Journal of Pediatric Surgery 53 (2018) 644–646
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Evolution of practice in the management of parapneumonic effusion and empyema in children☆ D. Griffith ⁎, M. Boal, T. Rogers Department of Surgery, Bristol Royal Hospital for Children, Upper Maudlin Street, Bristol, BS28BJ, UK
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Article history: Received 28 March 2017 Received in revised form 22 May 2017 Accepted 9 July 2017 Key words: Parapneumonic effusion Thoracotomy Video-assisted thoracoscopic surgery Urokinase
a b s t r a c t Aim: To assess the evolution in management of children with parapneumonic effusion and empyema in a tertiary referral centre. Method: We conducted a retrospective case note review of paediatric patients with parapneumonic effusion, pleural effusion and pleural empyema between December 2006 and December 2015. Digital database searches were performed to identify demographic data, referring hospital, radiological and microbiological investigations. Length of stay and morbidity were analysed. Results: One hundred fifteen patients had 159 interventions over the study period. Fifty-four children were successfully treated with intercostal drainage (ICD) and urokinase fibrinolysis alone. There were 19 primary video assisted thoracoscopic surgeries (VATS) and 12 VATS after initial intercostal drains. Thirty-three children required a thoracotomy, a reduction of 26% from the previous era (p = 0.009). The median length of stay was 9 days (range 2–54). Conclusion: Parapneumonic effusion can be successfully treated with intercostal drainage and intrapleural fibrinolytics, but a proportion requires further surgical intervention. In our hospital, increased utilisation of fibrinolysis and VATS occurred with a corresponding decrease in the need for thoracotomy. Patients needing thoracotomy all had severe disease on ultrasound, but ultrasound did not reliably predict failure of fibrinolytic therapy. Level of Evidence: III Crown Copyright © 2017 Published by Elsevier Inc. All rights reserved.
The incidence of parapneumonic effusion in the paediatric population has increased worldwide [1–3]. Pneumonia may result in parapneumonic effusion that may progress to empyema over three stages. The first stage describes an inflammatory exudate, clear in appearance, of low viscosity and sterile. Stage two results from translocation of white blood cells into the fluid with deposition of fibrin in the pleural space. This causes loculation of fluid and viscid pus. Stage three describes advanced pathology with formation of a thick membrane covering the visceral pleura, causing a rigid ‘peel’ or ‘rind,’ limiting lung expansion and ventilation [4,5] (Table 1). Less than 1% of childhood pneumonias are complicated by pleural empyema [6]. The British Thoracic Society (BTS) guidelines for the management of pleural infection in children mandates pre-intervention ultrasound imaging of the thorax, prompt insertion of an intercostal drain when indicated, use of intra-pleural fibrinolytic therapy via the intercostal drain, and a low rate of drain loss [7]. Some centres advocate early surgical debridement and this approach is reflected by reports in ☆ Disclosure. Conflicts of Interest: None Declared. ⁎ Corresponding author at: Department of HPB Surgery, Derriford Hospital, Derriford Road, Plymouth, PL68DH, UK. E-mail address: dgriffi
[email protected] (D. Griffith). http://dx.doi.org/10.1016/j.jpedsurg.2017.07.017 0022-3468/Crown Copyright © 2017 Published by Elsevier Inc. All rights reserved.
the last decade showing increased use of video-assisted thoracoscopic surgery [8]. A previous report from our centre described thoracotomy in 50% of patients with empyema or parapneumonic effusion [9]. We analysed our more recent experience at a tertiary referral centre to describe how treatment of this condition has evolved over the last two decades and how best to select different treatment options. 1. Method Our centre is a secondary care facility for a major city and a tertiary referral centre for paediatric surgery. We performed a retrospective case note review of paediatric patients up to the age of 16 admitted between December 2006 and December 2015. Our hospital databases were interrogated to identify those children with parapneumonic effusion, pleural effusion and pleural empyema. Cases of pleural effusion without a suspected infective cause were excluded. Demographic data, referral data, radiology reports, microbiology reports, co-morbidities, treatment, length of stay, morbidity and outcomes were analysed. Analgesia and anaesthetic techniques were not assessed. For those patients receiving fibrinolysis, the regimen consisted of Urokinase (40,000 U in 40 ml 0.9% saline) twice daily instilled through the ICD, with a 4 h dwell time.
