INTRODUCTION — Adult T cell leukemia-lymphoma (ATL) is a peripheral T cell neoplasm associated with infection by the human T-lymphotropic virus, type I (HTLV-1). Although it is considered one of the highly aggressive T cell non-Hodgkin lymphoma (NHL) variants, the disease course is variable and sometimes quite indolent.
Four clinical variants of ATL have been described: acute, lymphoma-type (lymphomatous), chronic and smoldering; these appear to have differing genomic alterations and varying clinical courses, and may require different treatment.
The treatment of ATL is discussed here. The epidemiology, pathogenesis, clinical features, pathology, and diagnosis of ATL are discussed separately. (See "Clinical manifestations, pathologic features, and diagnosis of adult T cell leukemia-lymphoma".)
INDICATIONS FOR TREATMENT — As mentioned above, there are four clinical variants of ATL: acute, lymphoma-type, chronic, and smoldering [1,2]. These differ greatly in their presentation and prognosis. Therapy is usually offered to patients with acute, lymphoma-type, or unfavorable chronic type ATL while patients with typical chronic or smoldering ATL are observed initially. This is principally because conventional chemotherapy does not appear to improve the survival of patients with chronic or smoldering ATL [3,4]. The five-year survival rate of patients with chronic and smoldering ATL was 47 percent in one study [5].
As an example, a retrospective evaluation of 26 patients with smoldering ATL reported that 14 (54 percent) were alive without tumor progression at median follow-up of 6.5 years [4]. For those who died, the median time to transformation to a more aggressive variant was 38 months.
In contrast, most patients with acute or lymphoma-type ATL have a survival without treatment measured in days to weeks. A brief description of the clinical variants of ATL is given below. This is described in more detail separately. (See "Clinical manifestations, pathologic features, and diagnosis of adult T cell leukemia-lymphoma".)
PRETREATMENT EVALUATION — The pretreatment evaluation both determines the bulk of disease and provides information about the individual's comorbidities that are likely to have an impact on treatment options. In addition to a history and physical examination, it is our practice to perform the following pretreatment studies in patients with ATL [6]:
General approaches to the diagnostic work-up and staging of non-Hodgkin lymphoma are presented separately (table 1). (See "Clinical presentation and diagnosis of non-Hodgkin lymphoma" and "Initial evaluation and staging of non-Hodgkin lymphoma".)
INITIAL TREATMENT
Overview — Patients with acute, lymphomatous, or unfavorable chronic type ATL progress quickly without treatment and have a median overall survival measured in months. Treatment of these variants has been challenging since the tumor cells have an intrinsic resistance to most chemotherapeutic agents and because the patients have an underlying immunocompromised state associated with their HTLV-1 infection. Cell-mediated immunity is impaired in ATL patients while humoral immunity remains intact.
The greatest experience with ATL comes from the Japan Clinical Oncology Group (JCOG). The best treatment for these patients is unclear and patients should be enrolled in clinical trials whenever possible. However, for patients who are not eligible for a clinical trial or for those who do not wish to participate in a trial, we offer the following guidelines. Combination chemotherapy, as described in the next section, is the main treatment option [6,11]. When added to conventional therapy, the defucosylated humanized anti-CCR4 antibody mogamulizumab appears to improve response rates and progression-free survival, but is not widely available outside of Japan. Autologous hematopoietic cell transplantation (HCT) does not appear to be effective. Allogeneic HCT may be appropriate for patients with a related or unrelated donor.
Multiagent regimens — The optimal chemotherapy combination for patients with ATL is unclear and many intensive regimens have been investigated [3,12-17]. Patients may initially respond to treatment with combination chemotherapy regimens devised for advanced, aggressive NHL, but relapses are common [18]. The median survival time for patients with acute, lymphoma-type, or unfavorable chronic type ATL treated in prospective trials that employed multiagent chemotherapy has ranged from 5 to 13 months.
Of those evaluated in prospective trials, the regimen that appears to result in the longest median survival is VCAP-AMP-VECP (also known as LSG15), which includes treatment with vincristine, cyclophosphamide, doxorubicin, prednisone, ranimustine, vindesine, etoposide, and carboplatin [11]. The use of VCAP-AMP-VECP is supported by prospective phase II and III trials [16,17]:
All patients with acute, lymphoma-type, or unfavorable chronic type ATL should be treated with combination chemotherapy. Given a 10 to 25 percent risk for involvement of the central nervous system (CNS) at diagnosis or relapse, we recommend that all patients receive intrathecal chemotherapy for CNS prophylaxis [20,21]. The evidence supporting this recommendation is discussed elsewhere. (See "Secondary involvement of the central nervous system by non-Hodgkin lymphoma".)
