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Ann Thorac Surg 2006;82:279-287
© 2006 The Society of Thoracic Surgeons
a Division of General Thoracic Surgery, Mayo Clinic College of Medicine, Rochester, Minnesota
b Division of Plastic and Reconstructive Surgery, Mayo Clinic College of Medicine, Rochester, Minnesota
Accepted for publication January 10, 2006.
* Address correspondence to Dr Allen, Division of General Thoracic Surgery, Mayo Clinic, 200 First St SW, Rochester, MN 55905 (Email: allen.mark{at}mayo.edu).
Presented at the Fifty-second Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 10–12, 2005.
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Abstract |
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METHODS: Data were analyzed from our prospective database on 84 consecutive patients with postpneumonectomy empyema from July 1988 to June 2004.
RESULTS: There were 73 men and 11 women. Median age was 62 years (range, 35 to 77). Indications for pneumonectomy were malignancy in 77 patients and benign disease in 7. The pneumonectomy was done at our institution in 43 patients and elsewhere in 41. A right pneumonectomy was performed in 66 patients and a left in 18. All patients were managed with the Clagett procedure consisting of open pleural drainage, serial operative debridements, and eventual chest closure after filling the pleural cavity with antibiotic solution. A bronchopleural fistula was present in 55 patients and was closed in all. A muscle flap was used to reinforce the bronchial stump in 60 patients (71%), 51 with a bronchopleural fistula, and 9 without. Operative mortality was 7.1%. Median follow-up was 1.5 years (range, 0 to 22). Overall, 81% of patients had a healed chest wall without evidence of recurrent infection. The bronchopleural fistula remained closed in all patients. Median overall survival was 3.4 years with a 5-year survival of 44.5%. Age less than 65 years and an interval between pneumonectomy and empyema of greater than 15 weeks were independent predictors of improved long-term survival.
CONCLUSIONS: The Clagett procedure remains safe and successful in the majority of patients with postpneumonectomy empyema. Age less than 65 years and a long interval between pneumonectomy and empyema are important determinants of outcome.
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Introduction |
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Material and Methods |
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The records of these 84 patients were reviewed for age, sex, comorbidities, presence of obesity (body mass index [BMI] >30 kg/m2), smoking history, indication for pneumonectomy, type of pneumonectomy (pneumonectomy versus completion pneumonectomy), side of pneumonectomy, presence of prepneumonectomy empyema, adjuvant chemo/radiation therapy, time interval between pneumonectomy and PPE, presence of BPF, type and number of procedures, complications and outcomes.
Time to the development of PPE was calculated from the date of pneumonectomy to the date of diagnosis of PPE. Patients with lung cancer were staged using the American Joint Committee on Cancer (AJCC) staging system [4]. Operative mortality included those patients who died within the first 30 days of reopening the pleural cavity (first stage Clagett procedure) and those who died later but during the same hospitalization. Patients were followed until death or for at least 1 year after chest closure. The chest wall incision was defined as healed or not healed at final follow-up. If the incision had a superficial infection or if the pleural cavity was open, the thoracotomy incision was defined as not healed. The presence or absence of BPF was determined by clinical history, physical examination, chest roentgenogram, and bronchoscopy as needed at follow-up.
Management Strategy
Operative management of PPE was determined by the presence or absence of an associated BPF. Initial tube thoracostomy was performed as needed to drain the infected pleural space and protect the contralateral lung. All patients then underwent the first stage of the Clagett procedure [2]. The thoracotomy was reopened in the operating room, with the contralateral lung protected by either a double-lumen tube or mainstem bronchus intubation. After evacuation of the pleural contents and debridement, the mediastinum was inspected for the presence of a BPF. The bronchial stump was further examined by flooding the pleural cavity with saline and observing for escape of air bubbles from the mediastinum with an increase in airway pressure. If no fistula was present, the wound was debrided and packed with gauze soaked in debridement antibiotic solution (DABS) (500 mg neomycin, 100 mg polymyxin B sulfate, and 80 mg gentamicin per liter of saline). The packing was then changed every 48 hours in the operating room. If necessary, further debridement was also accomplished before the wound was redressed. When granulation tissue developed, the dressing was then changed on the patient's floor several times a day. Additional cleansing at these dressings changes was obtained with a pulsatile hand held shower head or Water Pik device (Zimmer, Warsaw, Indiana).
Pleural space tissue cultures were not used to determine timing of chest wall closure. Instead, when healthy granulation tissue was present throughout the pleural space with no evidence of gross exudates, the cavity was completely filled with DAB's antibiotic solution, and the chest wound closed in layers with the skin closure being water tight (Clagett closure). No effort was made to completely fill the pleural cavity with either muscle or other autogenous tissue.
