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Original Research: CANCER |

Surgical Management and Outcomes of Elderly Patients With Early Stage Non-small Cell Lung CancerLung Cancer in the Elderly: Postoperative Outcomes: A Nested Case-Control Study FREE TO VIEW

Caroline Rivera, MD; Pierre-Emmanuel Falcoz, PhD; Alain Bernard, PhD; Pascal A. Thomas, PhD; Marcel Dahan, PhD
Author and Funding Information

From the Department of Thoracic Surgery (Dr Rivera), Haut Lévêque Hospital, University of Bordeaux, Bordeaux; Department of Thoracic Surgery (Dr Falcoz), Civil Hospital, University of Strasbourg, Strasbourg; Department of Thoracic Surgery (Dr Bernard), Bocage Hospital, University of Dijon, Dijon; Department of Thoracic Surgery (Dr Thomas), North Hospital, University of Marseille, Marseille; and Department of Thoracic Surgery (Dr Dahan), Larrey Hospital, University of Toulouse, Toulouse, France.

Correspondence to: Caroline Rivera, MD, Thoracic Surgery, Haut Lévêque Hospital CHU Bordeaux, Ave de Magellan 33604 Pessac, Bordeaux, France; e-mail: krorivera@yahoo.fr


Funding/support: The authors have reported to CHEST that no funding was received for this study.

For editorial comment see page 839

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;140(4):874-880. doi:10.1378/chest.10-2841
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Background:  The number of oncogeriatric patients with non-small cell lung cancer (NSCLC) is expected to increase in the next decades.

Methods:  We used the French Society of Thoracic and Cardiovascular Surgery database Epithor that includes information on > 140,000 procedures from 98 institutions. We prospectively collected data from January 2004 to December 2008 on 1,969 patients aged ≥ 70 years with NSCLC stage I or II and matched them with 1,969 control subjects aged < 70 years for sex, American Society of Anesthesia score, performance status, and FEV1. Surgical treatment and postoperative outcomes were compared between the two age groups.

Results:  The absence of radical lymphadenectomy was more frequent in the older patients (14%, n = 269) than in the younger patients (9%, n = 170) (P < .0001). There was no significant difference in type of resection between older and younger patients, respectively (pneumonectomy, 8% [n = 164] vs 11% [n = 216]; lobectomy, 79% [n = 1,559] vs 77% [n = 1,521]; bilobectomy, 4% [n = 88] vs 5% [n = 97]; sublobar resection, 7% [n = 143] vs 6% [n = 118]; P = .08). Differences in number (P = .07) and severity (P = .69) of complications were not significant. Postoperative mortality was higher in elderly patients at every end point (30-day mortality, 3.6% [n = 70] vs 2.2% [n = 43] [P = .01]; 60-day mortality, 4.1% [n = 80] vs 2.4% [n = 47] [P = .003]; 90-day mortality, 4.7% [n = 93] vs 2.5% [n = 50] [P = .0002]).

Conclusions:  Elderly patients with NSCLC should not be denied pulmonary resection on the basis of chronologic age alone. Among patients aged ≥ 70 years, 90-day mortality compared acceptably with mortality among younger matched patients. Additionally, the data show that for older patients, a 90-day mortality better represents their real mortality risk than 30- or 60-day figures. Our contemporary, multiinstitutional data importantly reveal that elderly patients, compared with their younger counterparts, do not have increased morbidity, incidence, or severity after pulmonary resection.

Figures in this Article

The geriatric population is expanding rapidly; thus, patients aged > 70 years with non-small cell lung cancer (NSCLC) are more commonly coming under the care of the oncologist and the thoracic surgeon.1 Widespread smoking cessation has produced two effects: decreased risk of death from coronary artery disease and a delay for the development of lung cancer.2 The elderly will continue to comprise a larger proportion of the population worldwide, and the number of oncogeriatric patients with NSCLC, subsequently, is expected to increase in the next decades.

Geriatric oncology is an important challenge. Elderly patients with cancer are significantly underrepresented in clinical studies, including those in lung cancer.3 Increasingly, elderly patients with NSCLC are being referred to thoracic surgeons for curative pulmonary resection.4 The life-limiting factor in these patients with early stage NSCLC is not age but, rather, the cancer.5 The benefits and the risks of surgical treatment in this subpopulation should be assessed. Therefore, an important need exists to thoroughly establish data regarding operative risks for elderly patients. The purpose of this study was to examine the modalities of the surgical treatment of patients aged ≥ 70 years with early stage NSCLC and to assess their postoperative morbidity and mortality, matching them to younger patients with similar characteristics.

