Original Article
A Randomized Trial of Induction Chemotherapy plus High-Dose Radiation versus Radiation Alone in Stage III Non-Small-Cell Lung Cancer
N Engl J Med 1990; 323:940-945October 4, 1990
- Abstract
- Abstract
Background.
For patients with locally or regionally advanced non-small-cell lung cancer radiation is the standard treatment, but survival remains poor. We therefore conducted a randomized trial to determine whether induction chemotherapy before irradiation improves survival.
Methods.
All the patients had documented non-small-cell cancer of the lung with Stage III disease established by clinical or surgical staging. Eligibility requirements included excellent performance status, minimal weight loss, and visible disease on radiography. Patients randomly assigned to group 1 received cisplatin (100 mg per square meter of body-surface area given intravenously on days 1 and 29) and vinblastine (5 mg per square meter given intravenously on days 1, 8, 15, 22, and 29) and then began radiation therapy on day 50 (60 Gy over a 6-week period). Patients assigned to group 2 received the same radiation therapy but began it immediately and received no chemotherapy.
Results.
The eligible patients in group 1 (n = 78) and group 2 (n = 77) were comparable in terms of age (median, 60 years), sex, performance status, histologic features, stage of disease, and completeness of radiation therapy. The median survival was greater for those in group 1 — 13.8 versus 9.7 months (P = 0.0066 by log-rank test). Rates of survival in group 1 were 55 percent after one year, 26 percent after two years, and 23 percent after three years, as compared with 40, 13, and 11 percent, respectively, in group 2. Those in group 1 had a higher incidence of serious infections requiring hospitalization (7 percent, vs. 3 percent in group 2) and severe weight loss (14 percent vs. 6 percent), but there were no treatment-related deaths.
Conclusions.
In patients with Stage III non-small-cell lung cancer, induction chemotherapy with cisplatin and vinblastine before radiation significantly improves median survival (by about four months) and doubles the number of long-term survivors, as compared with radiation therapy alone. Since three quarters of the patients still die within three years, however, further improvements in systemic and local therapy are needed. (N Engl J Med 1990; 323:940–5.)
Media in This Article
Figure 1
Survival According to Treatment Group among Eligible Patients with Stage III Non-Small-Cell Cancer of the Lung.Figure 2
Failure-free Survival According to Treatment Group among Eligible Patients Enrolled in Cancer and Leukemia Group B Protocol.Article Activity
- Article
PATIENTS with Stage III non-small-cell lung cancer are those who, after clinical or surgical staging (or both) at the time of diagnosis, have no demonstrable distant metastases but do have locally extensive or invasive disease or involvement of mediastinal lymph nodes.1 , 2 The cancer is generally considered incurable by surgery because of the association of these findings with micrometastatic disease. For many years, radiation therapy has been the treatment of choice for such patients,3 although the practice has been questioned.4 On the basis of comparative clinical trials, doses of 5000 to 6000 cGy are considered standard,5 although such treatment is associated with a median survival of only 9 to 11 months, with a 2-year survival of 10 to 20 percent and a 3-year survival of 5 to 10 percent.6
Given the presence of micrometastatic disease, effective systemic therapy should improve survival in Stage III non-small-cell lung cancer. In multi-institutional cooperative clinical trials in patients with metastatic lung cancer, platinum-based combination chemotherapy has produced response rates of 20 to 25 percent.7 8 9 Recent randomized trials comparing the best supportive care with platinum-based chemotherapy demonstrated a survival advantage for patients with advanced disease who received chemotherapy.10
In our experience, the combination of vinblastine and cisplatin produced a response rate of 22 percent in patients with metastatic non-small-cell lung cancer.9 Two cycles of this therapy were well tolerated, and less than 40 percent of the patients had evidence of progressive disease during the first two treatment cycles despite the extent of their tumors. Patients with disease limited to the chest who have an excellent performance status and have received no previous chemotherapy are twice as likely to respond to chemotherapy as patients with poor performance status, substantial weight loss, or previous therapy.11 For these reasons, a few weeks of neoadjuvant or induction12 , 13 chemotherapy with vinblastine and cisplatin before the start of radiation therapy seemed rational, and we undertook this prospective randomized trial. Others may prefer to consider this trial a comparison of immediate radiotherapy with chemotherapy plus delayed radiotherapy.
