Original Article
Dasatinib in Imatinib-Resistant Philadelphia Chromosome–Positive Leukemias
N Engl J Med 2006; 354:2531-2541June 15, 2006
- Abstract
Background
The BCR-ABL tyrosine kinase inhibitor imatinib is effective in Philadelphia chromosome–positive (Ph-positive) leukemias, but relapse occurs, mainly as a result of the outgrowth of leukemic subclones with imatinib-resistant BCR-ABL mutations. We evaluated dasatinib, a BCR-ABL inhibitor that targets most imatinib-resistant BCR-ABL mutations, in patients with chronic myelogenous leukemia (CML) or Ph-positive acute lymphoblastic leukemia (ALL).
Methods
Patients with various phases of CML or with Ph-positive ALL who could not tolerate or were resistant to imatinib were enrolled in a phase 1 dose-escalation study. Dasatinib (15 to 240 mg per day) was administered orally in four-week treatment cycles, once or twice daily.
Results
A complete hematologic response was achieved in 37 of 40 patients with chronic-phase CML, and major hematologic responses were seen in 31 of 44 patients with accelerated-phase CML, CML with blast crisis, or Ph-positive ALL. In these two phases, the rates of major cytogenetic response were 45 percent and 25 percent, respectively. Responses were maintained in 95 percent of patients with chronic-phase disease and in 82 percent of patients with accelerated-phase disease, with a median follow-up more than 12 months and 5 months, respectively. Nearly all patients with lymphoid blast crisis and Ph-positive ALL had a relapse within six months. Responses occurred among all BCR-ABL genotypes, with the exception of the T315I mutation, which confers resistance to both dasatinib and imatinib in vitro. Myelosuppression was common but not dose-limiting.
Conclusions
Dasatinib induces hematologic and cytogenetic responses in patients with CML or Ph-positive ALL who cannot tolerate or are resistant to imatinib. (ClinicalTrials.gov number, NCT00064233.)
Media in This Article
Animation
Activity of the ABL kinase inhibitor dasatinib in imatinib-resistant Philadelphia chromosome–positive leukemias.
Figure 1
Kaplan–Meier Analysis of Progression-free Survival among Patients with CML or ALL Associated with Dasatinib.Article Activity
- Article
Animation
Activity of the ABL kinase inhibitor dasatinib in imatinib-resistant Philadelphia chromosome–positive leukemias.
Chronic myelogenous leukemia (CML) is associated with a chromosomal translocation that produces the Philadelphia chromosome (Ph).1 This fusion gene encodes a chimeric protein, BCR-ABL, that is associated with uncontrolled activity of the ABL tyrosine kinase and can recapitulate features of CML in laboratory models.2 Imatinib, an orally available ABL kinase inhibitor, can induce hematologic and cytogenetic remission in all stages of CML, as well as in Ph-positive acute lymphoblastic leukemia (ALL), with minimal toxicity.3,4 Imatinib is now first-line therapy for newly diagnosed CML.5
However, resistance to imatinib has become increasingly important.6,7 Furthermore, nearly all patients with chronic phase CML have persistent disease, measurable by polymerase chain reaction (PCR) and indicative of a reservoir of residual leukemia cells that may be a source of relapse.8-10 Relapse during imatinib treatment is most often caused by mutations in the kinase domain of BCR-ABL that interfere with imatinib binding.11-13
Dasatinib (BMS-354825, Bristol-Myers Squibb) is an orally available ABL kinase inhibitor that differs from imatinib in that it can bind to both the active and inactive conformations of the ABL kinase domain.14-16 Dasatinib also inhibits a distinct spectrum of kinases that overlaps with the array of kinases that imatinib inhibits.17 Since it has less stringent binding requirements than does imatinib, dasatinib has activity against many imatinib-resistant kinase domain mutations of BCR-ABL. In cell-line models, dasatinib inhibited 18 of 19 imatinib-resistant BCR-ABL mutations within a narrow concentration range, similar to that required to block wild-type BCR-ABL.14,18 The only exception is a single mutation deep within the ATP-binding pocket of the ABL tyrosine kinase (T315I) that confers a high degree of resistance to imatinib and dasatinib and to the imatinib analogue AMN-107,19 presumably as a result of steric hindrance caused by replacement of threonine with the bulkier isoleucine residue.