Data Collection: Epithor

The French Society of Thoracic and Cardiovascular Surgery database Epithor was established in 2003 as a voluntary initiative of general thoracic surgeons. To date, this population-based registry includes > 140,000 procedures and is implemented daily by 98 private and public institutions. The methodology of this database has been previously described.68 The Institutional Review Board of the French Society of Thoracic and Cardiovascular Surgery approved the electronic prospective database used for this study as well as the study itself (approval number 2010-9-23-20-43-27-RiCa). Patient consent was obtained for entry into the database, and patients were aware that these data would be used for research purposes.

Patients

We prospectively collected data on 8,279 patients with NSCLC stage I or II who were operated on between January 2004 and December 2008. Seventy centers were effectively contributing to Epithor during this 5-year period. The study population comprised 1,969 patients aged ≥ 70 years. In order to compare patients with similar characteristics, we matched them to 1,969 younger patients for sex, American Society of Anesthesia score, performance status, and FEV1. The control subjects were randomized using a stratified sampling method from the 6,310 patients aged < 70 years in the national cohort.

Clinical Variables and Outcomes

Variables used to match elderly to younger patients were considered as categorical: sex, American Society of Anesthesia score (1 and 2, ≥ 3), performance status (0 and 1, ≥ 2), and FEV1 (≥ 60%, < 60%). We collected further data on BMI and number of comorbidities. The number of comorbid diseases per patient, considered as a categoric variable, was used because recent consistent data based on Epithor suggests the superiority of this variable on the types of individual comorbidities in a predictive model for in-hospital mortality.7 Lung cancer presentation also was detailed with histology and stage of primary bronchogenic neoplasm in accordance with the American Joint Committee on Cancer.9

To characterize surgical treatment, we reviewed the following variables: type of procedure (wedge resection or segmentectomy as sublobar resections, lobectomy, bilobectomy, pneumonectomy), type of mediastinal lymph node dissection (no lymph node dissection, sampling, radical lymphadenectomy), surgical approach (open thoracotomy, video-assisted thoracic surgery), and surgical resection margins (complete, R0; microscopically invaded, R1; macroscopically invaded, R2). Surgical outcome was based on perioperative data on hospital length of stay (LOS), morbidity, and postoperative mortality. On the one hand, the number of complications per patient was analyzed. On the other hand, we distinguished major complications from minor complications according to the classification system recently proposed by Seely and coworkers10 for severity of complications after thoracic surgery (e-Tables 1). Mortality rates were collected at 30, 60, and 90 postoperative days for all patients regardless of hospital discharge status.

Statistical Analysis

Statistical analyses were performed using the XLSTAT system with XLSTAT-Life extension for Microsoft Excel (Addinsoft SARL; Paris, France). We compared surgical treatment and outcomes between patients aged ≥ 70 years and younger control subjects. Binary and categoric variables were compared with χ2 test and continuous variables with unpaired t test.

In the present study, missing data on BMI (0.5%, n = 20), lymph node dissection (3.1%, n = 124), and LOS (0.6%, n = 24) were considered to be missing at random, assuming that the fact that the data were missing was not related to the true values of the missing data.11 We excluded them from the statistical analysis because of the small proportion they represented. We made no formal correction of the P values for multiple comparisons, but given the number of comparisons, the threshold of significance would likely be less than P = .02.

Patient Characteristics and Lung Cancer Presentation

We analyzed the data of 3,938 patients. The results are presented in Table 1. Among the elderly patients, mean (95% CI) age was 75.1 years (74.9-75.2) vs 58.8 years (58.5-59.1) in the control group. Older patients presented with a mean BMI of 25.7 kg/m2 (25.5-26.0), which was significantly higher than that in the younger patients (mean, 24.9 kg/m2; 95% CI, 24.7-25.1; P < .0001). The groups were otherwise similar for comorbidities (P = .26) and distribution of lung cancer stage (P = .13) (Table 1). Histologic subtypes were significantly different between the two age groups (P < .0001). There were more cases of adenocarcinoma (56.9%, n = 1,121) than squamous-cell carcinoma (35.6%, n = 700) in the younger group, whereas these subtypes were more equilibrated in the older group (48.5% [n = 954] and 45.1% [n = 888], respectively) (Table 1).

Table Graphic Jump Location
Table 1 —Patient Characteristics and Lung Cancer Presentation

Data are presented as mean (95% CI) or % (No.). ASA = American Society of Anesthesia.

