Original Article
All-trans-Retinoic Acid in Acute Promyelocytic Leukemia
N Engl J Med 1997; 337:1021-1028October 9, 1997
- Abstract
Background
All-trans-retinoic acid induces complete remission in acute promyelocytic leukemia. However, it is not clear whether induction therapy with all-trans-retinoic acid is superior to chemotherapy alone or whether maintenance treatment with all-trans-retinoic acid improves outcome.
Methods
Three hundred forty-six patients with previously untreated acute promyelocytic leukemia were randomly assigned to receive all-trans-retinoic acid or daunorubicin plus cytarabine as induction treatment. Patients who had a complete remission received consolidation therapy consisting of one cycle of treatment identical to the induction chemotherapy, then high-dose cytarabine plus daunorubicin. Patients still in complete remission after two cycles of consolidation therapy were then randomly assigned to maintenance treatment with all-trans-retinoic acid or to observation.
Results
Of the 174 patients treated with chemotherapy, 120 (69 percent) had a complete remission, as did 124 of the 172 (72 percent) given all-trans-retinoic acid (P = 0.56). When both induction and maintenance treatments were taken into account, the estimated rates of disease-free survival at one, two, and three years were 77, 61, and 55 percent, respectively, for patients assigned to chemotherapy then all-trans-retinoic acid; 86, 75, and 75 percent for all-trans-retinoic acid then all-trans-retinoic acid; 75, 60, and 60 percent for all-trans-retinoic acid then observation; and 29, 18, and 18 percent for chemotherapy then observation. By intention-to-treat analysis, the rates of overall survival at one, two, and three years after entry into the study were 75, 57, and 50 percent, respectively, among patients assigned to chemotherapy, and 82, 72, and 67 percent among those assigned to all-trans-retinoic acid (P = 0.003).
Conclusions
All-trans-retinoic acid as induction or maintenance treatment improves disease-free and overall survival as compared with chemotherapy alone and should be included in the treatment of acute promyelocytic leukemia.
Media in This Article
Figure 4
Kaplan–Meier Product-Limit Estimate of Overall Survival According to Intention-to-Treat Analysis for Patients Receiving Daunorubicin plus Cytarabine or All-tran s-Retinoic Acid as Induction Therapy.Figure 1
Kaplan–Meier Product-Limit Estimate of Disease-free Survival from the Time of Complete Remission for Patients Randomly Assigned at Induction to Either Daunorubicin plus Cytarabine or All-tran s-Retinoic Acid.Article Activity
- Article
Acute promyelocytic leukemia is a distinct subtype of acute myeloid leukemia1 in which a balanced reciprocal translocation between chromosomes 15 and 17 results in the union of portions of the promyelocytic leukemia gene with the gene for retinoic acid receptor alpha.2 This chimeric gene encodes the promyelocytic leukemia–retinoic acid receptor alpha fusion protein.3-6 Although 65 to 80 percent of patients with acute promyelocytic leukemia have a complete remission with standard chemotherapy,7,8 approximately 10 to 20 percent die either before or during chemotherapy of bleeding attributable to disseminated intravascular coagulation, fibrinolysis, and proteolysis.9 All-trans-retinoic acid differentiates leukemic promyelocytes into mature cells.10,11 Phase 2 clinical trials have demonstrated that all-trans-retinoic acid induces complete remission in most patients, with rapid resolution of the coagulopathy and few deaths during induction therapy.12-19 The duration of complete remission with all-trans-retinoic acid alone is usually brief, and postremission chemotherapy is required to diminish the likelihood of relapse.12-19 This study was designed to compare the rates of complete remission, disease-free survival, overall survival, and toxic effects associated with all-trans-retinoic acid therapy with those associated with conventional chemotherapy in patients with previously untreated acute promyelocytic leukemia and to determine the value of maintenance therapy with all-trans-retinoic acid.
Methods
Eligibility Criteria
The eligibility criteria were a diagnosis of acute promyelocytic leukemia established on the basis of bone marrow morphology, no prior chemotherapy except hydroxyurea, normal hepatic and renal function, and an Eastern Cooperative Oncology Group performance status of 0 (normal activity) to 3 (in bed more than 50 percent of the time). Cytogenetic evaluation for t(15;17) was mandatory; however, the results did not affect eligibility. The diagnostic bone marrow findings were centrally reviewed within each cooperative group. The immunophenotypic and molecular analyses were performed according to the guidelines of each participating cooperative group and are not described here.
