Published online August 14, 2006
PEDIATRICS Vol. 118 No. 3 September 2006, pp. e547-e553 (doi:10.1542/peds.2005-2719)
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ARTICLE

Therapy of Parapneumonic Effusions in Children: Video-Assisted Thoracoscopic Surgery Versus Conventional Thoracostomy Drainage

Beth A. Kurt, MDa, Kimberly M. Winterhalter, MDa, Robert H. Connors, MDa,b, Bradford W. Betz, MDc and John W. Winters, MDa

a Pediatrics
b Surgery
c Radiology, DeVos Children's Hospital, Grand Rapids, Michigan


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. Controversy surrounds the optimal treatment of parapneumonic effusions. This trial of pediatric patients with community-acquired pneumonia and associated parapneumonic processes compared primary video-assisted thoracoscopic surgery with conventional thoracostomy drainage.

DESIGN. A prospective, randomized trial was conducted at DeVos Children's Hospital (Grand Rapids, MI) between November 2003 and May 2005. All of the patients under 18 years of age with large parapneumonic effusions were approached for enrollment in the study. After enrollment, each patient was randomly assigned to receive either video-assisted thoracoscopic surgery or thoracostomy tube drainage of the effusion. Subsequent therapies (fibrinolysis, imaging, and further drainage procedures) were similar for each group per protocol.

RESULTS. Eighteen patients were enrolled in the study: 10 in video-assisted thoracoscopic surgery and 8 in conventional thoracostomy. The groups were demographically similar. No mortalities were encountered in either group, and everyone was discharged from the hospital with acceptable outcomes. Yet, there were multiple variables that demonstrated statistical difference. Hospital length of stay, number of chest tube days, narcotic use, number of radiographic procedures, and interventional procedures were all less in the patients who underwent primary video-assisted thoracoscopic surgery. In addition, no patient in the video-assisted thoracoscopic surgery group required fibrinolytic therapy, which was also statistically different from the thoracostomy drainage group.

CONCLUSIONS. The outcomes of this study strongly suggest that primary video-assisted thoracoscopic surgery for evacuation of parapneumonic effusions is superior to conventional thoracostomy drainage.

Key Words: empyema • video-assisted thoracoscopic surgery • thrombolytics • thoracotomy • parapneumonic effusion

Abbreviations: VATS—video-assisted thoracoscopic surgery • CT—computed tomography • CXR—chest radiograph • WBC—white blood cell

Approximately 1.2 million people per year are affected by pneumonia in the United States.1,2 In pediatric patients, parapneumonic effusion complicates pneumonia 36% to 57% of the time,3 with a range of incidence between 0.4 and 6.0 cases per 1000 pediatric admissions.4 Although parapneumonic effusions are a relatively common entity, optimal management remains controversial. Therapeutic options include antibiotics, thoracentesis,5 thoracostomy tube drainage,6,7 fibrinolysis,8,9 video-assisted thoracoscopic surgery (VATS),10,11 and thoracotomy.12,13

In 1962, the American Thoracic Society (described the formation of a parapneumonic effusion along a 3-stage continuum.14 Based on the disease pathophysiology, all parapneumonic processes are exudates resulting from an inflamed pleural membrane from an adjacent pneumonia. In the early exudative phase (stage 1), the parapneumonic effusate has a normal glucose and pH. The intermediate fibrinopurulent phase (stage 2) is heralded by an increase in fibrin, polymorphonuclear neutrophils, and lactic dehydrogenase, with decreases in glucose and pH. Because of the fibrin deposition, loculations of fluid begin to form in the pleural space. Finally, in the late organizing phase (stage 3), fibroblastic growth extending from the visceral and parietal pleurae causes the formation of a restrictive pleural peel that entraps the lung and impairs its function.

Historically, the treatment of parapneumonic effusions has most often included a primary nonoperative regimen (antibiotics and thoracentesis or chest tube drainage). Although antibiotic administration and chest tube thoracostomy may be adequate therapy for early (stage I) parapneumonic effusions, the presence of loculations and fibrinous adhesions often limits the success of this therapy. Many times it is difficult to clinically and radiographically differentiate between stage 1 and stage 2 disease. Thus, this primary nonoperative approach frequently results in prolonged hospitalizations.