Surgical Treatment

Management analysis showed that surgical procedures were not significantly different between elderly and younger patients (Table 2). The distribution of the different types of resections was comparable between the groups (P = .08). Sublobar resections were as frequent in elderly patients (7.3%, n = 143) as in younger patients (6.0%, n = 118). A majority of patients underwent radical mediastinal lymphadenectomy in the two groups (elderly patients, 86.0% [n = 1,646]; younger patients, 91.1% [n = 1,729]), but it was statistically more frequent in younger patients (P < .0001) (Table 2). The frequency of use of video-assisted thoracic surgery was exactly the same for both age groups (2.8%, n = 56). Finally, the distribution of surgical resection margins was comparable between the groups (P = .69). Incomplete resections accounted for < 2.5% in both groups (Table 2).

Table Graphic Jump Location
Table 2 —Surgical Treatment and Frequency of Sentinel Events

Data are presented as % (No.).

Hospital LOS

LOS was relatively long for both older patients (mean, 13.0 days; 95% CI, 12.6-13.4) and younger patients (mean, 12.3 days; 95% CI, 11.9-12.8), with P = .02. Median LOS may better represent the distribution of hospital LOS in the studied groups (Fig 1, Table 3). It was 11 days and 10 days for elderly and younger patients, respectively, with all types of pulmonary resections included.

Figure Jump LinkFigure 1. Hospital length of stay after pulmonary resection for early stage non-small cell lung cancer.Grahic Jump Location
Table Graphic Jump Location
Table 3 —Reported Postoperative Outcomes

Data are presented as mean % (No.), unless otherwise indicated. LOS = length of stay.

a 

No. complications per patient.

b 

Patients presenting with at least one major complication were considered patients with major complications and those presenting with at least one minor complication without any major complications were considered patients with minor complications.

c 

This variable represents the distribution of major and minor complications within patients presenting with at least one complication.

Morbidity

The results on morbidity are shown in Table 3. The number of complications per patient was not different between the two age groups (P = .07). The percentage of patients presenting one or more complications after pulmonary resection for early stage NSCLC was 40.0% (n = 788) for elderly patients and 36.3% (n = 714) for younger patients. In addition, we distinguished major complications from minor complications as described in e-Table 1 to address the different severity of the observed morbidity. The frequency of major complications was comparable between elderly patients (16.6%, n = 328) and younger patients (14.7%, n = 290), with P = .05 (Table 3). A further analysis was performed to determine the distribution of major and minor complications within the complications, taking into consideration patients presenting with at least one complication. We observed that the complications that arose in elderly patients were not more severe than those in younger patients (41.6% [n = 328] vs 40.6% [n = 290]; P = .69) (Table 3).

Postoperative Mortality

Mortality was analyzed to assess postoperative outcomes. The 30-day mortality after pulmonary resection for early stage NSCLC was 3.6% (n = 70) for elderly patients and 2.2% (n = 43) for younger patients (P = .01). The 60-day mortality rate was higher for elderly patients (4.1%, n = 80) than for younger patients (2.4%, n = 47) (P = .003). The number of patients who died within 90 postoperative days was also higher for elderly patients (4.7%, n = 93) than for younger patients (2.5%, n = 50) (P = .0002). Status at the time of hospital discharge was also available for all patients. Fifty elderly patients died before leaving the surgical department, and 20 younger patients died during hospital stay.

A further analysis was performed to determine whether the patients in the older group who died were those with major complications. We analyzed the distributions of deaths within 30, 60, and 90 postoperative days in patients who presented no complication, at least one minor complication (without major complication), and at least one major complication (Table 4). As expected, postoperative deaths were significantly more frequent in patients who presented with major complications in both patient groups (P < .0001). We compared these distributions of deaths between the two groups to determine whether major complications had more deadly consequences on elderly patients than on younger ones. We found no statistically significant difference in mortality between the groups at 30, 60, or 90 days postoperation (P > .02).

Table Graphic Jump Location
Table 4 —Distributions of Deaths Among Patients Presenting or Not Presenting With Postoperative Complications
a 

Patients presenting at least one major complication were considered “major complications” patients and patients presenting at least one minor complication without any major complication were considered ”minor complications” patients.

