Original Article
Effects of Concomitant Cisplatin and Radiotherapy on Inoperable Non-Small-Cell Lung Cancer
N Engl J Med 1992; 326:524-530February 20, 1992
- Abstract
- Abstract
Background and Methods.
Cisplatin (cis-diamminedichloroplatinum) has been reported to enhance the cell-killing effect of radiation, an effect whose intensity varies with the schedule of administration. We randomly assigned 331 patients with nonmetastatic inoperable non—small-cell lung cancer to one of three treatments: radiotherapy for two weeks (3 Gy given 10 times, in five fractions a week), followed by a three-week rest period and then radiotherapy for two more weeks (2.5 Gy given 10 times, five fractions a week); radiotherapy on the same schedule, combined with 30 mg of cisplatin per square meter of body-surface area, given on the first day of each treatment week; or radiotherapy on the same schedule, combined with 6 mg of cisplatin per square meter, given daily before radiotherapy.
Results.
Survival was significantly improved in the radiotherapy—daily-cisplatin group as compared with the radiotherapy group (P = 0.009): survival in the radiotherapy—daily-cisplatin group was 54 percent at one year, 26 percent at two years, and 16 percent at three years, as compared with 46 percent, 13 percent, and 2 percent, respectively, in the radiotherapy group. Survival in the radiotherapy—weekly-cisplatin group was intermediate (44 percent, 19 percent, and 13 percent) and not significantly different from survival in either of the other two groups. The survival benefit of daily combined treatment was due to improved control of local disease (P = 0.003). Survival without local recurrence was 59 percent at one year and 31 percent at two years in the radiotherapy—daily-cisplatin group; 42 percent and 30 percent, respectively, in the radiotherapy—weekly-cisplatin group; and 41 percent and 19 percent, respectively, in the radiotherapy group. Cisplatin induced nausea and vomiting in 86 percent of the patients given it weekly and in 78 percent of those given it daily; these effects were severe in 26 percent and 28 percent, respectively.
Conclusions.
Cisplatin, given daily in combination with the radiotherapy described here to patients with nonmetastatic but inoperable non—small-cell lung cancer, improved rates of survival and control of local disease at the price of substantial side effects. (N Engl J Med 1992;326: 524–30.)
Media in This Article
Figure 1
Overall Survival in the Treatment Groups.Figure 2
Survival without Local Recurrence.Article Activity
- Article
NON—SMALL-CELL lung cancer is the most frequent cause of death due to cancer in men in the Western world, and its incidence among women is rapidly increasing. The poor prognosis of patients with locally advanced tumors has remained essentially unchanged in recent decades. At diagnosis, only 25 percent of all patients are considered candidates for surgery.1 The five-year survival rate is 25 percent among patients with resectable disease.2 Radiotherapy is frequently considered for patients with localized inoperable disease; they are selected on the basis of prognostic factors, such as cancer stage (TNM status), performance status, weight loss, and other factors.3 , 4 In such patients it is important to distinguish between palliative and curative treatment. For patients treated palliatively, several radiotherapy schedules have been proposed.5 , 6 The dose of radiation for patients undergoing curative treatment should be at least 50 Gy, preferably exceeding a dose of 60 Gy given over a period of five to six weeks or the equivalent.7 , 8 This approach achieves one-year and two-year survival rates of 45 percent and 15 percent, respectively; the five-year survival is approximately 5 percent. These disappointing results can be partially explained by local recurrences. Higher doses of radiotherapy are associated with improved local control and survival.8 , 9 It is difficult to establish a reliable dose–response curve, however, because of problems encountered in assessing tumor regression and local tumor control. The upper dose limit is set by the occurrence of tissue damage, which also depends on the choice of radiation fields. Because local disease recurs in at least 40 to 60 percent of patients given high-dose radiotherapy,8 9 10 11 there is a need for methods of enhancing or potentiating radiation damage in tumors, such as the use of radiosensitizers.
