Original Article
Dose and Dose Intensity of Adjuvant Chemotherapy for Stage II, Node-Positive Breast Carcinoma
N Engl J Med 1994; 330:1253-1259May 5, 1994
- Abstract
Background
Adjuvant chemotherapy is widely used for breast cancer and is known to extend survival. Some clinicians seek a greater survival benefit by increasing the intensity of the dose, whereas others lower it to diminish toxicity.
Methods
The Cancer and Leukemia Group B (CALGB) conducted a randomized trial of different levels of doses and dose intensity (dose per unit of time) of adjuvant chemotherapy in 1572 women with node-positive, stage II breast cancer who were assigned to three treatment groups. One group received 400 mg of cyclophosphamide per square meter of body-surface area and 40 mg of doxorubicin per square meter once every 28 days and 400 mg of fluorouracil per square meter twice every 28 days, for six cycles. Another group received 50 percent higher doses of the three drugs (600 mg, 60 mg, and 600 mg, respectively) but for only four cycles, so that the total dose was identical in these two groups but the dose intensity was higher in the second. The third group of women received half the total dose used in the other two groups and at half the dose intensity used in the second group.
Results
After a median of 3.4 years of follow-up, the women treated with a high or moderate dose intensity had significantly longer disease-free survival (P<0.001) and overall survival (P = 0.004) than those treated with a low dose intensity, in three-way log-rank comparisons. However, the difference in survival between the two groups treated with a moderate or high dose intensity was not significant. These results are consistent with either a dose-response effect or a threshold level of the dose or dose intensity.
Conclusions
The doses of chemotherapy used to treat breast cancer, especially early breast cancer, should not be reduced if the maximal benefit is to be achieved. .
Media in This Article
Figure 1
Actuarial Disease-free and Overall Survival According to Dose Intensity of Chemotherapy in Women with Stage II Breast Cancer.Figure 2
Actuarial Disease-free Survival According to Menopausal Status.Article Activity
- Article
Randomized clinical trials have established that adjuvant chemotherapy increases the survival of patients with breast cancer1-3. As a result of these studies, large numbers of women with breast cancer now receive adjuvant chemotherapy. However, it is not clear whether the dose and intensity (dose per unit of time) of the treatment affect the outcome. These variables are important because escalating the dose and intensity of chemotherapy adds to its acute toxicity and costs.
Chemotherapeutic agents can have steep dose-response curves in studies of animal tumors and in in vitro models of human tumors, yet there is no clear evidence that variations in the dose of adjuvant chemotherapy improve survival in women with breast cancer4. Bonadonna and Valagussa examined this question in a retrospective analysis of two of their clinical trials with cyclophosphamide, methotrexate, and fluorouracil5. They found that disease-free survival was longer in the patients who received a higher percentage of the intended dose of chemotherapy than in those who received a lower percentage. This result may have been due to a dose-response effect, or the patients who were able to tolerate higher doses of chemotherapy may have been more likely to survive longer. It is also possible that the women who survived longer had a smaller tumor burden or a better host response to the tumor than those who survived for a shorter period.
Other retrospective analyses have either supported or contested the benefit of high-dose adjuvant chemotherapy, as compared with low-dose therapy6. A small randomized trial by Abeloff et al. compared cyclophosphamide, methotrexate, and fluorouracil in the doses used by Bonadonna and Valagussa with the same drugs given in doses reduced by more than 50 percent7. There was no significant difference in the rate of relapse between the two treatment groups. A retrospective analysis of randomized trials by the Cancer and Leukemia Group B (CALGB 8082) and the Ludwig Breast Cancer Study Group (trial I) revealed significant differences in the dose intensity of the chemotherapy delivered, yet there were no differences in disease-free or overall survival8,9.