Study Design
Induction Therapy
Patients were randomly assigned to receive either 45 mg of daunorubicin per square meter of body-surface area per day by intravenous bolus on days 1 through 3, plus 100 mg of cytarabine per square meter per day by continuous intravenous infusion on days 1 through 7; or 45 mg of all-trans-retinoic acid (Vesanoid, Hoffmann–LaRoche, Nutley, N.J.) per square meter per day orally, divided into two doses given every 12 hours. Patients less than three years of age received either all-trans-retinoic acid, as described, or 1.5 mg of daunorubicin per kilogram of body weight per day by intravenous infusion on days 1 through 3, plus 3.3 mg of cytarabine per kilogram per day by continuous intravenous infusion on days 1 through 7. For patients assigned to cytotoxic chemotherapy, a second induction cycle with identical doses and schedules was given if disseminated intravascular coagulation recurred or the fibrinogen level declined and 50 percent or more of the promyelocytes in the bone marrow were abnormal after the first cycle. If the white-cell count was more than 10,000 per cubic millimeter, hydroxyurea was given before all-trans-retinoic acid. Patients received all-trans-retinoic acid until complete remission occurred, or for a maximum of 90 days. When serious toxic effects occurred, all-trans-retinoic acid was withheld until the effects diminished to a mild level and was then resumed at 75 percent of the initial dose. Patients who had unacceptable levels of toxic effects while taking all-trans-retinoic acid or who did not have a complete remission after a maximum of 90 days crossed over to chemotherapy. All-trans-retinoic acid was supplied by the National Cancer Institute. Patients who did not have a complete remission with chemotherapy received no further protocol therapy and were treated at the physician's discretion.
Consolidation Therapy
Patients who had a complete remission with chemotherapy or all-trans-retinoic acid received two cycles of consolidation therapy. The first cycle was identical to the induction chemotherapy. The second cycle consisted of high-dose cytarabine (2 g per square meter) as a 1-hour intravenous infusion every 12 hours for four consecutive days, with 45 mg of daunorubicin per square meter per day by intravenous infusion on days 1 and 2. For patients less than three years of age, the second cycle consisted of 67 mg of cytarabine per kilogram as a 1-hour intravenous infusion every 12 hours for four consecutive days, with 1.5 mg of daunorubicin per kilogram per day by intravenous infusion on days 1 and 2.
Maintenance Therapy
Patients in complete remission after both cycles of consolidation chemotherapy, irrespective of which induction therapy they had received, were randomly assigned either to a maintenance regimen of 45 mg of all-trans-retinoic acid per square meter per day given orally in divided doses every 12 hours for one year or to observation. Patients who were intolerant of induction therapy with all-trans-retinoic acid were directly assigned to observation.
Definition of Outcome
Toxic effects were graded according to the Common Toxicity Criteria of the National Cancer Institute. Complete remission and relapse were defined according to National Cancer Institute criteria.20 Patients who were in clinical complete remission that was not confirmed by bone marrow findings were considered not to have had a response. Disease-free survival was defined as the time from the beginning of complete remission to relapse, death from any cause, or censoring of the data on the patient.
Supportive Care
Coagulopathy was treated at the physician's discretion. If the white-cell count rose during therapy to more than 30,000 per cubic millimeter, all-trans-retinoic acid was stopped, hydroxyurea was given until the white-cell count decreased to 10,000 per cubic millimeter, and then all-trans-retinoic acid was resumed.
Management of Retinoic Acid Syndrome
Retinoic acid syndrome was diagnosed in patients with unexplained fever, weight gain, respiratory distress, interstitial pulmonary infiltrates, and pleural or pericardial effusions.21 All-trans-retinoic acid was discontinued at the earliest signs of the syndrome, and dexamethasone was instituted (10 mg twice daily) for at least three days. After resolution of the symptoms, all-trans-retinoic acid was resumed at 75 percent of the initial dose. If there was no recurrence, the dose of all-trans-retinoic acid was increased to the initial dose after three to five days.
Statistical Analysis
Univariate associations between dichotomous variables were evaluated with Fisher's exact test. Associations involving ordered categorical variables were evaluated with the Wilcoxon rank-sum test.22 Analyses of the joint association of multiple variables with response were performed with logistic regression. Univariate and multivariate analyses of disease-free survival and overall survival were performed with proportional-hazards regression. Survival distributions were estimated with the methods of Kaplan and Meier.23
This study was designed with formal interim monitoring involving three planned analyses with an O'Brien–Fleming boundary. The study was unblinded by the Eastern Cooperative Oncology Group Data Monitoring Committee at the second analysis with 50 percent of the data available because of conclusive differences in disease-free survival between the two induction-therapy groups. The following groups of patients were excluded from the analyses of toxic effects and response to induction and maintenance therapy: patients who were removed from the study after randomization but before initiation of any study medication, because of their medical condition; patients who were found not to meet entry criteria on review; patients who were found not to have acute promyelocytic leukemia on review of bone marrow morphology; and patients on whom too little information was provided after the initiation of therapy. All patients with a confirmed complete remission who were enrolled in the study were considered in the analyses of maintenance therapy, although patients assigned directly to observation were omitted from analyses comparing the randomized treatment groups. To avoid bias, patients who had a complete remission after crossing over to chemotherapy were omitted from the primary analyses of induction and maintenance therapy, since crossover to all-trans-retinoic acid was not available to patients assigned to induction chemotherapy who did not have a complete remission.
