By Suchar, Adam M; Zureikat, Amer H; Glynn, Loretto; Statter, Mindy B; Et al
ADAM M. SUCHAR, B.S., AMER H. ZUREIKAT, M.D., LORETTO GLYNN, M.D., MINDY B. STATTER, M.D., JONGIN LEE, M.D., DONALD C. LIU, M.D., PH.D.
From the University of Chicago Comer Children’s Hospital, Chicago, Illinois
Video-assisted thoracoscopic decortication (VATD) has been established as an effective and potentially less morbid alternative to open thoracotomy for the management of empyema. However, the timing and role of VATD for advanced pneumonia with empyema is still controversial. In assessing surgical outcome, the authors reviewed their VATD experience in children with empyema or empyema with necrotizing pneumonia. The charts of 42 children who underwent VATD at our institution between July 2001 and July 2005 were retrospectively reviewed for surgical outcome. For purposes of analysis, patients were cohorted into four classes with increasing severity of pneumonia: 1 (-) intraoperative pleural fluid cultures, (-) necrotizing pneumonia, 18 (43%); 2 (+) pleural fluid cultures, (- ) necrotizing pneumonia, 10 (24%); 3 (-) pleural fluid cultures, (+) necrotizing pneumonia, 6 (14%); 4 (+) pleural fluid cultures, (+) necrotizing pneumonia, 8 (19%). A P value of
EMPYEMA THORACIS COMPLICATES the course of 2% to 8% of children hospitalized for pneumonia in the United States,1 and has significant morbidity, mortality, and consumption of hospital resources if not recognized or treated appropriately. Recent studies have noted an increase in the incidence of pediatric empyema cases.2- 4 Despite this condition being relatively common, the management of empyema in children remains controversial. The armamentarium of therapeutic options includes intravenous antibiotics with repeated thoracentesis,5 chest tube drainage,6, 7 image-directed drainage,8 fibrinolytics,9, 10 video-assisted thoracoscopic decortication (VATD),11-13 minithoracotomy,14 open drainage, and formal thoracotomy with decortication.15 There is still no consensus regarding the ideal treatment or even the ideal timing of various treatment options available.
Empyema is believed to originate as a parapneumonic fluid collection subsequently infected by an adjacent lung infection. The American Thoracic Society has classified empyema as having three fairly dynamic stages. Stage I or acute exudative phase is characterized by pleural inflammation that has lead to an accumulation of thin, free-flowing pleural fluid with low cellular content; some investigators refer to this stage as a parapneumonic effusion. The fluid is not thick enough to prevent the lung from reexpanding when the fluid is drained. Stage II is the fibropurulent phase characterized by thick exudates with bacterial invasion and accumulation of polymorphonuclear leukocytes and fibrin, which can result in the formation of loculations. Stage III, or the chronic organizing phase, is characterized by a thick inelastic fibrotic peel that can lead to complete parenchymal entrapment. Although antibiotics with repeated thoracentesis may be adequate for stage I disease, the presence of loculations and fibrinous adhesions as seen in later stages makes simple drainage difficult, if not impossible.16
Recent reports have indicated the success of VATD in the treatment of pediatric empyema thoracis, resulting in shorter hospital stays, decreased overall number of procedures, shorter period of chest tube drainage, greater postoperative comfort, decreased costs, and smaller scars when compared with other treatment modalities.17-20 While the efficacy of VATD in empyema has been noted, there have been no investigations to date that have looked at the timing and use of VATD in complicated pneumonias including necrotizing pneumonia. The purpose of this study was to analyze the role of VATD for the treatment of complicated empyema in the presence of necrotizing pneumonia, especially those caused by multidrug resistant organisms, notably methicillin-resistant S. aureus (MRSA) seen in large tertiary care children’s hospitals today. Furthermore, a new surgical classification system, the University of Chicago Empyema Classification System (UCEC) for empyema is proposed. Since empyema is not a homogenous entity, it is likely that different treatment strategies may be appropriate for different presentations and manifestations of empyema. Thus, it is the authors’ belief that the proposed classification system would allow for investigation of the efficacy of VATD in the management of empyema of varying severity.