D. Griffith et al. / Journal of Pediatric Surgery 53 (2018) 644–646
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Table 1 Ultrasound stages of parapneumonic effusion and single primary intervention. Staging of effusion pre-op
ICD VATS Thoracotomy Total
Total
1
2
3
12 0 0 12
15 10 0 25
18 4 7 29
45 14 7
2. Results One hundred fifteen patients were admitted during the study period. 60 were female and 55 were male. The mean age at admission was 4.95 years (range 61 days to 14.66 years). Medical comorbidities were present in 16 patients, of which asthma was the most common (4 children). Seventy six patients (66%) were referred from 14 different referring hospitals. Admissions were highest in December and March, showing a biphasic pattern across the years of study. In cases that required more than one intervention, the decision to escalate treatment was made by a team including respiratory physicians and surgeons. The surgical approach considered the complexity of the empyema and the surgeon's experience in thoracoscopic surgery. Initial treatment with antibiotics was often commenced at referring hospitals, with some centres inserting intercostal drains. Pre-operative chest ultrasound was performed in 95 patients (82.6.3%). Computed tomography (CT) of the chest was performed in 2 patients at their referring hospital before transfer. The staging of parapneumonic effusion by ultrasound is described below (Table 1). Assessment of the ultrasound findings grouped patients into 3 stages of severity: Stage 1: anechogenic collections without loculations. Stage 2: fibrinous septations but no homogeneous echogenic loculations or thickened parietal rind. Stage 3: complex ultrasound appearance with either thickened ‘rind’, multiple loculations, or entrapped underlying lung. Most pleural fluid samples did not culture any organisms, but most positive cultures grew Streptococcus pneumoniae (Table 2). One patient had concurrent streptococcus pneumoniae and H1N1 influenza A. Results were not available in 12 patients. It is not certain if this was because no fluid was sent or whether a change of pathology systems meant there was no result transferred from the previous system. Eighty-six children had an initial ICD and fibrinolysis, of whom 54 patients (62.8%) were successfully treated without further surgical intervention; 22 (26.1%) of children were referred from other hospitals for failed treatment with ICD and fibrinolysis. Primary VATS procedures were done in 19 patients. VATS following failure of ICD treatment was performed in 12 patients. Of the 31 VATS procedures, 2 were
Fig. 1. Surgical intervention sequence.
immediately converted to thoracotomy and a further 2 required a subsequent thoracotomy and decortication (Fig. 1). Primary thoracotomy was performed in 10 patients (8.7%), 4 with pneumatocoele or pneumothorax, 2 for lung necrosis and 4 for thick peel on imaging. A second thoracotomy was performed on 1 patient after they developed a bronchopleural fistula. Treatment with ICD followed by thoracotomy occurred in 18 patients. Overall, 32 (27.8%) children required more than one intervention and 159 total procedures were performed. Previous research published from the same centre demonstrated a high thoracotomy rate of 50% between 1998 and 2001 [9]. Along with the increase in VATS, since its adoption at our centre, the thoracotomy rate has been reduced by 26%, which is statistically significant, as demonstrated in Table 3. The median length of stay (LOS) was 9 days (range 2–54 days). The length of stay before transfer from the referring hospital was not available for analysis. The median LOS after ICD was 7.5 days, post primary VATS was 6 days and post primary thoracotomy was 5 days. The patient with a 2 day LOS was transferred to another centre for extra-corporeal membrane oxygenation (ECMO). The patients requiring the longest LOS had respiratory failure needing admission to the paediatric intensive care unit renal failure requiring haemofiltration. Intercostal drains fell out in 2 patients at their referring hospitals, one required a VATS procedure and the other a thoracotomy. Three intercostal drains fell out at our centre, 4 further drains were required for persistent effusion after intervention, without other adverse US findings. The overall surgical complication rate was 8.2%, with no mortality (Table 4). 3. Discussion
Table 2 Pleural fluid organisms. Organism cultured
Frequency
%
No growth Streptococcus pneumoniae Streptococcus pyogenes Fusobacterium necrophorum Haemophilus influenzae Mycobacterium Streptococcus intermedius Chlamydia psittacae Chlamydia pneumoniae Staphylococcus aureus Human metapneumovirus H1N1 A Adenovirus Rhinovirus No culture result
58 27 9 1 1 1 1 1 1 1 2 1 1 1 12
49.2 22.9 7.6 0.8 0.8 0.8 0.8 0.8 0.8 0.8 1.7 0.8 0.8 0.8 10.2
Paediatric parapneumonic effusion is associated with a significant surgical healthcare burden. Our study demonstrates that a causative organism can be elusive in most cases. This has been previously reported and is possibly due to the initial antibiotic treatment for suspected pulmonary infection sterilising the effusion, with the inflammatory process continuing. Several studies reported an increase in the incidence of parapneumonic effusion in the late nineties and early 2000s
Table 3 Surgical procedures at the regional referral centre. Intervention
2006–2015
1998–20019
p†
Intercostal drain VATS Thoracotomy
54 31 33
22 0 24
p = 0.056687 p = 0.000064 p = 0.009
†
chi-Square test.
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D. Griffith et al. / Journal of Pediatric Surgery 53 (2018) 644–646
duction of VATS to our centre has coincided with a significant reduction (Table 3) on the thoracotomy rate, 50% decrease in 10 years.
Table 4 Surgical complications.
