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Original Research: LUNG CANCER |

Survival Following Lobectomy and Limited Resection for the Treatment of Stage I Non-small Cell Lung Cancer ≤ 1 cm in Size: A Review of SEER Data FREE TO VIEW

Max Kates, BA; Scott Swanson, MD; Juan P. Wisnivesky, MD, DrPH
Author and Funding Information

From the Mount Sinai School of Medicine (Mr Kates) and the Divisions of General Internal Medicine and Pulmonary, Critical Care, and Sleep Medicine (Dr Wisnivesky), Mount Sinai School of Medicine, New York, NY; and the Division of Thoracic Surgery (Dr Swanson), Brigham and Women’s Hospital, Boston, MA.

Correspondence to: Juan P. Wisnivesky, MD, DrPH, Department of Medicine, Mount Sinai School of Medicine, One Gustave L. Levy Place, Box 1087, New York, NY 10029; e-mail: juan.wisnivesky@mssm.edu


For editorial comment see page 481.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (http://www.chestpubs.org/site/misc/reprints.xhtml).


© 2011 American College of Chest Physicians


Chest. 2011;139(3):491-496. doi:10.1378/chest.09-2547
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Published online

Background:  Although lobectomy is the standard treatment for stage I non-small cell lung cancer (NSCLC), recent studies have suggested that limited resection may be a viable alternative for small-sized tumors. The objective of this study was to compare survival after lobectomy and limited resection among patients with stage IA tumors ≤ 1 cm by using a large, US-based cancer registry.

Methods:  Using the Surveillance, Epidemiology, and End Results (SEER) registry, we identified 2,090 patients with stage I NSCLC ≤ 1 cm in size who underwent lobectomy or limited resection (segmentectomy or wedge resection). We used propensity score analysis to adjust for potential differences in the baseline characteristics of patients in the two treatment groups. Overall and lung cancer-specific survival rates of patients undergoing lobectomy vs limited resection were compared in stratified and adjusted analyses, controlling for propensity scores.

Results:  Overall, 688 (33%) patients underwent limited resection. For the entire cohort, we were not able to identify a difference in outcomes among patients treated with lobectomy vs limited resection, as demonstrated by an adjusted hazard ratio (HR) for overall survival (1.12; 95% CI, 0.93-1.35) and lung cancer-specific survival (HR, 1.24; 95% CI, 0.95-1.61). Similarly, when the cohort was divided into propensity score quintiles, we did not find a difference in survival rate between the two groups.

Conclusions:  Limited resection and lobectomy may lead to equivalent survival rates among patients with stage I NSCLC tumors ≤ 1 cm in size. If confirmed in prospective studies, limited resection may be preferable for the treatment of small tumors because it may be associated with fewer complications and better postoperative lung function.

For patients with stage IA non-small cell lung cancer (NSCLC), lobectomy with mediastinal lymph node dissection is considered the standard therapy, with 5-year survival rates of up to 70%.1 However, although lobectomy is the best available therapy for these patients, the procedure can be associated with considerable morbidity and mortality, particularly among the elderly and patients with multiple comorbidities or poor lung function.2

When making decisions regarding which type of resection to recommend, surgeons must balance the potential long-term benefits of more extensive resections with the risks of perioperative complications and mortality, decreased postoperative lung function, and potential limited ability to resect any future new primary lung cancers that may develop.3,4 For small, localized tumors, there is controversy as to whether limited resections (segmentectomy or wedge resection) can be used to achieve long-term outcomes that are similar to lobectomy. Current recommendations for lobectomy over limited resection for tumors ≤ 3 cm in size are based on the results of a single, randomized controlled trial (RCT) of 267 stage IA patients.5 More recently, these results have been challenged by several retrospective studies that suggest that limited resection may be equally effective for the treatment of stage IA tumors ≤ 2 cm, particularly among elderly patients.6-10 However, limited resection may not be an adequate alternative for younger patients with small tumors, given that these patents have a longer life expectancy and consequently are at higher risk of tumor recurrence.11 Although controversy still surrounds tumors in the 2-to-3-cm range, tumors ≤ 1 cm in size are more likely to be localized; thus, it is appealing to consider using a more limited surgical approach regardless of the patient’s age. Data from a single institution study including patients with tumors ≤ 1 cm in size showed equivalence in outcomes after limited resection and lobectomy.12 However, these results have yet to be validated in other cohorts. The aim of this study was to compare the survival of patients with stage IA NSCLC ≤ 1 cm in size after lobectomy or limited resection in a large, US-based cancer registry.

