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Ann Thorac Surg 2005;79:1137-1141
© 2005 The Society of Thoracic Surgeons

Original articles: General thoracic

Survival After Pathological Stage IA Nonsmall Cell Lung Cancer: Tumor Size Matters

Özcan Birim, MDa, A. Pieter Kappetein, MD, PhDa,*, Johanna J.M. Takkenberg, MD, PhDa, Rob J. van Klaveren, MD, PhDb, Ad J.J.C. Bogers, MD, PhDa

a Department of Cardiothoracic Surgery, , Rotterdam, The Netherlands
b Department of Pulmonology, Erasmus MC Rotterdam, Rotterdam, The Netherlands

Accepted for publication September 24, 2004.

* Address reprint requests to Dr Kappetein, Department of Cardiothoracic Surgery, Room BD 156, Erasmus MC, PO Box 2040, 3000 CA Rotterdam, The Netherlands (E-mail: a.kappetein{at}erasmusmc.nl).


   Abstract
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 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: This study evaluates prognostic factors for survival in completely resected pathological stage IA nonsmall cell lung cancer with special emphasis on tumor size and assesses tumor recurrence rate by actual and actuarial analysis.

METHODS: From January 1989 to December 2001, 130 consecutive resections for pathological stage IA nonsmall cell lung cancer were performed. Pathological tumor size was categorized into 0 to 20 mm and 21 to 30 mm. Each patient was scaled according to the Charlson Comorbidity Index. The Kaplan-Meier method was used for estimation of actuarial recurrence rate and the cumulative incidence method was used to estimate the actual recurrence rate. Risk factors for overall and disease free survival were determined by univariate and multivariate Cox regression analysis.

RESULTS: Overall 5-year survival for patients with tumors 0 to 20 mm and 21 to 30 mm was 69% and 51%, respectively (p = 0.038). Disease-free survival at 5 years was 68% and 48%, respectively (p = 0.015). Only 27 patients had a recurrence and 69 patients died during follow-up. The actual 10-year recurrence rate was lower than the actuarial recurrence rate (23% vs 29%). Larger tumor size (relative risk 1.6; 95% confidence interval 1.0 to 2.7), Charlson Comorbidity Index score greater than or equal to 3 (relative risk 3.7; 95% confidence interval 1.7 to 8.0), and pneumonectomy (relative risk 2.1; 95% confidence interval 1.1 to 4.2) independently predicted adverse outcome.

CONCLUSIONS: Tumor size affects survival in resected stage IA nonsmall cell lung cancer. Current definition of stage IA disease should be substaged into two separate stages. In patients with early-stage lung cancer and relatively good prognosis actual recurrence rate is more realistic than the actuarial recurrence rate.


   Introduction
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 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
The incidence of nonsmall cell lung cancer (NSCLC) is increasing in the western world and still remains the leading cause of cancer-related mortality for both men and women [1]. Early-stage disease is usually treated surgically when possible and has the best prognosis. Several studies have demonstrated that tumor size is highly prognostic for survival [2, 3]. As a result stage I was subdivided into IA (tumor size < 3 cm, T1N0M0), and IB (tumor size > 3 cm, T2N0M0), in the current staging system in 1997 [4].

In recent years, there has been regained interest for the early screening and detection of lung cancer [5, 6]. However, more frequent chest radiographic screening has not shown to result in reduced lung cancer mortality [7]. With the widespread availability and increasing use of advanced staging techniques, such as spiral computed tomography (CT) scan, lesions smaller than 1 cm can be identified [8]. Nevertheless, if detection and treatment of smaller lesions is not associated with improved survival, early screening of lung cancer using CT scan may not result in reduced lung cancer mortality. Until now there is only limited and conflicting evidence available on the affect of tumor size on prognosis of patients with pathological stage IA NSCLC [2, 9–12].