In the early 1980s, cisplatin (cis-diamminedichloroplatinum) was heralded as a drug that could possibly increase radiation-induced damage to tumors. Possible mechanisms included radiosensitization of hypoxic cells, inhibition of repair of sublethal or potentially lethal damage, increased induction of chromosomal aberrations, and binding to thiols.12 13 14 15 The in vitro results were confirmed by studies in animals.16 , 17 The optimal dose and schedule for combination treatment with radiation and cisplatin have not been precisely established.13 , 14 Administering cisplatin shortly before or shortly after daily irradiation is considered to have the greatest tumoricidal effects.18 19 20 21 A single dose of the drug before a series of five fractions of irradiation is also effective against some types of tumor,20 with better preservation of normal tissue.18 In a recent phase III study, combined treatment produced a higher response rate but no survival benefit.22
The Radiotherapy and Lung Cancer Cooperative Groups of the European Organization for Research and Treatment of Cancer (EORTC) recently initiated a randomized phase II (preliminary) study to compare radiotherapy alone with radiotherapy plus cisplatin given on the first day of each treatment week, and with radiotherapy preceded daily by cisplatin, in patients with inoperable non—small-cell lung cancer.23 24 25 No acute or late toxic effects were observed after the addition of cisplatin, except nausea and vomiting.26 The trial was continued as a phase III study, with survival as the most important end point; the 100 patients of the phase II study were included in the present trial, which was designed to determine whether cisplatin enhanced the effect of irradiation in patients with inoperable lung cancer and whether this effect was dependent on the treatment schedule.
Methods
Criteria for Eligibility
Patients were included in the trial if they had inoperable non—small-cell lung cancer in Stage I, II, or III that had been confirmed histologically; had no evidence of distant metastases on clinical or biochemical examination; were no more than 70 years old; had medical contraindications to operation; had a performance status of 2 or less according to the scales of the Eastern Cooperative Oncology Group27; and had a creatinine clearance rate of ≥1.2 ml per second (70 ml per minute).
After informed consent was obtained from eligible patients, they were stratified according to treatment center, tumor histopathology, and tumor stage at the time of randomization. Screening tests, hematologic analysis, chest radiography, and CT scanning of the chest were required before randomization; bone or brain scintigraphy (or both) or liver ultrasonography (or all three) was performed if distant metastases were suspected.
Treatment
Patients were randomly assigned to one of three treatment groups. The first group received radiotherapy alone. Radiation was administered for two weeks in a dose of 3 Gy given 10 times, followed by a rest period of three weeks (Table 1Table 1
Three Regimens for Treating Non—Small-Cell Lung Cancer.). The dose, specified on the central axis midway between the beam entrances, was given in five fractions a week; one fraction was delivered each day from two opposing anterior—posterior fields. Radiation was again administered for two weeks in a dose of 2.5 Gy given 10 times, from two to three oblique fields so that the spinal cord was spared (maximal total dose, 40 Gy). The dose was specified at the intersection of the beam axes.The second treatment group received the same radiotherapy as the first group; radiotherapy was combined with treatment with cisplatin in a dose of 30 mg per square meter of body-surface area, given intravenously on day 1 of each treatment week, after parenteral prehydration with 1 liter of 2.5 percent glucose in 0.45 percent sodium chloride and posthydration with 2 liters of solution. The third treatment group received the same radiotherapy as the first group; radiotherapy was preceded daily by treatment with intravenous cisplatin in a dose of 6 mg per square meter. An oral fluid intake of 2 liters over a 24-hour period had to be ensured; if it could not, the patient was hospitalized to monitor fluid balance.
The first course of radiotherapy had to include treatment of the primary tumor, the ipsilateral hilar and mediastinal lymph nodes from the thoracic inlet to 5 cm below the carina. A 2-cm tumor-free margin was required. The inferior mediastinum was included when lesions were located in the lower lobe. The supraclavicular areas were included for any tumor in the upper lobe or superior mediastinum. In the second course of radiotherapy, the tumor observed at presentation and the involved nodal regions had to be encompassed by the 90 percent isodose curve, with a margin of no more than 2 cm. The total dose to the spinal cord was limited to 40 Gy. During treatment, blood tests were performed and creatinine clearance was measured once a week in the patients in the two groups given cisplatin. A chest radiograph was obtained before the start of the second part of the radiotherapy to assess tumor response.
Evaluation of Response and Toxicity
The patients' responses and acute and late toxic reactions were evaluated according to the criteria of the World Health Organization.27 After treatment, the patients were observed at six-week intervals during the first year and at three-month intervals thereafter. At follow-up, chest radiography, weight measurement, determination of performance status, hematologic tests, and biochemical blood tests were mandatory, with further investigation if metastasis was suspected. Late lung injury was scored as grade 1 if the chest film showed faint shadowing and as grade 2 if it showed moderate shadowing, both without distortion of anatomy; injury was scored as grade 3 if the film showed faint shadowing and as grade 4 if it showed moderate or dense shadowing, with distortion of anatomy. If radiologic evaluation demonstrated a complete response, a bronchoscopy with biopsy was required for confirmation.