We suggest the use of VCAP-AMP-VECP plus intrathecal chemotherapy rather than other regimens of combination chemotherapy. When available, we suggest the addition of mogamulizumab to VCAP-AMP-VECP. This regimen requires six to eight months of weekly chemotherapy with G-CSF support. The trials supporting the use of this regimen enrolled patients up to the age of 69 years. The ranimustine and vindesine used in this regimen are not available in some countries, including the United States. For patients treated by clinicians who do not have access to these agents, an acceptable alternative regimen is hyperfractionated cyclophosphamide, vincristine, doxorubicin, and dexamethasone (hyper-CVAD). While hyper-CVAD is frequently used to treat other forms of T cell lymphoma, there are limited data regarding the use of hyper-CVAD for the treatment of ATL [22].
Although some investigators have reported anecdotal experiences suggesting the efficacy of oral etoposide, the evidence supporting its efficacy is inadequate, and most patients with aggressive subtypes of ATL cannot be controlled with oral etoposide for a clinically meaningful duration [23,24].
Elderly patients — As previously noted, VCAP-AMP-VECP plus intrathecal chemotherapy is associated with significant toxicity. Elderly patients (principally those older than 70 years of age) are less able to tolerate this aggressive regimen. Thus, for patients over 70 years old, we suggest the use of CHOP or CHOP-like regimens, based on the subgroup analysis of the phase III study described above [17].
Supportive factors — The treatment of patients with ATL requires close attention to the following issues that often surround chemotherapy administration:
Antiviral therapy — The benefit of antiviral agents in ATL is controversial. The HTLV-1 virus is thought to be in a latent state in patients with ATL and so antiviral agents, if active, would be expected to act through a mechanism other than antiviral activity [26]. Small, prospective trials and retrospective analyses performed outside of Japan have evaluated the use of the antiviral agent zidovudine (AZT) plus interferon alpha in the treatment of newly diagnosed or relapsed ATL [27-33]. Median survival times with this regimen have ranged from 6 to 18 months. Some of these trials included patients with less aggressive variants of ATL who would be expected to have a good prognosis without any treatment.
A 2010 meta-analysis of AZT plus interferon-alpha incorporated data from 245 patients with acute (47 percent), chronic (7 percent), smoldering (4 percent), or lymphoma-type (42 percent) ATL [34]. For the 207 patients whose first-line therapy was recorded, the following five-year overall survival rates were reported:
Patients with acute, chronic, and smoldering ATL appeared to benefit from first-line antiviral therapy, whereas patients with lymphoma-type ATL did not. For patients with chronic or smoldering ATL, this combination was reported to result in 100 percent five-year survival. Based on the results of this retrospective analysis, the investigators suggested this combination regimen as the first-line therapy in leukemic subtypes of ATL [35]. While encouraging, we believe that this approach needs further prospective study before it can be widely applied.
Hematopoietic cell transplantation — Both autologous and allogeneic hematopoietic cell transplantations (HCTs) have been attempted to improve outcomes in patients with ATL. Although experience is somewhat limited, autologous HCT does not appear to be of benefit due to frequent early relapses [36]. Allogeneic HCT offers a potential graft-versus-leukemia effect and may be considered for patients with an available donor [37,38].
A number of small non-randomized studies have evaluated the role of myeloablative and nonmyeloablative allogeneic HCT in this disorder [37,39-43]. Treatment-related mortality was high, although long-term survival was achieved in some patients, with evidence of a graft-versus-HTLV-1 and a graft-versus-tumor effect [41,44]. After allogeneic HCT, provirus load was significantly decreased in some patients [41,45], suggesting that anti-HTLV-1 immune response is enhanced in these patients. Phase II studies of nonmyeloablative and myeloablative allogeneic HCT are underway in Japan [3,46,47].
Retrospective data are available from Japan regarding 386 patients with ATL who underwent allogeneic HCT from an HLA-matched related donor (154 patients), HLA-mismatched related donor (43 patients), unrelated marrow donor (99 patients), or unrelated cord blood donor (90 patients) [48]. After a median follow-up of 41 months, the estimated three-year survival rate was 33 percent. Four factors were significantly associated with worse outcomes: age >50 years, male sex, disease not in complete remission at the time of HCT, and unrelated donor source.
