|Year : 2021 | Volume
| Issue : 3 | Page : 341-345
Empyema thoracis in children: Can pleural fluid culture positivity affect the outcome?
Indra Kumar Sharma, Durgesh Kumar, Anshuman Tripathi
Department of Pediatrics, Uttar Pradesh University of Medical Sciences, Etawah, Uttar Pradesh, India
|Date of Submission||21-Jul-2021|
|Date of Decision||22-Jul-2021|
|Date of Acceptance||02-Aug-2021|
|Date of Web Publication||13-Sep-2021|
Dr. Durgesh Kumar
302, Type-5, New Campus, Uttar Pradesh University of Medical Sciences, Saifai, Etawah, Uttar Pradesh
Source of Support: None, Conflict of Interest: None
Background: Empyema thoracis in children continues to be a major problem with significant morbidity in developing countries despite recent advances in management. This study was aimed to evaluate the clinico-etiology and compare the outcomes of sterile and culture-positive pleural fluid empyema thoracis in North Indian children. Patients and Methods: A total of sixty admitted children satisfying the inclusion criteria were enrolled in the study from October 2018 to September 2020 with parental consent. Bacteriological etiology was confirmed by pleural fluid culture. Disease outcome was evaluated by duration of chest tube insertion, hospital stay, mortality, and successfully discharged patients. The outcomes were compared between patients with sterile and positive pleural fluid culture. Results: The average age of the patients was 4.72 ± 3.52 years with male preponderance (male/female ratio: 1.3:1). Forty-five percent of the patients were between 1 and 5 years. The most common predisposing factor was pneumonia. Fever and cough were the most common manifestations. Pleural fluid culture was positive in 28.3%, with Staphylococcus aureus being the most common organism isolated. Intercostal drainage (ICD) tube was used in 93.3% of the patients and was successful in 80%. The average period of ICD tube placement was 9 ± 4.18 days while hospital stay was 21 ± 9.12 days. Mortality was 1.7%. No statistical significant difference was found in outcomes between patients with sterile and culture-positive pleural fluid. Conclusions: S. aureus was the most common cause of empyema thoracis in this study. The high proportion of culture-negative specimens indicates that pleural fluid culture is not a satisfactory diagnostic tool to find the causative organism.
Keywords: Intercostal drainage tube, pneumonia, Staphylococcus aureus, Streptococcus pneumoniae
|How to cite this article:|
Sharma IK, Kumar D, Tripathi A. Empyema thoracis in children: Can pleural fluid culture positivity affect the outcome?. Indian J Respir Care 2021;10:341-5
|How to cite this URL:|
Sharma IK, Kumar D, Tripathi A. Empyema thoracis in children: Can pleural fluid culture positivity affect the outcome?. Indian J Respir Care [serial online] 2021 [cited 2022 Aug 11];10:341-5. Available from: http://www.ijrc.in/text.asp?2021/10/3/341/325896
| Introduction|| |
Empyema of thorax is one of the common diseases of pleural cavity and more prevalent in developing countries. Parapneumonic effusion and empyema are the known complications of bacterial pneumonia. Almost 25% of the children with pneumonia develop empyema as a complication. Empyema can also develop in primary tuberculous pleural effusion. This may be due to progression of a direct infection in the pleural cavity or from thoracic lymph nodes or by hematogenous spread. Thoracic empyema is one of the important causes of hospitalization of children in developing countries including India.
Although thoracic empyema is not a major cause of mortality in pediatric population, it does cause significant morbidity and often presents a therapeutic challenge. The long-term outcome in children with pyothorax is usually very good. In the last two decades, the incidence of empyema is increasing. The bacteriology of pleural infection is also changing due to widespread use of conjugate pneumococcal vaccine., The increasing incidence, associated morbidity, consumption of scarce hospital resources, and controversial optimal management of the disease make pyothorax a significant health issue in developing countries.
