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Ann Thorac Surg 2003;76:1854-1858
© 2003 The Society of Thoracic Surgeons


Original article: general thoracic

Is open thoracotomy still a good treatment option for the management of empyema in children?

Christos Alexiou, FRCSa, Anuj Goyal, MBBSa, Richard K. Firmin, FRCSa, Mark St. J. Hickey, FRCSIa*

a Department of Cardiothoracic Surgery, Glenfield General Hospital, Leicester, United Kingdom

* Address reprint requests to Dr Hickey, Department of Cardiothoracic Surgery, Glenfield General Hospital, Groby Rd, Leicester LE3 9QP, UK
e-mail: mark.hickey{at}uhl-tr.nhs.uk

Presented at the Poster Session of the Thirty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2003.


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
BACKGROUND: The incidence of pediatric postpneumonic empyema increases, and there is little consensus on its management. Open thoracotomy has been linked with high morbidity and prolonged hospitalization. Our aim was to review the outcome after open thoracotomy and to provide a set of data for comparison with other treatment modalities.

METHODS: Forty-four children (median age, 8 years, 2 months to 16 years) undergoing surgery for postpneumonic empyema between 1993 and 2002 in our unit were studied.

RESULTS: The median time from onset of symptoms to admission in a pediatric unit was 8 days (range, 2 to 63 days), the median time from pediatric admission to surgical referral was 3 days (range, 0 to 19 days), and the median time from surgical admission to thoracotomy was 1 day (range, 0 to 2 days). Eight children had a chest drain before surgical admission. Six patients, who were referred late (19 to 69 days), had lung abscesses. A limited muscle sparing thoracotomy (44 patients), formal decortication (36 patients), lung debridement (5 patients), and lobectomy (1 patient) were performed. After thoracotomy, median time to apyrexia was 1 day (range, 0 to 27 days) and drain removal was 3 days (range, 1 to 16 days). A pathogen was isolated in 21 patients. There were no deaths. Four children with abscesses remained septic and had lobectomies (2 patients) and debridements (2 patients). The median postoperative hospital stay was 5 to 53 days. One child had postpneumonic empyema develop and had decortication 3 months postoperatively. At follow-up, all children were doing well and had satisfactory radiographs. The Kaplan-Meier 5-year and 10-year survival rate, freedom from any reoperation, and freedom from hospital readmission were 100%, 87%, and 98%, respectively.

CONCLUSIONS: Open thoracotomy remains an excellent option for management of stage II–III empyema in children. When open thoracotomy is performed in a timely manner there is low morbidity and it provides rapid resolution of symptoms with a short hospital stay. However, delayed referrals may result in advanced pulmonary sepsis and a protracted clinical course. The late results are encouraging. Use of thoracoscopy or fibrinolysis should be considered on the basis of their own merit, not on the assumption of probable adverse outcomes after thoracotomy.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Pulmonary infection is the most frequent cause of empyema in adults and children [1, 2]. Thoracic empyema in the pediatric population is uncommon, affecting about 0.6% of children hospitalized with pneumonia [2, 3]. There is evidence that the incidence of empyema is increasing in the United Kingdom, the United States, and elsewhere [3, 4]; however the reasons for this are not entirely clear. The number of children referred for surgical treatment of postpneumonic empyema in our unit over the last 10 years has risen exponentially (Fig 1).



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Fig 1. Surgery for pediatric empyema at Glenfield General Hospital between 1993 and 2002.

 
An empyema typically progresses through three phases. The early exudative phase with thin fluid and a few cells (stage I), the fibrinopurulent phase with large quantities of white cells and fibrin, resulting in loculations and the formation of a limited membrane around the lung (stage II), and an organizing phase with fibroblasts growing into the exudates producing an inelastic membranous "peel" that encases the lung limiting its mobility (stage III).

Treatment options include thoracentesis and antibiotics with chest drainage, instillation of fibrinolytic agents into the pleural cavity, open thoracotomy with decortication, and more recently, video assisted thoracoscopic surgery (VATS).

