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Ann Thorac Surg 2009;88:362-371. doi:10.1016/j.athoracsur.2009.04.035
© 2009 The Society of Thoracic Surgeons
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Sreekumar Subramanian
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Right arrow Lung - cancer

Original Articles: General Thoracic

Impact of Smoking Cessation Before Resection of Lung Cancer: A Society of Thoracic Surgeons General Thoracic Surgery Database Study

David P. Mason, MDa,*, Sreekumar Subramanian, MDa, Edward R. Nowicki, MD, MSa, Joshua D. Grab, MSb, Sudish C. Murthy, MD, PhDa, Thomas W. Rice, MDa, Eugene H. Blackstone, MDa,c

a Department of Thoracic and Cardiovascular Surgery, Heart and Vascular Institute, Cleveland Clinic, Cleveland, Ohio
c Department of Quantitative Health Sciences, Research Institute, Cleveland Clinic, Cleveland, Ohio
b Duke Clinical Research Institute, Duke University, Durham, North Carolina

Accepted for publication April 1, 2009.

* Address correspondence to Dr Mason, Cleveland Clinic, Department of Thoracic and Cardiovascular Surgery, 9500 Euclid Ave, Mail Stop J4-1, Cleveland, OH 44195 (Email: masond2{at}ccf.org).

Presented at the Forty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Francisco, CA, Jan 26–28, 2009.


GENERAL THORACIC SURGERY: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Background: Smoking cessation is presumed to be beneficial before resection of lung cancer. The effect of smoking cessation on outcome was investigated.

Methods: From January 1999 to July 2007, in-hospital outcomes for 7990 primary resections for lung cancer in adults were reported to the Society of Thoracic Surgeons General Thoracic Surgery Database. Risk of hospital death and respiratory complications was assessed according to timing of smoking cessation, adjusted for clinical confounders.

Results: Hospital mortality was 1.4% (n = 109), but 1.5% in patients who had smoked (105 of 6965) vs 0.39% in those who had not (4 of 1025). Compared with the latter, risk-adjusted odds ratios were 3.5 (p = 0.03), 4.6 (p = 0.03), 2.6 (p = 0.7), and 2.5 (p = 0.11) for those whose timing of smoking cessation was categorized as current smoker, quit from 14 days to 1 month, 1 to 12 months, or more than 12 months preoperatively, respectively. Prevalence of major pulmonary complications was 5.7% (456 of 7965) overall, but 6.2% in patients who had smoked (429 of 6941) vs 2.5%% in those who had not (27 of 1024). Compared with the latter, risk-adjusted odds ratios were 1.80 (p = 0.03), 1.62 (p = 0.14), 1.51 (p = 0.20), and 1.29 (p = 0.3) for those whose timing of smoking cessation was categorized as above.

Conclusions: Risks of hospital death and pulmonary complications after lung cancer resection were increased by smoking and mitigated slowly by preoperative cessation. No optimal interval of smoking cessation was identifiable. Patients should be counseled to stop smoking irrespective of surgical timing.

Most patients who are candidates for pulmonary resection are past or present smokers [1]. A common problem is counseling smokers before the operation about smoking cessation and how it will affect their operative risk. Some studies suggest that active smoking increases operative risk, although to what extent remains unclear [2–4]. Should resection be delayed in favor of a period of smoking cessation or performed immediately to minimize cancer progression? To answer this question, we queried the Society of Thoracic Surgeons (STS) General Thoracic Surgery Database and compared in-hospital mortality and major pulmonary complications of patients who had never smoked vs those who quit smoking at increasing time intervals before resection for lung cancer.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 Acknowledgments
 References
 
Data Source
The STS established the ongoing prospective General Thoracic Surgery Database on January 1, 1999. Data are submitted voluntarily for quality monitoring by multiple hospitals, group practices, and surgeons throughout the United States, which for this study included 79 centers. Each center or surgeon completes a standardized form that is keyed into certified software and harvested annually for submission to the Duke Clinical Research Institute, which is charged with maintaining and analyzing these data in compliance with the Health Insurance Portability and Accountability Act (HIPAA) of 1996. Variables collected include patient demographics, comorbidities, smoking history, pulmonary function testing, clinical and pathologic cancer staging, surgical details, postoperative events, and hospital and 30-day mortality [5].

