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Role of upfront autologous transplant for peripheral T-cell lymphoma patients achieving a complete remission with first-line therapy: a systematic review and meta-analysis

Bone Marrow Transplantation (2024)Cite this article

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Abstract

There is currently no consensus on the role of upfront autologous transplantation (ASCT) for patients with peripheral T-cell lymphomas (PTCL), especially in patients achieving first complete remission (CR1) following chemotherapy, and data in the literature is conflicting. A systematic review and meta-analysis was performed to address this question. We searched key databases from January 2000 to February 2022. Six prospective and eleven retrospective studies were included among 2959 unique records. Median follow up in these studies ranged from 22 to 94 months. There was a trend towards benefit in PFS (HR = 0.80, 95% CI 0.62–1.05, p = 0.11) and OS (HR = 0.79, 95% CI 0.57–1.09, p = 0.15) in the ASCT compared to chemotherapy only group. Importantly, in transplant eligible patients in CR1, a significant benefit was demonstrated in both OS (HR = 0.59, 95% CI 0.36–0.95, p = 0.03) and PFS (HR = 0.61, 95% CI 0.47–0.81, p = 0.0004) in the ASCT group. Amongst the nodal PTCL subgroups, ASCT showed a significant PFS benefit for the AITL subgroup (HR = 0.43, 95% CI 0.20–0.94, p < 0.03) but not PTCL-NOS or ALK−ve ALCL subgroups. Our findings support upfront ASCT for transplant eligible PTCL patients achieving CR1 post chemotherapy. In particular, patients with AITL exhibited a significantly better PFS after upfront ASCT.

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Fig. 1: PRISMA flow diagram of study screening and selection.
Fig. 2: Meta-analysis of the HRs of PFS in patients with PTCL treated with ASCT consolidation in comparison with those receiving conventional chemotherapy alone.
Fig. 3: Meta-analysis of the HRs of OS in patients with PTCL treated with ASCT consolidation in comparison to those receiving conventional chemotherapy alone.
Fig. 4: Meta analysis of the HRs of PFS and OS in the AITL subgroup, treated with ASCT consolidation in comparison with those receiving conventional chemotherapy alone.
Fig. 5: Funnel plot.

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All data generated or analysed during this study are included in this published article.

References

  1. Bellei M, Nabhan C, Pesce EA, Conte L, Vose JM, Foss F, et al. The value and relevance of the T cell lymphoma registries and international collaborations: the case of COMPLETE and the T-cell project. Curr Hematol Malig Rep. 2015;10:448–55.

    Article  PubMed  Google Scholar 

  2. Laurent C, Baron M, Amara N, Haioun C, Dandoit M, Maynadie M, et al. Impact of expert pathologic review of lymphoma diagnosis: study of patients from the French Lymphopath Network. J Clin Oncol. 2017;35:2008–17.

    Article  PubMed  Google Scholar 

  3. Vose J, Armitage J, Weisenburger D, International TCLP. International peripheral T-cell and natural killer/T-cell lymphoma study: pathology findings and clinical outcomes. J Clin Oncol. 2008;26:4124–30.

    Article  PubMed  Google Scholar 

  4. Park S, Ko YH. Peripheral T cell lymphoma in Asia. Int J Hematol. 2014;99:227–39.

    Article  CAS  PubMed  Google Scholar 

  5. Yoon SE, Song Y, Kim SJ, Yoon DH, Chen TY, Koh Y, et al. Comprehensive analysis of peripheral T-cell and natural killer/T-cell lymphoma in Asian patients: a multinational, multicenter, prospective registry study in Asia. Lancet Reg Health West Pac. 2021;10:100126.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ellin F, Landstrom J, Jerkeman M, Relander T. Real-world data on prognostic factors and treatment in peripheral T-cell lymphomas: a study from the Swedish Lymphoma Registry. Blood. 2014;124:1570–7.

    Article  CAS  PubMed  Google Scholar 

  7. d’Amore F, Relander T, Lauritzsen GF, Jantunen E, Hagberg H, Anderson H, et al. Up-front autologous stem-cell transplantation in peripheral T-cell lymphoma: NLG-T-01. J Clin Oncol. 2012;30:3093–9.

    Article  PubMed  Google Scholar 

  8. Reimer P, Rudiger T, Geissinger E, Weissinger F, Nerl C, Schmitz N, et al. Autologous stem-cell transplantation as first-line therapy in peripheral T-cell lymphomas: results of a prospective multicenter study. J Clin Oncol. 2009;27:106–13.