The number of elderly patients with lung cancer continues to grow, and as such, recent multicenter data regarding their operative risk is needed to construct an appropriate risk-benefit ratio for curative operative treatment. In this study, we used a national database, Epithor, that is representative of French surgeons’ habits reflecting the variability of surgical technique and postoperative management. In order to improve data quality in Epithor, patient data are recorded exclusively by means of pull-down menus to avoid disparities of data entry. In addition, multiple coherence tests are automatically carried out to warn the contributing center of any anomaly. Surgeons can check the quality of their data entry by comparison with national data through a quality score ranging from 0% to 100%. The exhaustive collection of the data also is monitored by the onsite quality audit that takes place in the departments involved in Epithor, checking data accuracy, filling rates, and interobserver variability.

Examining surgical treatment, we found that the distribution of the different types of pulmonary resections was similar in both study groups (P = .08). The fact that elderly patients get the same operations as identically staged younger patients is a change from older literature. Indeed, in a retrospective review of 14,555 patients included from 1992 to 1997 with NSCLC stage I or II from the Surveillance, Epidemiology, and End Results Registry (SEER), the frequency of limited resections increased with age, and the number of pneumonectomies and lobectomies decreased with age.12 Recent surgical literature is more optimistic about offering curative surgery to appropriately selected very elderly patients.1315 These data may have been incorporated into practices. In the present study, which had a similar population to that in the SEER study (NSCLC stage I and II) but also included patients between 2004 and 2008, frequencies of sublobar resections, pneumonectomies, and lobectomies were not different between patients aged ≥ 70 years and < 70 years. These results should be contrasted with our recently published descriptive study on all stages of lung cancer in octogenarians, in which we observed that very elderly patients underwent more sublobar resections than patients aged < 80 years.8

In the present study, elderly patients underwent significantly fewer radical mediastinal lymphadenectomy procedures (86.0%, n = 1,646) than younger patients (91.1%, n = 1,729, P < .0001). Mediastinal lymph node sampling seemed to be a more frequently used approach in elderly patients (10.7%, n = 205) than in younger patients (5.7%, n = 109). In fact, modality of lymph node dissection was already reported as a major difference in lung cancer surgical treatment in octogenarians.8

Reluctance to recommend surgery for elderly patients is partly based on the expectation that the rate of complications is higher in this group.14 Matching patients with similar characteristics, our nested case-control study allowed us to compare morbidity and mortality rates between the two age groups. The results on morbidity show that there was no obvious difference in number (P = .07) or severity (P = .69) of complications between elderly patients and their younger counterparts. This result is consistent with previously published data on morbidity in elderly patients after pulmonary resection.16 In addition, we noted that hospital LOS was about 1 day longer in patients aged ≥ 70 years (P = .02); this may be a clinically and fiscally significant difference. Nevertheless, it is notable that we did not observe any difference in morbidity related to this more prolonged hospital LOS.

Advanced age was shown to be a risk factor for mortality following thoracotomy in a 1983 multiinstitutional investigation of the Lung Cancer Study Group in which the 30-day postoperative mortality rate for patients aged > 70 years undergoing pulmonary resection was 7.1%, whereas the rate for patients aged < 60 years undergoing the same procedure was 1.3%.17 More recent data suggest that results have improved for patients ≥ 70, with 30-day mortality after lung resection ranging from 1.3% to 4.2%.1820 The present study results agree with these data: Mortality during the first postoperative month was higher for elderly patients (3.6%) than for younger patients (2.2%) (P = .01), but both rates remained relatively low. As far as we know, there are no consistent data published on 60-day and 90-day postoperative mortality after pulmonary resection in elderly patients. A recent study comparing different definitions of postoperative mortality after lung resection showed that 30-day mortality rates compared with 90-day mortality probably underestimate the consequences of the surgical procedure.21 In the present study, the difference observed in postoperative mortality between older and younger patients became more obvious and more important as we prolonged the postoperative period. Indeed, 90-day mortality was almost twice as high for elderly patients (4.6%) as for younger patients (2.5%), with a P value decreasing to .0002. Moreover, we observed a 30.6% increase in mortality in elderly patients from 30 to 90 postoperative days, whereas mortality in younger patients increased 13.6%.

The limited data on long-term follow-up is the main shortcoming of the Epithor database. Taking into account life expectancy, long-term survival is essential to the discussion of therapies for lung cancer in older individuals. Missing information in the database about detailed perioperative treatment22 and individual selection processes23 were limitations we could not overcome in this study. Similarly, disposition at the time of hospital discharge was not available. We did not know whether patients were discharged to a secondary convalescent care facility, whether they received home physical therapy, or whether they did not need further professional rehabilitation services. Considering the studied population, this bias could be an important one in LOS interpretation. Data on quality of life after pulmonary resection24 also is lacking in this study.