Results
Accrual
Four hundred one patients from six cooperative oncology groups were enrolled in the study between April 1992 and February 1995. The data were analyzed as of February 1997. Of these 401 patients, 55 were excluded from detailed analysis: 23 because they did not have acute promyelocytic leukemia according to morphologic criteria, 14 because of their medical condition before any study treatment was given, 7 because they did not meet the entry criteria, and 11 because data on them were inadequate. Thus, 346 patients who could be evaluated were included in the analyses of the toxic effects and the outcome of the induction treatment, and 378 were included in the intention-to-treat analysis of survival. The characteristics of the 346 patients who could be evaluated are shown in Table 1Table 1
Base-Line Characteristics of 346 Patients with Acute Promyelocytic Leukemia..Induction Therapy
Complete Remission
Of the 174 patients who could be evaluated and who received chemotherapy, 120 (69 percent) had a complete remission, and of the 172 patients who could be evaluated and who were treated with all-trans-retinoic acid, 124 (72 percent) had a complete remission (P = 0.56). The rates of complete remission in patients with and without the microgranular variant (M3v) of acute promyelocytic leukemia were essentially the same (70 and 75 percent, respectively). The rate of complete remission for the 221 patients with t(15;17), by standard karyotyping, was 72 percent: 81 of 117 patients given chemotherapy (69 percent) and 79 of 104 patients treated with all-trans-retinoic acid (76 percent, P = 0.29). The rate of complete remission for the 22 patients lacking t(15;17) was 61 percent: 7 of 10 patients receiving chemotherapy (70 percent) and 6 of 12 patients receiving all-trans-retinoic acid (50 percent, P = 0.67). Four of the six patients receiving all-trans-retinoic acid who lacked t(15;17) and who had a complete remission tested positive for the promyelocytic leukemia–retinoic acid receptor alpha fusion transcript. The molecular analyses for the promyelocytic leukemia–retinoic acid receptor alpha fusion transcript have been described elsewhere.24
Crossover Patients
Fifteen patients assigned to induction therapy with all-trans-retinoic acid discontinued the drug because of resistant disease (4 patients) or toxic effects (11 patients) and crossed over to chemotherapy. The toxic effects in these 11 patients included acute thyroiditis, pulmonary hemorrhage, and vasculitis in 1 patient each and the retinoic acid syndrome in 8 patients. The four patients with resistant disease received all-trans-retinoic acid for 15, 24, 29, and 98 days. One of these four patients was positive for the promyelocytic leukemia–retinoic acid receptor alpha fusion transcript, and the others were negative. Ten of the 15 patients who discontinued all-trans-retinoic acid had a complete remission with chemotherapy. The cytogenetic findings in the 15 patients were as follows: t(15;17), 8 patients; trisomy 8, 1 patient; t(11;17), 1 patient; normal, 1 patient; and unknown, 4 patients.
Induction Failures and Toxic Effects
There were 43 deaths within 28 days among the 346 patients who could be evaluated (12.4 percent of patients; 95 percent confidence interval, 9.2 to 16.4 percent) (Table 2Table 2
Severe, Life-Threatening, and Lethal Toxic Effects during Induction Therapy.). There was no difference in mortality during induction treatment between the two groups, with 24 deaths among patients who received chemotherapy (14 percent) and 19 among those who received all-trans-retinoic acid (11 percent, P = 0.52). Of the patients who received chemotherapy, 12 died of intracerebral hemorrhage, 10 of infection, 1 of pulmonary toxic effects, and 1 of cardiopulmonary arrest. Of the patients who received all-trans-retinoic acid, 10 died of hemorrhage, 2 of infection, 2 of acute myocardial infarction, 3 of pulmonary complications (including 2 patients with the retinoic acid syndrome), 1 of hepatic toxic effects, and 1 of thrombosis.The toxic effects are listed in Table 2. The incidence of severe hemorrhage was the same in the two groups. There were fewer serious infections among the patients treated with all-trans-retinoic acid (25 percent) than among those receiving chemotherapy (52 percent). However, more patients treated with all-trans-retinoic acid had serious pulmonary toxic effects (21 percent) than did patients receiving chemotherapy (6 percent). Pseudotumor cerebri developed in at least four patients (two adults and two children) in the group receiving all-trans-retinoic acid.
Hyperleukocytosis
Seventy-four of the 172 patients assigned to all-trans-retinoic acid (43 percent) received hydroxyurea. Fifteen patients received hydroxyurea before receiving all-trans-retinoic acid to reduce the white-cell count to below 10,000 per cubic millimeter. The other 59 patients received hydroxyurea after starting all-trans-retinoic acid to maintain the white-cell count below 30,000 per cubic millimeter. Five of the 10 patients with fatal hemorrhage in the group receiving induction therapy with all-trans-retinoic acid had received hydroxyurea.
Retinoic Acid Syndrome
Retinoic acid syndrome developed in 45 of the 172 patients who could be evaluated (26 percent) in the group receiving induction therapy with all-trans-retinoic acid after a median of 12 days (range, 2 to 47). Forty-four of the 45 patients with the retinoic acid syndrome were treated with dexamethasone. Among the 45 patients, the syndrome resolved in 43 patients, and the other 2 died. Seven additional patients had signs or symptoms suggestive of the syndrome, but concurrent medical problems complicated the diagnosis.
Consolidation Therapy
Of 244 patients who could be evaluated and who had a complete remission, 229 received both cycles of consolidation chemotherapy. There were no lethal toxic effects during consolidation therapy. Fifteen patients received only one cycle. Nine of these patients discontinued treatment and received no further protocol therapy after cycle 1 of consolidation therapy; the other six did not receive cycle 2 of consolidation therapy because of toxic effects during cycle 1 and underwent random assignment to maintenance therapy directly. Daunorubicin was omitted in one or both consolidation cycles in 26 patients, in most cases because of decreased cardiac function. Twenty-two of these patients had been assigned to induction chemotherapy, and four had been assigned to induction therapy with all-trans-retinoic acid, with approximately equal numbers assigned to each maintenance treatment.