Patient Population
From January 1999 to July 2007, 7990 patients underwent pulmonary resection for primary lung cancer whose data were available on smoking and smoking cessation, hospital death, and postoperative pulmonary complications. Excluded from analysis were patients aged younger than 18 years, those undergoing emergency operations, and those with missing data on age, gender, or operation date. Patient and cancer characteristics and details of pulmonary resection, stratified by smoking status and timing of smoking cessation, are reported in Table 1. Pulmonary complications could not be assessed in 25 patients who died on the day of operation; thus, 7965 patients were available for analyzing occurrence of pulmonary complications.


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  		Table 1 Characteristics of Patients and Their Therapy According to Smoking Status
 
Smoking Definitions
Patients were stratified into five groups by smoking status and timing of smoking cessation according to STS data collection fields:
Group 1: Active smoker or quit within 2 weeks of operation (current smoker)
Group 2: Quit more than 14 days to 1 month before operation
Group 3: Quit 1 to 12 months before operation
Group 4: Quit more than 12 months before operation
Group 5: Never smoked, or smoked fewer than 100 cigarettes in their lifetime

Among the 7990 patients, 6965 (87%) had a smoking history, and 1025 (13%) had never smoked. Of the 6965 patients with a history of smoking, 4026 (58%) had quit smoking more than 12 months preoperatively. Among the remaining patients with a history of smoking, 1595 (23%) were current smokers, 404 (6%) had quit more than 14 days to 1 month before resection, and 940 (12%) had quit between 1 and 12 months before resection (Fig 1).


Figure 1
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  		Fig 1. Interval of smoking cessation before resection for lung cancer among 6941 patients with a history of smoking.

 
End Points
Hospital mortality
Hospital mortality was defined as death occurring within the hospitalization during which the operation was performed. This was chosen over either 30-day or operative mortality because of increased completeness of data.

Pulmonary complications
Pulmonary complications collected on the STS data form and believed to importantly affect the postoperative course were chosen to form a composite end point. These included prolonged ventilation (> 48 hours postoperatively), need for reintubation, atelectasis requiring bronchoscopy, tracheostomy, pneumonia, and development of acute respiratory distress syndrome.

Data Analysis
A nonparsimonious mixed model with logit link was used to generate risk-adjusted comparisons of hospital mortality and pulmonary complications according to smoking status and timing of smoking cessation. Individual institutions were incorporated as random effects. Patient characteristics (including spirometry and pack-years of smoking), pathologic cancer classifications, prior cancer therapy, comorbidities, clinical status at time of operation, and details of the pulmonary resection were selected to be included in the models for risk adjustment according to their clinical relevance (Appendix). Categories of some ordinal variables were collapsed because of small numbers (Appendix). Missing values for variables were handled in several ways, including removal of patients from the analysis (rare), informative imputation, and 10-fold multiple imputation (Appendix) [6]. Reported model-based statistics are based on the aggregated results for the multiple imputation.


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  		Variables Included in Logistic Regression Modeling
 

   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 Acknowledgments
 References
 
Hospital Mortality
Although overall hospital mortality was low at 1.4% (109 of 7990), it was 1.5% among current or past smokers (105 of 6965) compared with 0.3% among patients who had never smoked (4 of 1025, Table 2). Mortality was lower among patients with longer intervals of smoking cessation before resection (Table 3, Fig 2); however, no sharp transition to low risk was identified. Cause of death was not available in the STS database.


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  		Table 2 Outcome After Resection for Lung Cancer According to Smoking Status
 

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  		Table 3 Multivariable Logistic Model of Hospital Mortality After Resection for Lung Cancer
 

Figure 2
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  		Fig 2. Forest plot shows odds ratios and 95% confidence intervals for hospital mortality according to interval of smoking cessation compared with patients who have never smoked (odds ratio of 1.0).

 
Pulmonary Complications
Major pulmonary complications were infrequent (5.7% of patients; 456 of 7965); however, they occurred more often in current or past smokers (6.2%; 429 of 6941) than in those who had never smoked (2.6%; 27 of 1024). The risk of pulmonary complications steadily decreased as the interval between smoking cessation and the operation increased (Table 4, Fig 3), but there was no sharp transition suggesting optimal timing of smoking cessation before operation.