This paper reports the results of a prospective, randomized trial of adjuvant cyclophosphamide, doxorubicin, and fluorouracil in three groups of patients. Conducted by the CALGB (see the Appendix), the trial was designed to test the hypothesis that increases in the dose and dose intensity would lead to improved disease-free and overall survival. Group 1 received chemotherapy at twice the dose and dose intensity of the regimen used in group 3. Group 2 received the same total dose as that used in group 1 but over a 50 percent longer period, resulting in a lower dose intensity (Table 1Table 1
Drug Regimens Used as Adjuvant Chemotherapy in Three Groups of Patients with Stage II Breast Cancer.). We report the initial results of this trial at a median of 3.4 years of follow-up.Methods
Patient Selection
CALGB 8541, which began in January 1985, was for women with histologically confirmed unilateral stage II adenocarcinoma of the breast (T1 or T2N1M0)10. To be eligible, patients had to be at least 16 years of age and not pregnant, with a performance score of 0 or 1 (no symptoms or minimal symptoms), no previous or concomitant cancer, and no serious medical or psychiatric illness that would prevent informed consent or intensive treatment. Primary therapy consisted of a radical or modified radical mastectomy or breast-conservation therapy with excision of the tumor to the extent of clear margins, dissection of levels 1 and 2 axillary lymph nodes, and irradiation after chemotherapy. Breast-conservation therapy, with stratification for this method of treatment, was added to the original protocol eight months after the study had begun. When breast-conserving therapy was used, radiation at a dose of 5040 cGy was delivered to the entire breast by tangential fields in 28 fractions. An electron-beam boost of 1504 cGy was administered to the area of excision in eight fractions.
In 1988, an addendum to the protocol required the addition of tamoxifen after the administration of cyclophosphamide, doxorubicin, and fluorouracil in patients who were perimenopausal or postmenopausal and positive for estrogen receptors. This change was based on emerging evidence of the effectiveness of antiestrogen therapy in such women3. Patients already participating in the study who met one or more of these criteria could be given tamoxifen at a time decided on by their treating physicians. All chemotherapy was begun within six weeks after definitive surgical treatment. All drugs were administered intravenously, and no dose reductions were scheduled. White-cell and platelet counts were obtained weekly, and treatment on day 1 of a cycle was delayed if the white-cell count was less than 3500 per cubic millimeter or if the platelet count was less than 100,000 per cubic millimeter. Chemotherapy doses were calculated on the basis of actual, not ideal, body weight.
The patients were stratified according to primary treatment (mastectomy or breast conservation), menopausal status (before, during, or after menopause), number of positive lymph nodes (one to three, or more than three), and estrogen-receptor status (positive or negative). The patients were randomly assigned to receive chemotherapy at a dose intensity that was high (group 1), moderate (group 2), or low (group 3).
Statistical Analysis
The primary objective was to compare the disease-free survival of patients randomly assigned to group 1 with the survival of those randomly assigned to group 3. Disease-free survival was defined as the time from randomization to a documented relapse or death without a relapse. Data on patients who were still alive and free of disease were censored at the date of the last contact. Overall survival was defined as the time from randomization to death from any cause.
Differences in disease-free and overall survival were evaluated with the proportional-hazards model11 for multivariate analyses and the log-rank test and stratified log-rank test12 for univariate analyses. Differences in patient characteristics were evaluated with the chi-square test,13 for categorical variables, and Wilcoxon's rank-sum test,13 for continuous variables. Median survival and time-to-event curves were calculated by the Kaplan-Meier method14.
Multivariate analyses of disease-free survival were performed every four to six months after a median of one year of follow-up. These analyses were reported to an independent protocol-monitoring committee responsible for deciding to terminate the trial early if statistical differences emerged on the basis of group sequential methods15 for evaluating disease-free and overall survival. Patient-enrollment goals were increased twice, first to 1150 women, to allow for the inclusion of patients treated with breast-conservation therapy, and then to 1570, to accommodate the anticipated diminished rate of failure with the addition of tamoxifen in perimenopausal or postmenopausal women who were positive for estrogen receptors. The second of these revised goals was reached in March 1991, and the trial was closed. The next scheduled analysis demonstrated a significant difference in survival between treatment groups, with the nominal P value by multivariate analysis (P<0.001) crossing the truncated O'Brien-Fleming boundary (approximately P = 0.0026). Physicians of patients in group 3 were notified, and the patients were given the option of receiving an increased dose and dose intensity.
According to the a priori study design, data on the patients who had undergone breast-conservation therapy and on those receiving tamoxifen were to be analyzed in separate strata. A subgroup analysis was to be performed for each of the stratified subgroups. Data for all groups were analyzed by intention-to-treat methods.
