Journal of Clinical Oncology, Vol 21, Issue 6
(March), 2003: 1029-1034
© 2003 American Society for Clinical Oncology
Effect of Number of Lymph Nodes Sampled on Outcome in Patients With Stage I Non–Small-Cell Lung Cancer
Ajeet Gajra,
Nancy Newman,
Gary P. Gamble,
Leslie J. Kohman,
Stephen L. Graziano
From the Veterans Affairs Medical Center; and the State University of New York Upstate Medical University, Syracuse, NY.
Address reprint requests to Ajeet Gajra, MD, 800 Irving Ave (111H), Syracuse, NY 13210; email: ajeet.gajra{at}med.va.gov.
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ABSTRACT
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Purpose: We postulate that surgical sampling and pathologic evaluation of lymph nodes of surgical specimens from patients with stage I non–small-cell lung cancer (NSCLC) can have an effect on the time to recurrence and survival of these patients.
Patients and Methods: We analyzed data on 442 patients with stage I NSCLC who were treated with surgical resection and some form of lymph node sampling. Associations between total lymph nodes sampled and disease-free survival (DFS) and overall survival (OS) were investigated. The effect of total lymph node stations sampled and the surgical techniques (random lymph node sampling, systematic sampling [SS], or complete mediastinal lymph node dissection [MLND]) on DFS and OS was also studied. Complete MLND and SS were defined as dissection or sampling of levels 4, 7, and 10 for right-sided lesions and levels 5 or 6 and 7 for left-sided lesions.
Results: Patients were divided into quartiles on the basis of total number of lymph nodes sampled. Improved DFS and OS were associated with greater number of lymph nodes sampled. SS and MLND were associated with improved survival compared with random lymph node sampling. The total number of lymph nodes sampled maintained strong significance in the multivariate analysis.
Conclusion: These results indicate that examining a greater number of lymph nodes in patients with stage I NSCLC treated with resection increases the likelihood of proper staging and affects patient outcome. Such information is important not only for therapy and prognosis of individuals but also for identifying those who may benefit from adjuvant therapy.
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INTRODUCTION
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LUNG CANCER remains a major health problem in the United States, with an estimated overall 5-year survival rate of 14%.1 Although patients with stage I non–small-cell lung cancer (NSCLC) fare significantly better than those with more advanced disease, a significant fraction of the patients with stage I NSCLC have disease recurrence and die after a curative resection.2 Various pathologic and molecular markers have been assessed for their role in identifying the patients at high risk for recurrence. However, the tumor-lymph node-metastasis system stage remains the most important determinant of prognosis. The role of adjuvant therapy, chemotherapy, and/or radiation therapy is at best inconclusive. We postulate that surgical sampling and pathologic evaluation of lymph nodes of surgical specimens from patients with stage I NSCLC can have an effect on the time to recurrence and the survival of these patients. Recently, it has been shown that assessment of a greater number of lymph nodes correlates with improved survival in patients with pathologic stage T1 to T2, N0 colorectal, breast, and bladder cancers.3–5
The role of mediastinal lymphadenectomy in the staging and treatment of NSCLC remains controversial. Accurate intraoperative staging of NSCLC requires some assessment of the mediastinal lymph nodes. However, the degree to which the mediastinal lymph nodes should be sought and the extent of their removal remain controversial. Current surgical practice varies from mere visual inspection of the unopened mediastinum to radical lymphadenectomy. In all surgical cooperative group trials in North America, lymph node sampling is standard. There is some indication that complete ipsilateral mediastinal lymph node dissection (MLND) is important for accurate staging as well as overall survival (OS).6–8 Furthermore, the therapeutic effect of extensive mediastinal lymphadenectomy has been the subject of debate.9 A large, prospective randomized multicenter trial of mediastinal lymph node sampling versus complete lymphadenectomy during pulmonary resection in patients with N0 or N1 (less than hilar) NSCLC is currently under way (American College of Surgeons Oncology Group, ACOSOG protocol Z0030).