There is little consensus on the most appropriate type and timing of therapy. Thoracentesis, antibiotic treatment, and chest tube drainage usually suffice for stage I disease, but more needs to be done for advanced empyema. The proponents of VATS [57] and fibrinolysis [8, 9] link thoracotomy with high morbidity and prolonged hospital stay, but a recent report has challenged this view [10].

Early and limited muscle-sparing thoracotomy has been our treatment of choice for children with stage II–III empyema. The purpose of this study was to review the outcome obtained with this therapeutic approach and to provide a framework of data for comparison with other treatment modalities.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The Glenfield General Hospital in Leicester is a tertiary referral center providing adult and pediatric cardiac and thoracic surgery services in a population of 2 million residents living in East Midlands, England.

Children suffering from pneumonia in this region are first seen by general practitioners who usually commence with empirical antibiotic treatment, and refer those patients with persistent symptoms to pediatricians. The children who have empyema develop that is either unresponsive to medical management (which may include chest tube drainage and fibrinolysis) or is considered to be too advanced to be treated by nonsurgical means based on its clinical and radiologic features, are referred to the pediatric cardiothoracic surgeons (RKF, MSJH). The surgeons have no input in any aspect of the management of these children before the surgical referral, the timing of which was at the discretion of the attending pediatricians.

Between 1993 and 2002, 46 children underwent thoracotomy for empyema in our unit. Two children, whose medical records could not be found, were excluded from the study. The remaining 44 patients are the subjects of this report, which involved 22 boys and 22 girls with a median age of 8 years (range, 2 months to 16 years).

Data collection and statistics
Data were collected retrospectively by a detailed review of the patients' medical records. Additional information was obtained by contacting the referring pediatricians and the general practitioners.

Continuous variables are presented with median values and ranges, and proportions as percentages. Freedom from any reoperation, hospital readmission, and survival rates were calculated with the product limit method of the Kaplan-Meier test. The statistical SPSS package (version 11.5 [SPSS Inc, Chicago, IL]) was used for data analysis.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Preoperative clinical features and investigations
Cough, dyspnea, malaise, and chest pain were the more common presenting symptoms. All children had fever before thoracotomy, despite having received as many as five various types of antibiotics.

The diagnosis of empyema was based on hematologic, microbiologic, and imaging investigations and was confirmed at operation. A chest radiograph was performed on all children, a chest ultrasound in 38 patients, and computed tomography of the chest in 9.

A chest drain was inserted in 8 patients before surgical referral, producing a minimal amount of drainage in 6. A chest drain insertion was not attempted in the remaining 36 children, because their clinical status and the findings of their chest ultrasounds were indicative of the need for surgical intervention.

The offending pathogens were identified in 21 patients (48%) (10 patients before and 11 after the operation). These were Streptococcus pneumoniae in 11, Staphylococcus aureus in 6, Myobacterium tuberculosis in 2, and mixed microorganisms in 2 children.

Time between onset of symptoms and surgery
The overall median time elapsed between onset of symptoms and thoracotomy was 14 days (range, 4 to 69 days). The median time between onset of symptoms and admission to a pediatric unit was 8 days (range, 2 to 63 days). The median time from pediatric hospital admission to surgical referral was 3 days (range, 0 to 19 days). From the onset of admission to the cardiothoracic unit, surgery was carried out after a median time of 1 day (range, 0 to 2 days) (Fig 2).



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Fig 2. Breakdown of the time interval elapsed between onset of symptoms and operation.

 
Perioperative management
A small, approximately 4-cm long, muscle-sparing thoracotomy was performed in most patients (extended as required in older children and in those having coexisting lung abscess), the loculi were broken down, the pleural cavity, and parietal and visceral pleural were thoroughly debrided, and the chest was closed in layers having previously inserted one or two intercostal chest drains.

A thick fibrous visceral pleural peel (encasing the lung) was present in 34 patients who required a formal decortication.

Six children had severe coexisting pulmonary sepsis. Five of these children had a lung abscess managed with lung debridement, and 1 had lobar necrosis necessitating a lobectomy. When necessary, an intercostal muscle flap was used to cover the raw surface areas of the lung after debridement. The time interval between onset of symptoms and thoracotomy in these children was 19 to 69 days, considerably longer than the median time of 14 days observed for the entire group (Fig 2).

After the operation, children were extubated in the operating room or in the pediatric intensive care unit.

