Original Article
Lasting Remissions in Hairy-Cell Leukemia Induced by a Single Infusion of 2-Chlorodeoxyadenosine
N Engl J Med 1990; 322:1117-1121April 19, 1990
- Abstract
- Abstract
2-Chlorodeoxyadenosine is a simple purine nucleoside that has previously been shown to be effective in the treatment of low-grade malignant disorders of lymphoid tissue, including chronic lymphocytic leukemia and non-Hodgkin's lymphoma. Because of these encouraging results, we treated 12 patients with another low-grade B-cell neoplasm, hairy-cell leukemia. The patients received 2-chlorodeoxyadenosine (0.1 mg per kilogram of body weight per day) by continuous infusion for seven days.
All the patients responded to treatment. Eleven had complete remissions characterized by the normalization of peripheral blood and bone marrow and disappearance of tumor masses. The longest remission has been 3.8 years. None of the patients have relapsed, and the median duration of remission has been 15.5 months. No serious toxic reactions occurred as a result of 2-chlorodeoxyadenosine therapy.
These results suggest that 2-chlorodeoxyadenosine may be the most effective therapy available for hairy-cell leukemia. The administration of 2-chlorodeoxyadenosine resulted in a higher rate of complete remission than is observed with interferon alfa, and it required no maintenance therapy. Its toxicity may be lower than that of deoxycoformycin, and the responses were achieved with single courses of treatment. (N Engl J Med 1990; 322:1117–21.)
Media in This Article
Figure 1
Effect of Splenectomy and 2-Chlorodeoxyadenosine (CdA) Therapy on the Course of Hairy-Cell Leukemia, According to the Changes in the Numbers of Platelets (Solid Triangles) and Polymorphonuclear Neutrophils (PMN; Open Diamonds) and the Hemoglobin Level (Stippled Area below Solid Line).Figure 2
Marrow-Biopsy Specimen Obtained from Patient 5 before Treatment (Hematoxylin and Eosin; Panel A, ×25; Panel B, ×90).Article Activity
- Article
FIRST described by Bouroncle et al. in 1958 as leukemic reticuloendotheliosis,1 hairy-cell leukemia is now recognized to be a low-grade B-cell neoplasm.2 If untreated, this disorder follows a chronic, inexorable course, usually characterized by progressive pancytopenia.
Because of our success in the treatment of another B-cell neoplasm, chronic lymphocytic leukemia, with the deoxyadenosine analogue 2-chlorodeoxyadenosine,3 we have now undertaken a trial of this agent in hairy-cell leukemia. An adenosine deaminase—resistant purine analogue, 2-chlorodeoxyadenosine selectively accumulates as the 5′–triphosphate derivative in cells rich in deoxycytidine kinase. The cytotoxic activity of 2-chlorodeoxyadenosine is independent of cell division.4 Presumably because of its high cellular specificity, 2-chlorodeoxyadenosine has previously been found to be remarkably devoid of the toxic side effects usually associated with chemotherapeutic agents against cancer. Unlike deoxycoformycin, which has also been studied recently in the treatment of hairy-cell leukemia, 2-chlorodeoxyadenosine is not an adenosine deaminase inhibitor. Since both drugs increase the levels of deoxynucleotides, there are some similarities in their spectrums of activity.
We report the results of 2-chlorodeoxyadenosine therapy in 12 patients with this relatively rare disorder. Our findings demonstrate that long-lasting remissions are induced with a single course of treatment without any serious side effects.
Methods
Eligibility
To be eligible, patients required an unequivocal diagnosis of hairy-cell leukemia based on marrow-aspiration and biopsy results. Evidence of active disease, such as neutropenia, thrombocytopenia, anemia, symptomatic adenopathy, or repeated infections, was a prerequisite for entry into the study, but previous treatment was not. There were no age restrictions. Patients were excluded if they had active systemic infection or abnormal renal or hepatic function at the time of treatment, or if they had received any treatment, including glucocorticoids, within three months before the study began. The study was approved by our institutional review board, and written informed consent was obtained from all patients.
Study Population
From 1986 to 1989, 12 patients met the eligibility criteria for enrollment in the study. There were 11 men and 1 woman, ranging in age from 36 to 61 years. Seven of the 12 patients had previously undergone splenectomy. Five of the patients had been treated with interferon alfa; two had had no response, and three had had partial responses but the disease later progressed or therapy was discontinued because of toxicity. The characteristics of the study population are summarized in Table 1Table 1
Demographic Characteristics of the 12 Patients with Hairy-Cell Leukemia Enrolled in the Study..Drug Therapy and Monitoring for Toxicity
2-Chlorodeoxyadenosine was synthesized and purified at the Scripps Clinic and Research Foundation as described previously.5 All patients were hospitalized in the General Clinical Research Center of the Green Hospital of Scripps Clinic.
