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J Thorac Cardiovasc Surg 2006;132:1382-1388
© 2006 The American Association for Thoracic Surgery

General Thoracic Surgery

Long-term survival and recurrence in patients with resected non–small cell lung cancer 1 cm or less in size

Department of Cardiothoracic Surgery, Weill-Cornell Medical Center, New York, NY.

Read at the Eighty-sixth Annual Meeting of The American Association for Thoracic Surgery, Philadelphia, Pa, April 29-May 3, 2006.

Received for publication April 17, 2006; revisions received August 16, 2006; accepted for publication August 31, 2006.

^_* Address for reprints: Nasser K. Altorki, MD, Department of Cardiothoracic Surgery, Suite M404, New York Presbyterian Hospital—Weill Medical College of Cornell University, 525 East 68th St, New York, NY 10021 (Email: nkaltork{at}med.cornell.edu).

	Abstract

Top Abstract Introduction Patients and Methods Results Discussion References

 
OBJECTIVE: With the widespread use of computed tomography and the emergence of screening programs, non–small cell lung cancer is increasingly detected in sizes 1 cm or less. We sought to examine the long-term survival and recurrence patterns after resection of these tumors.

METHODS: We conducted a retrospective review over a 15-year period to identify patients with surgically resected non–small cell lung cancer measuring 1 cm or less. Medical records were reviewed, and survival data were analyzed by the Kaplan-Meier method.

RESULTS: There were 83 patients (26 men, 57 women) with a median age of 67 years (range 43-88 years). Median tumor size was 0.90 cm. Lobectomy was performed in 71 patients, bilobectomy in 1, pneumonectomy in 1, segmentectomy in 5, and wedge resection in 5. Postoperative stage was IA in 67 patients, IB in 4, IIA in 1, IIB in 4, IIIA in 2, and IIIB in 5. Median follow-up was 31 months. There was 1 operative death (1.2%). In 5 (31.3%) of the 16 patients with non-IA disease, recurrent cancer developed after resection. No recurrences were observed in the 67 patients with stage IA disease. The 5- and 10-year overall survivals for the entire cohort were 86% and 72%, respectively, and the disease-specific survival was 91% at both time points. For patients with stage IA disease, 5- and 10-year survivals were 94% and 75%, respectively, and the disease-specific survival was 100% at both time points.

CONCLUSION: Eighty-one percent of patients with resected non–small cell lung cancer measuring 1 cm or less had stage IA disease. After surgical resection, recurrence is rare and long-term survival is excellent.

	Introduction

Top Abstract Introduction Patients and Methods Results Discussion References

 
Lung cancer is the leading cause of cancer deaths in the United States. In 2005, an estimated 173,000 Americans were diagnosed with lung cancer, and 164,000 of them will die of their disease.¹ The majority of patients with non–small cell lung cancer (NSCLC) have metastatic or locally advanced disease at presentation, whereas less than 15% present with stage I disease, in which surgical resection results in a 5-year survival of 60% to 80%. The improved survival after surgical resection seen in patients with stage I disease has led to renewed interest in screening programs for lung cancer with the promise of detecting smaller and potentially more curable tumors. With the increased prevalence of screening programs as well as the widespread use of high-resolution computed tomography (CT), NSCLC is more frequently detected in sizes 1 cm or less. However, it is still uncertain whether detection of smaller tumors translates into improved long-term survival. Very few studies have reported the long-term survival and recurrence patterns after resection of these small lesions. There is also controversy regarding the optimal surgical approach for these small tumors. In this study, we reviewed our experience in patients with resected NSCLC measuring 1 cm or less in size to determine the overall and disease-specific survival as well as tumor recurrence after surgical resection.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Discussion References

 
Patients
We conducted a retrospective review of all patients with NSCLC in a prospective database to identify patients with pathologic NSCLC measuring 1 cm or less that was surgically resected at our institution from January 1991 to December 2005. Patients who had neoadjuvant therapies before resection were excluded. A total of 83 patients were identified. Hospital and office records of each patient were reviewed for demographic and clinical data including age, gender, smoking status, preoperative pulmonary functional assessment, preoperative radiologic assessment, associated comorbidities, and clinical stage. Records were also reviewed for perioperative and pathologic data, including surgical approach, extent of resection, 30-day operative mortality (defined as death during the same hospitalization or within 30 days after the operation), complications, length of stay, tumor size, histologic type, pathologic stage, and use of adjuvant therapy. Staging was done according to the TNM classification of the American Joint Committee for Cancer Staging and Revised International System for Staging Lung Cancer.² Follow-up was obtained through office visits and telephone interviews.