If a BPF was present, the bronchial stump was isolated in the mediastinum. Long bronchial remnants were reclosed at the carina. Short stumps were completely opened and the margins resected and reapproximated with polypropylene sutures. The reclosed stump was then reinforced with intrathoracic transposition of extrathoracic skeletal muscle by anchoring the muscle to the stump with interrupted sutures in such a way that the stump was completely covered by viable muscle [5]. If insufficient bronchial tissue was present to allow closure of the fistula, the muscle was first placed in apposition to the bronchial opening by suturing the muscle directly to the margin of the fistula (muscle plug) and then wrapping the muscle around the airway (Fig 1). The pleural cavity was then filled with gauze soaked in DAB's solution and managed as described above.
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2 test and Fisher's exact test were employed [8, 9]. Kaplan-Meyer analysis with log-rank test was used to determine long-term survival and the status of the thoracotomy wound at follow-up [10]. A p value of less than 0.05 was considered statistically significant. Commercially available statistical software (JMP, Cary, North Caroline) was used to perform the statistical analyses. Univariate analysis was performed using all risk factors. Statistically significant univariate variables were used to construct a multivariate model. Multivariate analysis was performed to identify independent determinants of long-term survival. Cox proportional hazard method was used to construct a model for long-term survival [11].
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Results |
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Twenty-nine patients (34%) had a PPE without an associated BPF (Fig 2). Intrathoracic transposition of muscle was done in 9 (31.0%) of these patients (Table 4). The muscle was used to reinforce a repaired esophagopleural fistula in 3 patients and to protect vital structures exposed during the process of debridements in the remaining 6 patients (heart in 2, bronchus in 2, superior vena cava in 1, and aorta in 1).
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When the pleural cavity was clean after serial debridements, the pleural space was filled with DAB's antibiotic solution and closed (second stage of the Clagett procedure) in 75 (25 of the 29 patients without a BPF and 50 of the 55 patients with a BPF) of the 84 patients (89.3%; Fig 2). The chest in the remaining 9 was not closed because of the discovery of metastases in 5, death from multiorgan failure in 2, and patient preference in 2 (1 of these patients had his chest successfully closed at another institution 45 days after discharge from our institution).
The initial chest closure failed before hospital discharge in 16 patients; none, however, had a recurrence of the BPF. The chest was again reclosed using the second stage of the Clagett procedure, and 14 of these patients were successfully dismissed from the hospital with a closed incision. The remaining 2 patients died in the hospital. At the time of hospital discharge, 73 patients had a closed chest wall.
Overall, 84 patients underwent a median of 7 operations (range, 1 to 25), and this number did not differ with the presence or absence of a BPF. Median hospitalization was 30 days (range, 2 to 425). Complications occurred in 46 patients (55%; Table 5). Tracheostomy was necessary in 12 patients, all of whom had repair of a BPF. There were 6 deaths (operative mortality, 7.1%); 5 from respiratory failure (3 with a tracheostomy). Operative mortality was 7.2% (4 of 55) for patients with BPF and 6.8% (2 of 29) for those without BPF (p = 0.95) (Table 6).
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Seven patients were dismissed from the hospital with their chest open and required periodic dressing changes. One of these patients had his chest wall closed 45 days later at another institution. At follow-up, this patient's chest wall remains closed and well healed at 15 months. The chest wall in the remaining 6 patients remained open until their death. Altogether, 74 patients eventually had their chest wall successfully closed (73 at our institution and 1 elsewhere).
The chest wall remained closed and well-healed in 68 of the 74 patients (89.5%) in whom the chest wall was eventually closed. Twelve patients did not have a healed thoracotomy at the time of follow-up. As discussed above, 6 of these patients never were surgically closed; all were managed with a chronic open window. The chest wall closure opened after discharge in 6 other patients and was treated with dressings until death because of severe comorbidities; none closed spontaneously.
Median survival was 3.4 years. Five-year survival was 44.5% (Fig 3). Significant univariate and multivariate predictors of improved long-term survival were age less than 65 years and an interval between pneumonectomy and development of PPE greater than 15 weeks (Tables 7 and 8).