Before the initiation of therapy all patients had a complete physical examination, imaging of the chest, abdomen, and pelvis by computerized axial tomography (CT), and a complete blood count and underwent electrocardiography. In addition, marrow aspiration and biopsy, cytochemical examination of the marrow and blood film for tartrate-resistant acid phosphatase, and a complete panel of blood chemistry tests (Chem-24, Boehringer–Mannheim Diagnostics, Indianapolis) were performed. A single continuous seven-day infusion of 2-chlorodeoxyadenosine (0.1 mg per kilogram of body weight per day) was then administered to each patient.
During the administration of 2-chlorodeoxyadenosine the results of daily physical examinations, complete blood counts, and plasma 2-chlorodeoxyadenosine levels5 were recorded. On alternate days a complete panel of blood chemistry tests was performed. Each patient was given 300 mg of allopurinol daily as prophylaxis against the development of hyperuricemia as a result of tumor breakdown.
After therapy, the patients were discharged from the hospital and monitored approximately weekly for the first month after therapy and monthly thereafter. Blood counts were performed until maximal improvement had been achieved. At that time, a complete reevaluation, including imaging and marrow aspiration and biopsy, was performed.
Toxicity was evaluated according to standard criteria.6
Response Criteria
A complete remission was defined as the complete disappearance of all evidence of disease.6 The complete blood count had to show more than 1.5×109 neutrophils per liter, more than 12.0 g of hemoglobin per deciliter, more than 130×109 platelets per liter, and the absence of any abnormal lymphocytes, with reversion to negative of the tartrate-resistant acid phosphatase stain (when positive initially). The disappearance of all evidence of disease on marrow aspiration and biopsy was required. Physical examination and imaging studies had to demonstrate the disappearance of all abnormal lymph nodes and of hepatosplenomegaly.
A partial remission was defined as an improvement of more than 50 percent in all abnormally low blood counts and a reduction of more than 50 percent in the absolute count of hairy cells in the peripheral blood and marrow. On physical examination and imaging studies, a reduction of more than 50 percent in hepatomegaly, splenomegaly, and adenopathy was required. Patients who did not meet the criteria for complete or partial remission were judged to be in the "no response" category.
The duration of the response was measured from the initiation of 2-chlorodeoxyadenosine therapy.
Results
Eleven of the 12 patients had a complete remission after the single infusion of 2-chlorodeoxyadenosine, and 1 had a partial response. This patient had hematologic improvement, a reduction in spleen size, and a 50 percent decrease in the involvement of the marrow, but refused further therapy because he felt well. The clinical and laboratory data for all 12 patients before and after treatment are summarized in Table 2Table 2
Laboratory Findings in 12 Patients with Hairy-Cell Leukemia before and after Treatment with 2-Chlorodeoxyadenosine.*.The clinical course of the first patient treated is summarized in Figure 1Figure 1
Effect of Splenectomy and 2-Chlorodeoxyadenosine (CdA) Therapy on the Course of Hairy-Cell Leukemia, According to the Changes in the Numbers of Platelets (Solid Triangles) and Polymorphonuclear Neutrophils (PMN; Open Diamonds) and the Hemoglobin Level (Stippled Area below Solid Line).. This course is typical of that followed by all the patients who had a complete remission. Characteristically, the total leukocyte count decreased, starting a few days after the infusion was begun, with a rapid decline in the number of hairy cells in the circulation. Normalization of the hemoglobin level, neutrophil level, and platelet count occurred within eight weeks after the initiation of therapy, and a marrow examination at this time confirmed the achievement of a complete remission. Typical marrow findings before and after treatment are shown in Figures 2Figure 2Marrow-Biopsy Specimen Obtained from Patient 5 before Treatment (Hematoxylin and Eosin; Panel A, ×25; Panel B, ×90). and 3Figure 3
Marrow-Biopsy Specimen Obtained from Patient 5 123 Days after Treatment (Hematoxylin and Eosin; Panel A, ×50; Panel B,×90)., respectively. None of the 11 patients have relapsed; the duration of complete remission has ranged from 7 to 46 months after the beginning of treatment, with a median duration of remission of 15.5 months (Table 3Table 3
Type and Duration of Response Achieved in 12 Patients with Hairy-Cell Leukemia.).The toxicity of 2-chlorodeoxyadenosine seemed to be very limited. Six patients had a decrease in the neutrophil count with treatment. Most of these six patients had severely compromised neutrophil counts at the start of therapy due to the disease but, despite a further decrease in the neutrophil count, had no infections. The neutrophil count returned to normal within 30 days of treatment. The other six patients, who had no decrease in the neutrophil count with therapy —although many had neutropenia due to disease — also had a normal neutrophil count after therapy. No other hematologic toxicity was encountered in this series of patients. Seven of the 12 patients had increases in temperature to more than 38°C during or immediately after the infusion of 2-chlorodeoxyadenosine. They were treated empirically with antibiotics, but no infections could be documented. The time of the temperature elevations coincided in each case with the rapid decline in the number of circulating hairy cells, and defervescence occurred within 3 to 10 days (median, 5), at which time most of the hairy cells had been cleared from the blood. Fever is not a known side effect of 2-chlorodeoxyadenosine,3 and we are inclined to attribute the fever in these seven patients to the release of pyrogens from tumor cells, although the occurrence of an undiagnosable intercurrent infection in each patient cannot be excluded. No patient had nausea, vomiting, hair loss, conjunctivitis, skin rash, or abnormal liver or kidney function. No opportunistic infections developed in any of the patients. One patient, who had esophageal candidiasis before treatment with 2-chlorodeoxyadenosine, responded well to treatment.