Methods
An institutional review board approved retrospective chart review of 42 consecutive pediatric empyema thoracis patients who underwent video-assisted thoracoscopic decortication (VATD) at the University of Chicago Children’s Hospital between July 2001 and July 2005 was conducted. The following data were obtained from the chart review: age, gender, duration of presurgery antibiotics, treatment and operative details, imaging studies, site of pneumonia, anesthesia, culture reports, incidence of necrotizing pneumonia, duration of chest tube drainage and fever, hospital length of stay, and outcome on follow-up. All patients were treated by the pediatric surgical service. The study contained 21 female and 21 male patients. The average patient age was 5.9 years (range, 4 months to 19 years). All patients were determined to have empyema thoracis by clinical examination and appropriate radiological studies (chest X-ray, ultrasound, and/or CT scan). All patients received varying courses of intravenous antibiotics before VATD, with some having had preVATD thoracentesis and/or thoracostomy tube placement. VATD was performed in all cases after initiation of intravenous antibiotics. Indications for VATD in all cases included persistent fever, leukocytosis, supplemental oxygen requirement, and loculated pleural fluid collection by ultrasound or CT. Thoracostomy tubes were removed when patients defervesced (24 hours) and thoracostomy drainage was minimal. Patients were discharged from the surgery service when afebrile for >24 hours after thoracostomy removal with an acceptable chest x-ray. Mean follow-up was 171.8 days (range 28-281 days). Preoperative length or duration was defined as the interval between the date of hospital admission at our institution and surgical intervention. Time to surgical discharge was defined as the interval between surgery and definitive chest tube removal. The duration of postoperative length of stay was defined as the interval between date of surgical intervention and date of hospital discharge.
For purposes of analysis, patients were cohorted in to a class within the UCEC system. This classification system is depicted in Fig. 1. Organisms defined as pathogens included 5. pneumoniae, S. sanguis, Staphylococcus aureus, group A Streptococcus, and coagulase negative Staphylococcus. A P value of
Surgical Technique
The operation performed was a modification of a well-described technique.16 After induction of general anesthesia, a single-lumen endotracheal tube was inserted and the patient placed in a lateral decubitus position with the involved side facing up. In brief, two or three 5 mm trocar sites were placed along the chest wall to allow adequate visualization and comprehensive access for various angles of dissection to lyse fibrinopleural adhesions and/or exudates. All purulent tissue and fibrin peel within the pleural cavity and the lung parenchyma were evacuated thoracoscopically, and the infected necrotic lung tissue was excised and removed. Pleural fluid and fibrinopleural exudates were sent for Gram stain and culture. The procedure was terminated when all lobes were clearly visualized, the visceral pleura was satisfactorily freed of exudates, and the lung was completely reexpanded with positive pressure ventilation. An appropriate sized thoracostomy tube was placed at the conclusion of each case and directed posteriorly and superiorly for better drainage.
FIG. 1. The University of Chicago Empyema Classification System\.
Results
Forty-two patients with empyema thoracis were treated with VATD at our institution between July 2001 and July 2005. The mean age was 5.9 years (range, 4 months to 19 years), there were 21 males and 21 females (sex ratio 1:1). All patients received a course of intravenous antibiotics before VATD (average, 7.5 days; range 1-36 days). Mean number of preoperative days was 4.37 (range, 1 day to 14 days).
VATD was successfully completed in all 42 patients with no mortality. 35/42 (82%) had
TABLE 1. Localization of Pneumonia, Causing Empyema
18 (43%) patients had intraoperative pleural fluid cultures that showed growth. All of these patients had received intravenous antibiotics for at least 24 hours prior to surgery. Table 2 shows the identified bacterial species in patients’ pleural fluid cultures. Of the 14 patients with necrotizing pneumonia, 8 (57%) had positive intraoperative cultures. The average time to defervescence (
There were no returns to the operating room or deaths. All patients were afebrile before discharge. Follow-up data was available for all children with a mean of 171.8 days (range 28-281 days). Symptoms had resolved in all the children. Chest radiography also showed marked resolution of previous radiographic abnormalities. In those patients diagnosed with necrotizing pneumonia, all 14 children were found to have evidence of lung parenchymal preservation with improved aeration on follow-up CT scan and/or chest x-rays. There were no recurrences and no hospitalizations of discharged patients.
