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Stem cell transplantation for T-cell lymphomas in Taiwan

Abstracts

T-cell lymphomas are generally aggressive malignancies with poor prognosis. There are no standard treatment guidelines for T-cell lymphomas, and the timing of stem cell transplantation (SCT) is not well known. In this study, we investigated the outcomes of Taiwanese patients with T-cell lymphomas after SCT. We retrospectively analyzed 131 patients with T-cell lymphomas receiving SCT (autologous: 90, allogeneic: 41) from 2009 to 2014. More autologous SCT recipients were ALCL or in complete remission, and more allogeneic recipients had advanced disease. 56 patients who were sensitive to chemotherapy underwent SCT as upfront setting. The 2-year PFS and OS rates were 67.0 and 64.5%, respectively. Regarding disease status before transplantation, patients with CR1 had the best outcomes. Among different subtypes, patients with natural killer/T-cell lymphomas showed the worst outcomes, with 2-year OS rate of 23.5%. The OS rates for the other three major subtypes were as follows: 72.9% for ALCL; 75.0% for AITL; and 51.4% for PTCL-NOS. For more rare subtypes, such as ATLL and SPTCL, data from our study show that SCT can be beneficial. We concluded that upfront autologous SCT is feasible and effective for patients with low PIT, and disease status at transplant is the strong predictor of outcome.

Introduction

T-cell lymphomas are heterogeneous malignancies that account for 15–20% of all lymphomas [1]. The major subtypes of T-cell lymphomas have been found to geographically vary and have been investigated by the International Peripheral T-cell Lymphoma Project, which involves 22 centers worldwide and consists of participants from North America, Europe, and Asia. In North America and Europe, PTCL not otherwise specified (PTCL-NOS) is the most common subtype. Natural killer/T-cell lymphoma (NKTCL) and adult T-cell leukemia/lymphoma (ATLL) are more common in Asia, especially in the area where human T-cell leukemia virus type I is endemic [2]. In Taiwan, according to the Taiwan Cancer Registry, there are about 330 new cases of T-cell lymphoma every year that account for 10–15% of the non-Hodgkin lymphoma cases, and PTCL-NOS (28%), NKTCL (18%), and angioimmunoblastic T-cell lymphoma (AITL) (14%) represent the three most common subtypes of T-cell lymphomas (Fig. 1) [3].

Fig. 1
figure1

Relative incidence of T-cell lymphoma subtypes in Taiwan

T-cell lymphomas are generally aggressive malignancies and have a poor prognosis compared with their B-cell counterparts. First-line chemotherapy often consists of CHOP (cyclophosphamide, doxorubicin, vincristine, and prednisolone) or CHOP-like regimens. However, except for patients with anaplastic lymphoma kinase (ALK)-positive anaplastic large-cell lymphoma (ALCL), who have better outcomes, patients with other types of T-cell lymphomas still have very limited long-term disease-free survival despite aggressive chemotherapy [4].

Currently, there are no established standard treatment guidelines for T-cell lymphomas. For better outcomes, several studies were performed on patients with T-cell lymphomas in which patients receiving autologous or allogeneic stem cell transplantations (SCTs) had longer remission periods compared with those treated with chemotherapy. Most of these reports came from western countries, but few have been prepared in Japan [5,6,7]. Key questions still exist, including the identification of ideal candidates, optimal SCT timing, and the potentially different efficacy of autologous and allogeneic SCTs. Due to the heterogeneous distribution of T-cell lymphomas in different areas, we chose to investigate the clinical outcomes in patients with T-cell lymphomas after SCT in Taiwan to address the lack of data published to date.

Materials and methods

Study design

We retrospectively analyzed data collected by the Taiwan Society of Blood and Marrow Transplantation. Altogether, 15 hospitals in Taiwan participated in this registration study. A total of 131 patients with T-cell lymphoma were included in this study; they received SCT between January 2009 and December 2014. All patients gave their written informed consent for treatment. Each pathology report was classified according to the 2008 edition of the WHO classification of lymphoid neoplasms. The patients received either autologous or allogeneic SCT depending on the attending physician’s clinical judgment based on unfavorable prognostic factors, such as high-risk T-cell lymphomas, refractory or relapsed disease, and underlying medical status.

