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Ann Thorac Surg 1997;64:1402-1407
© 1997 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Effectiveness of Postoperative Irradiation in Stage IIIA Non–Small Cell Lung Cancer According to Regression Tree Analyses of Recurrence Risks

Divisions of Radiation Oncology, Thoracic Surgery, and Biostatistics, Mayo Clinic, Rochester, Minnesota

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Background. In the setting of grossly resected stage IIIA (N2 involvement) non–small cell lung carcinoma, the role of adjuvant postoperative thoracic radiation therapy (TRT) remains controversial. This study was initiated to subcategorize these patients into high-, intermediate-, and low-risk groups with respect to local recurrence and survival rates, and to determine whether there were certain subgroups of patients who were particularly likely or unlikely to benefit from postoperative TRT.

Methods. Two hundred twenty-four patients were studied. A regression tree analysis was used to separate patients who had undergone operation alone into groups that had a high, intermediate, or low risk of local recurrence and death. The effect of adjuvant postoperative TRT then was examined in each of these groups.

Results. The use of adjuvant postoperative TRT (compared with operation alone) was associated with an improvement in freedom from local recurrence and survival for patients who had an intermediate or high risk of local recurrence and death. However, the greatest level of improvement in freedom from local recurrence (p < 0.0001) and survival (p = 0.0002) associated with the use of adjuvant postoperative TRT was in the high-risk group. Similarly, but of lesser magnitude, the intermediate-risk group had improved freedom from local recurrence and survival rates with the use of adjuvant postoperative TRT (p = 0.002 and p = 0.01, respectively). For the low-risk group, the freedom from local recurrence and survival rates were not statistically different between the patients who received adjuvant postoperative TRT and those who underwent observation.

Conclusions. Patients with non–small cell lung carcinoma involving ipsilateral mediastinal lymph nodes (stage IIIA) who undergo gross resection and who are at either high or intermediate risk for local recurrence and death are likely to benefit from adjuvant postoperative irradiation. The role of radiation therapy in low-risk patients is unclear. Prospective confirmation of these observations is warranted.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
See also page 1407.

The presence of a survival benefit conferred by postoperative thoracic radiation therapy (TRT) in the setting of resected non–small cell lung cancer with pathologically involved ipsilateral mediastinal lymph nodes (N2, as defined by the American Joint Committee on Cancer [AJCC] [1]) remains controversial [2–9]. Many older retrospective studies, including one from our institution that evaluated a group of these patients treated from 1982 to 1986 [3], have suggested that the use of adjuvant postoperative TRT (compared with observation) is associated with an improved survival rate [4–6]. However, at least three contemporary randomized studies have failed to prove the benefit of this therapy [7–9]. Many of the early retrospective studies and all the prospective studies included small numbers of patients with involvement of N2 lymph nodes, and therefore did not have adequate power to assess differences in survival for patients who received adjuvant TRT compared with those who did not. More recently, a separate retrospective analysis from this institution, evaluating patients treated from 1987 to 1993, strongly suggested that the use of postoperative TRT led to higher rates of both local control (p = 0.0001) and survival (p = 0.0001) compared with observation. This latter study was strengthened by the fact that it included a sufficient number of patients with involvement of N2 lymph nodes (224 patients) to allow for meaningful comparisons of various cohorts of patients while it controlled for potential imbalances in prognostic factors through the use of a multivariate analysis [10, 11].

For patients with N2 disease who undergo complete gross resection, multiple tumor-related prognostic factors have been identified. These factors have included the number of involved N1 nodes [11], number of involved N2 nodes [9, 12], number of involved mediastinal nodal stations (as defined by Naruke and colleagues [13]) [3, 14], location of nodal involvement within the mediastinum [3, 6, 12–16], presence or absence of extracapsular nodal extension [17], pathologic margin status [11], AJCC T-stage [12, 15], status of the mediastinum on preoperative chest computed tomographic (CT) scan [15, 18], and status of the mediastinum on preoperative mediastinoscopy [19]. This list of prognostic factors for non–small cell lung cancer is lengthy but not exhaustive. Clearly, some of these patient and tumor characteristics are not independent prognostic factors. Further work will be necessary to decipher their interplay.