On completion of surgery, the assessment and reporting of lymph node specimens for evaluation of metastatic disease are not uniform, and they vary between laboratories and individual pathologists. This variation has led to recent guidelines for the processing and reporting of lymph node specimens submitted for evaluation of metastatic disease.10
The objective of this study was to evaluate the association between the number of lymph nodes sampled and recurrence and survival for patients with stage I NSCLC.
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METHODS
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Patients
Five hundred ninety-four patients with stage I NSCLC who underwent curative-intent surgery between 1979 and 1995 were identified from four hospitals in Syracuse, NY: University (State University of New York, Upstate Medical University), Veterans Affairs, Crouse, and St. Joseph’s Hospitals. Local institutional review board approval was obtained, but the study was exempted from informed consent by the patients or surrogates. The patients were identified from tumor registries, operating room records, and records of individual thoracic surgeons. Cases were excluded if there were two primary tumors at the time of diagnosis (9 patients), the patient did not leave the hospital after surgery or died within 30 days of surgery (20 patients), or did not meet the definition of stage I (T1 or T2, N0, M0) as defined by the American Joint Committee on Cancer (AJCC; Fig 1 ).11 Once identified, the patients’ charts, including pathology and operative reports, were reviewed, and the data were coded. Patients were excluded if the pathology report did not include microscopic description of at least one lymph node that was assessed and found to be negative for evidence of malignancy. Another 123 patients were excluded because adequate follow-up data were not available (69 patients), lymph nodes were not sampled at surgery (33 patients), or lymph nodes were not assessed miscroscopically by the pathologist (21 patients). Lymph nodes assessed at the time of mediastinoscopy (when performed), as well as the time of thoracotomy, were taken into account. The N1 lymph node count was obtained from the pathology reports. The N2 lymph node count was obtained by reviewing the operative notes and pathology reports. If more than one sample was obtained from a single station during mediastinoscopy, it was counted as a single lymph node. The mediastinal stations were defined as described in the AJCC cancer staging manual.11 Stations 1 through 9 were considered mediastinal nodes, and sampling/dissection at each of these levels was given a score of one. The characteristics of the remaining 442 patients are shown in Table 1. The pathology report and operative notes were obtained for each case. The number of lymph nodes was ascertained from the pathology report, and the number of stations was evaluated from the operative notes and pathology reports. The sampling operative procedures were defined per the definitions used by the Eastern Cooperative Oncology Group in the ECOG 3590 trial (Intergroup, INT 0115).9 Thus, systematic sampling (SS) was defined as removal or sampling of at least one lymph node at levels 4, 7, and 10 each for right-sided tumors and at levels 5 or 6 and 7 for left-sided tumors. Nodes sampled at mediastinoscopy within a month of the surgery were included only for patients who underwent lymph node sampling and not for patients who underwent lymphadenectomy. If patients had fewer lymph nodes sampled than as defined above, they were considered to have "random" sampling only. The patients who underwent complete MLND had complete lymph node dissections as dictated by prevailing surgical standards. Thus, patients who underwent right thoracotomy had superior mediastinal, hilar, subcarinal, inferior pulmonary, lobar, and interlobar lymph node dissection. At left thoracotomy, MLND was defined as anterior mediastinal, aortopulmonary window, subcarinal, hilar, tracheobronchial, inferior pulmonary ligament, lobar, and interlobar dissection. All studies were performed without knowledge of the patient’s outcome.
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Fig 1. Lymph node stations for lung cancer staging (reprinted with permission from the American College of Surgeons Oncology Group11).
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The following clinical and pathologic parameters were studied for each case: age, sex, T stage, tumor size, histologic type and grade, presence of mucin, pleural invasion, preoperative mediastinoscopy, and the number and stations of lymph nodes sampled and pathologically assessed. Because this is a retrospective analysis, information on some of the secondary variables studied was not universally available. Thus, 24 patients were lacking information regarding mucin expression (poor staining, lack of adequate tumor in the block, etc), and information regarding mediastinoscopy was only available on 334 patients. The numbers in Tables 1 and 3 reflect the actual number of patients for which information on any given variable was available.
