Original Article
Recombinant Granulocyte-Macrophage Colony-Stimulating Factor after Autologous Bone Marrow Transplantation for Lymphoid Cancer
N Engl J Med 1991; 324:1773-1778June 20, 1991
- Abstract
Background.
The period of neutropenia after autologous bone marrow transplantation results in substantial morbidity and mortality. The results of previous phase I-II clinical trials suggest that recombinant human granulocytemacrophage colony-stimulating factor (rhGM-CSF) may accelerate neutrophil recovery and thereby reduce complications in patients after autologous bone marrow transplantation.
Methods.
We conducted a randomized, double-blind, placebo-controlled trial at three institutions. The study design and treatment schedules were identical, and the results were pooled for analysis. One hundred twenty-eight patients were enrolled. Sixty-five patients received rhGM-CSF in a two-hour intravenous infusion daily for 21 days, starting within four hours of the marrow infusion, and 63 patients received placebo.
Results.
No toxic effects specifically ascribed to rhGM-CSF were observed. The patients given rhGM-CSF had a recovery of the neutrophil count to 500×106 per liter 7 days earlier than the patients who received placebo (19 vs. 26 days, P<0.001), had fewer infections, required 3 fewer days of antibiotic administration (24 vs. 27 days, P = 0.009), and required 6 fewer days of initial hospitalization (median, 27 vs. 33 days; P = 0.01). There was no difference in the survival rate at day 100.
Conclusions.
In patients undergoing autologous bone marrow transplantation for lymphoid neoplasia, rhGM-CSF significantly lessens morbidity. Further studies will be required to establish its optimal dosage and schedule of administration. (N Engl J Med 1991; 324:1773–8.)
Media in This Article
Figure 1
Kaplan–Meier Analysis of the Time Required for the Absolute Neutrophil Count to Reach or Exceed 500 Cells per Cubic Millimeter on Two Consecutive Days in 65 Patients Who Received rhGM-CSF and 63 Patients Who Received Placebo.Figure 2
Mean Daily Absolute Neutrophil Counts in 65 Patients Who Received rhGM-CSF and 63 Patients Who Received Placebo.Article Activity
- Article
AUTOLOGOUS bone marrow transplantation has become a standard form of therapy for patients with recurrent lymphoma. This procedure is associated, however, with a 5 to 15 percent risk of fatal complications. Most patients who undergo autologous bone marrow transplantation remain pancytopenic for three to four weeks, and as a result they can have serious morbidity. The mean duration of hospitalization for autologous bone marrow transplantation is 40 to 50 days.1 2 3 4 5
Recombinant human granulocytemacrophage colony-stimulating factor (rhGM-CSF) is a regulatory glycoprotein that promotes the survival, proliferation, and maturation of myeloid cells. It also enhances the function of mature neutrophils and monocytes.6 , 7 Data from controlled trials in nonhuman primates undergoing autologous bone marrow transplantation suggest that rhGM-CSF induces early neutrophil recovery without substantial toxicity.8 , 9 Phase I-II trials in patients undergoing autologous bone marrow transplantation indicate that rhGM-CSF is well tolerated at doses up to 250 μg per square meter of body-surface area, and comparisons with historical control patients suggest that rhGM-CSF accelerates neutrophil recovery and decreases the number of episodes of infection when the drug is administered in a two-hour infusion.10 11 12 To evaluate the possible benefit of rhGM-CSF, a randomized, double-blind, placebo-controlled trial was undertaken involving three independent institutions.
Methods
Selection of Patients
Patients with lymphoid neoplasia, including acute lymphocytic leukemia, Hodgkin's disease, and non-Hodgkin's lymphoma, who were undergoing autologous bone marrow transplantation were eligible for this study. Patients receiving autologous peripheral-blood progenitor cells were excluded. Consecutive patients were accrued independently over the same period at three centers: the Dana–Farber Cancer Institute, in Boston; the University of Nebraska Medical Center, in Omaha; and the Fred Hutchinson Cancer Research Center, in Seattle. Informed consent, conforming to the guidelines of the Food and Drug Administration and those of institutional review boards, was required at all centers.
