Pediatric Respirology and Critical Care Medicine

: 2020  |  Volume : 4  |  Issue : 3  |  Page : 41--45

A follow-up study for pulmonary function evaluation in children with complicated parapneumonic pleural effusion

Yu-Jen Wei1, Ying-Tzu Ju1, Ming-Lin Hsieh1, Ming-Ho Wu2, Jing-Ming Wu1, Jieh-Neng Wang1,  
1 Department of Pediatrics, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan, Taiwan
2 Department of Surgery, Tainan Municipal Hospital, Tainan, Taiwan

Correspondence Address:
Jieh-Neng Wang
Department of Pediatrics, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, 138 Sheng Li Road, Tainan 70428


Objectives: Although children with complicated parapneumonic effusions (CPEs) clinically improve within weeks after being discharged from the hospital, it remains unclear whether the injury and subsequent repair of the damaged lung allow a full return to premorbid lung function. We investigated the pulmonary function status in children whose CPE had been treated with different modalities. Patients and Methods: We therefore enrolled forty patients with a history of CPE: (1) patients treated with systemic antibiotics and conventional chest tube therapy only (control Group 1, n = 11); (2) patients treated with systemic antibiotics, conventional chest tube therapy, and intrapleural fibrinolytic therapy (Group 2, n = 20); and (3) patients treated with surgical intervention in addition to prior medical treatment (Group 3, the surgical rescue group, n = 9). Pulmonary function tests were done when patients had been discharged at least for 1 year. We used a spirometry test for pediatric pulmonary functions. Results: The basic demographic data of the three groups were not significantly different. The forced volume vital capacity (FVC) and forced expiratory volume in 1 s (FEV1) were significantly higher in Group 2 patients (percentage of the predicted value in FVC: 87.6% ± 8.5% versus 79.2% ± 13.4% (Group 1) vs. 77.6% ± 9.0% (Group 3)). Significantly, fewer Group 2 patients had abnormal pulmonary function (P < 0.05). Conclusions: Our data support a growing body of evidence that empyema in children may lead to reduced lung function later in life for a subset of patients.

How to cite this article:
Wei YJ, Ju YT, Hsieh ML, Wu MH, Wu JM, Wang JN. A follow-up study for pulmonary function evaluation in children with complicated parapneumonic pleural effusion.Pediatr Respirol Crit Care Med 2020;4:41-45

How to cite this URL:
Wei YJ, Ju YT, Hsieh ML, Wu MH, Wu JM, Wang JN. A follow-up study for pulmonary function evaluation in children with complicated parapneumonic pleural effusion. Pediatr Respirol Crit Care Med [serial online] 2020 [cited 2022 Jan 24 ];4:41-45
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Pleural effusions are common complications of pediatric bacterial pneumonias. They occur in 21%–91% of cases.[1],[2] Failure to control the pleural process may lead to progressive disease and complicated parapneumonic effusions (CPEs) or empyema.[3],[4],[5] Children with CPE typically have compromised gas exchange, which must be managed with several days of hospitalization using systemic antibiotic treatment, chest tube drainage, intrapleural fibrinolytic therapy, or surgical intervention.[6] While most children clinically improve within a few weeks after they have been discharged from the hospital, it remains unclear whether the injury and subsequent repair of the damaged lung allow a full return to premorbid lung function.

There is increasing evidence that lower respiratory tract infections in childhood are associated with subsequent reduced lung function.[7],[8],[9],[10] However, studies[11],[12],[13],[14] on pulmonary function tests (PFTs) in children who have had empyema or pleural effusions report inconsistent findings, and not all studies on PFTs in children have found abnormalities after empyema.[15],[16] Moreover, the dearth of follow-up pulmonary function studies preclude comparing the efficacy of different CPE treatment modalities. Our previous studies[17],[18] showed that intrapleural fibrinolytic treatment is a safe and effective adjunct therapy, and that it should be attempted early on, when children are first diagnosed with CPE.