Patients were selected from the Surveillance, Epidemiology, and End Results (SEER) program, which has collected clinicopathologic data on all incident cancer cases in specified geographic areas of the United States since 1972. The SEER program is a population-based cancer registry sponsored by the National Cancer Institute that routinely collects information on the incidence and survival rates of cancer in 18 areas of the United States. The SEER population is highly representative in terms of geography, socioeconomic status, race/ethnicity, and age. Between 1988 and 2005, the included regions represented approximately 14% to 26% of the US population. We selected all patients with histologically confirmed stage IA NSCLC diagnosed between 1988 and 2005 who were not identified from autopsy or death certificate data. The analysis included all patients with tumor size ≤ 1 cm who underwent lobectomy (SEER codes 30-31) or limited resection (segmental or wedge resection; SEER codes 20-22).

Sociodemographic data, including age, sex, race, ethnicity, and marital status, were obtained from SEER. Cases were classified according to the criteria of the American Joint Committee on Cancer.13 Tumor site (upper/middle/lower lobe) and histology (adenocarcinoma, bronchoalveolar carcinoma, squamous, large cell carcinoma, or other) were obtained from SEER. The number of lymph nodes sampled was also obtained from SEER, as was use of postoperative radiotherapy. Overall and lung cancer-specific survival was determined as the interval from the date of cancer diagnosis to the date of death reported in the registry. Those surviving past December 31, 2005, were classified as censored (alive at the end of follow-up). For the analysis using lung-cancer-specific survival, deaths from causes other than lung cancer were treated as censored observations. The cause of death was coded using SEER data, which were obtained from death certificates.

Statistical Analysis

Differences in distribution of sex, age, race/ethnicity, marital status, number of lymph nodes resected, tumor location, histology, and treatment with postoperative radiotherapy between patients who underwent lobectomy or limited resection were evaluated using the χ2 test. We used a propensity score analysis to minimize potential biases caused by the nonrandom assignment of patients to lobectomy vs limited resection. The propensity score is the probability of being assigned to a treatment group (ie, limited resection or lobectomy), based on the patient’s baseline sociodemographic and tumor characteristics.14-16 To estimate the propensity of undergoing limited resection, we used a logistic regression model that included age, sex, race/ethnicity, marital status, tumor location, and histology as covariates. After this model was fitted, we used multiple regression analysis to test whether, after adjusting for the estimated propensity scores, the patient’s baseline characteristics were well balanced across the two treatment groups.

A Cox proportional hazards model was used to compare overall and lung-cancer-specific survival of patients who underwent limited resection vs lobectomy. First, propensity scores were included as a covariate in a Cox model, and survival of patients who underwent limited resection vs lobectomy were assessed using data from the entire cohort. Second, we stratified patients into quintiles based on their propensity scores and compared the survival of patients treated with limited resection or lobectomy using a Cox model within each propensity score quintile. Prior studies show similar results with limited resection in the elderly but there are fewer data available for younger patients, who may have a higher risk of recurrence. Thus, we performed secondary analyses stratifying the sample according to the patient’s age (≤ 70 vs ≥ 70 years). All the Cox models were adjusted for the number of lymph nodes sampled, a variable that influences survival but was not included in the propensity score model because it is not a preoperative characteristic.17 We tested the assumption of proportionality of hazards using a log-log survival plot.

Based on the number of deaths observed among patients in the entire cohort, we estimated that the study had an 80% power to detect an increased hazard of death among patients treated with limited resection of 1.25 at a 0.05 significance level. Analyses were performed using SAS software (SAS Institute; Cary, North Carolina). The study was reviewed by Mount Sinai School of Medicine’s institutional review board and classified as exempt.

