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a Department of Surgery, Mount Sinai Medical Center, New York, New York
b Division of Thoracic Surgery, Mount Sinai Medical Center, New York, New York
c Division of Thoracic Surgery, Brigham and Women's Hospital, Boston, Massachusetts
d Division of Thoracic Surgery, Massachusetts General Hospital, Boston, Massachusetts
e Duke Clinical Research Institute, Duke University Medical Center, Durham, North Carolina
Accepted for publication May 11, 2010.
* Address correspondence to Dr Weiser, Mount Sinai Medical Center, Department of Cardiothoracic Surgery, 1190 Fifth Ave, Box 1028, New York, NY 10029 (Email: todd.weiser{at}mountsinai.org).
Presented at the Forty-sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 25–27, 2010.
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Abstract |
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Methods: All patients who had undergone pneumonectomy between January 2002 and December 2007 were identified in the STS GTDB. Among 80 participating centers, 1,267 patients were selected. Logistic regression analysis was performed on preoperative variables for major adverse outcomes.
Results: The rate of major adverse perioperative events was 30.4%, including 71 patients who died (5.6%). Major morbidity was defined as pneumonia, adult respiratory distress syndrome, empyema, sepsis, bronchopleural fistula, pulmonary embolism, ventilatory support beyond 48 hours, reintubation, tracheostomy, atrial or ventricular arrhythmias requiring treatment, myocardial infarct, reoperation for bleeding, and central neurologic event. Patients with major morbidity had a longer mean length of stay compared with patients without major morbidity (13.3 versus 6.1 days, p < 0.001). Independent predictors of major adverse outcomes were age 65 years or older (p < 0.001), male sex (p = 0.026), congestive heart failure (p = 0.04), forced expiratory volume in 1 second less than 60% of predicted (p = 0.01), benign lung disease (p = 0.006), and requiring extrapleural pneumonectomy (p = 0.018). Among patients with lung carcinoma, those receiving neoadjuvant chemoradiotherapy were more at risk for major morbidity than patients without induction therapy (p = 0.049).
Conclusions: The mortality rate after pneumonectomy by thoracic surgeons participating in the STS database compares favorably to that in previously published studies. We identified risk factors for major adverse outcomes in patients undergoing pneumonectomy.
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Introduction |
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A prognostic model generated from a multiinstitutional prospective database to ascertain patient risk factors associated with morbidity and mortality after pneumonectomy was reported in 1999 [6]. This study was performed as a subset analysis under the National Veterans Affairs Surgical Quality Improvement Program. Although a valuable report, the patients of this study may not adequately reflect those of the general population. Additionally, this model lacks several important patient characteristics clinically relevant to the decision-making process for consideration of pneumonectomy.
To address the limitations inherent in these studies, we sought to determine risk factors associated with adverse outcomes after pneumonectomy by analyzing The Society of Thoracic Surgeons (STS) General Thoracic Surgery Database (GTDB).
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Material and Methods |
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Patient Population
Between January 2002 and December 2007, there were 1,306 patients who underwent pneumonectomy. Patients were excluded from analysis if they were younger than 18 years, underwent emergency operations, had missing data on age or sex, and had laterality for the side of resection listed as "both." These requirements excluded 39 patients; thus, 1,267 patients were included in the final analysis.
Outcome Definitions
Postoperative events were those defined by the STS GTDB guidelines [7]. Hospital mortality was defined as death during the same hospitalization or within 30 days of the procedure. The hospital mortality of 5.6% (71 of 1,267) was determined to be too low to be utilized as the sole endpoint to ascertain significant risk factors. It was, therefore, decided to analyze a composite major morbidity/mortality adverse outcome for the risk factor analysis. Adverse outcome measure selection was on the basis of clinical judgment and preliminary data analysis. Death at discharge or within 30 days of surgery, pneumonia, empyema requiring treatment, sepsis, evidence of adult respiratory distress syndrome, bronchopleural fistula, pulmonary embolus, initial ventilation beyond 48 hours, reintubation, tracheostomy, atrial or ventricular arrhythmias requiring treatment, myocardial infarct, reoperation for bleeding, and new central neurologic event were selected as adverse postoperative conditions. The presence of any one or more of these entities defined an adverse outcome.
