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Ann Thorac Surg 2004;77:271-277
© 2004 The Society of Thoracic Surgeons

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Original article: general thoracic

Pulmonary resection in octogenarians with stage I nonsmall cell lung cancer: a 22-year experience

^a The Johns Hopkins Medical Institutions, Baltimore, Maryland, USA

^* Address reprint requests to Dr Yang, 624 Osler, 600 N. Wolfe St, Baltimore, MD 21287, USA
e-mail: syang{at}jhmi.edu

Presented at the Poster Session of the Thirty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2003.

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
BACKGROUND: Recent reports indicate that age is not a contraindication to pulmonary resection for octogenarians with nonsmall cell lung cancer (NSCLC), but other data are lacking. The purpose of this study was to determine outcomes in these patients, particularly short- and long-term survival with stage I disease.

METHODS: A retrospective cohort of 68 octogenarians with NSCLC who underwent curative resection from 1980 to 2002 was followed-up for outcomes.

RESULTS: Median age was 82 years old (range, 80–87 years old) consisting of 44 males (65%), with a mean follow-up of 32 months (range, 1–178 months). Operations included: 47 lobectomies (69%), 11 wedge resections (16%), 5 segmentectomies (8%), 4 bilobectomies (6%), and 1 pneumonectomy (1%). There were 31 adenocarcinomas (46%), 18 squamous carcinomas (26%), 12 bronchioalveolar carcinomas (18%), 4 large cell carcinomas (6%), and 3 miscellaneous malignant neoplasms (4%). Median hospital stay was 7 days (range, 3–53 days). Thirty-day mortality was 8.8% (n = 6) with 83% developing cardiopulmonary complications. Overall actuarial survival at 1, 3, and 5 years was 73%, 51%, and 34%, respectively. Of 41 patients (60%) with stage I disease, 23 were T1 lesions. Five-year survival was significantly different between stages Ia and Ib patients (61% and 10%, respectively, p = 0.001). Patients in more advanced stages had a 5-year survival of 3/27 (11%). Multivariate analysis identified advanced tumor stage, lower ASA physical status, and low FEV₁ as factors associated with poorer long-term survival.

CONCLUSIONS: The 5-year survival, particularly in patients with stage Ia tumors with favorable ASA and FEV₁, supports the notion that health status and tumor stage outweigh chronologic age in determining surgical candidates.

	Introduction

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The majority of patients with nonsmall cell lung cancer (NSCLC) are diagnosed between the ages of 50 and 80 years old [1, 2]. In fact, 90% of patients with NSCLC will present before the age of 80 years [3]. Increasingly, however, patients over 80 years old with NSCLC are being referred to thoracic surgeons for curative pulmonary resections. Due to lengthening in overall life expectancy as well as the aging of the post-World War II baby boomers, the number of people over 65 years old in the United States continues to climb rapidly. By 2050, the population over 65 years old will swell from about 33.2 million in 1994 to over 80 million [4, 5]. The most significant increase will be in the octogenarians with those greater than or equal to 85 years old growing from a 1994 population of about 3 million to 19 million people by 2050; a sixfold increase [5].

In 2000 the conditional probability of survival for an 80-year-old person (years on average a person is expected to live, assuming that they survive to age 80) in the United States was 8.6 years (7.6 years for males and 9.1 years for females) [6]. This suggests that the life-limiting factor in octogenarians with lung cancer is not their age, but rather their cancer [7]. Operative management, therefore, offers the greatest potential for quality longevity to exceed the anticipated survival of untreated or conservatively managed disease. The urgency for surgery in these octogenarians with lung cancer assumes the same relative importance as for younger patients [8].

In the past, age greater than 80 years old was considered a relative contraindication to pulmonary resection, prompting some to advocate nonoperative management in this age group [9, 10]. During the last two decades, however, numerous studies involving lung resections in the octogenarian have dismissed older accounts of prohibitively high mortality rates, and have suggested that lobectomies, in particular, are safe and effective [1, 11–19]. These studies, however, have involved small populations, while detailed data with multivariate analysis concerning clinical characteristics, comorbidity, and long-term survival have been lacking.