The analysis included 2,090 patients with stage I NSCLC ≤ 1 cm in size. Of these, 688 (33%) underwent limited resection. The median follow-up time for the entire cohort was 37 months; the minimal follow-up (for patients diagnosed in December 2004) was 1 year. Patients ≤ 60 years of age had a median follow-up time of 44 months, compared with 38 months for patients 60 to 70 years of age, and 31 months for patients > 70 years of age. Overall, 1,351 patients (64%) were alive at the end of the study period (December 31, 2005) and thus, were treated as censored observations in the survival analysis. Baseline characteristics are reported in Table 1. Limited resection was more likely to be performed on older patients (P < .001), women (P < .049), and those who were unmarried (P < .001). Additionally, lower lobe tumors (P < .001) and adenocarcinomas (P < .001) were more likely to be treated with limited resections. Patients undergoing limited resection were more likely to have a lower number of lymph nodes sampled (P < .001) and were more likely to have postoperative radiation therapy (P < .001). All covariates were balanced among patients treated with limited resection and lobectomy after adjusting for propensity scores (P values > .39 for all comparisons) (Table 1).

Table Graphic Jump Location
Table 1 —Baseline Characteristics of Patients in the SEER Registry With ≤ 1 cm Stage I NSCLC Who Underwent Limited Resection or Lobectomy, 1988-2005

NSCLC = non-small cell lung cancer; SEER = Surveillance, Epidemiology, and End Results.

a 

P values for analysis adjusting for propensity scores are shown.

b 

Number of lymph nodes resected is not a preoperative factor because this occurs during or after the surgery. Thus, they are not included in the propensity score model because they should not influence the decision to perform limited resection vs lobectomy.

Using Cox regression analysis and adjusting for propensity scores, we could not identify a difference in overall survival rates between patients who received lobectomy vs limited resection (hazard ratio [HR], 1.12; 95% CI, 0.93-1.35) (Table 2). Similarly, we did not find a significant difference in survival rates in secondary analyses using lung-cancer-specific survival (HR, 1.24; 95% CI, 0.95-1.61). When the cohort was divided into propensity score quintiles, with the exception of the second quintile, we could not confirm a difference in survival rates among patients who underwent either surgical procedure (HR range, 0.81-1.82). In secondary analyses stratified by age, we did not find a significant association between type of surgery and overall survival (HR, 1.26; 95% CI, 0.99-1.61) or lung-cancer-specific survival rates (HR, 1.44; 95% CI, 0.96-2.17) among patients < 70 years of age. Similarly, for patients ≥ 70 years of age, we could not confirm a difference in overall (HR, 0.99; 95% CI, 0.74-1.33) and lung-cancer-specific (HR, 1.19; 95% CI, 0.84-1.67) survival rates across treatment groups.

Table Graphic Jump Location
Table 2 —Results of Propensity Score Analysis Comparing Survival Rates of Patients Treated With Limited Resection vs Lobectomy

All models were adjusted for the number of lymph nodes sampled during surgery. HR = hazard ratio.

a 

Quintiles represent patients grouped on the basis of propensity scores.

Although it has been reported previously that patients with small-sized stage IA NSCLC can undergo resections of less than one lobe without leading to worse survival outcomes, controversy still remains regarding the treatment of choice for these tumors. In this study, we did not find a significant difference in survival among patients with stage IA NSCLC ≤ 1 cm in size treated with lobectomy vs limited resection. Our findings suggest that limited resection may be considered for the treatment of tumors ≤ 1 cm in size, because the literature shows that limited procedures are associated with less morbidity and preserve more lung parenchyma.1,3 These results should be confirmed in prospective clinical trials.