We hypothesized that breaking down the formation of fibrous pleural loculations as early as possible prevented additional lung damage. We therefore wanted to follow-up our previous patients by investigating the pulmonary function status in these children who recovered from CPE managed using different treatment modalities.

 Patients and Methods

Patient selection

Potential study participants admitted to National Cheng Kung University Hospital for CPE between January 1, 1992, and January 31, 2005, were identified from our existing patient database.[17],[18] Inclusion criteria based on the current definitions of CPE that required chest tube drainage included at least one of the following characteristics of pleural effusion: PH <7.2, glucose <40 mg/dL, total protein >5 g/dL, lactate dehydrogenase >1,000 IU/L, a grossly purulent appearance, or a positive Gram stain.[17],[18],[19] The exclusion criteria were one or more of the following: age <5 years at the time of the pulmonary function evaluation, discharged from the hospital because of CPE when <1 year old, or a medically significant history of diseases that affect lung function (excluding mild intermittent asthma). Patients who met the inclusion criteria were sent a letter asking whether they would be willing to participate in the study.

We divided the patients into three groups based on previous studies: those who had been given (1) systemic antibiotics plus conventional chest tube therapy only (conventional group); (2) systemic antibiotics, conventional chest tube therapy, and early intrapleural fibrinolytic therapy (either streptokinase or urokinase) (fibrinolytic Group); and (3) open chest surgical intervention (decortication, empyemectomy, or both) in addition to prior medical therapy (Surgical Rescue Group). The surgical intervention was done after 7 days of persistent fever (body temperature >38.0°C) despite appropriate therapy or because of a lung abscess proved by computer tomography of the chest. Indications for surgery remained the same during the entire study period.[17],[18] To verify the referenced normal data in Zapletal et al.,[20] we enrolled thirty healthy age-matched children as a local control group.

Patients participating in the study filled in a questionnaire on their respiratory symptoms and medications since hospital discharge and were given a physical examination and a PFT. Their previous admission charts were reviewed to collect the basic information. The study protocol was approved by our institutional review board, and written informed consent was obtained from the patients' parents.

Pulmonary function testing

Spirometry, using standard procedures recommended by the American Thoracic Society (ATS),[21] was used to test pulmonary function in all participants (Model 2000 Easy-One Spirometer; NDD Medical Technologies, Andover, MA).[22] Each child was briefly instructed on the particulars of the test by the same technician, who was blinded to each patient's clinical history. Each testee's nose was sealed manually or with appropriately sized spirometry nose clips. All PFTs were completed between July 1 and September 30, 2006. All measured indices for spirometry are expressed as a percentage of the predicted normal values based on the results reported in Zapletal et al.[20]

Interpretation of pulmonary function test

Spirometry results that did not meet the ATS criteria for acceptability and reproducibility were excluded from the analysis.[23] Each participant's lung function test result was classified as normal, obstructive, or restrictive. We defined obstructive function as a predicted forced expiratory volume in 1 s (FEV1)/forced volume vital capacity (FVC) ≤80% with either a predicted FEV1 of ≤80% or a predicted mean forced expiratory flow during the middle half of the FVC (FEF25–75) of ≥65%. The definition for restrictive function was an FVC ≤80%, with a normal or elevated FEV1/FVC.[12]

Statistical analysis

We used a one-way ANOVA with post hoc test to compare, between each pair of groups, continuous variables: age at illness, age at PFT, body weight, body height, length of hospital stay for CPE, fever duration after initial treatment, and pulmonary function parameters. To compare category variables such as gender, CPE etiologies, and the number of patients with abnormal pulmonary function, we used a Chi-square test. For numbers <5, we used Fisher's exact test. Statistical significance was set at P < 0.05. Data are means ± standard deviation.