Recurrence rate is thought to be the lowest in stage IA NSCLC patients. Patients within this stage do not always die as a result of their tumor. Currently, the Kaplan-Meier (actuarial) method [13] is generally used to estimate the recurrence rate in lung cancer patients. However, recently the cumulative incidence (actual) method proved to be a more valid method for estimating the probability of occurrence of a nonfatal time-related event because it estimates the percentage of patients who will actually have an event [14–16].

Therefore, the aims of this study were to evaluate tumor size as a prognostic factor for survival in completely resected pathologic stage IA NSCLC patients, and to estimate the actual versus actuarial risk of tumor recurrence.


   Material and Methods
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 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Retrospectively, the medical records of 139 consecutive patients who underwent complete resection for pathologic stage IA primary NSCLC at the Department of Cardio-Thoracic Surgery of the Erasmus Medical Center in Rotterdam (between January 1, 1989, and December 31, 2001) have been reviewed. Patients who had a second primary lung tumor were included in this study. Patients were followed with regular visits to the outpatient clinic. Civil administrations were consulted to assess late mortality. Follow-up was completed in all patients through July 2003. Median follow-up was 6.8 years. Overall survival time was defined as the difference between the date of surgery and the date of last follow-up. Disease-free survival was defined as the difference between the date of surgery and the date of local or distant recurrence of disease or the date of last follow-up in case of no recurrence. Hospital mortality was defined as death occurring within 30 days of surgery or any death later during the same postoperative hospital stay.

In all patients diagnostic work-up included a complete medical history, physical examination, plain chest radiography, electrocardiography, routine laboratory tests, lung function tests, and CT of the chest and upper abdomen. Patients were found to have positive mediastinal lymph nodes if mediastinal lymph nodes on computed tomography scan were more than 10 mm in diameter. Additional staging procedures, ie, mediastinoscopy, liver, bone, and brain scans were selectively performed to aid in treatment planning according to best clinical practice at the time of presentation. Each patient was scaled preoperatively according to the Charlson Comorbidity Index [17–19]. The index can be divided into four comorbidity grades: 0, 1 to 2, 3 to 4, and 5 or more.

Histologic typing occurred according to the World Health Organization Histologic Typing of Lung Tumors [20]. Pathologic staging of the patients occurred according to the international TNM classification for lung cancer [4]. Staging was based on pathological assessment of the primary tumor and lymph node assessment was carried out with preoperative mediastinoscopy or surgical sampling of bronchopulmonary, hilar, and mediastinal lymph nodes. The surgical-pathologic size of the primary tumor was obtained by measuring the greatest diameter of the fresh surgical specimen by the pathologist. Patients were categorized as patients with pathologic tumors of 0 to 20 mm in diameter (n = 75) and 21 to 30 mm in diameter (n = 55).

The following risk factors for overall and disease-free survival were evaluated: sex, age, type of surgery, histologic cell type, tumor size, congestive heart failure, coronary artery disease, chronic obstructive pulmonary disease, forced expiratory volume in 1 second (unknown in 9 patients), and Charlson Comorbidity Index.

Discrete variables are displayed as proportions, continuous variables as means ± standard deviations unless specified otherwise. The {chi}2 or Fisher exact test was used to analyze the categorical data. Continuous variables were analyzed using the Student's t test. Long-term survival curves were estimated by the Kaplan-Meier method, and the resulting survival curves were compared with the Breslow test. The Kaplan-Meier method was used for estimation of actuarial recurrence rate and the cumulative incidence method was used to estimate the actual recurrence rate. Univariate and multivariate Cox proportional hazard analysis within different time intervals determined risk factors for long-term survival. The Cox proportional multivariate analyses were performed with a stepwise forward regression model in which each variable with a p-value of less than 0.20 in the univariate analysis was entered in the model. Relative risks are reported with 95% confidence intervals.