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Comment |
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Samuel Robinson, from the Mayo Clinic, originally advocated open pleural drainage for chronic empyema in 1915 [15, 16]. Our management of PPE described in the current series evolved from the initial report by Clagett and Geraci [1] in 1963. Clagett's contribution was a two-stage procedure (Clagett procedure) that consisted first of open pleural drainage, and then, when the pleural cavity was clean, filling the pleural space with antibiotic solution and closing the chest wall. Stafford and Clagett subsequently reported a series of 18 patients treated with this technique. Although initially only approximately 60% successful, repeating the Clagett procedure eventually resulted in nearly 90% of their patients having a healed chest wall without drainage. Failure, however, was most often by recurrent BPF and recontamination of the pleural space. Recognizing this, Pairolero and associates [3] modified the Clagett procedure by reinforcing the closed bronchial stump with intrathoracic transposition of extrathoracic skeletal muscle. They reported that 84.0% of their patients had a healed chest wall with no evidence of infection and that 85.7% of BPFs remained successfully closed.
Our current series reinforces the success of the modified Clagett procedure in this difficult group of patients. The BPF in all patients were eventually successfully closed, although the BPF in 18% of patients had to be reclosed at least once. Similarly, the second stage of the Clagett procedure resulted in a healed chest wall without drainage in nearly 90% of patients who were closed.
Early management of PPE includes drainage of the empyema, especially if a BPF is present. Tube thoracostomy drainage should be performed in the acute phase of the empyema and patients should be instructed to lie with their operative side dependent until the empyema can be drained to prevent spillage into the remaining lung. Our series potentially shows the importance of this, since most of our operative mortality was secondary to respiratory failure from pulmonary infection that may have occurred from spillage of the empyema across the BPF into the contralateral lung. When pneumonia develops in these patients, prolonged ventilatory support may be required, increasing the risk of reopening the repaired BPF.
The reasons for failure of the second stage Clagett procedure are more difficult to determine. Patients with recurrent cancer or other life-threatening medical problems are not candidates for closure, a situation that occurred in 8% of our patients. These patients are best treated expectantly with simple dressings of the chest cavity. Patients who experienced late failure usually were usually severely malnourished and often immunocompromised. Maintaining optimal nutrition is important in this group of patients.
Closed irrigation has been proposed as an alternative treatment for PPE. Gossot and coworkers [17] described using thoracoscopy to remove as much infected tissue from the pleural space and to wash and drain the cavity. Although this technique was successful in 73% of their patients, the authors concluded that their follow-up period was "too short to draw definite conclusions," and that this procedure should not be used if a BPF is present.
Operative mortality in our series was 7.1%, with nearly all secondary to respiratory failure. Others have reported a similar mortality rate [18]. Hollaus and colleagues [19] reported on 96 patients with BPF after pneumonectomy with an operative mortality of 31%. Their approach to repair was with thoracoplasty, and they did not use the Clagett procedure in their series. As in our series, almost all the deaths were from respiratory failure, emphasizing the importance of early drainage to protect the remaining lung from cross over soilage.
In conclusion, the modified Clagett procedure remains safe and successful in the majority of patients with postpneumonectomy empyema and associated BPF. Reinforcing the closed bronchial stump with transposed muscle is an excellent strategy to prevent reopening of the fistula. Age less than 65 years and an interval between pneumonectomy and empyema of less than 15 weeks are important determinant of improved outcome.
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Thoracic Surgery Residents Association (TSRA) |
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John R. Mehall, MD
Vice-President
Rakesh M. Suri, MD
Past-President
D. Michael McMullan, MD
Representatives
The Society of Thoracic Surgeons
Daniel Boffa, MD
Michael Davidson, MD
John R. Mehall, MD
American Association of Thoracic Surgeons
Sanjay Samy, MD
Robert Merritt, MD
AATS Web Page Committee
Ali Khoynezgad, MD
Joint Council for Thoracic Surgery Education
Anastasios Konstantakos, MD
Rakesh M. Suri, MD
Residency Review Committee
Seenu Reddy, MD
AAMC Organization of Resident Representatives
Grayson Wheatley, MD
Parvez Sultan, MD
CTSNet.org Residents Section Editor
Vinod Thourani, MD
AMA Resident/Fellow Section
Sandeep Khandhar, MD
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Discussion |
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In view of the fact that a couple of your patients required ultimately three operations, is there a time when you would advocate a sternotomy or partial sternotomy to provide proximal stump closure with a stapler or something else to try and treat BPF? And the other question would be, what is your antimicrobial regimen when you close a BPF? Do you use antifungals, antibacterials, do you just go with the cultures, et cetera? Thank you again for a very nice paper.
DR ZAHEER: Thank you very much. These are excellent questions. There are series in the literature that advocated closing a bronchopleural fistula via a sternotomy. We at the Mayo Clinic have not used that approach because of the concern about infecting the sternum after a sternotomy. No patients in this series had their BPF closed through a sternotomy.
