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Ann Thorac Surg 2002;74:876-884
© 2002 The Society of Thoracic Surgeons
a Division of General Thoracic Surgery, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA
b Section of Biostatistics, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA
* Address reprint requests to Dr Miller, Emory University Clinic, 1365 Clifton Road NE, Atlanta, GA, USA 30322
e-mail: daniel_miller{at}emoryhealthcare.org
Presented at the Forty-eighth Annual Meeting of the Southern Thoracic Surgical Association, San Antonio, TX, Nov 8–10, 2001.
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Abstract |
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Methods. We retrospectively reviewed all patients who underwent completion pneumonectomy from January 1985 through September 1998 at the Mayo Clinic in Rochester, MN. Factors affecting operative mortality and postoperative morbidity and were analyzed using univariate and multivariate analysis.
Results. There were 115 patients (73 men and 42 women), with a median age of 64 years (range, 12 to 83 years). Indication for pneumonectomy was benign disease in 57 patients (49.6%), lung cancer in 51 (44.3%) and metastatic disease in 7 (6.1%). There were 24 deaths (mortality 20.9%, 95% CI 13.9% to 29.4%). Mortality for patients undergoing completion pneumonectomy for benign disease, lung cancer, and metastatic cancer was 26.3%, 17.6%, and 0%, respectively (p = 0.24). Factors adversely affecting mortality with univariate analysis included advanced age (p = 0.004), preoperative corticosteriod use (p = 0.01), decreased preoperative diffusion capacity of lung to carbon monoxide (p = 0.01), intraoperative blood transfusion (p = 0.04), and excessive crystalloid infusion within the first 12 hours (p = 0.01) and 24 hours (0.03) postoperatively, respectively. Factors adversely affecting mortality with multivariate analysis included advanced age (p = 0.001), preoperative corticosteriod use (p = 0.002), and low preoperative hemoglobin (p = 0.02). Cardiopulmonary complications occurred in 72 patients (63.7%). Factors adversely affecting morbidity with univariate analysis included benign disease (p = 0.002), decreased preoperative diffusion capacity of lung to carbon monoxide (p = 0.04), bronchial stump reinforcement (p = 0.0001), and excessive crystalloid infusion within the first 12 hours (p = 0.006) and 24 hours (p = 0.02) postoperatively, respectively. Factors adversely affecting morbidity with multivariate analysis included advanced age (p = 0.005) and bronchial stump reinforcement (p = 0.001).
Conclusions. Multiple factors adversely affect operative mortality and cardiopulmonary morbidity after completion pneumonectomy. Although completion pneumonectomy remains a high-risk procedure, especially for benign disease, it still should be considered a treatment option in selected patients.
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Introduction |
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TopAbstractIntroductionMaterial and methodsResultsCommentDiscussionReferences |
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Material and methods |
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TopAbstractIntroductionMaterial and methodsResultsCommentDiscussionReferences |
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Operative mortality included both those patients who died within the first 30 days after operation and those who died later but during the same hospitalization. Postoperative cardiopulmonary morbidity was defined as respiratory failure with or without acute respiratory distress syndrome (ARDS), pneumonia, secretion retention, postpneumonectomy pulmonary edema, cardiac arrhythmia, myocardial infarction, cardiac herniation, and congestive or right heart failure. Postoperative respiratory failure was considered to be present if any of the following criteria were present: mechanical ventilatory support greater than 24 hours, noninvasive positive pressure ventilation required at any time, or supplemental oxygen required after hospital dismissal. Retained secretions were considered to be present when bronchoscopy was necessary for removal.