SCT regimens

We characterized myeloablative and reduced intensity conditioning (RIC) regimens by conditioning regimen intensity according to established criteria [8]. The myeloablative regimens used included Bu/Cy (busulfan and cyclophosphamide) and Cy/TBI (cyclophosphamide and total body irradiation). The RIC regimens included the combinations of fludarabine with melphalan, cyclophosphamide, or busulfan.

Response criteria and statistical analysis

We assessed the treatment response to chemotherapy and SCT according to the International Workshop Criteria [9]. First complete remission (CR1) was defined as complete remission (CR) after primary chemotherapy, and primary refractory CR or relapsed chemosensitive CR was defined as CR2 after salvage chemotherapy. Primary induction failure (PIF) and sensitivity to chemotherapy were defined as a partial response (PR) to treatment without reaching CR. Relapse was defined as the recurrence of lymphoma after CR. Progression-free survival (PFS) was defined as the time from the date of transplant to the date of progression/relapse or death, and overall survival (OS) was defined as the time from the date of transplant until death from any cause. Nonrelapse mortality (NRM) was defined as death without evidence of lymphoma progression or relapse. The response to SCT was regularly evaluated after transplantation by imaging modalities and clinical observation. OS and PFS were estimated using the Kaplan–Meier method.

Results

Patient characteristics

A total of 131 T-cell lymphoma patients who received autologous (n = 90) or allogeneic (n = 41) SCT were included in this study. The major histological subtypes were PTCL-NOS (n = 35), ALCL (n = 29), AITL (n = 20), and NKTCL (n = 19). Other subtypes of lymphoma (n = 28) included subcutaneous ATLL (n = 9), panniculitis-like T-cell lymphoma (SPTCL; n = 7), enteropathy-associated T-cell lymphoma (EATL) (n = 2), hepatosplenic T-cell lymphoma (HSTCL) (n = 2), post-transplant lymphoproliferative disease (PTLD) (n = 2), and CD8-positive epidermotropic cytotoxic T-cell lymphoma (n = 1). Five patients had T-cell lymphoma without detailed histological subtypes. Most patients received CHOP or CHOP-like regimen as their first-line chemotherapy. All patient characteristics are listed in Table 1.

Table 1 Characteristics of patients

Due to some lymphoma subtypes having low patient numbers, we mainly focused on PTCL-NOS, ALCL, AITL, and NKTCL, which comprised 78.6% of the 131 patients. ALCL histology occurred more frequently among the recipients of autologous SCT than among the allogeneic SCT recipients (28.9 vs. 7.3%, respectively), and most of them received SCT in complete remission (58.9 vs. 26.8%, respectively). Allogeneic SCT recipients were more likely to have advanced (Ann Arbor stage III–IV) disease compared to patients receiving autologous SCT (92.7 vs. 68.9%, respectively).

Myeloablative conditioning was used more commonly than RIC in allogeneic SCT (88 vs. 12%, respectively). The graft source was peripheral blood for all patients. Transplantation-related characteristics are listed in Table 2.

Table 2 Transplantation-related characteristics

Outcome by lymphoma subtype

PFS and OS were further analyzed by lymphoma subtype. With a median follow-up of 21.2 months for the entire group, among the four major subtypes, patients with NKTCL had the worst outcomes, with 2-year PFS and OS rates of 44.9% [95% confidence interval (CI) 17.5–62.3%] and 23.5% (95% CI 0–48.9%), respectively. Nine patients experienced relapse and eventually died of the disease, two patients died of acute graft-versus-host disease (GVHD), and one patient succumbed to infection. The PFS and OS rates for the other three subtypes were as follows: 57.1% (95% CI 36.9–77.3%) and 72.9% (95% CI 53.1–86.7%) for ALCL; 84.7% (95% CI 68.5–100%) and 75.0% (95% CI 52.0–98.0%) for AITL; and 51.6% (95% CI 32.2–71.0%) and 51.4% (95% CI 33.4–69.4%) for PTCL-NOS (Fig. 2). The relapse rates among patients with PTCL, NOS, ALCL, and AITL were 42.9, 41.3, and 15%, respectively. Detailed patient characteristics are listed in Table 3.