Maintenance Therapy
Of the 237 patients who entered the maintenance phase of the trial, 14 were excluded from the analysis of the induction phase, 14 did not have a complete remission confirmed by bone marrow findings (6 who received all-trans-retinoic acid and 8 who received chemotherapy), 4 who were intolerant of all-trans-retinoic acid were directly assigned to observation, and 6 who crossed over from all-trans-retinoic acid to chemotherapy during induction treatment were excluded from the analysis of the results of maintenance therapy. Thus, 199 patients were randomly assigned to either maintenance therapy with all-trans-retinoic acid (94 patients) or observation (105 patients) and were included in this portion of the analysis. Of the 94 patients who were assigned to all-trans-retinoic acid, 64 (68 percent) completed the full one year of all-trans-retinoic acid. The reasons for stopping early included relapse (12 patients), toxic effects (14 patients), withdrawal of consent (2 patients), complicating disease (1 patient), and withdrawal from the study (1 patient). The median duration of maintenance therapy with all-trans-retinoic acid for patients who stopped early was 5 months (range, 1 week to 11 months). Toxic effects among these patients included headache (three patients), depression (one patient), elevated aminotransferase levels (three patients), rash (two patients), cardiac effects (two patients), nausea (one patient), pseudotumor cerebri (one patient), and distal-digit vaso-occlusive syndrome (one patient).
Toxic Effects of Maintenance Therapy
Of the 94 patients assigned to all-trans-retinoic acid, 34 (36 percent) had severe or life-threatening toxic effects. These effects included neurotoxicity in 11 patients, of whom 5 had headache, 3 (2 children and 1 adult) had pseudotumor cerebri, 2 had hearing loss, and 1 had depression; infections in 7 patients; and hepatotoxicity in 5 patients (hyperbilirubinemia or aminotransferase elevation). Four episodes of severe toxic effects (infection, hepatotoxicity, headache, and hypertriglyceridemia) occurred in 3 of the 105 patients assigned to observation.
Disease-Free Survival
Effect of Induction Treatment
With a median follow-up of 30 months for surviving patients, the estimated 1-, 2-, and 3-year rates of disease-free survival from the time of entering complete remission were 57, 43, and 32 percent, respectively, for patients who could be evaluated and who received induction chemotherapy. There were 70 relapses among these 120 patients (Figure 1Figure 1
Kaplan–Meier Product-Limit Estimate of Disease-free Survival from the Time of Complete Remission for Patients Randomly Assigned at Induction to Either Daunorubicin plus Cytarabine or All-tran s-Retinoic Acid.). For patients who received induction therapy with all-trans-retinoic acid, the estimated one-, two-, and three-year rates of disease-free survival were 87, 70, and 67 percent, respectively. There were 36 relapses among these 124 patients (P<0.001).Effect of Maintenance Treatment
Of the 94 patients assigned to maintenance treatment with all-trans-retinoic acid, 29 relapsed, as compared with 60 of the 105 patients assigned to observation. The estimated one-, two-, and three-year rates of disease-free survival from the date of assignment to maintenance therapy or observation were 82, 68, and 65 percent, respectively, for patients assigned to all-trans-retinoic acid, and 53, 40, and 40 percent, respectively, for patients assigned to observation, regardless of the induction regimen (P<0.001, with stratification according to induction regimen) (Figure 2Figure 2
Kaplan–Meier Product-Limit Estimate of Disease-free Survival from the Time of Random Assignment to Maintenance with All-tran s-Retinoic Acid or to Observation.).Combined Effects of Induction and Maintenance Treatments
There were 19 relapses among the 48 patients who received induction chemotherapy with daunorubicin plus cytarabine and maintenance therapy with all-trans-retinoic acid, 10 relapses among the 46 patients who received all-trans-retinoic acid for both induction and maintenance, and 21 relapses among the 54 patients who received all-trans-retinoic acid for induction and no maintenance therapy; all these numbers are significantly lower than the 39 relapses among the 51 patients who never received all-trans-retinoic acid (P<0.001) (Figure 3Figure 3
Kaplan–Meier Product-Limit Estimates of Disease-free Survival on the Basis of Both the Type of Induction Therapy and the Type of Maintenance Therapy.).Overall Survival
The estimated rates of overall survival at one, two, and three years from entry into the study for the 346 patients who could be evaluated were 75, 57, and 50 percent, respectively, for patients who received induction chemotherapy, and 84, 74, and 71 percent, respectively, for patients who received induction therapy with all-trans-retinoic acid (P<0.001). The overall survival rates in the intention-to-treat analysis of all patients at one, two, and three years were 75, 57, and 50 percent, respectively, among the 190 patients assigned to chemotherapy, and 82, 72, and 67 percent, respectively, among the 188 patients assigned to all-trans-retinoic acid (P = 0.003) (Figure 4Figure 4
Kaplan–Meier Product-Limit Estimate of Overall Survival According to Intention-to-Treat Analysis for Patients Receiving Daunorubicin plus Cytarabine or All-tran s-Retinoic Acid as Induction Therapy.).Discussion
This study shows that all-trans-retinoic acid given as induction or maintenance therapy results in improved disease-free survival and overall survival, as compared with chemotherapy alone, in patients with newly diagnosed acute promyelocytic leukemia. All-trans-retinoic acid given during induction did not improve the rate of complete remission or decrease early mortality, but it reduced the likelihood of relapse. It is not clear whether the use of all-trans-retinoic acid for both induction and maintenance is superior to the use of the drug only during induction, or whether maintenance with all-trans-retinoic acid actually prevents, rather than delays, relapse.