We describe a clinical evaluation of dasatinib in a phase 1, open-label, dose-escalation study in patients with CML or Ph-positive ALL who could not tolerate or were resistant to imatinib. The ongoing study began in November 2003, and the last patient was enrolled in April 2005. The study was approved by the institutional review boards at the University of California at Los Angeles (UCLA) and the M.D. Anderson Cancer Center in Houston.
Methods
Patients and Study Design
Patients who were at least 14 years of age were eligible if they had Ph-positive chronic-phase or accelerated-phase CML or blast crisis or Ph-positive ALL and hematologic resistance or intolerance to imatinib, and all patients provided written informed consent. Chronic-phase CML was defined by the presence of less than 15 percent blasts, less than 20 percent basophils, and less than 30 percent blasts plus promyelocytes in peripheral blood or bone marrow and a platelet count of at least 100,000 per cubic millimeter, with no extramedullary involvement. Blast crisis was defined by the presence of at least 30 percent blasts in peripheral blood or bone marrow or extramedullary infiltrates of leukemic cells (other than the spleen or liver). Patients were classified as having accelerated-phase disease if they did not fulfill criteria for chronic-phase disease or blast crisis but did meet any of the following criteria: the presence of at least 15 percent but less than 30 percent blasts in peripheral blood or bone marrow, the presence of at least 20 percent basophils in peripheral blood or bone marrow, the presence of at least 30 percent blasts plus promyelocytes (but less than 30 percent blasts) in peripheral blood or bone marrow, or a platelet count of less than 100,000 per cubic millimeter unrelated to therapy. Patients with accelerated-phase disease or blast crisis who had met the criteria for chronic-phase disease at the time of entry were enrolled as having chronic-phase CML. Patients with Ph-positive ALL had at least 30 percent lymphoblasts in peripheral blood or bone marrow without previous evidence of chronic-phase CML.
Hematologic resistance to imatinib was classified as primary (a lack of adequate response) or acquired (a relapse after an initial response), as detailed in Table 1 of the Supplementary Appendix (available with the full text of this article at www.nejm.org). Patients with cytogenetic or molecular resistance, but without hematologic resistance, to imatinib were not eligible. Patients were considered to be unable to tolerate imatinib if they had discontinued imatinib treatment as a result of nonhematologic toxic effects of any grade.
The primary objective of this study was to define the tolerability and safety of dasatinib. Secondary end points were the determination of pharmacokinetic properties and antileukemic activity of dasatinib and the examination of potential correlates of clinical response to the BCR-ABL genotype. Initially, dasatinib was administered only to patients with chronic-phase disease on a once-daily schedule for five consecutive days, followed by two days without treatment (a regimen of five days “on” and two days “off”) every week. The study protocol permitted progression to the administration of continuous daily doses of dasatinib and dose escalation. After obtaining pharmacokinetic data on the initial chronic-phase cohorts, we amended the protocol to include twice-daily administration of dasatinib for patients following the regimen of five days on and two days off and the regimen of continuous daily doses. After clinical activity was observed in chronic-phase CML, the protocol was amended to include patients with the other phases of CML or with Ph-positive ALL, all of whom were treated twice daily.
Assessment of Toxic Effects and Response
Patients were seen weekly for the first 12 weeks, monthly for the next 12 weeks, and then every 3 months. Complete and differential blood counts were obtained twice weekly for the first 12 weeks, every 2 weeks for 12 weeks, and every 6 weeks thereafter. Morphologic and cytogenetic analyses of bone marrow were performed every three months or more frequently in patients with accelerated-phase CML, CML with blast crisis, or Ph-positive ALL if such analysis was clinically indicated. Adverse events were evaluated throughout the study and graded according to the National Cancer Institute's Common Terminology Criteria for Adverse Events, version 3.0.20
In patients with chronic-phase disease, hematologic responses were scored as either a complete response or no response (Table 2 of the Supplementary Appendix). A complete response was defined by a white-cell count of no more than the upper limit of normal; a platelet count of less than 450,000 per cubic millimeter; the absence of blasts or promyelocytes in peripheral blood; the presence of less than 5 percent myelocytes plus metamyelocytes in peripheral blood; and the absence of extramedullary involvement (including a normal-size liver and spleen on physical examination). Progressive disease was defined as a progression to accelerated-phase disease or blast crisis or an inability to maintain a complete response even with dose escalation.