    Article  CAS  PubMed  Google Scholar 

  9. Yin J, Wei J, Xu JH, Xiao Y, Zhang YC. Autologous stem cell transplantation as the first-line treatment for peripheral T cell lymphoma: results of a comprehensive meta-analysis. Acta Haematol. 2014;131:114–25.

    Article  CAS  PubMed  Google Scholar 

  10. Jethwa KD, Bishton MJ, Fox CP. The role of high-dose chemotherapy and autologous stem cell transplant for treatment-naIotave patients with peripheral T-cell lymphoma: a systematic review of the literature. Br J Haematol. 2017;178:476–9.

    Article  PubMed  Google Scholar 

  11. Zhai Y, Wang J, Jiang Y, Wu W, Lv Y, Xu H, et al. The efficiency of autologous stem cell transplantation as the first-line treatment for nodal peripheral T-cell lymphoma: results of a systematic review and meta-analysis. Expert Rev Hematol. 2022;15:265–72.

    Article  CAS  PubMed  Google Scholar 

  12. Park SI, Horwitz SM, Foss FM, Pinter-Brown LC, Carson KR, Rosen ST, et al. The role of autologous stem cell transplantation in patients with nodal peripheral T-cell lymphomas in first complete remission: report from COMPLETE, a prospective, multicenter cohort study. Cancer. 2019;125:1507–17.

    Article  CAS  PubMed  Google Scholar 

  13. Fossard G, Broussais F, Coelho I, Bailly S, Nicolas-Virelizier E, Toussaint E, et al. Role of up-front autologous stem-cell transplantation in peripheral T-cell lymphoma for patients in response after induction: an analysis of patients from LYSA centers. Ann Oncol. 2018;29:715–23.

    Article  CAS  PubMed  Google Scholar 

  14. Yam C, Landsburg DJ, Nead KT, Lin X, Mato AR, Svoboda J, et al. Autologous stem cell transplantation in first complete remission may not extend progression-free survival in patients with peripheral T cell lymphomas. Am J Hematol. 2016;91:672–6.

    Article  CAS  PubMed  Google Scholar 

  15. García-Sancho AM, Bellei M, López-Parra M, Gritti G, Cortés M, Novelli S, et al. Autologous stem-cell transplantation as consolidation of first-line chemotherapy in patients with peripheral T-cell lymphoma: a multicenter GELTAMO/FIL study. Haematologica. 2022;107:2675–84.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4:1.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283:2008–12.

    Article  CAS  PubMed  Google Scholar 

  18. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality of non-randomized studies in meta-analysis. Available online: https://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed on 2 November 2012).

  19. Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17:2815–34.

    Article  CAS  PubMed  Google Scholar 

  20. Egger M, Zellweger-Zahner T, Schneider M, Junker C, Lengeler C, Antes G. Language bias in randomised controlled trials published in English and German. Lancet. 1997;350:326–9.

    Article  CAS  PubMed  Google Scholar 

  21. Al-Mansour Z, Li H, Cook JR, Constine LS, Couban S, Stewart DA, et al. Autologous transplantation as consolidation for high risk aggressive T-cell non-Hodgkin lymphoma: a SWOG 9704 intergroup trial subgroup analysis. Leuk Lymphoma. 2019;60:1934–41.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Savage KJ, Horwitz SM, Advani R, Christensen JH, Domingo-Domenech E, Rossi G, et al. Role of stem cell transplant in CD30+ PTCL following frontline brentuximab vedotin plus CHP or CHOP in ECHELON-2. Blood Adv. 2022;6:5550–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Advani RH, Skrypets T, Civallero M, Spinner MA, Manni M, Kim WS, et al. Outcomes and prognostic factors in angioimmunoblastic T-cell lymphoma: final report from the international T-cell Project. Blood. 2021;138:213–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cho H, Yoon DH, Shin DY, Koh Y, Yoon SS, Kim SJ, et al. Current treatment patterns and the role of upfront autologous stem cell transplantation in patients with peripheral T-cell lymphoma: a Korean nationwide, multicenter prospective registry study (CISL 1404). Cancer Res Treat. 2023;55:684–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Iriyama N, Takahashi H, Hatta Y, Miura K, Kobayashi Y, Kurita D, et al. Efficacy of a dose-intensified CHOP (Double-CHOP) regimen for peripheral T-cell lymphomas. Oncol Rep. 2013;29:805–11.

    Article  CAS  PubMed  Google Scholar 

  26. Huang H, Liu S, Chen X, Jin Z, Wu D. Outcome of autologous hematopoietic stem cell transplantation in first complete remission in patients with low-risk peripheral T-cell lymphomas (PTCLs). Hematol Oncol. 2019;37:464–5.