The rate of complete remission we found with all-trans-retinoic acid (72 percent) is lower than the 91 percent reported in the only other randomized study of the drug in acute promyelocytic leukemia,25 but the two studies are not directly comparable, since most patients assigned to all-trans-retinoic acid by Fenaux and colleagues also received standard chemotherapy along with all-trans-retinoic acid to control hyperleukocytosis. Single-institution and multi-institution phase 2 studies report rates of complete remission of 86 to 100 percent with all-trans-retinoic acid alone.13-19 The lower rate reported here is partly attributable to our requirement of rigorous documentation of complete remission. If we included patients believed to be in complete remission by their treating physicians who had long survival but inadequately confirmed complete remissions, either because of lack of documentation (seven patients) or failure to be assigned to maintenance treatment (six patients), our rate of complete remission would be about 80 to 85 percent. Furthermore, if the crossover patients were included among the patients given all-trans-retinoic acid who had a complete remission, the rate of complete remission would be 78 percent (134 of 172 patients).
The disappointing outcome with chemotherapy alone (18 percent disease-free survival at three years) is not easily explained. Although our results are less favorable than those reported in earlier analyses of the effect of chemotherapy in acute promyelocytic leukemia,7,8,26,27 they are similar to the results of the randomized study by Fenaux et al.25 The outcome of our patients who did not receive the full dose of daunorubicin during consolidation treatment did not differ from that of patients who received the full dose of the drug.
A number of questions remain. First, can retinoid toxicity, particularly the retinoic acid syndrome, be reduced? A major toxic effect of all-trans-retinoic acid is the retinoic acid syndrome; eight patients with the disorder discontinued all-trans-retinoic acid and crossed over to chemotherapy. The strategies of administering prophylactic corticosteroids28 or using a lower dose of all-trans-retinoic acid29 (15 to 20 mg per square meter per day) have not yet been evaluated in randomized trials.
Second, would concurrent induction treatment with all-trans-retinoic acid and chemotherapy improve the outcome over that with all-trans-retinoic acid alone? Avvisati and colleagues30 had excellent results with all-trans-retinoic acid plus idarubicin. Their findings suggest that further investigation of the simultaneous administration of all-trans-retinoic acid and chemotherapy is warranted. The combination may prevent hyperleukocytosis, reduce the incidence of the retinoic acid syndrome, lead to a higher rate of complete remission, and improve the long-term outcome.
Third, what would be the best chemotherapy to administer with all-trans-retinoic acid for induction and consolidation therapy? In one study conducted before all-trans-retinoic acid was available, high-dose daunorubicin for induction resulted in an excellent outcome.31 It may even be possible to omit cytarabine from a regimen containing all-trans-retinoic acid.32
Fourth, can a subgroup of patients at high risk for relapse be identified? The reverse-transcriptase–polymerase-chain-reaction (PCR) assay can successfully detect minimal residual disease,33 and a positive PCR result after consolidation chemotherapy may predict relapse.34,35
Finally, is there a role for bone marrow transplantation in patients who are PCR-positive but in clinical remission?
This study shows that all-trans-retinoic acid, when given during induction or maintenance therapy, improves disease-free survival and overall survival in patients with newly diagnosed acute promyelocytic leukemia over that obtained with chemotherapy alone. Given the decrease in the duration of hospitalization, the use of blood products, and the cost of care in patients treated with all-trans-retinoic acid,36,37 we recommend the use of all-trans-retinoic acid for induction therapy in all patients with acute promyelocytic leukemia. Further follow-up is needed to define its role as maintenance therapy more precisely.
Presented in part at the 36th meeting of the American Society of Hematology, Seattle, December 1–5, 1995.
Coordinated by the Eastern Cooperative Oncology Group (Robert L. Comis, M.D., Group Chair) and supported in part by Public Health Service grants from the National Cancer Institute and the Department of Health and Human Services.
Source Information
From the Northwestern University Medical School and the Robert H. Lurie Cancer Center of Northwestern University, Chicago (M.S.T.); Dana–Farber Cancer Institute, Boston (J.W.A.); Greenebaum Cancer Center, University of Maryland School of Medicine, Baltimore (C.A.S.); Fred Hutchinson Cancer Research Center, University of Washington, Seattle (F.R.A.); Children's Hospital–Oakland, Oakland, Calif. (J.H.F.); Texas Children's Cancer Center, Houston (A.O.); National Cancer Institute of Canada Clinical Trials Group, Kingston, Ont. (L.S.); University of New Mexico, Albuquerque (C.W.); Roswell Park Memorial Institute, Buffalo, N.Y. (C.D.B.); University of Rochester, Rochester, N.Y. (J.M.R.); and Albert Einstein Cancer Center, Montefiore Medical Center, Bronx, N.Y. (P.H.W.).