In patients with accelerated-phase disease, CML with blast crisis, or Ph-positive ALL, hematologic responses were scored as a major response (<5 percent blasts), a minor response, or no response (Table 2 of the Supplementary Appendix). Two subgroups were included in a major hematologic response: no evidence of leukemia and complete hematologic response, on the basis of whether full recovery of blood counts was achieved. Confirmed responses were those that persisted for four weeks. Any patient with a major or minor response who subsequently did not meet these criteria during a two-week period was considered to have progressive disease. The disease of patients with accelerated-phase CML was considered to have progressed if blast crisis developed. The disease of patients with blast crisis or Ph-positive ALL was considered to have progressed if the number of blasts in peripheral blood or bone marrow increased despite at least four weeks of treatment. Cytogenetic responses were defined as follows, on the basis of the percentage of Ph-positive cells in metaphase in bone marrow: complete response, 0; partial response, 1 to 35 percent; minor response, 36 to 65 percent; minimal response, 66 to 95 percent; and no response, 96 to 100 percent. The rate of major cytogenetic response included patients with complete or partial cytogenetic response.
Analysis of Mutational Status
Blood samples were collected from all patients for analysis of BCR-ABL mutations at baseline, and sequencing of the BCR-ABL kinase domain was conducted at a central laboratory, as described previously.12 Approximately 1500 nucleotides spanning the BCR-ABL catalytic domain were sequenced, with the use of BCR-ABL complementary DNA (cDNA) amplified by reverse-transcriptase PCR (RT-PCR) from peripheral blood as a template. At least 10 independent BCR-ABL clones were sequenced from each patient.
Study Responsibilities
The study was designed by academic investigators and a representative of the sponsor, Bristol-Myers Squibb. Data were collected at UCLA and at the M.D. Anderson Cancer Center under the supervision of academic investigators and then were analyzed at Bristol-Myers Squibb by company representatives and by Drs. Sawyers and Talpaz; the latter academic investigators vouch for the accuracy and completeness of the data analysis.
Results
Patients
A total of 84 patients were enrolled in the study: 40 with chronic-phase CML, 11 with accelerated-phase CML, 23 with myeloid blast crisis, and 10 with lymphoid blast crisis or Ph-positive ALL (Table 1Table 1
Baseline Characteristics of the Patients.). Of these 84 patients, 50 (60 percent) had received previous chemotherapy (excluding hydroxyurea) and 12 (14 percent) had undergone bone marrow or stem-cell transplantation. Seventy-two patients (86 percent) were resistant to imatinib, and all but 12 had received imatinib in daily doses of 600 mg or greater. Twelve patients (14 percent) could not tolerate imatinib because of abnormal liver-function tests, rash, bone pain, fatigue, or depression. Mutations in the BCR-ABL kinase domain were detected in 60 patients (71 percent) (more detail is available in Tables 3 and 4 of the Supplementary Appendix).Toxic Effects
Grade 3 or 4 neutropenia occurred in 45 percent of patients with chronic-phase disease and in 89 percent of patients with accelerated-phase disease, CML with blast crisis, or Ph-positive ALL (Table 2Table 2
Highest Grade of Adverse Hematologic and Nonhematologic Events during the Study.). Among the patients with accelerated-phase CML, CML with blast crisis, or Ph-positive ALL, 55 percent had grade 3 or 4 myelosuppression at the start of the study, as is typical in this population of patients (Table 5 of the Supplementary Appendix). Grade 3 or 4 thrombocytopenia occurred in 35 percent of patients with chronic-phase disease and in 80 percent of patients with accelerated-phase disease, CML with blast crisis, or Ph-positive ALL. Myelosuppression required the interruption of treatment in about 60 percent of patients and generally resolved within three months, often in association with a cytogenetic response. Twenty-five percent of patients required a reduction in the dose of dasatinib (Table 6 of the Supplementary Appendix).Fifteen patients had pleural effusions that could not be attributed to known causes and were therefore deemed to be treatment-related. The effusions were managed with diuretics, thoracentesis, or pleurodesis. Other adverse events were grade 1 or 2 diarrhea (23 percent), peripheral edema (19 percent), and headache (10 percent). In seven patients, grade 3 or 4 abnormalities in liver-function tests developed, but these effects resolved within two to three weeks without a modification in the dose. Grade 1 or 2 hypocalcemia was noted in about 60 percent of patients but was asymptomatic and did not worsen with continued therapy (Table 7 of the Supplementary Appendix). A maximum tolerated dose was not determined, and no patient withdrew from the study as a result of toxic effects. Patients who entered the study as a result of imatinib intolerance did not have similar complications with dasatinib.