With the widespread use of CT imaging and the possible implementation of lung cancer screening programs, tumors are being identified at earlier stages and smaller sizes than ever before. This trend places a burden on the surgeon, because concerns regarding short- and long-term complications from the resection take on a greater role with small tumors, which may have a lower risk of recurrence.1821 In general, surgeons are concerned about performing a more conservative operation to treat patients with lung cancer who are otherwise good surgical candidates. Thus, limited resection is currently reserved for patients with poor lung function or multiple comorbidities, who may not tolerate a more extensive surgery. However, for elderly patients, some studies and surgeons favor more limited treatments, given concerns about perioperative mortality with lobectomy. A study by Mery et al,18 which also used SEER data, showed that patients > 75 years of age with tumors ≤ 3 cm in size had similar survival rates after limited resection or lobectomy, suggesting that these procedures may be equivalent in the elderly. A study using the SEER-Medicare registry also showed similar survival rates among elderly patients with tumors ≤ 2 cm in size treated with limited resection or lobectomy.10 Unlike these prior studies, which focused on older patients, our data included patients of all ages.

The lack of an association between the type of resection and survival found in this study is consistent with some prior studies that included patients with larger tumors. Okada and colleagues22 analyzed 1,272 consecutive patients undergoing NSCLC surgery in their institution and found that for tumors ≤ 2 cm in size lobectomy had no survival advantage over segmentectomies. Other single-institution studies of smaller tumors have similarly not found a difference in survival with lobectomy.6,8 However, along with collecting data from single institutions, most of these studies did not use advanced methods to control for selection bias. The only study that evaluated survival rates after limited resection vs lobectomy in 100 patients with tumors ≤ 1 cm in size did not find a significant difference in mortality.12 Similarly, we were not able to confirm a difference in survival rate between limited resection and lobectomy among patients with NSCLC ≤ 1 cm in size in a large representative sample of the general population; thus, this study extends the results of previous analyses.

Currently, the equivalence of limited resection and lobectomy for early NSCLC is being investigated in two RCTs. In the United States, an RCT began in 2007 that will enroll 1,300 patients with NSCLC tumors ≤ 2 cm in size who have been assigned to lobectomy vs limited resection.23 In Japan, an ongoing study is enrolling patients with adenocarcinomas ≤ 2 cm in size with a predominant solid component on chest CT scan and comparing lobectomy vs limited resection in that subgroup.23 Our data did not find a difference among patients with tumors ≤ 1 cm in size, and thus may provide an impetus for physicians to enroll eligible patients into these studies. Because randomized trials use strict inclusion criteria to select patients, this observational study can help generalize the results of these RCTs to broader populations of patients with NSCLC.

There are several strengths and limitations of this study that should be noted. Because SEER is a nationally representative population, the generalizability of our findings should be quite good and should be less susceptible to referral patterns and other potential biases of single-institution studies. Geographic regions included in SEER encompass varying levels of urbanization, income strata, and education, and thus mirror the diversity of the general US population. Participating areas have demonstrated levels of ascertainment as high as 98%, showing that most eligible cases are captured in the registry.

The SEER registry obtains information regarding the cause of death from death certificates. Despite the fact that death certificate information is a unique source of information on incidence, prevalence, and mortality, studies have questioned the reliability of death certificates in correctly attributing cause of death.24 However, the underlying cause of death among patients with lung cancer has been found to be > 90% accurate in a large registry.25 The SEER registry does not contain information regarding comorbidities and pulmonary function, two factors that play a role in the selection of surgical treatment of lung cancer. However, patients who undergo limited resection tend to have worse comorbidities and poorer lung function; thus, our results should be conservative. Additionally, information regarding surgical technique (video assisted vs open procedures) and perioperative morbidity and mortality were not available in SEER. Thus, we could not assess if there are differences in the perioperative outcomes of patients undergoing minimally invasive incisional approaches vs thoracotomy.

In summary, our results suggest that there are similar survival rates among patients receiving limited resection vs lobectomy for ≤ 1 cm stage IA tumors, regardless of age. When our findings are viewed along with previously reported data demonstrating that limited resection is associated with fewer postoperative complications and better lung function, it would seem that limited resection may be preferable for tumors ≤ 1 cm in size, when technically possible. However, for a definitive recommendation, these findings should be confirmed in RCTs, particularly those that allow for longer follow-up of younger patients, possibly in conjunction with a comparison of less-invasive operative techniques.