Discussion
For a quarter of a century after the recognition of hairy-cell leukemia as a diagnostic entity, treatment was most unsatisfactory. Management was largely limited to splenectomy and low-dose chemotherapy. Although isolated success was reported with aggressive chemotherapy, there was sufficient potential for a worsening of the patient's condition to discourage most physicians from such therapeutic adventures. It is ironic that within a very short time, two relatively effective treatments — interferon alfa and deoxycoformycin — have been introduced. Both are vastly superior to earlier therapies, but neither is ideal.
Interferon alfa appears to be capable of inducing a clinical response in 80 percent of patients with hairy-cell leukemia,7 8 9 but the rate of complete remission is low (10 to 15 percent), maintenance therapy is required, and the remissions are not lasting. Furthermore, interferon is expensive, and its administration is associated with toxic effects, including an influenza-like syndrome, nausea and vomiting, malaise, skin disorders, and nervous system disorders. The results with deoxycoformycin10 seem to be more favorable. In various studies, clinical response rates of 70 to 90 percent and rates of complete remission of 30 to 90 percent have been achieved. However, even at low doses, deoxycoformycin appears to be more toxic than 2-chlorodeoxyadenosine. Treatment with deoxycoformycin has been associated in some patients with nausea and vomiting, conjunctivitis, lethargy, skin rash, and renal and central nervous system toxicity. In addition, it may induce marked immunosuppression with a prolonged reduction in the number of circulating CD4 T lymphocytes.11 Moreover, deoxycoformycin has proved very difficult to produce in quantity and is therefore very costly.
The results of treatment with 2-chlorodeoxyadenosine compare very favorably with those of all currently available treatments. Over 90 percent of our patients had a complete remission (Table 3), and none have relapsed. Hairy cells disappeared from the blood and marrow, extra-marrow lesions disappeared, and peripheral-blood counts returned to normal (Table 2). The treatment regimen was easy to administer, and in each case remission occurred after a single seven-day infusion of the drug. 2-Chlorodeoxyadenosine has not produced the spectrum of toxic effects associated with deoxycoformycin therapy. In Phase I studies, the dose-limiting toxic effect was bone marrow suppression. At the low doses used here to induce remission, serious marrow suppression was not observed. The contrasting side effects of 2-chlorodeoxyadenosine and deoxycoformycin are not surprising; they are consistent with the divergent pharmacologic actions of the two agents. A tight binding inhibitor of adenosine deaminase, deoxycoformycin can elevate plasma levels of deoxyadenosine and adenosine, with resultant inhibition of S-adenosyl-L-homocysteine hydrolase and potential changes in the function of adenosine receptors.12 13 14 15 16 17 2-Chlorodeoxyadenosine, by contrast, is a deoxyadenosine analogue that has no direct effect on S-adenosyl-L-homocysteine metabolism18 or adenosine receptors.
Although not yet commercially available, 2-chlorodeoxyadenosine is quite simple to synthesize in large quantity; availability should not be a problem, as it has been with deoxycoformycin. Its toxicity, not only in the present series but in a much larger group of patients with chronic lymphocytic leukemia and non-Hodgkin's lymphoma, has proved remarkably low. These considerations suggest that 2-chlorodeoxyadenosine may well be the drug of choice in the treatment of hairy-cell leukemia. The duration of remission in the first patients that we treated has been remarkably long, especially in view of the fact that only a single seven-day course of the drug was given. The malignant clone in hairy-cell leukemia appears to be one that proliferates very slowly. Thus, if relapses occur, they may be quite late. It will take a considerably longer follow-up of these patients to determine whether an actual cure can be achieved. We believe that the theoretical risk of late toxic effects, such as prolonged immunosuppression or second neoplasms, is relatively low because of the high percentage of remissions achieved with a single low-dose course of therapy. In the future, further Phase II testing and Phase III comparison trials will be necessary to compare the efficacy and toxicity of 2-chlorodeoxyadenosine and deoxycoformycin in hairy-cell leukemia.
Supported by grants (FD-R-000280, GM23200, and MOI RR00833) from the National Institutes of Health, a Clinical Investigator Award (CA01100), and the Alec Tapper Memorial Cancer Fund.
We are indebted to Drs. William Miller, Charles Kossman, James Holbert, Fred Williams, Zella Zeigler, Hope Rugo, Curt Ries, Michael Boxer, and Mark Adler; to Patricia A. Morin, R.N.; and to the staff of the General Clinical Research Center for their assistance with this study; and to Dr. Robert Lukes for his review of some of the slides.
Source Information
From the Department of Molecular and Experimental Medicine, Research Institute of Scripps Clinic, Scripps Clinic and Research Foundation, La Jolla, Calif. Address reprint requests to Dr. Piro at 10666 N. Torrey Pines Rd., La Jolla, CA 92037.
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