Original Article
Chemotherapy of Advanced Hodgkin's Disease with MOPP, ABVD, or MOPP Alternating with ABVD
N Engl J Med 1992; 327:1478-1484November 19, 1992
- Abstract
- Abstract
Background and Methods.
MOPP (mechlorethamine, vincristine, procarbazine, and prednisone) has been the standard treatment for Hodgkin's disease for almost 20 years. In a randomized, multicenter trial, we compared three regimens of primary systemic therapy for newly diagnosed advanced Hodgkin's disease in Stages IIIA2, IIIB, and IVA or IVB: (1) MOPP alone given for 6 to 8 cycles, (2) MOPP alternating with ABVD (doxorubicin, bleomycin, vinblastine, and dacarbazine) for 12 cycles, and (3) ABVD alone for 6 to 8 cycles. Patients in a first relapse after radiation therapy were eligible. No additional radiation therapy was given. Patients who did not have a complete response or who had a relapse with either MOPP alone or ABVD alone were switched to the opposite regimen.
Results.
Of 361 eligible patients, 123 received MOPP, 123 received MOPP alternating with ABVD, and 115 received ABVD alone. The patients were stratified according to age, stage, previous radiation, histologic features, and performance status. The overall response rate was 93 percent, with complete responses in 77 percent: 67 percent in the MOPP group, 82 percent in the ABVD group, and 83 percent in the MOPP—ABVD group (P = 0.006 for the comparison of MOPP with the other two regimens, both of which contained doxorubicin). The rates of failure-free survival at five years were 50 percent for MOPP, 61 percent for ABVD, and 65 percent for MOPP—ABVD. Age, stage (III vs. IV), and regimen influenced failure-free survival significantly. Overall survival at five years was 66 percent for MOPP, 73 percent for ABVD, and 75 percent for MOPP—ABVD (P = 0.28 for the comparison of MOPP with the doxorubicin regimens). MOPP had more severe toxic effects on bone marrow than ABVD and was associated with greater reductions in the prescribed dose.
Conclusions.
In this trial, ABVD therapy for 6 to 8 months was as effective as 12 months of MOPP alternating with ABVD, and both were superior to MOPP alone in the treatment of advanced Hodgkin's disease. ABVD was less myelotoxic than MOPP or ABVD alternating with MOPP. (N Engl J Med 1992;327:1478–84.)
Media in This Article
Figure 1
Failure-free Survival According to Primary Chemotherapeutic Regimen.Figure 2
Overall Survival According to Primary Chemotherapeutic Regimen.Article Activity
- Article
THE introduction of MOPP (mechlorethamine, vincristine, procarbazine, and prednisone) was a seminal event in the treatment of Hodgkin's disease, demonstrating the principles and success of combination chemotherapy when effective drugs are given in a cyclic schedule and leading to subsequent successful trials in non-Hodgkin's lymphoma and other cancers.1 The long-term results achieved with MOPP were influenced by the quantity of tumor, the performance status, and accompanying constitutional symptoms, as well as by previous chemotherapy, age, tolerance by bone marrow, and the dose intensity of the active agents.2 3 4 5 6 7 MOPP was found to have substantial toxic effects, including sterilization in both sexes, long-term subclinical immunosuppression, and secondary myelodysplasia or acute nonlymphocytic leukemia.8 9 10 Less acutely toxic variants of MOPP that contain alkylating agents, such as ChlVPP (chlorambucil, vinblastine, procarbazine, and prednisone), have similar benefits and also present the risk of secondary leukemia.11
Chemotherapeutic regimens composed of drugs differing in structure, toxicity, and activity and intended to be used as second-line or alternative treatments were developed at the Milan Cancer Institute beginning with ABVD (doxorubicin [Adriamycin], bleomycin, vinblastine, and dacarbazine) as a combination treatment presumed to be non—cross-resistant.12 A relatively high level of activity as second-line therapy was noted for ABVD, especially in patients who had relapses after a complete remission with MOPP therapy.13 14 15 16 The Milan group noted that ABVD was not associated with either permanent male sterility or treatment-induced myelodysplasia or leukemia.17 , 18 It proved to be the standard second-line treatment of choice until it was included as primary treatment of Stage IV disease in a program in which MOPP and ABVD were given alternately for up to 12 cycles. The apparent superiority of the alternating program over MOPP alone in a single randomized trial led to the widespread use of this prolonged program, which offered the toxic potential of both MOPP and ABVD.19
In 1982 the Cancer and Leukemia Group B (CALGB) began a randomized trial comparing the efficacy and toxicity of ABVD alone with those of MOPP alone, and with a third group in which previously untreated patients were given MOPP in alternation with ABVD as primary therapy for 12 monthly cycles. Patients with Stage IIIA2, IIIB, or IVA or IVB Hodgkin's disease and those with a relapse after definitive radiotherapy for localized disease were treated.
