Journal of Thoracic Oncology:
Comparative Outcomes of Elderly Stage I Lung Cancer Patients Treated with Segmentectomy via Video-Assisted Thoracoscopic Surgery versus Open Resection
Smith, Cardinale B. MD, MSCR*; Kale, Minal MD†; Mhango, Grace MPH†; Neugut, Alfred I. MD, PhD‡§; Hershman, Dawn L. MD, MS‡§; Mandeli, John P. PhD‖; Wisnivesky, Juan P. MD, DrPH†¶
*Tisch Cancer Institute, † Department of Medicine, Division of General Internal Medicine, Mount Sinai School of Medicine, NY, New York; ‡ Department of Medicine, Division of Hematology/Oncology, Columbia University, NY, New York; §Department of Epidemiology, Mailman School of Public Health, Columbia University, NY, New York; and Departments of ‖Preventive Medicine and ¶ Medicine, Division of Pulmonary and Critical Care Medicine, Mount Sinai School of Medicine, NY, New York.
Disclosure: Dr. Wisnivesky has relationships with Executive Health Exam International (member of research board), Novartis Pharmaceutical (lecture honorarium), United Biosource (consultant), Merck (consultant), IMS Health (consultant), and GlaxoSmithKline (chronic obstructive pulmonary disease research grant). Dr. Neugut has relations with EHE International (member of research board). The other authors declare no conflict of interest.
Address for correspondence: Cardinale B. Smith, MD, MSCR, Division of Hematology/Medical Oncology and Brookdale Department of Geriatrics and Palliative Medicine, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, Box 1079, New York, NY 10029. E-mail: email@example.com
Introduction: Video-assisted thorcacic surgery (VATS) is considered an alternative to open lobectomy for the treatment of non–small-cell lung cancer (NSCLC). Limited data are available, however, regarding the equivalence of open versus VATS segmental resections, particularly among elderly patients.
Methods: From the Surveillance, Epidemiology, and End Results–Medicare database we identified 577 stage I NSCLC patients aged more than 65 years treated with VATS or open segmentectomy. We used propensity score methods to control for differences in the baseline characteristics of patients treated with VATS versus open segmentectomy. Outcomes included perioperative complications, need for intensive care unit, extended hospital stay, perioperative mortality, and survival.
Results: Overall, 27% of patients underwent VATS. VATS-treated patients had lower rates of postoperative complications (odds ratio [OR]: 0.55, 95% confidence interval [CI]: 0.37–0.83), intensive care unit admissions (OR: 0.18, 95% CI: 0.12–0.28), and decreased length of stay (OR: 0.41, 95% CI: 0.21–0.81) after adjusting for propensity scores. Postoperative outcomes were not significantly different across groups after adjusting for surgeon characteristics. Overall (hazard ratio: 0.80, 95% CI: 0.60–1.06) and lung cancer–specific (hazard ratio: 0.71, 95% CI: 0.45–1.12) survival was similar across groups.
Conclusions: VATS segmentectomy can be safely performed among elderly NSCLC patients and is associated with equivalent postoperative and oncologic outcomes.
Full lobar resection remains the procedure of choice for patients with early-stage non–small-cell lung cancer (NSCLC).1 However, this recommendation is based on the results of a single randomized controlled trial that showed an increased risk of recurrence, but no differences in overall survival, among patients treated with lobectomy versus lesser resections.2 More recent data suggest that limited resections, and in particular segmentectomy, may lead to equivalent oncologic outcomes in patients with tumors less than 2 cm in size, specifically in the elderly.3–7 Moreover, limited resections are also indicated for the treatment of patients with limited cardiopulmonary reserve, multiple comorbidities, or those patients who are not considered candidates for lobar resection.8
Over the past decade, video-assisted thoracic surgery (VATS) has been rapidly adopted as an appropriate technique for performing full lobar resections for early-stage lung cancer. Current data suggest that this approach is associated with better perioperative outcomes and may be equivalent to open resection in terms of oncologic results.9–11 However, only a few single-center studies have evaluated the outcomes after VATS versus open segmentectomy for lung cancer.12–15 Thus, limited data exist regarding the potential advantages of VATS for lung cancer patients who are not candidates for lobectomy.
In this study, we used population-based data from a national cancer registry to compare perioperative outcomes and long-term survival among stage I NSCLC patients more than 65 years of age who were treated with VATS versus open segmentectomy.
