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Collaborative quality consortia can facilitate implementation of quality measures arising from clinical databases. Our statewide general thoracic surgery (GTS) collaborative investigated the influences of cigarette smoking status on mortality and major morbidity following lobectomy for lung cancer.
Methods
Society of Thoracic Surgeons General Thoracic Surgery Database records were identified from 14 institutions participating in a statewide thoracic surgical quality collaborative between 2012 and 2017. We excluded patients with nonelective procedures, stage 0 tumors, American Society of Anesthesiologists class VI disease, and missing clinical characteristics. Outcomes analysis included the combined mortality and major postoperative morbidity rates and the influence of patient characteristics, including smoking status, on composite rate and on postoperative complications.
Results
The study cohort included 2267 patient records for analysis. Overall combined mortality and major morbidity rate was 10.2% (n = 231). Postoperative 30-day mortality was 1.5%, and major morbidity 9.6%. Significant predictors of the combined outcome included male sex (P = .004), body mass index (P < .001), Zubrod score (P = .02), smoking pack-years (P = .03), and thoracotomy (P < .001). Higher American Society of Anesthesiologists disease class and advanced tumor stage were marginally associated with worse combined outcome (P = .06). Smoking status; that is, current, past (no smoking within 30 days), or never smoked, was not associated with worse combined outcome (P = .56) and had no significant influence on major complications.
Conclusions
Smoking status was not associated with worse outcomes; however, smoking dose (pack-years) was associated with worse combined mortality and major morbidity. A statewide quality collaborative provides constructive feedback for participating institutions and surgeons, promoting quality improvement in perioperative patient care strategies and improved outcomes.
In a statewide general thoracic surgery collaborative study, smoking status had no significant influence on mortality and major morbidity following lobectomy for lung cancer.
A statewide quality collaborative allows unblinded data socialization and provides constructive and actionable feedback for participating institutions and thoracic surgeons. This review process can incentivize and improve practice approaches for lobectomy in lung cancer patients.
The Michigan Society of Thoracic and Cardiovascular Surgeons (MSTCVS) was founded in 1965 recognizing the evolution of thoracic and cardiovascular surgery as a specialty. Initial annual meetings were implemented as part of the American College of Surgeons Michigan Chapter meetings and evolved into separate MSTCVS meetings in the 1980s.
The MSTCVS Quality Collaborative (MSTCVS-QC) was established in 2001, embedded within the society, both to create a voluntary statewide data review and to incorporate concepts of structure, process, and outcomes into this review process with the goal to improve patient care associated with major adult cardiac operations in Michigan.
Blue Cross and Blue Shield of Michigan (BCBSM) and Blue Care Network offered partial financial support for the MSTCVS-QC in 2006 as part of the BCBSM Value Partnerships program.
During June 2014, the MSTCVS-QC further expanded to include general thoracic surgery to identify areas for quality improvement for lung and esophageal cancer resections. The MSTCVS-QC allows utilization of the Society of Thoracic Surgeons General Thoracic Surgery Database (STS-GTSD) from individual participant sites statewide for outcomes review. Regional data are reviewed twice per year at our February and August MSTCVS-QC meetings. By examining regional data as a collaborative, the goals include decreasing variation associated with lobectomies for lung cancers, identifying best practices among participants and improving the quality of care for these patients statewide.
This review describes the findings of a voluntary statewide review of preoperative smoking status and its influence on mortality and major morbidity
BCBSM funded expansion of the MSTCVS-QC to include volunteer STS-GTSD participants in 2014.
This study was approved on March 14, 2019, by the Institutional Review Board of the University of Michigan Medical School (IRB HUM00160943, notice of determination of not regulated status) and waived the need for Informed Written Consent for Publication.
Study Cohort
A retrospective review of prospectively collected data was designed. The STS-GTSD records from 14 participating institutions in Michigan (see Appendix E1 for contributing centers) were queried for all patients undergoing lobectomy for lung cancer between January 2012 and December 2017. All records were submitted to the STS-GTSD using the major procedure Data Collection Form version 2.3.
