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Eur J Cardiothorac Surg 2007;32:422-430. doi:10.1016/j.ejcts.2007.05.028
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

Reviews

Current surgical treatment of thoracic empyema in adults

Thomas F. Molnar*

Department of Surgery, Medical School, University of Pécs, Pécs, Hungary

Received 19 March 2007; received in revised form 24 May 2007; accepted 31 May 2007.

* Corresponding author. Address: H-7633 Pécs, Ifjúság u 13, Hungary. Tel.: +36 30 6403362; fax: +36 72 536 496. (Email: mft{at}iseb.pote.hu).


   Abstract
Top
 Abstract
1. Introduction
 2. Basics
 3. Array of methods
 4. Discussion
 5. Conclusion
 References
 
A review of the recent literature on treatment modalities of adult thoracic empyema was conducted in order to expose the controversies and verify where consensus exists. Critical reading filtered through clinical experience was the method followed. The roles of surgical drainage, lavage techniques, debridement via VATS, decortication, thoracoplasty and open window thoracostomy were considered using the Oxford Center of Evidence Based Medicine criteria. The roles of the different therapeutical modalities were interpreted in the light of the triphasic nature of empyema thoracis. The randomised controlled trials came up with conflicting results. With two exceptions all of the papers reviewed provide level (2b) or below evidences. The lack of a single ideal treatment modality or policy reflects the complexity of the diagnosis and staging of this heterogeneous disease. Basic elements of intervention – drainage, different evacuation techniques, decortication, thoracoplasty and open window thoracostomy – are well-established technical modalities; however, neither a universally acceptable primary modality nor the gold standard of their sequence is available. Drainage remains to be the initial treatment modality in Phase I disease. Debridement via VATS is a safe, reliable and efficient method in the fibrinopurulent phase. Organised pleural callus requires formal decortication. Open window thoracostomy is a simple and safe procedure for high-risk patients and results in quick detoxication. Thoracoplasty kept its final role in pleural space management. Acute postoperative bronchial stump insufficiency requires immediate surgery. Evacuation of toxic material is mandatory. No single-stage procedure offers a solution. An optimised agressivity treatment modality should be tailored to the condition of the patient and to the potential of the persisting cavity. Decision-making involves a triad consisting of the aetiology of empyema (i.e. primary vs secondary), general condition of the patient and stage of disease, while considering the triphasic nature of development of thoracic empyema. The current attitudes show that the present concepts are based mainly on expert opinion. Flexibility and patience on behalf of the surgeon and nursing staff, the patient and the hospital management, as well as a good understanding of the complexity of this condition are the cornerstones of the treatment. No exclusive sequence of procedures leading to a uniformly predictable successful outcome is available. Individualised approaches can be recommended based on institutional practice and local protocols. Thoracic empyema in general seems to remain resilient to fit completely into the categories of evidence-based medical approach.

Key Words: Empyema thoracis • Percutaneous thoracostomy • Open thoracic window • Fibrinolysis • Decortication • Thoracoplasty • Video-assisted surgery • Surgical decision-making


   1. Introduction
Top
 Abstract
 1. Introduction
2. Basics
 3. Array of methods
 4. Discussion
 5. Conclusion
 References
 
Thoracic empyema, the inflammatory process in a preformed anatomical space defined by the visceral and parietal pleura, was one of the first recognised thoracic pathological entities that had been a therapeutic challenge. Since then it seems to resist proper evidence-based approaches so far. As a paradoxical result of increased life expectancy, improved survival of malignant diseases and extended operability criteria within and outside the scope of thoracic surgery, the pool of potential candidates for empyema thoracis is expanding. Antibiotic abuse led to increased numbers of therapy-resistant cases and the tuberculosis did not cease to be a permanent threat either. Immunocompromised conditions – either iatrogenic (transplantation and cancer therapy) or the result of drug abuse and HIV [1] – impose further risk in developing thoracic empyema. The utmost need of commonly accepted definitions, and consensus in the categories is highlighted by the fact that thoracic empyema is located on the interface between thoracic surgery and pneumonology on the one hand and trauma surgery on the other.

The protean face of the disease, diabolically masquerading its own clinical manifestation, is not helpful either. This nature of the condition is exposed by Graham's comment on the paradigm shifting work of Samson and Burford on the efficacy of decortication of thoracic empyema, adding:

‘You men who have been working in World War II have not been seeing empyema. Empyema is an abscess of the pleural cavity. It is a word that was used by Hippocrates to mean abscess ... You have been seeing infections attenuated by drugs which were not known in 1941 ... and much less known to Hippocrates ... if you had talked to Hippocrates about this as empyema, he would have said: ‘I don’t understand what you are talking about’ [2].’

Thoracic empyema might be considered too complex to discuss as a unique clinical picture. However, the common and dominating inflammatory nature of the disease, the uniform pathological changes and the shared treatment modalities (the armamentarium available) to correct them provide a rationale for treating thoracic empyema as an entity.

Attempts to obtain data using DynaMed (http://search.ebscohost.com) clinical reference tool failed to find any item for empyema thoracis clinical evidence. The Cochrane Database of Systematic Reviews [3] reveals serious limitations as far as thoracic surgical aspects are concerned. Conclusions of a previous small RCT [4] had to be revaluated by a recent report with a diagonally opposite outcome [5], which makes thoracic empyema an eminent example of the complexities Tom Treasure detailed in our speciality [6].

The method of the present systemic review applies to the categories (Table 1 ) developed by the Oxford Centre for Evidence Based Medicine (OCEBM) (http://www.cebm.net/levels_of_evidence.asp.2001) and previously used in the speciality [7].


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  		Table 1 Levels of sources of evidence according to the OCEBM
 
Medline through PubMed was used for the primary article search, limiting the time frame from 1 January 2000 to 1 October 2006, employing the following terms: empyema thoracis (n = 81), thoracic empyema (n = 764), postoperative empyema (n = 355) and postpneumonic empyema (n = 19). Using additional keywords such as intercostal catheter/drain, decortication, thoracostomy, thoracoplasty and VATS failed to present other than duplicate titles. The extraordinary healing potential of paediatric patients puts them beyond the scope of the present review as they are more responsive to more conservative treatment regimes [8]. Consequently in this article only the treatment modalities of adults (over 16 years) and the usual upper limit for admissions to a paediatric profile department are discussed.