MATERIALS AND METHODS
We identified study subjects from the Surveillance Epidemiology and End Results (SEER) database, a registry maintained by the National Cancer Institute, which contains information on all new cases of cancer from several geographic areas of the United States. Cancer information in SEER for patients 65 years of age and older has been linked to Medicare claims to create the SEER-Medicare database.16 The study cohort consisted of primary cases of pathologically confirmed, stage I non–small-cell lung cancer (NSCLC) who received treatment between 1994 and 2007. Analyses were restricted to patients who underwent segmentectomy via VATS or open thoracotomy. We excluded patients with tumors more than 5 cm in size, who would not be good candidates for limited resection as well as members of health maintenance organizations (for whom Medicare does not collect claims), and patients without continuous Part B (outpatient) coverage (to ensure comprehensive claims data to assess comorbidities and chemotherapy). To have at least 1 year of Medicare claims for assessing comorbidities before surgery, we limited the study to patients more than 65 years of age at the time of lung cancer diagnosis.
Information on sociodemographic characteristics (age, sex, race/ethnicity, and marital status) was obtained from SEER. Socioeconomic status was estimated based on mean income levels in the patients’ census area or zip-code, as provided by Medicare. We used SEER data on tumor extension, size, lymph node status, and presence or absence of metastasis to classify patients according to the most recent edition of the Tumor, Node, and Metastasis classification developed by the American Joint Committee on Cancer.17 Cancers were categorized as adenocarcinoma, squamous cell carcinoma, large-cell carcinoma, and other histologic types by using International Classification of Diseases-O-2 morphology codes provided by SEER. The burden of comorbidities was estimated according to the adaptation by Deyo et al.18 of Charlson’s index using inpatient and outpatient Medicare claims; the total comorbidity score was calculated applying lung cancer–specific weights.
We used Medicare claims to identify the use of diagnostic and staging procedures (bronchoscopy, fine-needle aspiration, positron emission tomography scan, or mediastinoscopy) as well as preoperative testing (ventilation perfusion scans and/or cardiac stress testing). The Home Health Agency file includes information regarding the use of home services among Medicare beneficiaries. As these services (skilled-nursing care, home health aide, physical therapy, speech therapy, occupational therapy, and medical social services) are limited to homebound patients, we used these claims as indicators of poor performance status.
Patients who underwent segmectectomy were identified using SEER data (surgical code 22); use of VATS was determined from physician claims (Current Procedural Terminology [CPT]-4 code: 32663). Data on postoperative radiotherapy use were obtained from SEER and Medicare records;19 chemotherapy treatment was ascertained from Medicare impatient, physician, and outpatient claims by applying validated algorithms.20
Information about surgeons performing these segmentectomies was obtained from the Physician Masterfile maintained by the American Medical Association (AMA). The AMA database includes information about the physician’s age, sex, type of practice (private versus government or academic), and practice specialty (thoracic surgeon versus others also available in Medicare claims).21 Physician-specific procedure volume was ascertained from Medicare billing claims. These data were used to rank surgeons into quartiles according to their average volume of claims for all types of lung cancer resections.22
Study outcomes included postoperative complications defined as respiratory complications, extrapulmonary infections, cardiovascular complications, thromboembolic events, and need for transfusions within 30 days of surgery.23 Postoperative need for intensive care monitoring was determined using inpatient Medicare files. Patients requiring more than 14 days of inpatient care after surgery were classified as having a prolonged hospitalization.23 Finally, perioperative mortality was defined as any death within 30 days of surgery as reported by Medicare.24
Overall survival was calculated as the period of time since the date of surgery to the date of death or last follow-up available in Medicare (December 31, 2009). Lung cancer–specific survival was determined by using cause of death information provided by SEER (obtained from death certificates); these analyses used a censoring date of December 31, 2007.
Baseline sociodemographic and tumor characteristics of patients treated with VATS versus open segmentectomy were compared with a t-test or χ2 test, as indicated. We used generalized estimation equation models to compare the surgeon characteristics while accounting for the correlated nature of the data as some providers performed multiple resections.
We used propensity score methods to adjust for potential selection bias in the use of VATS versus open segmentectomy.25 We fitted a logistic regression model that predicted the use of VATS segmentectomy based on baseline patient characteristics (sociodemographic factors, tumor characteristics, diagnostic and staging workup, and use of home services). Once the final model was developed, we estimated the probability for each patient to undergo VATS resection based on his or her preoperative characteristics and evaluated whether the distribution of these covariates were well balanced across groups after adjusting for propensity scores.
