Original Article
A Randomized Trial Comparing Preoperative Chemotherapy Plus Surgery with Surgery Alone in Patients with Non-Small-Cell Lung Cancer
N Engl J Med 1994; 330:153-158January 20, 1994
- Abstract
Background
The efficacy of surgery for patients with non-small-cell lung cancer is limited, although recent studies suggest that preoperative chemotherapy may improve survival. We conducted a randomized trial to examine the possible benefit of preoperative chemotherapy and surgery for the treatment of patients with non-small-cell lung cancer.
Methods
We studied 60 patients (59 men and 1 woman) with stage IIIA non-small-cell lung cancer. The patients were randomly assigned to receive either surgery alone or three courses of chemotherapy (6 mg of mitomycin per square meter of body-surface area, 3 g of ifosfamide per square meter, and 50 mg of cisplatin per square meter) given intravenously at three-week intervals and followed by surgery. All patients received mediastinal radiation after surgery. The resected tumors were evaluated by means of K-ras oncogene analysis and flow cytometry.
Results
The median period of survival was 26 months in the patients treated with chemotherapy plus surgery, as compared with 8 months in the patients treated with surgery alone (P<0.001); the median period of disease-free survival was 20 months in the former group, as compared with 5 months in the latter (P<0.001). The rate of recurrence was 56 percent in the group treated with chemotherapy plus surgery and 74 percent in the group treated with surgery alone. The prevalence of mutated K-ras oncogenes was 15 percent among the patients receiving preoperative chemotherapy and 42 percent among those treated with surgery alone (P = 0.05). Most of the patients treated with chemotherapy plus surgery had tumors that consisted of diploid cells, whereas the patients treated with surgery alone had tumors with aneuploid cells.
Conclusions
Preoperative chemotherapy increases the median survival in patients with non-small-cell lung cancer.
Media in This Article
Figure 1
Kaplan-Meier Plot of Disease-free Survival in Patients with Stage IIIA Lung Cancer Treated with Surgery Alone (Dashed Line) or Chemotherapy plus Surgery (Solid Line).Figure 2
Kaplan-Meier Plot of Overall Survival in Patients with Stage IIIA Lung Cancer Treated with Surgery Alone (Dashed Line) or Chemotherapy plus Surgery (Solid Line).Article Activity
- Article
At present, the role of surgery in the treatment of patients with non-small-cell lung cancer, stage IIIA (locally invasive primary tumors or tumors associated with involvement of the ipsilateral mediastinal lymph nodes [N2]), is controversial1,2. An evaluation of the results of surgery is limited by variations in the proportion of patients with stage IIIA disease detectable by computed tomography (CT) and the definition of complete resection3. In four separate studies of a total of 1180 patients who underwent tumor resection, the five-year survival rates ranged from 14 to 30 percent1,3-5.
Preoperative chemotherapy may improve the prognosis for patients with stage IIIA non-small-cell lung cancer. In one study the response rate was 60 percent, half the patients were able to undergo resection, and the median survival was increased by eight months6. In several phase 2 trials of preoperative chemotherapy in a total of 463 patients, the response rates ranged from 51 to 77 percent, 63 to 90 percent of the patients had resectable tumors after chemotherapy, the median period of survival ranged from 13 to 32 months, and the 3- to 5-year survival rates ranged from 17 to 40 percent7-13. Factors such as the heterogeneity of the patients studied, variations in the extent of resection, and lack of a consensus about inclusion criteria limit the conclusions that can be drawn from these studies. A few randomized studies have addressed the benefit of preoperative chemotherapy14-16. Among the patients in these trials, the three-year survival rate ranged from 25 to 40 percent for those treated with chemotherapy plus surgery and from 15 to 40 percent for those treated with surgery alone. Our trial was designed to assess the effect of preoperative chemotherapy on the survival of patients with stage IIIA non-small-cell lung cancer. The chemotherapy regimen was designed to result in a 60 percent response rate, a rate of disease progression during chemotherapy of less than 10 percent, and only mild toxicity. We also tested the effect of chemotherapy on tumor-cell DNA and examined the mutational state of the K-ras oncogene. A combination of mitomycin, ifosfamide, and cisplatin, as described by Cullen et al.,17 was chosen as the preoperative chemotherapeutic regimen.