Methods
Eligibility
The eligibility of the patients was determined by a medical and a radiation oncologist before treatment assignment. The patients had pathologically documented non-small-cell lung cancers, including squamous-cell carcinoma, adenocarcinoma, and large-cell anaplastic carcinoma. Patients with mixed tumors were admissible if only non-small-cell elements were identified. Patients had to have disease in stage T3 or N2, but M0. The lung-cancer staging system available when this protocol was initiated in 19841 defined a T3 tumor by its closeness to the carina and invasion of the mediastinum, chest wall, or neurovascular tissues; N2 disease was defined by mediastinal lymphadenopathy; and M0 was defined as the absence of distant metastases. Patients with involvement of supraclavicular or scalene lymph-nodes (or both) or cytologically malignant pleural effusions were excluded because of the poor prognosis associated with such metastases. Surgical staging was not required. Radiologic evaluation consisted of chest roentgenography, bone scanning, and computerized axial tomography of the chest and upper abdomen, including the adrenals. Brain imaging was not required in the absence of symptoms or signs suggestive of brain metastases. The patients had measurable disease (defined as any mass measurable in two perpendicular diameters), disease that could be evaluated (defined as any radiographically visible lesion that could not be accurately measured in two dimensions), or both. Pleural effusions were considered neither measurable nor capable of evaluation, and patients with malignant effusions were ineligible. A performance status of 0 or 1 was required, meaning that patients could carry out normal daily activities and were restricted only in vigorous activity. Patients were ineligible if they had lost more than 5 percent of their body weight during the preceding three months. Previous chemotherapy or radiation therapy was not allowed. Laboratory measures required at entry included a hematocrit higher than 30 percent, leukocyte count higher than 3.5×109 per liter, platelet count higher than 100×109 per liter, and blood urea nitrogen, creatinine, and bilirubin levels less than 1 1/2 times the upper range of normal for the laboratories of the participating institutions.
Therapy
Chemotherapy consisted of vinblastine (5 mg per square meter of body-surface area given in an intravenous bolus on days 1, 8, 15, 22, and 29) and cisplatin (100 mg per square meter given intravenously over a 30-to-60-minute period on days 1 and 29). The doses were modified on the basis of blood counts and tests of renal and hepatic function on the day of therapy.9 If either drug was withheld on day 29, both drugs were delayed until day 36. No chemotherapy was given after day 36, to avoid delaying radiation therapy.
Radiation therapy was started on day 50 (3 weeks after the completion of chemotherapy) for patients assigned to both chemotherapy and radiation (group 1), and within 5 days after entry for the patients assigned to radiation alone (group 2), for whom the first day of therapy was defined as day 1. External-beam photon radiation at megavoltage levels was administered with isocentric tele-therapy with a source-to-axis distance of more than 80 cm at a maximal dose of more than 50 cGy per minute. Treatment volumes consisted of original and boost volumes irradiated sequentially. The original volume was based on x-ray films and scans taken before cytotoxic therapy. The original volume included the primary lesion with a 1.5-cm margin, the ipsilateral pulmonary hilum with a 1.5-cm lateral margin, and an inferior margin that extended either 4.0 cm below the carina or 2.0 cm below the inferior border of any radiographically visible tumor. The upper mediastinal treatment field extended a maximum of 1.0 cm lateral to the involved mediastinum. The ipsilateral supraclavicular fossa was included laterally to the midclavicular line (except for left-lower-lobe lesions, for which both supraclavicular fossae were treated), up to the cricoid cartilage, and down to the lower border of the clavicle. The boost volume included the primary lesion before therapy, with a 1.5-cm margin. The ipsilateral supraclavicular fossa was included in the boost volume in patients with apical lesions.