Statistical Methods
The primary end point of this study was disease-free survival (DFS), which was defined as time from surgery to first locoregional or distant recurrence or to death. The OS was calculated from the date of surgery. An observation was censored at last follow-up if the patient was alive or if the patient had died from a cause other than the original NSCLC. Survival distributions for DFS and OS were estimated with the Kaplan-Meier method and compared with the log-rank test.12 The effect of lymph node evaluation was studied by total number of lymph nodes recovered by quartiles, number of mediastinal lymph node stations sampled, and type of surgical sampling procedure. Cox regression was used to determine simultaneously the associations between survival and the following potentially prognostic variables: number of lymph nodes assessed (by total numbers and stations), age (continuous variable), sex, operative procedure (lobectomy, bilobectomy, or pneumonectomy versus wedge resection), T stage (T1, T2), tumor differentiation (well-differentiated and moderately differentiated v poorly differentiated), and expression of mucin (yes, no).
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RESULTS
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Of the 442 patients included on the study, there were 262 males and 180 females. The median age at diagnosis was 65 years, with a range of 34 to 86 years. Adenocarcinoma was the predominant histology, and the majority of the patients were treated by lobectomy. The patient characteristics are listed in Table 1. The details in lymph node assessment are listed in Table 2. The median follow-up time for the group was 5.22 years. The median 5-year survival for the group was 70%, and the 5-year DFS was 64%. Patients were divided into quartiles on the basis of total number of lymph nodes sampled. For the first through the fourth quartiles (zero to three, four to six, seven to nine, and more than nine lymph nodes), the 5-year OS and DFS rates were 47%, 73%, 76%, and 79% (P < .0001) and 43%, 67%, 76%, and 75% (P < .0001), respectively (Table 3). The Kaplan-Meier survival curves for OS and DFS are depicted in Figs 2 and 3, respectively. At least six pathologic lymph nodes need to be studied to accurately define lymph nodal status. For patients with six or fewer lymph nodes assessed, DFS was 52%, and the patients with more than six lymph nodes assessed had DFS of 75% at 5 years (P < .001; Fig 4; Table 3).
Patients who underwent random sampling had worse outcomes when compared with those that had SS or complete MLND. The DFS rates at 5 years were 51%, 80%, and 80% (P < .0001) for random sampling, SS, and MLND, respectively (Fig 5). There was no difference for DFS and OS at 5 years when SS was compared with complete MLND.
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Fig 5. Disease-free survival with method of lymph node sampling, random versus systematic sampling (includes systematic sampling and mediastinal lymph node dissection).
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The number of mediastinal stations sampled were studied, as defined by the American Thoracic Society.11 Levels 10 and higher were considered N1 lymph nodes and not included. Patients with a greater number of mediastinal stations studied had an improved DFS and OS compared with patients with fewer mediastinal stations studied (Figs 6 and 7).
In the multivariate analysis, the total number of lymph nodes assessed maintained strong correlation with decreased risk for recurrence and improved OS (Table 4). The other significant factors associated with reduced DFS and OS were a higher T stage and wedge resection. A model evaluating SS and MLND versus random sampling was also examined. In that model, random sampling conferred a relative risk of 1.99 for death and 1.76 for recurrence (P < .001).
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DISCUSSION
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A 64% 5-year DFS rate for the patients in this series reinforces the fact that there is considerable room for improvement, because more than one third of the patients die of this potentially curable disease. Further, it is consistent with the survival for stage I NSCLC that is found in the existing literature.
