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Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 3  |  Issue : 1  |  Page : 3-12

Clinicopathological characteristics, prognostic factors, and outcomes in peripheral T-cell lymphoma: Experience from a single center in India


1 Department of Medical Oncology, Cancer Institute, Chennai, Tamil Nadu, India
2 Department of Pathology, Cancer Institute, Chennai, Tamil Nadu, India

Date of Submission10-Oct-2019
Date of Decision04-Nov-2019
Date of Acceptance03-Dec-2019
Date of Web Publication24-Feb-2020

Correspondence Address:
Venkatraman Radhakrishnan
Department of Medical Oncology, Cancer Institute, Adyar, Chennai, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/CRST.CRST_85_19

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  Abstract 


Background: Peripheral T-cell lymphomas (PTCL) are a heterogeneous group of diseases with aggressive behavior and inferior outcomes as compared to B-cell lymphomas. We report the outcomes from a single center over a period of 18 years.
Methods: The baseline clinical features, pathological subtypes, and prognostic factors of all patients with PTCL treated at our center between January 2000 and December 2017 were retrospectively analyzed. Event-free survival (EFS) and overall survival (OS) were calculated using the Kaplan–Meier method and prognostic factors were compared using the log-rank test.
Results: During the study period, 144 patients (2–74 years) were diagnosed with PTCL. Male patients were 101 (70%) and females were 43 (30%). Mean age at diagnosis was 43.5 years (20–74 years) for adults (≥ ≥18 years). Of the 144 patients, 42 (29%) had limited stage (Stage I/II) and 102 (71%) had advanced-stage disease (III/IV). The most common histological diagnosis was PTCL-not otherwise specified observed in 61 patients (42.4%) followed by anaplastic large-cell lymphoma (ALCL) in 65 patients (45.2%). The median duration of follow-up was 70.5 months (range, 1–218 months). Five-year OS and EFS for the entire population were 55% and 33%, respectively. Patients with limited stage had better survival when compared to those with advanced disease. Five-year EFS was 52% versus 25% (P = 0.006) and 5-year OS was 70% versus 47% (P = 0.02) in limited and advanced stage, respectively. Patients with PTCL, anaplastic lymphoma kinase (ALK)-positive ALCL and ALK-negative ALCL had 5-year EFS and OS of 20% and 38%, 46% and 76%, 43% and 76%, respectively (P value for EFS = 0.009 and OS < 0.001).
Conclusion: Majority of patients with PTCL at our center presented with advanced-stage disease. Outcomes of patients with ALCL are better than those diagnosed with other subtypes of PTCL.

Keywords: Chemotherapy, India, low- and middle-income country, lymphoma, peripheral T-cell lymphomas, survival


How to cite this article:
Kesana SS, Ganesan P, Sagar TG, Kannan K, Ganesan TS, Danushkodi M, Mehra N, Jayachandran P K, Joshi A, Kumar A, Selvarajan G, Sundersingh S, Radhakrishnan V. Clinicopathological characteristics, prognostic factors, and outcomes in peripheral T-cell lymphoma: Experience from a single center in India. Cancer Res Stat Treat 2020;3:3-12

How to cite this URL:
Kesana SS, Ganesan P, Sagar TG, Kannan K, Ganesan TS, Danushkodi M, Mehra N, Jayachandran P K, Joshi A, Kumar A, Selvarajan G, Sundersingh S, Radhakrishnan V. Clinicopathological characteristics, prognostic factors, and outcomes in peripheral T-cell lymphoma: Experience from a single center in India. Cancer Res Stat Treat [serial online] 2020 [cited 2020 Apr 10];3:3-12. Available from: http://www.crstonline.com/text.asp?2020/3/1/3/279150




  Introduction Top


Peripheral T-cell lymphomas (PTCL) constitute about 10%–20% of all non-Hodgkin lymphomas and are generally more aggressive than B-cell lymphomas.[1],[2],[3] A higher incidence of PTCL has been reported from Southeast Asia.[1],[4] PTCL constitutes a heterogeneous group of conditions which can be broadly divided into nodal, extranodal, leukemic, and cutaneous groups. According to the World Health Organization 2016 classification, there are more than 20 different subtypes of PTCL and the common histological subtypes include PTCL, not otherwise specified (NOS), anaplastic large cell lymphoma (ALCL), angioimmunoblastic T-cell lymphoma (AITL) followed by rarer entities such as natural killer T-cell lymphoma, hepatosplenic T-cell lymphoma (HSTCL), subcutaneous panniculitis T-cell lymphoma, adult T-cell leukemia/lymphoma (ATLL), and others.[5]