All clinical information and surgical and pathology reports were reviewed by the study cochairs to verify the eligibility of the patients and their tumor and nodal characteristics. Members of the CALGB Data Audit Committee made site visits to all the participating institutions to verify compliance with federal regulations and protocol requirements, including those regarding eligibility, treatment, toxic effects, and outcome. Such an on-site review of medical records was performed for a randomly selected subgroup of 376 patients (24 percent) from all the participating institutions.
Results
A total of 1572 patients from 26 institutions and their affiliates were enrolled in the study. Twenty-two patients withdrew from the study before they received treatment, and follow-up data were inadequate for 21 patients. The results reported here are for 1529 patients, with a median follow-up of 3.4 years. Sixty-eight patients (4 percent) did not meet one or more eligibility criteria, most often because of a tumor size that exceeded 5 cm. However, no randomized patients were excluded if follow-up data were available and they had received treatment. Analyses of the data with and without these 68 patients revealed no differences in outcome. The clinical characteristics of the patients are shown in Table 2Table 2
Characteristics of Patients at the Time of Enrollment in the Study..Outcome
Both disease-free and overall survival were longer in patients who were treated with a high dose at a moderate or high intensity (groups 1 and 2) than in those treated with a low dose at a low intensity (group 3), and a three-way comparison was significant by a log-rank analysis (Figure 1Figure 1
Actuarial Disease-free and Overall Survival According to Dose Intensity of Chemotherapy in Women with Stage II Breast Cancer.). Paired comparisons demonstrated significant differences between groups 1 and 3 and groups 2 and 3 in terms of both disease-free and overall survival (Table 3Table 3
Disease-free and Overall Survival in the Three Treatment Groups at Three Years.).The large size of this trial allowed an analysis of a priori subgroups. Table 4Table 4
Hazard-Rate Ratios and Pairwise Comparisons of Disease-free Survival in Subgroups of Patients with Various Clinical Characteristics. lists the hazard ratios and univariate P values for these subgroups. The difference in survival between groups 1 and 3 was remarkably uniform across all subgroups in which there was a sufficient number of events to allow an analysis of differences. The survival difference in smaller subgroups, such as postmenopausal women who were negative for estrogen receptors, or subgroups with few treatment failures, such as women with tumors less than 2 cm in diameter and those with one to three positive nodes, was not significant.The effect of the two higher-dose regimens of adjuvant chemotherapy on disease-free survival was as great in postmenopausal women as it was in premenopausal women (Figure 2Figure 2
Actuarial Disease-free Survival According to Menopausal Status.). The difference in overall survival, according to the chemotherapy dose, between premenopausal and postmenopausal women is shown in Figure 3Figure 3
Actuarial Overall Survival According to Menopausal Status.. The difference had a P value of 0.03 by the log-rank test.Table 5Table 5
Sites of Recurrent Disease in the Three Treatment Groups. provides data on initial relapses in each treatment group. Patients in group 3 had a significantly higher number of relapses at all sites than did patients in group 1 or group 2. Among the patients in group 3, local relapses were more frequent than distant relapses. This raises the possibility that the dose may be more effective in controlling local disease than in controlling distant metastases. When patients who first had a relapse at a local site were excluded from the analysis, disease-free survival was still longer in the patients given the higher doses (P = 0.04 for a three-way comparison; P = 0.01 for a two-way comparison between groups 1 and 3). However, this analysis assumes that local and distant failures were independent events, which was not likely16. For this reason, data on all local relapses, not just the first relapse, are being collected to perform a proper analysis of the question of dose in relation to local and distant disease.Toxicity
Toxicity was directly related to dose intensity. According to standard CALGB grading criteria, grade III or IV leukopenia (grade III: 1000 to 1999 cells per cubic millimeter; grade IV: <1000 cells per cubic millimeter) occurred in 65 percent of the patients in group 1, in 16 percent of those in group 2, and in less than 5 percent of those in group 3. Grade III or IV thrombocytopenia (grade III: 25,000 to 49,999 cells per cubic millimeter; grade IV: <25,000 cells per cubic millimeter) occurred in 18 percent of the women in group 1 but in less than 2 percent of those in groups 2 and 3. Nausea affected 39 percent, 35 percent, and 20 percent of the patients in groups 1, 2, and 3, respectively. Grade III or IV stomatitis (grade III: painful erythema, edema, ulcers, and inability to eat; grade IV: painful erythema, edema, ulcers, and requirement of enteral or parenteral nutrition) occurred in 10 percent of the patients in group 1. There were two treatment-related deaths: one patient in group 3 died of septic shock and one patient in group 1 died of cardiomyopathy three years after treatment. Ninety-one patients were withdrawn from the study before completion of all the assigned cycles of chemotherapy. Consent to continue in the study was withdrawn by 36 women; 27 withdrew because of excessive toxicity, 11 because of a relapse during treatment, and 17 for various other reasons. Virtually all the assigned doses were actually delivered. Over 95 percent of the patients received at least 90 percent of their assigned dose. Intravenous administration of drugs ensured compliance and distinct differences in dose intensity among the three treatment groups.
