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Ann Thorac Surg 2002;73:1545-1551
© 2002 The Society of Thoracic Surgeons
a Division of General Thoracic Surgery, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA
b Section of Biostatistics, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA
* Address reprint requests to Dr Miller, Division of General Thoracic Surgery, Mayo Clinic and Mayo Foundation, 200 First Street, SW, Rochester, MN 55905 USA
e-mail: miller.danielmd{at}mayo.edu
Presented at the Thirty-seventh Annual Meeting of The Society of Thoracic Surgeons, New Orleans, LA, Jan 29–31, 2001.
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Abstract |
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Methods. The records of all patients were reviewed who underwent resection of solitary non–small cell lung cancers 1 cm or less in diameter from 1980 through 1999.
Results. The study included 100 patients (56 men and 44 women) with a median age of 67 years (range 43 to 84 years). Lobectomy was performed in 71 patients, bilobectomy in 4, segmentectomy in 12, and wedge excision in 13. Ninety-four patients had complete mediastinal lymph node dissection. The cancer was an adenocarcinoma in 48 patients, squamous cell carcinoma in 26, bronchioloalveolar carcinoma in 19, large cell carcinoma in 4, adenosquamous cell carcinoma in 2, and undifferentiated in 1. Tumor diameter ranged from 3 to 10 mm. Seven patients had lymph node metastases (N1, 5 patients; N2, 2 patients). Postsurgical stage was IA in 92 patients, IB in 1, IIA in 5, and IIIA in 2. There were four operative deaths. Follow-up was complete in all patients and ranged from 4 to 214 months (median 43 months). Eighteen patients (18.0%) developed recurrent lung cancer. Overall and lung cancer-specific 5-year survivals were 64.1% and 85.4%, respectively. Patients who underwent lobectomy had significantly better survival and fewer recurrences than patients who had wedge excision or segmentectomy (p = 0.04).
Conclusions. Because recurrent cancer and lymph node metastasis can occur in patients with non–small cell lung cancers 1 cm or less in size, lobectomy with lymph node dissection is warranted when medically possible.
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Material and methods |
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3 cm) from January 1980 through December 1999. Carcinoid and neuroendocrine tumors were excluded. A total of 1,417 patients were identified. One hundred of these patients (7.1%) had tumors that were 1 cm or less in diameter and these patients formed the basis of this study. All patients were staged postsurgically according to the TNM classification of the American Joint Committee for Cancer Staging and Revised International System for Staging Lung Cancer [2]. The medical record of each patient was examined for age and sex, preoperative pulmonary status and comorbidities, histology and tumor grade, tumor diameter, postsurgical stage, extent of pulmonary resection, and adjuvant chemotherapy or radiation therapy. Follow-up was obtained from the medical records, tumor registry surveys, and telephone interviews.
Statistical analysis
Operative mortality included patients who died within the first 30 days after operation and those who died later but during the same hospitalization. Analysis was carried out with the patients first divided into two groups by the type of oncologic procedure performed (formal resection [lobectomy] versus limited resection [segmentectomy and wedge excision]) and then by specific type of resection (lobectomy, segmentectomy, and wedge excision). Overall and lung cancer-specific survival was estimated by the Kaplan–Meier method using the date of the pulmonary resection as the starting point and the date of death or last follow-up as the end point [3]. The influence of variables on survival was analyzed using the log-rank test and the Cox proportional hazards model for continuous variables and for multivariate analysis [4]. All factors with a univariate significance of p less than 0.25 were entered into a multivariate Cox model for overall survival and lung cancer-specific survival [5]. The Wilcoxon rank sum test was used for group differences among continuous variables and Fisher’s exact test was used to test for association between pairs of categorical variables [6, 7]. A p value of less than 0.05 was considered significant.
Clinical findings
There were 56 men and 44 women with a median age of 67 years (range 43 to 84 years). Seventy-seven patients underwent a preoperative pulmonary function test. Median forced expiratory volume in 1 second (FEV1) was 65% of predicted (range 19% to 100% of predicted). Sixteen patients had abnormal pulmonary function (FEV1 less than 50% predicted) consistent with significant chronic obstructive pulmonary disease. Ninety patients were chronic cigarette smokers; 40 smoked up until the day of their operation, 7 smoked within 90 days of operation, and 43 had quit smoking more than 90 days before their operation. Ten patients never smoked.
Nineteen patients were symptomatic at the time of diagnosis: 14 had respiratory symptoms, which included fever, cough, and shortness of breath, and 5 presented with hemoptysis. The tumor was detected on chest radiograph in the patients presenting with respiratory symptoms, and with bronchoscopy in the patients who presented with hemoptysis. The tumor was discovered because of evaluation for other medical conditions in the remaining 81 patients: 68 had an abnormal chest radiograph and 13 had an abnormal computed tomography (CT). Three of these patients had their tumors detected because of enrollment in a low-dose spiral CT screening study for lung cancer.
