year n 4 n 1 n 1 n 6 Breaths/min Heart rate (beats/min) Temperature ( C) to 6 years n 8 n 9 n 10 n 27 Breaths/min b Heart rate b Temperature b years n 9 n 5 n 2 n 16 Breaths/min b Heart rate b Temperature b a Mean standard deviation. b P 0.05 for chest tube then video-assisted thoracoscopic surgery, vs. other groups. had significantly higher protein concentrations than patients in the other groups. Patient outcome The outcome of patients as a function of treatment strategy is illustrated in Figure 2. Patients undergoing primary chest tube treatment followed by VATS had a significantly longer hospital stay than other the groups. Moreover, patients undergoing primary VATS accumulated significantly lower total hospital charges. There was no statistically significant difference among groups in the length of stay in the ICU. DISCUSSION In the present study, we reviewed the management of empyema and parapneumonic effusion in patients with community-acquired pneumonia. Although retrospective, this study provides clear evidence in favor of VATS-assisted pleural debridement rather than chest tube placement as primary therapy. These findings were not affected by patient demographics, initial vital signs, or initial antibiotic usage, all of which were essentially the same among groups. Potential reasons for the better outcome of primary VATS may lie in the shortcomings of chest tube drainage. Tubes that are placed by interventional radiologic techniques tend to be of small caliber and therefore prone to clogging, resulting in loss of effectiveness after several days. Tubes that are placed through an open, non-interventional approach may not be located optimally within the loculated cavity. As such, approximately 40% of patients treated by primary chest tube placement required a subsequent VATS procedure. By contrast, VATS-directed therapy allows precise placement of the chest tube in addition to thorough removal of pleural fluid and peel on the surface of the lung. Perhaps more importantly, it expedites full lung expansion, thus shortening hospitalization [13,16]. Taken together, these factors may explain why a superior outcome was observed with primary VATS. TABLE 3. CHEST RADIOGRAPH FINDINGS BY TREATMENT GROUP BY PERCENTAGE a Radiographic Primary chest tube Chest tube, then Primary VATS All patients finding (n 21) VATS (n 15) (n 13) (n 49) Consolidation Mediastinal shift a Collapse Air bronchogram a a P 0.05 for chest tube, then video-assisted thoracoscopic surgery, vs. other groups.

6 322 AZIZ ET AL. TABLE 4. PLEURAL FLUID FINDINGS BY TREATMENT GROUP a Primary chest tube Chest tube, then VATS Primary VATS All patients (n 21) (n 15) (n 13) (n 49) Glucose (mg/dl) White blood cells/mm 3 ph LDH (U/L) Protein (mg/dl) b a Mean standard deviation. b P 0.01 for primary video-assisted thoracoscopic surgery vs. primary chest tube. A considerable portion of the patients who underwent primary chest tube treatment later required VATS-assisted pleural debridement, leading to a longer ICU stay and significantly prolonged hospitalization. We note that although there was no observed adverse effect of VATS therapy in the current study, the performance of this procedure does require general anesthesia. At our institution, we tend to place pediatric chest tubes using either general anesthesia or deep sedation, so that a trip to the operating room generally is required by all patients with complicated pneumonia with parapneumonic effusion or empyema. This may explain in part the finding that total hospital charges actually were lower in patients treated by primary VATS (see Fig. 2). We also determined that the choice of antibiotics after the procedure did not influence the intervention performed (see Fig. 1). This may reflect the fact that most patients had been on antibiotic therapy for an extended time before admission to our hospital, as manifested by the fact that pleural fluid was likely to be sterile at the time of drainage (data not shown). We note that the development of treatment guidelines for pa- FIG. 2. Effect of treatment on outcome in pediatric patients with pneumonia and parapneumonic effusion/empyema. (A) Days spent in ICU. (B) Total days hospitalized. (C) Total hospital cost. CT chest tube; CT/VATS chest tube placement followed by video assisted thoracoscopic assisted surgical pleural debridement; VATS primary videoassisted thoracoscopic assisted surgical pleural debridement.

