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Eur J Cardiothorac Surg 2009;36:914-918. doi:10.1016/j.ejcts.2009.06.017
Copyright © 2009, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
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Chronic postpneumonic pleural empyema: comparative merits of thoracoscopic versus open decortication

Giuseppe Cardilloa,*, Francesco Carleoa, Luigi Carbonea, Marco Di Martinoa, Lorenzo Salvadoria, Lea Petrellab, Massimo Martellia

a Unit of Thoracic Surgery, Carlo Forlanini Hospital, Azienda Ospedaliera San Camillo-Forlanini, Rome, Italy
b Department of Studi Geoeconomici, Linguistici, Statistici, Storici per l’Analisi Regionale, La Sapienza University of Rome, Rome, Italy

Received 16 February 2009; received in revised form 23 May 2009; accepted 12 June 2009.

* Corresponding author. Address: Unit of Thoracic Surgery, Carlo Forlanini Hospital, Via Portuense 332, 00149 Rome, Italy. Tel.: +39 06 55180681; fax: +39 06 6638734. (Email: gcardillo{at}scamilloforlanini.rm.it).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 References
 
Objective: We seek to evaluate the comparative merits of thoracoscopic versus open decortication in the surgical management of patients with chronic postpneumonic pleural empyema. Methods: From January 1996 to December 2006, 308 patients (180 males, 128 females, mean age: 56.3 years, range: 17–82 years) with chronic postpneumonic pleural empyema underwent decortication after failure of conservative treatment. Results: Decortication was performed by open thoracotomy in 123 (39.9%) patients (OT) and by videothoracoscopy (VT) in 185 (60.1%). Mortality was 1.29% (4/308). Morbidity was 21.1% (65/308). At 6 months follow-up, three VT patients showed recurrent empyema and underwent re-do surgery by video-assisted-thoracoscopy (VATS) (one patient) or by thoracotomy (two patients). The videothoracoscopic approach showed statistically significant better results in terms of in-hospital postoperative (day 1 and day 7), pain (p < 0.0001), postoperative air leak (p = 0.004), operative time (p < 0.0001), hospital stay (p = 0.020) and time to return to work (p < 0.0001). The analysis of postoperative pain at 6 months follow-up showed no significant differences among the different groups. Conclusions: In the light of our experience, videothoracoscopic decortication appears to be the surgical treatment of choice for chronic postpneumonic pleural empyema even if a multicentric-randomised trial should be performed before videothoracoscopic decortication becomes the gold standard for the treatment of pleural empyema.

Abbreviations: VATS = video-assisted-thoracoscopy • CH = Charrier

Key Words: Empyema • Thoracoscopic surgery • Pleural diseases


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 References
 
Every year, approximately 1 million patients with pneumonia require hospitalisation in the United States [1]. Up to 40% of them develop an associated pleural effusion: most of such cases (around 85%) will completely resolve with antibiotic treatment and the remaining (15%, around 60 000 patients) will develop pleural empyema. According to the American Thoracic Society classification [2], pleural empyema are staged as stage I, uncomplicated exudative effusion without loculation; stage II, fibrinopurulent effusion with loculation, also called Light's complicated pleural effusion; and stage III, pleural thickening with entrapment of the underlying lung [1–5].

The appropriate management of pleural empyema remains controversial: pleural drainage is effective in stage I patients and surgery is reserved for complicated cases (stages II and III) in which organisation of the fibrinous clots into fibrotic peel could determine lung encasement.

In these cases, lung decortication is necessary. Currently, the most favoured approach for decortication is open thoracotomy, although in the past decade some series with small samples have been published in favour of the VATS approach [6–9]. In this article, we seek to evaluate the comparative results of videothoracoscopic versus open decortication in a series of 308 patients with chronic postpneumonic pleural empyema treated at our institution.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 References
 
We retrospectively analysed the clinical records of 308 patients with chronic postpneumonic pleural empyema (stages II and III) who underwent pleuropulmonary decortication through open thoracotomy or videothoracoscopy after failing of conservative treatments from January 1996 to December 2006 at the Unit of Thoracic Surgery, Carlo Forlanini Hospital, Rome.