Methods
Eligibility
Patients 16 years of age or older who had biopsy-proved Hodgkin's disease were eligible for the trial, and all biopsy specimens were reviewed by the Central Lymphoma Trial Pathology Panel. Previously untreated patients were required to be in clinical and pathological Stage IIIA2, IIIB, or IVA or IVB, according to the modified Ann Arbor criteria.20 Patients with recurrent disease after primary radiation therapy for localized disease were also eligible, but at least three months had to have elapsed since the completion of radiation therapy. At least one tumor mass measurable by physical or radiologic examination was required. Adequate renal and hepatic function was also required, together with the presence of a normal reserve of bone marrow. Liver enlargement in itself, splenomegaly when it constituted the only measurable mass, bone-scan abnormalities without lytic lesions on plain x-ray film, and cytologically negative effusions were not considered measurable for the purposes of this trial. The presence of multiple positive lesions on a bone scan with radiographic evidence of lysis or sclerosis was considered a positive indication of bone involvement. Abnormal results on liver-function studies without proof of Hodgkin's disease at biopsy were not considered evidence of hepatic involvement. Minimal peripheral-blood hemoglobin concentrations in excess of 10 g per deciliter, white-cell counts in excess of 3.5×103 per cubic millimeter, and platelet counts in excess of 100×103 per cubic millimeter were required, unless there was bone marrow or splenic involvement, or a documented immunologic mechanism that could explain the lower blood counts.
An unambiguously positive lymphangiogram or abdominal CT scan was considered sufficient to document abdominal lymph-node involvement. Laparotomy was required only in patients who would otherwise be in clinical Stage I or II and who had equivocal or negative radiographic studies of the abdomen.
As part of the quality-assurance program of the CALGB, members of the Data Audit Committee visit all the participating institutions at least once every three years. The visitors verify compliance with federal regulations and protocol requirements, including those pertaining to eligibility, treatment, tumor response, and follow-up, in a sample of protocols at each institution. For 154 (39 percent) of the 395 patients treated in this study, a cohort in which all the participating institutions were represented, the medical records were reviewed in this manner.
Chemotherapeutic Regimens
After stratification according to age, stage, histologic features, previous radiation therapy, performance status, and the presence of a mediastinal mass, the patients were randomly assigned to one of three chemotherapy programs: MOPP, ABVD, or MOPP and ABVD given alternately.
The MOPP regimen was given according to the original program of the National Cancer Institute, except that the dose of vincristine was required not to exceed 2.0 mg.1 The ABVD regimen was given according to the scheme of the Milan Cancer Institute.21 In these two treatment groups, the cycles of MOPP and ABVD were repeated every 28 days until there was a complete response, after which two additional cycles were given, for a minimum of six cycles and a maximum of eight. Patients with stable or progressive disease after two full cycles, those who did not have a complete response after six cycles, and those who had a relapse after a complete response were switched to the alternative regimen. The MOPP-ABVD alternating program was given according to the scheme of the Milan Cancer Institute, with MOPP and ABVD given in alternation for a total of 12 cycles. Prednisone was given in cycles 1 and 7 only.19 Patients who had no response or who had progressive disease after four cycles were excluded from the trial. Those who did not have a complete response after 12 cycles were considered to have had a failure of induction therapy and were followed until there was progression of their disease.