Hematologic and Cytogenetic Responses
The rates of complete hematologic response and major cytogenetic response in the 40 patients with chronic-phase CML were 92 percent and 45 percent, respectively (Table 3Table 3
Treatment Response.). Most of the complete hematologic responses occurred at doses of dasatinib of 50 mg per day or more, whereas most cytogenetic responses required higher doses (Table 8 of the Supplementary Appendix). A cytogenetic response was more common in patients with chronic-phase disease who had had a previous cytogenetic response while receiving imatinib. Of 16 patients who had had a previous major cytogenetic response while receiving imatinib, 13 had a major cytogenetic response while receiving dasatinib. However, of 18 patients who had had no cytogenetic response while receiving imatinib, 5 had a cytogenetic response while receiving dasatinib, and 9 patients who had had only minor or partial responses while receiving imatinib had a complete cytogenetic response while receiving dasatinib. The rates of hematologic and cytogenetic response among patients who were treated with the once-daily regimen were similar to the rates among those treated twice daily.The rate of major hematologic response in patients with CML in the accelerated or blast phase or those with Ph-positive ALL was 70 percent. These responses were confirmed after four weeks in 6 of 9 patients with accelerated-phase disease, 7 of 14 patients with myeloid blast crisis, and 5 of 8 patients with either lymphoid blast crisis or Ph-positive ALL. Major cytogenetic responses were observed in all three groups of patients with accelerated-phase disease (Table 3).
In patients with chronic-phase or accelerated-phase CML, responses were maintained after 2 to 19 months of follow-up (Figure 1Figure 1
Kaplan–Meier Analysis of Progression-free Survival among Patients with CML or ALL Associated with Dasatinib.). All patients with chronic-phase or accelerated-phase disease who had a complete or major hematologic response remain in the study, with the exception of one patient with chronic-phase disease who chose to withdraw from the study to undergo allogeneic marrow transplantation when a donor became available. In contrast, responses in patients with CML with myeloid or lymphoid blast crisis or with Ph-positive ALL were generally short-lived. Despite the high rate of major hematologic response, all but one of the patients with lymphoid blast crisis or Ph-positive ALL had a relapse after a median follow-up of four months (range, one to eight). In a similar manner, only 6 of 14 patients (43 percent) with CML with myeloid blast crisis who had a major hematologic response are still participating in the study, with follow-up ranging from 5 to 12 months. However, three of these patients have sustained complete cytogenetic remission at 10, 11, and 12 months each.Clinical Response and BCR-ABL Genotype
Of 84 study patients, 60 (71 percent) had BCR-ABL mutations detected at baseline (Figure 2BFigure 2
Correlation of the BCR-ABL Genotype with Hematologic and Cytogenetic Responses.). The BCR-ABL mutations in 56 of these 60 patients had been reported previously in association with imatinib resistance, but 4 patients had new BCR-ABL mutations identified within the kinase domain (Tables 3 and 4 of the Supplementary Appendix). The contribution of these mutations to imatinib resistance will need to be assessed in vitro and confirmed in other clinical isolates.Hematologic and cytogenetic responses were observed broadly across all BCR-ABL genotypes, with the exception of T315I, the single mutation predicted to confer cross-resistance to dasatinib and imatinib in preclinical studies.14,18 In two patients who did not have a response to treatment, this mutation was the dominant pretreatment genotype and was one of four distinct imatinib-resistant subclones detected at baseline in a third patient, who did not have a response. This case is of particular interest because the three clones expressing BCR-ABL alleles F359V, M244V, and G250E, all of which were predicted to retain sensitivity to dasatinib on the basis of preclinical studies, were gradually extinguished during 60 days of treatment (Figure 2C). In contrast, the T315I clone, which initially represented a minor fraction of the imatinib-resistant population, expanded during therapy and was the only clone detected at clinical relapse. A fourth patient also had disease progression with T315I, but the mutation was not detected among the 10 clones sequenced before dasatinib treatment.