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  		Table 4 Multivariable Logistic Model of Pulmonary Complications After Resection for Lung Cancer
 

Figure 3
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  		Fig 3. Forest plot shows odds ratios and 95% confidence intervals for pulmonary complications according to interval of smoking cessation compared with patients who have never smoked (odds ratio of 1.0).

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 Acknowledgments
 References
 
Most patients undergoing pulmonary resection for bronchogenic carcinoma have some smoking history, and many are active smokers [3]; however, the optimal timing of smoking cessation before pulmonary resection remains uncertain. In delaying the operation, thoracic surgeons must balance the risk of local tumor growth (tumor doubling) [7], risk of metastasis, and patient anxiety [8] against the benefit of reduced operative risk [9]. This clinical dilemma arises frequently: Almost 30% of patients in this STS database study were active smokers or had quit smoking within the previous month.

This study evaluated a large cohort of patients undergoing resection for lung cancer using registry data collected from multiple institutions, with a focus on determining the optimal timing of smoking cessation before resection. When this study was conceived, the expectation was that smoking cessation would lead to rapid lowering of risk, likely within weeks, such that risk would be indistinguishable from that of patients who had never smoked. Surprisingly, this return toward normal was prolonged and an optimal time frame likely far greater than would be clinically recommended before cancer resection. Although any smoking, past or current, was clearly associated with increased hospital mortality and more pulmonary complications, overall mortality was impressively low and major pulmonary complications surprisingly few.

Principal Findings
Mortality
The low mortality after pulmonary resection noted in this study was similar to recently published multi-institutional studies of pulmonary resection for malignancy performed by experienced surgeons [10, 11]. However, we found that any history of smoking, past or current, was associated with a negative impact on mortality after pulmonary resection, with large increases in relative risk. When evaluating the timing of operation related to smoking cessation, risk appeared to steadily decrease as the interval of smoking cessation increased. Reasons for this finding are likely multifactorial. Smoking cessation improves pulmonary function, both objectively and subjectively [12–14]. However, improvements in spirometry, ciliary clearance, and immune mechanisms occur over prolonged periods [15, 16]. In addition, a decrease in sputum production occurs weeks to months after cessation [13, 17–19]. The combined, deleterious effects of smoking likely contribute to mortality, but are less with longer interval of cessation.

Although in this study relative risk appears higher for patients who quit smoking more than 14 days to 1 month before operation than for current smokers, confidence intervals are wide and overlapping, and clinical importance, if any, is unclear. Contrary to the notion that a short period of smoking cessation will result in reduced surgical risk, these data demonstrate that even after a year of smoking cessation, risk-adjusted mortality remains elevated compared with lifetime nonsmokers, suggesting that adverse effects never completely disappear. This may be due to cardiovascular risk factors that, although controlled for in our multivariable analysis, still negatively affect operative outcome in smokers despite a long period of smoking respite.

There is a paucity of information about the impact of smoking cessation on hospital mortality after lung cancer resection. The few studies that have been performed have focused on long-term survival rather than in-hospital death. Smoking cessation has been shown to be associated with increased long-term survival, and active smoking has the highest risk of cancer-related and overall death [20–22]. This study demonstrates that although hospital mortality is higher for smokers after pulmonary resection, the risk appears to be modified by cessation and improved with a longer interval of cessation. Therefore, surgeons should counsel smokers that risk remains elevated regardless of timing of cessation, but that quitting holds a benefit that improves over time. Although the relative risk of current smokers or recent quitters is substantial, unduly delaying the operation does not seem justified because of the low overall hospital mortality noted in this study and the long period during which risk remains elevated.

Pulmonary complications
Occurrence of pulmonary complications in this study was considerably lower than in other studies focusing on pulmonary complications after pulmonary resection; in some studies, they occurred in more than 50% of patients [23–25]. However, this may be partly accounted for by definitions of pulmonary complications that differ widely from study to study. These include the more subtle findings of atelectasis to the most severe pulmonary complications such as acute respiratory distress syndrome. When defining pulmonary complications in this study, we chose only those we believed importantly affected a patient's postoperative course and were potentially life threatening.

This study found that smoking had less of an effect on pulmonary complications than on mortality. Risk of pulmonary complications steadily decreased among patients with longer interval of smoking cessation, and risk began to converge to that of patients who had never smoked. Explanation for this finding likely includes the time required for the deleterious impact on lung function to recede on a macroscopic, microscopic, and functional level.