Analgesia was provided by means of intercostal nerve blocks with a local anesthetic agent (bupivacaine), intravenous opioids, and oral analgesics. Early removal of the chest drains and ambulation were strongly encouraged.

Early outcome
Thirty-five children stayed in the pediatric intensive care unit for a median of 2 hours (range, 2 to 48 hours), and 5 of these children were ventilated for up to 1 day.

After thoracotomy, the median time until apyrexia was 1 day (range, 0 to 27 days). The chest drains were removed after a median of 3 days (range, 1 to 16 days) with a median drainage of 250 mL in total (range, 55 to 980 mL).

Four children who had lung abscess exhibited severe persistent sepsis, despite the administration of intravenous antibiotics. Two of these children underwent lobectomy, and the other 2 had further lung and pleural debridement. One of these children had a hemothorax develop, and thus had an exploratory thoracotomy.

All children recovered well and left the hospital after a median stay of 5 days (range, 4 to 53 days).

Follow-up
Children were seen in the outpatient clinics by surgeons or pediatricians at 6 weeks after hospital discharge and subsequently at 3-month intervals until complete radiologic resolution of empyema signs. Thereafter, these patients have been under the care of their family doctors.

Late outcome
One child had postpneumonic empyema develop and underwent a further thoracotomy and decortication 3 months postoperatively, and thereafter had an uncomplicated recovery.

There have been no other late problems or hospital readmissions related to the empyema.

At latest follow-up all patients were in excellent clinical condition and had satisfactory chest radiographs. The Kaplan-Meier 5-year and 10-year survival rate was 100%, freedom from any reoperation was 87% ± 5%, and freedom from hospital readmission associated with the empyema was 98% ± 2% (Fig 3).



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Fig 3. Kaplan-Meier survival rate, freedom from any reoperation, and hospital readmission.

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
We have conducted this study stimulated by the cited increasing incidence of pediatric empyema [3, 4], the continuous uncertainty as to its most appropriate management, and the expressed concerns for possible adverse effects of thoracotomy.

There has been a significant rise in the number of children referred for surgery to our unit over the last decade, but there are no data available to confirm whether this reflects a real increase or not of empyema cases in East Midlands. However, a true increase in the incidence of pediatric empyema recently has been recorded in the neighboring region of West Midlands [4]. The reason for this trend is not fully understood, but changes in the practice of antibiotic prescribing and the vaccination program (favoring the emergence of more virulent microorganisms) are quoted as a possible explanation [3]. In this study, the aggressive nature of the offending microorganisms is suggested by the presence of stage III empyema among children undergoing early thoracotomy (ie, within 14 days after the onset of their symptoms).

Mavroudis and colleagues [11] provided data on the infectious potential of main bacterial groups. In their animal studies, gram-negative bacteria produced a more severe infection than their gram-positive counterparts. Anaerobic bacteria failed to produce clinical empyema, but it enhanced the virulence of S. aureus and Escherichia coli [11]. In keeping with previous clinical reports [1, 510], S. pneumoniae and S. aureus were the most common pathogens in this series.

Clinical and experimental [12] experience have shown that stage I empyema can be managed with antibiotics and chest tube drainage. A more elaborated treatment is needed for stage II and III disease. There are no controlled trials to compare the merit of each therapy. As a result, the established institutional practices and management algorithms depend on available facilities and expertise.

As a tertiary specialist cardiothoracic center, we are at the receiving end dealing with children who had a failed trial of nonsurgical management of variable duration. These children are usually referred with advanced empyema and are frequently very sick and in need of immediate surgical intervention. In these circumstances an early, limited muscle-sparing thoracotomy is our preferred approach.

Some authors, advocating the use of VATS or fibrinolysis, acknowledge that thoracotomy with decortication produces good results, but suggest that it carries high morbidity and requires prolonged hospitalization [59], often quoting articles published in the 1970s and 1980s.

This study shows evidence in the current era that performing thoracotomy in children with advanced empyema has a low morbidity and results in prompt resolution of pyrexia (median, 1 day), early drain removal (median, 3 days), and short hospital stay (median, 5 days) with most patients. Similar results after early open thoracotomy and decortication (time to apyrexia, 1 to 2 days; drain removal, 2 days; and hospital stay, 4 days) have been recently reported from another center in the United Kingdom [10].

