Original Article
Cyclosporine, Methotrexate, and Prednisone Compared with Cyclosporine and Prednisone for Prophylaxis of Acute Graft-versus-Host Disease
N Engl J Med 1993; 329:1225-1230October 21, 1993
- Abstract
Background
Acute graft-versus-host disease (GVHD) following allogeneic bone marrow transplantation remains a serious problem. In a clinical trial, we tested the combination of cyclosporine and prednisone with and without methotrexate for the prevention of GVHD.
Methods
One hundred fifty patients with either acute leukemia in first complete remission, chronic myelogenous leukemia in first chronic phase, or lymphoblastic lymphoma in first complete remission were enrolled in the study. All the patients were given fractionated total-body irradiation (1320 cGy) and etoposide (60 mg per kilogram of body weight) in preparation for transplantation, and received bone marrow from genotypically histocompatible donors. To prevent GVHD, they were randomly assigned to prophylactic treatment with either cyclosporine, methotrexate, and prednisone or cyclosporine and prednisone without methotrexate. All the patients received standardized supportive care after transplantation, including intravenous gamma globulin.
Results
Patients receiving cyclosporine, methotrexate, and prednisone had a significantly lower incidence of acute GVHD of grades II to IV (9 percent) than those receiving cyclosporine and prednisone (23 percent, P = 0.02). Multivariate regression analysis demonstrated that an increased risk of acute GVHD was associated with an elevated serum creatinine concentration (P = 0.006) and treatment with cyclosporine and prednisone alone (P = 0.02). The lower incidence of acute GVHD was not associated with a higher rate of relapse of leukemia or lymphoma. There was no significant difference in disease-free survival at three years between the two treatment groups (64 percent with the three-drug regimen vs. 59 percent with the two-drug regimen, P = 0.57).
Conclusions
The combination of cyclosporine, methotrexate, and prednisone was more effective in preventing acute GVHD of grades II to IV than was the combination of cyclosporine and prednisone without methotrexate.
Media in This Article
Figure 1
Regimen for the Three-Drug Group (Cyclosporine, Methotrexate, and Methylprednisolone or Prednisone).Figure 2
Cumulative Probability of Acute GVHD (Grades II to IV), According to Treatment Group.Article Activity
- Article
Acute graft-versus-host disease (GVHD) is a serious problem in recipients of allogeneic bone marrow grafts1. Several approaches have been used to prevent it. Removal of T cells that are responsible for acute GVHD2,3 resulted in a lower incidence of this complication but a higher incidence of graft failure and relapse3,4. Another approach to the prophylaxis of acute GVHD is the use of immunosuppressive drugs such as methotrexate, cyclosporine, and cyclophosphamide, either singly or combined with other agents, including prednisone5-10. Recently, the use of intravenous immune globulin has also been shown to decrease the incidence of acute GVHD11.
Two prospective randomized trials in patients with leukemia or aplastic anemia have shown that the combination of cyclosporine and methotrexate was superior to either drug alone in preventing GVHD6,12. Even with this regimen, however, the incidence of acute GVHD (grades II to IV) was 20 to 30 percent6,13. Although prednisone is the most effective drug for therapy of acute GVHD, its use in combination with cyclosporine, methotrexate, or cyclophosphamide has also been shown to be effective for prophylaxis of acute GVHD8-10,14-16.
In 1976 we began a series of sequential trials of prophylaxis of acute GVHD. In a prospective randomized comparison, cyclosporine combined with prednisone reduced the incidence of GVHD of grades II to IV from 47 to 28 percent, as compared with methotrexate combined with prednisone16. Modifying the combination of cyclosporine and prednisone by increasing the dose of prednisone and starting to give this drug on day 710 rather than on day 1516 further reduced the incidence of grades II to IV GVHD, to 12 percent (unpublished data). We conducted a randomized study to determine whether the addition of three doses of methotrexate to the combination of cyclosporine and prednisone would further decrease the incidence of acute GVHD.
Methods
Patients
All clinical protocols were approved by the institutional review boards at Stanford University Medical Center and the City of Hope National Medical Center. The risks and benefits of the treatment regimens were explained to each patient in detail during at least two outpatient visits and again on the day of admission. Written consent was obtained from all patients and, for minors, from a parent or guardian.