Data Analysis
Baseline characteristics of patients who experienced and did not experience major postoperative adverse events were compared using the 
2 test. Based on the results of the univariate analysis, literature review, and clinical judgment, selected variables were included in a multivariate analysis to identify independent predictors of major postoperative morbidity and mortality. Categories of some ordinal variables were collapsed because of small numbers or clinical relevance. Missing values for variables were imputed using 10-fold multiple imputation [8]. Clinical staging and the diffusing capacity for carbon monoxide variables were excluded from the analysis on the basis of high frequency of missing data (more than 30%). As an additional measure of postoperative complications, we compared the number of patients in the two groups who had a prolonged length of stay, which was defined as a total length of stay of more than 14 days after surgery [9].
An attempt was made to analyze the association between STS participant volume and incidence of postoperative morbidity and mortality after pneumonectomy. However, review of the distribution of annual pneumonectomy volume of each participating site demonstrated that the median volume was less than 5 procedures per year, with 75% of institutions performing fewer than 8 pneumonectomies yearly. The interinstitutional volume was decided to be too low to perform a meaningful analysis.
All statistical tests reported in the manuscript were performed with the SAS 9.0 statistical package (SAS Institute, Cary, NC).
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Results |
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Table 2 describes the associations between patient characteristics and the endpoint of major morbidity/mortality. Age 65 years and older, sex, many medical comorbidities, and steroid use were predictors of major morbidity or mortality. Of all patients with malignancy, receiving induction radiation therapy was not associated with an increased risk of morbidity or mortality. However, the administration of neoadjuvant chemotherapy resulted in a significantly increased risk of developing adverse perioperative events. A worse percent of predicted preoperative forced expiratory volume in 1 second (FEV1) significantly increases the risk of major adverse outcome of patients undergoing pneumonectomy (p = 0.002). The etiology of the disease requiring pneumonectomy and the type of resection were also predictors of major adverse outcomes. Undergoing resection for nonmalignant lung disease or any type of pleural disease put patients at higher risk for having a major complication. Extrapleural or completion pneumonectomy increases this risk as well. Perioperative mortality data demonstrated that mortality rates for extrapleural (8.5%) and completion procedures (7.6%) trended higher than for those seen with standard and intrapericardial approaches (4.9%) or carinal pneumonectomy (3.5%). Pneumonectomy mortality rates for patients undergoing resections for benign lung disease was 7.1% and that seen after resection of primary lung cancer was 5.3% (data not shown).
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Comment |
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The operative mortality in patients undergoing pneumonectomy by sites contributing to the STS GTDB was 5.6%. The overall mortality rate compares favorably to the incidence reported in single-institution studies [3, 14] and to the one multiinstitutional prospective study performed in the United States [6]. Through the Commission on Cancer of the American College of Surgeons national hospital survey performed in 2001, operative mortality for patients undergoing pneumonectomy for nonsmall-cell lung cancer was found to be 8.5% for the 1,507 patients undergoing this procedure [15]. A selection bias may exist in this report owing to the nature of participants contributing cases to the GTDB and may explain the slightly improved mortality rate seen in this report. As described earlier, enrollment in the database is on a voluntary basis, and as such, surgeons and institutions that participate in this endeavor may be more interested in improving patient outcomes. Additionally, most surgeons partaking in the GTDB are board-certified thoracic surgeons, which also may play a role in improved outcomes after pneumonectomy. Improved mortality rates with regard to pneumonectomy have been shown to exist for board-certified thoracic surgeons compared with general surgeons, 11.8% versus 20.2%, respectively [16].
Our multivariable regression analysis identified several patient characteristics associated with increased risk of major adverse events. Patient age more than 65 years was found to be an independent predictor of an adverse event after pneumonectomy. This effect of advancing age corresponds to data presented by the Lung Cancer Study Group as well as the National Veterans Affairs Surgical Quality Improvement Program, both of which found increasing risk of perioperative mortality for all lung resections across older age groups [6, 13]. Increased risk of major adverse events were reported in association with advanced age as reported by several single-institution studies as well [3–5, 14]. Interestingly, male sex was also found to be associated with major perioperative morbidity/mortality in this analysis. The reason for this interesting observation remains unknown.