Fig. 2
figure2

a PFS by T-cell lymphoma subtype. b OS by T-cell lymphoma subtype

Table 3 Patient’s characteristics according to different subtypes

Outcome by disease status

Regarding disease status before transplantation, patients with CR1 had the best outcomes, with 2-year PFS and OS rates of 80.5% (95% CI 37.4–91.4%) and 66.0% (95% CI 40.4%–91.7%), respectively. Patients with relapsed disease had poor 2-year OS rates (49.2% for patients who were sensitive to chemotherapy and 33.3% for those who were not) (Fig. 3). Among six patients with relapsed disease who were refractory to chemotherapy, five patients experienced disease relapse after SCT with inferior outcomes. As for patients with CR1, ≥CR2, PIF, and relapsed disease but sensitive to chemotherapy, the relapse rates were 15.8, 28.9, 32.4, and 62.5%, respectively.

Fig. 3
figure3

a PFS by different disease status. b OS by different disease status

Fifty-six patients (PTCL-NOS: 18, AITL: 10, ALCL: 8, NKTCL: 7, ATLL: 8, others: 5) who were sensitive to chemotherapy underwent SCT during CR1 (n = 19) or PIF (n = 37) as upfront setting. The 2-year PFS and OS rates were 67.0% (95% CI 51.8–82.4%) and 64.5% (95% CI 51.1–78.1%), respectively. Twenty-nine patients received autologous SCT, and 27 patients received allogeneic SCT. Allogeneic SCT recipients more commonly had advanced disease (85.2% with stage IV disease compared with 48.4% in the autologous SCT group), and more autologous SCT recipients were in CR (44.8%, compared with 23.2% in the allogeneic SCT group). The relapse rate was similar in the autologous (27.6%) and allogeneic (25.9%) groups. Seven autologous SCT recipients died due to relapsed disease (n = 3), sepsis (n = 2), pneumonia (n = 1), or secondary malignancy (n = 1, acute myeloid leukemia). Thirteen allogeneic SCT recipients died of relapsed disease (n = 7), sepsis (n = 2), acute GVHD (n = 2, 47, and 74 days after transplant), fungal pneumonia (n = 1), and of unknown cause (n = 1). Among the different subtypes, all patients with AITL (n = 10) receiving SCT (autologous: 8; allonegeic: 2) remained disease-free. Six patients with PTCL-NOS, two patients with ALCL, and three patients with NKTCL experienced relapse.

Autologous vs. allogeneic transplantation

Autologous SCT recipients had 2-year PFS and OS rates of 56.0% (44.0–68.0%) and 62.6% (51.0–74.2%). Altogether, 36 patients (40%) experienced relapse after autologous SCT during the follow-up period. The rate of NRM was 6.7% (n = 6). Five patients died due to infection (four patients died within 100 days of transplant) and one patient developed acute myeloid leukemia after 45 months. Eleven patients received a second SCT (one autologous and ten allogeneic SCT), but only one allogeneic SCT recipient remained disease-free and alive. Three patients died due to relapsed disease and the other seven patients due to infection (bacterial infection: 4; hepatitis B flare-up: 2; cytomegalovirus pneumonitis: 1).

The 2-year PFS and OS rates for allogeneic SCT recipients were 66.4% (50.0–82.8%) and 47.2% (30.2–64.2%), respectively (Fig. 4). Twelve patients (29.2%) relapsed and 11 died due to disease progression. One patient underwent a second allogeneic SCT, but still experienced disease progression. Other causes of death included infection (n = 5), GVHD (n = 2), and undetermined causes (n = 2), resulting in an NRM rate of 21.9%. Regimen intensity (myeloablative conditioning, n = 28; RIC, n = 13) had no impact on overall survival.