We estimated the rates of surgical complications among patients treated with VATS versus open segmentectomy and calculated unadjusted odds ratios [ORs] with 95% confidence intervals (CIs). Of 577 patients in the study, we were able to match 537 (93%) to AMA records containing information about surgeon characteristics. Of note, surgical specialty and provider volume were available for all patients as these data are provided or estimated based on Medicare claims. We conducted two adjusted analyses; first, we evaluated the adjusted odds of complications after controlling for propensity scores (i.e., summarizing baseline patient characteristics) using logistic regression analyses. Then, we used a generalized mixed linear model (logit link) to compare the odds of complications among patients treated with VATS versus open segmentectomy after adjusting for propensity scores and physician factors.
We used Cox regression analyses to assess the hazard of all cause and lung cancer–specific mortality after controlling for propensity scores. To confirm these findings, we conducted secondary analyses stratifying the sample into five propensity score quintiles and matching VATS and open segmentectomy patients based on their propensity score values. We then repeated these comparisons also adjusting for physician characteristics; these analyses were performed using a Cox model for correlated data.26 Finally, we conducted analyses adjusting for year of diagnosis to control for potential time trends in the use of other lung cancer treatments.
On the basis of the number of stage I patients treated with segmentectomy in SEER-Medicare, we estimated that the study had 80% or more power to detect a 10% difference in the rates on any postoperative complications among the two study groups. The study was also powered to detect an approximately 35% increase in the risk of death among VATS-treated patients. All analyses were conducted with SAS statistical software (SAS Statistical Institute, Cary, NC) using two-sided p values and a 0.05 significance level. The study was considered exempt by the Icahn School of Medicine at Mount Sinai Institutional Review Board and therefore did not require a full review.
We identified 577 stage I NSCLC patients in the SEER-Medicare database who were treated with segmentectomy between 1994 and 2007. Of these, 27% (n=153) underwent VATS resection. Baseline patient and physician characteristics of patients treated with VATS versus open segmentectomy are shown in Table 1. On average, VATS-treated patients were older (p=0.007), more likely to be white (p=0.001), had higher estimated income (p<0.0001), and a lower number of comorbidities (p=0.04). In terms of tumor characteristics, patients who underwent VATS were more likely to have T1a cancers (p=0.008) and adenocarcinomas (p=0.03). The number of lymph nodes removed (p=0.16) as well as the use of adjuvant chemotherapy (p=0.78) or postoperative radiotherapy (p=0.09) was not significantly different across study groups.
Surgeons performing VATS segmentectomies were, on average younger (p<0.001); however, there were no significant differences in the distribution of other physician characteristics such as sex (p=0.68), practice setting (p=0.70), or thoracic surgery certification (0.07). VATS segmentectomies were mostly performed by high-volume surgeons (p<0.001). The distribution of baseline patient characteristics was well balanced among patients who underwent VATS versus open segmentectomy after adjusting for propensity scores (Table 1).
Overall, 39.2% of patients treated with open resection had at least one surgical complication compared with 26.1% of VATS-treated patients (OR: 0.55, 95% CI: 0.37–0.83; Table 2). The most common postoperative problem was respiratory complications; this was not significantly different between the two groups (OR: 0.68, 95% CI: 0.44–1.04). Extrapulmonary infections (OR: 0.33, 95% CI: 0.11–0.95) were less frequent among patients who underwent VATS; there were no significant differences in the distribution of other complications. VATS-treated patients were less likely to require intensive care unit admission (OR: 0.18, 95% CI: 0.12–0.28) or to have an extended hospital stay (OR: 0.41, 95% CI: 0.21–0.81). Perioperative mortality was not significantly different between groups (OR: 0.42, 95% CI: 0.09–1.87). Similar results were obtained in analyses adjusting for propensity scores. However, the distributions of all postoperative complications, requirement for intensive care unit admission, extended length of stay, and perioperative mortality were not significantly different between patients treated with VATS versus those treated with open segmentectomy after adjustment for surgeon characteristics. These results were confirmed in analyses adjusting for year of diagnosis.
Analyses adjusting for propensity scores showed that overall survival (hazard ratio: 0.80, 95% CI: 0.60–1.06) and lung cancer–specific survival (hazard ratio: 0.71, 95% CI: 0.45–1.12) was not significantly different for patients treated with VATS versus those treated with open segmentectomy (Table 3). Similar results were obtained in analyses stratifying as well as matching by propensity scores as well as in models adjusting for surgeon factors or year of diagnosis.