During the five-year period between December 1986 and December 1991, 150 patients were enrolled in the study. These patients represented a uniform group of “best-risk candidates” with acute leukemia, lymphoblastic lymphoma in first remission, or chronic myelogenous leukemia in first chronic phase. Patients with acute lymphoblastic leukemia or lymphoma were considered to be at high risk for relapse. All patients received bone marrow grafts from genotypically matched donors. Patients were stratified before randomization according to their age and type of leukemia. One hundred forty-nine patients could be evaluated for analysis. One patient died on day 19 (after transplantation but before engraftment) and could not be evaluated for GVHD, but was included in the survival analysis. All the other patients survived for at least 32 days after grafting. Three patients declined to receive the assigned regimen: two patients had been assigned to the three-drug regimen (cyclosporine, methotrexate, and prednisone or methylprednisolone) but chose to receive the two-drug regimen (cyclosporine and prednisone or methylprednisolone), and one patient assigned to the two-drug regimen preferred to receive the three-drug regimen. One other patient was assigned to the three-drug regimen, but did not receive methotrexate because renal insufficiency developed. All 149 patients who could be evaluated for GVHD were analyzed according to their original treatment assignment (intention-to-treat analysis). Their characteristics are shown in Table 1Table 1
Characteristics of the Patients, According to Treatment Group..Preparatory Regimen
All patients received a uniform preparatory regimen consisting of total-body irradiation with 1320 cGy, given in 11 fractions on day -7 through day -4, and etoposide in a dose of 60 mg per kilogram of body weight, infused intravenously over a four-hour period on day -3 as previously described17,18. The bone marrow was infused on day 0.
GVHD Prophylaxis
All patients received cyclosporine by continuous intravenous infusion with a loading dose, starting on day -2 (Figure 1Figure 1
Regimen for the Three-Drug Group (Cyclosporine, Methotrexate, and Methylprednisolone or Prednisone).). Serum cyclosporine concentrations were measured twice a week by immunoassay (TDx System, Abbott Laboratories, Abbott Park, Ill.)19. Patients assigned to the three-drug regimen received a reduced dose of methotrexate if they had renal or hepatic dysfunction or extensive mucositis. Methylprednisolone treatment was begun on day 7, with a dose of 0.5 mg per day given intravenously; this dose was doubled on day 15. On day 29, oral prednisone was substituted for intravenous methylprednisolone; the dose was slowly tapered and discontinued. If acute GVHD of grades II to IV developed, methylprednisolone was given intravenously in a dose of 2 mg per kilogram.The amount of each drug actually administered was determined by a review of records and expressed as a percentage of the planned dose. Measurements of serum cyclosporine during the time of risk of acute GVHD were obtained from laboratory records.
Grading of Acute GVHD
Acute GVHD was graded uniformly by clinical investigators at the two study centers according to previously described criteria20. Retrospective chart reviews were also performed at the end of the trial. All patients with a rash suggesting GVHD underwent biopsy to document involvement with acute GVHD. Biopsies of the liver and gut were performed if clinically indicated.
Supportive Care
All patients were hospitalized in private rooms with a high-efficiency particulate air-filtration system. Reverse-isolation techniques as well as masks and gowns were used if a patient's neutrophil count was less than 500 per cubic millimeter. Broad-spectrum antibiotics were used to treat initial episodes of fever, and a low dose of amphotericin B (0.15 mg per kilogram) was given to all patients as prophylaxis, beginning on day 1. All blood products were irradiated (2500 cGy) before they were infused. Intravenous immune globulin (Gammagard, Baxter Healthcare, Hyland Division, Glendale, Calif.; or Gamimune N, Cutter Biologicals, Elkhart, Ind.) was administered to all patients in a dose of 500 mg per kilogram every other week from day -7 to day 100.
Patients who were seropositive for cytomegalovirus or who received bone marrow from a donor seropositive for the virus underwent bronchoalveolar lavage on day 35. Those whose bronchoalveolar-lavage material was found to be positive for cytomegalovirus received prophylaxis with ganciclovir as previously described21. None of the 150 patients enrolled received any hematopoietic growth factors.
Statistical Analysis
The patients' characteristics and the outcomes in the two treatment groups were compared by Pearson's chi-square test or Fisher's exact test for frequency data and by Wilcoxon's rank-sum test for continuous data. All tests used an alpha level of 0.05 and a two-sided alternative hypothesis. The primary variable in the analysis of outcomes was acute GVHD. The Mantel-Haenszel chi-square test was used to test for an increased risk of acute GVHD, with adjustment for any significant differences in patients' characteristics. Probabilities of survival, relapse, and acute GVHD over time were estimated with the product-limit method of Kaplan and Meier and were compared by the log-rank statistic22. The time to the development of acute GVHD was also examined by univariate and stepwise Cox regression analyses. All variables found to have a P value of less than 0.10 in univariate analyses were considered candidate variables for multivariate analysis. The results presented include our findings as of September 30, 1992.