From January 1, 1992, to January 31, 2005, we identified 72 patients who met our stipulated definition of CPE and who had received a complete course of treatment in our hospital. Forty-nine (68%) responded to our invitation and agreed to participate in this study. Five of the 49 had PFTs that did not conform to ATS guidelines, three had active symptoms of current respiratory disease, and one had a history of persistent asthma controlled with medication; all nine were thus excluded from the analysis. We finally enrolled and analyzed forty participants (16 boys and 24 girls; age range: 61–178 months; mean age: 90.1 ± 22.7 months).

The mean age at the time of illness was 43.5 ± 21.7 months (range: 8–130 months). There were 11 participants in the conventional Group, 20 in the fibrinolytic Group (11 had been given streptokinase, and 9 had been given urokinase), and 9 in the surgical rescue group (seven had been given conventional treatment before surgery and two had been given fibrinolytic therapy before surgery). In the surgical rescue group, eight participants had been given a lobectomy for lung abscess, and one had been given decortication only. Twenty (50%) participants had manifested culture-proven bacterial pathogens (Streptococcus pneumoniae [n = 17], Pseudomonas aeruginosa [n = 2], and Staphylococcus aureus [n = 1]). The physical examinations for all participants were normal, and all were clinically asymptomatic [Table 1]. Although participants in the surgical rescue group were significantly younger at the time of their illness, and the time from hospital discharge to the test was significantly shorter in the fibrinolytic Group, the age at PFT, gender, body weight, and body height did not significantly differ.{Table 1}

Thirty healthy children (15 boys and 15 girls; age range: 60–146 months; mean age: 84.4 ± 25.1 months) were enrolled as the local control group. There were no significant differences between the local control group and the fibrinolytic group. Both FVC and FEV1 were significantly higher in the fibrinolytic group than in the surgical rescue group and conventional group (percentage of the predicted value in FVC: 87.6 ± 8.5 vs. 77.6 ± 9.0 vs. 79.2 ± 13.4; percentage of the predicted value in FEV1: 89.7 ± 10.9 vs. 75.1 ± 17.4 vs. 80.5 ± 16.2) [Table 2]. Although FVC, FEV1, FEF25–75, FEF25, and FEF50 were higher in the conventional group than in the surgical rescue group, the differences were not significant. The fibrinolytic group had significantly fewer participants with abnormal pulmonary function than did the other two groups [Table 3]; P < 0.05]. The proportion of parenchyma damage is higher in surgical group.{Table 2}{Table 3}


Although empyema is not unusual in either adults or children, there are some differences. Empyema is rarely associated with any mortality in children in developed countries, and the long-term survival is excellent with surgical or medical treatment.[24],[25],[26] Therefore, attention should be paid to the recovery of pulmonary function. In this study, we found that up to 25% of children with CPE were classified as having abnormal pulmonary function, although they remained asymptomatic even after they had been discharged from hospital for at least 1 year. Our data support a growing body of evidence that, for a subset of patients, pediatric empyema leads to reduced lung function later in life.

Among studies[11],[12],[14],[15],[16],[27] that have addressed the long-term outcomes of children who recovered from empyema, the most consistent findings are a complete clinical recovery with no residual symptoms, and a complete return to normal of chest X-rays. One study[26] found that even at 6 months posttreatment for empyema, nearly 90% of patients had abnormal chest X-rays; a more recent study[28] that reviewed ventilation-perfusion scans reported that the scan data were nearly normal.[28] Gocmen et al.[15] reported that patients given only conservative treatment had normal pulmonary function 3 months posttreatment, and Hoff et al.[16] reported normal pulmonary function in children with empyema treated with decortication. Other studies[12],[14] reported evidence of restrictive patterns of lung function in children with a history of empyema. In the current study, although lung function was normal in most patients 2 years after discharge, ten of the forty patients still had evidence of abnormal pulmonary function (restrictive or obstructive pattern). Three possible reasons for the different findings in these studies are dissimilarities in PFT equipment, different reference standards, and a lack of consensus pediatric guidelines for defining obstructive and restrictive PFT patterns. Differences in the patient populations studied, including the severity of the pleural inflammation at the time of illness and the infectious agents causing the effusions, may also have contributed to the long-term effects on pulmonary function in these study populations. In the present study, the initial clinical parameters in the surgical rescue group were more severe than in the other two groups, which may also be a morbidity cofactor for abnormal pulmonary function. In addition, there might have been a degree of selection bias in the study because the participants were not randomly selected patients but volunteers.