Discussion
Imatinib can produce durable cytogenetic remission with minimal toxic effects in most cases of chronic-phase CML.5 Yet additional therapies are clearly needed to address the growing problem of relapse. A detailed understanding of the molecular basis of imatinib resistance, primarily as a result of mutations in the BCR-ABL gene, led to the evaluation of dasatinib. Some imatinib-resistance mutations encode amino acid substitutions in the BCR-ABL kinase domain at residues that directly contact imatinib. More common are mutations that alter the flexibility of the BCR-ABL kinase domain and destabilize the specific inactive conformation to which imatinib binds.21 Dasatinib binds to the ABL kinase domain in a manner distinct from that of imatinib and thereby retains activity against nearly all imatinib-resistance mutations (Figure 2A). In addition to point mutations, amplification of the BCR-ABL gene is associated with imatinib-related relapse in advanced-phase CML.11 BCR-ABL–independent pathways have also been implicated in some cases.22,23
Our results demonstrate that dasatinib has clinical activity in all stages of imatinib-resistant CML and Ph-positive ALL, including resistance caused by BCR-ABL gene mutation. Furthermore, the correlation of the BCR-ABL genotype with a clinical response to dasatinib mirrors predictions from preclinical findings, in that none of the three patients with a T315I mutation that was detected before treatment had a response to dasatinib.
In addition to the induction of remission in patients with a broad range of imatinib-resistant BCR-ABL mutations, dasatinib had activity in patients who had received little or no cytogenetic benefit from imatinib. The ability of dasatinib to induce cytogenetic responses in patients with imatinib resistance raises the possibility of clinical benefit in other patients with CML who have a suboptimal response to imatinib (i.e., residual Ph-positive cells in the marrow) but who have no evidence of frank hematologic resistance to imatinib. Dasatinib may have this additional activity because it inhibits BCR-ABL kinase activity more effectively than does imatinib. Another possibility relates to the differential susceptibility of imatinib and dasatinib to drug efflux pumps, such as multidrug resistance protein 1 (P-glycoprotein), which are highly expressed in hematopoietic stem cells. Imatinib is a substrate of P-glycoprotein, whereas dasatinib is not. Dasatinib may therefore achieve a higher intracellular concentration than imatinib. A third possibility is that the many additional kinases that are targeted by dasatinib contribute to a cytogenetic response.
The major adverse effect of dasatinib was reversible myelosuppression. We cannot tell whether the myelosuppression was solely the result of the action of dasatinib against Ph-positive leukemia cells or of a more general hematopoietic toxic effect. Myelosuppression typically resolved in patients who had a cytogenetic remission and has not been a complication of dasatinib treatment in patients with solid tumors,24 but further studies are needed to clarify the nature of dasatinib-associated myelosuppression. Nonmalignant pleural effusions developed in 15 patients, often in the absence of edema, whereas the common imatinib-related side effect of periorbital edema was less frequent. Other frequent imatinib-associated side effects, such as muscle cramps and nausea, were rarely observed. An important finding is that patients who could not tolerate imatinib and were treated with dasatinib did not have a recurrence of nonhematologic toxic effects (e.g., liver-function abnormalities and rash) that were associated with imatinib.