As mentioned above, a persistent air leak after removal of the initial thoracostomy tube developed in a 13-month old MRSA positive male with necrotizing pneumonia. A diagnosis of bronchopleural fistula was entertained with clinical resolution at 16 days after placement of a second thoracostomy tube.
Discussion
A variety of recent reports have documented the success of VATD in the treatment of children with empyema, resulting in shorter hospital stays, decreased overall number of procedures, shorter period of chest tube drainage, greater postoperative comfort, and smaller scars when compared with other treatment modalities.17-19 Additionally, decreased costs also have been documented. Although surgery may carry a higher initial cost, these patients have fewer procedures overall and tend to experience shorter periods of hospitalization, resulting in lower costs overall.20 On the basis of these results, many pediatric surgeons have come to consider VATD a more effective and efficient approach for the treatment of children with empyema.
TABLE 2. Microorganism Profile in Patients with a Positive Intraoperative Pleural Fluid Culture
TABLE 3. Summary of Data Based on Intra-operative Culture Findings and Presence or Absence of Necrotizing Pneumonia
TABLE 4. Summary of Data Using the University of Chicago Empyema Classification System
In children presenting with empyema today, it is becoming evident that not all empyemas can be treated as equal. Pneumonia seems to be showing new epidemiology. Increased incidence, newly aggressive organisms with multidrug resistance, and more severe morbidity with necrotizing forms have been reported.3,4,21 The purpose of this study was to document our institution’s experience with VATD since 2001 in complicated empyemas, i.e., the presence of necrotizing pneumonia, a not uncommon sequelae of multiresistant organism- related pneumonias, particularly MRSA.
In our tertiary care hospital, most of the children presented with symptoms for more than one week. The effusion amounts were usually moderate to massive with many pneumonias complicated by multidrug resistant organisms and/or necrotizing pneumonia. The prevalence of these advanced pneumonias led us to adopt the classification system for empyemas that is presented in this article. It was our belief that such a classification system, used in conjunction with the established staging system, would allow us to better tailor treatment regimens for patients with a wide spectrum of empyema.
In most studies performed before the early 1980s, the pathogens isolated most commonly in children with empyema were S. pneumonia, S. aureus, Haemophilus influenzae, or organism of unknown etiology. In more recent studies, the species isolated most commonly are S. pneumoniae, β-hemolytic streptococci, and especially in the last 5 years, Staphylococcus aureus. S. aureus, one of the most common pathogens found in our intraoperative pleural fluid cultures, is known to be associated with high rates of complicated pneumonia that result in effusions, empyema, pneumatoceles, and abscesses.22 At present, the rates of community-acquired MRSA are rising,23 which poses new challenges to successful treatment. In our study, 71.4% of our 5. aureus pleural fluid isolates were MRSA. This further supports our observation of the disturbing pattern of multidrug resistant organisms associated with pneumonias seen at our institution.
Our data indicate that VATD can be used safely in the full range of empyemas as characterized by our classification system. We have demonstrated the efficacy of VATD for use in the least severe cases, described by class 1, to the most severe cases of combined necrotizing pneumonia and persistence of live bacterial pleural infection, as described by class 4. The results show that class 4 patients do have an overall longer hospitalization post surgery, most likely due to the time necessitated to successfully eradicate multi-drug resistant infections. However, there was found to be no difference between any of the groups for time to chest tube removal/ surgical discharge, which are considered by the authors to be more critical endpoints in evaluating the utility of treatment. One could propose based on this data that earlier use of VATD in the most complicated empyema, i.e., class 4 (positive intraoperative cultures in spite of a course of intense preoperative antibiotics; presence of necrotizing pneumonia) is indicated and might even be encouraged to promote earlier resolution of disease and shorter hospitalization. Moreover, of the patients with necrotizing pneumonia, all 14 children demonstrated evidence of lung parenchymal preservation with improved aeration on follow-up radiographic study (chest X-ray or CT scan).