In another analysis of this patient cohort, patients who developed either mild to moderate (grade 1/2) or severe (grade 3/4) acute graft-versus-host disease (GVHD) had a significantly lower disease-related mortality when compared with those patients who did not develop GVHD [49]. Patients with grade 1/2 GVHD had superior overall survival than those without GVHD (hazard ratio [HR] 0.65; 95% CI 0.45-0.93). In contrast, survival was inferior in patients with grade 3/4 GVHD (HR 1.64; 95% CI 1.10-2.42), likely due to an increase in treatment-related mortality (HR 3.50; 95% CI 2.01-6.11).
In another analysis, this cohort was expanded to include 586 patients with ATL who underwent allogeneic HCT between 1992 and 2009 [50]. For the 280 patients who underwent myeloablative conditioning, median overall survival (OS) and estimated three-year survival were 9.5 months (95% CI 6.7-18.0 months) and 39 percent (33 to 45 percent), respectively. Corresponding values for the 306 patients who underwent reduced intensity conditioning were 10 months (7.2 to 14.0 months) and 34 percent (29 to 40 percent), respectively. When compared with myeloablative conditioning, reduced intensity conditioning was associated with a trend towards less treatment-related mortality (HR 0.786; 95% CI 0.538-1.148), but greater leukemia-related mortality (HR 1.579; 95% CI 1.080-2.308).
Another retrospective analysis included 40 patients with acute or lymphoma-type ATL who had undergone allogeneic HCT either as part of their initial therapy or at relapse [37]. All but one of the patients was treated with a myeloablative conditioning regimen. At the time of transplant, 15 were in CR, 13 in PR, 3 had stable disease, and 9 had progressive disease. Of the patients evaluable after HCT, all but one achieved a CR. The median survival time of all cases after HCT was 9.6 months. There were 16 deaths related to transplant. The three-year rates of overall survival and relapse-free survival were 45 and 34 percent, respectively. Acute and chronic graft-versus-host disease developed in 26 and 15 patients, respectively. Among the 10 patients who relapsed after HCT, five were able to achieve a second CR. Three of these CRs were obtained by reduction or cessation of immunosuppressive therapy alone suggesting a graft-versus-ATL effect.
PATIENT FOLLOW-UP — After completion of the initially planned treatment of ATL, patients should be evaluated to determine the disease response to treatment and should be followed longitudinally for relapse.
Patients with ATL are immunocompromised and are therefore at risk for potentially lethal opportunistic infections with organisms such as Pneumocystis jirovecii (previously carinii), Candida, cytomegalovirus, and Strongyloides stercoralis [3]. While prophylaxis for such infections is generally given, clinicians need to consider these organisms when patients decompensate. (See "Epidemiology, clinical manifestations, and diagnosis of Pneumocystis pneumonia in non-HIV-infected patients" and "Strongyloidiasis" and "Diagnosis of cytomegalovirus" and "Overview of Candida infections".)
Response evaluation — One month following the completion of planned therapy (or sooner if the outcome is unfavorable), the response to treatment should be documented by history, physical examination, and laboratory studies (complete blood count, lactate dehydrogenase, and biochemical profile). The post-treatment imaging study of choice in patients remains computed tomography (CT). Although positron emission tomography (PET) scans have not been prospectively validated in patients with ATL, we perform a combined PET/CT, if available.
Using information gathered from the history, physical, and CT scan, disease response is determined using the Japan Clinical Oncology Group (JCOG) response criteria [6]:
Patients who fail to obtain a complete response are treated as refractory disease. This is discussed below. (See 'Treatment of recurrent or refractory disease' below.)
Surveillance for relapse — Following the completion of therapy, restaging, and documentation of complete remission, patients are seen at periodic intervals to monitor for treatment complications and assess for possible relapse. The frequency and extent of these visits depends upon the comfort of both the patient and physician. There have been no prospective, randomized trials comparing various schedules of follow-up. Our approach is based upon the following general understandings:
Our approach to patient surveillance is to schedule patient visits monthly during the first year, every two months during the second year, and every three months starting two years after complete response. At these visits, we perform a history and physical examination, complete blood count with differential, evaluation of the peripheral smear, chemistries, LDH, and flow cytometry for CD4, CD8, and CD25 [51].
It is recommended that relapsed disease suggested by changes on imaging be confirmed by biopsy. As such, a biopsy is recommended to document relapsed disease before proceeding to salvage therapy.
In some patients with ATL relapse occurs as the appearance of leukemic cells in the peripheral blood alone. In addition, it is sometimes difficult to recognize leukemic cells by morphology alone. In such situations, flow cytometry of the peripheral blood mononuclear cells, especially evaluating the T4:T8 ratio, is easily performed and effective for estimating the leukemic cell kinetics in the peripheral blood. In particular, since ATL cells show a characteristic phenotype that is both CD4 and CD25 positive, flow cytometry can be performed in most cases to identify leukemic cells in the peripheral blood.