In an effort to understand the surgical outcome of octogenarians with lung cancer, the purpose of this study was to examine our experience at the Johns Hopkins Hospital over 22 years (1980–2002). Preoperative variables pertaining to the patient's fitness for surgery, and degree of operability were assessed for their predictive validity in determining acute as well as long-term survival.

	Patients and methods

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Population
Data were acquired on 2693 patients who underwent major pulmonary resections (Current Procedural Terminology [CPT] codes 32440–32445 and 32480–32488) between January 1, 1980 and December 31, 2002 diagnosed with nonsmall cell bronchogenic carcinoma (International Classification of Diseases, ninth revision, Clinical Modification [ICD-9-CM] codes 162.3–162.9). Approval to perform this study was obtained from the Institutional Review Board of the Johns Hopkins Medical Institutions. Patients were excluded if they underwent resection for pulmonary metastases; operation for diagnostic biopsies; thoracoscopy; and explorations that were not considered complete and curative. The study population comprised 68 octogenarian patients with a primary bronchogenic neoplasm, and who were operated on with curative intent. During this same study period, 408 octogenarians were diagnosed at the Johns Hopkins Hospital with lung cancer, giving a resectability rate of approximately 17% (68/408). Most patients who were denied lobectomies either had nonpulmonary comorbidities that preempted resection or surgically unresectable disease. Even though our cohort represents a highly selected group of greater than 80-year-old patients with excellent general medical conditions, our rate of resectability is higher than observed in other studies of octogenarians [1, 20].

Patient clinical variables and outcomes
A total of 53 separate preoperative variables and 18 postoperative complications occurring within 30 days of the index operation were recorded for each patient using clinical charts, the institution's cancer registry, and clinical databases. Variables chosen for this study were based on evidence from other large investigations in patients irrespective of age undergoing thoracic surgery, and pertained primarily to pulmonary function, comorbidity, nutrition, performance status, staging, operation performed, histologic tumor type, hospital stay, postoperative complications, and time to death [21, 22]. To ensure accuracy of the abstraction process, 7 of 68 charts were randomly reexamined by a separate reviewer; there was a 98% concordance in the data variables between reviewers. The preoperative laboratory values closest to the operation date were recorded. All patients staged before 1997 were reclassified according to the new TNM classification criteria [23], and reported as pathologic staging. Mediastinal lymph node sampling was performed as systematic sampling of levels 2, 4, 7, 8, 9, and 10 on the right; and 5, 6, 7, 8, 9 on the left side. All patients who received segmentectomy or greater resections received mediastinal nodal sampling except for 2 patients with segmentectomies, one of whom had a T4 lesion.

Patients were followed to their last date of follow-up or until death. Vital status data were provided by the National Death Index of the National Center for Health Statistics. Survival was defined as the interval between date of surgery and date of death or last follow-up. Deaths included all causes, and was not specifically cancer related.

Statistical analysis
The Kaplan-Meier product limit method and the log-rank test were used for survival analysis. The association of factors with time-to-event endpoints was estimated using the Cox proportional hazards model for multivariate analysis. Results of the Cox model analysis are reported as relative risks with 95% confidence intervals. Comparison of continuous and dichotomous variables between groups was performed using the paired Student's t-test (two-tailed) and ² tests, respectively. Results were considered significant for p values less than or equal to 0.05. All analyses were accomplished using the STATA statistical software (STATA Corp, College Station, TX).

	Results

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Demographics of the entire cohort
Table 1 summarizes descriptive characteristics of the study population. Most patients were male smokers, with the incidence of those with any smoking history being 77%. Forty-one patients (60%) underwent resection for stage I disease. Two patients were upstaged to stage IV because of metastatic lesions outside of the index lobe of the primary tumor. Adenocarcinoma (n = 31, 46%) and squamous (n = 18, 26%) carcinomas were the predominant histologic cell types, although 66% (45/68) of all malignancies occurred on the right side. Symptomatic patients were only a small majority of those seen (54%). Almost all the octogenarians in the study were Eastern Cooperative Oncology Group (ECOG) status 0 or 1 (67/68, or 99%).