Many retrospective case series have suggested that children who experience failure of conventional chest tube therapy exhibit improvement after thoracotomy or VATS,15–20 especially if the procedure is performed early.21,22 Based on these reports, many pediatric surgeons have come to consider primary VATS a better approach for children suffering from parapneumonic processes.10 A recent meta-analysis23 suggested that primary surgical intervention for pediatric parapneumonic effusions was best, which was consistent with the results of the prospective, randomized study done by Waite et al24 in adults. However, to our knowledge there has never been a prospective pediatric study to confirm this hypothesis. The purpose of this study was to prospectively compare multiple variables in pediatric patients undergoing primary VATS versus conventional thoracostomy drainage of parapneumonic effusions.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Following a protocol approved by the Institutional Review Board of DeVos Children's Hospital, informed consent was obtained for 18 patients from November 2003 through May 2005. Any patient between the ages of 0 to 18 years of age with evidence of community-acquired bacterial pneumonia and an associated parapneumonic effusion was considered for enrollment into the study. These patients underwent a contrasted chest computed tomography (CT) scan to document parenchymal disease and degree of pleural involvement. Any patient with an effusion that was ≥1.5 cm (widest pleura-to-pleura collection per CT imaging), who was clinically judged to require evacuation (fever, tachypnea, persistent chest or abdominal pain, or leukocytosis), was eligible for inclusion in the study. Criterion for exclusion were: hospital-acquired pneumonia, previous drainage procedure, uncorrected cardiac disease, known immunocompromise, preexisting bronchopleural fistulas, contraindication to fibrinolytic therapy, or suspected nonbacterial infection. All of the patients received appropriate antibiotics for the most likely pathogens before enrollment.

Using a random number method in groups of 10 generated by a Spectrum Health research nurse, patients were assigned either to a primary conventional thoracostomy arm or to a VATS arm. Those randomly assigned to the conventional thoracostomy arm (see Fig 1) had chest tube placement within 24 hours of effusion detection. If the chest radiograph obtained within 24 hours of the procedure showed significant clearing, then the thoracostomy tube was left in place until it drained <1 mL/kg per day for >24 hours. If there was incomplete resolution of the effusion on the follow-up chest radiograph (≥0.5 cm of pleural fluid or obvious loculations), fibrinolytic therapy with reteplase (1 unit in 50 mL normal saline) was administered through the chest tube as long as there was no evidence of bleeding. A dose of 1 mL/kg of this reteplase mixture was given, with a minimum dose of 25 mL, and a maximum dose of 100 mL ≤4 times a day. Treatment with reteplase was continued as long as the chest tube output remained >1 mL/kg per day for a maximum of 5 days. If chest tube output was <1 mL/kg per day after fibrinolytic therapy, and if a parapneumonic effusion persisted, then the patient underwent CT-guided pigtail catheter placement with fibrinolytic instillation via the pigtail catheter. The chest tubes were removed once there was <1 mL/kg per day of pleural fluid output for >24 hours. If a residual effusion existed despite placement of a pigtail catheter and the patient was not clinically improving, then the patient was evaluated for rescue VATS or open thoracotomy by the pediatric surgeons.


Figure 1
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  		FIGURE 1 Algorithm outlining randomization and intervention for study.

 
Patients randomly assigned to the surgical arm had primary video-assisted thoracoscopic drainage of the chest within 24 hours of diagnosis of a parapneumonic effusion. To accomplish this, patients were placed under general endotracheal anesthesia. A hydrolaparoscope introduced into the pleural space was used to irrigate the pleural cavity and disrupt loculations with blunt dissection technique. Debridement was continued until the pleural surfaces of the lung were sufficiently clear. The lung was then fully reexpanded. At the conclusion of the procedure, a chest tube was placed through one of the existing port sites used for the VATS procedure. The chest tube was left in place until it drained <1 mL/kg per day and there was documented resolution of the parapneumonic effusion. In the case of a persistent effusion, a similar protocol was followed in terms of fibrinolysis and subsequent drainage procedures (see Fig 1).

Primary variables compared between groups were length of hospital stay and duration of chest tube drainage. Secondary variables included fever duration, days of oxygen and narcotic use, number of radiographic procedures, number of drainage procedures, and procedure/sedation time, as well as the need for fibrinolysis. In addition, a cost analysis was done to compare facility, physician, and total charges between groups.

A sample size of 30 was chosen to have an 80% power to detect a predicted difference of 4 days in the mean length of hospitalization. This estimate was based on retrospective data from DeVos Children's Hospital and from case studies reporting length of hospitalization for VATS and conventional thoracostomy drainage of parapneumonic effusions in children. Comparisons between the 2 treatment groups were made with the Mann-Whitney test or, where appropriate, a Fisher's exact test. A P ≤ 0.05 was considered statistically significant. Summaries are expressed as mean ± SD except where the median value (25th–75th percentile) was felt to best represent the data set.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
During this time period, 20 patients were identified with parapneumonic effusions. One declined participation in the study and another was felt to have pleural disease secondary to a nonbacterial process, but the other 18 patients were successfully enrolled in the study. No enrolled patient withdrew from the study (see Fig 1).