TREATMENT OF RECURRENT OR REFRACTORY DISEASE — There is little information on the treatment of recurrent or refractory ATL and patients should be referred for enrollment in clinical trials. Although not widely available outside of Japan, mogamulizumab is well tolerated and active in this setting. Other areas of investigation include the use of antiviral agents or antibody therapy. Patients who have undergone allogeneic hematopoietic cell transplantation (HCT) may respond to withdrawal of immunosuppression or immunotherapy with donor lymphocyte infusion (DLI). (See 'Antiviral therapy' above and 'Hematopoietic cell transplantation' above and "Immunotherapy for the prevention and treatment of relapse following hematopoietic cell transplantation".)
ATL cells express CCR4 on the surface [52]. A defucosylated humanized anti-CCR4 antibody (mogamulizumab) has been reported to be effective to ATL cases and has been approved for use in Japan [53,54]. A multicenter phase II trial evaluated the use of mogamulizumab monotherapy in 28 patients with relapsed acute (52 percent), lymphomatous (22 percent), or chronic (26 percent) ATL [54]. Toxicity was mostly mild to moderate with the most common toxicities being infusion reactions (89 percent) and rash (63 percent). The overall response rate was 50 percent (29 percent complete) and median progression-free and overall survival of 5.2 and 13.7 months, respectively.
Limited experience with the anti-CD52 antibody alemtuzumab has also been reported [55,56]. There has also been interest in the use of arsenic trioxide with or without interferon alpha and in the use of all-trans retinoic acid (tretinoin) [32,57-59]. Other new agents for the potential application to the treatment of ATL include pralatrexate (anti-folate), bortezomib (proteasome inhibitor), forodesine (purine nucleoside phosphorylase inhibitor), histone deacetylase inhibitor, and lenalidomide [47].
There is a paucity of data regarding the efficacy of radiation therapy in patients with ATL. A retrospective analysis of 10 consecutive patients with relapsed or refractory ATL treated with radiation therapy (mean 35.4 Gy; range 12 to 60 Gy) reported that all patients had an at least partial response with 40 percent attaining a complete response within the treatment field [60]. Toxicity was generally mild to moderate and included cutaneous reactions, mucositis, and ocular toxicity. Radiation therapy may provide palliation of patients who have symptoms related to a single disease site.
In a retrospective analysis of 35 patients with relapsed or refractory ATL following allogeneic HCT, the median time to relapse was less than four months [38]. The median survival time following relapse was 6.2 months and 19 percent of patients were alive at three years. A complete remission (CR) was attained in 2 of 29 patients following withdrawal of immunosuppression, and in 4 of 9 patients following DLI with or without prior cytoreductive therapy. Six patients had discontinued immunosuppressive therapy prior to relapse. Of these, the three with local recurrence attained a CR with cytoreductive therapy, while the three with systemic recurrence progressed despite cytoreductive therapy. A worsening of graft-versus-host disease (GVHD) was seen in 6 of 9 patients receiving DLI.
PROGNOSIS — As described separately, there are four clinical variants of ATL: acute, lymphoma-type, chronic, and smoldering. These differ greatly in their presentation and prognosis. The clinical course of acute and lymphoma-type ATL is aggressive with survival without treatment measured in months. In contrast, most cases of chronic or smoldering ATL are more indolent with survival without treatment measured in years. (See 'Indications for treatment' above.)
Prognostic indices used for other non-Hodgkin lymphomas, such as the International Prognostic Index, are not very useful in this patient population, largely because the vast majority of patients would be classified as having intermediate- or high-risk [61]. As such, efforts have been made to develop and validate a prognostic index specific for patients with acute or lymphoma-type ATL.
A retrospective Japanese study of 807 patients with newly diagnosed acute or lymphoma-type ATL diagnosed between 2000 and 2009 randomly divided subjects into two groups that were used to create and validate a prognostic index for acute and lymphoma-type ATL (the ATL-PI) [61]. The median survival was 7.7 months overall. A point-based system was developed using the presence or absence of the following markers of poor outcome in the training group:
Total scores ranged from zero to six. This prognostic model separated the validation group into three populations with different outcomes: high (5 or 6 points), intermediate (3 or 4 points), and low (0, 1, or 2 points) risk groups that had median survival times of 4.6, 7.0, and 16.2 months, respectively. Corresponding rates of overall survival at two years were 6, 17, and 37 percent, respectively.
SUMMARY AND RECOMMENDATIONS
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