All patients had a clinical history of pneumonia no more than 6 months before surgery. Patients with HIV were not included in this study. To confirm empyema's stage, data pertaining to all patients were reviewed according to the lasting of symptoms (from in-hospital admission to surgery), and to the following radiological features on computed tomography (CT) scan of the thorax which was performed on all patients: loculations of pleural fluid, air–fluid levels, pleural enhancement or thickening, chest deformation and mediastinic shift. Patients’ data are shown in Table 1 .


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  		Table 1 Patients data according to surgical approach.
 
A multidisciplinary team (MDT) meeting (thoracic surgeons, pneumologists, pathologists, anaesthesiologists, health-care professionals and the Review Board) in the light of the increasing use of VATS at our institution pushed thoracic surgeons in September 2000 to start thoracoscopic decortication and to progressively leave open thoracotomy decortication in October 2001. The results of such experience have been progressively presented and validated at our MDT meetings.

Patients undergoing thoracotomy (OT group) were treated from January 1996 to October 2001; patients undergoing VATS (VT group) were treated from September 2000 to December 2006. After surgery, air leak was assessed by registrars and staff surgeons according to the Macchiarini's visual scale during morning and afternoon clinical rounds [10]. All patients were followed up 1 month, 3 and 6 months after surgery with clinical interview and chest radiograph. Postoperative pain was assessed using a 10-point numeric scale questionnaire (1 being no pain at all), recorded on day 1 and day 6 after surgery, and at 6-month follow-up clinics (Table 2 ).


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  		Table 2 Postoperative outcomes.
 
Institutional Review Board approval and individual patient consent were obtained.

2.1 Surgical technique
All patients underwent general anaesthesia using double-lumen endotracheal tube for selective ventilation and were then placed in the lateral decubitus position.

2.1.1 Thoracotomy
A postero-lateral serratus anterior-sparing thoracotomy with rib spreading (but without rib resection) was performed. All fibrin septae were cut and fissures were dissected free. A complete decortication (including visceral and parietal pleura) was carried out to enable lung expansion to be obtained in all patients. At the end of the procedure, two large-bore (28 CH and 32 CH) chest tubes were placed through separate incisions.

2.1.2 VATS
The procedure was performed by means of a three-port access. Based on preoperative CT scan, suitable intercostal sites were selected for port placement. The first 1-cm port was placed in the area of pleural collection by aspiration of the fluid collection with a needle. Once a pleural space was created, the remaining two ports (1 cm each) were placed under thoracoscopic vision to avoid injury to underlying lung parenchyma. No utility incision was performed. No Weitlaner retractor was used. Fluid, loculations and septa were removed under endoscopic vision by use of the sucker, a ring clamp and endoscopic forceps. Material for microbiological analysis was collected in all patients. Adherent peel was carefully removed from visceral pleural surface and the lung was freed circumferentially from the apex to the diaphragm. Complete decortication of the visceral pleura and the fissures was performed by use of an endoscopic dissector device and a peanut dissector as in open decortication. Parietal pleural was removed at the level of empyematic collection. Conversion to thoracotomy and open decortication was considered if it was not possible to dissect completely the peel from the underlying lung surfaces. At the end of the procedure, two chest tubes (28 CH and 32 CH) were placed. In case of air leak or bleeding along the parenchymal surface, fibrin glue was used (Tisseel, Baxter, Deerfield, MA, USA) either in open or in VATS procedure.

2.2 Statistical analysis
Continuous variables were reported as mean standard deviation (SD) when normally distributed, otherwise as median.

To evaluate the homogeneity between VT patients and OT patients according to preoperative patients’ characteristics showed in Table 1, the proportion test (multinomial when appropriate) was used for categorical variables (sex, empyema stage, procedures performed before surgery, interval between hospital admission and surgery, co-morbidities, positive pleural fluid culture or Gram's stain or pus like-effusion) and the Student's t-test for a continuous variable (age).