Intentional segmentectomy has been increasingly used to resect small (≤2 cm) stage I lung cancers, particularly in elderly patients. This surgical technique is also frequently performed in the treatment of lung cancer patients with limited cardiopulmonary reserve or other contraindications to full lobectomy. In this population-based study, we found that VATS and open segmentectomies are associated with similar rates of postoperative complications, but with equivalent oncologic outcomes. Most VATS procedures were performed by high-volume surgeons, a pattern that may explain, in part, the favorable outcomes associated with this technique in previously published single-center studies.12–15 These data suggest that VATS can be safely performed and may be an appropriate choice for the management of elderly patients with early-stage NSCLC who are undergoing limited resection.
Data from the Lung Cancer Study Group showed that early-stage lung cancer patients with tumors that were 3 cm or lesser in size who are treated with limited pulmonary resections (wedge and segmentectomy) have an increased risk of local recurrence (one sided p value 0.02).2 Since then, multiple observational studies from single centers, as well as data from a large registry study, have shown similar oncological outcomes after lobectomy and limited resections in patients with smaller (≤2 cm) NSCLCs.3–7 In terms of the type of limited resection, anatomic segmentectomy is associated with improved lung cancer survival compared with wedge resections.27 The potential indication of limited resections for small tumors is very relevant given the increased use of chest computed tomography, allowing for detection of early lung cancers. Moreover, the results of the recently completed National Lung Cancer Screening Trial suggest that low-dose computed tomography screening for lung cancer may become adopted in clinical care.28 As screen-detected cancers tend to be less than 1 cm in size and some may be less aggressive, limited resection may also provide an option to lobectomy for the treatment of these patients. Finally, lesser resections will continue to offer an alternative to radiotherapy or radiofrequency ablation for the management of patients who are poor candidates for full resection.
VATS lobectomy has emerged during the past two decades as an accepted alternative to open resection for patients with early-stage NSCLC. Several retrospective comparative studies have reported that VATS is associated with reduced pain and improved quality of life in the postoperative period, shorter length of hospital stay, and lower costs. The literature also suggests that risk of recurrence and lung cancer death are equivalent after either VATS or open lobectomy.9,10,29 However, there is limited information about the use of VATS segmentectomy for the treatment of lung cancer. Few studies comparing patients undergoing VATS versus open segmentectomy reported mixed results including either similar or decreased duration of chest tube use, hospital length of stay, postoperative complications, and costs.12–15 Rates of locoregional recurrence were similar in the two groups although one study showed improved long-term survival with VATS.13 However, these studies were conducted in single academic centers, reported outcomes of resections performed by a limited number of surgeons, enrolled relatively small numbers of patients, and included mixed diagnoses, such as with single lung metastasis.
Our study adds to the literature by reporting the outcomes of a relatively large, population-based sample of patients with stage I NSCLC treated with VATS versus open segmentectomy. Consistent with prior studies of patients undergoing lobectomy, we found that VATS segmentectomy was associated with lower rates of some postoperative complications and decreased the length of stay.12–15 However, we found considerable differences in the characteristics of providers performing these procedures; most VATS were done by high-volume surgeons. High surgical volume has been associated with decreased perioperative deaths30,31 and our adjusted analyses showed no significant differences in postoperative complications, suggesting that some of the advantages of VATS may be explained by provider factors. We also showed that VATS and open procedures are associated with similar long-term oncologic outcomes, including overall and lung cancer–specific survival.
The study has some strengths and limitations that are worth mentioning. The SEER registry includes information from all new lung cancer cases diagnosed in multiple geographic areas in the United States. Consequently, our results should be less affected by local practice patterns and the generalizability of our findings to other lung cancer patients should be high. Our cohort was relatively large compared with those of prior studies and we had long-term follow-up on these patients, ensuring sufficient statistical power to compare outcomes after VATS versus open resection. Despite this, the overall numbers of segmentectomies performed during the study period may seem low. However, the number of segmentectomies reported in this study is consistent with that in other recent studies evaluating the role of segmentectomy in patients with lung cancer.32–34 Our study was limited to patients aged 65 years or above, patients not enrolled in a health maintenance organization, and those with continuous part B (outpatient) coverage. These exclusion criteria allow for inclusion of the most comprehensive claims data. This analysis relies on the use of codes and claims in the SEER and Medicare databases that document the type of surgical procedure performed. Although there has been no systemic validation of these codes, we believe billing codes to be fairly accurate as they reflect the type of procedures surgeons believe they performed. In addition, there are potential legal ramifications for falsifying billing codes. Although SEER is a national, population-based registry that is highly generalizable, during the study period SEER collected information on approximately 25% of the U.S. population. This may contribute to the low numbers of reported segmentectomies in this study and in the literature. The type of surgical technique was not randomly assigned among study subjects, creating the possibility of selection bias. We used propensity score methods to balance the distribution of measured confounders; however, observational data do not provide the same level of evidence as a prospective trial on the equivalence of these procedures. We used validated algorithms to identify postoperative complications and other postoperative outcomes. However, we did not have detailed information on other relevant process measures such as duration of surgery, intraoperative blood loss, and duration of computed tomography use or clinically important patient-level outcomes including pain, lung function, or quality of life. Similarly, SEER does not capture information about the presence of locoregional recurrences. Thus, we were not able to compare differences in these outcomes among patients in the two study groups. Additional studies should also evaluate whether VATS procedures are associated with lower costs.