Of the 1219 articles found when searching, 92 were considered relevant following a quick two-step (title/abstract) evaluation. The following specific predetermined exclusion criteria: non-adult patients, lack of clear definition/stage of empyema, complete outcome/complication/conversion data list, left 51 eligible papers. Unfortunately, non-English articles had to be excluded. Case reports, otherwise relevant, were not excluded. Subjectively selected papers from the pre-2000 era were also incorporated where the review required it. The selected papers were then reviewed and filtered through the clinical experience of the reviewer in the third step. The level of OCEBM evidence appears in the text in semicircular brackets where it is relevant.


   2. Basics
Top
 Abstract
 1. Introduction
 2. Basics
3. Array of methods
 4. Discussion
 5. Conclusion
 References
 
2.1 Definition
Thoracic empyema is a dynamic process, inflammatory in origin and taking place within a preformed space bordered by both the visceral and parietal pleura. It is a complex clinical entity, neither a sole clinical, laboratory, nor a radiological diagnosis. A significant lack of detectable causative organisms (frank sterile pus) reported between 47% and 56% [9–11] complicates further definition. In this paper, the entities are discussed according to Light's classification of the parapneumonic effusions from 4 to 7 (i.e. simple complicated to complex empyema) [12].

The following criteria [13] were accepted for the diagnosis of thoracic empyema, irrespective of their origin:

1. Frank pus at tapping or organisms demonstrated on Gram stain (direct) or culture (indirect), or all of the tests positive for:
2. pH below 7.2, glucose level of fluid less than 400 mg/l, LDH above 1000 IU/ml, protein level above 3 g/ml and WBC over 15 000 cells/mm3.
3. Physical, radiological and laboratory signs accompanied the relevant clinical picture.

Imaging techniques like chest X-ray, fluoroscopy, chest ultrasound and CT have their own role, but the basic methods of anamnesis, physical examination and (guided) tapping and analysis of the specimen are of eminent importance [13,14].

2.2 Origin and taxonomy
The most common form of empyema thoracis is post- or parapneumonic, representing 40–60% [15,16] of all cases. From 5% to 20% all post- or parapneumonic effusions become thoracic empyema [9,17]. Thirty percent or less of all the adult cases originate in thoracic surgical procedures (lung, oesophageal, mediastinal or other intrathoracic procedures) [18]. About 1.6–4.2% of thoracic trauma develops empyema thoracis [19,20]. Other sources like non-operative oesophageal, subdiaphragmatic and infected malignant pleural effusions are occasionally mentioned [21].

Taxonomy of thoracic empyema (Table 2 ) offers the didactic advantage of exposing the relations among origin, stage and therapeutical options. Decision-making rests upon these three pillars. The question is, how and to what extent should the individual elements be weighted in the particular case. An empyema was designated primary (PTE) if there were no previous surgical interventions involving the chest or no data of other mechanic insult (trauma). Pneumonia-related (post- or parapneumonic effusion) complicated effusion and fibrinopurulent-stage empyema are the most frequent forms. Tuberculotic (specific) empyema, infected malignant pleural effusion and empyema of unknown origin or idiopathic are less frequent [4,5,8–11,15,17].


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  		Table 2 Classification of thoracic empyema
 
A thoracic empyema is secondary (STE) if it follows a chest trauma. Most frequently it is a surgical trauma, in the majority of the cases a lung resection [18]. Penetrating or blunt chest trauma (direct contamination or superinfection of a retained clot) is another cause of secondary thoracic empyema [19,20]. The distinction between primary and secondary thoracic empyema may sound artificial and yet the tag reflects the basic difference in their optimal approaches.

2.3 Pathology
The complete unintervened process of development of thoracic empyema takes about 5–6 weeks, if a full-blown sepsis does not kill the patient earlier, but the length of the individual stages is not clearly defined (Fig. 1 ). While the date of the diagnosis is usually well documented, the origin of the whole process, especially in primary thoracic empyema, too frequently disappears in the haziness of the personal anamnesis.


Figure 1
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  		Fig. 1. Time-scale and overlapping of stages of thoracic empyema. The ‘fog’ function of an uncertain prehistory is intended as a fine adjusting element helping to approach the theoretical origin of clinical events.

 
The triphasic nature of the disease is well established [21–23]. In Stage I (exudative phase) the visceral pleura remains elastic and dimensions of the thoracic cavity are maintained. Stage II (transitional or fibrinopurulent) is typified by turbid and infected fluid, which becomes thick and purulent. The fibrin deposits construct bridges which septate the effusions creating multiple loculations. In Stage III (organising or consolidative phase) this is replaced by formal granulation tissue [24]. A sheet of inflammatory tissue would gradually compress the underlying tissue, causing contraction of the affected hemithorax. Finally, the mediastinum is shifted ipsilaterally, the diaphragm is elevated and the spaces between the ribs are narrowed.


   3. Array of methods
Top
 Abstract
 1. Introduction
 2. Basics
 3. Array of methods
4. Discussion
 5. Conclusion
 References
 
The primary therapeutic aim: ‘ubi pus evacua’ – if you find pus remove it – has not changed since the age of Celsus. Only in a short period of hope, at the advent of penicillin and its derivates, the thought flared up of the needlessness of surgical methods. This mirage reappears again and again. The aim of the surgical therapy is local infection control if possible, but without elimination of the pleural dead space with impending colonisation it is hardly achievable. The combinations and sequence of surgical methods listed in Table 3 are summarised in the ‘empyema diamond’ diagram (Fig. 2 ).


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  		Table 3 Array of treatment modalities coping with empyema thoracis
 

Figure 2
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  		Fig. 2. Treatment modalities according to the therapeutic pathways: the empyema diamond (Source: Molnar TF, Benkö I: Management of primary empyema thoracis. 4th European Conference on General Thoracic Surgery, Cordoba, Spain, 1996, Abstract Book 059).

 
3.1 Tube/closed thoracostomy/intercostal catheter (ICC)/intercostal drain (ICD)
Thoracocentesis (tapping) with a large bore needle [9] is for diagnosis and (3b) or below evidences support its usefulness in early empyema cases [9,10,25]. Drainage performed as a single procedure is usually a first-line intervention with a success rate for PTE between 67% and 74% [26–28]. Common sense dictates that the more Stage I cases included in a series, the better the success rate. Series focusing on subsequent surgeries report a 36–65% failure rate of simple tube drainage [9,17]. The lower efficacy of the method in trauma-related empyema thoracis reflects the high proportion of Stage III cases and low-risk younger patients [19]. The mortality of thoracic empyema treated by drainage ranges is at 11–24% [3,9,10,28,29].