Address reprint requests to Dr. Tallman at the Robert H. Lurie Cancer Center of Northwestern University, Division of Hematology–Oncology, Northwestern University Medical School, 233 E. Erie St., Suite 700, Chicago, IL 60611.
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- Citing Articles (256)
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Muhamed Baljevic, Jae H. Park, Eytan Stein, Dan Douer, Jessica K. Altman, Martin S. Tallman. (2011) Curing All Patients with Acute Promyelocytic Leukemia: Are We There Yet?. Hematology/Oncology Clinics of North America 25:6, 1215-1233
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Jordi Rodon, Charlotte D. Jacobs, Quincy Chu, Eric K. Rowinsky, Arturo Lopez-Anaya, Chris H. Takimoto, Heather A. Wakelee. (2011) A phase I pharmacokinetic study of bexarotene with paclitaxel and carboplatin in patients with advanced non-small cell lung cancer (NSCLC). Cancer Chemotherapy and Pharmacology
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Surajit Das, Wai Kiong Ng, Parijat Kanaujia, Sanggu Kim, Reginald B.H. Tan. (2011) Formulation design, preparation and physicochemical characterizations of solid lipid nanoparticles containing a hydrophobic drug: Effects of process variables. Colloids and Surfaces B: Biointerfaces 88:1, 483-489
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Marvin M. van Luijn, Theresia M. Westers, Martine E.D. Chamuleau, S. Marieke van Ham, Gert J. Ossenkoppele, Arjan A. van de Loosdrecht. (2011) Class II–Associated Invariant Chain Peptide Expression Represents a Novel Parameter for Flow Cytometric Detection of Acute Promyelocytic Leukemia. The American Journal of Pathology 179:5, 2157-2161
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Tomohiko Kamimura, Toshihiro Miyamoto, Mine Harada, Koichi Akashi. (2011) Advances in therapies for acute promyelocytic leukemia. Cancer Science 102:11, 1929-1937
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Karen A. Breen, David Grimwade, Beverley J. Hunt. (2011) The pathogenesis and management of the coagulopathy of acute promyelocytic leukaemia. British Journal of Haematologyno-no
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Anca G. Gocan, Doris Bachg, A.E. Schindler, U.D. Rohr. (2011) Managing immunity in resistant cancer patients correlates to survival: results and discussion of a pilot study. Hormone Molecular Biology and Clinical Investigation 8:2, 455-469
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Manu D. Tiwari, Sarika Mehra, Sameer Jadhav, Jayesh R. Bellare. (2011) All-trans retinoic acid loaded block copolymer nanoparticles efficiently induce cellular differentiation in HL-60 cells. European Journal of Pharmaceutical Sciences
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Bayard L Powell. (2011) Arsenic trioxide in acute promyelocytic leukemia: potion not poison. Expert Review of Anticancer Therapy 11:9, 1317-1319
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J. H. Park, B. Qiao, K. S. Panageas, M. J. Schymura, J. G. Jurcic, T. L. Rosenblat, J. K. Altman, D. Douer, J. M. Rowe, M. S. Tallman. (2011) Early death rate in acute promyelocytic leukemia remains high despite all-trans retinoic acid. Blood 118:5, 1248-1254
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Jae H Park, Martin S Tallman. (2011) Managing acute promyelocytic leukemia without conventional chemotherapy: is it possible?. Expert Review of Hematology 4:4, 427-436
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L. Rubinstein, M. LeBlanc, M. A. Smith. (2011) More Randomization in Phase II Trials: Necessary but not Sufficient. JNCI Journal of the National Cancer Institute 103:14, 1075-1077
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S Lehmann, A Ravn, L Carlsson, P Antunovic, S Deneberg, L Möllgård, Å Rangert Derolf, D Stockelberg, U Tidefelt, A Wahlin, L Wennström, M Höglund, G Juliusson. (2011) Continuing high early death rate in acute promyelocytic leukemia: a population-based report from the Swedish Adult Acute Leukemia Registry. Leukemia 25:7, 1128-1134
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Bo Cai, Weidong Yang, Yu Zhao, Lei Yuan, Lili Wang, Li Gao, Nan Wang, Li Yu, Chunji Gao. (2011) Successful management with an effective induction regimen followed by allogeneic hematopoietic stem cell transplantation for promyelocytic blast crisis of chronic myelogenous leukemia. Annals of Hematology
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Irene Ma, Alison L. Allan. (2011) The Role of Human Aldehyde Dehydrogenase in Normal and Cancer Stem Cells. Stem Cell Reviews and Reports 7:2, 292-306
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Ebtesam Ibrahim Ahmad, Hosneia kh. Akl, Mona E. Hashem, Tarek Ali M. Elgohary. (2011) The biological characteristics of adult CD34+ acute promyelocytic leukemia. Medical Oncology
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Marise R. Heerma van Voss, Petra Groep, Joost Bart, Elsken Wall, Paul J. Diest. (2011) Expression of the stem cell marker ALDH1 in BRCA1 related breast cancer. Cellular Oncology 34:1, 3-10