The preparative regimens used before transplantation differed among the three institutions. At the Dana–Farber Cancer Institute, all the patients received cyclophosphamide (60 mg per kilogram of body weight, given on each of two successive days) and 1200 cGy of total-body irradiation, administered in 200-cGy fractions twice a day over a three-day period. All the patients received autologous bone marrow treated with B-cell monoclonal antibodies plus complement at the time of marrow collection.4 , 13 Only patients with lymphoma cells that expressed Bl antigen (CD20) were eligible for this trial.
At the University of Nebraska Medical Center, the patients received one of four preparative regimens, depending on the disease, the disease phase, and the amount of previous radiotherapy. Patients with Hodgkin's disease received four doses of cyclophosphamide (each dose, 1.5 g per square meter), six doses of etoposide (125 to 150 mg per square meter, given twice a day for three days), and one dose of carmustine (300 mg per square meter). Patients with indolent and early aggressive non-Hodgkin's lymphoma received two doses of cyclophosphamide (each dose, 60 mg per kilogram) and six doses of total-body irradiation (200 cGy given twice a day for three days, for a total dose of 1200 cGy). Patients with responsive non-Hodgkin's lymphoma received one dose of carmustine (300 mg per square meter), four doses of cyclophosphamide (each dose, 35 mg per kilogram), eight doses of cytarabine (each dose, 100 mg per square meter), and eight doses of etoposide (100 mg per square meter, given twice a day for four days). Patients with high-risk lymphoma received 2 doses of cyclophosphamide (each dose, 2.5 g per square meter), 1 dose of carmustine (300 mg per square meter), 12 doses of hydroxyurea (1.5 g per square meter, given every six hours for three days), and 6 doses of etoposide (150 mg per square meter, given twice a day for three days). The patients were stratified according to the stage of disease and the preparative regimen. Marrow purging was not used.
At the Fred Hutchinson Cancer Research Center, the preparative regimen for all patients consisted of cyclophosphamide (60 mg per kilogram, on each of two successive days) and total-body irradiation (1200 to 1440 cGy) over a period of six days. The patients were stratified according to diagnosis (acute lymphocytic leukemia, lymphoma with a favorable prognosis, or lymphoma with an unfavorable prognosis3) and according to whether they received marrow purged with a B-antigen monoclonal antibody. The decision to treat the marrow in vitro with B, monoclonal antibody was based on whether the phenotype of the tumor was known and on whether it was reactive to anti-B1 monoclonal antibodies.
Clinical Monitoring
The patients were routinely given transfusions when the hematocrit was less than 30 percent, and they received platelet transfusions when platelet counts were less than 20×109 per liter (20,000 per cubic millimeter). They were regularly started on broad-spectrum intravenous antibiotics when the absolute neutrophil count fell below 500×106 per liter at the Fred Hutchinson Cancer Research Center. At the Dana–Farber Cancer Institute and the University of Nebraska Medical Center, patients who had an absolute neutrophil count below 500×106 per liter were not given intravenous antibiotics until they had a fever. Amphotericin (0.5 to 1.0 mg per kilogram) was usually added empirically when the patients remained neutropenic and febrile for more than four days despite the use of broad-spectrum antibiotics. The patients were monitored with daily physical examinations, daily blood counts, electrolyte measurements, and kidney-function tests. Liver-function tests and additional laboratory tests of serum were performed three times a week.
Study Design
This was a prospective, randomized, double-blind, placebo-controlled trial with a target accrual of 120 patients. A total of 128 patients were accrued. They were registered and randomly assigned to treatment groups with computer-generated random numbers just before the start of the preparative regimen. All the registered patients were evaluated.