Figure 1 . illustrates the Kaplan-Meier plots of survival for the study population categorized by stage. Median survival for stage I patients was better compared with more advanced stages of disease (54 months vs 18 months, respectively), but this difference did not achieve statistical significance over the entire study period. If subgrouped as stage Ia and stage Ib disease, not only does there emerge a significant difference in survival between stage Ia and Ib groups (Fig 2), . but also stage Ia patients achieved a significant survival advantage versus more advanced disease at 10 years (Fig 3). Using a one-way analysis of variance, differences in preoperative risk factors between patients with stage Ia and those with more advanced stages of disease did not explain the significant disparity in survival (Table 4).

View larger version (19K): [in this window] [in a new window]   Fig 1. Overall survival of lung cancer patients over 80 years old; stage I versus stages II–IV. Differences in overall survival were evaluated using the log-rank test. Although overall survival over 10 years was not significantly different, median survival for stage I patients was longer than for stage II–IV patients (54 months vs 18 months).

View larger version (19K): [in this window] [in a new window]   Fig 2. Overall survival of lung cancer patients over 80 years old; stage IA versus stage IB. Differences in the Kaplan-Meier curves were evaluated using the log-rank test. Patients with stage IA disease had significantly longer 1-, 3-, and 5-year survivals than patients with stage IB disease (91%, 76%, 62% vs 66%, 37%, 10%, respectively; p = 0.001).

View larger version (20K): [in this window] [in a new window]   Fig 3. Overall survival of lung cancer patients over 80 years old; stage IA versus stages IB–IV. Differences in the Kaplan-Meier curves were evaluated using the log-rank test. Patients with stage IA disease had significantly longer 1-, 3-, 5-, and 10-year survivals than patients with stages IB–IV disease (91%, 76%, 62%, 19% vs 64%, 36%, 18%, 5%, respectively, p = 0.001).

	Comment

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It is interesting to speculate that the poor long-term survival in the stage Ib patients is due to the presence of occult micrometastases to regional and mediastinal lymph nodes that remained undetected by histological examination. Recently, we described a population of stage I lung cancer patients from our institution who could be molecularly upstaged due to occult lymph node metastases [26]. Using TP53 and Kras mutational analysis, we identified 28% (9/32) of stage I patients who had micrometastases in regional and mediastinal lymph nodes, but due to the small sample size, the study did not detect any significantly poorer survival in patients with and without micrometastases. In addition to stage Ib, outcomes in more advanced stages in this present study were also poor with only 3 of 27 patients (11%) surviving beyond 5 years. Pagni and colleagues [14] similarly reported in octogenarians undergoing pulmonary resections that those beyond N0 disease fared poorly, but offered no separate analysis of cumulative survival for patients with T2N0 disease. The cumulative evidence suggests that accurate preoperative clinical staging is imperative, and implies a need for more liberal use of sensitive imaging modalities, such as positron-emission tomographic scans, to stage octogenarians.

By multivariate analysis using the Cox Proportional Hazards Model, a patient's tumor stage, FEV₁ less than 1.5, and ASA status were powerful, independent predictors of long-term survival in this study. The literature is replete with evidence that operative risk and long-term survival are adversely affected after major pulmonary resections if tumor stage and objective pulmonary function are used as predictive variables; however, using the ASA status as a predictor of longer term outcome is not as widely accepted. The ASA classification of physical status was developed for assessing perioperative risk rather than predicting long-term survival. The ASA class, however, closely coincides with preoperative comorbidity, and has been recently demonstrated to be a useful measure of both comorbidity and long-term prognosis in an elderly cohort of head and neck surgical cancer patients [27]. Furthermore, it has the advantage of widespread use and is readily available in the medical record.