7 CHEST TUBE VS. VATS IN PEDIATRIC EMPYEMA 323 tients with complicated empyema which may include administration of fibrinolytic agents into the chest tube may identify at presentation those patients who could benefit from primary chest tube placement, although the current data favor consideration of primary VATS in the pediatric population [5,6,21 23]. Finally, we note that during the course of the study, treatment approaches did not change meaningfully, so caregiver preference remained the primary determinant of the initial choice of treatment. These findings provide a rationale for the performance of a prospective trial to evaluate the optimal treatment approach. In summary, we have determined that initial management of children with complicated empyema by VATS-assisted drainage of the pleural space provides better outcomes than other modalities. More prospective data will permit formulation of patient-specific criteria to determine the optimal management strategy. REFERENCES 1. Baltimore RS. Pleural effusion, empyema, and lung abscess. In: Jenson HB, ed. Pediatric Infectious Diseases: Principles and Practice. 2 edition. Philadelphia. WB Saunders, 2002: Tan TQ, Mason EO Jr, Wald ER, et al. Clinical characteristics of children with complicated pneumonia caused by Streptococcus pneumoniae. Pediatrics 2002; 110: Byington CL, Spencer LY, Johnson TA, et al. An epidemiological investigation of a sustained high rate of pediatric parapneumonic empyema: Risk factors and microbiological associations. Clin Infect Dis 2002;34: Gates RL, Hogan M, Weinstein S, Arca MJ. Drainage, fibrinolytics, or surgery: A comparison of treatment options in pediatric empyema. J Pediatr Surg 2004;39: Ulku R, Onen A, Onat S, et al. Intrapleural fibrinolytic treatment of multiloculated pediatric empyemas. Pediatr Surg Int 2004;20: Ekingen G, Guvenc BH, Sozubir S, et al. Fibrinolytic treatment of complicated pediatric thoracic empyemas with intrapleural streptokinase. Eur J Cardiothorac Surg 2004;26: Maier A, Domej W, Anegg U, et al. Computed tomography or ultrasonically guided pigtail catheter drainage in multiloculated pleural empyema: A recommended procedure? Respirology 2000;5: Chang JH. Progress in pediatric surgery: Historical aspects. Prog Pediatr Surg 1991;27: Ozcelik C, Ulku R, Onat S, et al. Management of postpneumonic empyemas in children. Eur J Cardiothorac Surg 2004;25: Chen SM, Sheu JN, Chen JP, Yang MH. Communityacquired Pseudomonas aeruginosa pneumonia complicated with loculated empyema in an infant with selective IgA deficiency. Acta Paediatr Taiwan 2002;43: Cohen G, Hjortdal V, Ricci M, et al. Primary thoracoscopic treatment of empyema in children. J Thorac Cardiovasc Surg 2003;125: Rodgers BM. The role of thoracoscopy in pediatric surgical practice. Semin Pediatr Surg 2003;12: Liu HP, Hsieh MJ, Lu HI, et al. Thoracoscopic-assisted management of postpneumonic empyema in children refractory to medical response. Surg Endosc 2002;16: Waller DA. Thoracoscopy in management of postpneumonic pleural infections. Curr Opin Pulm Med 2002;8: Kercher KW, Attorri RJ, Hoover JD, Morton D Jr. Thoracoscopic decortication as first-line therapy for pediatric parapneumonic empyema: A case series. Chest 2000;118: Grewal H, Jackson RJ, Wagner CW, Smith SD. Early video-assisted thoracic surgery in the management of empyema. Pediatrics 1999;103:e Patton RM, Abrams RS, Gauderer MW. Is thoracoscopically aided pleural debridement advantageous in children? Am Surg 1999;65: Klena JW, Cameron BH, Langer JC, et al. Timing of video-assisted thoracoscopic debridement for pediatric empyema. J Am Coll Surg 1998;187: Rizalar R, Somuncu S, Bernay F, et al. Postpneumonic empyema in children treated by early decortication. Eur J Pediatr Surg 1997;7: Johna S, Alkoraishi A, Taylor E, et al. Video-assisted thoracic surgery: Applications and outcome. J Soc Laparoendosc Surg 1997;1: Paz F, Cespedes P, Cuevas M, et al. Pleural effusion and complicated empyema in children: Evolution and prognostic factors. Rev Med Chil 2001;129: Finck C, Wagner C, Jackson R, Smith S. Empyema: Development of a critical pathway. Semin Pediatr Surg 2002;11: Coote N, Kay E. Surgical versus non-surgical management of pleural empyema. Cochrane Database Syst Rev 2005:CD Address reprint requests to: Dr. David J. Hackam Division of Pediatric Surgery Children s Hospital of Pittsburgh Desoto Wing 4A Fifth Ave. Pittsburgh, PA david.hackam@chp.edu