Study Medication
The patients randomly assigned to placebo received 50 ml of normal saline with 0.1 percent human serum albumin in a bag marked "study medication." The patients randomly assigned to rhGM-CSF received 250 μg of yeast-derived GM-CSF per square meter per day (specific activity, 5×107 colony-forming units per milligram; Immunex, Seattle; supplied by Hoechst—Roussel Pharmaceuticals, Somerville, N.J.), mixed with 50 ml of normal saline and 0.1 percent human serum albumin in a bag also labeled "study medication." In both instances, the study medication was begun within four hours of the completion of the autologous marrow infusion (day 1) and given in a two-hour infusion daily for 21 consecutive days.
Patients
One hundred twenty-seven patients with lymphoid cancer and one patient with acute nonlymphocytic leukemia were registered. Their characteristics are summarized in Table 1Table 1
Characteristics of the Patients According to Treatment Group.*. There were no significant differences between the two groups. All patients were followed for at least 100 days after autologous bone marrow transplantation.Data Handling
The day of recovery to a count of 100×106, 500×106, and 1000×106 absolute neutrophils per liter (100, 500, and 1000 per cubic millimeter) and of recovery to a count of 1000×106 white cells per liter was defined as the day when the first of two consecutive measurements on two different days was made at or above this specific level. Megakaryocyte engraftment was defined as the occurrence of a platelet count of at least 20×109 cells per liter that was sustained without platelet transfusions for seven days or more. A 28-day period (21 days of treatment with the study medication and 7 days of observation) was used for all data related to toxicity, fever, infections, and antibiotics. Documented infection was defined in febrile patients as the occurrence of a single blood culture positive for any organism other than coagulase-negative staphylococcus (for which two positive blood cultures were required, to help exclude contaminated samples). Patients with invasive infection in a closed body fluid or organ that was documented histologically, on culture, or both were also considered to have documented infection.
Statistical Analysis
Demographic comparisons were made with the Cochran—MantelHaenszel technique.14 Categorical variables, such as sex, were compared with use of the Cochran—MantelHaenszel chi-square statistic for general association. Numerical variables, such as age, were compared with use of the Cochran—MantelHaenszel chi-square analysis-of-variance statistic for the comparison of means. Comparisons of time-to-event outcomes, such as duration of hospitalizaron and time to engraftment, were performed with the Wilcoxon test.15 The Wilcoxon test places more weight on differences between treatment groups earlier in the course of the experiment than does the log-rank test. The effect of rhGM-CSF on increases in white-cell counts does not extend beyond the treatment period. One would therefore anticipate that differences between the treatment groups during the course of bone marrow transplantation probably occur within the 21-day treatment period. The comparison of categorical outcomes was performed with the same Cochran—MantelHaenszel chi-square statistic as was used for the categorical demographic outcomes. For the comparison of data involving counts, such as the number of days with fever, we used the Cochran—MantelHaenszel chi-square statistic for ridit scores, a rank-based, nonparametric procedure. Fisher's exact test was used to compare the incidence of infection and toxic effects. Chi-square statistics for the comparisons of efficacy were computed with stratification according to center.