Improving the efficacy of the drainage by irrigation is a well-established technique [30], either by cyclic (alternative or tidal) or continuous (two or more tubes, suction–irrigation systems) irrigation [31,32]. Only anecdotal reports exist with regard to the solution. Saline is the more widely used substance to dilute the causative organisms and to evacuate the debris by washing out. Iodine and derivates are extensively used on the continent but not approved in this application in the British National Formulary [33]. Strictly speaking, the practice is based on historical observations like the Carrell-Dakin method [30] and personal conviction. Efficacy of local antibacterial treatment lacks firm evidence, but again there are no reliable arguments against those positive anecdotal observations based on plausible assumptions. It is agreed that a positive culture and antibiogram are the sine qua non of this sort of therapy [34].

Personal experiences, conventions, training, schooling, conviction and accessibility of technicalities, manpower (nursing) are the variables of the details of this technique. In this rich field of individual approaches with firm convictions, controlled data are scarce. It is obvious that the more sophisticated an empyema treating system is, the higher the chance for a successful outcome. It may be related to the amount of devotion to the patient and the system rather than the real difference in efficacy of the methods.

Site of drainage (dependent point) and number and size of drains are empiric. Where numbers are available, Ch28 seems to be the accepted lower gauge, but Ch32 or over is not uncommon either. Neither question of pain control nor of physiotherapy as factors influencing the quality of life and outcome was raised specifically in any of the referred material [25–34]. The force and the type of the suction, the tube setting and specification of systems used are among the unexplored details. According to (2b) level evidences [20] drainage is usually a first-line therapeutic modality. On rare occasions permanent tube thoracostomy can provide a final solution when others failed [35].

3.2 Fibrinolysis, enzymatic/chemical decortication
Breaking the septa of the empyema cavity and degrading the devitalised, necrotic mass covering the inner surface by intrapleural instillation of streptokinase in order to make it accessible for drainage was initially described by Tillet et al. in 1951 [36].

Contrary to previous convincing reports [4] recent (1a) level evidence did not find enzymatic decortication [5] superior to tube thoracostomy treatment. On the other hand at (2a) level the success rate with ICC alone versus ICC and streptokinase were 67.1% versus 87.7%. Multiple regression analysis has proven fibrinolysis as a sole independent factor for better outcome [37]. Where Stage III empyema cases were excluded, similar results were reported [9]. All of the above listed procedures share the advantage of local anaesthesia. They are considered to be minor surgeries, despite presenting the maximum of agressivity the individual patient can cope with in a non-negligible portion of the cohorts.

3.3 Video-assisted empyema surgery (debridement/evacuation)
In this group of procedures misnomers flourish. Evacuation of necrotic material from the cavity, essentially from the parietal wall, is, by definition, debridement. Decortication, a procedure known since 1885 [30,38,39] – the peeling of the organised coat of the visceral pleura – is the very essence of the operation. Papers heralding VATS decortication [40,41] uniformly fail to demonstrate in their Methods section that a standard Fowler-Delorme procedure was performed. This manoeuvre is a technically demanding procedure even under direct tactile and full visual control. Therefore, it seems to be reasonable to discuss all video-assisted clearings here under the title of evacuation in which debridement [42] is the core of the procedure, irrespective of their own usage of terminology. Pathoanatomy offers the evidence, as there is no distinctive and, therefore, removable cortex prior to at least the first 4 weeks [24,40].

From the mid-1990s, thoracoscopic evacuation of empyema sac has gained popularity [42]. Subsequent papers have supported the original observations and notes on limitations [40]. Success rate ranges from 68% to 93% (from (2b) to (3b)) [17,21,40–43], and seems to be in close correlation with the composition of the investigated patient group. The more the Stage III empyema – or in general, the longer the anamnesis – the higher the failure rate [17,44], necessitating further surgery such as decortication, open window thoracostomy and thoracoplasty, in order of frequency. The conversion rate is 5–8% [40,42], and is 10–25% of a second-stage, open decortication [40,41]. Patients with a history shorter than 4 weeks had a good chance to be cured by VATS alone [40,42] while histories over 5 weeks (presumed Stage III) tended to necessitate a decortication [17,21,42] (3b). Preselection bias interferes with the outcome rather than treatment modalities themselves.

There seems to be an undisputed superiority of VATS procedures as far as early posttraumatic cases are concerned [41,43]. Evidence (3b) suggests that following a failed tube thoracostomy a VATS evacuation is more beneficial than after an interim attempted fibrinolysis [21]. An ultrasonic device was recently published [44], which can improve the efficacy of the breakdown manoeuvres during VATS debridement.

The quality of the underlying lung is a decisive factor in outcome. Potential for ‘restitutio ad integrum’ – restoring the original parenchyma volume in order to fill the space – is the key element. Evacuation of infected posttraumatic effusion facilitates quick re-expansion of the healthy underlying lung, a significantly different situation from a lung recovering from a lobar pneumonia. Underlying diseases such as cancer and tuberculosis, either debilitating the recoil capacity of the lung tissue or destroying the barrier function of the pleural surface, leading to bronchopleural fistula like emphysema and other conditions resulting in honeycomb lung, are the main factors responsible for failure. The 30-day mortality of the patients treated by this modality is 3.4–4.2% [17,21,27,31,40].

3.4 Open surgical methods for empyema
3.4.1 Decortication
Decortication is the method of choice when the underlying lung is unable to expand (trapped lung) due to the established thick inflammatory coat and the patient is fit enough for major intervention. Decortication, a procedure originally used for the treatment of tuberculotic and posttraumatic-trapped lung [2,30], relies on lung elasticity in order to fill the cavity, freeing the encased parenchyma from the compressing inflammatory coat. Where the case history is longer than 6 weeks, which is equivalent to a Stage III disease, the recommendations are concordant, if the patient is fit for surgery [10,26]. The majority of the Fowler-Delorme procedures are performed for Stage III postpneumonic empyema [21,45] or following trauma [19,26]. Stage III empyema reduces lung perfusion to 20–25% on the involved side. Decortication can double this value and improve vital capacity from 62% up to 80% and FEV1 from 50% to 69%. In spite of improvement in values, the function of the affected lung remains impaired [46]. The remaining ventilation/perfusion mismatch is due to multilevel functional lung damage [47]. In patients with a longstanding posttuberculotic collapsed lung with minimal perfusion, decortication can be attempted but the outcome is unpredictable [48]. As far as the patient is symptomatic, the benefit of the procedure is proven (2b) [45–49]. However, decortication is not indicated and observation is warranted for asymptomatic patients [50].

Patients undergoing VATS for empyema are likely to be converted to open procedure (i.e. decortication) in 3.8–40% depending on the delay in decision even as early as in Stage II [17,51]. There is a recent shift to muscle-sparing (axillary) thoracotomy, narrowing the agressivity gap between VATS and open surgery. Bronchopleural, pleurocutaneous fistula might necessitate additional parenchyma sparing lung resection in up to 10.1% of the cases [21].