Mediastinoscopy was performed in 9 patients: 4 had lymphadenopathy greater than 1.5 cm in diameter and 5 had normal lymphadenopathy on CT, but had associated medical comorbidities. A curative lung resection (R0) was performed in every patient. Bilobectomy was performed in 4 patients, lobectomy in 71, segmentectomy in 12, and wedge excision in 13; 2 of these patients had their wedge excision performed thoracoscopically. Reasons for limited resection included poor pulmonary reserve in 12 patients, associated comorbidities in 6, prior lung operation in 3, combined operation with a cardiac procedure in 2, incorrect original diagnosis in 1, and incidental finding in 1. Ninety-four patients had complete mediastinal lymph node dissection.
The tumor was an adenocarcinoma in 48 patients, squamous cell carcinoma in 26, bronchioloalveolar carcinoma in 19, large cell carcinoma in 4, adenosquamous cell carcinoma in 2, and undifferentiated in 1. The tumor was grade 3 or 4 in 66 patients and ranged in diameter from 3 to 10 mm; 57 tumors measured 10 mm. The tumor was located in the periphery of the lung in 89 patients, centrally in 3, and endobronchially in 8. Seven patients had lymph node metastases: N1 nodes were present in 5 and N2 nodes in 2. The postsurgical stage was IA in 92 patients, IB in 1, IIA in 5, and IIIA in 2.
No patient received radiation or chemotherapy before operation. Five patients had adjuvant treatment: radiation therapy was administered in 2, chemotherapy in 2, and both chemotherapy and radiation treatment in 1. Patients were selected to receive adjuvant therapy at the discretion of the surgeon and consulting oncologist.
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Results |
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Patients were divided into two groups for comparison by the type of oncologic procedure. The formal resection group included 75 patients who underwent bilobectomy and lobectomy. The limited resection group consisted of the remaining 25 patients, who underwent either a segmentectomy or wedge excision. There was no difference observed between these two groups with regard to preoperative variables except for degree of airway obstruction (Table 2). Median %FEV1 was 68% of predicted for the formal resection patients compared with 49% of predicted for the limited resection group (p = 0.001). Similarly, no differences existed between these groups with regard to perioperative variables (Table 3).
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Lymph node metastases were present in 7 patients, 6 in the formal resection patients and one in the limited resection patients. Lymph node metastases adversely affected survival, but not significantly. If hilar or mediastinal lymph nodes were metastatically involved, the overall 5-year survival was 43% (95% CI 18% to 100%) and if the lymph nodes were not involved with cancer, the 5-year survival was 66% (95% CI 55% to 78%) (p = 0.15) (Fig 5). Five-year lung cancer-specific survival was 87% (95% CI 77% to 97%) without lymph node metastases and 64% (95% CI 34% to 100%) with lymph node metastases. Again, this difference was not significant, but trending toward significance (p = 0.08) (Fig 6).
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Comment |
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Earlier screening trials using sputum cytology and chest radiographs did detect cancer at an early stage, but failed to demonstrate a decrease in mortality. As a result, these diagnostic modalities for lung cancer screening did not become widely accepted [9, 10]. More recently, screening trials using low-dose spiral CT are underway to detect even earlier disease (tumors less than 1 cm) with the hope that lung cancer mortality can be reduced [11]. Once detected, however, controversy exists as to the extent of pulmonary resection necessary (limited versus lobectomy) for cure. Controversy also exists as to the need for complete lymphadenectomy versus lymph node sampling.
The extent of surgical resection in patients with stage I NSCLC has been the subject of controversy for decades among surgeons and oncologists. Historically, lobectomy with mediastinal lymph node dissection has been considered the standard of care for stage I disease because this method allows removal of the entire primary tumor and the peripheral and central lymphatic drainage pathways that are potential sites of local and regional recurrence [12].
Several authors have suggested that limited pulmonary resection (wedge excision or segmentectomy) may be adequate surgical treatment for patients with early stage NSCLC [13–15]. However, these reports and others have demonstrated that local recurrence is higher with limited resection and survival may be compromised [16, 17]. With the development of video-assisted thoracic surgery (VATS), the role of limited resection in the treatment of early NSCLC has received increased attention [18]. In our series, no patient had a VATS lobectomy, but 2 patients had a VATS wedge excision.
Arguments favoring limited resection include low morbidity and mortality and, potentially, a shorter hospitalization. This advantage is especially relevant in patients with poor pulmonary function in whom limited resection techniques have evolved as a means of preserving pulmonary function. However, because the main goal of treatment for lung cancer is to cure the disease, limited resection should not be recommended unless medically necessary and every attempt should be made to perform a formal lobectomy to improve survival.