Congestive heart failure was an infrequent comorbidity found among patients undergoing pneumonectomy in this database, with only 24 patients of the 1,267 analyzed (1.9%) having this condition. It was, however, found to be an important predictor for adverse outcome. Given the right heart dysfunction that can be caused by pneumonectomy [17], the association of preexisting heart failure with an increased risk of major morbidity/mortality after pneumonectomy is not surprising.
Preoperative appraisal of pulmonary function factors has been comprehensively studied to forecast morbidity and mortality after pulmonary resection. Many different values have been found to be predictive of pulmonary complications and mortality in patients undergoing lung resection. For example, FEV1, forced vital capacity, diffusion capacity of lung for carbon monoxide (DLCO), and postoperative predicted data have all been studied [1, 18, 19]. We investigated the role of pulmonary insufficiency as measured by percent predicted FEV1 on major morbidity/mortality after pneumonectomy. Unfortunately, in 21% of the patients undergoing pneumonectomy, percent FEV1 data were missing. We chose to utilize the 10-fold multiple imputation to address this issue. In the multivariate analysis, patients with percent predicted FEV1 less than 60 were found to experience significantly higher rates of postoperative complications when compared with patients whose percent predicted FEV1 was 80 or greater. We would have liked to analyze the effect of DLCO in patients undergoing pneumonectomy; however, nearly half of the data sheets for these patients were missing these data.
In this study, we did not find a correlation between cigarette smoking history and adverse postoperative events after pneumonectomy. A report from this STS GTDB was recently published examining the effect of smoking cessation on pulmonary complications and mortality after lung cancer resection [12]. All types of pulmonary resection were included in this analysis. Using multivariate analysis, statistically significant increased mortality was observed in current smokers and those who quit smoking between 2 to 4 weeks before surgery. We did not observe this detrimental effect of cigarette use on major adverse outcomes after pneumonectomy. This finding can potentially be explained by encompassing multiple major complications with mortality data, as explained previously, and by so few of the patients (n = 48) in the major morbidity/mortality group having never smoked. Our finding contradicts that observed by Patel and colleagues [1], who reported significant rates of perioperative morbidity in patients undergoing elective pneumonectomy who were smoking cigarettes up to the time of surgery.
The impact of induction therapy on perioperative morbidity and mortality in patients undergoing pneumonectomy for bronchogenic carcinoma has been the source of considerable debate. Increased risk of adverse events has been seen in several studies where patients have mainly received platinum-based chemotherapy before pneumonectomy [20, 21]. The experience in other single-institution, retrospective analyses have not seen this detrimental impact [22, 23]. The effect of neoadjuvant chemoradiotherapy on outcomes after pneumonectomy for patients with nonsmall-cell lung cancer has also been extensively reported by single institutions in retrospective, nonrandomized, studies. The centers reporting these studies tend to have differing experiences with regard to impact of induction therapy on patient outcome after pneumonectomy for lung cancer. Based on their incidence of major adverse events, these analyses either support [24, 25] or argue against [26] the use of preoperative chemoradiotherapy in patients requiring a pneumonectomy for the complete resection of malignant disease. There has been one recent, prospective, randomized clinical trial performed to examine the effects of neoadjuvant chemoradiotherapy versus definitive chemoradiation for stage IIIA nonsmall-cell lung cancer. This North American Intergroup trial 0139 found no survival benefit in the surgical group when a pneumonectomy was performed in contradistinction to the benefit seen in patients requiring only lobectomy [27]. This finding was attributed to the high mortality rate (25.9%) observed in the pneumonectomy group. In our study, increased rates of major adverse events were seen in patients undergoing pneumonectomy for lung cancer after neoadjuvant chemoradiotherapy versus chemotherapy alone. This observation further highlights the need for a multiinstitutional, prospective, randomized trial to ascertain the utility of pneumonectomy in patients who require induction chemoradiotherapy to address locally advanced disease.