Statistical Analysis
Statistical analysis was performed with SPSS statistical software (SPSS Inc, Chicago, Ill). Overall and disease-specific survival of the entire cohort and for two subgroups (stage IA group and stage non-IA group) was analyzed by the Kaplan-Meier method. In this study, overall survival is defined as the percentage of patients who have survived for a defined period of time after surgical resection. Disease-specific survival is defined as the percentage of patients who have survived lung cancer for a defined period of time after surgical resection. In calculating this percentage, we counted only deaths from lung cancer, excluding patients who died of other causes. The log-rank test was used to determine significance of survival distributions among groups. Independent t tests were used for two-group comparisons of continuous variables. Categorical data in cross-tabulation tables were compared by the Fisher exact test or the Pearson ² test. Nonparametric data were analyzed with the Mann-Whitney U test. This study was approved by the Institutional Review Board of the Weill Medical College of Cornell University.

	Results

Top Abstract Introduction Patients and Methods Results Discussion References

 
Clinical Findings
During the 15-year study period from January 1991 to December 2005, 83 patients were identified (26 men, 57 women) with a median age of 67 years (range 43-88 years). The number of NSCLCs 1 cm or less in size increased steadily over the study period. The numbers of resected tumors were 8, 21, and 54 over the 3 consecutive 5-year periods. These represented 3.8%, 5.8%, and 7.0% of the total number of surgical resections for NSCLC over the same time periods. Seventy-eight patients were smokers and 5 were never-smokers. Of the smokers, 17 were current and 61 were former smokers. Median pack-years of all smokers was 40. Seventeen patients had respiratory symptoms at presentation, which included cough, shortness of breath, and fever. The majority of the tumors were discovered incidentally by CT or chest radiograph. Tissue diagnoses were obtained by CT-guided fine needle aspiration in 48 patients and flexible bronchoscopy in 1 patient. In the remaining 34 patients, the diagnosis was suggested by a positive result on positron emission tomography (PET) scanning (n = 13) or suspicious findings on CT scanning (n = 21). Twenty-one patients were enrolled in the Early Lung Cancer Action Project (ELCAP) screening program and had their tumors detected by low-dose CT. Pulmonary function tests were performed in 70 patients. Mean forced expiratory volume in 1 second was 83% of predicted (range 36%-100%). Mean forced vital capacity was 87% of predicted (range 53%-100%). Mean diffusing capacity was 76% of predicted (range 31%-100%).

PET Scanning
PET scanning was obtained preoperatively in 37 patients in whom a standard uptake value was reported. Twenty-two patients had a positive finding. The median standard uptake value for a positive result was 2.7 g/mL. The histologic characteristics for the 22 PET-positive tumors were as follows: adenocarcinoma in 17 (mixed subtype of adenocarcinoma with bronchoalveolar features in 3, bronchoalveolar carcinoma subtype in 2), squamous cell carcinoma in 2, and large cell carcinoma in 3. Of 4 patients with pathologic N1 disease, only 1 patient’s nodal disease was PET positive preoperatively. One of 2 patients with pathologically confirmed N2 disease had a preoperative PET scan that showed no uptake in the mediastinum. Of the 5 patients with intralobar satellite lesions (T4), 3 patients had a preoperative PET scan. In all 3 patients the PET scan failed to identify the satellite lesions.

Surgical Approach and Extent of Resection
All surgical procedures are listed in Table 1. Eighteen patients underwent mediastinoscopy. The indications for mediastinoscopy were lymphadenopathy (>1.5 cm on CT) in 3 patients, central tumor in 2, positive mediastinal uptake on PET in 2, associated medical comorbidities in 3, and surgeon preferences in 8. One patient was found to have N2 disease by mediastinoscopy. Lobectomy was the most commonly performed resection. Bilobectomy was done in 1 patient because of an endobronchial tumor at the bifurcation of the middle and lower lobe bronchus. In another patient, a pneumonectomy was performed because of a centrally located tumor involving the bifurcation of the left upper and lower lobe bronchus. Limited resections were done in 10 patients (5 segmentectomies, 5 wedge resections). The reasons for limited resection included compromised pulmonary reserve in 6 patients, prior lobectomy in 1, associated comorbidities in 1, and incorrect initial frozen-section diagnosis in 2. As presented in Table 2, the group with limited resection had significantly compromised preoperative pulmonary reserve compared with patients with anatomic resections. Seventy-four (89%) patients had mediastinal lymph node dissection. All patients had curative R0 resections.