Results
Hematologic Responses
Neutrophil recovery occurred earlier in the patients who received rhGM-CSF than in the patients who received placebo (Table 2)Table 2
Median Values for HematopoieticCell Recovery in the Two Groups of Patients, as Determined on the Basis of Absolute Neutrophil Count and Independence from Platelet Transfusions.. The time required to reach an absolute neutrophil count of 500×106 per liter for all patients is shown in Figure 1Figure 1Kaplan–Meier Analysis of the Time Required for the Absolute Neutrophil Count to Reach or Exceed 500 Cells per Cubic Millimeter on Two Consecutive Days in 65 Patients Who Received rhGM-CSF and 63 Patients Who Received Placebo.. Fifty-nine percent of the patients who received rhGM-CSF reached an absolute neutrophil count ≥500×106 per liter, and 39 percent reached an absolute neutrophil count ≥1000×106 per liter, within 21 days of the marrow infusion, as compared with 32 and 11 percent (P = 0.002 and P<0.001, respectively) of the patients who received placebo. Figure 2Figure 2Mean Daily Absolute Neutrophil Counts in 65 Patients Who Received rhGM-CSF and 63 Patients Who Received Placebo. shows the mean absolute neutrophil counts plotted against the time from bone marrow transplantation. There was no difference between the patients in the rhGM-CSF and placebo groups in mean absolute neutrophil count during the first 10 days. The time required to reach an absolute neutrophil count ≥100×106 cells per liter was one day less in the rhGM-CSF group than in the placebo group. After day 14, when this occurred, the curves diverged, reaching a maximal difference on the day of discontinuation of rhGM-CSF (day 21). Over the next 72 hours, a plateau was observed in the rhGM-CSF curve, but no change in the placebo curve. The time needed to reach a total white-cell count above 1.0×109 per liter was 3 1/2 days less in the patients who received rhGM-CSF (P = 0.014). The patients with Hodgkin's disease who received rhGM-CSF reached an absolute neutrophil count of 500×106 cells per liter by day 24, as compared with day 30 in the patients who received placebo. Among the patients who did not receive total-body irradiation, neutrophil recovery to 500×106 cells per liter was achieved six days earlier with rhGM-CSF. The inclusion or absence of total-body irradiation in the preparative regimen did not correlate with the time of neutrophil recovery (P = 0.592). The patients in the rhGM-CSF group became independent of platelet transfusions after 26 days, as compared with 29 days for the patients in the placebo group (P = 0.611). The patients who received rhGM-CSF required a median of 8 units of red cells, as compared with 10 units for the patients who received placebo (P = 0.047).Infections
The percentage of patients with fever on at least one day did not differ between the two groups (97 percent in each group), and in both groups the median duration of febrile episodes was eight days. After the patients became neutropenic, the number of days with fever still did not differ between groups. Documented infection developed, however, in 11 of the rhGM-CSF—treated patients (17 percent) during the first 28 days, as compared with 19 of the patients receiving placebo (30 percent) (P = 0.096). In the rhGM-CSF group, no bacterial infection was documented other than streptococcal bacteremia (nine infections), whereas in the placebo group, in addition to seven streptococcal infections, other bacterial infections were documented eight times. These infections included staphylococcal bacteremia (four) and fusobacterium bacteremia, corynebacterium bacteremia, staphylococcal cellulitis, and legionella pneumonia (one infection each). Only two of the rhGM-CSF—treated patients had infections other than with streptococcus; both had fungemia from candida species. By comparison, 12 patients receiving placebo had infections other than with streptococcus (P= 0.004). In addition to the eight bacterial infections, two involved candida fungemia and two involved disseminated aspergillosis. None of the patients who received rhGM-CSF had two or more positive blood cultures, as compared with six of the patients who received placebo (10 percent). Ninety percent of the patients in both groups who had documented infections had them when the absolute neutrophil count was ≤500×106 per liter. The median duration of therapy with amphotericin was not significantly different between the rhGM-CSF and the placebo groups (0 and 5 days, respectively; P = 0.37). The median duration of intravenous antibiotic therapy was shorter, however, in the rhGM-CSF group (24 days) than in the placebo group (27 days) (P = 0.009).
Toxicity
There were no differences between groups in the frequency of side effects associated with the study drug. The adverse events observed in more than 20 percent of the patients in each treatment group included fever, edema, nausea, vomiting, diarrhea, asthenia, anorexia, malaise, rash, dyspnea, gastrointestinal hemorrhage, and mucositis. The incidence of toxic effects previously suggested to be related to rhGM-CSF,10 11 12 such as myalgia, malaise, bone pain, diarrhea, and rash, was not different between the two groups.
The toxicity of rhGM-CSF could not be distinguished from that related to marrow transplantation. In seven patients the study drug was discontinued early because of suspected toxicity. Four of these patients had received rhGM-CSF, and three had received placebo. The study drug was discontinued early because of pulmonary infiltrates in one patient in the rhGM-CSF group and two patients in the placebo group. The study drug was discontinued in one patient in each group because of fever, and in two patients in the rhGM-CSF group — one because of thrombocytopenia and the other because of a pulmonary embolus.