The primary endpoints of analysis were operative mortality and postoperative morbidity. The effects of risk factors on these endpoints were evaluated with both univariate and multivariate analysis. Risk factors represented by continuous variables were assessed using two-sample t tests [5] when the data were approximately normal and by using rank sum tests [6] when the data were found to be not sufficiently gaussian. The effects of categorical variable [6] risk factors were evaluated using 
2 tests [7] and Fisher’s exact tests [8]. Multiple logistic regression [9] was used during multivariate analysis to simultaneously evaluate the effects of risk factors. Specifically, stepwise selection was used to identify significant predictors. Variables found to be significant in the logistic regression models were reported using odds ratios with 95% confidence intervals (CI). All statistical tests were two-sided, with the threshold of significance set at p less than 0.05. All analyses were conducted using SAS (SAS Institute Inc, Cary, NC). The study was approved by the Mayo Foundation’s Institutional Review Board.
Clinical findings
There were 115 patients (73 men and 42 women). Median age was 64 years and ranged from 12 to 83 years. Indication for pneumonectomy was benign disease in 57 patients (49.6%), lung cancer in 51 (44.3%), and metastatic cancer in 7 (6.1%). Benign conditions included postoperative bronchopleural fistula (BPF) in 21 patients, destructive lung disease in 14, bronchiectasis in 10, aspergillosis in 9, and lobar torsion in 3. The cell type in the 51 patients who had primary lung cancer was squamous cell carcinoma in 32 patients, adenocarcinoma in 8, bronchoalveolar cell carcinoma in 4, large cell carcinoma in 3, carcinoid tumor in 3, and blastoma in 1. Pathologic stage of the primary cancers was stage IA in 22 patients, IIA in 4, IIIA in 23, and stage IIIB in 2. The original site of the cancers metastatic to the lungs was soft tissue sarcoma in 3 patients, osteogenic sarcoma in 2, and melanoma and breast carcinoma in 1 patient each.
Associated comorbities were present in 65 patients (56.5%) and included chronic obstructive pulmonary disease in 46 (40.0%), coronary artery disease in 13 (11.3%), cardiac dysrrhythmias in 12 (10.4%), diabetes mellitus in 9 (7.8%), corticosteroid use in 8 (7.0%), asthma in 6 (5.2%), valvular heart disease in 6 (5.2%), alcoholism in 5 (4.3%), and others in 16 (13.9%). A total of 37 patients (32.1%) had undergone preoperative therapy that included chemotherapy within 3 months of CP in 16 cases, radiation therapy in 19, and both in 2.
In all, 88 patients (78.8%) were chronic cigarette smokers (median 50 pack-years, range 10 to 99 pack-years); 22 (26.8%) had smoked during the 8 weeks preceding CP. Median percent predicted forced expiratory volume in 1 second (FEV1) was 60 (range 29% to 122%). Preoperative pulmonary function and gas exchange are summarized in Table 1. Weight loss before CP occurred in 10 patients (8.7%) and ranged from 1.8 to 18.2 kg (median 7.3 kg). Body mass index (BMI) ranged from 15 to 41 kg/m2 (median 24 kg/m2).
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Completion pneumonectomy was on the right in 73 patients (63.5%) and on the left in 42 (36.5%). Intrapericardial dissection was required in 62 patients (53.9%). An extended resection included resection of parietal pleura in 16 patients (13.9%), chest wall in 9 (7.8%), left atrium in 3 (2.6%), diaphragm in 2 (1.7%), and superior vena cava, esophageal muscle, and main pulmonary artery in 1 patient each (0.9%). Extracorporeal circulation was used in 1 patient (0.9%). Mediastinal lymphadenectomy was completed in 54 patients (47.0%) and mediastinoscopy was performed in 12 patients (10.4%); all lymph nodes biopsied were negative for metastatic disease.
The bronchus was closed with a stapler in 109 patients (94.7%) and hand-sutured in 6 (5.3%). The bronchial stump was reinforced with muscle in 54 and parietal pleura in 10. The muscle used was the serratus anterior in 47 patients, latissimus dorsi in 4, pectoralis major in 2, and a combination in 1. Tube thoracostomy was placed in 77 patients (67.0%); the chest tube was removed in the operating room in 53 patients, during postoperative day 1 in 19 patients, postoperative day 2 in 4 patients, and postoperative day 3 in 1 patient.