With respect to the aetiology, up to 80% of posttraumatic empyema requires formal decortication [19,41]. Reoperation rate after failed decortication is half of that following VATS procedure. The mortality of decortication is 1.3–6.6% [26,29,50].

3.4.2 Thoracoplasty
Collapse therapy – remodelling the osteomuscular wall of the thoracic cage in order to control the underlying inflammatory process – was among the first effective thoracic surgical procedures [52]. In modern times, the aim of the procedure is space filling: either by diminishing the distance between the lung parenchyma by collapsing the roof of the chest and/or filling the space with viable tissue (omentum, muscle transposition). This procedure can be performed alone or in combination with other modalities, like re-do stump closure. In spite of modern prosthesis technology, no recent reports [53] are available on contemporary usage of non-biological plombage. Proper surgical technique and planning are needed to avoid deformities like scoliosis and other related consequences [54]. Unresponsive cases to less aggressive multiple treatments may obviate the need for thoracoplasty [52,55]. Thoracoplasty with or without myoplasty is a viable consolidating step in sequential empyema surgery. Previous procedures include fenestration in 17–72% to sterilise the cavity [56–58]. Postpneumonectomy traction diverticulum caused oesophagopleural fistula was treated by fenestration followed by thoracoplasty [56]. Thoracomyoplasty was successfully applied in simultaneous bronchopleural and oesophagopleural fistulas after pneumonectomy [59]. The usual problem of the plombage, the too small volume of filling material, can be solved by plastic surgical methods [60,61]. Combination of thoracoplasty and omental pedicled flap for chronic empyema due to bronchopleural fistula (BPF) can achieve an 82.6% success [57] (3b). In selected cases it is a first-line procedure rather than being a last resort when every previous attempts failed [52] (3b). The 11% failure rate includes those who will carry on with permanent thoracostomy [55]. The overall mortality in these low case number series is about 4.3–5% [55,57,62].

3.4.3 Open window thoracostomy (OWT)/fenestration/empyema marsupialisation
For debilitated patients with thoracic empyema, thoracoplasty is not a viable alternative and as tube thoracostomy with or without VATS debridement would fail to control the disease, open window thoracostomy should be offered [12]. Marsupialisation of the cavity via rib(s) resection and open drainage is a well-established [62,63] method of low risk. Consequences concerning quality of life in patients with OWT remain unexplored so far. It is the choice of treatment if there is a permanent supply of causative organisms due to bronchopleural fistula (BPF). It can be applied either as a definite treatment with intent to cure, a preliminary procedure prior to definite treatment [58,64] or as a last resort procedure when others have failed to achieve a relatively stable disease [35,65]. Muscle transposition is proposed as the space becomes sterile-cleansed [61,66]. Recurrent cancer, poor function and persisting local infections are common causes of open window failure [67].

In contemporary thoracic surgical practice the postoperative empyema, usually with BPF, is the main indication [13,34] of the procedure, and is relatively rare (even as low as 3%) in postpneumonic, primary thoracic empyema cases [21,17]. This is an externalisation via unroofing the empyema cavity at the dependent point. The originally intended valve mechanism of the Eloesser flap, introduced in 1935 [63], went through several modifications, reaching the present form, where the inverted flap attached to the floor of the cavity gets daily packings [68].

Altogether, 2–10% of pneumonectomies [35,68] are followed by development of a bronchopleural fistula. Postpneumonectomy thoracic empyema is a result of bronchopleural fistula in 80–100% of the cases [56,69,70], with a mortality ranging between 5% and 25% on average [66] with up to 40% if pleuropneumonectomy is performed [71] with a maximum value of 75% [35].

The (3b) level evidences are uniform in differentiating and decision-making according to the acuteness of the clinical picture. Half of the BPFs develop within 4 weeks following surgery [69]. Right- sided BPF develops in 75–100% [64,66,67,70,72] of the cases. The closer the onset of the stump insufficiency is to the time of surgery, the worst the prognosis [64,70]. Immediate postoperative bronchopleural fistula (within 1 week), resulting in acute empyema thoracis, usually presents as a fulminant Stage II disease. This dramatic clinical picture of impending sepsis necessitates a prompt decision. Removal of toxic material and control of supply line of the infected agents are the aims to be achieved by the surgical interventions.

Clagett's procedure [69,70,72,73] is the best-evidenced (3b) method for historical reasons. The complex procedure consists of open pleural drainage, serial operative debridement and eventual chest closure after filling the pleural cavity with antibiotic solution [70]. Window making, fenestration, is part two of the procedure [34]. Daily irrigation with antibiotics [69] or regular open packings complete the procedures. Observational studies prove that timing of initiation of therapy is crucial. When reoperation was within 12 h even 100% success rate was reported. Realistically, a one-in-four mortality [64] can be expected. The temptation to not use thoracostomy was proven to be a risk factor [64]. Early thoracostomy allows time for improvement of nutritional status increasing the chances of a successful operative closure. Muscle flap coverage of the stump or filling the resulted space is performed in 87% of the cases [70], leading up to a complete healing in 75–81% of the cases [58,68,70].

As an alternative to the staged and time-consuming Clagett procedures, Weder applies the repetitive thoracotomy and debridement policy [74]. Stuffing the cleansed cavity with antiseptic packages and changing them regularly are the essence of the method. This standardised concept of repeated debridement is applied equally to early and late postoperative empyema in a sequential, pre-planned standardised way [75]. The premeditative repetitive pattern has previously proven its value in non-thoracic suppurative-necrotic processes like pancreatitis. This technique seems to be applicable not only to treat but also to prevent empyema in high-risk procedures like completion pneumonectomy for infective diseases [76].

Solution of chronic or late postoperative empyema also consists of drainage, debridement, closure of BPF when present and space obliteration [76,77]. Onset of BPF later than 15 weeks is an independent predictor of a positive outcome [70]. BPF smaller than 3 mm may respond to thoracoscopic debridement alone or in combination with open window thoracostomy [76]. Operative closure of the bronchial stump can be performed via the previous thoracotomy or transsternally using a transpericardial approach [64,77]. Re-amputation of the stump or, on rare occasions, carinal resection is anecdotally reported. Remodelling the osteomuscular chest wall and/or facilitation of granulation, further on external tissue plombage, are the methods of space management as were discussed above. Chronic fistulas frequently require two or more procedures [58,66,67]. Decision-making can hardly be overselective. On the lower end of surgical agressivity with regard to BPF treatment, local filling of the hole is reported in cases of limited dehiscences measuring maximum 3–5 mm. These limited case series consist of manoeuvres relying on local tissue healing potentials with time-gain for scar formation. Transbronchial methods include glueing [78] or chemical cauterisation [79]. The logical solution of expandable covered metallic stents [80,81] is anecdotally reported. Unfortunately, no recent evidence is available with Mill's positive–negative pressure balance bottle-system [82].