In this study, participants in the surgical rescue group had the lowest FVC and FEV1. A possible explanation of why this was so may be that those patients had been given surgery only after medical therapy had failed. According to our previous management policy,[17],[18] surgical intervention (decortication or lobectomy) was given only after a patient had 7 days of persistent fever (body temperature >38.0°C) despite appropriate therapy or because of a lung abscess identified by a computed tomography scan of the chest. At this stage, empyema may progress through a loculated, fibrinopurulent stage to the final organizing stage.[4],[5] Therefore, early intervention to lyse fibrin deposits in the pleural space may improve long-term outcomes. This may also explain why participants in this study's fibrinolytic group had a better FVC than those in the conventional group. Our previous studies[17],[18] showed that fibrinolytic therapy increased the volume of chest tube drainage concurrent with clinical improvement. Intrapleural administration of fibrinolytic agents has been proved to effectively lyse fibrous pleural material and to break down septa.[17],[18],[19],[26],[29] However, we could not exclude that open thoracotomy itself may disrupt chest-wall mechanics and affect lung function irrespective of the underlying indication for surgery. Recently, video-assisted thoracoscopic surgery (VATS) has been proposed[30] as a less invasive surgical technique suitable for primary procedures. The exact point at which thoracoscopy becomes useful in the management of pleural sepsis remains unclear and is even less well defined than the role of fibrinolytics.[26]

In the present study, ten of the forty patients had evidence of abnormal pulmonary function (restrictive or obstructive pattern) as late as 2 years after they had been discharged from hospital. This restrictive pattern may reflect residual parenchymal or pleural disease in which loculations that bridge the parietal and visceral pleura have not completely resolved and thus prohibit full lung expansion. Another study[12] suggested that bacterial infection may injure and scar airways, which will lead to persistent obstruction in growing children. However, the limitation of lung function was mild in this subset of patients and appeared to be clinically insignificant with no abnormalities detected on physical examinations; none of the patients was taking daily respiratory medicine. To screen for high-risk patients, a follow-up PFT is, therefore, important. Spirometry is the most commonly used PFT for patients with CPE. A portable spirometer is more convenient than a standard spirometer for clinical recordings pulmonary function.[22]

The major limitation of this study is that our study population was small. Studies with much larger populations are necessary to verify our conclusions. All of our study participants underwent a single lung function assessment several years after they had been discharged from the hospital. It would have been beneficial to have begun longitudinally monitoring their lung function from soon after discharge. This would have helped us determine whether lung function initially recovers before subsequently deteriorating or whether it fails to recover at all.


This study showed that although all the study participants who had recovered from empyema were asymptomatic, there was still a relatively high incidence of study participants with abnormal pulmonary function, especially those who had needed and been given more invasive surgical intervention. Perhaps the latter had presented with a more severe clinical condition. Our data also indicate that early intervention to lyse fibrous pleural effusion leads to, or is at least correlated with, better pulmonary function outcomes. Because we had no follow-up pulmonary function data from patients who underwent mini-invasive procedures, such as VATS, to confirm our findings, it is necessary to evaluate the follow-up pulmonary function data of more patients who were given different types of treatments.


This work was supported by intramural grant NCKUH-10903044 from National Cheng Kung University Hospital, Tainan, Taiwan. The institute supports the pulmonary function test lab, statistical analysis, and publication charge.

Financial support and sponsorship

This study was supported by intramural grant NCKUH-10903044 from the National Cheng Kung University Hospital.

Conflicts of interest

There are no conflicts of interest.


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