We excluded nonelective procedures, patients with occult or stage 0 tumors, and American Society of Anesthesiologists (ASA) class VI disease. We also excluded 111 patients with missing data on race, body mass index (BMI), peripheral vascular disease, reoperation, cerebrovascular history, ASA class, preoperative forced expiratory volume in 1 second (FEV1), Zubrod score,
Composite outcome of having either mortality or at least one major morbidity, as defined by the 2016 STS Lung Cancer Resection Risk Model, was reported.
Major postoperative complications include pneumonia, acute respiratory distress syndrome, bronchopleural fistula, pulmonary embolus, initial ventilator support >48 hours, respiratory failure, tracheostomy, myocardial infarction, or unexpected return to the operating room.
was used to assess the association between the composite mortality/major morbidity rates and risk covariates taken and modified from the 2016 STS Lung Cancer Resection Risk Model
; age; male gender; FEV1 (% of predicted); BMI; cerebrovascular disease; hypertension; steroids therapy; congestive heart disease; coronary artery disease; peripheral vascular disease; dialysis; diabetes; preoperative chemotherapy within 6 months; Zubrod score; cigarette smoking status and smoking pack-years; ASA class; reoperation; tumor pathological American Joint Committee on Cancer seventh edition staging; and operative approach (ie, open/thoracotomy or video-assisted thoracoscopic surgery/robotic). Dialysis and renal failure are highly correlated (Spearman correlation coefficient, 0.95). To avoid multicollinearity, only dialysis was included in the statistical model. Cigarette smoking status was defined as current smokers (within 30 days before admission or surgery), past smokers (have not smoked within 30 days before admission), or never smoked.
The models included the random hospital intercept to account for clustering of patients within each hospital. The most parsimonious model was selected by lasso regression. The set of coefficient estimates was determined using the optimal tuning parameter that leads to minimum Akaike information criterion. The starting model included all the above risk factors, yet the final model retained FEV1 (% of predicted), Zubrod score, ASA class, smoking pack-years, male gender, BMI, coronary artery disease, tumor pathologic staging and thoracotomy/video-assisted thoracoscopic surgery procedure approach. Although smoking status was not selected by lasso in the final model, considering it is the risk factor of interest for this study, it was included to assess its contribution.
Results
Of 2492 patient records, 2267 had complete data upon review of the Data Collection Forms and were included in the analysis cohort after the exclusion criteria were applied. The baseline characteristics of the study population are shown in Table 1. Overall, composite mortality/major morbidity rate was 10.2% (n = 231). Postoperative 30-day mortality rate was 1.5% (n = 34). Postoperative major morbidity rate was 9.6% (n = 218). Rates of individual major postoperative morbidities are shown in Table 2. Smoking status did not show a significant influence on individual major postoperative morbidities (Table 2). Table 3 demonstrates the odds ratio estimates of important patient baseline characteristics from the final regression model to composite mortality/major morbidity. Significant predictors of composite mortality/major morbidity in our final model included male sex (P = .004), BMI (P < .001), particularly BMI < 20 and BMI 35 to 40, Zubrod score (P = .02), smoking pack-years (P = .03), and open (thoracotomy) approach (P < .001). To explore the relationship of pack-years with outcome, a loess plot and restricted cubic spline plot was generated (Figure 1, A and B). Both demonstrated a relatively linear relationship with no identified pack-year threshold. A receiver operator characteristic curve was also plotted between sensitivity and (1-specificity) with varying pack-year points (Figure 2). The smooth curve also illustrates that there was no particular pack-year threshold for which an event was likely to occur. In our final model, tumor pathological staging and ASA class appeared to be associated with worse composite outcome but the relationship was not statistically significant (P = .06 for each covariate). Advanced tumor stage (stage IIIA or IIIB) was associated significantly with worse composite outcome (P = .007). Cigarette smoking status was not associated with the composite outcome of mortality or major morbidity (P = .56).