The rationale underlying the use of dasatinib for imatinib-resistant CML may have implications for other kinase-dependent cancers. Kinase-domain mutations, which were initially discovered as a resistance mechanism in CML, have been described in lung cancer, gastrointestinal stromal tumor, and the hypereosinophilic syndrome with resistance to kinase inhibitors.25-29 The activity of dasatinib in cases of CML with imatinib resistance is likely the result of the drug's less stringent conformational binding requirements relative to imatinib and suggests a general approach in which kinase-dependent cancers are treated with a combination of inhibitors that differ in their kinase-binding properties.
Although the clinical results reported here support the use of dasatinib as single-agent therapy for imatinib-resistant CML and Ph-positive ALL, acquired resistance to dasatinib may be the eventual outcome, as already observed in many of the patients with blast crisis and Ph-positive ALL who were treated in this trial. Preclinical studies have identified several BCR-ABL mutations that confer resistance to dasatinib but not to imatinib, providing a rationale to explore combination therapy as initial treatment for CML.30 For these reasons, successful long-term treatment of CML may require a cocktail of kinase inhibitors with activity against all drug-resistant BCR-ABL mutations (including T315I), analogous to the success of highly active antiretroviral therapy in the treatment of infection with the human immunodeficiency virus. Elsewhere in this issue of the Journal, Kantarjian et al.31 report that the kinase inhibitor nilotinib has a relatively favorable safety profile and is active in imatinib-resistant CML.
Supported by grants from the Leukemia and Lymphoma Society and a grant (MO1-RR-00865) from the General Clinical Research Centers of the National Institutes of Health. Dr. Shah is the recipient of a Career Development Award for Special Fellows from the Leukemia and Lymphoma Society. Dr. Sawyers is an investigator at the Howard Hughes Medical Institute and is the recipient of a Doris Duke Distinguished Clinical Scientist Award.
Drs. Talpaz, Kantarjian, and Cortes report having received research support from Bristol-Myers Squibb. Drs. Shah, Nicoll, and Sawyers report being coinventors on a patent filed by UCLA on the use of mutations in the BCR-ABL kinase domain for diagnostic or therapeutic purposes. Drs. Nicaise, Bleickardt, Blackwood-Chirchir, and Huang and Ms. Iyer and Ms. Chen are employees of Bristol-Myers Squibb. Dr. Decillis was formerly an employee of Bristol-Myers Squibb and is currently an employee of Novartis Pharmaceuticals. No other potential conflict of interest relevant to this article was reported.
Drs. Talpaz and Sawyers contributed equally to this article.
We are indebted to Elisabeth Haddad, Bojidar (Bobby) Grozdev, Shela Broussard, Mary Carroll, Chris Lacke, Barbara van Leeuwen, Doreen Tuozzoli, and Maria Grasic for their assistance with clinical trial coordination; to John Tokarski and Francis Lee for their assistance in the preparation of the crystallographic figure; and to Ingo Mellinghoff for comments on the manuscript.
Source Information
From the Departments of Leukemia (M.T., H.K., J.C., S.O.) and Experimental Therapeutics (M.T., N.D.), M.D. Anderson Cancer Center, Houston; Jonsson Comprehensive Cancer Center, University of California at Los Angeles, Los Angeles (N.P.S., J.N., R.P., C.L.S.); Bristol-Myers Squibb, Wallingford, Conn. (C.N., E.B., V.I., T.-T.C., A.P.D.), and Lawrenceville, N.J. (M.A.B.-C., F.H.); and Howard Hughes Medical Institute, Chevy Chase, Md. (C.L.S.).
Address reprint requests to Dr. Sawyers at Jonsson Comprehensive Cancer Center, University of California at Los Angeles, 11-934 Factor Bldg., 10833 LeConte Ave., Los Angeles, CA 90095, or at csawyers@mednet.ucla.edu.
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