The dose to the original volume was 40 Gy in 20 fractions of 200 cGy each, given over a period of four weeks. The dose to the boost volume was 20 Gy in 10 fractions of 200 cGy each, given over a period of two weeks. The total tumor dose was thus 60 Gy. The maximal dose to any point along the spinal cord was 46 Gy — 40 Gy to the original volume and 6 Gy to the boost volume. Prophylactic cranial radiation was not given.
Study Design, Data Analysis, and Quality Assurance
The trial was a prospective, randomized, nonblinded study. The central office of the Cancer and Leukemia Group B stratified patients according to histologic type to ensure a balanced distribution between treatment groups, and then randomly assigned the patients in each stratum without blocking to receive either radiation alone (group 2) or chemotherapy followed by radiation (group 1). The primary study objective was to compare overall survival in the two treatment groups. A sample size of 240 was planned on the basis of a projected 50 percent change in survival after two years for two-sided tests with an alpha of 0.05 and a beta of 0.80. Secondary objectives included the assessment of failure-free survival, toxicity, and rates of tumor regression.
A formal protocol-monitoring committee participated in interim assessments of this trial. Data were analyzed in detail twice a year. Reports to the members of the group contained only aggregate data on survival and response, as recommended.14 Group sequential methods accounting for multiple sequential interim analyses of the data were used with a truncated O'Brien—Fleming sequential boundary.15 , 16
The characteristics of the patients before treatment and their rates of response were compared by Pearson's chi-square test for contingency tables or the corresponding exact test.17 Survival was calculated from the date of study entry until the date of death or most recent follow-up examination. Failure-free survival was calculated from the date of study entry to the date of evidence of progressive disease, relapse after response, or death from any cause. Failure-free and overall survival were calculated by the Kaplan–Meier life-table method.18 Comparisons of survival were performed with the log-rank test for censored data or a Cox model to control for prognostic factors.19 , 20 All statistical comparisons were made with two-tailed tests.
Members of the Cancer and Leukemia Group B audit committee visit all participating institutions at least once every three years to verify compliance with federal regulations and protocol requirements. A cohort of 38 patients (21 percent) in this study, from all the participating institutions, had such review. Radiation therapy was monitored by the Quality Assurance Review Committee in Providence, Rhode Island, and subsequently by an ad hoc committee of Cancer and Leukemia Group B radiotherapists. Data were available for full review in 151 patients. Tumor volume was judged with the use of conventional chest films and computerized tomographic scans. Major deviations from the protocol were defined as the failure to include the entire tumor volume as demonstrated by computerized tomography or the delivery of less than 90 percent of the prescribed tumor dose.
Response Criteria
Clinical response was assessed after the completion of chemotherapy in group 1, one month after the completion of radiation therapy in both groups, and then every two months thereafter. A complete response was defined as the disappearance for at least four weeks of all measurable disease or disease that could be evaluated, and the absence of new lesions. For measurable disease, a partial response was defined as a four-week reduction of more than 50 percent in the sum of the products of the cross-sectional diameters of all measurable lesions, and the absence of new lesions. For disease that could be evaluated, regression was defined as a decrease in tumor size for more than eight weeks that was agreed on by two independent observers. Stable disease was defined as a reduction of less than 50 percent or an increase of less than 25 percent in the sum of the products of the cross-sectional diameters of all measured lesions and no clear-cut regression or progression of disease for at least eight weeks. Progressive disease or relapse was defined as an increase of more than 25 percent in the sum of the products of the cross-sectional diameters of measured lesions, an increase in disease that could be evaluated, or the appearance of new lesions.
Results
Patients were enrolled from May 1984 to May 1987. Interim analysis showed that the difference in survival between groups had reached a level of significance sufficient to permit the termination of patient enrollment.15 , 16 Accordingly, the trial was closed after 180 patients had been enrolled.
Twenty-five patients (14 percent) were excluded from the current analysis because of ineligibility. Seven patients from each treatment group were discovered to be ineligible before therapy began. Four patients in group 1 were subsequently deemed to be ineligible: two with metastatic disease, one with a performance status of 2, and one in whom all measurable tumor had been resected. Seven patients assigned to group 2 were subsequently determined to be ineligible: four with metastatic disease, one with metastatic disease and a performance status of 2, and two with Stage II disease. Two patients with a performance status of 2, one in each group, were prospectively enrolled because the limitations on their activity were related to reversible, noncancerous conditions.