In summary, our study shows that VATS is an adequate approach to perform segmentectomy in stage I NSCLC patients. This technique seems to lead to similar postoperative and long-term outcomes when compared with open segmentectomy.
This study used the linked SEER-Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors. The authors acknowledge the efforts of the Applied Research Program, National Cancer Institute; the Office of Research, Development and Information, CMS; Information Management Services (IMS), Inc.; and the Surveillance, Epidemiology, and End Results (SEER) Program tumor registries in the creation of the SEER-Medicare database.
The work was supported by the Agency for Health Care Research and Quality [grant number: R01HS019670-01].
1. The NCCN Clinical Practice Guidelines in Oncology: Non-small cell lung cancer (Version V.I.2010).
2. Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg. 1995;60:615–22 discussion 622.
3. Kodama K, Doi O, Higashiyama M, Yokouchi H. Intentional limited resection for selected patients with T1 N0 M0 non-small-cell lung cancer: a single-institution study. J Thorac Cardiovasc Surg. 1997;114:347–353
4. Koike T, Togashi K, Shirato T, et al. Limited resection for noninvasive bronchioloalveolar carcinoma diagnosed by intraoperative pathologic examination. Ann Thorac Surg. 2009;88:1106–1111
5. Mery CM, Pappas AN, Bueno R, et al. Similar long-term survival of elderly patients with non-small cell lung cancer treated with lobectomy or wedge resection within the surveillance, epidemiology, and end results database. Chest. 2005;128:237–245
6. Warren WH, Faber LP. Segmentectomy versus lobectomy in patients with stage I pulmonary carcinoma. Five-year survival and patterns of intrathoracic recurrence. J Thorac Cardiovasc Surg. 1994;107:1087–93 discussion 1093.
7. Wisnivesky JP, Henschke CI, Swanson S, et al. Limited resection for the treatment of patients with stage IA lung cancer. Ann Surg. 2010;251:550–554
8. Keenan RJ, Landreneau RJ, Maley RH Jr, et al. Segmental resection spares pulmonary function in patients with stage I lung cancer. Ann Thorac Surg. 2004;78:228–33 discussion 228.
9. Flores RM, Park BJ, Dycoco J, et al. Lobectomy by video-assisted thoracic surgery (VATS) versus thoracotomy for lung cancer. J Thorac Cardiovasc Surg. 2009;138:11–18
10. Nicastri DG, Wisnivesky JP, Litle VR, et al. Thoracoscopic lobectomy: report on safety, discharge independence, pain, and chemotherapy tolerance. J Thorac Cardiovasc Surg. 2008;135:642–647
11. Swanson SJ, Herndon JE 2nd, D’Amico TA, et al. Video-assisted thoracic surgery lobectomy: report of CALGB 39802–a prospective, multi-institution feasibility study. J Clin Oncol. 2007;25:4993–4997
12. Schuchert MJ, Pettiford BL, Pennathur A, et al. Anatomic segmentectomy for stage I non-small-cell lung cancer: comparison of video-assisted thoracic surgery versus open approach. J Thorac Cardiovasc Surg. 2009;138:1318–25.e1
13. Atkins BZ, Harpole DH Jr, Mangum JH, Toloza EM, D’Amico TA, Burfeind WR Jr. Pulmonary segmentectomy by thoracotomy or thoracoscopy: reduced hospital length of stay with a minimally-invasive approach. Ann Thorac Surg. 2007;84:1107–12 discussion 1112.