Methods
Patients
We studied 60 patients with histologically confirmed non-small-cell lung cancer in stage IIIA according to the tumor-node-metastasis (TNM) classification18. A bronchoscopy was performed, and biopsy specimens and washings were obtained to determine the extent of involvement of the tracheobronchial tree. Eligibility criteria included the presence of measurable lesions that could be evaluated, a Karnofsky performance score of 70 or higher, a leukocyte count above 4000 per cubic millimeter, a platelet count above 100,000 per cubic millimeter, normal renal and hepatic function, and adequate pulmonary function. Pulmonary function was assessed by calculating the ratio of the forced expiratory volume in one second (FEV) to the forced vital capacity (FVC). A predicted postoperative FEV equal to at least 1 liter and more than 34 percent of the normal value was required for enrollment in the study. In borderline cases, ventilation-perfusion scanning was also performed to predict postoperative pulmonary function19,20.
A medical panel composed of a thoracic surgeon, a radiologist, a chest physician, and a medical oncologist confirmed the stage of disease in each patient. Mediastinoscopy or mediastinotomy with a biopsy was carried out in all patients with N2 disease detected by CT (83 percent of the patients treated with chemotherapy plus surgery and 63 percent of those treated with surgery alone). CT of the brain was performed if the histologic studies showed that the primary tumor was an adenocarcinoma or if neurologic signs suggested that the disease involved the central nervous system. Radionuclide bone scanning was carried out if either the clinical symptoms suggested bone infiltration or the serum alkaline phosphatase concentration was elevated. Lymphadenopathy was evaluated by CT; metastatic lymph nodes were defined as mediastinal nodes larger than 10 mm along their short axis or subcarinal nodes larger than 15 mm21. If the radiologist on the medical panel saw no adenopathy on the CT scan, the patient was considered to have no mediastinal involvement. In all patients with N2 disease that was confirmed histologically, the disease was apparent on the CT scan but not on the plain chest film. The presence of satellite nodules, defined as well-circumscribed accessory foci of carcinoma adjacent to the primary tumor but clearly separated from it by normal parenchyma, was considered to signify a subcategory of stage IIIA disease classified as T3 disease22.
The study protocol was approved by the research review committee for the protection of human subjects at each institution participating in the study. All patients gave informed consent.
Treatment
Patients were randomly assigned to undergo either immediate surgery or surgery preceded by three courses of chemotherapy given at three-week intervals. The chemotherapeutic regimen consisted of mitomycin (6 mg per square meter of body-surface area given in an intravenous bolus dose), ifosfamide (3 g per square meter mixed with mesna [1 g per square meter] and given intravenously over the course of three hours), and cisplatin (50 mg per square meter given intravenously over the course of one hour). Additional mesna and hydration were given as described by Cullen et al.17. As antiemetic therapy, metoclopramide (3 mg per kilogram of body weight) was given intravenously 30 minutes before and 90 minutes after the chemotherapy. Dexamethasone (20 mg) was given intravenously with the first dose of metoclopramide; lorazepam (1.5 mg per square meter) was given orally at the same time. The chemotherapy was administered on an outpatient basis. After the third course of chemotherapy, just before surgery, chest CT was repeated to assess the response to chemotherapy. The patients judged to have resectable tumors then underwent surgery.
A thoracotomy was performed within four to five weeks after the third course of chemotherapy in the patients thought to have resectable tumors. During the operation, the ipsilateral mediastinal and subcarinal lymph nodes were resected, as were the subaortic, para-aortic, and paraesophageal nodes. However, mobilization of the aortic arch and the descending aorta to allow more extensive removal of the superior mediastinal nodes was not performed23.
Patients randomly assigned to undergo surgery without chemotherapy were operated on within two weeks after enrollment. Both patient groups received mediastinal radiation, begun approximately four weeks after surgery and given in a combination of parallel opposed, anterior, and posterior oblique fields. A daily dose of 1.8 to 2.0 Gy delivered in the central axis at the midplane was given five days per week until the patient had received a cumulative dose of 50 Gy. Field outlines extended from the thoracic inlet to 5 cm below the carina. The field included the bronchial stump, ipsilateral hilum, and vascular shadows of the mediastinum bilaterally. The total dose to the spinal cord was 40 Gy.
All patients were reevaluated every three months with a physical examination, laboratory tests, chest films, and chest and abdominal CT scans. A complete response to preoperative chemotherapy was defined as the absence of all radiographic abnormalities after chemotherapy, and a partial response was defined as a reduction of 50 percent or more in the product of two perpendicular diameters of the tumor. Stable disease was defined as less than a 50 percent reduction in the tumor, less than a 25 percent increase in the sum of the products of two perpendicular diameters of all measured lesions, and no new lesions. Progressive disease was defined as an increase of more than 25 percent in the product of two perpendicular diameters of any measured lesion.