It should be noted that this study did not aim to compare conservative management (i.e., antibiotics thoracentesis/chest tube) with antibiotics plus surgical intervention. Moreover, we did not have access to data allowing us to determine retrospectively the effect of prehospitalization antibiotics; this is considered irrelevant because premedication would possibly predispose to the development of more virulent, resistant bacterial species, creating a more severe (positive culture) course of the disease, for which the use of VATD is indicated anyway.
It is the authors’ belief that the use of VATD is clearly indicated for instances of complicated empyema, especially in today’s hostile environment where multidrug resistant organisms, such as MRSA, are wreaking havoc with worsening sequelae. Moreover, we are encouraged to support the notion that VATD is useful as an early and efficacious intervention in the myriad of clinical presentations of empyema.
REFERENCES
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13. Rodriguez JA, Hill CB, Loe WA Jr, et al. Video-assisted thoracoscopic surgery for children with stage II empyema. Am Surg 2000:66:569-72.
14. Miller JI. Empyema thoracis. Ann Thorac Surg 1990;50: 343-4.
15. Alexiou C, Goyal A, Firmin RK, Hickey MS. Is open thoracotomy still a good treatment option for the management of empyema in children? Ann Thorac Surg 2003:76:1854-8.
16. American Thoracic Society. Management of nontuberculous empyema. Am Rev Respir Dis 1962:85:935-93.
17. Avansino JR, Goldman B, Sawin RS, Flum DR. Primary operative versus nonoperative therapy for pediatric empyema: A meta-analysis. Pediatrics 2005;115:1652-9.
18. Liu HP, Hsieh MJ, Lu HI, et al. Thoracoscopic-assisted management of postpneumonic empyema in children refractory to medical response. Surg Endosc 2002; 16:1612-4.
19. Chang YT, Dai ZK, Kao EL, et al. Thoracoscopic decortication: First-line therapy for pediatric empyema. Eur Surg Res 2005;37:18- 21.
20. Meier AH, Smith B, Raghavan A, et al. Rational treatment of empyema in children. Arch Surg 2000;135:907-12.
21. Whitney CG, Parley MM, Hadler J, et al. Increasing prevalence of multidrug-resistant Streptococcus pneumonias in the United States. N Engl J Med 2000:343:1917-24.
22. Heffner JE. Pneumonia: Infection in the pleural space. Clin Chest Med 1999;20:607-22.
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Presented at the Annual Scientific Meeting and Postgraduate Course Program, Southeastern Surgical Congress, Lake Buena Vista, FL, February 18-21, 2006.
Address correspondence and reprint requests to Donald C. Liu, M.D., Ph.D, University of Chicago Comer Children’s Hospital, 5841 South Maryland Avenue, MC 4057, Chicago, IL 60637.
DISCUSSION
RICHARD R. RICKETTS, M.D. (Atlanta, GA): The authors present a retrospective review of 42 children (average age, 5.9 years) treated during a 4-year period with early thoracoscopic decortication for empyema complicating advanced pneumonia. Of their 42 patients, 43 per cent had negative cultures and no necrotizing pneumonia (Group I), 24 per cent had positive cultures and no necrotizing pneumonia (Group II), 14 per cent had negative cultures with necrotizing pneumonia (Group III), and 19 per cent had positive cultures with necrotizing pneumonia (Group IV). Overall, one-third of their patients had necrotizing pneumonia. All patients underwent successful thoracoscopic decortication with no mortality, minimal morbidity, no conversions to open thoracotomy, and no secondary thoracotomies on follow-up CT scans. The only difference between the four groups was an increased length of stay between Groups I and IV.