Fall Out Re-accumulation of effusion Re-admission Peritoneal port Significant Bleed
Chest drain
VATS
Thoracotomy
2 1 2 -
1 2 1 -
3 1
[1–3,10–12]. Some studies reported a decline following the introduction of conjugate pneumococcal vaccine, with immunisation in the UK beginning in 2006 [10,13]. The vaccine was modified to encompass more serotypes in March 2010, after concern regarding an increase in specific serotypes not covered by the existing vaccine [14]. Streptococcus pneumoniae was the most common causative organism in this cohort, as reported in other research [1–3,10–12]. Eastham et al. (2004) demonstrated different pneumococcal serotypes on PCR, in patients with negative fluid culture results [12]. This is favourable in comparison to previously published data, however our cohort was not randomised to treatment allocation [5,6,15,16]. The BTS Guidelines (2005) do not state accepted drain loss rate, but our figure of 3.14% is low [7]. The proportion of patients requiring intervention more invasive than intercostal drain was 37.1% and includes those patients that had primary VATS or thoracotomy or those that required surgical management for complications of the disease process. This includes those patients with broncho-pleural fistulae. Other studies have reported high intervention rates other than ICD [5,12,16]. Thoracoscopic drainage has increased in utilisation since description of the technique by Kern and Rodgers in 1993 [17]. The benefit is the ability to mechanically breakdown fibrous septae, decorticate the lung, drain and irrigate the pleural cavity to allow lung expansion. Some authors have postulated that because intercostal drainage in children often requires a general anaesthetic for physical and mental wellbeing and procedural safety, an initial thoracoscopy could be of benefit [6]. This group found that patients undergoing primary VATS procedure had significantly shorter duration of antibiotic therapy, shorter time with ICD in situ and shorter hospital stay. Patients also experienced fewer invasive procedures and no thoracotomies, in comparison to a group initially managed with and ICD and fibrinolysis [6]. In 2005, a Cochrane Library review found only one appropriate RCT on the topic with questions over validity and bias, however it did suggest a higher primary treatment success for VATS and shorter length of stay [4]. This review does not describe a randomised trial of interventions, but adoption of novel techniques has been successful locally. The intro-
4. Conclusion This research from a UK regional paediatric referral centre demonstrates the limited success of intrapleural fibrinolytic therapy and reduction in thoracotomy rates with increased utilisation of VATS procedures. A multidisciplinary approach with radiologists, physicians and surgeons is essential in managing paediatric parapneumonic effusion. References [1] Li S, Tancredi D. Empyema hospitalizations increased in US children despite pneumococcal conjugate vaccine. Pediatrics 2010;125(1):26–33. [2] Yu D, Buchvald F, Brandt B, et al. Seventeen-year study shows rise in parapneumonic effusion and empyema with higher treatment failure after chest tube drainage. Acta Paediatr 2014;103(1):93–9. [3] Mahon C, Walker W, Drage A, et al. 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. [4] Coote N, Kay E. Surgical versus non-surgical management of pleural empyema. Cochrane Database Syst Rev 2005(4):CD001956. [5] Long A, Smith-Williams J, Mayell S, et al. ‘Less may be best’—Pediatric parapneumonic effusion and empyema management: Lessons from a UK centre. J Pediatr Surg 2016;51(4):588–91. [6] Cohen G, Hjortda V, Ricci M, et al. Dinwiddie et al. Primary thoracoscopic treatment of empyema in children. J Thorac Cardiovasc Surg 2003;125(1):79–84. [7] Balfour-Lynn I, Abrahamson E, Cohen G, et al. Parikh et al. BTS guidelines for the management of pleural infection in children. Thorax 2005;60(Suppl. 1):i1–i21. [8] Bishay M, Short M, Shah K, et al. Efficacy of video-assisted thoracoscopic surgery in managing childhood empyema: a large single-centre study. J Pediatr Surg 2009; 44(2):337–42. [9] Hilliard T, Henderson A, Langton Hewer S. Management of parapneumonic effusion and empyema. Arch Dis Child 2003;88(10):915–7. [10] Byington C, Spencer L, Johnson T, et al. An epidemiological investigation of a sustained high rate of pediatric parapneumonic empyema: risk factors and microbiological associations. Clin Infect Dis 2002;34(4):434–40. [11] Buckingham S, King M, Miller M. Incidence and etiologies of complicated parapneumonic effusions in children, 1996 to 2001. Pediatr Infect Dis J 2003; 22(6):499–503. [12] Eastham K, Freeman R, Kearns A, et al. Clinical features, aetiology and outcome of empyema in children in the north east of England. Thorax 2004;59(6):522–5. [13] Public Health England. Immunisation against infectious diseases. https://www.gov. uk/government/collections/immunisation-against-infectious-diseasethegreenbook, Accessed date: 14 October 2016. [14] Hanquet G, Kissling E, Fenoll A, et al. Pneumococcal serotypes in children in 4 European countries. Emerg Infect Dis 2010;16(9):1428–39. [15] Thomson A, Hull J, Kumar M, et al. Randomised trial of intrapleural urokinase in the treatment of childhood empyema. Thorax 2002;57:343–7. [16] Goldin A, Parimi C, LaRiviere C, et al. Outcomes associated with type of intervention and timing in complex pediatric empyema. Am J Surg 2012;203(5):665–73. [17] Kern J, Rodgers B. Thoracoscopy in the management of empyema in children. J Pediatr Surg 1993;28(9):1128–32.