14. Leshnower BG, Miller DL, Fernandez FG, Pickens A, Force SD. Video-assisted thoracoscopic surgery segmentectomy: a safe and effective procedure. Ann Thorac Surg. 2010;89:1571–1576
15. Shiraishi T, Shirakusa T, Iwasaki A, Hiratsuka M, Yamamoto S, Kawahara K. Video-assisted thoracoscopic surgery (VATS) segmentectomy for small peripheral lung cancer tumors: intermediate results. Surg Endosc. 2004;18:1657–1662
16. Warren JL, Klabunde CN, Schrag D, et al. Overview of the SEER-Medicare data: content, research applications, and generalizability to the United States elderly population. Med Care. 2002;40:IV-3–18
17. Rami-Porta R, Crowley JJ, Goldstraw P. The revised TNM staging system for lung cancer. Ann Thorac Cardiovasc Surg. 2009;15:4–9
18. Deyo RA, Cherkin DC, Ciol MA. Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol. 1992;45:613–619
19. Virnig BA, Warren JL, Cooper GS, Klabunde CN, Schussler N, Freeman J. Studying radiation therapy using SEER-Medicare-linked data. Med Care. 2002;40(8 Suppl):IV–49
20. Warren JL, Harlan LC, Fahey A, et al. Utility of the SEER-Medicare data to identify chemotherapy use. Med Care. 2002;40(8 Suppl):IV–55
21. Baldwin LM, Adamache W, Klabunde CN, Kenward K, Dahlman C, L Warren J. Linking physician characteristics and medicare claims data: issues in data availability, quality, and measurement. Med Care. 2002;40(8 Suppl):IV–82
22. Schrag D, Earle C, Xu F, et al. Associations between hospital and surgeon procedure volumes and patient outcomes after ovarian cancer resection. J Natl Cancer Inst. 2006;98:163–171
23. Shapiro M, Mhango G, Kates M, et al. Extent of lymph node resection does not increase perioperative morbidity and mortality after surgery for stage I lung cancer in the elderly. Eur J Surg Oncol. 2012;38:516–522
24. Kates M, Perez X, Gribetz J, Swanson SJ, McGinn T, Wisnivesky JP. Validation of a model to predict perioperative mortality from lung cancer resection in the elderly. Am J Respir Crit Care Med. 2009;179:390–395
25. Rubin DB. Estimating causal effects from large data sets using propensity scores. Ann Intern Med. 1997;127(8 Pt 2):757–763
26. Wei LJ, Lin DY, Weissfeld L. Regression Analysis of Multivariate Incomplete Failure Time Data by Modeling Marginal Distributions. Journal of the American Statistical Association. 1989;84:1065–1073
27. Smith CB, Swanson SJ, Mhango G, Wisnivesky JP. Survival after segmentectomy and wedge resection in stage I non-small-cell lung cancer. J Thorac Oncol. 2013;8:73–78
28. Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. New Engl J Med. 2011;365:395–409
29. Whitson BA, Groth SS, Duval SJ, Swanson SJ, Maddaus MA. Surgery for early-stage non-small cell lung cancer: a systematic review of the video-assisted thoracoscopic surgery versus thoracotomy approaches to lobectomy. Ann Thorac Surg. 2008;86:2008–16 discussion 2016.
30. Birkmeyer JD, Stukel TA, Siewers AE, Goodney PP, Wennberg DE, Lucas FL. Surgeon volume and operative mortality in the United States. N Engl J Med. 2003;349:2117–2127
31. Birkmeyer JD, Sun Y, Goldfaden A, Birkmeyer NJ, Stukel TA. Volume and process of care in high-risk cancer surgery. Cancer. 2006;106:2476–2481
32. Whitson BA, Groth SS, Andrade RS, Mitiek MO, Maddaus MA, D’Cunha J. Invasive adenocarcinoma with bronchoalveolar features: a population-based evaluation of the extent of resection in bronchoalveolar cell carcinoma. J Thorac Cardiovasc Surg. 2012;143:591–600.e1
33. Whitson BA, Groth SS, Andrade RS, Maddaus MA, Habermann EB, D’Cunha J. Survival after lobectomy versus segmentectomy for stage I non-small cell lung cancer: a population-based analysis. Ann Thorac Surg. 2011;92:1943–1950
34. Smith CB, Swanson SJ, Mhango G, Wisnivesky JP. Survival after segmentectomy and wedge resection in stage I non-small-cell lung cancer. J Thorac Oncol. 2013;8:73–78
Video-assisted thoracic surgery; Segmentectomy; Lung cancer; Outcomes; Comparative effectiveness
Copyright © 2014 by the European Lung Cancer Conference and the International Association for the Study of Lung Cancer.
Highlight selected keywords in the article text.