Some studies have described increased perioperative risk seen in patients undergoing right-sided pneumonectomy [5, 20, 28]. This mostly relates to the higher incidence of bronchopleural fistulas seen in right pneumonectomies. We did not observe an adverse impact of laterality on outcomes after pneumonectomy in this study even after the use of induction chemoradiotherapy. The rate of bronchopleural fistula formation was only 0.8% (n = 10). This rate may be explained by a heightened awareness of this often fatal complication along with implementation of protective bronchial stump coverage strategies to minimize bronchopleural fistula formation.
Occasionally, pneumonectomy is required to address benign lung pathology. Indications usually include multidrug-resistant Mycobacterium tuberculosis, atypical mycobacterial infections, bronchiectasis, and other necrotizing or opportunistic infections. Our analysis found that patients are at increased risk for major morbidity/mortality when pneumonectomy was performed for benign conditions of the lung. Conlan and associates [29] reported a two-center experience with such pathology. This series records a favorable 2.4% hospital mortality rate in 124 patients. Bronchopleural fistulas developed in 7 patients (5.6%), and postpneumonectomy empyemas developed in 19 patients (15.3%). Comparable rates of morbidity and mortality were seen in another modern report of pneumonectomy for benign lung disease [30].
The last significant risk factor identified for adverse outcomes after pneumonectomy was the need for extrapleural pneumonectomy. Extrapleural pneumonectomy was first utilized to address extensive pleural and parenchymal infections of the hemithorax and now is more widely applied to patients with malignant pleural mesothelioma. At institutions with an expertise in this procedure, the associated risks of this extensive operative intervention are acceptable with reported rates of morbidity and mortality of 60% and 4% ,respectively [31]. Operative mortalities published from other centers range from 5.7% to 15% [32, 33]. The mortality rate seen with extrapleural pneumonectomy performed by thoracic surgeons contributing to the STS GTDB is 8.5% (12 of 139 patients).
There are several limitations to this study. One salient concern centers on the lack of a formal audit of this voluntary and self-reported database. Certainly, the possibility exists for underreporting of complications and perioperative mortality. There may, in fact, be some surgeons and institutions with a relatively high rate of complications that decide not to contribute their surgical volume to this database. That may result in studies whose results are not reflective of the majority of thoracic surgeons. However, there is no reward for "gaming" the system, and we doubt any intentional bias. Another significant limit is missing data. Many data fields that happen to be quite relevant to this study had significant deficiencies. As mentioned earlier, analysis based on clinical staging of primary lung cancer and percent predicted DLCO was not performed owing to inadequate data reporting. All other missing data were addressed with imputation methods that we felt adequately accounted for incomplete data reporting. The GTDB Task Force has addressed this issue regarding missing data in the most recent version (v2.081) of the data collection form [34]. Certain fields, such as pulmonary function testing, are now a required component for record inclusion and records that fail to completely record these critical data fields are excluded from data analysis.
In conclusion, we report that pneumonectomies performed by thoracic surgeons contributing to the STS GTDB perform pneumonectomies with favorable rates of mortality and major morbidity. Adverse prognostic factors were age 65 or older, male sex, presence of preoperative congestive heart failure, FEV1 less than 60% of predicted, the need for extrapleural pneumonectomy, and the use of preoperative chemotherapy or chemoradiotherapy. Among patients undergoing pneumonectomy for lung cancer, chemoradiotherapy, but not chemotherapy alone, was associated with adverse outcomes. Knowledge of these factors can help to identify patients who are at increased risk for unfavorable outcomes after pneumonectomy.
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Discussion |
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I may have not seen this correctly, but it looked like when you evaluated the group as a whole, preoperative chemotherapy was an independent risk factor for complications or your combined mortality complications, but when you pulled out all the patients with lung cancer who got neoadjuvant therapy, it wasn't. Am I correct in saying that?
DR SHAPIRO: Yes, you're right.
DR FORCE: I don't understand how that can be. Could you explain these results?