Fig. 4
figure4

a PFS by different types of transplantation. b OS by different types of transplantation. (Color figure online)

Rare lymphoma subtypes

Other subtypes of lymphoma (n = 28) included ATLL (n = 9), SPTCL (n = 7), EATL (n = 2), HSTCL (n = 2), PTLD (n = 2), and CD8-positive epidermotropic cytotoxic T-cell lymphoma (n = 1).

Eight ATLL patients received allogeneic SCT and one received autologous SCT, and all of them had the acute variant of the disease. The autologous SCT recipient underwent transplant in the CR1 state and has remained disease-free for 7 months so far. Seven patients in PR and one patient with relapsed disease resistant to chemotherapy received allogeneic SCT. Four patients remain disease-free and alive, and three patients have survived for >4 years. Three patients died due to relapsed disease with a median OS of 3.7 months, and one patient died due to acute GVHD at 74 days after transplant.

Of the seven SPTCL patients, four received allogeneic SCT with RIC and three received autologous SCT. One patient was in CR1, three in CR2, one in PR, and two with relapsed disease. One patient died 270 days after allogeneic SCT due to infection (pulmonary Mycobacterium avium intracellular complex infection), and one patient experienced relapse after autologous SCT, but survived after salvage chemotherapy at the last follow-up point. The other five patients remained in remission with a median follow-up time of 23 months (9.6–60 months).

Discussion

For chemosensitive relapsed or refractory aggressive B-cell lymphomas, SCT has proved to be beneficial, with a long-term survival rate of 50% [10]. However, the role of SCT in PTCLs was not clear. Also, considering the high relapse rates of T-cell lymphomas, it is common for many patients to receive more than two lines of chemotherapy before SCT. Such late referral has been considered unfavorable, and front-line SCT is expected to solve this problem. Due to the rarity and heterogeneity of T-cell lymphomas, randomized trials on SCT are still lacking. However, some trials have suggested that SCT has advantages for T-cell lymphomas. According to several retrospective and prospective trials, autologous SCT is safe and beneficial to chemosensitive disease; however, patients with chemorefractory disease still have a poor prognosis after SCT [5, 11,12,13,14,15,16]. Upfront autologous SCT seems to improve long-term PFS for patients achieving CR or PR before SCT [17, 18]. Allogeneic SCT is considered a curative treatment modality with a graft versus lymphoma effect, but the role of upfront allogeneic SCT is not clear considering its relative higher rates of NRM. Some trials have demonstrated that allogeneic SCT can prolong the OS of patients with relapsed or refractory disease to 35–50% at a follow-up period of 3–5 years [15, 19, 20].

In the present study, we retrospectively analyzed the clinical information and outcome of SCT in a total of 131 patients from 15 hospitals in Taiwan between 2009 and 2014. Compared to the autologous group, in the allogeneic group, there were more patients with high-risk features, such as non-ALCL histology, bone marrow involvement, advanced stage at diagnosis, relapsed disease, and refractory to chemotherapy. The 2-year PFS and OS in autologous SCT recipients were 56.0 and 62.6%, respectively, compared to 66.4 and 47.2% in the allogeneic group. Relapse rate was higher in the autologous group (40 vs. 29.2%), and NRM was higher in the allogeneic group (21.9 vs. 6.7%). Although allogeneic SCT did not result in a survival benefit compared with autologous SCT, the patients in the allogeneic SCT group had more advanced disease with a lower relapse rate. For fit patients with advanced disease, allogeneic SCT may provide better disease control without increased toxicity.

In the analysis by disease status before SCT, patients in CR1 had the best outcomes. The cases included in the present study may have been heterogeneous, but the outcomes were comparable to those in previous studies and superior to those achieved with conventional chemotherapy [2, 5, 14, 15, 17]. We had also included the international prognostic index (IPI), prognostic Index for T-cell lymphoma (PIT), and bone marrow involvement at diagnosis in our analyses, but these showed no impact on PFS and OS. Some studies had identified high PIT (PIT: 3–4) as a significant risk factor of poor prognosis after transplantation [17, 21, 22], which was not shown in our study possible due to the small number of patients.