Staphylococcus aureus is reported as the most common causative organism of thoracic empyema in developing countries, while it is Streptococcus pneumoniae in the developed world.,, Factors responsible for high incidence of empyema in the developing world are indiscriminate use of antibiotics in treatment of pneumonia, delay in diagnosis of pneumonia, low socioeconomic status, and malnutrition. In this antimicrobial era, the incidence of this disease is still not decreasing in developing countries. Keeping all these facts in mind, we conducted this study in our epidemiological setup to evaluate the clinico-etiology and to compare the outcome in children in relation to pleural fluid culture which may help to optimize the existing management guidelines of empyema for developing countries.
| Patients and Methods|| |
This prospective cross-sectional study was undertaken in a tertiary hospital of North India between October 2018 and September 2020. Approval was obtained from the institutional ethics committee. Children admitted between 0 and 14 years of age with thoracic empyema were enrolled in the study. Informed and written consent was taken from patients' parents/guardians. The inclusion criterion was the aspiration of pus (white blood cell [WBC] count >5000/mm3) from the pleural cavity of the patient or bacteria isolated in pleural fluid. Children with the diagnosis of tuberculous pleural effusion, prior chest tube drainage before admission, significant chest deformity, and posttraumatic empyema were excluded from the study. A standardized case report form was developed to collect data on demographics, nutritional status, immunization, clinical, diagnostic, treatment, and outcome measure of all cases. In all cases, basic investigations, chest X-ray, pleural fluid analysis with culture, and sensitivity were sent along with blood culture and sensitivity. Ultrasonography (USG) of chest was also done. Computerized tomography (CT) scan of chest was done only in cases with radiological suspicion of multiloculation or nonimprovement following therapy. A sample of 10 ml pleural fluid was collected in a sterile culture bottle during thoracocentesis with aseptic technique or at the time of intercostal drainage (ICD) tube insertion and sent for cell type and count, glucose, lactate dehydrogenase level, Gram's stain, acid-fast Bacillus stain, culture, and sensitivity.
All cases were initially managed with chest tube drainage in combination with empirical intravenous (IV) antibiotics according to hospital protocol to cover the likely causative organisms and supportive treatment. Antipyretics and analgesics were also administered as indicated. Good nursing care along with appropriate dietary intake with nutritional supplements if necessary was given to each patient. Response to treatment was defined as reduction of respiratory distress, better air entry, and improvement of chest X-ray and USG finding. In case of persistence of fever, poor oral intake, continued drainage, and raised counts despite initial antibiotic therapy, antibiotics were upgraded including treatment for methicillin-resistant S. aureus, Pseudomonas, and anaerobic bacteria. Once culture results from the pleural fluid were obtained, antibiotics were replaced according to the sensitivities of the grown culture. Antibiotics were not discontinued following a negative culture, but prolonged empirical antibiotics were administered to these patients. Once fever and sepsis settled, the route of antibiotic administration was changed to oral. The antibiotic therapy was generally continued for at least 3 weeks, but prolonged course of antibiotics was necessary for the patients who did not improve. Inflammatory markers (WBC count and C-reactive protein) were used as guides to extend the duration of antibiotic treatment. The intercostal drain was clamped and removed on clinical and radiological improvement (expansion of lung on chest radiograph) and no or minimal output (<25 ml/day) for 3 consecutive days. A chest CT was obtained in those patients who did not respond to this treatment, developed complication or who did not show lung expansion on chest X-ray. They were then referred to a cardiothoracic surgeon for video-assisted thoracoscopic surgery (VATS) or thoracotomy with decortication [Figure 1].
Patients were discharged when chest tube was removed, no fever was recorded for at least 7 days, tachypnea was absent, and the child was taking orally well. Each patient was followed up on an outpatient department (OPD) basis for at least three visits to study the outcome (visits on 1, 3, and 6 weeks). Clinical examination of each patient was done in OPD and a chest radiograph was advised if found necessary.