The patients who received rhGM-CSF and those who received placebo did not differ in median values for the maximal serum bilirubin concentration (21 μmol per liter [1.2 mg per deciliter] in both groups, P = 0.527) or creatinine concentration (88 μmol per liter [1.0 mg per deciliter] and 107 μmol per liter [1.2 mg per deciliter]; P = 0.292) within the first 28 days. There was also no difference during the first 28 days in the severity of mucositis (P = 0.262) or in the median number of days on which morphine was required (P = 0.445).
Duration of Initial Hospitalization
The initial hospitalization was shorter in the patients who received rhGM-CSF (Fig. 3). Fifty-seven percent of these patients were discharged by day 28, as compared with 38 percent of the patients receiving placebo (P = 0.002). The median duration of the initial hospital stay after autologous bone marrow transplantation in the rhGM-CSF group was 27 days, as compared with 33 days in the placebo group (P = 0.01).
Relapse and Survival to Day 100
There was no difference in the rates of actual or actuarial relapse or survival to day 100 between the two groups. Sixty-three of the rhGM-CSF—treated patients (97 percent) had complete remission, as compared with 56 of the patients receiving placebo (89 percent). Nine of the rhGM-CSF—treated patients (14 percent) relapsed before day 100, as compared with six (10 percent) of the patients who received placebo. All patients who relapsed had a recurrence of their primary disease. Eighty-eight percent of the patients who received rhGM-CSF were alive 100 days after bone marrow transplantation, as compared with 87 percent of the patients who received placebo. For the patients who died within 100 days, the causes of death are shown in Table 3Table 3
Causes of Death within the First 100 Days after Transplantation in the rhGM-CSF and Placebo Groups..Discussion
The primary objective of this trial was to determine whether rhGM-CSF has salutary effects on the course of patients undergoing autologous bone marrow transplantation. Data from phase I—II trials in such patients suggested that rhGM-CSF was minimally toxic at doses that appeared to accelerate hematopoietic recovery.10 11 12 The data from this prospective, randomized study demonstrate that treatment with rhGM-CSF by two-hour infusion was not toxic in patients undergoing autologous bone marrow transplantation and did accelerate the recovery of neutrophils after transplantation. Despite reports from others that a continuous infusion of rhGM-CSF was associated with a greater proliferation of neutrophils than was a bolus infusion, the toxicity of the continuous infusion appeared greater.16 Furthermore, in Seattle, patients who received rhGM-CSF by continuous infusion before beginning this trial did not have an earlier recovery of the neutrophil count than patients who received the drug on the two-hour infusion schedule.17 Further randomized trials will be necessary to determine whether this is the optimal dose and schedule for rhGM-CSF.
Overall, there was a trend toward fewer infections in the rhGM-CSF group. Although rhGM-CSF was not protective against streptococcal bacteremia, which is generally a catheter-associated infection, infections with organisms other than streptococci were substantially fewer in the patients who received rhGM-CSF. Furthermore, a significant reduction in the number of days of intravenous antibiotics was observed in these patients. Treatment with rhGM-CSF may protect against infection in patients undergoing autologous bone marrow transplantation by two mechanisms. It shortens the period of neutropenia during which patients are placed at high risk, and it may increase the functional activity of neutrophils, monocytes, and tissue macrophages, thus increasing the antibacterial and antifungal effectiveness of the cells that are present during the period of neutropenia. Although a previous report suggested that when given by continuous infusion, rhGM-CSF might decrease the effectiveness of phagocytes by interfering with their ability to migrate to areas of inflammation,18 data from trials in animals19 20 21 and the present data suggest that the administration of rhGM-CSF reduces infection. The numbers of febrile days and infections with streptococcal bacteremia were not different between the two groups, however.