Author contributions:Mr Kates: contributed to the scope and design of the study and to the research concept, obtaining permissions for data use, analyzing and interpreting the data, and drafting and revising the manuscript.

Dr Swanson: contributed to interpreting the data and revising the manuscript.

Dr Wisnivesky: contributed to the scope and design of the study, analyzing and interpreting the data, and drafting and revising the manuscript.

Financial/nonfinancial disclosures: The authors have reported to CHEST the following conflicts of interest: Dr Wisnivesky received a grant for a COPD study from GlaxoSmithKline and lecture fees from Novartis, and serves on the research advisory board for EHE International. Mr Kates and Dr Swanson have reported that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

HR

hazard ratio

NSCLC

non-small cell lung cancer

RCT

randomized controlled trial

SEER

Surveillance, Epidemiology, and End Results

Strand TE, Rostad H, Møller B, Norstein J. Survival after resection for primary lung cancer: a population based study of 3211 resected patients. Thorax. 2006;618:710-715. [CrossRef] [PubMed]
 
Little AG, Rusch VW, Bonner JA, et al. Patterns of surgical care of lung cancer patients. Ann Thorac Surg. 2005;806:2051-2056. [CrossRef] [PubMed]
 
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;781:228-233. [CrossRef] [PubMed]
 
Landreneau RJ, Sugarbaker DJ, Mack MJ, et al. Wedge resection versus lobectomy for stage I (T1 N0 M0) non-small-cell lung cancer. J Thorac Cardiovasc Surg. 1997;1134:691-698. [CrossRef] [PubMed]
 
Ginsberg RJ, Rubinstein LV. Lung Cancer Study Group Lung Cancer Study Group Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Ann Thorac Surg. 1995;603:615-622-. [CrossRef] [PubMed]
 
El-Sherif A, Gooding WE, Santos R, et al. Outcomes of sublobar resection versus lobectomy for stage I non-small cell lung cancer: a 13-year analysis. Ann Thorac Surg. 2006;822:408-415. [CrossRef] [PubMed]
 
Okada M, Koike T, Higashiyama M, Yamato Y, Kodama K, Tsubota N. Radical sublobar resection for small-sized non-small cell lung cancer: a multicenter study. J Thorac Cardiovasc Surg. 2006;1324:769-775. [CrossRef] [PubMed]
 
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;1074:1087-1094. [PubMed]
 
Nakamura H, Kawasaki N, Taguchi M, Kabasawa K. Survival following lobectomy vs limited resection for stage I lung cancer: a meta-analysis. Br J Cancer. 2005;926:1033-1037. [CrossRef] [PubMed]
 
Wisnivesky JP, Henschke CI, Swanson S, et al. Limited resection for the treatment of patients with stage IA lung cancer. Ann Surg. 2010;2513:550-554. [CrossRef] [PubMed]
 
Kraev A, Rassias D, Vetto J, et al. Wedge resection vs lobectomy: 10-year survival in stage I primary lung cancer. Chest. 2007;1311:136-140. [CrossRef] [PubMed]
 
Miller DL, Rowland CM, Deschamps C, Allen MS, Trastek VF, Pairolero PC. Surgical treatment of non-small cell lung cancer 1 cm or less in diameter. Ann Thorac Surg. 2002;735:1545-1551. [CrossRef] [PubMed]
 
Mountain CF. Revisions in the International System for Staging Lung Cancer. Chest. 1997;1116:1710-1717. [CrossRef] [PubMed]
 
Rubin DB, Thomas N. Matching using estimated propensity scores: relating theory to practice. Biometrics. 1996;521:249-264. [CrossRef] [PubMed]
 
Rubin DB. Estimating causal effects from large data sets using propensity scores. Ann Intern Med. 1997;1278 Pt 2:757-763. [PubMed]
 
D’Agostino RB Jr. Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med. 1998;1719:2265-2281. [CrossRef] [PubMed]
 