Despite the potential shortcomings, we believe that our findings are clinically useful. Surgical resection remains the treatment of choice for early stage NSCLC.17,25 There is a common perception that elderly patients will not tolerate surgical resection or will succumb to an illness other than lung cancer.23 However, as shown by Mery and coworkers,12 most deaths among patients in SEER with early staged NSCLC who did not undergo pulmonary resection were attributed to lung cancer across all age groups. Moreover, older patients seemed to be as likely as their younger counterparts to agree to cancer therapies for both curative and control purposes.27 The appropriateness of surgical treatment depends on the benefit to the patient. When treating elderly patients, decisions regarding the treatment strategy, therefore, must carefully balance the risks of postsurgical morbidity and mortality with those affecting cancer recurrence and long-term survival.

In conclusion, data from a large national database show that elderly patients did not present an increased risk of morbidity after pulmonary resection for early stage NSCLC. Furthermore, given the progression of mortality among the older cohort at the various intervals we studied (30, 60, and 90 days), the 90-day interval appears to be the most reflective of the postoperative mortality risk in patients aged ≥ 70 years.

Author contributions: Dr Rivera had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the analysis. She also confirmed that procedures were followed to an extent that convinced all authors that the results are valid and generalizable to a population similar to that enrolled in this study.

Dr Rivera: contributed to the conception and design of the study, data analysis and interpretation, drafting of the manuscript, and providing final approval of the version to be published.

Dr Falcoz: contributed to the conception and design of the study, data acquisition and interpretation, drafting the manuscript and revising it critically for important intellectual content, and providing final approval of the version to be published.

Dr Bernard: contributed to the data acquisition and interpretation, revising the manuscript critically for important intellectual content, and providing final approval of the version to be published.

Dr Thomas: contributed to the data acquisition and interpretation, revising the manuscript critically for important intellectual content, providing final approval of the version to be published.

Dr Dahan: contributed to the conception of the study, data acquisition and interpretation, drafting of the manuscript and revising it critically for important intellectual content, and providing final approval of the version to be published.

Other contributions: This work was performed at the French Society of Thoracic and Cardiovascular Surgery. We are grateful to all the French thoracic surgeons who participated in this study and have listed them in e-Appendix 1.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Role of sponsors: The Epithor database is the property of the French Society of Thoracic and Cardiovascular Surgery.

Additional information: The e-Table and e-Appendix can be found in the Online Supplement at http://chestjournal.chestpubs.org/content/140/4/874/suppl/DC1.

LOS

length of stay

NSCLC

non-small cell lung cancer

SEER

Surveillance, Epidemiology, and End Results Registry

Yancik R, Ries LA. Aging and cancer in America. Demographic and epidemiologic perspectives. Hematol Oncol Clin North Am. 2000;141:17-23 [CrossRef] [PubMed]
 
Halpern MT, Gillespie BW, Warner KE. Patterns of absolute risk of lung cancer mortality in former smokers. J Natl Cancer Inst. 1993;856:457-464 [CrossRef] [PubMed]
 
Edwards BK, Howe HL, Ries LA, et al. Annual report to the nation on the status of cancer, 1973-1999, featuring implications of age and aging on US cancer burden. Cancer. 2002;9410:2766-2792 [CrossRef] [PubMed]
 
Gridelli C, Rossi A, Maione P. Challenges treating older non-small cell lung cancer patients. Ann Oncol. 2008;19suppl 7:vii109-vii113 [CrossRef] [PubMed]
 
Yellin A. Bronchogenic carcinoma in the elderly. Ann Thorac Surg. 1985;406:637 [CrossRef] [PubMed]
 
Falcoz PE, Conti M, Brouchet L, et al. The Thoracic Surgery Scoring System (Thoracoscore): risk model for in-hospital death in 15,183 patients requiring thoracic surgery. J Thorac Cardiovasc Surg. 2007;1332:325-332 [CrossRef] [PubMed]
 
Bernard A, Rivera C, Pages PB, Falcoz PE, Vicaut E, Dahan M. Risk model of in-hospital mortality after pulmonary resection for cancer: a national database of the French Society of Thoracic and Cardiovascular Surgery (Epithor). J Thorac Cardiovasc Surg. 2011;1412:449-458 [CrossRef] [PubMed]
 