View this table: [in this window] [in a new window]   TABLE 4. Histopathologic characteristics of all 83 patients with resected 1 cm NSCLC

Overall and Disease-specific Survival
Median follow-up of all patients was 31 months. Nineteen percent of patients (n = 16) with resected NSCLC measuring 1 cm or less in size had greater than stage IA disease. Recurrent cancer developed after resection in 5 (31.3%) of the 16 patients with non-IA disease. Sites of recurrence were mediastinum, contralateral lung, brain, spine, and both spine and mediastinum in 1 patient each. The single patient with isolated mediastinal recurrence underwent surgical resection of the recurrence followed by adjuvant radiotherapy and is currently alive without disease recurrence 12 months after treatment. No recurrences were observed in the 67 patients with stage IA disease during the follow-up period. Five- and 10-year overall survival for the entire cohort was 86% (95% confidence interval [CI] 72%-93%) and 72% (95% CI 51%-85%), respectively (Figure 1). Patients were separated into stage IA and non-IA groups for survival comparison (Figure 2). For patients in stage IA, 5- and 10-year overall survivals were 94% (95% CI 79%-98%) and 75% (95% CI 48%-89%), respectively. For those with non-IA disease, 5- and 10-year overall survival was significantly decreased to 48% (95% CI 12%-77%) (P = .014).

View larger version (7K): [in this window] [in a new window]   Figure 1. Overall survival of 83 patients with NSCLC measuring 1 cm or less after resection. NSCLC, non–small cell lung cancer.

View larger version (9K): [in this window] [in a new window]   Figure 2. Overall survival of patients with NSCLC measuring 1 cm or less after resection, subdividing into pathologic IA and non-IA stage. NSCLC, non–small cell lung cancer.

View larger version (6K): [in this window] [in a new window]   Figure 3. Disease-specific survival of 83 patients with NSCLC measuring 1 cm or less after resection. NSCLC, non–small cell lung cancer.

View larger version (8K): [in this window] [in a new window]   Figure 4. Disease-specific survival of patients with NSCLC measuring 1 cm or less after resection, subdividing into pathologic IA and non-IA stage. NSCLC, non–small cell lung cancer.

	Discussion

Top Abstract Introduction Patients and Methods Results Discussion References

 
The diagnosis of bronchogenic carcinoma carries a dismal prognosis for the majority of patients. The stage of carcinoma at diagnosis remains one of the most important determinants of survival in NSCLC, with earlier-stage patients having a better chance of long-term survival.² For patients with resectable stage I disease, 5-year survival can be as high as 80%.³ Unfortunately, less than 15% of patients present with stage I disease. The improved survival in patients with stage I disease led to renewed interest in lung cancer screening programs with detection of smaller and possibly more curable tumors. The ultimate goal of lung cancer screening programs is to shift the stage distribution of tumors at the time of diagnosis to earlier stages, thus improving the overall curability of lung cancer. Indeed, screening studies have demonstrated a consistent stage shift with stage IA reported in as many as 80% of participants.⁴

Yet controversy still exits regarding the relationship between tumor size and survival within stage IA tumors. We⁵ and others^6,7 have shown improved survival for stage I tumors measuring less than 2 cm, whereas others investigators have not.^8,9 This issue has important implications for lung cancer screening with CT scanning. If there is no difference in survival between subcentimeter tumors and their larger counterparts, then the rationale for using CT scanning (as opposed to chest radiographs) in detecting small lesions is less compelling.

In the current study, 81% of patients with resected NSCLC measuring 1 cm or less had stage IA disease and had a 100% lung cancer–specific survival at 5 and 10 years. No recurrence was noted during our study period for patients with stage 1A disease. Other investigators have demonstrated this superior survival as well. Martini and associates¹⁰ noted in their review of 598 patients with resected stage I NSCLC that 35 patients had tumors measuring less than 1 cm with 5- and 10-year survivals of 97% and 93%. Miller and colleagues¹¹ reported on 100 patients with resected NSCLC measuring 1 cm or less, of whom 93 had stage I disease with a 5-year lung cancer–specific survival of 87%. Our finding supports the concept that size does have a strong impact on survival. If CT screening does indeed detect subcentimeter tumors and thus shifts the size and stage distribution of tumors at diagnosis, then the impact on lung cancer survival may be considerable. In the current series, 21 patients had their tumors discovered through the ELCAP screening program with low-dose CT. Eighteen patients (86%) had stage I disease and only 1 patient had N2 disease.

However, it appears that a subset of small tumors may have aggressive biologic behavior. Ohta and coworkers¹² have shown that nodal micrometastases were found in 20% of patients with adenocarcinoma measuring 1.1 to 2.0 cm in size and in 4 of 11 patients with tumor measuring 1.0 cm or less in size. In the current report of 83 patients, 16 patients had greater than stage IA disease, including N1 nodal metastasis in 4 patients and N2 metastasis in 2 patients. In addition, 5 patients had pleural invasion (T2 in 4, T3 in 1) and 5 patients had intralobar satellite lesions (T4). The survival in this non-IA group was significantly diminished compared with the IA group, mainly because of tumor recurrences.