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Basics
 3. Array of methods
 4. Discussion
5. Conclusion
 References
 
In the present review [83] of the observed outcomes following different treatment modalities, patient selection, cohort size, methods of randomisation and so on were not scrutinised in the study, which definitely weaken the power of the conclusions. Generally, the information available from the publications does not allow a clear differentiation in how much of the treatment effect is due to actual treatment differences and how much is due to the assignment of the patients to selective treatment modalities.

The very few controlled trials on this topic came up with conflicting results [4,5]. The relative lack of RCTs, reports considered as basics for clinical standard, does not mean that the mass clinical experience collected on this topic [1,5,9–82] would not be able to serve as a proper guideline. The reports reviewed, providing usually level (3b) or below evidences, still fit into a harmonious picture. The lack of a single ideal treatment modality or policy reflects the complexity of the diagnosis and staging of this heterogeneous disease. Decision-making protocols cannot function without clear and unmistakable categories. Basic elements of intervention – drainage, different evacuation techniques, decortication, thoracoplasty, open window thoracostomy – are well-established technical modalities; however, neither a universal primary modality nor the gold standard of their sequence is available.

The optimally aggressive treatment modality should be tailored to the condition of patients and to the healing potential of the persisting cavity. Decision-making relies on the triad of the aetiology of empyema (PTE vs STE), general condition of the patient and actual stage of disease, considering the triphasic nature of it. The basic differences in the behaviour of ‘naturally’ developing empyema cavity (i.e. postpneumonic) and of those infected spaces that have followed the removal of lung parenchyma dictate the choice of procedure (Fig. 3 ). Existence or lack of dead space within the pleural cavity is the definite distinction and decisive factor influencing outcomes following different therapeutical attempts. No effective infection control can be expected in the presence of an active cavity. The law of Nature – horror vacui – rules on these fields, too.


Figure 3
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  		Fig. 3. Connection between the stages of thoracic empyema and the best-evidenced methods of choice. The theoretical time-scale is not necessarily identical to the documented duration of the disease of the individual patient. The graphical representation is not intended to be considered as an absolute and exclusive scheme.

 
There are two main sources of the bias limiting the daily routine applicability of the (3b) reports. Preselection of patients into different modality groups a priori influences outcomes: the results are mirroring the attitude of the surgeon/team rather than the distance of the investigated method from the ideal treatment. In postpneumonic empyema, the surgeon's problem starts with the timing and circumstances of referral: called to see the empyema patient only when other (i.e. conservative) methods failed; only not to mention the case, when the typical empyema patient is referred to surgical care on a Friday afternoon, preferably on a long weekend. The highly selected cohort of patients with unreliable information on the origin of the process explains the uncertainties around the value of the individual procedures on the surgical pathway. In the average paper, a hierarchy of methods is evaluated – and with rare exceptions, the actually presented method is ‘proven’ to be the best.

The problem with postresectional thoracic empyema patients is similar. The higher the risk they have prior to the original operation, the higher their failure rates for less aggressive modalities when thoracic empyema develops. The fragility of these patients means that rather than operability, resectability is their burden.

Drainage remains to be the initial treatment modality in Stage I disease. The weight of additional elements in success/failure such as suction tactics, physiotherapy and nutritional status needs further clarification. There is no territory in our topic, where the ‘devil in the details’ rule would be stronger. The number of drains, their size, location, details of management and caring at multilevel, i.e. doctoral, nursing and physiotherapeutic, and of timing, frequency and duration of the exact manoeuvres are neglected aspects of studies. Debridement via VATS is a safe, reliable and efficient method in Stage II cases. VATS is not limited exclusively to Stage II disease. Video techniques have a role in Stage III thoracic empyema, too, as far as evacuation is concerned.

Organised pleural callus or cortex (Stage III) requires open surgery: formal decortication. A persisting cavity is a challenge without a single and uniform solution (Fig. 4 ). Open window thoracostomy, either through limited thoracotomy or VATS, represents a simpler and, therefore, safer procedure than thoracoplasty.


Figure 4
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  		Fig. 4. Approaches of the persisting space problem: (1) internal closure of BPF (endoscopic methods); (2) external closure of BPF (re-amputation, coverage); (3) diminishing the remaining space by de-roofing the musculoskeletal structures (thoracoplasty); (4) space occupying by muscle/omentum transposition (plombage); (5) establishing a persistent orifice (window/tube).

 
It is a valuable procedure as an initial step in cavity management and a unique and definite one for high-risk patients, too. Thoracoplasty, the conventional collapse procedure, lost its popularity against the alternative techniques, i.e. decortication and thoracostomy, but it has its final step role in pleural space management when other methods failed. Using aggressive methods in space sterilisation and obliterative techniques (pedicled muscle or omentum plombs) with preservation of the first rib in case of destroyed lung seems to be worthwhile to consider it as a real alternative.

Acute postoperative bronchial stump insufficiency requires immediate surgery, but to what extent? Evacuation of toxic material is mandatory. Closed drainage, open window thoracostomy, repetitive thoracotomies and cavity packing are equally viable options. Stabilised patients benefit from the attempts of surgical closure of the dehiscent stump. No single-stage procedure offers solution.

Irrespective of the above detailed differences in specific features of thoracic empyema, the basic rules for treatment remain the same:

(1) complete evacuation of the content of infected space
(2) elimination of cavity
(3) control of causative organisms/sterilisation
(4) forced auxiliary treatment such as aggressive physiotherapy, nutritional support in every phase of treatment.


   5. Conclusion
Top
 Abstract
 1. Introduction
 2. Basics
 3. Array of methods
 4. Discussion
 5. Conclusion
References
 
Summarising the current divergent attitudes towards this well-known entity of a sinister natural history one can say that thoracic empyema shows that present concepts are based mainly on the somehow paternalised OCEBM categories of level (3b) and expert opinion in the family of the evidences. Attempts of applicable risk stratification have failed so far; therefore, no other option than highly individualised approaches can be recommended. The thoracic surgeon should command all the possible techniques within their limitations to adjust it to his/her individual patient [84]. Flexibility and patience on behalf of the surgeon, nursing staff and the patient furthering the endeavour of hospital management to understand the complexity of this condition are the cornerstones of the treatment. Thoracic empyema is an eminent example, that no established method can be neglected by putting our surgical heritage on the dusty shelves of a distant corner.