Rivera C, Dahan M, Bernard A, Falcoz PE, Thomas P. Surgical treatment of lung cancer in the octogenarians: results of a nationwide audit. Eur J Cardiothorac Surg. 2011;396:981-986 [CrossRef] [PubMed]
 
Greene FLPD, Fleming ID, Fritz AG, Balch CM, Haller DG, Morrow M. AJCC Cancer Staging Handbook. 2002; New York, NY
 
Seely AJ, Ivanovic J, Threader J, et al. Systematic classification of morbidity and mortality after thoracic surgery. Ann Thorac Surg. 2010;903:936-942 [CrossRef] [PubMed]
 
Schafer JL. Multiple imputation: a primer. Stat Methods Med Res. 1999;81:3-15 [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]
 
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Bryant AS, Rudemiller K, Cerfolio RJ. The 30- versus 90-day operative mortality after pulmonary resection. Ann Thorac Surg. 2010;896:1717-1722 [CrossRef] [PubMed]
 
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Figures

Figure Jump LinkFigure 1. Hospital length of stay after pulmonary resection for early stage non-small cell lung cancer.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1 —Patient Characteristics and Lung Cancer Presentation

Data are presented as mean (95% CI) or % (No.). ASA = American Society of Anesthesia.

Table Graphic Jump Location
Table 2 —Surgical Treatment and Frequency of Sentinel Events

Data are presented as % (No.).

Table Graphic Jump Location
Table 3 —Reported Postoperative Outcomes

Data are presented as mean % (No.), unless otherwise indicated. LOS = length of stay.

a 

No. complications per patient.

b 

Patients presenting with at least one major complication were considered patients with major complications and those presenting with at least one minor complication without any major complications were considered patients with minor complications.

c 

This variable represents the distribution of major and minor complications within patients presenting with at least one complication.

Table Graphic Jump Location
Table 4 —Distributions of Deaths Among Patients Presenting or Not Presenting With Postoperative Complications
a 

Patients presenting at least one major complication were considered “major complications” patients and patients presenting at least one minor complication without any major complication were considered ”minor complications” patients.

References

Yancik R, Ries LA. Aging and cancer in America. Demographic and epidemiologic perspectives. Hematol Oncol Clin North Am. 2000;141:17-23 [CrossRef] [PubMed]
 
Halpern MT, Gillespie BW, Warner KE. Patterns of absolute risk of lung cancer mortality in former smokers. J Natl Cancer Inst. 1993;856:457-464 [CrossRef] [PubMed]
 
Edwards BK, Howe HL, Ries LA, et al. Annual report to the nation on the status of cancer, 1973-1999, featuring implications of age and aging on US cancer burden. Cancer. 2002;9410:2766-2792 [CrossRef] [PubMed]
 
Gridelli C, Rossi A, Maione P. Challenges treating older non-small cell lung cancer patients. Ann Oncol. 2008;19suppl 7:vii109-vii113 [CrossRef] [PubMed]
 
Yellin A. Bronchogenic carcinoma in the elderly. Ann Thorac Surg. 1985;406:637 [CrossRef] [PubMed]
 
Falcoz PE, Conti M, Brouchet L, et al. The Thoracic Surgery Scoring System (Thoracoscore): risk model for in-hospital death in 15,183 patients requiring thoracic surgery. J Thorac Cardiovasc Surg. 2007;1332:325-332 [CrossRef] [PubMed]
 
Bernard A, Rivera C, Pages PB, Falcoz PE, Vicaut E, Dahan M. Risk model of in-hospital mortality after pulmonary resection for cancer: a national database of the French Society of Thoracic and Cardiovascular Surgery (Epithor). J Thorac Cardiovasc Surg. 2011;1412:449-458 [CrossRef] [PubMed]
 
Rivera C, Dahan M, Bernard A, Falcoz PE, Thomas P. Surgical treatment of lung cancer in the octogenarians: results of a nationwide audit. Eur J Cardiothorac Surg. 2011;396:981-986 [CrossRef] [PubMed]
 
Greene FLPD, Fleming ID, Fritz AG, Balch CM, Haller DG, Morrow M. AJCC Cancer Staging Handbook. 2002; New York, NY
 
Seely AJ, Ivanovic J, Threader J, et al. Systematic classification of morbidity and mortality after thoracic surgery. Ann Thorac Surg. 2010;903:936-942 [CrossRef] [PubMed]
 
Schafer JL. Multiple imputation: a primer. Stat Methods Med Res. 1999;81:3-15 [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]
 
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    Print ISSN: 0012-3692
    Online ISSN: 1931-3543