Overall, 37 patients required a blood transfusion (median 4 U, range 1 to 22 U); 32 patients (15.1%) had intraoperative transfusions (median 3 U, range 1 to 22 U) and 17 (6.5%) had transfusions within the first 24 hours postoperatively (median 2 U, range 1 to 6 U). Preoperative serum hemoglobin level ranged from 8.0 to 16.9 g/dL (median, 12.6 g/dL). The median volume of crystalloid infused in the first 12 hours, including the intraoperative period, was 24.6 mL/kg (range, 3.2 to 118.4 mL/kg) and within the first 24 hours postoperatively was 33.2 mL/kg (range, 9.3 to 118.7 mL/kg).
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Results |
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Factors not affecting mortality or morbidity included gender, smoking history, time of smoking cessation, associated cardiovascular disease, chronic renal failure, diabetes mellitus, hematological disease, cirrhosis, nonpulmonary malignancy, BMI, weight loss, preoperative chemotherapy, preoperative radiation, preoperative percent predicted FEV1, total lung capacity and residual volume, PaO2 and PaCO2, side of resection, extent of resection, technique of bronchial stump closure, pathologic stage, and duration of ventilatory support.
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Comment |
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Completion pneumonectomy is technically demanding and is associated with significant operative mortality and postoperative morbidity. Historically, operative mortality for CP has ranged between 0% and 21% with a median of 10.8% (Table 7) [10–19]. The operative mortality for CP is greater than the 6.2% mortality reported for standard pneumonectomy by the Lung Cancer Study Group [20] and the 7.0% reported by us [21]. Mortality clearly varies with the indication for CP.
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Completion pneumonectomy operative mortality for lung cancer was considerably higher in our current series (17.6% vs 9.4%). In the cumulative review, operative mortality of a CP for lung cancer ranged from 0% to 17.6% (median, 9.3%). One possible explanation for this increase in mortality is that a greater percentage of patients had neoadjuvant treatment (32% vs 17%) in our current series. This nearly three-fold increase in mortality has not been demonstrated in current cooperative studies comparing the results of neoadjuvant therapy and surgery versus surgical resection alone [24–26]. The number of CP in those series are extremely rare, and a final conclusion cannot be made. Of the 470 pneumonectomies reported by Martin and colleagues [27] after neoadjuvant therapy, only one was a CP. In our current series, neoadjuvant therapy did not affect operative mortality and postoperative morbidity after CP.
We identified multiple factors that adversely affected operative mortality (Tables 2 and 3). Most of these variables were associated with preexisting lung disease—especially benign disease—and the impairment of gas exchange (diffusion capacity of the lung to carbon monoxide) that could reflect the extent of lung destruction and secondary pulmonary infection. Others have reported similar findings [28–31]. Our data also demonstrated that advanced age, low preoperative hemoglobin, and preoperative corticosteroid use adversely affected operative mortality after CP.
Advanced age influences mortality after pulmonary resection, and for this to be an independent predictor of increased mortality for this high-risk procedure is not surprising. The median age of the patients who died after CP was 10 years older than the patients who survived the procedure. Also, the median age of patients undergoing CP in this series was 5 years older than the patients in our earlier series.
Age can also be an advantage, especially in younger patients with metastatic disease. If patients can tolerate an aggressive approach for possible cure, even if a pneumonectomy is required to render the patient tumor free, then CP should be considered even if the patient has had previous resections. No patient in our two series or in the cumulative review died as a result of CP for metastatic disease.
Anemia has been associated with increased mortality in patients who undergo standard pneumonectomy, but this is the first time that it has been identified as an independent predictor of mortality after CP. We have no explanation for this association; however, possible explanations include advanced age, significant smoking history, presence of unknown coronary artery disease and chronic obstructive pulmonary disease. Harpole and colleagues [32] reported a correlation between a low hematocrit and the onset of atrial arrhythmias after pneumonectomy. Atrial arrhythmias was the most common cardiac complication in our series, which was also seen in an earlier series of standard pneumonectomies from our institution [33].