According to the International PTCL Project (IPTCLP), anaplastic lymphoma kinase (ALK)-positive ALCL has the best prognosis and PTCL-NOS has the poorest outcome.[2] Current recommendations for treatment in PTCL constitute multiagent chemotherapy with or without radiotherapy and consolidation with autologous stem cell transplantation (ASCT) except in ALK-positive ALCL where ASCT is not recommended in first remission.[5]

Various tools such as the International Prognostic Index (IPI) score, Prognostic Index for PTCL Unspecified (PIT) score, and the IPTCLP score have been formulated for prognostication in PTCL, but none of the scores have been found to be unanimously superior[6],[7],[8] Earlier studies on PTCL have highlighted the regional variations in the incidence of various subtypes as well as PTCL as a whole.[2],[5],[9] Although there are a few reports on the incidence and epidemiology of T-cell subtypes from India, there are limited data on the outcomes after therapy. The aim of the present study was to review the incidence of various types of PTCL, clinicopathological features, prognostic factors, and their outcomes in patients who were treated at our center.


  Methods Top


Patients

Patients between the ages of 2 and 74 years with a diagnosis of T-cell lymphoma, who received treatment at our center from January 2000 to December 2017 were included. The study was retrospective in nature and data were collected from the patient case records from tumor registry. Retrospective review of case records does not require ethics approval at our center; however, the study was conducted as per the guidelines of the Institutional Ethics Committee and according to the Declaration of Helsinki, Good Clinical Practice guidelines, and Indian Council of Medical Research guidelines for ethical conduct. Pretreatment characteristics (age, sex, clinical stage, Eastern Cooperative Oncology Group performance status [PS], disease bulk, and pathological subtype) were obtained from the medical records. Age-adjusted IPI, PIT, and IPTCLP scores were calculated retrospectively at the time of analysis. For the purpose of analysis, bulky disease was defined as any site of disease ≥10 cm in adults and ≥6 cm in children (age <18 years). The study included patients treated over a 17-year period, and during this time, the management of patients had evolved at our institute with advances in pathology, imaging, and treatment. Chest X-ray and ultrasound of the abdomen and pelvis were used for staging and response assessment during years 2000–2002, contrast-enhanced computed tomography (CECT) scan of chest, abdomen, and pelvis from 2003 to 2014 and since 2014, fluorodeoxyglucose positron emission tomography with computed tomography (PET-CT) is being used for staging and response assessment. Staging included unilateral bone marrow trephine biopsy. Histopathological examination and subtyping were done by experienced oncopathologists. Patients with T-cell lymphoblastic lymphoma and cutaneous T-cell lymphoma were excluded from the analysis.

Therapy

Patients at diagnosis were planned for either curative or palliative intent treatment based on the PS, comorbidities, and after discussion in the multidisciplinary tumor board. Patients who were planned for palliative treatment received either oral metronomic chemotherapy (OMC)[10] or palliative radiotherapy or best supportive care and those planned for curative intent received cyclophosphamide + adriamycin +vincristine + prednisolone (CHOP) or CHOP + etoposide (CHOPE) for PTCL, and Berlin-Frankfurt-Munster (BFM) 90/LMB-89 protocol for pediatric ALCL.[11],[12] Radiation was generally used in patients with bulky sites, extranodal disease, and for palliation. Few patients underwent ASCT in first complete remission (CR).

Response assessment and follow-up

Response to treatment was assessed clinically after every cycle of chemotherapy. Radiological response was assessed after 3–4 cycles of chemotherapy and at the end of therapy by CECT or PET-CT. Bone marrow biopsy was only repeated if it was positive for bone marrow involvement by disease at diagnosis. Patients were usually followed up once in 3 months for the first 2 years, 6-monthly from 3 to 5 years, and yearly thereafter. Follow-up was both passive as well as active, with the hospital tumor registry making efforts to ascertain the status of patients who had not reported for their scheduled clinical visits.