Thoracic empyema, a wolf in a sheepskin, does not allow recommending a clear single sequence of procedures leading to a uniformly predictable successful outcome. Institutional practice, local protocols based on past experience and individual case management with a flexibly optimised sequence of procedures may offer the best outcome.


   References
Top
 Abstract
 1. Introduction
 2. Basics
 3. Array of methods
 4. Discussion
 5. Conclusion
 References
 

  1. Mouroux J, Riquet M, Padovani B, Debesse B, Richelme H. Surgical management of thoracic manifestations in human immunodeficiency virus-positive patients: indications and results. Br J Surg 1995;82:39-43.[Medline]
  2. Samson PC, Buford TH. Total pulmonary decortications. Its evaluation and present concepts of indication and operative technique. J Thorac Surg 1947;16:153-157.
  3. Coote N, Kay E. Surgical versus non-surgical management of pleural empyema [Review]. The Cochrane Database of Systematic Reviews 2005, Issue 4 Art No: CD001956.pub2. doi:10.1002/14651858.CD001956.pub2.
  4. Wait MA, Sharma S, Hohn J, Dal-Nogare A. A randomized trial of empyema therapy. Chest 1997;111(6):1548-1551.[Medline]
  5. Maskell NA, Davies CWH, Nunn AJ, Hedley EL, Gleeson FV, Miller R, Gabe R, Rees GL, Peto TEA, Woodhead MA, Lane DJ, Darbyshire JH, Davies RJO (MIST1 Group). Controlled trial of intrapleural streptokinase for pleural infection. N Engl J Med 2005;352(9):865–74 (Erratum: N Engl J Med 2005;352(20):2146).
  6. Treasure T. The evidence on which to base practice: different tools for different times. Eur J Cardiothorac Surg 2006;30:819-824.[Free Full Text]
  7. Dunning J, Treasure T, Versteegh M, Nashef SAM. Guidelines on the prevention and management of de novo atrial fibrillation after cardiac and thoracic surgery. Eur J Cardiothorac Surg 2006;30:852-872.[Free Full Text]
  8. Spencer D. Empyema thoracis: not time to put down the knife. Arch Dis Child 2003;0:842-843.
  9. Ozol D, Oktem S, Erdinc E. Complicated parapneumonic effusion and empyema thoracis: microbiologic and therapeutic aspects. Resp Med 2006;100:286-291.[CrossRef][Medline]
  10. Anstadt MP, Guill CK, Ferguson ER, Gordon HS, Soltero ER, Beall AC, Musher DM. Surgical versus nonsurgical treatment of empyema thoracis: an outcomes analysis. Am J Med Sci 2003;326(1):9-14.[CrossRef][Medline]
  11. Lawrence DR, Ohri KS, Moxon RE, Townsend ER, Fountain SW. Thoracoscopic debridement of empyema thoracis. Ann Thorac Surg 1997;64:1448-1450.[Abstract/Free Full Text]
  12. Light RW. A new classification of parapneumonic effusions and empyema. Chest 1995;108:299-301.[Medline]
  13. Deas1auriers J, Mehran R. Handbook of perioperative care in general thoracic surgery. Mosby Philadelphia, Pennsylvania, USA: Elsevier; 2005.
  14. Orringer MB. Thoracic emypema – back to basics. Chest 1988;93:901-902.[Medline]
  15. Chapman SJ, Davies RJ. The management of pleural space infections. Respirology 2004;9:4-11.[CrossRef][Medline]
  16. De Hoyos A, Sunderasen S. Thoracic empyema. Surg Clin N Am 2002;82:643-671.[CrossRef][Medline]
  17. Luh SP, Chou MC, Wang LS, Chen JY, Tsai TP. Video-assisted thoracoscopic surgery in the treatment of complicated parapneumonic effusions or empyemas. Chest 2005;127:1427-1432.[CrossRef][Medline]
  18. Kacprzak G, Marciniak M, Addae-Boateng E, Kolodziej J, Pawelczyk K. Causes and management of postpneumonectomy empyemas: our experience. Eur J Cardiothorac Surg 2004;26:498-502.[Abstract/Free Full Text]
  19. Mandal AK, Thadepalli H, Mandal AK, Chettipalli U. Posttraumatic empyema thoracis: a 24-year experience at a major trauma center. J Trauma 1997;43:764-777.[Medline]
  20. Deneuville M. Morbidity of percutaneous tube thoracostomy in trauma patients. Eur J Cardiothorac Surg 2002;22(5):673-678.[Abstract/Free Full Text]
  21. Petrakis IE, Kogerakis NE, Drositis IE, Lasithiotakis KG, Bourous D, Chalkiadakis GE. Video-assisted thoracoscopic surgery for thoracic empyema: primarily, or after fibrinolytic therapy failure?. Am J Surg 2004;187:471-474.[CrossRef][Medline]
  22. Andrews NC, Parker EF, Shaw RR, Wilson NJ, Webb WR. Management of nontuberculous empyema: a statement of the subcommittee on surgery. Am Rev Respir Dis 1962;85:935.
  23. Editorial. Management of acute empyema. Chest 1992;102:1316–7.
  24. Mutsaers SE, Prele CM, Brody AR, Idell S. Pathogenesis of pleural fibrosis. Respirology 2004;9:428-440.[CrossRef][Medline]
  25. Storm HKR, Krasnik M, Bang K, Frimodt Moller N. Treatment of pleural empyema secondary to pneumonia: thoracocentesis regimen versus tube drainage. Thorax 1992;47:821-824.[Abstract]
  26. Thourani VH, Brady KM, Mansour KA, Miller JI, Lee RB. Evaluation of treatment modalities for thoracic empyema: a cost-effectiveness analysis. Ann Thorac Surg 1998;66:1121–27.
  27. Athanassiadi K, Gerazounis M, Kalantzi N. Treatment of post-pneumonic empyema thoracis. Thorac Cardiovasc Surg 2003;51:338-341.[CrossRef][Medline]
  28. Suchar AM, Zureikat AH, Glynn L, Statter MB, Lee J, Liu DC. Ready for the frontline: is early thoracoscopic decortication the new standard of care for advanced pneumonia with empyema?. Am Surg 2006;72(8):688-692.[Medline]
  29. Mandal AK, Thadepalli H, Mandal AK, Chetipally U. Outcome of primary emypema thoracis: therapeutic and microbiologic aspects. Ann Thorac Surg 1998;66:1782-1786.[Abstract/Free Full Text]