To gain better insight into the interplay of prognostic factors for patients who undergo total gross resection of stage IIIA non–small cell lung cancer, an attempt was made to use the previously noted prognostic factors to separate effectively patients into risk groups, with respect to both local control and survival, and to evaluate separately the role of adjuvant postoperative TRT in patients at comparatively low, intermediate, and high risk for both local recurrence and death.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Patients
To gather potential prognostic information on all patients who had undergone complete gross resection of stage IIIA (N2 involvement) non–small cell lung cancer between the years 1987 and 1993, the operative reports of all patients who had undergone thoracotomy for non–small cell lung cancer during this period were reviewed. Patients with contralateral mediastinal or supraclavicular involvement (N3), gross residual disease, or metastatic disease were excluded. Two hundred twenty-four patients were found to meet the defined criteria. This study involved a group of 224 patients with grossly resected stage IIIA non–small cell lung cancer who had been the subject of a previous report. In the previous report, the use of postoperative TRT in 88 of the 224 patients was associated with an improvement in freedom from local recurrence (FFLR) and overall survival compared with operation alone (136 patients). This result was confirmed in univariate and multivariate analyses [10, 11]. The present analysis was undertaken to combine multiple prognostic factors for the 136 patients who underwent operation alone in an effort to categorize them into risk groups (low, intermediate, and high) for local recurrence and survival. Subsequently, a secondary goal was to assess the role of radiation therapy in the various risk groups. To study these questions, a careful assessment was performed of each patient's preoperative evaluation, tumor characteristics, nodal characteristics, and subsequent treatment.

Preoperatively, the patients were deemed to be medical candidates for thoracotomy and mediastinal lymph node dissection. Preoperative studies were performed at the following frequencies: chest roentgenogram, 99.6%; chest CT, 79%; mediastinoscopy, 30%; bronchoscopy, 62%; and routine complete blood counts and chemistries, 100%. All patients then underwent thoracotomy and mediastinal nodal dissection. Of the 224 patients in this study, 33 (20 in the operation-alone group) underwent segmental or wedge resection, 115 (72 in operation-alone group) underwent lobectomy, and 76 (44 in the operation-alone group) underwent resection of more than one lobe or pneumonectomy. During the time frame of this study, the surgeons (VT, MA, PP, CD) adhered to a consistent surgical policy. This policy consisted of a complete mediastinal nodal dissection, which included resection of the following nodal groups: high paratracheal, mid/low paratracheal, subcarinal, paraesophageal, and inferior pulmonary ligament lymph nodes. Aortic and subaortic lymph nodes were dissected for left-sided tumors. Even though this general policy was undertaken, occasionally not all separate lymph node stations were labeled at the time of en-bloc resection or at the time of pathologic evaluation. However, review of pathologic reports showed that 98% of patients had multiple nodal stations identified and 51% had nodes from four or more stations identified.

On the basis of surgical and pathologic assessments, patients were assigned a surgical stage in accordance with the staging system of the AJCC [1]. In addition, AJCC N1 and N2 lymph nodes were assigned to 1 of 13 nodal stations (or levels) as adapted from Naruke and colleagues [13]. Superior mediastinal involvement was considered to be involvement of nodal stations 1 to 6, and inferior mediastinal involvement was considered to be involvement of nodal stations 7 to 9. Twenty-one of the 224 patients had at least one involved mediastinal lymph node that could not be classified retrospectively within the Naruke system. These lymph nodes were designated "mediastinal not otherwise specified" (mediastinal nos).

Adjuvant postoperative TRT was delivered in 88 of the 224 patients. The specifics of this therapy have been described previously [10, 11]; however, the median dose was 50.4 Gy in 5.5 weeks. During the time frame of this study, the Mayo radiation oncologists disagreed about the usefulness of postoperative TRT, and therefore the administration of treatment depended on the decision of the consulting radiation oncologist. Previously, it has been stated that there was a suggestion that patients with greater lymph node involvement were more likely to receive adjuvant TRT [10, 11]. Twenty-six of the 224 patients received adjuvant chemotherapy, and for 90% of those patients for whom the information was available, it was cisplatin-based. Twenty-four of the 26 patients who received chemotherapy also received TRT.

Statistical Analysis
Freedom from local recurrence and survival curves were calculated from the date of diagnosis using the method of Kaplan and Meier [20]. The log-rank analysis [21] was used to compare potential prognostic factors with respect to the previously outlined end points (FFLR and survival). Multivariate analysis by the method of Cox [22] was used to assess for the independence of prognostic factors.