K-ras Oncogene Point Mutations
Tumor specimens obtained at the time of surgery were fixed with formaldehyde, embedded in paraffin, and evaluated for point mutations at codons 12, 13, and 61 of the K-ras oncogene. DNA was isolated from 15-micrometer sections of tissue blocks with a rapid-lysis procedure. Conditions for the polymerase chain reaction and the detection of point mutations with mutation-specific oligonucleotides have been described by Slebos et al.24. Briefly, ras-specific sequences were amplified by the polymerase chain reaction for 35 cycles. DNA was subjected to electrophoresis on 4 percent agarose gel and then stained with homidium bromide. The amplified products of the polymerase chain reaction were denatured and dotted onto hybridization membranes. Each membrane was then hybridized separately for one hour with radiolabeled, mutation-specific oligonucleotide probes. Specific hybridization was detected by autoradiography at -70 °C for 18 to 24 hours.
Flow Cytometric Analysis
The tumors were analyzed by flow cytometry. Sections that were 50 micrometers thick were cut from each paraffin block that contained at least 25 percent neoplastic tissue and had no secondary degenerative changes (necrosis or hemorrhage). The tissue was deparaffinized, rehydrated, and incubated at 37 °C for one hour in a 0.5 percent pepsin solution (pH 1.5). Disaggregated tissue was filtered through a 35-micrometer nylon mesh, incubated with ribonuclease I (100 μg per milliliter), and then stained with propidium iodide (50 μg per milliliter) at 4 °C for a minimum of 12 hours and a maximum of 16 hours. Nuclear-cell suspensions were analyzed with a flow cytometer (FACScan, Becton Dickinson, San Jose, Calif.) and a CellFit program. An average of 10,000 cells from each sample were evaluated. Non-neoplastic lung parenchyma included in the same paraffin block or in another block from the same patient was used as a diploid standard. Diploid tumor cells were defined as cells having only one G0/G1 peak with a coefficient of variation of less than 8.0. Aneuploid cells were defined as cells with any distinct peak other than the G0/G1 peak, depending on the position of the aneuploid cells after the test sample had been mixed with the biologic standard (diploid control)25.
Study Design, Statistical Analysis, and Quality Control
The trial was designed as a prospective, randomized, nonblind study. Randomization of patients at participating centers was accomplished by telephone calls to the study office. The patients were stratified according to the size and location of the primary tumor, its histologic characteristics, and the number of N2 lymph-node groups that were positive for tumor cells. The primary objective was to determine whether preoperative chemotherapy would improve the anticipated five-year survival rate of 9 percent for patients with resectable stage IIIA disease confirmed by mediastinoscopy. The secondary objectives were to determine the rate of response to preoperative chemotherapy and related toxicity and to analyze the DNA content and K-ras oncogene activation in tumor samples obtained during surgery. The start of the study was considered to be the time of the first course of chemotherapy in the patients treated with chemotherapy plus surgery and the time of surgery in those treated with surgery alone. Follow-up analyses were carried out 12, 18, and 24 months after the start of the study by members of the Spanish Lung Cancer Group audit committee.
Parametric and nonparametric tests were used to compare the results in the two treatment groups. Survival curves, constructed with the date of randomization as the starting point, were computed according to the Kaplan-Meier method, and differences in survival were compared with the log-rank test for censored data. The Brookmeyer-Crowley method was used to calculate the confidence interval for the median period of survival26. A proportional-hazards regression analysis was used to determine the effects of different variables on survival. Six variables were analyzed: the size and location of the tumor, histologic characteristics, node stage, number of lymph-node levels affected, and treatment group. A score was assigned to each variable for the regression analysis. Qualitative data (the location of the tumor, histologic characteristics, and treatment group) were analyzed with chi-square tests. All reported P values are two-tailed; all analyses were performed with BMDP software27.
Results
Between December 1989 and May 1991, we enrolled 63 patients at the three hospitals participating in the study. An analysis28,29 after 24 months showed a significant difference in survival, and enrollment was therefore stopped. Three patients who were later found to be ineligible because of poor pulmonary function at the time of randomization were excluded from the analysis. Among the remaining 60 patients, 30 were assigned to preoperative chemotherapy, and 30 to immediate surgery. The oldest patient was 78 years old. All patients had a high Karnofsky score, and the majority had squamous-cell carcinoma. The median duration of follow-up among the surviving patients was 24 months in the chemotherapy-plus-surgery group and 19 months in the surgery group.