Corticosteroid use has a long history of associated complications after pulmonary resection related to impaired healing, prolonged air leaks, and development of opportunistic infections. Of our 8 patients who were being treated with corticosteroids before surgery, 5 (62.5%) died after CP, 3 of respiratory failure secondary to ARDS and 2 from complications of a BPF. Our current practice is to reinforce the bronchial stump with viable tissue (preferably extrathoracic muscle) in patients who are receiving corticosteroids at the time of pneumonectomy or CP to prevent the potentially fatal complication of a BPF.
An important question concerning CP is whether the side of the procedure increases operative risk. In a recent series of standard pneumonectomies for malignant disease reported by Bernard and colleagues [21] from our institution, a right pneumonectomy was associated with increased operative mortality. More recently, a study by Martin and associates [27] demonstrated that a right standard pneumonectomy performed after neoadjuvant therapy was an independent predictor of both increased operative mortality and morbidity. In the present series, however, there was no significant difference in mortality observed between a right CP (22%) and a left CP (19%) (p = 0.72). Also, there was no significant difference in cardiopulmonary complications between a right (65%) and a left (61%) CP (p = 0.65). Of note, however, all seven of the bronchopleural fistulas that developed postoperatively were on the right.
Complications occurred in 70% of our patients. Cardiopulmonary complications were the most common, accounting for 90% of these complications. Multiple factors adversely affect cardiopulmonary morbidity (Tables 5 and 6). Historically, respiratory and cardiac complications have been the most common, accounting for more than 50% of complications after CP (Table 8). Empyema and BPF also occur at a higher rate than normal. The majority of patients who undergo CP are at increased risk for BPF and empyema, because the CP is performed for benign diseases that include active infection and complications of previous resections, in the cases of lung cancer after radiotherapy, and in patients whose are immunocompromised because of advanced age, chronic corticosteriod use, or history of chronic debilitating disease.
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Potential operative problems include obliteration of the pleural and intrapericardial spaces by previous resection, radiation therapy, or past history of infection or other inflammatory processes. If adhesions and fibrosis involve the hilar vessels, intrapericardial control of the vessels is desirable. Intrapericardial dissection was required in more than 50% of our patients. Mobilization of the pulmonary artery is potentially dangerous if scar, fibrosis, or tumor is present that may result in massive hemorrhage and death if an injury occurs.
If the intrapericardial space is obliterated, especially on the left side, the pulmonary artery may be exposed posteriorly by first dividing the bronchus. This maneuver allows excellent control of the proximal pulmonary artery. This technique has been eloquently described by Mansour and Downey [36]. If problems develop on the right side, the pulmonary artery can be isolated by opening the pericardium posteriorly between the SVC and the ascending aorta or by dividing the bronchus first as described above. Only 1 patient (0.9%) in our series died intraoperatively secondary to a vascular injury (main pulmonary artery); however, more than 80% of the intraoperative deaths in the cumulative review (Table 7) were related to vascular injuries. Therefore, intrapericardial control to prevent intraoperative hemorrhage is critical in patients requiring CP. Attention to operative details is important to minimize blood loss and to restrict fluid infusion intraoperatively to minimize the potential for respiratory failure.
Excessive blood transfusions and crystalloid fluid infusion were both significant predictors of operative mortality and cardiopulmonary morbidity in our patients. These data support similar findings of other investigators that excessive fluid administration is both a significant factor in the genesis of respiratory complications and an independent predictor of mortality [21, 37, 38]. However, others have found no significant association between fluid administration and the development of pulmonary edema [39, 40]. Because of the retrospective nature of our series, we cannot conclude that excessive crystalloid infusion is a contributing factor in the development of postpneumonectomy pulmonary failure. However, it was associated with increased mortality and morbidity in this group of patients undergoing CP.