The characteristics of the 155 eligible patients are shown in Table 1Table 1
Characteristics of the Patients.. There were no significant differences between the two treatment groups in any of the characteristics listed. Forty-six percent of the patients assigned to radiation therapy alone (group 2) and 50 percent of those assigned to induction chemotherapy (group 1 ) underwent either mediastinoscopy or thoracotomy during their evaluation. None of the patients in this trial had complete surgical resection of disease before enrollment, and no patients underwent resection of residual disease after therapy.Median follow-up has now been 34 months. Significant differences between the two groups in survival (Fig. 1Figure 1
Survival According to Treatment Group among Eligible Patients with Stage III Non-Small-Cell Cancer of the Lung.) and failure-free survival (Fig. 2Figure 2Failure-free Survival According to Treatment Group among Eligible Patients Enrolled in Cancer and Leukemia Group B Protocol.) have persisted. The overall differences in survival were especially striking for patients with squamous-cell carcinoma or adenocarcinoma (Fig. 3Figure 3
Survival According to Treatment Group among Eligible Patients with Squamous-Cell Carcinoma. and 4Figure 4
Survival According to Treatment Group among Eligible Patients with Adenocarcinoma.). The observed difference in overall survival remained statistically significant when we controlled for sex, age, cell type, and performance status in a Cox model (P = 0.0075). The median survival for the entire study population has been 11 months. The median survival in group 2 has been 9.7 months, as compared with 13.8 months in group 1. Rates of survival in group 1 were 55 percent after one year, 26 percent after two years, and 23 percent after three years, as compared with 40, 13, and 11 percent, respectively, in group 2. Sixteen patients are known to have survived beyond two years in the group that underwent induction chemotherapy, and seven in the group that received radiation therapy alone. Nineteen of these 23 survivors were still alive at this writing, and the longest period of survival was more than 52 months.Some of the difference in survival was attributable to early deaths in the group that received radiation therapy alone. Within the first 15 weeks, there were 14 deaths in group 2, as compared with only 4 in group 1. Of the four early deaths in group 1, two were due to progressive disease, one was related to a cardiac disorder in a patient who had residual disease at autopsy, and one was due to massive hemoptysis within two weeks of study entry. Of the 14 early deaths in group 2, 8 were due to progressive disease, 3 to respiratory failure with persistent disease, 1 to hemoptysis, and 1 to a myocardial infarction; the 14th patient died of an unknown cause in a nursing home after completing radiation therapy. An analysis that excluded these 18 deaths was performed to compare survival between the two treatment groups among patients who had survived until day 105.21 There was still a trend toward a survival advantage for the patients who received induction chemotherapy (P = 0.059) (Fig. 5Figure 5
Landmark Analysis of Survival According to Treatment Group among Patients Alive on Day 105.).The rates of response in each treatment group are shown in Table 2Table 2
Tumor Response to Therapy.*. The difference in rates of response (44 of 78 vs. 33 of 77) was not significant (P = 0.092). After induction chemotherapy 28 patients in group 1 (36 percent) had responses, including 3 (4 percent) with complete and 17 (22 percent) with partial remissions and 8 (10 percent) with regression of disease that could be evaluated. Two patients with an indeterminate response on day 50 went on to have complete remission after radiation therapy. Of the 17 patients who had a partial response after chemotherapy, 6 had complete remission and 11 remained in partial remission after radiation therapy. Of the eight patients with disease that could be evaluated who had regression after chemotherapy, one subsequently had a complete response. Of the patients judged to have stable disease after chemotherapy, three had a complete response after radiation therapy.Serious toxic effects, especially neutropenic infections and vomiting, were more prevalent in the patients undergoing chemotherapy. The frequency of severe infections requiring hospitalization was 3 percent in group 2, as compared with 7 percent in group 1. Severe weight loss occurred in 6 percent of the patients undergoing radiation therapy, as compared with 14 percent of those undergoing induction chemotherapy. The frequency of vomiting requiring hospitalization was 5 percent in the chemotherapy group. There were no treatment-related deaths in either group. Of the patients assigned to group 1, 86 percent received both doses of cisplatin; 37 percent received all five doses of vinblastine, 35 percent received four doses, 14 percent three doses, 8 percent two doses, and 6 percent one dose. Chemotherapy did not impair the delivery of radiation therapy; 88 percent (69 of 78) of the patients in group 1 completed radiation therapy, whereas 87 percent (67 of 77) of those in group 2 completed treatment. The frequency of severe esophagitis or pneumonitis was only 1 percent in each treatment group.