There were no significant differences between the two groups in any of the characteristics listed in Table 1Table 1
Base-Line Characteristics of Patients with Non-Small-Cell Lung Cancer, According to Treatment Group.. Twenty-five of the 30 patients in the chemotherapy-plus-surgery group had N2 disease, as compared with 19 of the 30 in the surgery group. The remainder had T3N0 or T3N1 disease but with unfavorable prognostic factors, such as soft-tissue infiltration, rib involvement, or pericardial invasion. The median tumor size was larger than 5 cm in both groups (Table 2Table 2
Characteristics of the Tumors, According to Treatment Group.); four patients in the chemotherapy-plus-surgery group had satellite nodules. A large proportion of patients had lymph-node metastases at two N2 levels. All 30 patients in the chemotherapy-plus-surgery group received the three courses of chemotherapy as scheduled, with minimal or no toxic effects. The lowest leukocyte count was 2000 per cubic millimeter, and the lowest platelet count was 100,000 per cubic millimeter. There were no life-threatening episodes of neutropenia, and no patients had nephrotoxicity. Nausea and vomiting, when they occurred, were mild. Most patients had grade 1 or 2 alopecia.In the chemotherapy-plus-surgery group, 16 patients (53 percent) had a partial radiographic response, and 2 patients (7 percent) had a complete response. At the end of the study, 11 patients were deemed to have stable disease, and only 1 patient (3 percent) had progressive disease, as evidenced by liver metastases detected after chemotherapy; this patient did not undergo surgery. One patient who had a complete response and one who had a partial response refused the surgery. Twenty-three of the 27 patients who underwent surgery had a complete resection. The tumors in the other four patients were not resectable because of encasement of the great vessels. Only one patient, who had an adenocarcinoma and a complete response to chemotherapy, had no residual tumor in lung tissue or nodes removed during surgery. Four patients had no detectable primary tumor, but microscopical foci were found in the lymph nodes. In the surgery group, 27 of 30 patients had complete resections. There were no significant differences between the two treatment groups with respect to the surgical procedures that were used (Table 3Table 3
Response to Chemotherapy and Results of Surgery, According to Treatment Group.). Four patients died within 30 days after surgery, two in each treatment group (overall mortality rate, 7 percent): two patients died of pneumonia, one of an acute pulmonary embolism, and one of a bronchopleural fistula and respiratory arrest.There were significant differences in disease-free and overall survival between the two groups. The median period of disease-free survival in the surgery group was 5 months (95 percent confidence interval, 4 to 7), as compared with 20 months (95 percent confidence interval, 12 to 30) in the chemotherapy-plus-surgery group (P<0.001) (Figure 1Figure 1
Kaplan-Meier Plot of Disease-free Survival in Patients with Stage IIIA Lung Cancer Treated with Surgery Alone (Dashed Line) or Chemotherapy plus Surgery (Solid Line).). Similarly, the median overall survival in the surgery group was 8 months (95 percent confidence interval, 7 to 10), as compared with 26 months (95 percent confidence interval, 16 to 34) in the chemotherapy-plus-surgery group (P<0.001) (Figure 2Figure 2Kaplan-Meier Plot of Overall Survival in Patients with Stage IIIA Lung Cancer Treated with Surgery Alone (Dashed Line) or Chemotherapy plus Surgery (Solid Line).). The differences in survival between the two groups were significant irrespective of the patient's age, the histologic subtype of the tumor, its location and size, and the number of N2 levels involved. The risk of death in the surgery group was five times that in the chemotherapy-plus-surgery group (hazard ratio, 5; 95 percent confidence interval, 2 to 17). During follow-up, 56 percent of the patients in the chemotherapy-plus-surgery group had a relapse, as compared with 74 percent of those in the surgery group (P = 0.65). The tumor recurred at a local or regional site in 54 percent of the chemotherapy-plus-surgery group, whereas the tumor recurred as a metastasis in 55 percent of the surgery group.Tumor Evaluation
Among the 50 patients who had complete resections, biopsy specimens from all but 4 yielded adequate tissue for isolation of DNA and amplification by polymerase chain reaction. Amplification of DNA revealed K-ras oncogene point mutations in 3 of 20 patients (15 percent) in the chemotherapy-plus-surgery group and in 10 of 24 (42 percent) in the surgery group (P = 0.05). In three of the tumors from the surgery group, the normal DNA sequence at codon 12, GGT (guanine, guanine, and thymine), encoding glycine, was replaced by GAT (guanine, adenine, and thymine), encoding aspartic acid instead of glycine; three tumors contained GTT (guanine, thymine, and thymine), encoding valine; and two contained TGT (thymine, guanine, and thymine), encoding cysteine. The remaining two tumors contained mutations at codon 61, as did the three tumors from the patients in the chemotherapy-plus-surgery group. Of the three patients in the chemotherapy-plus-surgery group whose tumors had mutated K-ras oncogenes, two had no objective response to treatment: one died of local and regional disease, and the other had brain metastases after 21 months of follow-up and died 5 months later. The third patient, who had a partial response, had brain metastases and died after 14 months of follow-up. Of the 10 patients in the surgery group whose tumors contained mutated K-ras oncogenes, 9 died: 5 had bone metastases, 2 had liver metastases, 1 had distant lymph-node metastases, and 1 had a recurrence of the tumor at local and regional sites.