Fifty-six patients received SCT upfront in their first CR or PR, and the 2-year PFS and OS rates were 67.0 and 64.5%. It is noteworthy that all patients with AITL (n = 10) receiving SCT remained disease-free during the follow-up period. Due to the small size of our patient group, we cannot determine if reaching CR or PR before undergoing SCT has a clinical impact on the outcome.

Among the different subtypes, the patients with NKTCL had the worst outcome with a relapse rate of 47.3% (9 out of 19 patients relapsed after SCT). Compared to the poor median survival of relapsed/refractory NKTCL [2], SCT is still the first consideration for salvage therapy [23, 24].

Considering the more rare subtypes of lymphoma, nine patients with ATLL and seven patients with SPTCL who received SCT were included in the present study. Acute ATLL is an aggressive disease due to chemoresistance and severe immunosuppression. These patients may still benefit from chemotherapy induction with concurrent or sequential antiretroviral therapy, but with a high relapse rate [25]. A large Japanese study included 1792 ATLL patients defining a new risk stratification system (risk factors include acute variant, ECOG performance status 2-4, adjusted Ca ≥ 12 mg/dL, C-Reactive Protein ≥ 2.5 mg/dL and soluble IL-2 receptor > 5000 U/mL) to identify patients who may benefit from upfront allogeneic SCT [26]. The use of anti-CCR4 antibody Mogamulizumab before allogeneic SCT significantly worsens clinical outcome mainly because of an increased risk of severe/corticosteroid-refractory acute GVHD [27]. In the present study, five patients with acute ATLL remained in remission after SCT during a median follow-up time of 24 months, and three patients have survived for more than 3 years. Due to the rarity of SPTCL, there have been few reports on this condition; however, autologous or allogeneic SCT following high-dose chemotherapy has been considered an important treatment option for refractory or relapsed SPTCL [28,29,30]. In the present study, three patients with SPTCL received autologous SCT and four received allogeneic SCT, and the indications for SCT were either advanced (stage VI) or relapsed/refractory disease. Five patients remained in remission after a median follow-up time of 23 months. Considering the poor prognosis of patients with ATLL and SPTCL, even under intensive chemotherapy, SCT is considered an effective treatment in suitable patients.

Our study has several limitations. Due to the analysis being retrospective and the rarity of T-cell lymphomas, there are data missing from part of our patients’ clinical information, such as initial IPI, PIT score, the ALK status of ALCL patients, and the heterogeneity of our patient group. Among all patients, only four had high PIT (PIT: 3–4), and thus our study can suggest the effectiveness of SCT in patients with lower PIT (PIT: 0–2) but not with high PIT (PIT: 3-4), which were similar with previous published data [17, 21, 22]. However, because the disease has distinct clinical presentations in different geographic regions, our results may represent clinical practice for patients with T-cell lymphomas in Taiwan. CR1 is a strong predictor of longer survival. Regarding up-front SCT, autologous SCT seems to be feasible and safe for patients with lower PIT, but the benefits of more aggressive allogeneic SCT are still unclear. Future research into allogeneic SCT should aim to simultaneously reduce NRM and improve OS. Considering the poor outcome of SCT in patients with relapsed disease, early referral should be considered for high-risk patients. Among the different histological subtypes, the poor outcomes in patients with NKTCL cannot be overcome by either autologous or allogeneic SCT. For the more rare subtypes, such as ATLL and SPTCL, although the present study included only a few cases, data from our study as well as previous reports show that SCT can be beneficial.

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Hsu, YT., Tsai, HJ., Chang, J.S. et al. Stem cell transplantation for T-cell lymphomas in Taiwan. Bone Marrow Transplant 53, 993–1000 (2018). https://doi.org/10.1038/s41409-018-0116-6

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