Another beneficial surgical technique for prevention of postoperative complications is reinforcement of the mainstem bronchus stump with vascularized tissue to prevent a BPF. The bronchial stump must be managed with meticulous care, avoiding devascularization and excessive length. Our current practice is to reinforce the bronchial stump with extrathoracic muscle as a transposition flap if the hilum has previously been radiated, if resection is performed in the presence of acute or chronic infection, or if the patient has received corticosteroids preoperatively [41, 42]. Reinforcement with a muscle flap should also be used in repair of bronchopleural fistula. It is no surprise that reinforcement of the bronchus was an adverse independent predictor of postoperative morbidity in our series, because muscle transposition was used in patients who were considered at highest risk for fistula formation after CP that could potentially be fatal. This was a similar finding in a series of patients from our institution who underwent standard pneumonectomy and developed postoperative empyema and BPF [31].
During the postoperative period, it is essential to prevent pulmonary complications. Improved perioperative management related to anesthesia and critical care have reduced potentially fatal cardiopulmonary complications after CP. Newer anesthetic agents with minimal respiratory and cardiac depression have led to early extubation, which avoids tracheobronchitis and nosocomial infections from prolonged mechanical ventilation. If there are any signs to suggest a pulmonary infection antibiotic therapy is initiated immediately to prevent a postoperative pneumonia, which could prove to be fatal.
A pulmonary hygiene program is initiated immediately postoperatively consisting of aggressive chest physiotherapy, secretion control, and early ambulation with exercise in our inpatient pulmonary rehabilitation unit. Epidural anesthesia is used to reduce postoperative pain, which enables patients to clear secretions by improved cough, deeper inspiration, and early ambulation. However, because of concerns for infectious complications related to the epidural catheter in patients undergoing CP for acute infections, nonsedating analgesics such as ketorolac tromethamine are used to reduce postoperative pain. Minitracheostomies, a percutaneous catheter placed at bedside under local anesthesia, maybe use to facilitate suctioning and to stimulate coughing in patients without the morbidity of a standard tracheostomy.
If patients develop atrial arrhythmias, aggressive treatment using calcium channel blockers and/or ß-blockers is initiated to restore normal rhythm to improve atrial function. Pulmonary edema caused by impairment of atrial function related to atrial fibrillation can be detrimental in patients who have undergone a CP. Rapid-rate atrial arrhythmias may be the critical events that lead to fatal pulmonary impairment in marginal patients who have required a CP. Therefore, it is essential to restore normal sinus rhythm as soon as possible even if cardioversion is required. Atrial fibrillation accounted for 75% of cardiac complications in our patients undergoing CP.
In conclusion, multiple factors adversely affect operative mortality and cardiopulmonary morbidity following completion pneumonectomy. Prevention of complications at the time of operation and during the early postoperative period is essential to reduce operative mortality and postoperative morbidity. Although completion pneumonectomy remains a high-risk procedure, especially for benign disease, it still should be considered a treatment option in selected patients.
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Discussion |
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TopAbstractIntroductionMaterial and methodsResultsCommentDiscussionReferences |
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Dr Miller: Because of time limitations I could not present our intraoperative data, but one of the main problems we faced was extensive fibrosis and adhesions in the hilum of the lung; 60% of these patients required intraoperative dissection. Therefore, in patients undergoing a completion pneumonectomy, we do not hesitate to obtain proximal control of the hilar structures, especially the pulmonary artery, intrapericardially. If the pericardial space is obliterated, we will proceed posteriorly and divide the bronchus first, and then divide the pulmonary artery, which may decrease the risk of injury to the pulmonary artery and potential massive hemorrhage that may be fatal.