    Article  Google Scholar 

  27. Jiao Y, Liu W, Yi SH, Liu HM, Yu Y, Huang WY, et al. [A comparative analysis of autologous hematopoietic stem cell transplantation and chemotherapy alone in the treatment of nodal peripheral T-cell lymphoma in complete remission]. Zhonghua Xue Ye Xue Za Zhi. 2021;42:428–31.

    CAS  PubMed  Google Scholar 

  28. He XH, Li B, Zou SM, Dong M, Zhou SY, Yang JL, et al. Efficacy of peripheral blood stem cell transplantation versus conventional chemotherapy on anaplastic large-cell lymphoma: a retrospective study of 64 patients from a single center. Chin J Cancer. 2012;31:532–40.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Rohlfing S, Dietrich S, Witzens-Harig M, Hegenbart U, Schönland S, Luft T, et al. The impact of stem cell transplantation on the natural course of peripheral T-cell lymphoma: a real-world experience. Ann Hematol. 2018;97:1241–50.

    Article  PubMed  Google Scholar 

  30. Tang T, Khoo LP, Lim C, Ham JS, Kim SJ, Hong H, et al. Outcomes of patients with peripheral T-cell lymphoma in first complete remission: data from three tertiary Asian cancer centers. Blood Cancer J. 2017;7:653.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Ahn SY, Jung SY, Jung SH, Ahn JS, Lee JJ, Kim HJ, et al. Prognostic significance of FDG-PET/CT in determining upfront autologous stem cell transplantation for the treatment of peripheral T cell lymphomas. Ann Hematol. 2020;99:83–91.

    Article  PubMed  Google Scholar 

  32. Gleeson M, Peckitt C, Cunningham D, Gibb A, Hawkes EA, Back M, et al. Outcomes following front-line chemotherapy in peripheral T-cell lymphoma: 10-year experience at The Royal Marsden and The Christie Hospital. Leuk Lymphoma. 2018;59:1586–95.

    Article  PubMed  Google Scholar 

  33. El-Asmar J, Reljic T, Ayala E, Hamadani M, Nishihori T, Kumar A, et al. Efficacy of high-dose therapy and autologous hematopoietic cell transplantation in peripheral T cell lymphomas as front-line consolidation or in the relapsed/refractory setting: a systematic review/meta-analysis. Biol Blood Marrow Transplant. 2016;22:802–14.

    Article  PubMed  Google Scholar 

  34. Kyriakou C, Canals C, Goldstone A, Caballero D, Metzner B, Kobbe G, et al. High-dose therapy and autologous stem-cell transplantation in angioimmunoblastic lymphoma: complete remission at transplantation is the major determinant of Outcome—Lymphoma Working Party of the European Group for Blood and Marrow Transplantation. J Clin Oncol. 2008;26:218–24.

    CAS  PubMed  Google Scholar 

  35. Brink M, Meeuwes FO, van der Poel MWM, Kersten MJ, Wondergem M, Mutsaers P, et al. Impact of etoposide and ASCT on survival among patients aged <65 years with stage II to IV PTCL: a population-based cohort study. Blood 2022;140:1009–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.

    Article  PubMed  PubMed Central  Google Scholar 

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Author notes

  1. These authors contributed equally: L. Girard, Y. J. Koh, L. M. Poon, M. Samuel.

Authors and Affiliations

  1. Aberdeen Royal Infirmary, National Health Service Grampian, Aberdeen, UK

    L. Girard

  2. University College London Medical School, London, UK

    Y. J. Koh

  3. Department of Haematology Oncology, National University Cancer Institute, Singapore, Singapore

    L. P. Koh, Y. L. Chee, H. L. Chan, J. Lee, S. de Mel & L. M. Poon

  4. NUS Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore

    M. Samuel

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Contributions

LMP and SM were responsible for conceptualising the study, designing the review protocol, and coordinating the overall project including data analysis and data interpretation. SM was also conducted all the meta-regression analyses of the data as well as creating the figures in the study. LMP, LG and YJK were involved with writing the protocol and report, conducting the search, screening potentially eligible studies, extracting and analysing data, interpreting results and updating reference lists. LPK was responsible for screening potentially eligible studies. YLC, JL, HLC and SDM provided feedback on the report.

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Correspondence to L. M. Poon.

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Girard, L., Koh, Y.J., Koh, L.P. et al. Role of upfront autologous transplant for peripheral T-cell lymphoma patients achieving a complete remission with first-line therapy: a systematic review and meta-analysis. Bone Marrow Transplant (2024). https://doi.org/10.1038/s41409-024-02254-x

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