Original Article
Induction of Graft-versus-Host Disease as Immunotherapy for Relapsed Chronic Myeloid Leukemia
N Engl J Med 1994; 330:100-106January 13, 1994
- Abstract
Background
The ability of allogeneic bone marrow transplantation to cure chronic myeloid leukemia (CML) is due to both the conditioning regimen and the antileukemic effects of the lymphocytes in the grafted marrow. We studied the ability of interferon alfa-2b and infusions of mononuclear cells from the marrow donor to induce a graft-versus-leukemia reaction in patients with CML in relapse after bone marrow transplantation.
Methods
Eleven patients with relapsed CML after allogeneic bone marrow transplantation were treated with interferon alfa-2b and infusions of mononuclear cells. The patients were monitored for toxic effects, for hematologic and cytogenetic responses, and, with use of the polymerase chain reaction, for elimination of cells containing the bcr/abl messenger RNA transcript characteristic of the leukemic cells.
Results
Six of the eight patients with stable CML after relapse had complete remissions according to molecular genetic criteria, since no cells with bcr/abl messenger RNA transcripts were detected (the method can identify 1 leukemic cell among 1 million normal cells). The three patients with accelerated CML after relapse did not enter remission. Myelosuppression was prominent in eight patients. Grade I acute graft-versus-host disease (GVHD) occurred in six patients, and grade III acute GVHD occurred in three. Limited chronic GVHD developed in five patients.
Conclusions
The induction of a graft-versus-leukemia reaction with interferon alfa-2b and infusions of donor mononuclear cells in patients with CML in relapse after bone marrow transplantation is an effective antileukemic therapy that may offer an alternative to a second marrow transplantation.
Media in This Article
Figure 1
Treatment Protocol.Figure 2
Progressive Disappearance of Recipient's Cells after Infusions of Donor Mononuclear Cells.Article Activity
- Article
Allogeneic bone marrow transplantation cures over 50 percent of patients with chronic myeloid leukemia (CML) when performed during the chronic phase of the disease1,2. This response is related to both the conditioning regimen and the graft-versus-leukemia effect (the immune potential of the donor graft to react against the patient's leukemic cells). The success of allogeneic transplantation is limited in part by graft-versus-host disease (GVHD) and by the relapse of CML. Relapses can be cured with a second transplantation, but with increased regimen-related morbidity and poor survival rates3. A safer, more effective approach is clearly desirable. One such approach is the induction of a graft-versus-leukemia reaction without a second transplantation.
Graft-versus-leukemia effects have been demonstrated in animal models of transplantation,4,5 but evidence of their importance in clinical transplantation is indirect. For instance, the development of GVHD after transplantation is associated with protection against relapse2,6,7. In addition, in patients with CML, bone marrow grafts depleted of T cells result in a low incidence of GVHD but a relapse rate of 30 to 50 percent, as compared with a rate of 10 to 20 percent for unmodified bone marrow grafts1,2,6,8.
A graft-versus-leukemia reaction has been induced in patients with recurrent CML after bone marrow transplantation. Kolb et al. induced cytogenetic remissions in three patients with relapsed CML by administering interferon-alfa and mononuclear cells obtained from the original marrow donor9. Cytogenetic analysis is useful when approximately 1 in 30 cells contains the characteristic chromosomal translocation of CML (the Philadelphia chromosome [Ph1]). In this translocation, the abl proto-oncogene is translocated from chromosome 9 to chromosome 22 adjacent to the bcr gene. The polymerase chain reaction (PCR) is a far more sensitive method of detecting this translocation than is cytogenetic analysis; by amplifying transcripts of the chimeric bcr/abl gene, a single leukemic cell among 1 million normal cells can be identified10. Importantly, the detection of bcr/abl transcripts after transplantation correlates with an increased risk of relapse10. In case reports from other groups, the antileukemic effect of mononuclear-cell infusions was confirmed in three patients by PCR11,12. On the basis of these studies, we administered interferon alfa-2b and donor mononuclear cells to 11 patients with recurrent CML to induce a graft-versus-leukemia reaction, using serial tests for the bcr/abl transcripts to monitor the patients.