That smoking increases the risk of pulmonary complications in many fields of surgery was noted decades ago [26–29]. However, the usefulness and optimal timing of smoking cessation before operation to decrease pulmonary complications remain poorly defined. Two of the largest studies were performed in cardiac surgery patients and evaluated the relationship between development of pulmonary complications and interval of smoking abstinence [30, 31]. The conclusion was that at least 8 weeks of smoking abstinence was necessary before any reduction in pulmonary complications could be realized. In fact, one study suggested a paradoxic increase in the risk of pulmonary complications if the operation was performed with less than 2 months of smoking abstinence [31], but confidence limits, which were not provided, undoubtedly widely overlapped.

In thoracic surgery, findings of increased risk of pulmonary complications related to smoking have been demonstrated in several studies [23–25], although the timing and effect of smoking cessation on pulmonary complications after resection have been addressed in only a few small studies:

• Nakagawa and colleagues [32] studied 288 patients undergoing pulmonary resection and concluded that at least 4 weeks of smoking abstinence was necessary for a discernible reduction in pulmonary complications. However, small sample size and grouping together of all patients who stopped smoking more than 4 weeks before the operation limit the strength of this conclusion.
• Barrera and colleagues [33] studied smoking cessation in 300 patients undergoing pulmonary resection and noted no differences in development of pulmonary complications in patients who were active smokers compared with those who had less than 2 months of smoking cessation and those who had more than 2 months of smoking cessation. Small sample size was also a limiting factor in this study.
• Vaporciyan and colleagues [34] evaluated pulmonary complications after pneumonectomy and concluded that patients who smoked within 1 month of operation had the highest risk. Their focus on pneumonectomy prevents generalization of recommendations to lesser extent of pulmonary resection.

The consistent decrease noted in postoperative pulmonary complications as interval of smoking cessation increased in this study suggests that surgeons can safely counsel patients about the benefits of smoking cessation preoperatively, regardless of the interval. Although the relative risk of active smokers or recent quitters is substantial, unduly delaying the operation does not seem justified due to the low overall risk of pulmonary complications and the long period during which risk remains elevated.

Strengths and Limitations
This study has the advantage of being able to compare short-term postoperative survival and pulmonary complications in a large number of patients from multiple institutions for whom a wide range of patient, surgical, and pathologic variables was available. Its limitations include the self-reported and voluntary data collection system that lacks formal auditing and may predispose to underreporting of complications. The STS General Thoracic Surgery Database is relatively new and has not yet been mined extensively for research such as this. In addition, it does not currently have the penetration of the STS Adult Cardiac Database, so the results presented may not be representative of general thoracic surgery outcomes in the United States.

No objective verification of smoking status was performed by nicotine metabolite testing; rather, reliance was placed on patient self-reporting, which may be systematically biased toward claiming a longer interval of cessation than actual. In addition, coarse grouping of interval of smoking cessation on the STS data collection form precluded evaluating timing of cessation as a continuous variable.

Finally, spirometry data were missing for about one-third of patients, which, despite modern imputation methods, degrades the value of the contribution of these variables to the analysis. These variables, in fact, distinguish nonsmokers from smokers.

Conclusions
Smoking is associated with increased hospital death and risk of pulmonary complications after pulmonary resection for lung cancer, but risk declines with a longer interval of smoking cessation. However, no optimal interval of smoking cessation was identified. Patients should be counseled to stop smoking irrespective of surgical timing and advised that their operative risk, although elevated compared with nonsmokers, can be favorably modified by cessation.


   Appendix
 


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
Acknowledgments
 References
 
DR JOSEPH B. SHRAGER (Stanford, CA): That is very interesting. Wasn't there a large VA [Veterans Affairs] study that showed that there is actually increased mortality and complications if you quit within about 1 month of surgery and supposedly due to a hypersecretory response after surgery? I wonder if you can tell us in relation to that what the causes of mortality were in those patients who had an elevated mortality if they quit within 15 days of the operation. Were those not pulmonary mortalities?

DR SUBRAMANIAN: We do not have specific data on the cause of hospital mortality for these patients. There is a large VA study showing a paradoxically elevated risk. In our analysis of this paper and others, we recognize that those are not homogeneous groups of patients, and the confidence intervals of these data appear to be very wide. So 2 people could look at the same data, take into account the confidence intervals, and then make different conclusions. The confidence intervals in our paper are also very wide, leading to considerable overlap between the groups.