At our institution, the ASA status is formulated as a composite score assigned by at least two anesthesiologists in the anesthesia records at the time of operative assessment. Harpole and associates [22] included ASA status in their multiinstitutional outcome study of major pulmonary resections, but limited its use to predicting 30-day mortality. In our study, patients with a preoperative ASA status of 4 had a risk of death more than 6 times that of those with an ASA status of 2. It has been our clinical practice to ensure the proper selection of all candidates with lung cancer for pulmonary resection, especially the elderly, by a careful assessment of preoperative comorbidity. For over 10 years, management of the octogenarian patient has been given particular and special attention at weekly formal multidisciplinary conferences consisting of pulmonologists, thoracic surgeons, and medical and radiation oncologists. Careful assessment of preoperative cardiovascular and pulmonary fitness is performed by formal liaisons between members of this interdisciplinary team before recommendations for surgery are given. The ASA status may provide yet another useful and objectively standard clinical tool for this assessment.

In a study of this length that spans different eras of clinical practice, the impact of temporal bias must be addressed, and criticism can be levied that the results of earlier procedures may not reflect current clinical practice. It is possible that both known and unknown confounding variables attributable to medical progress, such as changes in technology, operative technique, personnel, medications, and practice guidelines, may have impacted significantly on clinical outcome [28]. In order to sort out the effect of these confounding variables, a multivariate analysis, including a variable denoting date of surgery, was performed on the entire cohort without reference to subgroups. The year that surgery was performed was not predictive of survival. Further consideration was given to the temporal distribution of the cases performed. A bimodal pattern was noted pre-1990 and post-1990, with most procedures (77%) occurring within the last decade. The development of a dedicated general thoracic surgical program, an increasingly aging patient population, and more aggressive patient selection were the most likely factors contributing to the increase in surgical activity in this age group since 1990. Patient selection before 1990 favored those with limited comorbidities with cardiopulmonary or neurologic conditions being present in only 6 of 11 patients (55%) compared with 46 of 49 patients (94%) post-1990. Pre-1990, there were also far fewer surgical candidates with FEV₁ less than 1.5L compared with post-1990 (2/13, 15% vs 18/33, 55%). Despite these recent changes in patients selected for surgery, postoperative morbidity and mortality in the pre-1990 and post-1990 groups were not statistically different. The most notable difference between the groups was the reduction in the median length of hospital stay (9 vs 6 days, p = 0.04); an increase in the percentage of patients released within 1 week postoperatively from 25% to 63%, p = 0.012.

In any study that involves surgery of the elderly, assessment of quality of life (QOL) postoperatively should be a secondary, but important objective. Because our data are retrospective and span more than two decades, precise measurement methods, such as standardized QOL questionnaires in use today, were not available. As a proxy variable, the return to and maintenance of preoperative levels of independence was estimated by whether or not a patient required convalescent care upon release from the hospital. Although this is an imprecise measure, the fact that nearly 80% of octogenarians in this cohort were discharged directly home suggests that most patients enjoyed a rapid return to preoperative baseline, and spent their remaining years in active, independent life. Although postoperative adjuvant therapies may also adversely affect quality of life, due to the retrospective nature of the study it was difficult to collect data from all patients who received postoperative therapy, especially if it was administered outside of our institution. Similarly, two decades of cause of death data were difficult to obtain retrospectively, and all of our survival analyses are limited to overall survival.

In summary, octogenarians should not be denied surgery solely due to age because properly selected greater than or equal to 80 year olds with lung cancer can be resected safely with acceptable long-term survival. Careful attention to preoperative clinical staging is important since octogenarians beyond very early staged disease fare poorly. Specific consideration of pulmonary functional studies and comorbidity disease status has high predictive validity for postoperative survival in these patients.

	Acknowledgments

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Dr Brock is a recipient of a research supplement award from the National Cancer Institute, grant CA84986. Dr Alberg is a recipient of a K07 award (CA73790) from the National Cancer Institute. This work was also supported in part by the NIH Grant CA58184. We would also like to thank Kathy Bender for her technical assistance in helping to prepare this manuscript.

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Malcolm V. Brock Stephen C. Yang Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Brock, M. V. Articles by Yang, S. C. Search for Related Content PubMed PubMed Citation Articles by Brock, M. V. Articles by Yang, S. C. Related Collections Lung - cancer