Methods
Patients' Characteristics
We studied 11 consecutive patients with CML in relapse after allogeneic bone marrow transplantation. All patients had a hematologic relapse requiring cytoreductive therapy. No patient required immunosuppression for chronic GVHD, and all the patients had an Eastern Cooperative Oncology Group performance status of 0 (a score of 0 indicates no symptoms, and a score of 4 severe disability). The study was approved by the Human Research Committee of Brigham and Women's Hospital, and written informed consent was obtained from all patients and donors.
The characteristics of the patients are shown in Table 1Table 1
Characteristics of the Patients.. All had undergone allogeneic transplantation of bone marrow obtained from an HLA-identical sibling for chronic CML. For prophylaxis against GVHD at the time of transplantation, nine patients received marrow grafts depleted of T cells13-15 and two patients received cyclosporine and methotrexate16. The median length of time from transplantation to relapse was 13 months (range, 6 to 44), and the median time from relapse to the first infusion of mononuclear cells was 22 months (range, 10 to 56) (Table 1). The grade of GVHD after initial transplantation is shown in Table 2Table 2
Extent of Acute and Chronic GVHD in 11 Patients with CML after Treatment with Interferon Alfa-2b and Mononuclear-Cell Infusions..CML was classified as being in a stable phase, an accelerated phase, or a blast crisis according to the criteria of the International Bone Marrow Transplant Registry,17 except that the disease in patients with complex chromosomal abnormalities was not classified as being in an accelerated phase unless other criteria were also met. Eight patients had stable CML, and three had accelerated CML. One patient (Patient 11) with accelerated CML had a blast crisis during therapy and withdrew from the study after two infusions of mononuclear cells to receive chemotherapy.
Interferon Therapy
The treatment protocol is shown in Figure 1Figure 1
Treatment Protocol.. The patients were taught to inject themselves with interferon alfa-2b (Intron A, Schering-Plough, Kenilworth, N.J.). The projected daily dose was 5 million units per square meter of body-surface area subcutaneously, although treatment was usually started at a lower dose and titrated according to the patient's tolerance and hematologic response. Reasons for reductions in the dose included the occurrence of severe influenza-like symptoms, depression, and a white-cell count below 4000 per cubic millimeter or a platelet count below 100,000 per cubic millimeter. Interferon alfa-2b alone controlled peripheral-blood counts in 10 patients; 1 patient required hydroxyurea in addition to interferon alfa-2b. Patients received interferon alfa-2b for 6 to 12 weeks before the first infusion of cells. Treatment with interferon alfa-2b was continued throughout the infusions and for four weeks after the final infusion.Infusions of Mononuclear Cells
Nine patients received four weekly infusions of mononuclear cells freshly obtained from the original bone marrow donor by leukapheresis (Figure 1). One patient (Patient 8) received only one infusion because of venous-access difficulties in the donor, and one patient (Patient 11) withdrew from the study, as noted above. The leukapheresis was carried out with a Cobe Spectra apheresis system (Cobe Laboratories, Lakewood, Colo.); the total dose of cells infused per patient is shown in Table 1.
Evaluation of Patient Response
The patients were evaluated at least weekly for evidence of GVHD, complete blood counts and differential counts were obtained, and serum electrolyte and liver-enzyme concentrations were measured. Bone marrow was obtained from most patients two weeks before the first infusion and two to eight weeks after the final infusion for evaluation of responses according to morphologic, cytogenetic, and molecular genetic criteria.
Acute GVHD was graded on a four-point scale (on which I indicates mild disease, and IV severe disease), and chronic GVHD was classified as limited or extensive, as previously described18,19. Skin or liver biopsies were performed when indicated for confirmation of GVHD. All patients with acute GVHD were initially treated with oral prednisone (1 to 3 mg per kilogram of body weight per day), with additional therapy given at the discretion of the investigators.
Definition of Remission and Statistical Analysis
The results are presented as of June 30, 1993. Hematologic remission was defined as the return of normal blood counts and bone marrow cellularity in the absence of antileukemic therapy. Several patients with mild, stable anemia or thrombocytopenia were considered to be in hematologic remission. Cytogenetic remission was considered to be present when all bone marrow metaphases were normal. (Cytogenetic analysis was performed by the cytogenetics laboratory at the Dana-Farber Cancer Institute, Boston.) Molecular genetic remission was defined as the inability to detect bcr/abl messenger RNA (mRNA) transcripts by PCR, as described below. The cumulative probability of entering molecular genetic remission was calculated according to the method of Kaplan and Meier,20 and the relation between the amount of cells infused and remission was evaluated with Student's t-test.