All the results collected were analyzed using SPSS software version 25 (IBM Corp. Released 2017. IBM SPSS Statistics for Windows, version 25.0. Armonk, NY, USA: IBM Corp). Results of categorical measurements were presented in number with percentage and results of continuous measurements as mean ± standard deviation. To study the correlation of patient outcome with pleural fluid culture, P value was calculated and it was considered statistically significant when a value was <0.05.
| Results|| |
We enrolled consecutive sixty patients for the study, fulfilling the inclusion criteria. The mean age of the patients was 4.72 ± 3.42 years which ranged from 2 months to 13 years, but 45% (27/60) of the affected patients were between 1 and 5 years. The overall male-to-female ratio was 1.3:1. Two-thirds of the patients were malnourished according to the Indian Academy of Pediatrics (IAP) classification of malnutrition and almost half were completely vaccinated up to the age. Bronchopneumonia was found to be the most common risk factor associated and fever and cough were the most common clinical features at the time of admission [Table 1].
|Table 1: Demographic and clinical characteristics of the study patients (n=60)|
Click here to view
Bacteriological etiology was confirmed by pleural fluid culture in 17 cases (28.3%), as shown in [Figure 2]. The most common organism isolated (10 cases) was S. aureus which was followed by S. pneumoniae (3 cases, 64.6%).
Out of 60 patients, 58 improved with treatment and were discharged. Only one patient did not improve and succumbed to his illness on the 4th day of chest tube insertion. One patient left the hospital against the medical advice. The average duration of ICD tube was 9 ± 4.18 days and hospital stay was 21 ± 9.22 days. When patients' outcomes were compared (in terms of period of ICD tube, final outcome, and hospital stay of the patients) between patients with sterile and positive pleural fluid culture, no statistically significant difference was found in the outcomes of the patients [Table 2].
Four patients (6.7%) were managed conservatively with IV antibiotics and supportive treatment along with thoracocentesis. ICD tube was used with IV antibiotics in the rest 56/60 (93.3%) patients for the management, but 8 patients (13.3%) did not improve with this and underwent surgical intervention. Six patients were managed with thoracoscopic debridement (VATS) and the remaining two needed open decortication thoracotomy [Table 3].
| Discussion|| |
This prospective observational study at a tertiary care center shows that mostly children under 5 years were affected with thoracic empyema and pneumonia was the most common predisposing risk factor. Fever, cough, and breathlessness were the common manifestations; good outcome was observed with conservative therapy. No statistically significant difference was found in outcomes of patients with and positive pleural fluid culture.
Empyema is more common in younger children. This holds true for our study also where 56.7% of the children below 5 years developed the disease. Other authors also reported maximum incidence of the disease under 5 years of age.,,, The age incidence has undergone a change over the years. Infants were more affected in the preantibiotic era, while in later years, preschool children are more affected. The high incidence of empyema in infants and children can be partly explained due to their increased susceptibility to staphylococcal and streptococcal pneumonia, which are the common causes of empyema. In the present study, pneumonia predisposed to 24/60 (40%) of empyemas which was similar to Buckingham et al. In our study, according to the IAP classification of malnutrition, 65% of the total patients were found to be malnourished. It is a known factor that malnutrition predisposes children to recurrent and complicated infections. Hence, the incidence of empyema is reported higher in malnourished children.
Fever was the most common (96.7%) manifestations found at admission followed by cough and breathlessness similar to many other studies.,,,, The decreased incidence of breathlessness at the time of admission may be due to prior treatment with antibiotics. Antibiotic administration prior to the referral may be the factor leading to chronicity.
Culture positivity was found 28% which was significantly lower than the other studies (34%–82%).,, Lower culture positivity might be due to the use of antibiotics before the admission, late referral to a higher center, and lack of better facilities for culture. Stankey et al. also found that the culture positivity decreased to 30% from 67% with the use of antibiotics. Another significant factor is the failure to culture anaerobes, which may be another cause of empyema in children. S. aureus has been the most isolated bacteria in this study cohort which has been reported to be more common than S. pneumoniae as a cause of empyema in Asian and African children.,,, Other causes in this study were S. pneumoniae, Pseudomonas, and Klebsiella pneumoniae. In developed countries, S. pneumoniae is the most common microorganism associated with empyema., Due to delay in seeking medical opinion, poor facilities for culture, and indiscriminate use of antibiotics, it is very difficult to isolate microorganisms in Indian conditions. Another factor is lack of universally accepted guidelines for management of pyothorax. We could not find any statistically significant difference in the outcomes of the patients in terms of duration of chest tube drainage, hospital stay, and final outcome between the patients with sterile and positive pleural fluid culture.