The dose-modification scheme used in this trial is shown in Table 1Table 1
Schedule of Dose Modification.. It was to be applied to an individual cycle and was not planned to be cumulative. No adjunctive radiation therapy was used in the primary treatment of patients in any of the three groups in this trial.Evaluation
Follow-up reports were required after every two cycles of treatment, every three months for the first two years after treatment, and every six months thereafter. A chest film was required after every two cycles of chemotherapy. Similarly, bone scans, scans of the liver and spleen, and abdominal x-ray assessment of residual lymphangiogram dye, if it appeared abnormal, were required after every two cycles.
Criteria for Response
A complete response was defined as the complete disappearance for at least four weeks of all abnormalities (clinical, physical, and biochemical) attributable to Hodgkin's disease. Documentation of a complete response must have been completed within four to six weeks of the completion of therapy. Incomplete regression of large masses that regressed rapidly and almost completely, with stabilization for at least two additional cycles, was considered to constitute a complete response. There was no evidence of residual disease at other sites during complete response.
A partial response was defined as a reduction of at least 50 percent for at least four weeks in the sum of the products of the perpendicular diameters of all measurable masses, with no new lesions appearing and no progression at the original sites of disease.
Improved status was defined as a reduction by less than 50 percent in the sum of the products of the perpendicular diameters of a lesion, with no new lesions and only minimal progression (<25 percent) in any measured lesion.
Progression was defined as an increase of more than 25 percent in the product of the perpendicular diameters of any measured lesion or the appearance of new lesions.
Failure-free Survival
Failure-free survival was defined as the interval from the date of entry into the trial to the date of progression from a partial remission, the date of relapse after a complete remission, or the date of death from any cause without a documented relapse. Because of the uncertainty concerning the interpretation of residual masses in Hodgkin's disease, some patients with an apparently partial response eventually have a complete response, with slow resolution of a residual fibrotic mass, or they remain in a stable partial response. In such patients failure-free survival is considered more accurate than other measures of the efficacy of therapy. Disease-free survival was measured as the time from the documentation of a complete response to a relapse or to death from any cause. Overall survival was measured from the time of entry into the study to the time of death from any cause.
Statistical Analysis
Rates of complete response were compared between treatment groups and according to the characteristics of patients, with the appropriate chi-square test used for contingency tables.22 Time-to-event distributions (for failure-free survival and survival) were estimated by the product-limit method of Kaplan and Meier.23 The statistical significance of the differences observed in the distributions of times to an event was assessed with the log-rank test.24 All P values reported are two-sided.
Results
A total of 400 patients not previously treated with systemic therapy were randomized after stratification for age, stage, and previous radiation therapy. Thirty-nine patients were excluded for the following reasons: 5 never received therapy according to the protocol, 10 did not meet the criteria for eligibility, 19 had diagnoses other than Hodgkin's disease, 3 had no central review of their pathologic conditions, and 2 had incomplete study data. Among the remaining 361 eligible patients, 123 were randomly assigned to MOPP, 115 to ABVD, and 123 to MOPP-ABVD. The median follow-up time was six years, and every patient was followed for at least four years. The median age was 34 years (range, 16 to 72), with 14 percent of patients between 50 and 59 years of age and 9 percent over the age of 60. Sixty-four percent were male. Thirty-six percent had Stage III disease, 47 percent had Stage IV disease, and 17 percent were in relapse after previous radiation therapy. Fifty-five percent had a performance status of 0 (Table 2Table 2
Characteristics of Patients According to Treatment Group.). The histologic subgroups included 68 percent with nodular sclerosis and 27 percent with mixed cellularity. The remainder of the tumors were lymphocyte-predominant (1 percent), lymphocyte-depleted (1 percent), or unclassified (3 percent). The clinical characteristics of the patients are shown in Table 2 according to treatment group. Twenty-four percent had a staging laparotomy as part of their initial evaluation.Induction of Remission