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Seonghoon Choi, Hyeong-Su Kim, Chang-Soo Jung, Seong-Woong Jung, Yun-Ja Lee, Jin-Kyeong Rheu, Jung-Rae Jo, Nam-Ho Lee. (2011) Reversible Symptomatic Myocarditis Induced by All-Trans Retinoic Acid Administration during Induction Treatment of Acute Promyelocytic Leukemia: Rare Cardiac Manifestation as a Retinoic Acid Syndrome. Journal of Cardiovascular Ultrasound 19:2, 95
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Farshid Dayyani, Hagop Kantarjian, Susan O'Brien, Sherry Pierce, Dan Jones, Stefan Faderl, Guillermo Garcia-Manero, Jorge Cortes, Farhad Ravandi. (2011) Outcome of therapy-related acute promyelocytic leukemia with or without arsenic trioxide as a component of frontline therapy. Cancer 117:1, 110-115
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M. S. Tallman, H. T. Kim, P. Montesinos, F. R. Appelbaum, J. de la Serna, J. M. Bennett, G. Deben, C. D. Bloomfield, J. Gonzalez, J. H. Feusner, M. Gonzalez, R. Gallagher, J. D. G.-S. Miguel, R. A. Larson, G. Milone, E. Paietta, C. Rayon, J. M. Rowe, C. Rivas, C. A. Schiffer, E. Vellenga, L. Shepherd, J. L. Slack, P. H. Wiernik, C. L. Willman, M. A. Sanz. (2010) Does microgranular variant morphology of acute promyelocytic leukemia independently predict a less favorable outcome compared with classical M3 APL? A joint study of the North American Intergroup and the PETHEMA Group. Blood 116:25, 5650-5659
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Deborah Kirk Walker, Jeanne Held-Warmkessel. (2010) Acute Promyelocytic Leukemia: An Overview With Implications for Oncology Nurses. Clinical Journal of Oncology Nursing 14:6, 747-759
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Sylvain Thépot, Lionel Ades, Pierre Fenaux. 2010. Acute Promyelocytic Leukemia: Manifestations and Therapy. , 169-179.
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B. L. Powell, B. Moser, W. Stock, R. E. Gallagher, C. L. Willman, R. M. Stone, J. M. Rowe, S. Coutre, J. H. Feusner, J. Gregory, S. Couban, F. R. Appelbaum, M. S. Tallman, R. A. Larson. (2010) Arsenic trioxide improves event-free and overall survival for adults with acute promyelocytic leukemia: North American Leukemia Intergroup Study C9710. Blood 116:19, 3751-3757
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Yue-Jun Liu, De-Pei Wu, Jian-Ying Liang, Hui-Ying Qiu, Zheng-Ming Jin, Xiao-Wen Tang, Cheng-Cheng Fu, Xiao Ma. (2010) Long-term survey of outcome in acute promyelocytic leukemia: a single center experience in 340 patients. Medical Oncology
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Changcheng Zheng, Xin Liu, Weibo Zhu, Jingsheng Wu, Xiaoyan Cai, Zimin Sun. (2010) Strategy to further increase of cure rate in acute promyelocytic leukaemia: low-dose all-trans retinoic acid and sequential maintenance cycle. British Journal of Haematology 151:4, 406-409
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Jacob M. Rowe, Haesook T. Kim, Peter A. Cassileth, Hillard M. Lazarus, Mark R. Litzow, Peter H. Wiernik, Martin S. Tallman. (2010) Adult patients with acute myeloid leukemia who achieve complete remission after 1 or 2 cycles of induction have a similar prognosis. Cancer 116:21, 5012-5021
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John H. Block. 2010. Vitamins. .
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M. Aljurf, F. Al Qurashi, F. Al Mohareb, E. Sahovic, F. Al Sharif, H. Al Zahrani, A. Al Shanqeeti, T. Owaidah, A. Iqbal, S. Z. A. Zaidi, Z. A. Nurgat, M. Sanz, N. Chaudhri. (2010) High efficacy and low toxicity of APL induction with concurrent idarubicin/ATRA followed by a novel and simplified outpatient post-remission therapy using single doses of idarubicin and intermittent ATRA. Medical Oncology 27:3, 702-707
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Ramzi Jeddi, Hèlà Ghédira, Yosr Ben Abdennebi, Karima Kacem, Ramzi Ben Amor, Lamia Aissaoui, Walid Bouterâa, Raihane Ben Lakhal, Hèla Ben Abid, Samia Menif, Zaher Belhadjali, Balkis Meddeb. (2010) ATRA and anthracycline-based chemotherapy in the treatment of childhood acute promyelocytic leukemia (APL): A 10-year experience in Tunisia. Medical Oncology
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Anna Martner, Fredrik B Thorén, Johan Aurelius, Jonas Söderholm, Mats Brune, Kristoffer Hellstrand. (2010) Immunotherapy with histamine dihydrochloride for the prevention of relapse in acute myeloid leukemia. Expert Review of Hematology 3:4, 381-391
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Reinier H. van Rijssel, Jurgen Wegman, Monique E. Oud, Steven T. Pals, Marinus H.J. van Oers. (2010) A case of ATRA-induced isolated myocarditis in the absence of circulating malignant cells: Demonstration of the t(15;17) translocation in the inflammatory infiltrate by in situ hybridisation. Leukemia Research 34:7, e142-e144
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Tsunayuki Kakimoto, Yosuke Takahashi, Hiroyuki Watanabe, Motoshi Matsuzawa, Yukinari Sanada, Kazuhito Suzuki, Ai Mihara, Sachiko Yoshida, Tomonori Nakazato. (2010) Primary multiple cerebral invasion in acute promyelocytic leukemia dramatically worsened by all-trans retinoic acid. Leukemia Research 34:5, e137-e139
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John H. Block. 2010. Selective Toxicity. .