Relapse

Relapses were confirmed by radiology and biopsy, wherever feasible. At relapse, depending on fitness of the patient and feasibility, various salvage regimens were used, and few patients underwent ASCT. Salvage regimens used were ifosfamide + carboplatin + etoposide, gemcitabine + dexamethasone + cisplatin (GDP), dexamethasone + cytarabine + cisplatin, infusional etoposide, vincristine, cyclophosphamide, adriamycin (EPOCH), methotrexate, adriamycin, cyclophosphamide, prednisone and bleomycin (MACOPB), and gemcitabine + oxaliplatin. Depending on the feasibility and response to treatment, some patients were taken up for stem cell transplantation (SCT) and remaining patients with partial response (PR) or stable disease were started on OMC with cyclophosphamide, etoposide, prednisolone, or lenalidomide.

Statistical analysis

Descriptive statistical analysis was done for the baseline variables. Overall survival (OS) was calculated from the date of start of therapy till death or last follow-up. Events for survival analysis included death for OS and death, disease progression, or relapse for event-free survival (EFS). EFS was calculated from the date of start of therapy till date of event. EFS and OS were analyzed by the Kaplan–Meier method[13] and risk factors were compared using the log-rank test for univariate analysis and Cox-proportional hazards model for multivariate analysis.[14],[15] Patients who were lost to follow-up were censored as alive at the last follow-up date. SPSS version 17.0 (SPSS Inc, IBM, Chicago, USA) was used for statistical analysis. P < 0.05 was considered statistically significant. Median follow-up was calculated for all patients using the reverse Kaplan–Meier method.


  Results Top


Baseline characteristics

We identified 144 patients of which 122 were adults (≥18 years) and 22 were pediatric. The median age at presentation was 43.5 years (range, 20–74) in adults and 10 years (2–18 years) in pediatric patients. The median duration of symptoms was 2 months. There were 101 (70%) males and 43 females (29.9%). The most common histological diagnosis was ALCL in 65 (45.2%) patients followed by PTCL-NOS in 61 (42.4%), NK-T-cell lymphoma in 9 (6.3%), AITL in 4 (2.8%), HSTCL in 2 (1.4%), ATLL in 2 (1.4%), and SPTCL in 1 (0.7%). Among the 65 patients with ALCL, 38 (26.4%) were ALK-positive, 8 (5.6%) were ALK-negative and ALK status was unknown in 19 (13.2%). Twenty-two (15.2%) patients were <18-year-old and all had ALCL (20 were ALK-positive and 2 were ALK-negative).

Forty-two patients (29.2%) had limited stage (Stage I/II) disease and 102 (70.8%) had advanced Stage (III/IV). Age-adjusted IPI scores and PIT scores were calculated in 127 patients as LDH data were available in only in 127 patients and IPTCLP score was calculated in 144 patients. [Table 1] and [Table 2] provide the demographic and clinical details of all patients and pediatric (age <18 years) versus adult patients, respectively.
Table 1: Baseline features in patients with various subtypes of peripheral T-cell lymphomas

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Table 2: Baseline features compared between the adult and pediatric population

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Treatment and outcomes

One hundred and thirty-three out of 144 (92.4%) patients were treated with curative intent and 11/144 (7.6%) with palliative intent. Among the 11 patients treated with palliative intent, 10 patients received OMC and 1 received intravenous chemotherapy. CHOP was given in 84 (58.3%) patients, CHOPE in 10 (6.9%), cyclophosphamide, vincristine and prednisolone (COP) in 6, COP + etoposide in 4, dexamethasone, ifosfamide, methotrexate, L-asparaginase and etoposide (SMILE) in 4, EPOCH in 2, MACOPB in 4, OMC in 10 and LMB-89 and BFM-85 protocols were given in 11 (7.6%) and 9 (6.2%) pediatric patients, respectively. SMILE chemotherapy regimen was used in patients with NK/T-Cell lymphoma. Crizotinib was used as the second-line agent in ALK-positive ALCL in 4 patients.