Most patients (56/60, 93%) underwent closed intercostal tube drainage in this study which was successful in 48 patients with an overall success rate of 80%, which was similar to other studies., Satpathy et al. reported an even higher success rate (90.5%) with conservative management. Intrapleural fibrinolytics are not used in our hospital setting, cost constraints being a factor although it is used globally as a medical therapy along with ICD in patients with loculated or thick pleural fluid. Surgery was performed in 8 (13.3%) patients for uncontrolled infection, persistent respiratory distress or pus discharge, large loculations with organized collection, or bronchopleural fistula. Surgical management included VATS and open thoracotomy. The use of VATS for the treatment of childhood empyema has increased during the past few years. It can either be the primary procedure or implemented in cases of failure of treatment with chest drainage. Unsuccessful tube drainage is associated with increased morbidity and longer hospital stay. Early surgical intervention may be performed in the patients who do not respond to a short course of ICD. Ekpe Akpan found decortication thoracotomy superior to ICD in pediatric nontraumatic empyema and recommended it as the primary treatment option when the empyema is chronic or loculated or with thickened pleural membranes.
The study has few limitations also. Many patients had received antibiotic prior to admission, and hence, the pleural fluid culture positivity was found to be low. Although intrapleural fibrinolytics is an accepted therapy in empyema, we did not use it. We could not do spirometry in follow-up because majority of the children were under 5 years of age. The follow-up period was short and so complete pleural recovery could not be documented. Moreover, the sample size was small, so further studies on larger sample size is essential for better results.
| Conclusions|| |
S. aureus is the most common cause of empyema thoracis in our setting. Pleural fluid culture results do not affect the outcomes of the disease. Culture sensitivity to find the causative organism may not be sufficient as it is found to be sterile in high proportion of patients. Conservative management with ICD and antibiotic therapy is effective in most of the cases, but in few cases, surgical intervention is also needed along with antibiotics and ICD for faster recovery.
We acknowledge the contribution of Dr. Sushil Kumar Shukla, M.Sc, Ph.D (Professor of Statistics, Uttar Pradesh University of Medical Sciences, Saifai, Etawah) for helping the statistical analysis.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Satpathy SK, Behera CK, Nanda P. Outcome of parapneumonic empyema. Indian J Pediatr 2005;72:197-9.
Elemraid MA, Thomas MF, Blain AP, Rushton SP, Spencer DA, Gennery AR, et al.
Risk factors for the development of pleural empyema in children. Pediatr Pulmonol 2015;50:721-6.
Chen KY, Hsueh PR, Liaw YS, Yang PC, Luh KT. A 10-year experience with bacteriology of acute thoracic empyema: Emphasis on Klebsiella pneumoniae
in patients with diabetes mellitus. Chest 2000;117:1685-9.
Mishra OP, Das BK, Jain AK, Lahiri TK, Sen PC, Bhargara V. Clinico-bacteriological study of empyema thoracis in children. J Trop Pediatr 1993;39:380-1.
Cohen E, Mahant S, Dell SD, Traubici J, Ragone A, Wadhwa A, et al.
The long-term outcomes of pediatric pleural empyema: A prospective study. Arch Pediatr Adolesc Med 2012;166:999-1004.
Yu D, Buchvald F, Brandt B, Nielsen KG. Seventeen-year study shows rise in parapneumonic effusion and empyema with higher treatment failure after chest tube drainage. Acta Paediatr 2014;103:93-9.
Burgos J, Falcó V, Pahissa A. The increasing incidence of empyema. Curr Opin Pulm Med 2013;19:350-6.
Dass R, Deka NM, Barman H, Duwarah SG, Khyriem AB, Saikia MK, et al.