Problems encountered in this series were related to the presence of lung abscess and lobar necrosis. Despite efforts to preserve lung parenchyma, persistent sepsis mandated lobar resection in 3 children (performed as a primary procedure in 1 and during the same hospital admission in 2) and further debridement in 2. Of note, these 5 children were referred late, having previously received ineffective chest drains and broad-spectrum antibiotics. It seems likely that such problems could have been avoided by earlier surgery, and the need for a timely surgical consultation can not be overemphasized [13]. Children referred within 2 weeks from the onset of their symptoms, had no pulmonary abscess and enjoyed a short and uncomplicated postoperative course.

Data of the long-term outcome after open surgery for advanced empyema are limited. This study demonstrates that thoracotomy achieves a lasting satisfactory result, as evidenced by a 5-year and 10-year Kaplan-Meier survival rate of 100% and freedom from hospital readmission of 98%. Hospital readmissions and reoperations adversely impact quality of life for the children and their families; it is encouraging that these were kept to a minimum.

The complications of incisional pain and scoliosis late after thoracotomy, which are well described in adult patients, were not observed in the present series. The capability of tissues to readily regenerate at pediatric age and the use of a muscle-sparing thoracotomy may in part account for this.

Other available treatment options for stage II–III empyema merit further discussion.

Intrapleural instillation of streptokinase or urokinase has been shown to increase the amount of chest drainage and effecting a cure in large proportions of patients in some studies [8, 9]. However, this requires general anesthesia for drain insertion, which can be painful and carries a small, but not negligible, risk of bleeding, anaphylaxis, and death. Seemingly less invasive, fibrinolysis can be traumatic and poorly tolerated by a "young" child. Also, the possible need for a subsequent rescue thoracotomy should not be underestimated. In a retrospective comparison, Balci and colleagues reported a success rate of 100% for thoracotomy and 68% for fibrinolysis, with 1 child in the latter group dying as a result of anaphylactic reaction and pleural hemorrhage [14].

Use of VATS for pediatric empyema has led to variable outcomes that may reflect the differences in the disease severity of the children involved. Steinbrecher and Najmaldin [15] and Tonz and colleagues [16] reported a failure rate of 70% and 100%, respectively, in small groups of children with multi-loculated, organizing empyema. Good results after VATS use at an earlier stage have been described by others [58] who propose this modality as a first line of treatment before chest drain insertion.

Comparison of published institutional experiences using differing treatment protocols should be undertaken cautiously, bearing in mind that the thoracotomy series tend to include more severely ill children.

Perceived advantages of VATS over open thoracotomy are speedier recovery and shorter hospitalization with less pain, better cosmesis, and improved late functional outcome.

However, compared with VATS, time to apyrexia, duration of chest drainage, and hospital stay, all appear to be more favorable after thoracotomy in the present study and in the recent report from Newcastle, United Kingdom [10] (Table 1).


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Table 1. Early Outcome After Treatment of Pediatric Empyema With Thoracotomy or Video-Assisted Thoracoscopic Surgery

 
Postoperative pain has not been a problem in this series. It has been effectively controlled by using intercostal nerve blocks, intravenous opioids and oral analgesics, and by encouraging early drain removal and ambulation.

Cosmesis may indeed be improved with VATS, although in most cases a thoracotomy incision of as little as 4 to 5 cm is not much longer than the added length of the skin incisions needed for thoracoscopy. In any case, we believe that the safety and efficacy of each procedure are more important considerations than the cosmesis.

In regard to the late functional outcome, previous studies have demonstrated similar respiratory function in children after open thoracotomy and tube drainage [17, 18].

Clearly, a prospective, controlled trial (stratifying the patients involved by disease severity) [19] is required to assess the merit of various treatment options available for stage II–III empyema.