DR SHRAGER: But there is overlap on the complication chart as well as on the mortality chart.

DR SUBRAMANIAN: That's right.

DR SHRAGER: So I am not sure why you are emphasizing necessarily the pulmonary complication finding when the mortality finding was higher in patients who quit close to the time of surgery.

DR DAVID H. HARPOLE (Durham, NC): I actually have the VA data to clarify that. What we found was that there was an association between people who stopped smoking and the increased rates of mortality and morbidity, but it actually covaried with the comorbidities of the patients, and what we found in our veteran population where smoking is endemic, the ones who actually quit, they quit because they were too sick to be smoking right before their surgery. I hate to say that, but that is actually what we found.

DR ROBERT CERFOLIO (Birmingham, Alabama): Dave, here is an idea: If they are too sick to smoke, don't operate on them.

DR HARPOLE: Exactly.

DR DAVID TOM COOKE (Sacramento, CA): That was a very good presentation. Is there a statistically significant difference between the smoking groups amongst each other or are the differences just trends?

DR SUBRAMANIAN: That is a very good question. There are no significant differences between groups.

DR COOKE: So looking at that data, if I have a stubborn patient who really can't get off the cigarettes, should I just look at that data and say, well, statistically there is no difference between that patient and someone who quit smoking 6 months prior, so I should go ahead and resect, regardless of smoking status? The second thing is, do you think there is any relevance in terms of how much someone smokes? Do they smoke a pack a day or are they down to 1 to 2 cigarettes a day?

DR SUBRAMANIAN: Those are excellent questions. With regard to your first question about the timing of operation, we believe that you should continue with the preoperative evaluation of the patient if he or she refuses to quit smoking. We advocate putting the patient in a smoking cessation program and aggressively working toward getting the patient to quit smoking. However, if the patient cannot quit, then continue with your evaluation and schedule the operation.

For the second question, our data looked at pack-year smoking history as a confounding variable. However, we do not have data on the interplay of various factors. For example, if you have a significant pack-year smoking history and severely reduced lung function, is there a benefit for you to stop smoking over patients with more normal lung function?

DR DANIEL L. MILLER (Atlanta, GA): I think a very important pulmonary complication which is not in your list is the requirement for supplemental oxygen therapy at dismissal. We have seen retrospectively in the patients who smoked within that 2-week period that about one third of those patients required oxygen therapy upon discharge. Do you have any data at all in regards to that?

DR SUBRAMANIAN: No. That is not a variable listed on the STS [Society of Thoracic Surgeons] database. I think on a larger note, the point you bring up is that the database should be expanded to collect additional variables. For example, as you noticed in our group, we don't have a separation of patients who were active smokers and those who quit, say, a week ago vs 2 weeks ago. Some of the heterogeneity in the literature on the effects of smoking cessation on outcomes is based on different complications that have been included.

DR CERFOLIO: Dan, I have seen a lot of your patients. I think they all go home on oxygen.

DR RICHARD R. O'REILLY (Bakersfield, CA): I was discouraged to see that even after a year of not smoking, they still had increased complications. Somewhere I had heard that 8 weeks was a good time, but most of my patients wouldn't wait for 8 weeks until you operate on them, and if you operate immediately, then there is this bronchorrhea of cessation of smoking. So some way or another, 3 weeks seemed to be optimum in my practice in the old days, although you seem to show that 15 to 30 days is worse than 1 to 15 days.

DR SUBRAMANIAN: I would like to clarify. Although results appear worse, outcomes of patients who quit smoking within 15 to 30 days of operation were not statistically significantly worse than those of either patients who had quit between 0 and 14 days or were active smokers.

DR CERFOLIO: One final question. How do we know the accuracy of this? This is by patient report. I think if you really talk to the patients, they tell you they stopped a month ago, but if you really talk to them, they had a cigarette right before surgery.

DR SUBRAMANIAN: That is an excellent point. Not only is self-reporting of smoking at issue, but also pack-year smoking history, because patients tend to underreport how much they have smoked.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
References
 
We thank Tess Parry for editorial assistance. This study was supported in part by the Kenneth Gee and Paula Shaw, PhD, Chair in Heart Research (Dr Blackstone) and the Daniel and Karen Lee Endowed Chair in Thoracic Surgery (Dr Rice).


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

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