As far as the antibiotics are concerned, we culture the pleural fluid at the time of the first operation when the thoracotomy is reopened. The antibiotic choice is based on the results of these cultures.
DR WILLIAM R. SMYTHE (Temple, TX): I enjoyed your paper very much, Dr Zaheer. It is hard to argue with great results. I am interested if you could describe what the mechanism of infection was for the, I think, 26 patients who had no bronchopleural or esophageal fistula in your study? And then secondly, in the age of thoracoscopic endeavor, we have found that in these patients who don't have bronchopleural fistulas but just have a contaminated space, that you can thoracoscopically debride them, place an irrigation catheter for several days, and then fill the pleural space up with that irrigation catheter after negative cultures are obtained—sort of a modified Clagett procedure—and would you consider using that in non-BPF patients? Thanks again. Very nice paper.
DR ZAHEER: Thank you very much, and again, excellent questions. The causes of infection in the non-BPF group included 3 patients who had a viscera to pleural fistula, 2 were from the stomach and 1 from the esophagus. In the others we didn't identify a specific cause. I suspect that contamination during the pneumonectomy resulted in the infection.
There is a series in the literature about the thoracoscopic approach to this problem. Mayo is a tertiary care referral center, and almost half of these patients were transferred from other institutions. Usually the infection is pretty well settled into the pleural cavity when we see them, and to break up and remove all the debris thoracopically is difficult. And so we haven't followed that approach, but for early infections without a BPF it may be useful.
DR CAROLYN E. REED (Charleston, SC): I really enjoyed your paper, and obviously we owe the Mayo Clinic a great debt for helping us deal with this very difficult complication. A couple of questions. One is, could you elaborate a little bit on the various muscles that you used to close the BPF? It seems that every patient that I have in South Carolina who gets transferred to me to do something with this has practically no muscles left at all, and maybe I am just dealing with a very malnourished population. So I think that is an important question.
The second is, could you also elaborate a little bit more on the respiratory deaths, because that is a very important mortality issue. Could you just tell us, were they all ARDS, pneumonias, or were some them due to the fact that you were operating on patients with one lung that already had been contaminated, et cetera? Thank you.
DR ZAHEER: Thank you, Dr Reed. Again, very good questions. In the manuscript, we went into detail about what muscles were used in these patients. Serratus anterior is the main muscle we used, but pectoralis major, latissimus dorsi, even free grafts using vastus lateralis and rectus femoris. Combination and even omentum were used. The choice depends upon how the previous thoracotomy was done and which muscles were saved. It also depends on the nutritional status of the patient; for example, in a nutritionally depleted patient, you cannot use the omentum because it doesn't have any substance to it. In the end, the choice is individualized based upon what the patient had previously; however, the serratus anterior is the muscle used most often.
As far as the respiratory deaths are concerned, it is a very important point, and we discussed that in the discussion part of our manuscript, that intervening in these patients early is the best approach to decrease mortality. If you leave the bronchopleural fistula open, the remaining lung gets contaminated by the infected fluid in the pneumonectomy space, and that leads to pneumonia, ARDS, and eventually death. In these patients, as you can see, most of the deaths were related to pulmonary problems. Of the 6 patients, 4 had ARDS, 1 had pneumonia that progressed. Respiratory complications are very important, and I think the best way to avoid it is to intervene early.
DR JOSEPH I. MILLER, JR (Atlanta, GA): I congratulate you on your series; a success rate of 75% to 80% is quite significant. I think the group of patients that we see are more similar to what Dr Reed sees: they are very sick, they are very ill. I would point out that Bob Ginsberg said before his death that he had essentially stopped operating on most bronchopleural fistulas. After they fail one time, he would attempt it, and then he would convert it to an Eloesser type flap, with which the majority of patients did well. We have seen that. I would say that, one, the mean number of operations listed on your slide was 7 with hospital days from 29 or 30 days up to 400-plus days on your slide. In today's cost of hospitalization, I personally would think that you should make a major attempt to close the fistula in the type Mayo or whatever type you want. But I would suggest in this group of very, very ill patients that the morbidity and mortality of an Eloesser flap in this group is essentially zero. Thank you.
DR ZAHEER: Thank you, Dr Miller. I want to note that Dr Miller has made great contributions in this field. I agree with you that it is a very costly and a labor-intensive endeavor to treat these patients. The length of stay and the number of operations vary with time. In the past, if you look at patients who we have treated in the 1980s, the length of stays were longer and the number of operations were higher. More recently, we try to get to these patients early, and if you get to them early, you can treat them in a shorter duration of time. I think it is a difference in philosophy; how conservative or aggressive you have to be depends upon a specific institution.
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