Molecular Genetic Analysis
Analysis of bcr/abl Transcripts
Peripheral-blood granulocytes, mononuclear cells, or bone marrow cells were obtained at various times after the infusion of mononuclear cells, and RNA was prepared as previously described10. RNA PCR was performed with an abl-sequence-specific reverse transcriptase primer followed by PCR amplification with abl- and bcr-specific primers10. Second-round PCR (35 cycles per round) with nested internal bcr and abl primers was performed on all samples, and amplification of the bcr/abl transcript was detected by visualization on ethidium bromide-stained agarose gels. Studies have shown that this method can detect 1 leukemic cell per 1 million normal cells10. The presence of intact RNA and the adequacy of the synthesis of complementary DNA were evaluated by single-round PCR with abl-sequence-specific PCR primers10. Mock RNA preparations were run as negative controls.
Analysis of Engraftment by PCR
Blood from Patients 2 and 3 was obtained before the mononuclear-cell infusions, and cells were separated by Ficoll-Hypaque centrifugation into layers of mononuclear cells and granulocytes. Aliquots of DNA (10 microliters) prepared from both cell fractions were used for amplification by PCR and engraftment analysis21,22. Patient DNA and donor DNA were screened for distinguishing polymorphisms with a series of PCR primers flanking known polymorphic regions22. Primers for the parathyroid hormone (PTH) gene23 identified a polymorphism in the host DNA but not in donor DNA (Figure 2Figure 2
Progressive Disappearance of Recipient's Cells after Infusions of Donor Mononuclear Cells.). After therapy, blood or bone marrow samples were obtained at various times. The DNA was amplified with PTH-specific primers, and the products were analyzed22. The host-specific allele was quantitated by hybridization with an oligonucleotide specific for the recipient allele, the probe was removed, and the sample was rehybridized with an internal oligonucleotide consisting of an invariable PTH sequence.Results
Response to Interferon Alfa-2b
Hematologic control of CML was achieved with interferon alfa-2b in 10 of the 11 patients. However, no patient had a cytogenetic or molecular genetic remission before the infusion of donor mononuclear cells. After 4 to 10 weeks of therapy with interferon alfa-2b, marrow biopsies showed hypercellularity (cellularity, 80 to >95 percent), with 74 to 100 percent of metaphases containing the Ph1 chromosome in all nine patients from whom we could aspirate marrow (eight patients had other complex karyotypic abnormalities). In the other two patients, cytogenetic studies of peripheral blood revealed Ph1-positive cells. We detected bcr/abl mRNA transcripts in the marrow or blood of all nine patients evaluated.
Hematologic Response to Interferon Alfa-2b and Mononuclear-Cell Infusions
The eight patients with stable CML had complete hematologic responses. After interferon alfa-2b was discontinued, the blood counts remained stable in these patients without the need for further treatment with interferon alfa-2b, hydroxyurea, or other types of cytoreductive therapy. Five patients had transient absolute granulocyte counts below 500 per cubic millimeter. In the patients who responded, the decline in peripheral-blood counts coincided with the development of clinically evident acute GVHD (Figure 3Figure 3
White-Cell Response in Two Patients with CML in Relapse after Infusions of Donor Mononuclear Cells.). A bone marrow evaluation two to eight weeks after the final infusion in six patients who responded showed a decrease in cellularity to 5 to 30 percent. One patient (Patient 5) died of aspergillus infection after grade III acute GVHD and profound pancytopenia developed. Bone marrow aplasia developed in a second patient (Patient 3). Quantitative analysis of peripheral blood from this patient immediately before the first infusion of mononuclear cells demonstrated residual production of donor granulocytes and mononuclear cells (Figure 2). Although more than 99 percent of hematopoiesis was of donor origin by day 115 (Figure 2), the patient's bone marrow remained hypocellular (95 percent fat), and she was dependent on platelet and red-cell transfusions. Hematopoietic recovery did not occur until donor bone marrow was administered on day 181; she was in complete remission after 558 days of follow-up (Figure 3).Cytogenetic and Molecular Genetic Responses