There is ongoing controversy as to the extent of resection necessary for stage I NSCLC. The Lung Cancer Study Group showed that for stage IA NSCLC, patients who underwent a limited resection (segmentectomy or wedge) had a higher recurrence rate and lower survival than did those treated by lobectomy.¹³ Miller and associates¹¹ demonstrated that for NSCLC measuring 1 cm or less, patients who underwent lobectomy had significantly improved survival and fewer recurrences than did those having limited resection. However, other authors have suggested that limited resections are adequate treatment for early-stage disease.^14-16 In our study, only 10 patients (12%) had limited resection, mainly because of poor pulmonary reserve and/or associated comorbidities. There was no significant difference in overall survival between patients with limited resection and those with anatomic resection. In the 67 patients with stage IA tumors, 8 patients had limited resection. No recurrence was noted in either the limited resection or the anatomic resection group during the follow-up period. Two limited resections were performed in the non-IA group for T2 N0 tumors with visceral pleural involvement. One patient had mediastinal recurrence that was treated with surgical resection and radiotherapy and is currently alive at 12 months without disease. Although the survival of patients with limited resection in this series suggests that limited resection for 1 cm or less tumors may have equivalent results to lobectomy, the small sample size examined precludes any definitive conclusions. Furthermore, we were unable to distinguish clinically, either by CT or PET scanning, patients who had nodal metastasis or intralobar metastasis before resection. Of the 4 patients with N1 nodal metastasis and 5 patients with intralobar metastasis on final pathologic examination, only 1 patient was staged clinically as having more advanced than IA disease before resection. Clearly, a large prospective randomized trial comparing limited resection with lobectomy is mandatory before firm recommendations are made favoring limited resections over lobectomy for these small tumors.

PET scanning was performed in 37 patients preoperatively and 15 patients had a negative result, with a false negative rate of 41%. Among the 5 patients with pathologic nodal disease (N1 or N2) who had preoperative PET scanning, PET was positive in only 1 patient’s nodal station. The false negative rates in detection of the primary tumor as well as nodal metastasis are unacceptably high. Indeed, we¹⁷ have previously reported our results of PET scanning in 64 patients with NSCLC measuring 2 cm or less. Forty-five percent of tumors had negative PET results, and the PET sensitivity and specificity for nodal metastases were only 45% and 89%. Even though PET scanning has recently become a routine tool in preoperative evaluations of patients with NSCLC, our findings suggest that PET scanning has a very limited role in diagnosis and staging of tumors measuring 1 cm or less.

In the current series, mediastinal lymph node dissection was performed in 74 patients, 89% of the cohort. The incidence of N2 nodal metastasis was 2.4%. It is doubtful that this low incidence of upstaging by mediastinal nodal dissection will translate into a meaningful survival benefit in this population of patients. The Z0030 trial sponsored by the American College of Surgeons Oncology Group was designed to determine the survival benefits of mediastinal lymph node sampling versus complete nodal dissection at the time of resection for NSCLC. Ideally, the results of this trial (unpublished data) will clarify the role of mediastinal lymph node dissection.

In this current study, no significant difference in overall survival was observed between the open and the thoracoscopic lobectomy groups. The median length of stay in the hospital for the thoracoscopic group was 4 days compared with 5 days in the open lobectomy group. Although there is no published large randomized prospective series to compare the two approaches, various investigators have shown that thoracoscopic lobectomy can be done safely¹⁸ and with uncompromised survival.^19-21 For patients with subcentimeter tumors, thoracoscopic lobectomy might be an attractive approach.

There are several limitations in this study. This is a surgical series of resected NSCLC with a pathologic size of 1 cm or less. Our survival results should not be extrapolated to all NSCLC tumors measuring 1 cm or less in size at the time of diagnosis, because patients with obvious mediastinal or distant metastases might not have been referred for surgical evaluation. Patients who received neoadjuvant therapies were also excluded in this study because the pathologic size at resection might reflect treatment effects and not the true pathologic tumor size at the time of diagnosis. The sample size in our series is also too small to make any definitive recommendations on the roles of limited resection and mediastinal lymph node dissection in the management of NSCLC measuring 1 cm or less in size. Large prospective randomized studies are necessary to address these issues.

In summary, the number of NSCLC tumors measuring 1 cm or less that are detected is increasing because of the widespread use of CT and the emergence of screening programs. Even though the majority of tumors at resection are in stage IA, some of these tumors may have intralobar satellites or lymph node metastases. After surgical resection of NSCLC tumors measuring 1 cm or less, recurrence is rare and long-term survival is excellent.

	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): Paul C. Lee Robert J. Korst Jeffrey L. Port Nasser K. Altorki Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Lee, P. C. Articles by Altorki, N. K. Search for Related Content PubMed PubMed Citation Articles by Lee, P. C. Articles by Altorki, N. K. Related Collections Related Article