Ludwig MS, Goodman M, Miller DL, Johnstone PA. Postoperative survival and the number of lymph nodes sampled during resection of node-negative non-small cell lung cancer. Chest. 2005;1283:1545-1550. [CrossRef] [PubMed]
 
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;1281:237-245. [CrossRef] [PubMed]
 
Gajra A, Newman N, Gamble GP, Abraham NZ, Kohman LJ, Graziano SL. Impact of tumor size on survival in stage IA non-small cell lung cancer: a case for subdividing stage IA disease. Lung Cancer. 2003;421:51-57. [CrossRef] [PubMed]
 
Wisnivesky JP, Yankelevitz D, Henschke CI. The effect of tumor size on curability of stage I non-small cell lung cancers. Chest. 2004;1263:761-765. [CrossRef] [PubMed]
 
Harpole DH Jr, Herndon JE II, Young WG Jr, Wolfe WG, Sabiston DC Jr. Stage I nonsmall cell lung cancer. A multivariate analysis of treatment methods and patterns of recurrence. Cancer. 1995;765:787-796. [CrossRef] [PubMed]
 
Okada M, Nishio W, Sakamoto T, et al. Effect of tumor size on prognosis in patients with non-small cell lung cancer: the role of segmentectomy as a type of lesser resection. J Thorac Cardiovasc Surg. 2005;1291:87-93. [CrossRef] [PubMed]
 
Clinical Trials.gov. Bethesda, MD: National Institutes of Health; 1997. Comparison of different types of surgery in treating patients with stage IA non-small cell lung cancer.http://clinicaltrials.gov/ct2/show/NCT00499330?term=calgb+140503&rank=1. Accessed July 29, 2009.
 
Kircher T, Nelson J, Burdo H. The autopsy as a measure of accuracy of the death certificate. N Engl J Med. 1985;31320:1263-1269. [CrossRef] [PubMed]
 
Spira A, Ettinger DS. Multidisciplinary management of lung cancer. N Engl J Med. 2004;3504:379-392. [CrossRef] [PubMed]
 

Figures

Tables

Table Graphic Jump Location
Table 1 —Baseline Characteristics of Patients in the SEER Registry With ≤ 1 cm Stage I NSCLC Who Underwent Limited Resection or Lobectomy, 1988-2005

NSCLC = non-small cell lung cancer; SEER = Surveillance, Epidemiology, and End Results.

a 

P values for analysis adjusting for propensity scores are shown.

b 

Number of lymph nodes resected is not a preoperative factor because this occurs during or after the surgery. Thus, they are not included in the propensity score model because they should not influence the decision to perform limited resection vs lobectomy.

Table Graphic Jump Location
Table 2 —Results of Propensity Score Analysis Comparing Survival Rates of Patients Treated With Limited Resection vs Lobectomy

All models were adjusted for the number of lymph nodes sampled during surgery. HR = hazard ratio.

a 

Quintiles represent patients grouped on the basis of propensity scores.

References

Strand TE, Rostad H, Møller B, Norstein J. Survival after resection for primary lung cancer: a population based study of 3211 resected patients. Thorax. 2006;618:710-715. [CrossRef] [PubMed]
 
Little AG, Rusch VW, Bonner JA, et al. Patterns of surgical care of lung cancer patients. Ann Thorac Surg. 2005;806:2051-2056. [CrossRef] [PubMed]
 
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;781:228-233. [CrossRef] [PubMed]
 
Landreneau RJ, Sugarbaker DJ, Mack MJ, et al. Wedge resection versus lobectomy for stage I (T1 N0 M0) non-small-cell lung cancer. J Thorac Cardiovasc Surg. 1997;1134:691-698. [CrossRef] [PubMed]
 
Ginsberg RJ, Rubinstein LV. Lung Cancer Study Group Lung Cancer Study Group Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Ann Thorac Surg. 1995;603:615-622-. [CrossRef] [PubMed]
 
El-Sherif A, Gooding WE, Santos R, et al. Outcomes of sublobar resection versus lobectomy for stage I non-small cell lung cancer: a 13-year analysis. Ann Thorac Surg. 2006;822:408-415. [CrossRef] [PubMed]
 