Dr Thomas A. D’Amico (Durham, NC): Dr. Miller, I really enjoyed that series and I am sure everyone recognizes the difficulty with it. I just have a couple of questions. I wonder if you could address what you think the etiology of the differences in mortality is for the two time periods? Were you more aggressive in the more modern series? Second, what were the exclusion criteria for pulmonary function tests? At what level did you exclude a patient, since so many of the patients probably had multiple bilateral operations? And third, I wonder if you could just share with us, since the patients with benign disease did worse, what was the range of diagnoses for the benign diseases?
Dr Miller: In regard to the mortality rate for the different indications for resection, the main difference was in our lung cancer patients. There was almost a twofold increase in mortality in this later series. The only variable that was different between the two studies was the percentage of patients that had neoadjuvant therapy; there was a 300% increase in the number of patients who underwent neoadjuvant treatment in this group presented today. However, with univariate and multivariate analysis neoadjuvant therapy had no affect on morbidity or mortality in the later group of patients who underwent completion pneumonectomy for lung cancer. In our current series, there was a 10-year increase in the median age of these patients compared to the earlier series, which could also account for the increased mortality.
In regard to pulmonary function, the median percent predicted FEV1 was 60%. It is interesting to note that 113 of these 115 patients had the previous resections performed only on the ipsilateral side. Just like our standard resections, we try to achieve a postoperative predictive FEV1 greater than 800 cc, but as you know from the lung volume reduction experience, a lower FEV1 can be tolerated.
The majority of patients who undergo completion pneumonectomy have already experienced a physiologic shift to the contralateral side. Therefore, the patients may have an advantage because of this early shift to the other side that may decrease the risk of postpneumonectomy pulmonary edema. Only one patient in our recent series experienced this usually fatal complication after pneumonectomy.
The benign lung diseases included postoperative bronchopleural fistula in 21 patients, only two of which had their initial procedure performed at our institution. Other benign diseases were destructive lung diseases in 14, bronchiectasis in 10, aspergillosis in 9, and lobar torsion in 3.
Dr Joseph M. Arcidi, Jr (Omaha, NE): I am surprised that one of the factors that perhaps was not delineated was whether the extent of the previous resection was a risk factor, because intuitively one would not have thought that a previous wedge or segmentectomy would have had the same morbidity or mortality risk as a prior lobectomy in your patients. Could you delineate that further?
Dr Miller: We analyzed each procedure statistically. The majority of the patients who had multiple wedges or segmentectomy were patients who had a completion pneumonectomy for metastatic disease. These patients were younger and had better underlying lung function. However, there was no difference in regard to morbidity or mortality on the basis of the previous type of resection. Also, we analyzed for extend of resection such as chest wall, superior vena cava, atrium and esophageal invasion, and again there was no difference statistically.
Dr Joe Putnam, Jr (Houston, TX): I enjoyed your presentation and applaud your efforts in achieving local disease control in these complex patients. The standard mortality for pneumonectomy is around 6% and you have much greater mortality in this selected population. How do you effectively communicate the risk and benefits to this complex patient population? Other alternatives for treatment, such as chemotherapy and radiation for recurrent malignancy or perhaps some other alternative for the benign disease, may also be appropriate alternatives. How are these alternatives considered in your evaluation? The challenge as you have outlined is to select the patients who will benefit best from completion pneumonectomy and still minimize risks.
Dr Miller: I agree with you a hundred percent, Bill. There has been a 100% increase in the number of cases that we did over that latter time period compared to our first series. I would agree that by looking at our present data and the factors that we have found we are going to be more selective in the future, especially in older patients and patients who had a history of chronic steroid use. Sixty-three percent of the patients who had previous corticosteroid use died.
Other treatment options such as chemotherapy and radiation may be a better option in older patients with poor pulmonary reserve who require completion pneumonectomy. However, we are seeing more patients who are surviving their initial lung cancer and are developing second lung cancers that have adequate pulmonary reserve and an increase in patients with opportunistic infections secondary to immunosuppression. In the future it is going to be more of a challenge and hopefully with better selection, attention to intraoperative techniques, and improved postoperative care, we can lower operative morbidity and mortality.
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