Six of the eight patients who had a hematologic response had a complete cytogenetic remission according to blood and bone marrow analyses and a complete molecular genetic remission as documented by the absence of detectable bcr/abl mRNA transcripts. The actuarial probability of entering a complete molecular genetic remission was 69 percent after a median follow-up of 355 days (range, 50 to 709) (Figure 4Figure 4
Actuarial Probability of Entering Molecular Genetic Remission.). The median length of time until bcr/abl transcripts were undetectable was 57 days (range, 42 to 116) after the first infusion of mononuclear cells. None of these six patients had a molecular genetic or cytogenetic relapse during a median follow-up of 461 days (range, 260 to 709). Hematopoiesis was confirmed to be of donor origin by sex-chromosome analysis, blood-type analysis, or the demonstration of the loss of a marker chromosome. In addition, PCR analysis of engraftment in Patient 2 (data not shown) and Patient 3 (Figure 2) demonstrated that more than 99 percent of hematopoiesis was of donor origin at the time of complete remission.The three patients with accelerated CML did not enter remission. However, Patient 7 improved, and her blood counts stabilized during treatment with a lower dose of interferon alfa-2b. Patient 11 withdrew from the study after two infusions to receive chemotherapy because of progression to blast crisis. Grade I acute GVHD developed in Patient 4, but she had no hematologic response and died of complications of blast crisis and sepsis 50 days after the first infusion.
Toxicity
Acute GVHD
Acute GVHD developed in nine patients a median of 32 days (range, 22 to 87) after the first infusion (Table 2). The number of infusions was not reduced in any patient as a result of acute GVHD, although grade I acute GVHD developed after only a single infusion in one patient who responded (Patient 8) (additional infusions could not be given because of venous-access difficulties in the donor). Six patients had grade I acute GVHD, and three patients grade III. All were initially treated with corticosteroids; three patients required additional treatment with cyclosporine, and one patient required additional treatment with azathioprine. One patient (Patient 6) with grade III acute GVHD also received antithymocyte globulin and interleukin-1-receptor antagonist,24 with complete resolution of the disease. All patients with a cytogenetic or molecular genetic response had GVHD. There was no correlation between the cell dose and either the response or the severity of GVHD.
Chronic GVHD
Limited chronic GVHD developed in five of the eight patients who were followed for more than 100 days (Table 2). Chronic GVHD was manifested by a recurrent skin rash in one patient, oral mucositis in two patients, biopsy-proved chronic GVHD of the liver25 in two patients, and synovitis in one patient. Chronic GVHD was controlled with immunosuppressive therapy in all five patients.
Opportunistic Infections
Life-threatening opportunistic infections developed in three patients during treatment for GVHD. One patient had granulocytopenia and died of aspergillus sepsis. The second patient had a facial abscess due to Staphylococcus aureus and aspergillus infection of the lung and liver, and the third patient had Pneumocystis carinii pneumonia and aspergillus infection of the lung and brain.
Discussion
Allogeneic bone marrow transplantation transfers both hematopoietic stem cells and alloreactive donor lymphocytes, which produce a form of adoptive immunotherapy. The antitumor effect mediated by immunocompetent donor cells is known as the graft-versus-leukemia effect and has been well characterized in murine models of transplantation4,5. In humans, the presence of the graft-versus-leukemia reaction has been supported by indirect evidence that relapse rates are significantly higher after T-cell depletion of donor bone marrow2,6,7 or syngeneic transplantation6. The development of GVHD after transplantation is associated with lower relapse rates,2,6,7 and patients with a relapse of leukemia may enter remission when GVHD follows the withdrawal of immunosuppression26.
The responses in this trial provide evidence of a graft-versus-leukemia reaction in humans with CML in relapse after bone marrow transplantation and extend prior observations that infusions of donor mononuclear cells are effective therapy for relapsed CML9,11,12. Follow-up data are still limited, but six of the eight patients with stable CML in relapse who were treated have had sustained molecular genetic remissions, and none have had another relapse. These results are encouraging, since the inability to detect bcr/abl transcripts by PCR after transplantation correlates with relapse-free survival10. The therapy was less effective for patients with accelerated CML.