Of the 46 specimens that contained enough tumor tissue for flow cytometry, 9 could not be analyzed (5 specimens from the surgery group and 4 from the chemotherapy-plus-surgery group) because of low-quality histograms. Only 5 of the 17 tumor specimens from the chemotherapy-plus-surgery group (29 percent) were aneuploid, whereas 14 of the 20 tumor specimens from the surgery group (70 percent) were aneuploid (P = 0.02). For three of the patients in the chemotherapy-plus-surgery group, biopsy tissue obtained before chemotherapy was analyzed, in addition to the tissue removed during the surgery that followed chemotherapy. In all three cases, the DNA content of the tumor was aneuploid in the specimen obtained before chemotherapy but diploid in the specimen obtained afterward.
Discussion
This phase 3 trial addressed the effect of preoperative chemotherapy on the survival of patients with clearly defined, stage IIIA non-small-cell lung cancer. The patients were stratified according to the location and size of the tumor and according to lymph-node status, because in other series30,31 survival varied according to the location and size of the primary tumor and the number of lymph-node levels involved. In our analysis, however, the location of the tumor, its size, and the number of N2 levels involved were not significant predictors of survival. The results of this trial demonstrate that preoperative chemotherapy improves survival.
Patients who have tumors with K-ras oncogene point mutations constitute a subgroup with a low rate of response to treatment, regardless of the stage of the disease32,33. In our previous study we found ras gene mutations in 20 percent of the patients with non-small-cell lung cancer whose tumors were resected, and this subgroup had the poorest survival34. The difference was also confirmed in the 12 patients with microscopical N2 disease: the median survival time was 15 months for the 9 patients who had tumors without K-ras oncogene mutations, as compared with 5 months for the 3 patients who had tumors with K-ras mutations34. Paradoxically, in the present study, the survival of the 24 patients in the surgery group who had complete resections was not related to the presence or absence of mutated K-ras oncogenes. This discrepancy may be explained by the fact that bulky disease (a large tumor and clinically detectable N2 disease) itself signifies an unfavorable prognosis, in comparison with microscopical metastases discovered in mediastinal lymph nodes after surgery.
The difference between the ploidy patterns in the two treatment groups can be attributed to the effect of chemotherapy or possibly to a secondary effect of the relative decrease in the number of tumor cells due to an increase in the number of inflammatory and stromal cells. The differences in ploidy between the groups were significant, indicating an effect of chemotherapy and confirming its effect on different tumors35. Chemotherapy may reverse the pattern of ploidy by selecting tumor subclones in which the DNA content is close to the diploid value and destroying those with a larger number of alterations in the DNA content.
Although the rules for stopping the trial were strictly followed, the early interruption in the enrollment of patients may raise questions about the validity of our results. However, the large and significant difference in survival between the two groups (P<0.001) leads us to conclude that the sample size and early termination of the trial do not affect the clinical importance of our results.
Presented in part at the 28th annual meeting of the American Society of Clinical Oncology, San Diego, Calif., May 17-19, 1992.
Supported in part by a grant from Bristol-Myers Squibb Company, Madrid, Spain.
We are indebted to the chest physicians, thoracic surgeons, medical oncologists, and radiotherapists at the participating hospitals; to Drs. M.H. Cullen and M.R. Green for their critical review of the manuscript; to Drs. J.J. Sanchez and I. Moreno for their assistance in the statistical analysis; and to Ms. M. O'Sullivan for her editing of the manuscript.
Source Information
From the Departments of Medical Oncology (R.R., S.L., Z.S., A.A.), Thoracic Surgery (J.M., M.C.), Pneumology (J.R., J.M.-P.), Radiology (A.O.), and Pathology (J.L.M., A.A.), University of Barcelona, Hospital de Badalona Germans Trias i Pujol, Barcelona; the Departments of Medical Oncology (J.G.-C.) and Thoracic Surgery (J.P.), Hospital La Fe, Valencia; and the Departments of Medical Oncology (C.C.) and Thoracic Surgery (A.C.), Hospital General, Valencia -- all in Spain.
Address reprint requests to Dr. Rosell at the Medical Oncology Department, University Hospital Germans Trias i Pujol, Box 72, 08916 Badalona (Barcelona), Spain.
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