The overall response rate was 93 percent. The rate of complete response for the entire group was 77 percent, with partial responses in 16 percent. Fourteen patients were considered improved, and no response or progression was noted in seven. Five additional patients were excluded from the study without evaluation and were considered to have had failures of treatment. The rates of complete response for the individual treatments were 67 percent for MOPP, 82 percent for ABVD, and 83 percent for MOPP-ABVD; there was a significantly higher rate of complete response in the groups with treatment containing doxorubicin as compared with MOPP alone (P = 0.006) (Table 3Table 3
Response to Treatment of Patients with Advanced Hodgkin's Disease, According to Regimen.). When MOPP alone was compared with ABVD, the relative risk was 0.83 (95 percent confidence interval, 0.71 to 0.96). The rate of complete response was adversely affected by age ≥50 years (67 percent vs. 80 percent for age <50; P = 0.01); by a performance-status score of 2, indicating that the patient was in bed less than half the time (52 percent vs. 80 percent for scores of 0 or 1; P = 0.001); by the presence of constitutional symptoms (73 percent vs. 84 percent without symptoms; P = 0.02); and by liver involvement (65 percent vs. 79 percent without such involvement; P = 0.02). Sex, stage, and histologic features did not influence response. The overall disease-free survival of patients with a complete response was 66 percent at five years and did not differ according to therapy.Failure-free Survival
The rate of failure-free survival for the entire group was 60 percent at five years. Significant differences in this measure were observed at five years in the treatment groups: 50 percent for MOPP, 61 percent for ABVD, and 65 percent for MOPP—ABVD (P = 0.02 for the comparison of MOPP with the other regimens) (Fig. 1Figure 1
Failure-free Survival According to Primary Chemotherapeutic Regimen.). When MOPP alone was compared with ABVD, the relative risk was 0.69 (95 percent confidence interval, 0.47 to 1.02; P = 0.006). The factors that influenced failure-free survival significantly were age (P = 0.002), regimen (P = 0.02), and stage (III vs. IV) (P = 0.03). Another clinical characteristic predictive of significantly lower rates of failure-free survival was the presence of two or more extranodal sites (P<0.001). This difference extended to overall survival (P = 0.03). There was no difference in predictive ability between Stage III and Stage IV with one extranodal site, but both were significantly better than Stage IV with two or more extranodal sites (P = 0.03). The overall five-year survival for the treatment groups was 66 percent for MOPP, 73 percent for ABVD, and 75 percent for MOPP-ABVD (P = 0.28 for the comparison of MOPP with the other regimens) (Fig. 2Figure 2Overall Survival According to Primary Chemotherapeutic Regimen.).Two general prognostic groupings are possible in the context of these prognostic factors: (1) a low-risk group composed of patients less than 50 years old with either Stage III disease or Stage IV disease with one extranodal site (57 percent of all the patients with a five-year failure-free survival of 70 percent), and (2) a high-risk group composed of patients who are over 50 years old or who have Stage IV disease with two or more extranodal sites (five-year failure-free survival, 45 percent). The statistical power to detect a difference between regimens according to risk group was small (78 percent) because of the size of the sample. The failure rate for MOPP in the low-risk group was 36 percent (24 of 67 patients), as compared with 57 percent (38 of 67) in the high-risk group; the rates were 31 percent and 38 percent, respectively, for ABVD.
Toxicity
The short-term toxic effects of each regimen are summarized in Table 4Table 4
Toxicity of Induction Therapy.. There were significant differences in the extent of hematologic toxicity noted with each regimen. In the two groups treated with regimens containing MOPP, neutropenia was severe in 47 to 53 percent of the patients and life-threatening in 21 to 28 percent, as compared with 18 percent and 3 percent, respectively, for ABVD alone (P<0.001), which resulted in a higher incidence of infectious complications. Clinically important severe pulmonary toxicity occurred in 6 percent of the ABVD group.At the time this article was written, 30 patients had died without progression of their Hodgkin's disease. Second tumors were found to be non—small-cell lung cancer in four patients (two treated with ABVD alone and two treated with MOPP—ABVD), all of whom were over 50 at the time of diagnosis of Hodgkin's disease. Two acute leukemias had occurred (one in the MOPP group and one in the MOPP—ABVD group). In the ABVD group, there were three cases of fatal pulmonary toxicity in older patients (42, 69, and 72 years of age), one of whom received ABVD after previous radiation therapy. Two deaths from cardiac failure occurred while patients were in remission, one of which may have been related to doxorubicin. The other causes of death included sepsis (six patients), pneumonias (three), accidents (two), Pneumocystis carinii pneumonia (one), cytomegalovirus pneumonia (one), pulmonary embolism (one), myocardial infarction (one), and unknown causes (four).