   Results
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 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Of the 139 patients, 6 patients received neoadjuvant therapy (chemotherapy or radiotherapy) and were excluded from this study. The remaining 133 patients had no positive mediastinal lymph nodes on CT scanning or mediastinal lymph node sampling by mediastinoscopy. Hospital mortality occurred in 3 patients (2.3%) and they were excluded from further analysis. Of the 130 patients enrolled in this analysis 94 (72%) were men and 36 (28%) were women. The mean age was 63 ± 9 years (range, 37 to 81 years old). The types of procedures performed consisted of pneumonectomy (11; 8%), bilobectomy (12; 9%), lobectomy (103; 79%), and wedge resection (4; 3%). Tumors were classified histologically as squamous cell carcinoma (56; 43%), adenocarcinoma (53; 41%), large cell carcinoma (16; 12%), and bronchoalveolar carcinoma (5; 4%). The mean pathologic tumor size was 20 ± 6 mm (range, 5 to 30 mm). Tumor size distribution is illustrated in Figure 1. The patient demographics are listed in Table 1.



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  		Fig 1. Distribution of pathological tumor size.

 

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  		Table 1. Patient Characteristics
 
Mean overall survival of the total study group was 7.7 years and the mean disease-free survival was 7.5 years. Five-year overall survival was 62% (95% confidence interval 53 to 71%) and disease-free survival was 59% (95% confidence interval [CI] 50% to 68%). Patients with tumors 0 to 20 mm in diameter had a 5-year overall and disease-free survival of 69% (95% CI 58% to 80%) and 68% (95% CI 57% to 79%), respectively. The 5-year overall and disease-free survival for patients with tumors 21 to 30 mm was 51% (95% CI 37% to 65%) and 48% (95% CI 34% to 62%), respectively. The difference in overall and disease-free survival between the two groups was highly significant (p = 0.038 and p = 0.015, respectively). The Kaplan-Meier overall survival curves are shown in Figure 2.



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  		Fig 2. Overall survival curves for patients with tumors 0 to 20 mm and 21 to 30 mm in diameter.

 
Of the total study population, 27 patients had a recurrence and 69 patients died during follow-up. The actual recurrence rate within 10 years was lower than the actuarial recurrence rate (23% vs 29%). The 2-year, 5-year, and 10-year actuarial freedom from recurrence was 88%, 81%, and 71%, respectively. Actual analysis yielded slightly higher percentages of freedom from recurrence: 89%, 83%, and 77%, respectively. When comparing patients with tumors 0 to 20 mm and 21 to 30 mm, 5-year actual freedom from recurrence was 88% versus 76%, respectively.

When evaluating risk factors for overall survival with the Cox proportional hazards analysis, in univariate analysis Charlson Comorbidity Index score equal to or greater than 3, larger tumor size, and pneumonectomy were predictive for impaired survival. In multivariate analysis, larger tumor size (relative risk 1.6; 95% confidence interval 1.0 to 2.7), Charlson comorbidity index score greater than or equal to 3 (relative risk 3.7; 95% CI 1.7 to 8.0), and pneumonectomy (relative risk 2.1; 95% CI 1.1 to 4.2) were associated with an impaired overall survival (Table 2). When assessing risk factors for disease-free survival, the same three risk factors were identified in the multivariate analysis.


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  		Table 2. Univariate and Multivariate Cox Proportional Hazard Analysis of Survival
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
According to the current lung cancer staging system stage I patients are subdivided in patients with tumors less than 3 cm and those greater than 3 cm. This difference is a result from several retrospective studies that have shown a survival advantage for patients with tumors less than 3 cm [2, 3]. These patients are categorized as stage IA. The survival of stage IA patients in our population was 62%, which is comparable to the 67% reported by Mountain [4]. However our study clearly demonstrates that there is a survival benefit for patients with tumors 0 to 20 mm compared with tumors 20 to 30 mm in diameter. Early detection of small tumors may have its impact on survival although lead-time bias, length-time bias, and overdiagnosis bias may play an important role. There is conflicting evidence to support the impact of tumor size as prognostic risk factor for survival in stage IA NSCLC patients [2, 9–12]. Table 3 summarizes studies of the prognosis of tumor size in patients with pathological stage IA NSCLC. Patz and coworkers [11] evaluated the relation between tumor size and survival in 510 consecutive patients with stage IA NSCLC and found no correlation between tumor size and survival. However they reported observed survival based on deaths from all causes rather than disease free survival, which is inappropriate in patients with stage IA disease because it is not unlikely that these patients die of another cause than lung cancer. In a review of 598 patients with stage I NSCLC, Martini and associates [2] demonstrated that size did impact survival within stage IA; the survival of patients with tumors less than 1 cm was higher than those whose tumors were between 1 cm and 3 cm. In another study by Port and colleagues [10], a difference in the 5-year lung cancer specific survival for stage IA tumors was noted for tumors less than 2 cm and those between 2 and 3 cm in diameter. Read and colleagues [12] also found a survival benefit for patients with tumors less than 2 cm.