Statistical analysis of surgical outcomes (operative time, postoperative stay, postoperative pain on day 1 and day 6 and 6 months after surgery, postoperative air leak, in-hospital stay and time to return to work) was performed in group OT and group VT. Unpaired t-test was used for operative time, postoperative stay, postoperative air leak, in-hospital stay and time to return to work. Mann–Whitney U test was used for postoperative pain at 1 and 6 days and at 6 months after surgery.

All tests were two-tailed with a significance level of p = 0.05 and were performed on statistical software NCSS 2004.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 References
 
In this study, 123 patients were treated by open thoracotomy and 185 by VATS, of which 174 patients underwent videothoracoscopy alone, and 11 were intra-operatively converted to open thoracotomy. In 91 cases (29.5%), no organisms were isolated from pleural debris or fluid. Conversion from VATS to open thoracotomy was needed in 11 patients (5.9%) all of whom had stage III pleural empyema, with a delay between hospital admission and surgery of more than 4 weeks in three patients and more than 6 weeks in eight patients. The overall postoperative mortality was 1.2% (4/308 cases). All of them were OT patients who achieved a 3.2% mortality rate (4/123): one patient died of sepsis 41 days after the operation and three patients died of unrelated disease (one of ictus cerebri and two of myocardial infarction, respectively, on the 13th, 17th and 26th postoperative days). Operative time was 79.6 ± 6.8 min and 70 ± 7.4 min, respectively, in OT and VT (p < 0.0001). Re-operation was performed in eight patients (six OT patients and two VT patients) because of bleeding. Postoperative overall morbidity was 21.1% (65/308), respectively, 25.2% (31/123) in OT patients and 18.3% (34/185) in VT patients (p = 0.1). Prolonged air leak, renal insufficiency requiring dialysis, wound dehiscence of open thoracotomy incision, loculated pleural effusion and residual pleural space were the most common complications.

After VATS, three patients showed recurrent empyema and underwent re-do surgery on the 42nd, 51st and 65th postoperative day by performing, respectively, a re-VATS and two open thoracotomies. No recurrence was seen in patients undergoing thoracotomy. Postoperative outcome (shown in Table 2) was evaluated according to postoperative air leak, operative time, in-hospital stay, time to return to work and postoperative pain between patients treated by open thoracotomy and VATS.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
References
 
In chronic pleural empyema, both perfusion and gas exchange in the lungs are decreased even if experimental studies stress that lung perfusion is much more impaired after decortication; vital capacity (VC) and forced expiratory volume in 1 s (FEV1) partly recover, perfusion through the affected side significantly improves and oxygen pressure and saturation increase [7,11]. Moreover, the occurrence of infection in the pleural cavity has a substantial morbidity despite decreased incidence due to effective antibiotic treatment [8].

Intrapleural fibrinolytic therapy, which has been proposed by some authors, [12,13] in our opinion, has no or a very little role in the clinical setting of patients with pleural empyema mostly due to the incomplete control of the infection and to the high number of side effects such as anaphylaxis, haemorrhage or pulmonary oedema [14,15]. The surgical treatment of chronic pleural empyema should achieve permanent control of the infection by evacuating loculated pus and fibrin debris, and prevent late pulmonary restriction resulting from lung fibrous encasement by removing the encasing membrane. The results of treatment must be independent from the surgical approach, either open or videothoracoscopic. The most effective tool should permit expeditious removal of parietal and visceral debris without injuring the lung with a low morbidity and mortality rate and a fast recovery.