DR SHAPIRO: We demonstrated that in patients with any thoracic malignancy, those undergoing induction chemotherapy with or without radiation have an increased risk for adverse postoperative events. However, in patients with primary lung cancer, neoadjuvant chemoradiotherapy, and not chemotherapy alone, was associated with poor outcomes. Primary lung cancer patients who received induction chemotherapy only, did demonstrate a trend towards significance. One possible explanation for this difference could be that with fewer patients in the primary lung cancer group, the power of the study wasn't high enough to show significance. Additionally, it is plausible that patients undergoing pneumonectomy for metastatic or pleural-based disease may have received significantly more preoperative cycles of chemotherapy before pneumonectomy. This may predispose patients to an increased risk for complications when compared with patients undergoing resection for primary lung cancer. The database does not capture amount of chemotherapy in the data collection form.
DR AKIF TURNA (Istanbul, Turkey): Did you differentiate the patients with left pneumonectomy and right pneumonectomy, and did you look at the risk factors separately in the patients with left and right pneumonectomy, especially in the patients who had chemoradiotherapy before the resection?
DR SHAPIRO: Yes, we looked if laterality of the resection plays a role in outcomes after pneumonectomy, as suggested by other publications. However, in our study, laterality was not an independent predictor of adverse outcomes. However, it showed a trend toward significance with almost 33% of patients after right pneumonectomy developing major postoperative events versus 28% of patients after left pneumonectomy. It is possible that increased awareness for bronchopleural fistula formation after right-sided pneumonectomy has led to protective strategies, such as viable tissue coverage, to prevent this catastrophic complication. In this series, the incidence of bronchopleural fistula formation was less than 1%.
DR TURNA: Did you have the information of the stump coverage in the database?
DR SHAPIRO: Unfortunately, the database does not collect information relating to bronchial stump coverage.
DR DAVID C. RICE (Houston, TX): I enjoyed your presentation. My question really pertains to your definition of a major complication. I may have misread your slides, but was atrial fibrillation considered a major cardiac complication?
DR SHAPIRO: Yes, we considered any atrial arrhythmias.
DR RICE: Okay. It's just that after certain procedures like extrapleural pneumonectomy, it's almost a normal, even expected event.
DR SHAPIRO: In previous publications it has been shown that postoperative atrial dysrhythmias are associated with prolonged length of stay, increased cost of treatment, and are a marker of other serious morbidities in patients during perioperative period. We thought that it would be important not to ignore it in our analysis.
DR RICE: Did you do the analyses with and without atrial fibrillation?
DR SHAPIRO: No, we did not.
DR CHRISTINE L. LAU (Charlottesville, VA): I have one more question. What made you decide to include benign disease? The purpose of this study was to find independent risk factors that would enable preoperative risk assessment. What are the risk factors that can help decide which patients will benefit from pneumonectomy and which will have unacceptably high risk?
DR SETH D. FORCE (Atlanta, GA): I have one question and one comment on the same lines as the question about atrial fibrillation. I think pulmonary complications was listed as a minor complication, is that correct, or no?
DR SHAPIRO: No, they were counted as major complications.
DR FORCE: That was major, okay. It seems like it would be interesting if you separated out your groups of patients with benign disease, malignant disease, and extrapleurals, which are really three completely different groups, and ran your analysis in parallel and then compared them just for interest to see how it would change your results. Because as Dr Lau pointed out, they are very different groups of patients with different risk factors and morbidities, and I just would think that would be an interesting addition to the paper.
DR SHAPIRO: We included the type of primary disease, malignant, benign or extrapleural, in logistic regression analysis. This analysis predicts independent variables by adjusting for other variables included in the multivariate analysis. Therefore, the independent risk factors identified in our paper should be applicable to any patient undergoing pneumonectomy.
DR FORCE: It may or it may weigh one specific group of patients more heavily. If, for example, extrapleural patients had more complications, that may have an effect on how the patients in the malignant or nonbenign category showed up. So it would be interesting to see whether it did change or not.
DR SHAPIRO: You're right. It is.
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