Study Design, Statistical Analysis, and Quality Control
The study was designed as a prospective, randomized three-group trial. Randomization was performed centrally by the EORTC Data Center; patients were assigned to receive radiotherapy alone, radiotherapy and 30 mg of cisplatin per square meter once a week, or radiotherapy and 6 mg of cisplatin per square meter once a day.
It was planned to enter 100 eligible patients in each group and to follow them until death or for 22 months. Survival curves were calculated according to the Kaplan–Meier technique. Survival at one, two, and three years was estimated. Comparisons were made by the log-rank test; this allowed the curves to be compared as a whole. A Cox proportional-hazards model was used to analyze treatment benefit; this model took into account possible prognostic factors.
Study centers that had entered more than 5 percent of the total number of patients required for the trial were visited by a review team. Patient charts, treatment data, and findings during follow-up were checked for 177 patients. The quality-control team discovered problems especially in the correct choice of field sizes for radiotherapy; these protocol violations were equally divided among the three treatment groups, with a slightly higher frequency in the two groups given cisplatin.28
Enrollment and Exclusion of Patients
Between June 1984 and May 1989, 331 patients were enrolled by 20 centers; 285 were entered by 10 institutes, of whom 167 were entered by four departments. The patients' characteristics were well balanced among the three treatment groups (Table 2Table 2
Characteristics of the Treatment Groups.*). Twenty-two patients were later found to be ineligible. All ineligible patients were included in the survival analyses. The reasons for ineligibility were distant metastases at the time of randomization (10 patients), a performance score of 3 according to the Eastern Cooperative Oncology Group (4 patients), an incomplete examination before randomization (2 patients), very extensive lesions (2 patients), malignant pericardial effusion (1 patient), stage N3 disease (1 patient), soft-tissue sarcoma (1 patient), and renal dysfunction (1 patient). Sixty-three patients could not be evaluated for response to treatment, and 45 could not be evaluated for toxic efffects (Table 3Table 3
Reasons for Not Evaluating Patients for Response and Toxic Reactions.).Results
Survival, Disease-free Survival, and Local Recurrence
Analysis was performed after a minimal follow-up period of 22 months. Survival was improved by adding a low daily dose of cisplatin to radiotherapy. In the radiotherapy group, the mean survival rate (±SD) was 46±4.7 percent at one year, 13±3.3 percent at two years, and 2±1.6 percent at three years; in the radiotherapy—weekly-cisplatin group, 44±4.8 percent, 19±4 percent and 13±3.7 percent, respectively; and in the radiotherapy—daily-cisplatin group, 54±4.9 percent, 26±4.4 percent, and 16±3.9 percent, respectively. The difference in one-year survival between the radiotherapy—daily-cisplatin group and the radiotherapy group was 8 percent (95 percent confidence interval, —5 to 22 percent), and the difference between the daily-cisplatin and weekly-cisplatin groups, 10 percent (95 percent confidence interval, —4 to 23 percent). The differences in two-year and three-year survival between the radiotherapy—daily-cisplatin group and the radiotherapy group were 13 percent (95 percent confidence interval, 2 to 23 percent) and 14 percent (95 percent confidence interval, 5 to 22 percent); the differences between the daily-cisplatin and the weekly-cisplatin groups were 7 percent (95 percent confidence interval, —0.5 to 19 percent) and 3 percent (95 percent confidence interval, —8 to 13 percent), respectively. Global comparison of all three treatment groups showed that survival improved when cisplatin was combined with radiotherapy (P = 0.054 overall; radiotherapy vs. radiotherapy plus any dose of cisplatin, P = 0.04) and increased significantly when cisplatin was given daily before radiotherapy (radiotherapy vs. radiotherapy plus daily cisplatin, P = 0.009) (Fig. 1Figure 1
Overall Survival in the Treatment Groups.). No significant difference was observed in overall survival when the weekly-cisplatin group was compared with the radiotherapy-alone group (P = 0.36).Complete and partial responses were assessed in 62 patients given radiotherapy alone, 59 given radiotherapy with weekly cisplatin, and 67 given radiotherapy with daily cisplatin (Table 4Table 4
Response to Treatment.). Disease-free survival was also improved when cisplatin was added, according to a comparison of the three treatment groups (P = 0.048 overall). Patients were classified according to the type of first recurrence, whether local, distant, or both (Table 5Table 5