The demographic data for the 2 treatment groups at the time of enrollment is summarized in Table 1. Gender, age, length of illness, antibiotic exposure before enrollment, and degree of leukocytosis were found to be similar in both groups. In an attempt to characterize the effusions, the effusate white cell count was compared and found to be not statistically significant. There were 2 patients in the thoracostomy group with positive effusate cultures (Streptococcus pneumoniae and Streptococcus pyogenes) and 3 in the VATS group (S pyogenes, methicillin-resistant Staphylococcus aureus, and Peptostreptococcus). One patient from each group required a critical care admission.


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  		TABLE 1 Demographic Comparison of the Two Treatment Groups

 
In reviewing the chest CT scans, a pediatric radiologist (B.W.B.) blinded to randomization found no significant difference in the distribution of chest disease between the 2 study groups. In particular, the width of effusions and frequency of loculations were similarly distributed (Table 1). Other CT findings, such as attenuation of effusions, extent of surrounding lung disease, lung necrosis, and intrathoracic adenopathy were also similar. CT findings that have been helpful in the identification of adult empyemas (parietal pleural enhancement and thickening >2 mm, thickening and increased attenuation of the extrapleural subcostal fat25) were not universally noted in our pediatric patients but were uniformly distributed between the groups.

The in-hospital outcomes for the 2 treatment groups are compared in Table 2. There were no mortalities in either group during the study period, and no clinically significant complications attributable to drainage procedures or fibrinolysis. No patient in either group had recurrence of effusions once the chest tube was removed. The patients in the VATS arm were found to have significantly shorter hospitalizations, as well as fewer days of chest tube drainage. As a result, patients who underwent VATS drainage required fewer narcotics. The duration of fever and oxygen need did not reach statistical significance, although they tended to be shorter in the patients who underwent VATS.


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  		TABLE 2 Patient Outcomes

 
Other monitored variables included radiographic procedures (chest CT scan and chest radiograph [CXR]) and interventional procedures. In both of these areas, there was a statistically significant reduction in the number of diagnostic and therapeutic procedures for those patients in the VATS arm. Furthermore, none of the patients in the VATS group required fibrinolytic therapy. As would be expected, the procedural time for VATS was longer, because more debridement and irrigation was performed, although the overall sedation time was not statistically different. Although there was a statistically significant difference in facility/hospital charges between the groups, when physician charges were added, this difference did not reach statistical significance.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The inflammatory environment of a parapneumonic effusion promotes the evolution of a free-flowing exudate to fibrinous loculations and, ultimately, collagen formation. Because fibrin formation impairs drainage of pleural fluid, treatment of a parapneumonic effusion early in its course (stage 1) is important for ease of drainage. Having said this, the management of parapneumonic effusions can be challenging and frustrating. Often it is difficult to assess whether the effusion is free flowing (stage I) for which simple thoracostomy drainage could be adequate, or if it has already progressed to an effusion with multiple loculations (stage 2).

Historically, at DeVos Children's Hospital, we tried to classify parapneumonic effusions using CT scan or ultrasound or by looking at the character of the fluid (lactic dehydrogenase, pH, white blood cells [WBCs], and Gram-stain). Unfortunately, many of our patients had effusions that seemed to be stage 1 (effusate pH > 7.3 and no documented loculations on imaging) but still required prolonged hospitalizations (mean: 12.1 days; range: 3–30 days) because of incomplete drainage accompanied by prolonged fevers and toxicity. As a result, we pursued approval for a prospective, randomized trial of thoracostomy drainage versus VATS drainage for parapneumonic effusions associated with community-acquired bacterial pneumonias. During the present study, every patient in the VATS arm had radiographic evidence of loculations (visible pleural adhesions or focal distortion of the visceral pleura) with visual confirmation in the operating room. The majority of patients in the thoracostomy arm also had radiographic evidence of loculations, which may account for their prolonged courses.

Despite the reported efficacy of different modalities for the treatment of pediatric parapneumonic effusions, a rational approach has been unclear because of the lack of prospective randomized trials. Our protocol, as outlined in Fig 1, specifically compared 2 commonly used therapies (chest tube thoracostomy and VATS), attempting to standardize management once the drainage device was in place.