Martini et al13 reported the importance of systematic lymph node dissection in stage I NSCLC. In this retrospective analysis, they found that 5- and 10-year survivals were significantly lower for the small subset of patients who did not undergo systematic lymph node sampling when they were compared with patients who underwent this procedure. The prognostic significance of the extent of lymph node dissection and evaluation in pathologic stage I NSCLC has been studied by Sawyer et al,14 who reported a statistically significant increase in locoregional recurrence and a decrease in OS in patients who had fewer than 15 lymph nodes dissected and pathologically assessed. In that study, a median of 23 lymph nodes were dissected and pathologically assessed. In the present study, however, the median number of lymph nodes assessed was six. The reason for this relatively small number is that our study included patients from 1978 until 1995, and systematic lymph node sampling was not well established at the institutes studied until the late 1980s. Further, although the majority of the patients in the current study were operated on at an academic center, one third were operated on at community hospitals, where aggressive lymph node sampling and pathologic assessment were not always followed. Despite the low median number, this study found that patients with fewer than six total lymph nodes and fewer than three mediastinal lymph nodes dissected and assessed had higher rates of recurrence and death when compared with patients with six or more total lymph nodes and three or more mediastinal lymph nodes assessed. The likely explanation for this observation is that having more lymph nodes dissected increases the staging accuracy, thereby appropriately upstaging the patients who would have otherwise been erroneously included among stage I patients. The other, less likely explanation is that removal of lymph nodes at lymphadenectomy may be therapeutic. There is indirect support for the association of radical systematic dissection (as opposed to lymph node sampling) with an improved outcome in patients with N2 disease.15 However, in a prospective randomized trial addressing this issue, Izbicki et al16 found that for patients with pN0 disease, lymphadenectomy did not have an effect on survival. Lymphadenectomy did appear to prolong relapse-free survival in patients with limited lymph node involvement (pN1 or pN2) in that trial. Sugi et al17 found that SS compared favorably with MLND in patients with T1, N0 tumors (size < 2 cm). No difference in recurrence and survival was found in this group with small primary tumors. However, in a recent retrospective analysis of 373 patients with stage II and IIIa NSCLC, the ECOG reported that systematic lymph node sampling is as efficacious as complete mediastinal lymph node dissection in staging patients with NSCLC.9 On subset analysis, this study found that complete mediastinal lymphadenectomy identified significantly more levels of N2 disease and was associated with improved survival only in patients with right-sided NSCLC. Wertzel et al18 assessed, among other factors, the number of lymph node sites sampled rather than the total number of lymph nodes, and they found no improvement in OS with increasing number of lymph node sites dissected. This may indicate the value of assessment of multiple lymph nodes at each site to improve the probability of identifying lymph nodes with metastatic disease and thereby identifying patients with "true" pathologic stage I NSCLC.
The simple explanation for our findings is the so-called "Will Rogers" phenomenon.19 When adequate lymph node sampling is not performed, the true N stage remains unrecognized because all the lymph nodes are not dissected and pathologically examined, which may result in a spurious downstaging of such patients. Nonetheless, these findings are important because, on the basis of the current surgical and pathologic evaluation processes, they indicate a significant role for lymph node assessment as a prognostic variable in stage I NSCLC. The results from the ongoing ACOSOG trial Z0030 should provide some definitive answers in this regard. However, it may take several years for those data to mature.
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DISCUSSION
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In addition to T stage, the total number of lymph nodes and lymph node levels sampled have a significant effect on DFS and OS in stage I NSCLC after resection. In this cohort of patients, age, sex, histology, and preoperative mediastinoscopy did not influence OS and recurrence-free survival. Patients with a greater number of total lymph nodes and lymph node stations assessed have a better outcome than those with fewer nodes and stations assessed. Similarly, patients undergoing SS and MLND have improved survival when compared with patients that undergo random sampling of mediastinal lymph nodes. This improved outcome is likely secondary to more accurate staging. Surgical resection should include adequate lymph node sampling and pathologic assessment.
These data are retrospective in nature, and they should be confirmed in prospective trials. On confirmation, they should help define surgical and pathologic practice of assessment of lymph nodes in patients with stage I NSCLC.
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ACKNOWLEDGMENTS
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Supported in part by the Veterans Affairs Merit Review Program.
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Submitted July 1, 2002;
accepted October 4, 2002.
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TOP
ABSTRACT
INTRODUCTION