Major deviations from the radiation protocol were detected in 34 of 151 cases. In 12 patients treatment failed to encompass all tumor in both the large and small irradiation ports, in 21 all tumor was not encompassed in the small field, and in 1 the delivered dose of radiation was less than 90 percent of the dose prescribed. Large-field errors were usually due to shadows seen on computerized tomograms but not on the port x-ray films; 15 of the small-field errors were due to failure to include mediastinal adenopathy. There were major violations in 16 patients (21 percent) in group 2 and in 18 (23 percent) in group 1. Six of these 34 patients have survived for more than two years; 5 of the 6 received induction chemotherapy.
There was no suggestion of a difference between the two groups in the sites of disease progression. A formal analysis of the sites could not be performed because uniform staging at the time of treatment failure was not possible. However, data forms were reviewed for all the patients who died before the analysis, including 64 who received radiation therapy alone (group 2) and 49 who received induction chemotherapy (group 1). Among those in group 2, 41 percent had cancer in the lung, 39 percent had lung and distant metastases, 6 percent had metastatic disease alone, and for 14 percent no information was available. Among those in group 1, 45 percent had cancer in the lung at relapse, 45 percent had lung and distant metastases, 4 percent had metastatic disease alone, and for 6 percent no information was available. Brain metastases were noted in 13 percent of the patients who received radiation therapy alone and 12 percent of patients who received chemotherapy and radiation.
Discussion
A major issue in lung cancer is the risk—benefit ratio of any therapeutic approach. The objective of this randomized prospective trial was to determine whether chemotherapy before high-dose radiation therapy would have a beneficial or detrimental effect as compared with radiation alone in patients with Stage III non-small-cell lung cancer. A five-week course of induction chemotherapy was associated with a four-month prolongation of median survival in the study population and a doubling of survival two and three years after study entry. This was achieved with a frequency of severe or life-threatening infections of only 7 percent, a frequency of chemotherapy-associated emesis requiring hospitalization of 5 percent, and no treatment-related deaths. Typically, such chemotherapy is now given in an outpatient setting, and advances in antiemetic therapy have greatly reduced the morbidity of cisplatin.22
Another issue in today's health care climate is the cost—benefit ratio of these therapies. On the basis of figures from a private metropolitan hospital, the current medical costs associated with six weeks of radiation therapy as delivered in this protocol are estimated to be $14,000, and the costs associated with chemotherapy are $3,500. This represents a 33 percent increase in cost for a 100 percent increase in survival after two and three years for patients who receive induction chemotherapy in addition to radiation therapy. Spread over the two patient populations, the cost per day of median survival is $47 for radiation therapy alone and $41 for chemotherapy plus radiation therapy. The additional cost of chemotherapy is $28 per day of increased median survival, or $8.50 per day of actual median survival for patients who received chemotherapy.
Approximately 120,000 new cases of non-small-cell lung cancer are diagnosed each year in the United States. Of these, 40,000 are Stage III disease, and it is estimated that 10,000 would satisfy the entry criteria of our protocol.23 Projections from this trial suggest that approximately 1500 additional patients per year could survive with the use of induction chemotherapy before high-dose radiation therapy. This represents a doubling of survival after two and three years. Because of the potential importance of this observation, other cooperative groups are conducting confirmatory trials of the approach. The Radiation Therapy Oncology Group and the Eastern Cooperative Oncology Group are jointly conducting a three-group trial including both our study treatments plus a third that involves only hyperfractionated radiation therapy. The Southwest Oncology Group is comparing induction cisplatin and etoposide chemotherapy followed by radiation therapy, with radiation therapy alone.