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  		Table 3. Summary of the Literature Assessing Prognostic Significance of Tumor Size in Pathological Stage IA Nonsmall Cell Lung Cancer
 
An explanation for the impaired survival in patients with larger tumors is an increase in the incidence of micrometastatic lymph nodes at the time of surgery. There is some evidence that smaller tumors metastasize to lymph nodes infrequently and thereby offer a greater chance of true cure following resection. In a study by Saito and coworkers [21], no nodal metastases were found in 55 patients with tumors less than 1 cm, whereas 4 of 46 patients with tumors 1 to 1.9 cm were found to have nodal spread. Therefore, earlier detection and treatment of NSCLC might increase the probability of curing lung cancer. However occult lymph node metastases may be present in small tumors at the time of diagnosis, and thus represent advanced stage disease despite their small size [22]. Preliminary spiral CT screening trials determined that up to 30% of small primary tumors metastasized to regional lymph nodes or distant sites on initial examination [6, 23]. In some cases tumors metastasize even when they are less than 1 mm [24], while others may remain curable until they reach several centimeters. In this regard, recurrence rate is thought to be the lowest in pathological stage IA NSCLC patients. Not all of these patients die as a result of their tumor. Currently, the Kaplan-Meier (actuarial) method is widely used and accepted as method to estimate the recurrence rate in NSCLC patients. However, death is competing with recurrence in this method because patients who died without recurrence are censored as patients who can still have a recurrence. It is important to estimate the recurrence rate as accurate as possible to give the best and correct advise to patients on the probability of ever developing a recurrence after surgical resection. The cumulative incidence analysis corrects major errors that can occur when failures due to other causes are treated as censored observations in a Kaplan-Meier analysis [14, 15]. When compared to standard actuarial analysis, recurrence rate according to the actual method yielded more favorable results for the long-term in our series. The most suitable reason for the small difference between actual and actuarial recurrence rate in our analysis is the small number of patients included. It is to be expected that this difference will be larger in larger series.

A limitation of our study is to be seen in its retrospective design. It is impossible to know what the cause of death was in some patients in whom recurrence was not mentioned in the records and no autopsy was performed, which may have influenced the results of our analysis.

In conclusion, the results obtained in this study highlight that size of the tumor affects survival in surgically resected stage IA NSCLC. Given that our results are consistent with most of the prior literature it is time to reconsider the current definition of stage IA disease and substage stage IA lesions in two separate stages. Because of the different cutoff points used for tumor size in the prior literature, it will be necessary to conduct further prospective research to obtain the best cutoff point. As size seems to be a prognostic factor for survival, improved small nodule detection may significantly improve lung cancer mortality. At this time one can only speculate about the potential role of spiral computed tomography screening in the early diagnosis of lung cancer until more data are available from randomized clinical lung cancer screening trials. Actuarial analysis underestimates the recurrence free survival compared to actual analysis by censoring all deaths without a recurrence. In patients with early-stage lung cancer and relatively good prognosis actual recurrence rate is more realistic than the actuarial recurrence rate.


   References
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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  10. Port JL, Kent MS, Korst RJ, Libby D, Pasmantier M, Altorki NK. Tumor size predicts survival within stage IA non-small cell lung cancer Chest 2003;124:1828-1833.[Abstract/Free Full Text]
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