Values are presented as n (%), mean ± standard deviation, or median (interquartile range). BMI, body mass index; FEV1, forced expiratory volume in 1 second; CHF, congestive heart failure; CAD, coronary artery disease; ASA, American Society of Anesthesiologists; VATS, video-assisted thoracoscopic surgery.
The odds ratio of worse composite outcome with each unit increase in smoking pack-years was only 1.01 (95% CI, 1.00-1.01). For every 10 pack-years increase, there was 6% increase in the odds of worse composite outcomes 1.06 (95% CI, 1.01-1.11).
Values are presented as odds ratio (95% confidence interval). BMI, Body mass index; FEV1, forced expiratory volume in one second; ASA, American Society of Anesthesiologists Classification; VATS, video-assisted thoracoscopic surgery.
∗ The odds ratio of worse composite outcome with each unit increase in smoking pack-years was only 1.01 (95% CI, 1.00-1.01). For every 10 pack-years increase, there was 6% increase in the odds of worse composite outcomes 1.06 (95% CI, 1.01-1.11).
Data from the STS-GTSD offer the opportunity to review institutional results, compare and understand variation, and create opportunities for dissemination of quality improvement strategies in thoracic surgical care.
represents the first MSTCVS-GTSD quality review initiative in the state of Michigan. Our analysis focused on the influence of smoking status on composite postoperative mortality and major morbidity.
The strength of this collaborative effort lies in the willingness of participants to share data openly. As has been described in prior studies reported by the cardiac surgery group, the MSTCVS-QC provides a statewide perspective of surgical practice. The MSTCVS general thoracic surgery quality collaborative, initiated in 2012, is derived from the ongoing efforts of the cardiac surgery collaborative that was established in 2001.
The primary aims are to review outcomes and to share best practices to improve outcomes for all participants. To our knowledge, there is no established minimum number of participants that ensures the success of a collaborative group, but our goal is to identify areas for improvement that might have a salutary effect for the patients served by collaborative participants. Other efforts in general thoracic surgery have been described and capture data provided by 5 and 14 total participant hospitals in Washington state
respectively. Identifying participants through a professional statewide surgical society is facile as such participants, solely by their society membership, likely have an interest in engaging other professionals within their community. The financial support provided to any individual participant program by the collaborative is directed toward providing a small fraction of salary effort for each of the data manager(s). For the purposes of reporting these data, the greater the number of participant programs, the larger the patient cohort from which outcomes can be studied. This is no different than multi-institutional studies that arise from the cooperative efforts of like-minded individuals.
Because of its frequency in the STS-GTSD, we chose outcomes following lobectomy for lung cancer as the first MSTCVS-QC thoracic quality review.
the composite mortality and major morbidity rate was 9.5% between January 2012 and December 2014 for all pulmonary resection approaches, compared with 10.2% in our study in which we limited the review of pulmonary resections for lung cancer to lobectomy only. The continued semiannual feedback to STS participants, including risk-adjusted performance reports,
has likely contributed to the comparable composite mortality and major morbidity rate we observed amongst our collaborative participants. Overall, operative mortality in the STS-GTSD has decreased from 2.2% during 2002-2008 to 1.4% during 2012-2014.
The influence of cigarette smoking and timing of its preoperative cessation on outcomes following lung cancer surgery have been unclear and considered controversial.