Myelosuppression and marrow hypoplasia after therapy were often dramatic and temporally related to the development of acute GVHD (Figure 3). Their occurrence can be explained by the elimination of leukemic hematopoiesis mediated by infused donor mononuclear cells before adequate donor hematopoiesis was reestablished. The lack of spontaneous recovery in Patient 3 was probably due to the presence of insufficient numbers of donor stem cells. Despite the fact that over 99 percent of the blood cells were derived from the donor, marrow hypoplasia persisted in this patient until additional bone marrow was infused, suggesting that the total number of stem cells was inadequate to sustain normal hematopoiesis. It is less likely that the infusion of donor bone marrow overcame cellular or humoral suppression of normal hematopoiesis, although this possibility cannot be excluded.
Mononuclear cells were administered without prophylactic immunosuppression 10 to 56 months after the initial transplantation. This delay may be responsible for the relatively mild GVHD that occurred despite the infusion of up to 10 times more T cells than are typically contained in unmanipulated donor bone marrow13-15. Previous attempts to augment the graft-versus-leukemia reaction with infusions of donor leukocytes in the immediate post-transplantation period resulted in more severe GVHD with no improvement in survival; this result was due at least in part to the increased mortality associated with GVHD27. GVHD may be less severe when its effects are separated from the tissue damage induced by the conditioning regimen28. Residual donor lymphocytes also may mediate immune tolerance, further limiting the severity of the GVHD reaction29.
The mechanism of the antileukemic reaction is probably cell-mediated cytotoxicity. Donor T cells are clearly important in the graft-versus-leukemia reaction,2,6,8 but other types of cells, including monocytes, natural killer cells, and hematopoietic progenitor cells, were also infused. Although cytotoxic T cells or natural killer cells may directly mediate the antileukemic reaction,30 other mononuclear cells may stimulate additional effector cells or cytokines. The target antigens of the antileukemic response are unknown but could include minor histocompatibility antigens of the host or possibly CML-specific antigens.
It is unlikely that interferon alfa-2b alone was responsible for the observed antileukemic effects. Interferon alfa-2b can induce occasional cytogenetic remissions when given as primary therapy for CML,31 but these remissions occur slowly,31 and molecular genetic remissions have not been documented32. Complete cytogenetic remissions have been obtained in a few patients with relapsed CML treated with interferon alfa-2b alone, although half ultimately relapsed again; bcr/abl transcripts were still detectable in the single patient tested33. No patient in our study had a cytogenetic remission before the infusion of mononuclear cells. However, interferon alfa-2b has antiproliferative effects and may result in cytoreduction. It may facilitate a cell-mediated antileukemic reaction directly34,35 or through the induction of additional cytokines. It can also increase the expression of major histocompatibility antigens on cells36 and restore the deficient expression of the adhesion molecule lymphocyte-function-associated antigen 3 on CML progenitor cells37. However, a similar graft-versus-leukemia reaction has been generated without the use of interferon alfa-2b in some patients11.
For patients with stable CML who have a relapse after allogeneic bone marrow transplantation, interferon alfa-2b and infusions of donor mononuclear cells can be effective antileukemic therapy. However, the durability of the remissions and the effect on survival remain to be determined. This therapy offers an alternative to a second bone marrow transplantation for patients with CML who have a relapse after allogeneic marrow transplantation.
Supported in part by grants from the National Institutes of Health (T32-HL07623 to Dr. Porter, CA39542 and CA58661 to Dr. Antin, R29DK43470-02 to Dr. Roth, and AI30018 to Dr. Ferrara) and the American Cancer Society (to Dr. Roth). Dr. Ferrara is a scholar of the Leukemia Society of America.
We are indebted to Dr. Mark A. Goldberg and Dr. Robert I. Handin for their critical review of the manuscript and many helpful suggestions.
Source Information
From the Division of Hematology-Oncology, Brigham and Women's Hospital and Harvard Medical School, Boston (D.L.P., C.M., J.L.M.F., J.H.A.), and the Division of Hematology-Oncology, University of Michigan Medical Center, Ann Arbor (M.S.R.).
Address reprint requests to Dr. Antin at the Division of Hematology-Oncology, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115.
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