Forty-three per cent of the patients overall, and 57 per cent of the patients with necrotizing pneumonia, had positive cultures. The most common organism was Staphylococcus aureus, and of these, 71 per cent were MRSA. The average time to defervescence was 3.1 days and the average time for removal of the chest tube after the VATD was 4.1 days. The average time to discharge after the VATD was 8 days.
Based on the results from this study and from a review of the current literature, the authors conclude that early VATD is “the new standard of care for advanced pneumonia with empyema.” Actually, this quote is from their title; in the article, the authors state that they “support the notion that VATD is useful as an early and efficacious intervention” in the treatment of empyema.
This incidence of postpneumonic empyema is on the rise. The authors report on 42 patients treated during a recent 4-year period (2001-2006).
Although I tend to agree with the authors that this is in fact the new standard of care for this disease, this article does not supply the data to support that conclusion. As the authors state in their paper that they have not randomized the patients to VATD therapy versus other forms of treating this disease such as prolonged intravenous antibiotics, the use of repeated thoracentesies, chest tube drainage with antibiotics, mini- thoracotomy, the use of fibrinolytics, or even open thoracotomy.
I have several questions for the authors. In very young and/or small patients, do you do your procedure strictly through the port sites, or do you enlarge one of the port sites into a “mini- thoracotomy” (as I do) to insert instruments to remove the fibropurulent peel? Do you use single lung ventilation in any of your patients, such as in older children, in which a double lumen tube is available and in younger patients, in which mainstem intubation can be accomplished? We tend to do so. How much of the peel do you remove? Do you try to get it all out or are you satisfied when the lungs can be fully inflated with positive pressure ventilation? Do you ever use fibrinolytics in the preoperative or postoperative period? If so, which one do you use and at what dose? Do you send your patients home on intravenous antibiotics through a PICC line? We do. If you do, which antibiotics do you use? Why have you developed your classification system when all patients are treated the same anyway?
DONALD C. LIU, M.D. (Chicago, IL): We examined this problem in adults and presented our findings last year and we concur with the authors’ conclusions.
A.H. ZUREIKAT, M.D. (Chicago, IL; Closing Discussion): Regarding your first question on the methodology of port sites, no we do not actually enlarge any of our port sites, regardless of the age group of the patient. We just use the initial port site insertion without any further enlargement. We do use single lumen endotracheal intubation for all of our patients.
We evacuate as much peel as possible that would enable us to fully see the lung re-expand on positive pressure ventilation after the operation is performed. If a peel is present and does not really influence the re-expansion of the lung, we will leave it.
The literature has shown some degree of success with fibrinolytics. However, there are failures that are associated with fibrinolytics. From our experience, we tend not to use fibrinolytics. The use of fibrinolytics causes the pleural cavity to be much more adherent, and the rate of future secondary mini- thoracotomies or full thoracotomies after fibrinolytics has been reported in the literature. We have found that to be very true. The lung and the pleural cavity are much more adherent after the use of fibrinolytics.
We agree with your institution’s regimen on intravenous antibiotics and PICC lines. One of the main reasons, as we have noted, that Class 4 patients have had a prolonged hospital stay is for the prolonged administration of antibiotics and for PICC line insertions. We do routinely, if patients still have evidence of infection, send patients home on IV antibiotics with the placement of a PICC line.
In terms of our classification system, we attempted early on to try to differentiate those patients who had mild disease from patients who had severe disease. This classification system was actually worked up before we commenced the study. The validity of this classification system in that if we can identify patients who are in Class 4 (that is patients who have positive cultures with positive necrotizing pneumonia as per CT scan preoperatively) is that if the CT scan enables us to diagnose these Class 4 patients preoperatively, we can readily tell our pediatrician or medical practitioner colleagues to actually send these patients over for earlier video-assisted thoracoscopic surgery (VATS) to prevent prolonged hospitalization and to institute early aggressive successful treatment for these patients.
DONALD C. LIU, M.D. (Chicago, IL; Closing Discussion): I just wanted to clarify two points. We do use single tubes ventilation and put air in the chest that acts just as well as a double luminal intubation.
As far as the port sites, to enlarge them, we use a grasper and sponge stick.
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