In conclusion, open thoracotomy remains an excellent option for the management of stage II–III empyema in children. Timely performed, open thoracotomy carries low morbidity, providing rapid resolution of symptoms with a short hospital stay. However, delayed referrals may result in advanced pulmonary sepsis and a protracted postoperative course. The late results are encouraging. Other treatment modalities (thoracoscopy, fibrinolysis) should be considered on the basis of their own merit, not on the assumption of probable negative effects after thoracotomy.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Mavroudis C., Symmonds J.B., Minagi H., Thomas A.M. Improved survival in management of empyema thoracis. J Thorac Cardiovasc Surg 1981;82:49-57.[Abstract]
  2. Lewis R.A., Feigin R.D. Current issues in the diagnosis and management of paediatric empyema. Semin Pediatr Infect Dis 2002;13:280-288.[Medline]
  3. Tan T.Q., Mason E.O., Jr, Wald E.R., et al. Clinical characteristics of children with complicated pneumonia caused by Streptococcus pneumoniae. Pediatrics 2002;110:1-6.[Abstract/Free Full Text]
  4. Rees J.H., Spencer D.A., Parikh D., Weller P. Increase in incidence of childhood empyema in West Midlands, UK. Lancet 1997;349:402.[Medline]
  5. Grewal H., Jackson R.J., Wagner C.W., Smith S.D. Early video-assisted thoracic surgery in the management of empyema. Pediatrics 1999;103:63.
  6. Kercher K.W., Attorri R.J., Hoover J.D., Morton D., Jr Thoracoscopic decortication as first-line therapy for pediatric parapneumonic empyema. Chest 2000;118:24-27.[Abstract/Free Full Text]
  7. Kern J.A., Rodgers B.M. Thoracoscopy in the management of empyema in children. J Pediatr Surg 1993;28:1128-1132.[Medline]
  8. Barbato A., Panizzolo C., Monciotti C., Marcucci F., Stefanutti G., Gamba P.G. Use of urokinase in childhood pleural empyema. Pediatr Pulmonol 2003;35:50-55.[Medline]
  9. Kilic N., Celebi S., Gurpinar A., et al. Management of thoracic empyema in children. Pediatr Surg Int 2002;18:21-23.[Medline]
  10. Carey J.A., Hamilton J.R.L., Spencer D.A., Gould K., Hasan A. Empyema thoracis: a role for open thoracotomy and decortication. Arch Dis Child 1998;79:510-513.[Abstract/Free Full Text]
  11. Mavroudis C., Ganzel B.L., Cox S.K., Polk H.C., Jr Experimental aerobic-anaerobic thoracic empyema in the guinea pig. Ann Thorac Surg 1987;43:298-302.[Abstract]
  12. Mavroudis C., Katzmark S.L., Ganzel B.L., Gray L.A., Jr, Polk H.C., Jr Successful treatment of empyema thoracis with polymethylmethacrylate antibiotic-impregnated beads in the guinea pig. Ann Thorac Surg 1988;46:615-618.[Abstract]
  13. Chen B.L.E., Langer J.C., Dillon P.A., et al. Management of late-stage parapneumonic empyema. J Pediatr Surg 2002;37:371-374.[Medline]
  14. Balci A.E., Eren S., Ulku R., Eren M.N. Management of multiloculated empyema thoracis in children: thoracotomy versus fibrinolytic treatment. Eur J Cardiothorac Surg 2002;22:595-598.[Abstract/Free Full Text]
  15. Steinbrecher H.A., Najmaldin A.S. Thoracoscopy for empyema in children. J Pediatr Surg 1998;33:708-710.[Medline]
  16. Tonz M., Ris H.B., Casaulta C., Kaiser G. Is there a place for thoracoscopic debridement in the treatment of empyema in children?. Eur J Pediatr Surg 2000;10:88-91.[Medline]
  17. Mayo P., Saha S.P. Acute empyema in children treated by open thoracotomy and decortication. Ann Thorac Surg 1982;34:401-407.[Abstract]
  18. Hoff S.J., Neblett W.W., Edwards K.M., et al. Parapneumonic empyema in children: decortication hastens recovery in patients with severe pleural effusions. Pediatr Infect Dis J 1991;10:194-199.[Medline]
  19. Ramnath R.R., Heller R.M., Ben-Ami T., et al. Implications of early sonographic evaluation of parapneumonic effusions in children with pneumonia. Pediatrics 1998;101:68-71.[Abstract/Free Full Text]



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