Results
Drug Administration
Both groups of patients had similar median serum concentrations of cyclosporine (367 ng per milliliter in the three-drug group and 391 ng per milliliter in the two-drug group, P = 0.28). The median percentage of methotrexate administered was 100 percent. All but one patient received the first and second doses. Seven patients did not receive the third (last) dose on day 6 because of extensive mucositis (four patients), renal dysfunction (one patient), or hepatic dysfunction (two patients). All patients received at least the target doses of methylprednisolone and prednisone, and several patients received higher doses to treat acute GVHD.
Engraftment
All patients had engraftment with donor cells according to assays using restriction-fragment-length polymorphisms or other suitable genetic markers. The results of granulocyte and platelet recovery are summarized in Table 2Table 2
Outcome According to Treatment Group.. All patients could be evaluated for granulocyte engraftment except one patient treated with the three-drug regimen, who died of sepsis on day 19. Patients receiving only cyclosporine and prednisone had significantly faster recovery of granulocyte counts (13 vs. 20 days, P<0.001) and platelet counts (17 vs. 23 days, P = 0.003). The delay in granulocyte engraftment, however, did not result in an increase in infectious complications. The platelet counts of six patients receiving cyclosporine, methotrexate, and prednisone and five receiving only cyclosporine and prednisone did not rise above 25,000 per cubic millimeter.Toxicity
No unexpected toxic reactions attributable to the prophylaxis of GVHD were observed, and there were no differences between the two treatment groups in the incidence of early infectious complications. Over 90 percent of the patients in each group required narcotics to control pain associated with mucositis.
The median peak serum bilirubin level was 2.2 mg per deciliter (38 μmol per liter) in the three-drug group and 1.8 mg per deciliter (30 μmol per liter) in the two-drug group (P = 0.08). The incidence of hepatic veno-occlusive disease was also similar in each group (two patients in the three-drug group and one in the two-drug group). The median peak serum creatinine levels of the groups did not differ significantly (1.5 vs. 1.6 mg per deciliter [130 vs. 140 μmol per liter], P = 0.20). As shown in Table 2, the causes of treatment failure associated with the two regimens were similar.
Acute GVHD
The overall incidence of acute GVHD is shown in Table 2 and Figure 2Figure 2
Cumulative Probability of Acute GVHD (Grades II to IV), According to Treatment Group.. Two interim analyses had demonstrated a trend in favor of the group receiving methotrexate (incidence of acute GVHD, 10 percent vs. 22 percent in each analysis; P = 0.13 and 0.06, respectively); the final analysis demonstrated a significant advantage in this group (9 percent vs. 23 percent, P = 0.02).Univariate Cox regression analysis (Table 3Table 3
Univariate Cox Regression Analysis of Time to Acute GVHD.) revealed several factors that were associated with the development of acute GVHD: the absence of methotrexate from the regimen (P = 0.02), granulocyte engraftment requiring less than 16 days (P = 0.06), elevation of the serum creatinine concentration (P<0.001), and older age at time of transplantation (P = 0.06). The stepwise Cox regression analysis revealed two factors that were independently predictive of the occurrence of acute GVHD: the absence of methotrexate from the regimen (P = 0.02; risk ratio, 2.67 [95 percent confidence interval, 1.10 to 6.49]) and elevation of the creatinine concentration (P = 0.006; risk ratio, 1.38 [95 percent confidence interval, 1.16 to 1.65]).Chronic GVHD
The incidence of chronic GVHD was similar in both treatment groups. Most patients had limited chronic GVHD (Table 2). However, eight patients receiving only cyclosporine and prednisone died of complications of chronic GVHD, as compared with three patients receiving cyclosporine, methotrexate, and prednisone (P = 0.09). As shown in Table 2, the median Karnofsky performance score in each group at the last evaluation was 90 (range, 60 to 100).
Recurrence of Leukemia
The lower incidence of acute GVHD (grades II to IV) in the group receiving methotrexate was not associated with a higher number of relapses. Relapse occurred in 16 patients: 9 patients receiving only cyclosporine and prednisone and 7 receiving these drugs and methotrexate (Table 2). The recurrence rate at three years was 13 percent in the three-drug group, and 16 percent in the two-drug group.