Type of First Recurrence of Non—Small-Cell Lung Cancer.). The time to local recurrence was significantly longer in the groups given cisplatin (P = 0.015), especially the group given it daily (P = 0.003) (Fig. 2Figure 2Survival without Local Recurrence.). The one-year and two-year survival without local recurrence was 41±5.6 percent and 19±5.1 percent, respectively, in the radiotherapy group; 42±5.7 percent and 30±6 percent in the radiotherapy—weekly-cisplatin group; and 59±5.8 percent and 31±6.3 percent in the radiotherapy—daily-cisplatin group. The differences at one and two years between the daily-cisplatin group and the radiotherapy-alone group were 18 percent (95 percent confidence interval, 3 to 34 percent) and 12 percent (95 percent confidence interval, —4 to 28 percent), respectively. There was no difference among the three groups in the time to distant metastasis (P = 0.37) (Fig. 3Figure 3
Survival without Distant Metastasis.).Toxicity
The incidence of esophagitis resulting from the combined treatment was not increased. The main toxic reactions during treatment were nausea and vomiting among the patients who received cisplatin. Renal and hematologic complications were few and seldom worse than grade 2 reactions as defined by the World Health Organization (Table 6Table 6
Reactions in Patients in Whom Toxicity Could Be Assessed.). The rate of late toxic reactions (more than six months after treatment) was not increased by the addition of cisplatin. The rates of pneumonitis, fibrosis, and respiratory symptoms were similar in the three treatment groups (Table 6). Two patients who received weekly cisplatin died, possibly because of treatment-related causes: one patient died of severe pulmonary fibrosis, and one patient had a fistula that developed between the bronchus and esophagus.Prognostic Factors and Multivariate Analysis
The factors studied as being possibly prognostic were the type of treatment, cancer stage (TNM system), performance status, weight change (loss), age, side of the lung with the tumor, and tumor site (location in upper lobes). Weight loss and performance status were confirmed as prognostic factors. Patients with any weight loss had a significantly worse survival rate than the patients without a weight loss (P<0.001). Asymptomatic patients had a better survival rate than those with symptoms (P<0.001). Patients whose primary tumor was located in the upper lobes had significantly better survival than those whose tumors were in other sites (P = 0.02). In the multivariate analysis, weight loss, performance status as defined by the Eastern Cooperative Oncology Group, and the type of treatment were found to have a significant association with survival (P = 0.001, 0.003, and 0.017, respectively). As a factor, the location of the tumor in the upper lobes approached significance (P = 0.065).
Discussion
The present study was based on the observation that cisplatin increases the therapeutic ratio of radiation, with the magnitude of the synergism depending on the schedule of administration of the two agents. Our findings confirmed this observation by showing that survival was significantly increased among patients with inoperable, nonmetastatic non—small-cell lung cancer when they were treated with radiotherapy and cisplatin daily as compared with radiotherapy alone. The improvement in survival was due to improved control of local disease. The difference was also significant after adjustment for known prognostic factors in a multivariate analysis. No improvement was seen after treatment with radiotherapy and weekly cisplatin. These clinical data confirm studies in animals in which the most effective treatment was found to be cisplatin given daily before each fraction of irradiation.18 19 20 21
The usual method for estimating the extent of local control may be biased if local recurrence and metastasis are not statistically independent events.30 However, if the cisplatin had an effect on occult metastasis, a delay in the appearance of distant disease would have been accompanied by decreased local control. Therefore, we think that the improvement in survival due to the addition of cisplatin to radiotherapy resulted from improved local control.
The toxicity observed in this study confirms earlier findings.25 The nausea and vomiting can now be dealt with more effectively by administering new antiemetic drugs, including serotonin antagonists.31 , 32 Esophagitis and late pulmonary toxic reactions were not aggravated by the combination treatment. Hospitalization was advised if patients were unable to manage a fluid intake of 2 liters per 24 hours. For the 28 percent of patients who continued to vomit after receiving antiemetic agents, admission was made obligatory.