Delivery of Chemotherapy
The protocol provided for the doses of myelosuppressive drugs to be modified according to the levels of white cells and platelets at the time scheduled for the receipt of the next cycle of chemotherapy (Table 1). Moreover, the protocol called for the modification of doses to 75 percent of the previous dose if the nadir white-cell count fell below 1×103 per cubic millimeter or the platelet count below 30×103 per cubic millimeter. An analysis of the doses administered was performed for the first 148 patients (49 receiving MOPP, 49 receiving ABVD, and 50 receiving MOPP—ABVD). Although 92 percent of the patients received the dose of mechlorethamine prescribed in the protocol in the first cycle of MOPP, there was a gradual reduction in the percentage of patients receiving 85 percent or more of the prescribed dose such that by cycle 6 only 24 percent of patients received that amount. This is in sharp contrast to the dosing of doxorubicin in the ABVD group, in which a full (≥85 percent) dose of the drug was given to more than 80 percent of patients in each of the first six cycles (Fig. 3Figure 3
Proportion of Patients Receiving the Full Dose of Mechlorethamine in MOPP or Doxorubicin in ABVD in Each of Six Cycles of Therapy.). In the MOPP—ABVD group there was an alternating pattern, with higher proportions of patients receiving full doses of mechlorethamine in cycles 3 and 5, the cycles that follow ABVD (72 percent and 70 percent, respectively), than in the comparable cycles in the MOPP group (50 percent and 37 percent). In the MOPP-ABVD group, however, there was a proportionally lower fraction of patients receiving full doses of doxorubicin in cycles 2, 4, and 6, the cycles after MOPP (56 percent, 55 percent, and 51 percent), than in equivalent cycles in the ABVD group (88 percent, 83 percent, and 83 percent).Results of Crossover after Failure of MOPP or ABVD
Eighty-one patients were switched to the alternative regimen, 51 of them because they did not have a complete response after six cycles or because their disease progressed during therapy (63 percent), with the remaining 30 patients (37 percent) having had a relapse after a complete response. Among the latter, only 10 patients had relapses after complete responses that had lasted more than one year. The overall rate of complete response with the second regimen was 46 percent (37 of 81); it was 35 percent (17 of 48) among those whose first regimen was MOPP. There was a significantly higher rate of complete response (61 percent, or 20 of 33) among those whose first regimen was ABVD (P = 0.025). Failure-free survival from the time of a crossover to ABVD was 15 percent at five years, as compared with 31 percent for a crossover to MOPP (P = 0.045) (Fig. 4Figure 4
Failure-free Survival after a Crossover from MOPP to ABVD (M→A) or Vice Versa (A→M) after Failure of the Initial Therapy Regimen.). The overall survival of the patients who had second-line treatment was 61 percent at three years and 40 percent at five years, with no differences related to the identity of the second-line treatment.Discussion
This trial demonstrated superiority for ABVD and MOPP—ABVD over MOPP alone in achieving complete remission and failure-free survival. The overall differences in failure-free survival appear to be confined to the effect of ABVD and MOPP-ABVD on the subgroup of patients with a poor prognosis. ABVD alone was as effective as MOPP in low-risk patients, but with less myelotoxicity. The fact that there are as yet no significant differences in overall survival reflects the generally long natural history of Hodgkin's disease in a substantial fraction of patients, even in relapse, and the salutary effect of second-line and even third-line chemotherapy. Alternatively, the differences in failure-free survival, though statistically significant, may not be great enough for a difference in survival, if any exists, to be detected without an even longer follow-up period.