Body weight did not influence disease-free or overall survival; when patients were divided into four groups according to body weight (<60 kg, 60 to 67 kg, 68 to 79 kg, and ≥ 80 kg), the P values by log-rank analysis were 0.53 for disease-free survival and 0.89 for overall survival. The administration of dexamethasone as an antinausea medication also did not affect the outcome.
Discussion
Dose
This randomized trial of adjuvant chemotherapy for stage II breast cancer demonstrates a difference in survival resulting from the use of different doses of chemotherapy given at different levels of intensity, even though the doses were within the conventional range. The original chemotherapy regimen was 400 mg of cyclophosphamide per square meter of body-surface area and 40 mg of doxorubicin per square meter, both given on day 1 in a 28-day cycle, and 400 mg of fluorouracil per square meter given on days 1 and 8 of the cycle17. This protocol approximates the regimen of a high dose given at a moderate level of intensity in group 2 in our study. The protocol for group 1 represents a 50 percent increase over the original regimen. In a pilot study, the degree of toxicity associated with the administration of a high dose at a high level of intensity was judged to be the maximum that could be accepted in a large, multi-institutional trial of adjuvant chemotherapy for stage II breast carcinoma18. Group 3 received half the dose received in the other two groups and at half the intensity of that received in group 1.
The dose-response effect refers to a relation in which the effect of a drug increases proportionally with increasing doses. This is different from the dose threshold, which is a dose below which there is no discernible effect. The results of our trial demonstrated at least a threshold effect of a regimen of cyclophosphamide, doxorubicin, and fluorouracil used as adjuvant chemotherapy for patients with early breast cancer.
The results also provide some evidence of a dose-intensity response. The dose rates for cyclophosphamide, doxorubicin, and fluorouracil were 150 mg, 15 mg, and 150 mg per square meter, respectively, per week in group 1; 100 mg, 10 mg, and 100 mg per square meter in group 2; and 75 mg, 7.5 mg, and 75 mg per square meter in group 3. Thus, the rate in group 1 was 50 percent higher than that in group 2, and the rate in group 3 was 50 percent of that in group 1. Although the overall and disease-free survival rates in group 3 were higher than those in group 2, the differences were not significant.
The use of bone marrow-stimulating factors and bone marrow transplantation makes further escalation of the dose intensity possible. Such treatments are currently being evaluated in national, cooperative group trials. However, the results of our trial cannot be used to justify a higher dose intensity than that used in group 1. The increase from a moderate to a high dose intensity was associated with an increase in morbidity. The white-cell nadir was considered to be in the life-threatening range (<1000 cells per cubic millimeter) in 21 percent of the patients in group 1 but in only 1 percent of those in group 2. Nevertheless, only 4 percent of the patients in group 1 required hospitalization. This increase in morbidity in group 1, as compared with group 2, was not accompanied by a significant increase in either disease-free or overall survival.