Several issues related to Stage III lung cancer were not addressed in our trial, including the effect of the new staging system and the effect of therapy on the quality of life. Patients enrolled in this trial did not have definitive surgical staging; therefore, we could not stratify our data according to the new Stage IIIA and IIIB subclasses.2 The possible value of surgical resection after chemotherapy, radiation therapy, or both was not addressed in this trial. Future trials should employ surgical staging and explore the value of chemotherapy in Stage II, IIIA, and IIIB non-small-cell lung cancer. Instruments to assess quality of life may facilitate assessment of the risk—benefit ratio of therapy in such patients.
Although a four-month improvement in median survival and an apparent doubling of overall survival is encouraging, our results suggest that even with induction chemotherapy, 75 percent of the patients with Stage III non-small-cell lung cancer will die within three years. Still better therapy is therefore needed, and exploration of improved radiation therapy, better chemotherapy, and biologic therapy is warranted. The value of new treatment programs can only be established by prospective randomized trials.
Conducted by the Cancer and Leukemia Group B and supported by grants from the National Cancer Institute and the T.J. Martell Foundation. Members from the following institutions participated in the study: University of California at San Diego — Mark Green (grant CA-11789); University of Missouri, Columbia — Michael Perry (CA-12046); University of Minnesota, Minneapolis — Bruce Peterson (CA-16450); University of Tennessee, Memphis — Alvin M. Mauer (CA-47555); Bowman-Gray School of Medicine, Winston-Salem, N.C — Robert Cooper (CA-03927); West Virginia University Medical Center, Morgantown — Peter Raich (CA-28562); Delaware Cancer Network, Wilmington, Del. — Robert Frelick (CA-28411); University of Maryland Cancer Center, Baltimore — Joseph Aisner (CA-31983); New York Hospital—Cornell Medical Center, New York — Richard T. Silver (CA-07968); Long Island Jewish Medical Center, New Hyde Park, N.Y. — Kanti Rai (CA-11028); Columbia University, New York — Sameer Rafla (CA-25119); Mount Sinai School of Medicine, New York — James F. Holland (CA-04457); Upstate Medical Center at Syracuse, Syracuse, N.Y. — Arland Gottlieb (CA-21060); Central Massachusetts Oncology Group, Worcester, Mass. — Mary Constanza (CA-37135); Harvard School of Public Health, Boston — James R. Anderson (CA-33601); Massachusetts General Hospital, Boston — Robert Carey (CA-12449); Rhode Island Hospital, Providence — Louis Leone (CA-08025); Dartmouth—Hitchcock Medical Center, Hanover, N.H. — Gibbons Comwell (CA-04326); McGill Cancer Center, Montreal — J.L. Hutchinson (CA-31809); Washington University Medical Center, St. Louis — Alan P. Lyss; University of Alabama, Birmingham — George Omura; and University of Cincinnati College of Medicine, Cincinnati — Orlando J. Martelo.
Presented in part at the Plenary Session of the 24th Annual Meeting of the American Society of Clinical Oncology, New Orleans, May 1988.
We are indebted to J. Kathleen Meyers for assistance in the preparation of the manuscript.
Source Information
From the Departments of Medicine (R.O.D., M.R.G.) and Radiology (S.L.S.), University of California, San Diego; the Department of Radiology, McGill University, Montreal (J.G.); the Department of Radiology, Dartmouth Medical School, Hanover, N.H. (W.L.E.); the Department of Medicine, University of Missouri, Columbia (M.C.P.); the Department of Biostatistics, Harvard School of Public Health, Boston (K.J.P.); Massachusetts General Hospital, Boston (R.W.C.); and the Dana–Farber Cancer Institute, Boston (E.F.F.). Address reprint requests to Dr. Dillman at the Hoag Cancer Center, 301 Newport Blvd., Newport Beach, CA 92658.
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