Advocates for limited resection argue that there is minimal risk of nodal involvement in these small tumors. Ishida and colleagues [19] found no lymph node metastases in patients with tumors 1 cm or less in size; however, 8 patients were included in this cohort. Also, in their series, tumors 1.1 to 2.0 cm had 17% nodal involvement whereas tumors 2.1 to 3.0 cm had lymphatic spread in 38% of cases. Others found similar results in the larger stage I adenocarcinomas [20, 21]. Seven percent of our patients had lymph node involvement even though the tumor measured 1 cm or less in diameter. Our study suggests that a patient with a 1-cm or smaller NSCLC should undergo a formal lobectomy with mediastinal lymph node dissection to ensure resection of all potential sites of lymphangitic spread. A recent nonrandomized trial showed that survival might be improved when complete lymphadenectomy is performed in patients with stage II and IIIA bronchogenic carcinoma [22]. Until the results of the American College of Surgeons Oncology Group Z0030 trial is known, complete mediastinal lymph node dissection should be performed. The Z0030 trial is a prospective randomized study of mediastinal lymph node sampling versus complete lymphadenectomy during pulmonary resection in patients with N0 or N1 (less than mediastinal) NSCLC. This trial is currently in its enrollment phase and the results will not be known for some time.
Three recent reports have examined the relationship between the extent of resection and survival in stage I NSCLC [16, 23, 24]. All three suggest that survival after lobectomy is superior to that after limited resection. Our overall 5-year survival was significantly improved for patients undergoing lobectomy when compared with limited resection. When further analysis subdivided the specific type of procedure performed, patients undergoing wedge excision had significantly worse overall and lung cancer-specific survival compared with lobectomy. The Lung Cancer Study Group (LCSG) demonstrated that patients who underwent segmentectomy and wedge excision had a higher recurrence rate and worse survival compared with lobectomy for stage IA NSCLC 3 cm or less in diameter [16]. From our data and the data from the LCSG, we would suggest that a standard lobectomy is preferred at this time for NSCLC less than 1 cm in diameter. Segmentectomy, however, may be an option in these smaller tumors. A large randomized study will be necessary to answer this question. Although we and others [20, 25–28] have examined the effect of tumor size on survival and local recurrence of resected stage I NSCLC, our current series is the first one to look at a consecutive cohort of NSCLCs 1 cm or less in diameter exclusively.
Tumor size and lymph node involvement are not the only factors that can impact survival after resection for stage IA disease. In a multivariate analysis of completed resected T1N0M0 tumors, Macchiarini and colleagues [29] were unable to correlate tumor size and survival. In their study, vascular invasion and mitotic index was the most important factors in predicting survival. In a similar study by Ichinose and colleagues [30], tumor size was not a significant predictor of survival, but with multivariate analysis, grade of differentiation and patterns of DNA ploidy significantly worsened survival in patients with stage I disease. Suzuki and colleagues [31] found that patients with stage IA who demonstrated moderate or poor differentiation or pleural involvement had a significant association with pathologic lymph node involvement, intrapulmonary metastasis, and lymphatic involvement by tumor. Even in lung cancers less than 2 cm in size, there was a high probability of local or regional recurrence when a limited lung resection was performed. In our study tumor differentiation was one of only two factors that significantly affected survival on multivariate analysis. Therefore, lung cancers 1 cm or less in diameter have the potential to spread locally, regionally, and even systemically.
Eighteen percent of our patients developed recurrent disease during the follow-up period. Locoregional recurrence is always a possibility especially after limited resection. The patients undergoing limited resection had higher overall and local recurrence rates than patients undergoing formal resection. Even though this difference was not significant, we found a 55% greater risk of developing recurrence after limited resection compared with lobectomy for NSCLC 1 cm or less in size. Similar results were demonstrated in the LCSG study in that 75% of patients developed higher local recurrence rate after limited resection then after lobectomy for all of stage IA disease [16]. When possible, formal resection with complete lymph node dissection is recommended to decrease the risk of recurrent disease.
The poor results in the limited group cannot be attributed to worst patient performance status preoperatively or more advanced disease at the time of resection as compared with the formal resection patients. The only difference between the groups on preoperative variables was preoperative pulmonary function. Both groups had reduced pulmonary function, but the level of impairment was only in the moderate range of severity. Also, among the patients with nodal metastases, fewer underwent limited resection (1) than formal resection (6). Therefore, the worst survival observed in the limited group could not be attributed to advanced disease at the time of resection or poor performance status preoperatively.
In conclusion, 1 cm NSCLC can lead to lymph node metastasis and survival can be affected by type of procedure performed at the time of resection. Formal lobectomy with lymph node dissection is warranted to achieve excellent long-term survival. The number of small lung cancers detected (1 cm in diameter or less) will likely continue to increase in the future as CT screening for lung cancer becomes more accepted. A prospective study is warranted to determine if lobectomy is the preferred treatment for these NSCLC 1 cm or less in size.