Menopausal Status
It has been difficult to demonstrate survival benefits from adjuvant chemotherapy in postmenopausal women. In a 1988 overview of all trials of adjuvant therapy, the reduction in the odds of death was 14 percent in 3746 women who received combination chemotherapy, as compared with those given no adjuvant treatment3. Ten percent of the women over 50 years of age in these studies were premenopausal. In an earlier study, the National Surgical Adjuvant Breast and Bowel Project found that patients 50 years of age or older survived longer when treated with a combination of doxorubicin and tamoxifen, as compared with those treated with tamoxifen alone. However, others have not demonstrated a similar benefit from doxorubicin-containing regimens for postmenopausal women19.
Our results provide evidence that a reduction in chemotherapy doses below the levels that have been shown in large clinical trials to improve outcomes in patients with breast cancer reduces the benefit of such adjuvant therapy. In this study, postmenopausal women treated with higher doses of adjuvant chemotherapy had a significantly longer survival than those given lower doses. Our data provide no evidence that an additional benefit will accrue from doses that are even higher than those employed in this trial. However, we believe that our results provide a rationale for randomized clinical trials of high-dose chemotherapy combined with autologous bone marrow transplantation or treatment with peripheral stem cells or hematopoietic growth factors.
Supported by grants (CA-12449, CA-35279, CA-33601, CA-03927, CA-07968, CA-35421, and CA-31946) from the National Cancer Institute.
Source Information
From the Winship Cancer Center, Emory University, Atlanta (W.C.W.); North Shore University Hospital, Manhassett, N.Y. (D.R.B.); the Department of Biostatistics, Harvard School of Public Health, Boston (A.H.K.); the Bowman Gray School of Medicine, Winston-Salem, N.C. (M.R.C., C.R.F.); Massachusetts General Hospital, Boston (J.Y.); St. Luke's Medical Center, Milwaukee (R.D.H.); New York Hospital and Cornell Medical Center, New York (A.M.); the S. Nevada Cancer Research Foundation, Las Vegas (J.A.E.); the Memorial Sloan-Kettering Cancer Center, New York (L.N.); the Frontier Science Technology and Research Foundation, Amherst, N.Y. (A.C.B.); the Dana-Farber Cancer Institute, Boston (E.F.); and the University of California, San Francisco, School of Medicine, San Francisco (I.C.H.).
Address reprint requests to Dr. Wood at the Department of Surgery, Emory University School of Medicine, 1364 Clifton Rd., N.E., Atlanta, GA 30322.
Appendix
The following members of the Cancer and Leukemia Group B participated in this study: R. Cooper, Bowman Gray School of Medicine, Winston-Salem, N.C.; G. Canellos, Dana-Farber Cancer Institute, Boston; M. Green, University of California, San Diego; R.T. Silver, New York Hospital-Cornell Medical Center, New York; R.W. Carey, Massachusetts General Hospital, Boston; J.F. Holland, Mount Sinai Hospital, New York; J. Aisner, University of Maryland Cancer Center, Baltimore; A. Gottlieb, Upstate Medical Center, Syracuse, N.Y.; K. Rai, Long Island Jewish Medical Center, New Hyde Park, N.Y.; M. Perry, University of Missouri, Columbia; A.P. Lyss, Washington University Medical Center, St. Louis; R. Weiss, Walter Reed Army Medical Center, Washington, D.C.; R.C. Bast, Duke University Medical Center, Durham, N.C.; L. Leone, Rhode Island Hospital, Providence; A.M. Mauer, University of Tennessee, Memphis; M. Costanza, Central Massachusetts Oncology Group, Worcester; N. Vogelzang, University of Chicago Medical Center, Chicago; B. Cooper, McGill Cancer Center, Montreal; R.R. Ellison, Columbia University, New York; S. Kopel, Maimonides Medical Center, Brooklyn, N.Y.; G. Omura, University of Alabama, Birmingham; B. Peterson, University of Minnesota, Minneapolis; G. Cornwell, Dartmouth Medical School-Norris Cotton Cancer Center, Hanover, N.H.; E.S. Henderson, Roswell Park Memorial Institute, Buffalo, N.Y.; H. Ozer, University of North Carolina, Chapel Hill; O. Martello, University of Cincinnati College of Medicine, Cincinnati; R. Frelick, Delaware Cancer Network, Wilmington; and G. Clamon, University of Iowa, Iowa City.
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