To group patients into high-, medium-, and low-risk categories with respect to the risk of local recurrence and death, information on multiple prognostic factors was accumulated before initiating a regression tree analysis. An attempt was made to include as many as possible tumor- and patient-related characteristics that may represent potential prognostic variables (see earlier). The following factors were considered: age, sex, histology, histologic grade, primary tumor location by lobe of lung, T stage, N stage, number of involved N1 lymph nodes, number of involved N2 lymph nodes, number of involved N2 nodal stations, number of dissected N2 nodal stations, mediastinal level of involvement (inferior versus superior versus both), status of mediastinal lymph nodes on preoperative chest CT (enlarged defined as >1 cm), margin status (positive versus negative), use of TRT, and use of chemotherapy. Next, regression tree analyses were performed according to the method of Breiman and associates [23] by considering the relative prognostic significance (with respect to FFLR and survival) of these factors. These regression tree analyses were performed on the patients who had undergone operation alone so as to group patients into risk categories. Subsequently, the influence of adjuvant postoperative TRT was assessed for the patients in each category.

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
The prognostic factors outlined earlier were assessed with respect to FFLR and survival by the log-rank analysis [21]. The factors that were retained for the FFLR and survival regression tree analyses (Table 1; the description of discordant is provided later) were those that displayed the greatest level of prognostic significance (p < 0.2). It is of note that all except one of the factors that previously had been found to be of independent prognostic significance on multivariate analysis [10, 11] were included in this present regression tree analysis. The one factor that was excluded was the status of the surgical margins. Only 3 of the 224 patients had positive surgical margins, and therefore the inclusion of this factor in a global risk assessment of the 224 patients was not relevant. The previously reported independent prognostic factors regarding FFLR [10, 11] were as follows: number of involved N1 lymph nodes as assessed on a continuum and status of the surgical margins. The previously reported independent prognostic factors regarding survival [10, 11] were as follows: number of involved N1 lymph nodes as assessed on a continuum and level of mediastinal involvement (inferior versus superior versus both). These factors remained the only independent prognostic factors even after the inclusion of a new factor in this analysis (status of preoperative CT scan).

In addition to the status of the preoperative chest CT, neither the finding of extracapsular nodal extension nor the results of preoperative mediastinoscopy were included in the regression tree analysis. The finding of extracapsular nodal extension was not noted routinely by the Mayo pathologists during the time frame of this study. Preoperative mediastinoscopy was performed in 30% of patients; however, only 6 patients were found to have N2 disease at this evaluation. Therefore, the inclusion of this factor in the regression tree analysis would not have been meaningful.

This analysis of potential prognostic factors related to local recurrence and survival began with an analysis of grouped couplets of prognostic factors and initially included only the 136 patients with operation alone. Through this process, the previously known association between the lobe of origin of the primary tumor and the level of mediastinal involvement was corroborated. It was found that upper lobe tumors more commonly metastasized to superior mediastinal lymph nodes compared with inferior mediastinal lymph nodes. In addition, the inferior (rather than superior) mediastinum was involved more commonly for lower lobe tumors. There also were trends toward decreased FFLR and survival for patients who presented with tumors in discordance with this "rule." The term "discordant" was used to refer to upper lobe or lower lobe tumors with inferior or superior mediastinal involvement, respectively. "Accordant" patients were found to have a 4-year FFLR rate of 47%, versus 31% for "discordant" patients (p = 0.08). The 4-year overall survival rate for accordant patients was 24%, compared with 14% for discordant patients (log-rank p = 0.07). This grouping proved to be useful for the remaining regression tree analysis of risk categories. It was discovered that the group of patients with middle lobe tumors or involvement of the mediastinal nos lymph nodes was found to have similar rates of local recurrence and overall survival compared with the accordant patients, and thus they were included in this group.

Using the prognostic factors outlined in Table 1, a regression tree analysis for FFLR was performed. The results of this analysis are shown in Figure 1 (low-risk group: 42 patients; intermediate-risk group: 69 patients; high-risk group: 24 patients [data missing on 1 patient]). The four variables shown to be the most useful for grouping nonirradiated patients into prognostic groups included the number of involved mediastinal levels (one level versus both superior and inferior levels), the number of involved N1 lymph nodes (none versus one or more), the AJCC T-stage (T1 to T2 versus T3 to T4), and the discordant versus accordant designations.

View larger version (35K): [in this window] [in a new window]   Fig 1. . Patients at low, intermediate (Int), and high risk for local recurrence were identified. (Neg = negative.)

View larger version (46K): [in this window] [in a new window]   Fig 2. . Patients at low, intermediate, and high risk for death were identified.