Our study did not demonstrate a significant influence of cigarette smoking status on composite mortality and major morbidity rates or on individual postoperative major morbidities, including pulmonary complications. We did observe a higher proportion of postoperative pulmonary complications (eg, pneumonia, respiratory failure, tracheostomy, and return to the operating room) in current smokers, although these differences did not reach significance (Table 2). The smoking dose, as determined by pack-years (ie, tobacco load), was minimally associated with worse composite outcomes. Illustrated in Figure 3, mortality and complication rates were analyzed as a function of pack-years stratified by tertiles. Complications were subcategorized as nonpulmonary and pulmonary compilations without mortality. Nonpulmonary complications include bronchopleural fistula, pulmonary embolism, myocardial infarction, and unexpected return to the operating room. Pulmonary complications include pneumonia, acute respiratory distress, initial ventilator support >48 hours, reintubation/respiratory failure, and tracheostomy. For every 10 pack-years increase, there was 6% increase in the odds of worse composite outcomes (hazard ratio, 1.06; 95% confidence interval, 1.01-1.11). Our study did not explore the association of smoking pack-years with specific postoperative pulmonary complication. Lugg and colleagues
demonstrated somewhat comparable end points with a higher rate of pulmonary postoperative complications with current smokers, and only a trend for a lower frequency of those rates with past smokers with cessation 6 weeks preoperatively. They did not identify any significant differences in 30- and 90-day mortality based on smoking status. Several other studies have suggested that smoking cessation at least 4 weeks preoperatively may be necessary for patients undergoing elective thoracic surgery to reduce pulmonary postoperative complications and mortality.
Relationship between the duration of the preoperative smoke-free period and the incidence of postoperative pulmonary complications after pulmonary surgery.
observed that smoking cessation before surgery has been shown to reduce rates of postoperative complications, particularly pneumonia, atelectasis, and intensive care unit stay duration. Conversely, strict adherence to mandate immediate smoking cessation before proceeding with resection could delay oncologic resection or limit access to care. In a retrospective study of 4984 patients with clinical stage IA squamous cell lung carcinoma, Yang and colleagues
in a review of 27,022 propensity-matched patients with clinical stage I non–small cell lung carcinoma found that delays in resection was independently associated with decreased median survival. In their institutional review of 971 patients, those in which resection was delayed were more likely to have worse postoperative outcomes (ie, pneumonia, respiratory failure, reintubation, and increased 30-day mortality).
Figure 3Mortality and complication rates as a function of pack-years stratified by tertiles. Nonpulmonary complications without mortality include bronchopleural fistula, pulmonary embolism, myocardial infarction, and unexpected return to the operating room. Pulmonary complications without mortality include pneumonia, acute respiratory distress, initial vent support >48 hours, reintubation/respiratory failure, and tracheostomy.
Overall, our significant predictors of composite mortality and major morbidity after lobectomy for lung cancer were similar to the predictors reported by Fernandez and colleagues
in the 2016 STS lung cancer resection risk model (Figure 4). The Zubrod score and ASA class continue to be strong predictors of the composite outcome in our study. Very low BMI remains a predictor for worse composite outcomes, compatible with the 2016 risk model. In contradistinction to the 2016 risk model, FEV1 (% of predicted) was not associated significantly with worse composite mortality and morbidity rate. This could be attributed to the relatively higher mean FEV1 (% of predicted) in our study population (85.3 ± 19.6) compared with other reports,
although mean FEV1 was not reported in the 2016 risk model. In this patient cohort, thoracotomy approach significantly predicted worse composite outcome, consistent with the risk model and several prior studies.
Representing 67% of the analyzed cases in this study, video-assisted thoracoscopic surgery and robotic approaches have been increasingly utilized, and were associated with decreased morbidity compared with thoracotomy approaches.
This study is limited because it is of retrospective nature. Patients' self-reporting of smoking status may not be reliable; many patients may underestimate their actual smoking habits because adult smokers often are highly stigmatized socially. Preoperative nicotine metabolite levels were not analyzed in our study cohort. In addition, the study population is limited to operations performed by cardiothoracic surgeons who participate in the STS-GTSD and who have volunteered to participate in this quality collaborative. Although this represents the majority of lobectomies for cancer performed by MSTCVS participant hospitals and surgeons, data from nonthoracic surgeons performing pulmonary resection in Michigan were not captured in this analysis. In a recent assessment reported by Tong and colleagues, STS-GTSD participant centers represented only 15% of centers within Michigan that performed at least 1 lobectomy reported to the Centers of Medicare and Medicaid Services during 2013. At the patient level in 2013, of the 11,018 lobectomies performed nationwide, nearly 40% (n = 4177) were performed by cardiothoracic surgeons participating in either the STS Adult Cardiac Surgery Database or the GTSD, with more than 75% (n = 3240) of the latter cohort performed by GTSD participants.