CR at end of treatment was observed in 84 (58.3%) patients, PR in 18 (13.2%) patients, and progressive disease in 41 (28.5%) patients. One patient died due to febrile neutropenia prior to response assessment. Overall response rate (CR + PR) was 70.8%. Only five patients (PTCL NOS) underwent transplant in CR at completion of first-line treatment (CR1). Eighteen patients with relapse were treated with salvage protocols and 9 were transplanted. Conditioning regimens used initially were lomustine + cytarabine + cyclophosphamide + etoposide (LACE), lomustine + etoposide + cytarabine + melphalan (LEAM). Due to unavailability of lomustine, carmustine (BCNU), etoposide + cytarabine + melphalan (BEAM) conditioning was used later. For allogenic stem cell transplant, fludarabine-melphalan (Flu-Mel) conditioning was used.

SCT was performed in 14 patients, 5 in CR1 (all PTCL NOS) and 9 after relapse (PTCL NOS [n = 4], ALK-positive ALCL [n = 2], ALK-negative ALCL [n = 2], HSPTCL [n = 1]). Of the 14 patients, 8 are in remission post transplantation (2 from CR1 and 6 from CR2) and 6 have relapsed.

Twenty-one patients were lost to follow-up. Seventy-seven patients had an event of which 24 had relapsed, 41 had disease progression, and 12 patients died. The 5-year EFS and OS for all the patients was 33% (95% confidence interval [CI] = 24.7%–41.6%) and 55% (95% CI 45.3%–66.4%) respectively. The median duration of follow-up of all patients was 70.5 months (range, 1–218 months). Patients with limited stage disease had 5-year EFS and OS of 52% (95% CI, 34.8%–68.9%) and 70% (95% CI, 56.3%–84.6%) respectively and patients with advanced stage disease had 5-year EFS and OS of 25% (95% CI, 15%–33.2%) and 48% (95% CI, 37.3%–58%), respectively (P = 0.006 for EFS and P = 0.02 for OS).

The 5-year EFS and OS of the adult and the pediatric patients were 41% and 70% and 50% and 86%, respectively (P = 0.6 for EFS and P = 0.4 for OS). Adult patients with limited stage disease had a better 5-year EFS and OS compared to advanced stage disease, although statistically not significant (5-year EFS 61% vs. 30% [P = 0.44] and 5-year OS: 94% vs. 66% [P = 0.45]).

Factors affecting outcomes

Patients with PTCL, ALK-positive ALCL, and ALK-negative ALCL had 5-year EFS and OS of 20% and 38%, 46% and 76%, and 43% and 76%, respectively (P = 0.009 for EFS and P < 0.001 for OS) [Figure 1]a and [Figure 1]b.
Figure 1: Kaplan–Meier curve showing event-free survival and overall survival in various subtypes of peripheral T-cell lymphomas

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Age ≤18 years and early stage disease were found to be significantly associated with better EFS and OS on multivariate analysis. Gender, the presence of B-symptoms, number of extranodal sites involved, LDH, and PS were not found to be significant on multivariate analysis for EFS and OS [Table 3]. The IPI, PIT, and IPTCLP scores were all found to be useful for the prognostication [Table 4] and [Figure 2],[Figure 3],[Figure 4]a, [Figure 4]b.
Table 3: Univariate analysis of factors predicting the survival

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Table 4: Univariate analysis of factors predicting the survival

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Figure 2: Kaplan–Meier curve showing overall survival and event-free survival according to the age-adjusted-International Prognostic Index score

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Figure 3: Kaplan–Meier curve showing overall survival and event-free survival according to the Prognostic Index for peripheral T-cell lymphomas unspecified (PIT) score

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Figure 4: Kaplan–Meier curve showing overall survival and event-free survival according to the International Peripheral T-cell Lymphoma Project score

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Patients who had an event in <24 months had a 5-year OS of 23% compared to patients who had an event beyond 24 months who had a 5-year OS of 91% (P = 0.002).


  Discussion Top


In our study, we found that PTCL NOS was the most common histology followed by ALK-positive ALCL, but AITL occurred in a lesser proportion as compared to what has been reported in other studies. Median age at diagnosis was 43.5 years in adults and 10 years in the pediatric population with male predominance (70%). Majority presented with advanced stage (70%). Survival outcomes were better in the pediatric population, in patients with limited stage disease and who did not have an event in the first 24 months. Pediatric population outcomes were better though majority present with increased B-symptoms, PS ≥2 or more, bulky, extranodal, and bone involvement as compared to adults.