View larger version (18K): [in this window] [in a new window]   Fig 3. . The freedom from local recurrence rates in the low-, intermediate-, and high-risk groups were found to be well separated.

View larger version (16K): [in this window] [in a new window]   Fig 4. . The survival rates in the low-, intermediate-, and high-risk groups were found to be well separated.

View larger version (23K): [in this window] [in a new window]   Fig 5. . Adjuvant irradiation was associated with a higher freedom from local recurrence rate in patients at both high risk (right; 46 patients) and intermediate risk (middle; 116 patients) for local recurrence. This also was true in low-risk (left; 61 patients) patients, although this difference was not statistically significant.

View larger version (18K): [in this window] [in a new window]   Fig 6. . Adjuvant irradiation was associated with a higher survival rate in patients at both high risk (right; 65 patients) and intermediate risk (left; 149 patients) for death. There were only 9 patients in the low-risk category.

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

In fact, the results of this analysis suggested that whereas both the intermediate-risk and the high-risk group experienced a radiation-associated survival benefit, it was the patients who were at highest risk for local recurrence who benefited the most. There was nearly a 10-fold increase in the 4-year actuarial survival rate for those high-risk patients who received adjuvant postoperative TRT compared with those who did not (37% versus 4%, respectively; p = 0.0002). This high level of significance associated with the improved survival for patients who received adjuvant postoperative TRT (compared with observation) in the high-risk group of patients was greater than the comparable comparison in the intermediate-risk (p = 0.01) and low-risk groups (p = 0.62). In addition, the use of adjuvant postoperative TRT (compared with observation) in the intermediate- or low-risk patients was associated with a 2-fold or lower increase in the actuarial 4-year survival rate. Therefore, even though the high-risk patients had the greatest chance of death caused by lung cancer (usually as a result of disseminated disease), this analysis suggested that many of these patients had localized disease at the onset of therapy, and therefore may benefit greatly from aggressive local therapy.

These defined risk categories for local recurrence and survival must be viewed only in the context of the study population, because stage IIIA (N2 involvement) non–small cell lung cancer currently affects a wide variety of patients. The patients in this study can be considered a relatively favorable group of patients with stage IIIA tumors, because they all had resectable disease and only 6 patients were found to have disease at mediastinoscopy or mediastinotomy (however, one or both of these procedures were performed in only 66 of the 224 patients). Because analyses of optimal therapy for these patients with stage IIIA disease were performed as outlined previously, it also is important to note that two recent randomized trials have demonstrated survival advantages with the administration of neoadjuvant chemotherapy followed by surgical resection versus surgical resection alone for patients with grossly involved N2 disease. The N2 disease in both studies had been diagnosed at prethoracotomy mediastinoscopy after detection by chest CT [24, 25]. The patients included in these analyses, therefore, may represent a group of patients with more advanced disease compared with those in the present analysis. Given the facts that the studies by Roth and colleagues [24] and Rosell and associates [25] included small numbers of patients, that the follow-up period was short in both studies, that the Roth study accrued patients at a very slow rate and then was discontinued in accordance with an unplanned interim analysis, and that patients with T3N0 disease made up approximately 25% of the patients in both studies (these patients would be expected to have a better prognosis [12, 13, 26–31]), neoadjuvant chemotherapy remains controversial and currently is being studied in a large intergroup trial. In addition, the role of neoadjuvant chemotherapy for nonbulky stage IIIA disease, as found in this study (only 33% of patients had enlarged N2 nodes on CT), currently is undefined and requires future study.

The significance of this study is the potential usefulness of the identified prognostic categorization for patients with stage IIIA (N2 involvement) non–small cell lung cancer who have undergone gross resection and mediastinal nodal dissection. The described categorization will help clinicians assess a given patient's risk of recurrence and may help in the stratification processes of future randomized studies for this group of patients. In addition, this study and the previously published multivariate analysis [10, 11] suggest that further prospective study of postoperative TRT is warranted for this group of patients.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Presented at the Poster Session of the Thirty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Feb 3–5, 1997.

Doctor Sawyer's current address is Walter Reed Army Medical Center, Washington, DC.

Address reprint requests to Dr Bonner, Mayo Clinic, CH-R, 200 First St, SW, Rochester, MN 55905.

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 

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This Article Abstract 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): Claude Deschamps Victor F. Trastek Peter C. Pairolero Mark S. Allen Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Sawyer, T. E. Articles by Li, H. Search for Related Content PubMed PubMed Citation Articles by Sawyer, T. E. Articles by Li, H. Related Collections Related Article