No consistent toxicity ascribed to rhGM-CSF was found in the present study; an equal number of patients in the two treatment groups had their drug discontinued prematurely. Other phase I—II trials suggest that in about 30 percent of patients therapy with rhGM-CSF is associated with mild toxicity, consisting of myalgia, joint pain, fatigue, nausea, diarrhea, and low-grade fever.22 23 24 The results of this trial suggest that these toxic effects are difficult to distinguish from those associated with marrow transplantation. The dose of rhGM-CSF in this trial was also lower, and the schedule (two-hour infusion) different, from those used in many other trials. This may have contributed to the lack of observed toxicity. There was also no difference with respect to more serious toxic effects, such as pericardial or pleural effusions, previously identified as being associated with rhGM-CSF at higher doses.10
Despite some earlier data suggesting that the administration of rhGM-CSF was associated with elevated platelet counts in primates and in patients after cytotoxic therapy,8 9 10 , 25 there were no consistent effects on platelet recovery in the present study. Surprisingly, the number of units of red cells infused was significantly lower in the patients who received rhGM-CSF. Other trials have not identified lower requirements for red-cell transfusion in association with rhGM-CSF administration.10 11 12 Further randomized trials will be needed to confirm this result before it can be concluded that rhGM-CSF stimulates recovery of red cells and platelets, as well as granulocytes, in patients undergoing autologous bone marrow transplantation. The patients who received rhGM-CSF still had two weeks of severe neutropenia and more than three weeks of thrombocytopenia, and they required a number of transfusions of platelets and red cells. Additional strategies to shorten the period of pancytopenia further are required. Such strategies might include combining rhGM-CSF with other cytokines, such as interleukin-326 27 28; providing a reinfusion of additional autologous peripheral-blood progenitor cells, collected after either cytokine stimulation or cytotoxic therapy25 , 29; or both.
Treatment with rhGM-CSF had no adverse effect on the stability of engraftment, relapse, or survival during the first 100 days after marrow infusion. This experience is consistent with long-term follow-up results in patients in phase I—II trials.30 Longer follow-up analysis of this group will be required, however, before statements about the effect of rhGM-CSF on the long-term likelihood of relapse or survival can be made. The present data suggest that rhGM-CSF is safe and effective, that it reduces neutropenia, and that it thereby reduces the morbidity of patients undergoing autologous bone marrow transplantation for lymphoid cancer. Although survival was not improved, there was a significant reduction in the duration of hospitalization as a result of decreased morbidity.
Supported by grants (CA 18029, CA 34183, and CA 47748) from the National Cancer Institute and the Department of Health and Human Services.
We are indebted to K. Blake and M. Whalen at the Dana–Farber Cancer Institute; to J. Pearson at the University of Nebraska Medical Center; to K. Shannon-Dorcy, K. Lilleby, and K. Lee for major assistance and data management in conducting this study; to V. Rutkowska for excellent assistance in the preparation of the manuscript; and to the nursing staff, attending staff, fellows, and physician assistants at the Dana–Farber Cancer Institute, the University of Nebraska Medical Center, and the Fred Hutchinson Cancer Research Center for outstanding patient care.
Source Information
From the Fred Hutchinson Cancer Research Center (J.N., J.W.S., C.D.B., J.A.H., F.R.A.), the University of Washington (J.N., J.W.S., F.R.A., C.D.B., J.A.H.), the Veterans Affairs Medical Center (J.N., J.W.S.), and the Immunex Corporation (N.O., S.G.), all in Seattle; the Dana–Farber Cancer Institute, Boston (S.N.R., A.S.F., J.R., L.M.N.); the University of Nebraska Medical Center, Omaha (P.J.B., J.M.V., J.O.A.); and Hoechst—Roussel Pharmaceuticals, Somerville, N.J. (D.O., M.G.). Address reprint requests to Dr. Nemunaitis at 111-ONC, Veterans Affairs Medical Center, 1660 S. Columbian Way, Seattle, WA 98108.
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