  30. Molnar TF, Hasse J, Jeyasingham K, Rendeki S. Changing dogmas: history of treatment for traumatic hemothorax, pneumothorax and empyema thoracis. Ann Thorac Surg 2004;77:372-378.[Abstract/Free Full Text]
  31. Cheng YJ, Wu HH, Chou SH, Kao EL. Video assisted thoracoscopic surgery in the treatment of chronic empyema thoracis. Surg Today 2002;32:19-25.[CrossRef][Medline]
  32. Ridely PD, Braimbridge MV. Thoracoscopic debridement and pleural irrigation in the management of empyema thoracis. Ann Thorac Surg 1991;51:461-464.[Abstract]
  33. British National Formulary. BNF49, March 2005, pp. 400 and 594. London, UK: British Medical Association; 2005.
  34. Miller JI. Postsurgical empyema. In: Shields TW, LoCicero Jr J, Ponn RB, editors. General thoracic surgery. 5th ed.. Philadelphia, PA: Lippincott Williams&Wilkins; 2000. pp. 709-716.
  35. Athanassiadi K, Kalavrouziotis K, Bellenis I. Bronchopleural fistula after pneumonectomy: a major challenge. Acta Chir Hung 1999;38(1):5-7.[Medline]
  36. Tillet SA, Sherry S, Read CT. The use of streptokinase-streptodornase in the treatment of postpneumonic empyema. J Thorac Surg 1951;21:275-297.[Medline]
  37. Misthos P, Sepsas E, Konstantnou M, Athanassiadi K, Skottis I, Lioulias A. Early use of intrapleural fibrinolytics in the management of postpneumonic empyema. A prospective study. Eur J Cardiothorac Surg 2005;28:599-603.[Abstract/Free Full Text]
  38. Delorme E. Nouveau Traitment des Empyémes chroniques. Gaz d. Hop 1894;67:94-96.
  39. Fowler GR. A case of thoracoplasty for the removal of a large cicatricial fibrous growth from the interior of the chest, the result of an old empyema. New York Med Rec 1893;44:638-839.
  40. Kim BY, Oh BS, Jang WC, Min YI, Park YK, Park YC. Video-assisted thoracoscopic decortication for management of postpneumonic pleural empyema. Am J Surg 2004;188(3):321-324.[CrossRef][Medline]
  41. O’Brien J, Cohen M, Solit R, Solit R, Lindenbaum G, Finnegan J, Vernick J. Thoracoscopic drainage and decortication as definitive treatment for empyema thoracis following penetrating chest injury. J Trauma 1994;36:536-539.[Medline]
  42. Lawrence DR, Ohri KS, Moxon RE, Townsend ER, Fountain SW. Thoracosocopic debridement of empyema thoracis. Ann Thorac Surg 1997;64:1448-1450.[Abstract/Free Full Text]
  43. Oguzkaya F, Akcali Y, Bilgin M. Videothoracoscopy versus intrapleural streptokinase for management of post-traumatic retained haemothorax: a retrospective study of 65 cases. Injury 2005;36:526-529.[CrossRef][Medline]
  44. Nakamura H, Taniguchi Y, Makihara K, Ohgi S. Ultrasonic pleural debridement of empyema. Ann Thorac Cardiovasc Surg 2001;7:62-64.[Medline]
  45. Melloni G, Carretta A, Ciriaco P, Negri G, Voci C, Augello G, Zannini P. Decortication for chronic parapneumonic empyema: results of a prospective study. World J Surg 2004;28(5):488-493.[CrossRef][Medline]
  46. Rzyman W, Skokowski J, Romanowicz G, Lass P, Dziadziuszko R. Decortication in chronic pleural empyema – effect on lung function. Eur J Cardiothorac Surg 2002;21(3):502-507.[Abstract/Free Full Text]
  47. Rzyman W, Skokowski J, Romanowicz G, Lass P, Murawski M, Taraszewska M, Dziadziuszko R. Lung function in patients operated for chronic pleural empyema. Thorac Cardiovasc Surg 2005;53:245-249.[CrossRef][Medline]
  48. Olgac G, Yilmaz MA, Ortakoylu MG, Kutlu CA. Decision making for lung resection in patients with empyema and collapsed lung due to tuberculosis. Thorac Cardiovasc Surg 2005;130:131-135[Discussion: 2005;130(6):1732].[CrossRef]
  49. Roberts JR. Minimally invasive surgery in the treatment of emphysema: intraoperative decision-making. Ann Thorac Surg 2003;76(1):225-230.[Abstract/Free Full Text]
  50. Doeskin P, Sahn SA. Trapped lung. Semin Respir Crit Care Med 2001;22(6):631-636.[CrossRef][Medline]
  51. Lardinois D, Gock M, Pezzeta E, Buchli C, Rousson V, Furrer M, Ris HB. Delayed referral and gram negative organisms increase the conversion thoracotomy rate in patients undergoing video-assisted thoracoscopic surgery for empyema. Ann Thorac Surg 2005;79(6):1851-1856.[Abstract/Free Full Text]
  52. Peppas G, Molnar TF, Jeyasingham K, Kirk A. Thoracoplasty in the context of current surgical practice. Ann Thorac Surg 1993;56:903-909.[Abstract]
  53. Tezel CS, Goldstraw P. Plombage thoracoplasty with Lucite balls. Ann Thorac Surg 2005;79:1063.[Free Full Text]
  54. Berry MF, Friedberg J. Chest wall/diaphragmatic complications – on prevention of postthoracotomy scoliosis. Thorac Surg Clin 2006;16:277-285.[CrossRef][Medline]
  55. Icard P, LeRochais JP, Rabut B, Cazaban S, Martel B, Evrard C. Andrews thoracoplasty as a treatment of post-pneumonectomy empyema: experience in 23 cases. Ann Thorac Surg 1999;68:1159-1163.[Abstract/Free Full Text]
  56. Inoue M, Nakanishi R, Osaki T, Yoshimatsu T, Yasumoto K. Esophagopleural fistula originating from diverticulum after pneumonectomy. A case report and review of the literature. J Cardiovasc Surg 1999;40:761-763.[Medline]
  57. Okumura Y, Takeda S, Asada H, Inoue M, Sawabata N, Shiono H, Maeda H. Surgical results for chronic empyema using omental pedicled flap: long-term follow-up study. Ann Thorac Surg 2005;79:1857-1861.[Abstract/Free Full Text]
  58. Regnard JF, Alifano M, Puyo P, Fares E, Magdeleinat P, Levasseur P. Open window thoracostomy followed by intrathoracic flap transposition in the treatment of empyema complicating pulmonary resection. J Thorac Cardiovasc Surg 2000;120:270-275.[Abstract/Free Full Text]