Okada M, Koike T, Higashiyama M, Yamato Y, Kodama K, Tsubota N. Radical sublobar resection for small-sized non-small cell lung cancer: a multicenter study. J Thorac Cardiovasc Surg. 2006;1324:769-775. [CrossRef] [PubMed]
 
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;1074:1087-1094. [PubMed]
 
Nakamura H, Kawasaki N, Taguchi M, Kabasawa K. Survival following lobectomy vs limited resection for stage I lung cancer: a meta-analysis. Br J Cancer. 2005;926:1033-1037. [CrossRef] [PubMed]
 
Wisnivesky JP, Henschke CI, Swanson S, et al. Limited resection for the treatment of patients with stage IA lung cancer. Ann Surg. 2010;2513:550-554. [CrossRef] [PubMed]
 
Kraev A, Rassias D, Vetto J, et al. Wedge resection vs lobectomy: 10-year survival in stage I primary lung cancer. Chest. 2007;1311:136-140. [CrossRef] [PubMed]
 
Miller DL, Rowland CM, Deschamps C, Allen MS, Trastek VF, Pairolero PC. Surgical treatment of non-small cell lung cancer 1 cm or less in diameter. Ann Thorac Surg. 2002;735:1545-1551. [CrossRef] [PubMed]
 
Mountain CF. Revisions in the International System for Staging Lung Cancer. Chest. 1997;1116:1710-1717. [CrossRef] [PubMed]
 
Rubin DB, Thomas N. Matching using estimated propensity scores: relating theory to practice. Biometrics. 1996;521:249-264. [CrossRef] [PubMed]
 
Rubin DB. Estimating causal effects from large data sets using propensity scores. Ann Intern Med. 1997;1278 Pt 2:757-763. [PubMed]
 
D’Agostino RB Jr. Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med. 1998;1719:2265-2281. [CrossRef] [PubMed]
 
Ludwig MS, Goodman M, Miller DL, Johnstone PA. Postoperative survival and the number of lymph nodes sampled during resection of node-negative non-small cell lung cancer. Chest. 2005;1283:1545-1550. [CrossRef] [PubMed]
 
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;1281:237-245. [CrossRef] [PubMed]
 
Gajra A, Newman N, Gamble GP, Abraham NZ, Kohman LJ, Graziano SL. Impact of tumor size on survival in stage IA non-small cell lung cancer: a case for subdividing stage IA disease. Lung Cancer. 2003;421:51-57. [CrossRef] [PubMed]
 
Wisnivesky JP, Yankelevitz D, Henschke CI. The effect of tumor size on curability of stage I non-small cell lung cancers. Chest. 2004;1263:761-765. [CrossRef] [PubMed]
 
Harpole DH Jr, Herndon JE II, Young WG Jr, Wolfe WG, Sabiston DC Jr. Stage I nonsmall cell lung cancer. A multivariate analysis of treatment methods and patterns of recurrence. Cancer. 1995;765:787-796. [CrossRef] [PubMed]
 
Okada M, Nishio W, Sakamoto T, et al. Effect of tumor size on prognosis in patients with non-small cell lung cancer: the role of segmentectomy as a type of lesser resection. J Thorac Cardiovasc Surg. 2005;1291:87-93. [CrossRef] [PubMed]
 
Clinical Trials.gov. Bethesda, MD: National Institutes of Health; 1997. Comparison of different types of surgery in treating patients with stage IA non-small cell lung cancer.http://clinicaltrials.gov/ct2/show/NCT00499330?term=calgb+140503&rank=1. Accessed July 29, 2009.
 
Kircher T, Nelson J, Burdo H. The autopsy as a measure of accuracy of the death certificate. N Engl J Med. 1985;31320:1263-1269. [CrossRef] [PubMed]
 
Spira A, Ettinger DS. Multidisciplinary management of lung cancer. N Engl J Med. 2004;3504:379-392. [CrossRef] [PubMed]
 
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