Although there were some missing patient details in the data collection forms, we believe that the STS-GTSD data quality is acceptable in our state as has been demonstrated across the GTSD nationally.
Onsite audits of STS-GTSD version 2.3 data were conducted at all 14 centers included in this analysis by MSTCVS-QC Coordinating Center staff.
We have demonstrated the feasibility of a statewide quality collaborative in general thoracic surgery that encompasses a broad range of practice settings. Our general thoracic semiannual quality collaborative meetings provide participants with feedback and constructive comparison of their operative outcomes in a regional and national perspective. The presentations of site-specific unblinded data create an environment for shared discussions in a nonjudgmental manner and sets the stage for a practical, opportunistic approach to analyze best practices and provide actionable steps to improve the quality of patient care.
Conclusions
Our MSTCVS-QC multi-institutional study identified several covariates that lead to increased composite mortality and major postoperative morbidity rates also supported by other studies including that minimally invasive (video-assisted thoracoscopic surgery/robotic) approaches for lobectomy in lung cancer demonstrate favorable outcomes. We demonstrated that smoking dose (ie, pack-years or tobacco load) was associated with worse outcomes, yet smoking status had no influence on postoperative composite mortality or major morbidity (Figure 4). The relatively higher mean FEV1 (% of predicted) in our cohort potentially contributes to the lack of association of smoking status with outcomes. Although our data do not support withholding surgical resection for curative intent in lung cancer based on a current smoking status alone, preoperative smoking cessation is still undoubtedly encouraged. Further regional quality initiatives in thoracic surgery with a collaborative approach provide an opportunity to enhance the understanding of practice variation, to investigate and support strategies that optimize lung cancer care and ultimately to improve patient outcomes.
The Journal policy requires editors and reviewers to disclose conflicts of interest and to decline handling or reviewing manuscripts for which they may have a conflict of interest. The editors and reviewers of this article have no conflicts of interest.
Appendix E1. The Society of Thoracic Surgeons General Thoracic Surgery Database Michigan Participating Institutions
Beaumont Hospital-Royal Oak
Beaumont Hospital-Troy
Borgess Medical Center, Kalamazoo
Bronson Methodist Hospital, Kalamazoo
Henry Ford Hospital, Detroit
Henry Ford Allegiance Health, Jackson
Henry Ford Macomb Hospital, Clinton Township
Mid-Michigan Medical Center, Midland
Munson Medical Center, Traverse City
Spectrum Health, Grand Rapids
St John Macomb Hospital, Warren
St Joseph Mercy Ann Arbor Hospital
St Joseph Mercy Oakland Hospital, Pontiac
Michigan Medicine, Ann Arbor
References
Prager R.L.
Armenti F.R.
Bassett J.S.
Bell G.F.
Drake D.
Hanson E.C.
et al.
Cardiac surgeons and the quality movement: the Michigan experience.
Relationship between the duration of the preoperative smoke-free period and the incidence of postoperative pulmonary complications after pulmonary surgery.
Funding for the Michigan Society of Thoracic and Cardiovascular Surgeons Quality Collaborative has been provided by Blue Cross and Blue Shield of Michigan (BCBSM) and Blue Care Network since 2006 as part of the BCBSM Value Partnerships program.
The article by Al Natour and colleagues1 shares valuable perspectives on the interplay between tobacco use and perioperative risk for lung resection. As tobacco use is the leading risk factor for developing lung cancer, and as nicotine is incredibly addictive, it is not surprising that some surgical patients are smoking and unable to quit. Physicians and patients may have a sense of futility—the patient has cancer, and they may consider it “too late.” In fact, the authors found no significant difference in mortality or complications between those who had quit and those who had not.
Smoking increases your risk of problems during and after your operation. Quit smoking 4-6 weeks before your operation. That is a morsel of strong advice among many provided in the surgical patient education program published by the American College of Surgeons to prepare for the best recovery after surgery.1
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