The therapeutic advantage of ABVD was probably achieved, at least in part, because doxorubicin could be delivered in full doses throughout the first six cycles. This was not the case for MOPP. The dose of vincristine in MOPP in this trial was set so that it would not exceed 2.0 mg for each cycle. In a recently published long-term follow-up analysis of the data from the National Cancer Institute, relatively higher doses of vincristine were given, since no maximal dose of vincristine was mandated.2 The five-year survival of the MOPP-treated patients in this trial is equivalent to those in all recently published series, including that of the National Cancer Institute.3 , 4 , 25 , 26
More recently, encouraging results with a hybrid regimen have led to the use of a program that entails fusing the treatment given on day 1 of the MOPP program with daily procarbazine treatment, reduced to seven days, and includes the use of doxorubicin (35 mg per square meter), vinblastine (6 mg per square meter), and bleomycin (10 mg per square meter) on day 8 of each cycle.27 The initial encouraging results led to a prospective trial comparing the hybrid regimen with MOPP alone for six to eight cycles, followed by three cycles of ABVD. Radiation therapy was given to sites larger than 5 cm in diameter at the start of therapy. A preliminary report described an early advantage for the hybrid regimen over the sequential use of MOPP—ABVD with respect to both survival and freedom from progression.28 Another trial has shown an advantage for MOPP—ABVD over a variant of MOPP, BCVPP (carmustine, cyclophosphamide, vincristine, procarbazine, and prednisone), with respect to both failure-free survival (61 percent vs. 48 percent, P = 0.06) and overall survival (75 percent vs. 65 percent, P = 0.05).25 An additional trial showed a similar advantage in failure-free survival for MOPP—ABVD over MOPP alone.26
Our trial illustrates the long time required for comparative therapeutic trials in Hodgkin's disease when groups of patients are matched with respect to prognostic factors, such as age and stage. The small differences in survival, if any, that are likely to be achieved require for their demonstration that large numbers of patients be followed for more than five years.
The data from this trial suggest that ABVD can be effectively substituted for MOPP and MOPP—ABVD in almost all patients with advanced Hodgkin's disease. The advantages of ABVD as compared with MOPP are its antitumor effect, accompanied by less acute and chronic myelotoxicity, in patients with a good prognosis and its superior performance with regard to failure-free survival in patients with a poor prognosis.
Supported by grants from the National Cancer Institute to the Cancer and Leukemia Group B at Dartmouth-Hitchcock Medical Center and its participating institutions (CA 31946).
*Deceased.
We are indebted to Ms. Barbara Santamauro of Frontier Science and Technology Research Foundation, Amherst, N.Y., and to Dr. Maurice Barcos, Department of Pathology, Roswell Park Memorial Institute, Buffalo, N.Y., for their contributions; to Dr. Gina Petroni, Duke University, for additional statistical support; to Dr. Raymond B. Weiss, Walter Reed Army Hospital, Washington, D.C.; to Dr. Karen Antman, who participated in the early phase of this trial; and to Dr. Emil Frei III for his continuous support.
The following Cancer and Leukemia Group B institutions also participated in this study: University of Chicago, Central Massachusetts Oncology Group, Columbia–Presbyterian Medical Center, Dartmouth—Hitchcock Medical Center, Long Island Jewish Hospital, Massachusetts General Hospital, University of Missouri at Columbia, Mount Sinai Hospital (New York), New York Hospital, Rhode Island Hospital, University of Tennessee, University of Maryland Cancer Center, and Walter Reed Army Medical Center.
Source Information
From the Division of Medical Oncology, Dana–Farber Cancer Institute, and the Department of Medicine, Harvard Medical School, Boston (G.P.C.); the University of Nebraska Medical Center, Omaha (J.R.A.); the Department of Biostatistics, Harvard School of Public Health, Boston (K.J.P.); the Department of Hematology, Righshospitalet, Copenhagen, Denmark (N.N.); the Department of Medicine, Bowman Gray School of Medicine, Winston-Salem, N.C. (M.R.C.); the Food and Drug Administration, Rockville, Md. (E.S.H.); the Department of Medicine, University of California at San Diego (M.R.G.); the Department of Medicine, State University of New York Health Science Center, Syracuse (A.G.); and the Department of Medicine, University of Minnesota, Minneapolis (B.A.P.). Address reprint requests to Dr. Canellos at the Dana–Farber Cancer Institute, 44 Binney St., Boston, MA 02115.
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