T-cell lymphomas have been reported to have a higher incidence in India compared to the Western world (20% vs. 10%).[16] When comparing the baseline features of our patients with other reports, we find that most of our findings were similar. PTCL-NOS was the most common subtype in adults, while ALK-positive ALCL was common in pediatric ages.[5],[17],[18] The proportion of patients with B-symptoms (41%), liver involvement (9%), and spleen involvement (22%) were also comparable. The proportion of patients with extranodal involvement (40%) was similar to Western literature but differed from an Indian study which had reported 60% extranodal disease.[18] Bone marrow involvement was observed in 12.5% of patients and is comparable to the study by Lokanatha et al.[18] However, bone marrow involvement up to 15%–39% has been reported in other studies.[6],[8],[17],[19] The only difference was the median age at diagnosis of 43 years which is a decade younger than that reported in Western literature[8],[19],[20] [Table 5].
Table 5: Review of the literature on peripheral T-cell lymphomas from India

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The prognosis in PTCL is based on the histological subtype and also the risk-adapted scoring system.[17],[18] Patients with ALK-positive ALCL have the best prognosis, whereas patients with PTCL-NOS have inferior outcomes despite intensive treatment including ASCT.[2] The survival outcomes were best for ALK-positive ALCL (5-year OS 70%) and worst in PTCL-NOS (5-year OS 32%) which are similar to the IPTCL data.[2] Interestingly, patients who did not have an event for 24 months after diagnosis (EFS24) had a significantly better OS compared to patients who had an event within 24 months of the diagnosis (5-year OS, 93.9% vs. 26.2% respectively). Our findings on EFS24 as a prognostic marker are similar to those reported by Maurer et al.[23]

High-dose chemotherapy with ASCT is generally recommended as consolidation in first CR for high-intermediate or high IPI non-ALK-positive PTCL. This is based on retrospective case series which have reported 3-year OS of 60%–85% among patients who underwent ASCT.[24],[25],[26] However, majority of our patients did not undergo ASCT in CR1 due to financial constraints. The 5-year EFS for the high-intermediate and high IPI patients in our cohort was a dismal 31% and 0%, respectively.

Patients with ALK-positive ALCL have better survival outcomes compared to patients with ALK-negative ALCL. In ALK-negative ALCL, rearrangements involving DUSP22 have outcomes comparable to those that are ALK-positive, whereas those with rearrangements involving TP63 have inferior survival.[27],[28],[29] Approximately 30% of ALK-negative ALCL are positive for DUSP22 rearrangement and 8% for TP63 rearrangement.[27] We did not check for DUSP22 or TP63 rearrangement in our patients.

Age-adjusted IPI, IPTCL, and PIT scores were all predictive of PFS and OS in our study cohort, thereby validating the scores in the Indian population. Anthracycline-based regimens like CHOP have been the backbone for treating PTCL for decades. A recent meta-analysis by Deng et al. showed no benefit of adding etoposide to CHOP in PTCL in terms of response rates and survival; however, the addition of etoposide was associated with increased toxicity.[30] Majority of the patients in our study received CHOP (65%) and only 10 patients (6%) received CHOPE and therefore the outcomes between the two groups were not compared.

The limitations of our study include the retrospective nature and inability to ascertain the ALK-status in patients with ALCL. DUSP22 and TP63 rearrangements were not checked in the ALK-negative ALCL cases. Majority of patients did not have access to SCT and newer agents such as brentuximab vedotin, and ALK inhibitors such as crizotinib and ceretinib in relapsed ALCL.[31] Also, there was a heterogeneity in the patient cohort as we included both adult and pediatric patients, who had differences in the clinical outcomes. However, the present study is one of the largest from India reporting the outcomes and prognostic factors for this rare disease.


  Conclusion Top


Majority of patients with PTCL at our center present with advanced stage disease. Outcomes of patients with ALCL are better than those with other histological subtypes. Hematopoietic SCT should be offered to high-risk patients achieving good response to chemotherapy. Novel therapies are necessary to improve the outcomes.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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