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Miguel A. Sanz, Pau Montesinos. (2010) Open issues on bleeding and thrombosis in acute promyelocytic leukemia. Thrombosis Research 125, S51-S54
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L. Ades, A. Guerci, E. Raffoux, M. Sanz, P. Chevallier, S. Lapusan, C. Recher, X. Thomas, C. Rayon, S. Castaigne, O. Tournilhac, S. de Botton, N. Ifrah, J.-Y. Cahn, E. Solary, C. Gardin, N. Fegeux, D. Bordessoule, A. Ferrant, S. Meyer-Monard, N. Vey, H. Dombret, L. Degos, S. Chevret, P. Fenaux, . (2010) Very long-term outcome of acute promyelocytic leukemia after treatment with all-trans retinoic acid and chemotherapy: the European APL Group experience. Blood 115:9, 1690-1696
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Takashi Miyoshi, Toshiyuki Arai, Kouhei Yamashita, Masataka Sasada, Takashi Uchiyama. (2010) NB4 cells treated with all-trans retinoic acid generate toxic reactive oxygen species that cause endothelial hyperpermeability. Leukemia Research 34:3, 373-378
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Felicetto Ferrara. (2010) Acute promyelocytic leukemia: what are the treatment options?. Expert Opinion on Pharmacotherapy 11:4, 587-596
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Myoung-Hyun Kim, Cheol-Soon Choi, Jae Wook Lee, Pil-Sang Jang, Nak-Gyun Chung, Bin Cho, Dae-Chul Jeong, Hack-Ki Kim. (2010) Outcome of childhood acute promyelocytic leukemia treated using a modified AIDA protocol. The Korean Journal of Hematology 45:4, 236
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M. S. Tallman, J. K. Altman. (2009) How I treat acute promyelocytic leukemia. Blood 114:25, 5126-5135
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John Gregory, Haesook Kim, Todd Alonzo, Rob Gerbing, William Woods, Howard Weinstein, Lois Shepherd, Charles Schiffer, Frederick Appelbaum, Cheryl Willman, Peter Wiernik, Jacob Rowe, Martin Tallman, James Feusner. (2009) Treatment of children with acute promyelocytic leukemia: Results of the first North American intergroup trial INT0129. Pediatric Blood & Cancer 53:6, 1005-1010
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John Gregory, James Feusner. (2009) Acute promyelocytic leukemia in childhood. Current Oncology Reports 11:6, 439-445
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Wenshu Yu, Christopher M. Burns. (2009) All-Trans Retinoic Acid-Induced Focal Myositis, Synovitis, and Mononeuritis. JCR: Journal of Clinical Rheumatology 15:7, 358-360
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Xue-Qun Luo, Zhi-Yong Ke, Li-Bin Huang, Xiao-Qing Guan, Ying-Chuan Zhang, Xiao-Li Zhang. (2009) Improved outcome for Chinese children with acute promyelocytic leukemia: A comparison of two protocols. Pediatric Blood & Cancer 53:3, 325-328
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Li Bao, Xijing Lu, Yueyun Lai, Xiaohui Zhang, Honghu Zhu, Yanrong Liu, Yazhen Qin, Xiao-Jun Huang. (2009) Therapy-related acute myeloid leukemia after successful therapy for acute promyelocytic leukemia with t(15;17): A case report and literature review. Leukemia Research 33:7, e64-e68
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Weiying Gu, Shaoyan Hu, Bai He, Guoqiang Qiu, Jinghong Ma, Zixing Chen. (2009) Metabolites of acute promyelocytic leukemia cells participate in contributing to hypertriglyceridemia induced by all-trans retinoic acid. Leukemia Research 33:4, 592-594
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Eytan Stein, Brandon McMahon, Hau Kwaan, Jessica K. Altman, Olga Frankfurt, Martin S. Tallman. (2009) The coagulopathy of acute promyelocytic leukaemia revisited. Best Practice & Research Clinical Haematology 22:1, 153-163
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Mark R. Green, Stephen L. George, Richard L. Schilsky. (2008) Tomorrow's Cancer Treatments Today: The First 50 Years of the Cancer and Leukemia Group B. Seminars in Oncology 35:5, 470-483
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Carlos Artur da Costa Moraes, Nádia Mendonça Trompieri, Francisco Hélder Cavalcante Felix. (2008) Pediatric Acute Promyelocytic Leukemia: All-transretinoic Acid Therapy in a Brazilian Pediatric Hospital. Journal of Pediatric Hematology/Oncology 30:5, 387-390
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