In the conventional thoracostomy arm, the length of hospitalization was consistent with historical controls from DeVos Children's Hospital. On the other hand, patients in the VATS arm revealed statistically significant decreases in various parameters, including length of stay, duration of chest tube drainage, narcotic use, radiation exposure, and need for further interventions (fibrinolysis or chest tubes). Although not reaching statistical significance, duration of fever, oxygen need, and total charges were lower in the VATS patients.

By creating a protocol for the postdrainage care, we attempted to remove the bias of how long to leave the chest tubes in place. We set 1 mL of pleural fluid per kilogram per day as the cutoff based on the concern that daily drainage above this amount could result in significant reaccumulation requiring subsequent drainage procedures. Regardless, the VATS patients reached this level much sooner than the thoracostomy patients and required no subsequent interventions.

A question might arise over the fibrinolysis protocol. A recent publication by Maskell et al26 questions the efficacy of fibrinolytic therapy in parapneumonic effusions, but the meta-analysis by Avansino et al23 suggests a significant benefit of fibrinolysis in pediatric parapneumonic effusions. Some centers use a much more aggressive regimen. Although a more aggressive fibrinolytic regimen may have shortened some of the treatment courses, it may also have increased the complication rate. It was interesting to note that none of the VATS patients required fibrinolytic therapy; the procedure was so efficacious that fibrinolysis to assist drainage was never deemed necessary.

Some clinicians may question whether a different imaging modality (ultrasound or MRI) may have been better than CT to confirm the presence of a parapneumonic effusion and to determine whether or not loculations were present in the pleural space. This topic has been debated in the literature with no definite conclusion.27–31 Ultrasound has been advocated to confirm the presence of an effusion because of its lower cost, greater availability, portability, discretionary use of sedation, and lack of ionizing radiation, and loculated effusions by ultrasound have correlated with exudative pleural chemistries.32,33 Some studies have based treatment of parapneumonic effusions on whether adhesions were present by ultrasound.34–36 However, sonography may not visualize all adhesions,20 which might influence clinical outcome.37

We consider CT to be the most informative imaging modality to evaluate children with parapneumonic effusions. CT provides a global depiction of chest disease that is useful in the assessment of morbidity and for planning therapy, especially VATS. CT can demonstrate the size and location of effusions, is sensitive in the detection of pleural adhesions,25 and can show the extent of lung involvement, including complications such as necrosis and abscess. There has been an increased awareness of the need to carefully consider how CT is used in children because of the potential cancer risks from ionizing radiation and the increased susceptibility of children to these effects.38 Optimizing CT techniques, as well as refining the indications for CT examinations, are important objectives to limit unnecessary radiation exposure. Our results show that the use of ionizing radiation can be minimized for patients with parapneumonic effusions if they are imaged early and aggressively managed. In our study, patients in the VATS arm required fewer CT scans and CXR than those in the thoracostomy arm.

Finally, some might argue that the number of patients enrolled in this study may not be a large enough sample to fully support the claim that primary VATS is the optimal intervention for pediatric parapneumonic effusions. Based on an estimated difference in length of stay and chest tube duration of 4 days, a study size of 30 patients was initially felt to be necessary. When we did an interval assessment, we found this difference to be closer to 7 days. As a result, the findings were found to be statistically and clinically significant after 18 patients. Therefore, we felt it relatively unethical to present either option as if they were equally efficacious. In addition, the data correlated well with the findings of the recent meta-analysis by Avansino et al23; thus, we determined that our data were reliable and reproducible.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
The outcomes of this study strongly suggest that primary VATS for evacuation of stage I or II parapneumonic effusions is superior to conventional thoracostomy drainage. This finding is consistent with case reports and meta-analyses that have been done previously. It argues that the best course of action may be to do VATS for all parapneumonic effusions that require a drainage procedure. A larger, multicenter study may be indicated to verify these findings within the pediatric population.


   ACKNOWLEDGMENTS
 
We thank Diann Reischman, PhD (Department of Statistics, Grand Valley State University), for assistance with the statistical analysis. We thank James Decou, MD, Neil Uitvlugt, MD, and Marc Schlatter, MD (Departments of Pediatrics and Surgery, DeVos Children’s Hospital) for their contributions to this study.


   FOOTNOTES
 
Accepted Mar 31, 2006.

Address correspondence to John W. Winters, MD, Department of Pediatrics, DeVos Children's Hospital, 100 Michigan St NE, MC 117, Grand Rapids, MI 49503. E-mail: drsjww{at}sbcglobal.net

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics



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