From a theoretical point of view, VATS decortication should be the gold standard for pleural empyema: high magnification rate with precise debridement and breakage of fibrinous septa or band; identification of debris and lung parenchyma with a very meticulous decortication. In a previous article, Angelillo-Mackinlay and colleagues [3] compared 33 patients surgically treated by thoracotomy versus 31 patients treated by VATS for pleural empyema; the conversion rate was 10%. The authors stated that video-assisted thoracic surgical treatment has the same rate of success as open thoracotomy, with an identical morbidity and mortality rate, but offers substantial advantages over thoracotomy in terms of resolution of the disease, hospital stay and cosmetic outcome. A recent retrospective article by Luh and colleagues [8] evaluating the outcome of 234 patients who underwent VATS for chronic pleural empyema showed the safety and efficacy of such procedure with a significantly lower morbidity and mortality rate compared to open thoracotomy: respectively, 5.6% in the VATS group versus 20% in the open thoracotomy group for morbidity rate, and 2% versus 10% for mortality rate; the conversion rate was 10.3%. Lardinois and colleagues [15] compared 150 patients undergoing open thoracotomy versus 178 patients undergoing VATS (with a 3-cm utility incision) for the treatment of pleural empyema. The conversion rate was extremely high (44%). Postoperative mortality showed a slight difference between the different approaches (3% in the VATS group versus 4% in the open thoracotomy group). A recent article by Chan and colleagues [9] compared 41 patients undergoing VATS decortication versus 36 undergoing open thoracotomy decortication. They reported no conversion rate, and found statistically significant less operative time, less postoperative pain, greater satisfaction with wounds and with the operation overall for patients undergoing VATS.

In our series, the conversion rate was 5.9% (11/185): all procedures were performed without any utility incision and without finger dissection (only instrumental decortication). Videothoracoscopic procedures were mostly (96.7%, 179/185) performed by the senior surgeon (MM). The overall operative mortality was extremely low (1.29%) and occurred only in cases belonging to the OT group. The videothoracoscopic approach showed statistically significant better results in terms of in-hospital postoperative (day 1 and day 7) pain (p < 0.0001), operative time (p < 0.0001), postoperative air leak (p = 0.004), hospital stay (p = 0.02) and time to return to work (p < 0.0001). The analysis of postoperative pain at 6 months follow-up showed no significant differences among the different groups.

Re-operation for bleeding was higher in OT patients (4.8%; 6/123) than in VT patients (1%; 2/185) (p = 0.09). Recurrence of empyema (1.6%; 3/185) was seen only in patients treated by VATS approach: all patients had a stage III empyema, with an interval from onset to surgery longer than 6 weeks in all patients. Operative time was statistically significantly less in VT than in OT patients. A greater cosmetic satisfaction and a greater patient acceptance was also reported in patients treated by videothoracoscopy. The recurrence of empyema, observed in 1.6% of the VT patients, is the only drawback of videothoracoscopic decortication but in selected recurrences re-do VATS can be safely performed, as we have done in one case. Recurrence has been linked to a stage III empyema and to a late interval from onset of symptoms to surgery.

The homogeneity of our series is stressed by the high and comparable number of patients in both groups and the common aetiology in all cases (postpneumonic empyema). Last but not least, almost all VATS cases (96.7%) were performed by the same surgeon.

In conclusion, in the light of the great majority of the recent reported articles [6,9,16–22] and of the present series, the minimally invasive approach appears to be the treatment of choice for pleural empyema, even if a multicentric-randomised trial should be performed before videothoracoscopic decortication becomes the gold standard for the treatment of pleural empyema.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 References
 

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  8. 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(4):1427-1432.[CrossRef][Medline]
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  10. Macchiarini P, Wain J, Almy S, Dartevelle P. Experimental and clinical evaluation of a new synthetic absorbable sealant to reduce air leaks in thoracic operations. J Thorac Cardiovasc Surg 1999;117:751-758.[Abstract/Free Full Text]
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  16. Suzuki T, Kitami A, Suzuki S, Kamio Y, Narushima M, Suzuki H. Video-assisted thoracoscopic sterilization for exacerbation of chronic empyema thoracis. Chest 2001;119(1):277-280.[CrossRef][Medline]
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