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The issue of how to treat patients with small solitary lung cancers is surely to be an important one as spiral CT screening becomes more prevalent: indeed, 80% of the tumors in this series were discovered incidentally. In their article they reported survival in terms of overall survival and also cancer-specific survival, and I believe that the latter is probably the most appropriate with which to look at the results. Their major conclusions involve the effect of lobectomy and also lymph node dissection. I found it surprising that although 89 of the 100 tumors were peripheral, only one of these tumors extended through the visceral pleura; there was only one tumor that became a stage IB. I would have expected a much higher incidence of patients having T2 lesions.
My questions are as follows. If you look at the lung cancer-specific 5-year survival, there was essentially no statistical difference in survival between lobectomies and limited resections, and therefore I would ask Dr Miller on what basis did he conclude that lobectomy is better? The second recommendation is that lymph node dissection should be done, and yet again, there was no statistical difference in cancer-specific survival whether lymph node dissection was performed or not. Indeed, staging was only changed in 7% of the patients, and one could argue that in the absence of any proven benefit from adjuvant therapy, this difference did not really matter much. Perhaps, Dr Miller, you could readdress the case for carrying out lymph node dissections in this group of patients.
Finally, we know that there should be about a 20% incidence of second primary cancers developing in this group, and indeed the cooperative groups are now testing in a randomized study if selenium can prevent these cancers. How do you know that some of your recurrences were not actually second primaries?
I congratulate Dr Miller and his coauthors on their results. As we look to determine through the time-honored method of randomized prospective trials the best way of treating these small tumors, formal lobectomy and lymph node dissection with its 91.9% cancer-specific 5-year survival has now been established by this study as the standard against which other treatments should be judged.
Thank you.
DR WILLIAM H. WARREN (Chicago, IL): This is an interesting and thought-provoking paper. I wonder if the authors could comment how many of these 5-mm lesions that were resected turned out not to be cancer. What were the criteria by which they decided to operate on 5-mm lesions? As you know, it can be extremely difficult to find these lesions intraoperatively, particularly if they are not subpleural. Did you use any localizing techniques?
DR MILLER: Doctor Feins, I would like to thank you for your comments. I agree with you that one of the major problems with retrospective studies is statistical analysis. In this study, 75 patients had undergone a lobectomy and 25 a limited resection consisting of either a wedge excision or segmentectomy. Although overall survival was statistically significant based on type of resection, lung cancer-specific survival was not, but there was a trend toward significance (p = 0.07). Even though the difference was not statistically significant we feel that the standard treatment at the present time for NSCLC less than 1 cm in diameter should be a lobectomy based on this trend.
Ninety-four of our patients had complete lymph node dissection. Again, the survival difference was not statistically significant (p = 0.06), but we believe that if we had had more patients in the limited resection group, the difference would be statistically significant. Here again is the drawback of a retrospective study.
There were 18 patients who developed recurrences; 7 occurred in the limited resection group and 11 in the lobectomy group. Of the 7 patients who had recurrences in the limited resection group, 4 were local. None of the patients developed a second primary tumor.
Doctor Warren, all of these tumors was primary bronchogenic carcinomas. Five tumors were less than 5 mm in size. It is of interest that the two 3-mm lung cancers were in the limited resection group. Both tumors were found incidentally in wedge excision specimens performed for diagnosis of an infiltrative process; one was a bronchoalveolar carcinoma and the other was an adenocarcinoma.
I agree with you that the detection of these lesions can be difficult at the time of planned thoracoscopic resection. Various techniques can be used to locate the lesion such as needle localization, methylene blue injection, agar injection, or intraoperative ultrasound. The majority of the time, however, you can find these lesions when they are located near the periphery of the lung by finger palpation. If the lesion is deep within the lung parenchyma, then repeating a CT scan in 3 months is an option that would allow the lesion to possibly grow so that thoracoscopic identification would be enhanced. I would not recommend proceeding directly to a thoracotomy for a lesion less than 5 mm in size unless growth of the lesion has been documented, thus preventing an unnecessary thoracotomy. The lung cancer for 3 of these patients was detected in our CT screening study for lung cancer.
I would like to close my comments by addressing the issue of lymph node dissection. Currently, the American College of Surgeons Oncology Group is sponsoring a study to determine the role of lymph node sampling versus complete lymph node dissection after formal resection for primary lung cancer. This study is the Z0030 trial and is in its enrollment phase. This trial will hopefully answer the question if complete lymph node dissection is warranted in conjunction with lobectomy for primary bronchogenic carcinoma of the lung. Until this study is completed and from our data presented today, we would recommend formal lobectomy with complete lymph node dissection for NSCLC 1 cm or less in diameter if the patient can tolerate the procedure medically.
Thank you.
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