Survival
Of the 150 patients enrolled, 101 (67 percent) survived for 9 to 70 months; the median follow-up was 31 months. The disease-free survival at three years (Figure 3Figure 3
Cumulative Probability of Disease-free Survival, According to Treatment Group.) was 59 percent in the group receiving only cyclosporine and prednisone and 64 percent in the group receiving these drugs and methotrexate (P = 0.57).Causes of Death
Twenty-six patients who received cyclosporine and prednisone and 22 patients who received these drugs and methotrexate had a relapse or died during the study (Table 2). The single largest cause of treatment failure was a recurrence of the underlying disease. All the causes of death are listed in Table 2. There was no significant difference between the two treatment groups in the incidence of causes of death.
Discussion
Cyclosporine combined with prednisone has been found to be superior to methotrexate combined with prednisone in preventing acute GVHD8,10,16. The combination of cyclosporine and methotrexate was superior to either drug alone13. However, the use of either of these two combination regimens was still associated with an incidence of acute GVHD (grades II to IV) of more than 20 percent. An attempt was made to reduce the incidence of acute GVHD further by adding three doses of methotrexate to cyclosporine combined with prednisone. We used three doses of methotrexate, since many patients never receive a fourth dose because of cumulative toxicity and since the toxicity of the prophylactic regimen against GVHD might add to the toxicity of the preparatory regimen containing etoposide23.
In this study, methylprednisolone was begun on day 7 rather than on day 15, and the dose of methylprednisolone used was higher than the dose we used previously16. Although the results of this phase 3 study with cyclosporine and prednisone were not as good as those of the phase 2 trial, they are similar to those of other studies of prophylaxis of acute GVHD with cyclosporine and prednisone8,10,24.
The cumulative incidence and characteristics of chronic GVHD that we observed are similar to those described by others10,25,26. Few patients had serious discomfort due to chronic GVHD. Most patients had mild changes in their skin or buccal mucosa that did not affect their daily activities. However, eight patients receiving only cyclosporine and prednisone had chronic GVHD and died of associated infections or bronchiolitis obliterans, whereas three patients receiving these drugs and methotrexate died of complications associated with chronic GVHD. The median Karnofsky performance score was 90 in both groups, and as described previously, the quality of life in the majority of the patients in the study was good27.
Despite the decrease in acute GVHD among the patients receiving methotrexate, their disease-free survival did not differ significantly from that of the patients not receiving this drug. Both groups of patients fared relatively well, with three-year disease-free survival rates of 59 and 64 percent; thus, a considerably larger number of patients would have to be enrolled to permit detection of a significant difference in disease-free survival.
In a previous study of prednisone combined with cyclosporine, the addition of methotrexate did not improve the results25. There were more cases of acute GVHD among the patients receiving cyclosporine, prednisone, and methotrexate when high-dose prednisone treatment (2 mg per kilogram) was begun on day 1 after allografting. This effect was avoided if prednisone was delayed until day 15. The differences in the dose and schedule of methotrexate and prednisone treatment may explain the observed differences between these studies.
For this study, we selected a uniform population of “best-risk” candidates for allogeneic bone marrow transplantation. We believed this to be the ideal group in which to study prophylaxis of acute GVHD, because confounding due to variations among preparatory regimens and differences in disease status is minimized. This ideal population may help explain the low incidence of acute GVHD and of recurrence of leukemia23.
Supported by grants (CA-30206 and CA-49605) from the National Cancer Institute.
We are indebted to the house staff, clinical fellows, and nursing staff of the bone marrow transplantation programs of Stanford University School of Medicine and the City of Hope National Medical Center for their outstanding patient care, to Dr. Frank Stockdale for his critical reading of the manuscript, and to Sara E. Clark for assistance in the preparation of the manuscript. We shall miss the important contribution to improved patient care and outcome made by Gerhard M. Schmidt, who died on May 5, 1993.
Source Information
From the Bone Marrow Transplantation Program (N.J.C., M.D.A., G.D.L., R.S.N., K.G.B.) and the Department of Health Research and Policy (R.M.W.), Stanford University, Stanford, Calif., and the Department of Hematology and Bone Marrow Transplantation (G.M.S., A.P.N., M.R.O., P.M.P., E.P.S., D.S.S., A.S.S., S.J.F.) and the Department of Biostatistics (J.C.N., A.C.D.), City of Hope National Medical Center, Duarte, Calif.
Address reprint requests to Dr. Chao at Stanford University Medical Center, 300 Pasteur Dr., Rm. H1353, Stanford, CA 94305.
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