Weekly cisplatin did not improve local control of the tumor or survival. In a trial comparing radiotherapy alone with radiation and weekly cisplatin (20 mg per square meter) for unresectable head and neck cancer, reported by Haselow et al.,22 response rates were higher with combined treatment but survival was not significantly different. Sauer et al.33 found no improvement in survival in patients with invasive bladder cancer treated with irradiation and daily cisplatin during the first and fifth weeks of treatment, as compared with historical controls. Local control was better in the cisplatin-treated group. Since these tumors are biologically different, no conclusions can be drawn from them in relation to our study of patients with lung cancer.
Simpson et al.34 have reported negative results of a trial comparing radiotherapy alone with radiotherapy combined with misonidazole for non—small-cell lung cancer. The dosage of misonidazole was limited by its neurotoxicity.
The high death rate among patients with non—small-cell lung cancer is attributable to distant metastases as well as a high rate of failure to contain the local spread of tumor.35 36 37 In one study, induction chemotherapy improved survival in patients with Stage III disease, as compared with radiotherapy alone, but it is not clear whether this improvement was due to control of local or distant tumor.35 Arriagada et al.36 treated patients with three monthly cycles of chemotherapy after high-dose radiotherapy. Distant metastases occurred less often in the combination-treatment group, although this did not lead to improvement in survival. Local control was very poor in both groups. Cox et al.38 described a randomized phase I/II trial to test a variety of regimens of hyperfractionated radiation. Survival was marginally improved in patients treated with 69.6 Gy, given in two fractions of 1.2 Gy per day.
Although our dose of radiotherapy is comparable to a dose of 60 Gy given over a six-week period in fractions of 2 Gy, our use of a split treatment period may be suboptimal because of repopulation of tumor cells during the rest period.39 Nevertheless, adding daily cisplatin treatment improved local control in this regimen of split-course radiotherapy.
Local cure is a necessary condition for long-term survival in non—small-cell lung cancer.40 Radiotherapy — accelerated, hyperfractionated, or combined with sensitizing drugs (or with all three features) —may further improve local control.
Supported by grants (5–U10-CA-11488–15 through 5–U10-CA-11488–19) from the National Cancer Institute and by grants (MR-066-B, MR-098-B(RS), ECI-1434–B7210–B6-B, PSS0017-B, MR4–002-B, and MR4–082-B) from the Commission of the European Communities.
We are indebted to the chest physicians, oncologists, and radiotherapists who were affiliated with the following institutes or cooperated with their departments: Radiotherapy Institute Heerlen, Heerlen, the Netherlands; Centre Hospitalier de Mulhouse, Mulhouse, France; Istituto Nazionale per la Ricerca sul Cancro, Genoa, Italy; Medical Academy of Gdansk, Gdansk, Poland; Inselspital Universität, Bern, Switzerland; Academisch Ziekenhuis, Leiden, the Netherlands; Instituto Valenciano—Oncologia, Valencia, Spain; Royal Marsden Hospital, Sutton Surrey, United Kingdom; Oncology Department, Ospedale San Giovanni, Turin. Italy; Kantonspital, Basel, Switzerland; Centre GF Leclerc, Dijon, France; Ospedale San Giovanni, Bellinzona, Switzerland; and the University of Arkansas, Little Rock.
Source Information
From the Radiotherapy and Lung Cancer Cooperative Groups of the European Organization for Research and Treatment of Cancer; the Netherlands Cancer Institute, Amsterdam (C.S.-K., O.D., N.v.Z., H.B.); Middelheim Ziekenhuis, Antwerp, Belgium (W.v.d.B., P.R.); St. Radboud Hospital, Nijmegen. the Netherlands (J.F., J.H.); Institute Jules Bordet, Brussels, Belgium (P.v.H., J.-P.S.); Data Center, European Organization for Research and Treatment of Cancer, Brussels (A.K.); Academisch Medisch Centrum, University of Amsterdam, Amsterdam (M.K., L.S.-U.); Dr. Bernard Verbeeten Institute, Tilburg, the Netherlands (B.M., A.N.); and Centre Hospitalier Universitaire de Tivoli, La Louviére, Belgium (A.R.). Address reprint requests to Dr. Schaake-Koning at the Department of Radiotherapy, the Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, the Netherlands.
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