Empyema thoracis: Analysis of 150 cases from a tertiary care centre in North East India. Indian J Pediatr 2011;78:1371-7.
Zampoli M, Kappos A, Wolter N, von Gottberg A, Verwey C, Mamathuba R, et al.
Etiology and incidence of pleural empyema in South African Children. Pediatr Infect Dis J 2015;34:1305-10.
Erlichman I, Breuer O, Shoseyov D, Cohen-Cymberknoh M, Koplewitz B, Averbuch D, et al.
Complicated community acquired pneumonia in childhood: Different types, clinical course, and outcome. Pediatr Pulmonol 2017;52:247-54.
Menon P, Rao KL, Singh M, Venkatesh MA, Kanojia RP, Samujh R, et al.
Surgical management and outcome analysis of stage III pediatric empyema thoracis. J Indian Assoc Pediatr Surg 2010;15:9-14.
] [Full text]
Togo S, Ouattara M, Sangaré I, Saye J, Touré C, Maiga I, et al. Management for Pediatric Pleural Empyema in Resource-Poor Country: Is Chest Tube Drainage with Antiseptic Lavage-Irrigation Better than Tube Thoracostomy Alone?. Surgical Science, 2015; 6: 541-8.
Saleem AF, Shaikh AS, Khan RS, Khan F, Faruque AV, Khan MA. Empyema thoracis in children: Clinical presentation, management and complications. J Coll Physicians Surg Pak 2014;24:573-6.
Buckingham SC, King MD, Miller ML. Incidence and etiologies of complicated parapneumonic effusions in children, 1996 to 2001. Pediatr Infect Dis J 2003;22:499-504.
Narayanappa D, Rashmi N, Prasad NA, Kumar A. Clinico-bacteriological profile and outcome of empyema. Indian Pediatr 2013;50:783-5.
Goyal V, Kumar A, Gupta M, Sandhu HP, Dhir S. Empyema thoracis in children: Still a challenge in developing countries. Afr J Paediatr Surg 2014;11:206-10.
] [Full text]
Almaramhy HH, Allama AM. Indicators for surgical intervention in thoracic empyema in children. Saudi Med J 2015;36:1061-6.
Grisaru-Soen G, Eisenstadt M, Paret G, Schwartz D, Keller N, Nagar H, et al.
Pediatric parapneumonic empyema: Risk factors, clinical characteristics, microbiology, and management. Pediatr Emerg Care 2013;29:425-9.
Stankey CT, Spaulding AB, Doucette A, Hamre KE, Wheeler W, Pomputius WF, et al.
Blood culture and pleural fluid culture yields in pediatric empyema patients: A retrospective review, 1996-2016. Pediatr Infect Dis J 2018;37:952-4.
Singh AP, Shukla AK, Sharma P, Shukla J. Surgical management of stage III pediatric empyema thoracis. Lung India 2018;35:209-14.
] [Full text]
Mahon C, Walker W, Drage A, Best E. Incidence, aetiology and outcome of pleural empyema and parapneumonic effusion from 1998 to 2012 in a population of New Zealand children. J Paediatr Child Health 2016;52:662-8.
Krenke K, Sadowy E, Podsiadły E, Hryniewicz W, Demkow U, Kulus M. Etiology of parapneumonic effusion and pleural empyema in children. The role of conventional and molecular microbiological tests. Respir Med 2016;116:28-33.
Liese JG, Schoen C, van der Linden M, Lehmann L, Goettler D, Keller S, et al.
Changes in the incidence and bacterial aetiology of paediatric parapneumonic pleural effusions/empyema in Germany, 2010-2017: A nationwide surveillance study. Clin Microbiol Infect 2019;25:857-64.
Hendaus MA, Janahi IA. Parapneumonic effusion in children: An up-to-date review. Clin Pediatr (Phila) 2016;55:10-8.
Ekpe EE, Akpan MU. Outcome of tube thoracostomy in paediatric non-traumatic pleural fluid collections. Afr J Paediatr Surg 2013;10:122-6. [Full text]
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]