  59. Trigui W, Le Pimpec-Barthes F, Shaker W, Lang-Lazdunski L, Riquet M. Simultaneous bronchopleural and esophagopleural fistulas after pneumonectomy. Ann Thorac Surg 2002;74:923-924.[Abstract/Free Full Text]
  60. Rand RP, Maser B, Dry G, Vallieres E. Reconstruction of irradiated postpneumonectomy empyema cavity with chain-link coupled microsurgical omental and TRAM flaps. Plast Reconstr Surg 2000;105:183-186.[CrossRef][Medline]
  61. Shimuzu J, Kinishite T, Tatsuzawa Y, Kawaura Y, Ishikura N, Oda M. Intrathoracic free musculocutaneous flap after open-window thoracostomy for chronic empyema. Thorac Cardiovasc Surg 2001;49(4):237-239.[CrossRef][Medline]
  62. Deslauriers J, Jacques LF, Gregoire J. Role of Eloesser flap and thoracoplasty in the third millennium. Chest Surg Clin N Am 2002;12:605-623.[CrossRef][Medline]
  63. Eloesser L. An operation for tuberculous empyema. Surg Gynecol Obstet 1935;60:1096-1097.
  64. De la Riviere AB, Defauw JJ, Knaepen PJ, van Swieten HA, Vandershueren RC, van den Bosch JM. Transsternal closure of bronchopleural fistula after pneumonectomy. Ann Thorac Surg 1997;64:954-957.[Abstract/Free Full Text]
  65. Gossot D, Stern JB, Galetta D, Debrosse D, Girard P, Callendro R, Harper L, Grunenwald D. Thoracoscopic management of postpneumonectomy empyema. Ann Thorac Surg 2004;78(1):273-276.[Abstract/Free Full Text]
  66. Kalweit G, Feindt P, Huwer H, Volkmer I, Gams E. The pectoral muscle flaps in the treatment of bronchial stump fistula following pneumonectomy. Eur J Cardiothorac Surg 1994;8(7):358-362.[Abstract]
  67. Massera F, Robustellini M, Pona CD, Rossi G, Rizzi A, Rocco G. Predictors of successful closure of open window thoracostomy for postpneumonectomy empyema. Ann Thorac Surg 2006;82:288-292.[Abstract/Free Full Text]
  68. Thourani VH, Lancaster RT, Mansour KA, Miller JI. Twenty-six years of experience with the modified eloesser flap. Ann Thorac Surg 2003;76:401-406.[Abstract/Free Full Text]
  69. Gharagozloo F, Trachiotis G, Wolfe A, DuBree KJ, Cox CL. Pleural space irrigation and modified Clagett procedure for the treatment of early postpneumonectomy empyema. J Thorac Cardiovasc Surg 1998;116:943-948.[Abstract/Free Full Text]
  70. Zaheer S, Allen MS, Cassivi SD, Nichols Jr FC, Johnson CH, Deschamps C, Pairolero PC. Postpneumonectomy empyema: results after the Clagett procedure. Ann Thorac Surg 2006;82:279-286.[Abstract/Free Full Text]
  71. Featherstone D. Pneumonectomy for inflammatory lung disease. Eur J Cardiothorac Surg 2000;18:429-434.[Abstract/Free Full Text]
  72. Hollaus PH, Huber M, Lax F, Wurnig PN, Bohm G, Pridun NS. Closure of bronchopleural fistula after pneumonectomies with a pedicled intercostal muscle flap. Eur J Cardiothorac Surg 1999;16:181-186.[Abstract/Free Full Text]
  73. Deschamps C, Pairolero PC, Allen MS, Trastek VF. Management of postpneumonectomy empyema and bronchopleural fistula. Chest Surg Clin N Am 1996;6(3):519-527.[Medline]
  74. Schneiter D, Cassina P, Korom S, Incl I, Al-Abdullatief M, Dutly A, Kestenholz P, Weder W. Accelerated treatment for early and late postpneumonectomy empyema. Ann Thorac Surg 2001;72:1668-1672.[Abstract/Free Full Text]
  75. Opitz I, Kestenholz P, Lardinoid D, Müller M, Rousson V, Schneiter D, Stahel R, Weder W. Incidence and management of complications after neoadjuvant chemotherapy followed by extrapleural pneumonectomy for malignant pleural mesothelioma. Eur J Cardiothorac Surg 2006;29:579-584.[Abstract/Free Full Text]
  76. Schneiter D, Kestenholz P, Dutly A, Korom S, Giger U, Lardinois D, Weder W. Prevention of recurrent empyema after pneumonectomy for chronic infection. Eur J Cardiothorac Surg 2002;21:644-648.[Abstract/Free Full Text]
  77. Athanassiadi K, Vassilikos K, Misthos P, Theakos N, Kakaris S, Sepsas E, Skottis I. Late postpnemonectomy bronchopleural fistula. Thorac Cardiovasc Surg 2004;52:298-301.[CrossRef][Medline]
  78. Clemson LA, Walser E, Gill A, Lynch JE, Zwischenberger JB. Transthoracic closure of a postpneumonectomy bronchopleural fistula with coils and cyanoacrylate. Ann Thor Surg 2006;82:1924-1926.[Abstract/Free Full Text]
  79. Forrester-Wood CP. Pneumonectomy and lobectomy: results and complications and their management: with a note on endoscopic cauterization for bronchial stump fistula principles and practice of surgical stapling. In: Ravitch MM, Steichen FM, editors. Chicago, London: Year Book Medical Publishers, Inc.; 1987. p. 292–303.
  80. Jones NC, Kirk AJ, Edwards RD. Bronchopleural fistula treated with a covered wallstent. Ann Thorac Surg 2006;81:364-366.[Abstract/Free Full Text]
  81. Garcia Franco CE, Flandes Aldeyturriaga J, Zapatero Gaviria J. Ultraflex expandable metallic stent for the treatment of a bronchopleural fistula after pneumonectomy. Ann Thorac Surg 2005;79:386.[Free Full Text]
  82. Mill JI, Fleming WH, Hatcher CR. Balanced drainage of the contaminated pneumonectomy space. Ann Thorac Surg 1975;19:585-588.[Abstract]
  83. Mahid SS, Hornung CA, Minor KS, Turina M, Galandiuk S. Systematic reviews and meta-analysis for the surgeon scientist. Br J Surg 2006;93:1315-1324.[CrossRef][Medline]
  84. Rothwell PM. External validity of randomised controlled trials: ‘to whom do the results of this trial apply?’. Lancet 2005;365:82-93.[CrossRef][Medline]




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